Articles are listed by year in reverse chronological order.


Provart, NJ, Alonso, J, Assmann, SM, Bergmann, D, Brady, SM, Brkljacic, J, Browse, J, Chapple, C, Colot, V, Cutler, S, Dangl, J, Ehrhardt, D, Friesner, JD, Frommer, WB, Grotewold, E, Meyerowitz, E, Nemhauser, J, Nordborg, M, Pikaard, C, Shanklin, J, Somerville, C, Stitt, M, Torii, KU, Waese, J, Wagner, D, McCourt, P (2016) 50 years of Arabidopsis research: highlights and future directions. New Phytol., 209(3), 921-44. PMID:26465351. doi:10.1111/nph.13687.
The year 2014 marked the 25(th) International Conference on Arabidopsis Research. In the 50 yr since the first International Conference on Arabidopsis Research, held in 1965 in Göttingen, Germany, 54,000 papers that mention Arabidopsis thaliana in the title, abstract or keywords have been published. We present herein a citational network analysis of these papers, and touch on some of the important discoveries in plant biology that have been made in this powerful model system, and highlight how these discoveries have then had an impact in crop species. We also look to the future, highlighting some outstanding questions that can be readily addressed in Arabidopsis. Topics that are discussed include Arabidopsis reverse genetic resources, stock centers, databases and online tools, cell biology, development, hormones, plant immunity, signaling in response to abiotic stress, transporters, biosynthesis of cells walls and macromolecules such as starch and lipids, epigenetics and epigenomics, genome-wide association studies and natural variation, gene regulatory networks, modeling and systems biology, and synthetic biology.
Tobin, C. J. and Meyerowitz, E.M. (2016) Real-time lineage analysis to study cell division orientation in the Arabidopsis shoot meristem. Plant Cell Division Methods and Protocols, ed. M.C. Caillaud, Methods in Molecular Biology 1370, 147- 167. doi 10.1007/978-1-4939-2_12.
Cells in the Arabidopsis shoot apical meristem are small and divide frequently throughout the life-time of the organism making them good candidates for studying the mechanisms of cell division in plants. But tracking these cell divisions requires multiple images to be taken of the same specimen over time which means the specimen must stay alive throughout the process. This chapter provides details on how to prepare plants for live imaging, keep them alive and growing through multiple time points, and how to process the data to extract cell boundary coordinates from three-dimensional images.
Gruel, J., Landrein, B., Tarr, P., Schuster, C., Refahi, Y., Sampathkumar, A., Hamant, O., Meyerowitz, E. and Jönsson, H. (2016) An epidermis-driven mechanism positions and scales stem cell niches in plants. Sci. Adv. 2, e1500989. doi 10.1126/sciadv.1500989.
How molecular patterning scales to organ size is highly debated in developmental biology. We explore this question for the characteristic gene expression domains of the plant stem cell niche residing in the shoot apical meristem. We show that a combination of signals originating from the epidermal cell layer can correctly pattern the key gene expression domains and notably leads to adaptive scaling of these domains to the size of the tissue. Using live imaging, we experimentally confirm this prediction. The identified mechanism is also sufficient to explain de novo stem cell niches in emerging flowers. Our findings suggest that the deformation of the tissue transposes meristem geometry into an instructive scaling and positional input for the apical plant stem cell niche.
Luo, CJ, Wightman, R, Meyerowitz, E, Smoukov, SK (2015) A 3-dimensional fibre scaffold as an investigative tool for studying the morphogenesis of isolated plant cells. BMC Plant Biol., 15, 211. PMCID:PMC4550058. PMID:26310239. doi:10.1186/s12870-015-0581-7.
Cell culture methods allow the detailed observations of individual plant cells and their internal processes. Whereas cultured cells are more amenable to microscopy, they have had limited use when studying the complex interactions between cell populations and responses to external signals associated with tissue and whole plant development. Such interactions result in the diverse range of cell shapes observed in planta compared to the simple polygonal or ovoid shapes in vitro. Microfluidic devices can isolate the dynamics of single plant cells but have restricted use for providing a tissue-like and fibrous extracellular environment for cells to interact. A gap exists, therefore, in the understanding of spatiotemporal interactions of single plant cells interacting with their three-dimensional (3D) environment. A model system is needed to bridge this gap. For this purpose we have borrowed a tool, a 3D nano- and microfibre tissue scaffold, recently used in biomedical engineering of animal and human tissue physiology and pathophysiology in vitro.


Melnyk, CW, Schuster, C, Leyser, O, Meyerowitz, EM (2015) A Developmental Framework for Graft Formation and Vascular Reconnection in Arabidopsis thaliana. Curr. Biol., 25(10), 1306-18. PMID:25891401. doi:10.1016/j.cub.2015.03.032.
Plant grafting is a biologically important phenomenon involving the physical joining of two plants to generate a chimeric organism. It is widely practiced in horticulture and used in science to study the long-distance movement of molecules. Despite its widespread use, the mechanism of graft formation and vascular reconnection is not well understood. Here, we study the dynamics and mechanisms of vascular regeneration in Arabidopsis thaliana during graft formation when the vascular strands are severed and reconnected. We demonstrate a temporal separation between tissue attachment, phloem connection, root growth, and xylem connection. By analyzing cell division patterns and hormone responses at the graft junction, we found that tissues initially show an asymmetry in cell division, cell differentiation, and gene expression and, through contact with the opposing tissue, lose this asymmetry and reform the vascular connection. In addition, we identified genes involved in vascular reconnection at the graft junction and demonstrate that these auxin response genes are required below the graft junction. We propose an inter-tissue communication process that occurs at the graft junction and promotes vascular connection by tissue-specific auxin responses involving ABERRANT LATERAL ROOT FORMATION 4 (ALF4). Our study has implications for phenomena where forming vascular connections are important including graft formation, parasitic plant infection, and wound healing.
Shapiro, BE, Tobin, C, Mjolsness, E, Meyerowitz, EM (2015) Analysis of cell division patterns in the Arabidopsis shoot apical meristem. Proc. Natl. Acad. Sci. U.S.A., 112(15), 4815-20. PMCID:PMC4403164. PMID:25825722. doi:10.1073/pnas.1502588112.
The stereotypic pattern of cell shapes in the Arabidopsis shoot apical meristem (SAM) suggests that strict rules govern the placement of new walls during cell division. When a cell in the SAM divides, a new wall is built that connects existing walls and divides the cytoplasm of the daughter cells. Because features that are determined by the placement of new walls such as cell size, shape, and number of neighbors are highly regular, rules must exist for maintaining such order. Here we present a quantitative model of these rules that incorporates different observed features of cell division. Each feature is incorporated into a "potential function" that contributes a single term to a total analog of potential energy. New cell walls are predicted to occur at locations where the potential function is minimized. Quantitative terms that represent the well-known historical rules of plant cell division, such as those given by Hofmeister, Errera, and Sachs are developed and evaluated against observed cell divisions in the epidermal layer (L1) of Arabidopsis thaliana SAM. The method is general enough to allow additional terms for nongeometric properties such as internal concentration gradients and mechanical tensile forces.
Kareem, A, Durgaprasad, K, Sugimoto, K, Du, Y, Pulianmackal, AJ, Trivedi, ZB, Abhayadev, PV, Pinon, V, Meyerowitz, EM, Scheres, B, Prasad, K (2015) PLETHORA Genes Control Regeneration by a Two-Step Mechanism. Curr. Biol., 25(8), 1017-30. PMID:25819565. doi:10.1016/j.cub.2015.02.022.
Regeneration, a remarkable example of developmental plasticity displayed by both plants and animals, involves successive developmental events driven in response to environmental cues. Despite decades of study on the ability of the plant tissues to regenerate a complete fertile shoot system after inductive cues, the mechanisms by which cells acquire pluripotency and subsequently regenerate complete organs remain unknown. Here, we show that three PLETHORA (PLT) genes, PLT3, PLT5, and PLT7, regulate de novo shoot regeneration in Arabidopsis by controlling two distinct developmental events. Cumulative loss of function of these three genes causes the intermediate cell mass, callus, to be incompetent to form shoot progenitors, whereas induction of PLT5 or PLT7 can render shoot regeneration hormone-independent. We further show that PLT3, PLT5, and PLT7 establish pluripotency by activating root stem cell regulators PLT1 and PLT2, as reconstitution of either PLT1 or PLT2 in the plt3; plt5-2; plt7 mutant re-established the competence to regenerate shoot progenitor cells but did not lead to the completion of shoot regeneration. PLT3, PLT5, and PLT7 additionally regulate and require the shoot-promoting factor CUP-SHAPED COTYLEDON2 (CUC2) to complete the shoot-formation program. Our findings uncouple the acquisition of competence to regenerate shoot progenitor cells from completion of shoot formation, indicating a two-step mechanism of de novo shoot regeneration that operates in all tested plant tissues irrespective of their origin. Our studies reveal intermediate developmental phases of regeneration and provide a deeper understanding into the mechanistic basis of regeneration.
Nimchuk, ZL, Zhou, Y, Tarr, PT, Peterson, BA, Meyerowitz, EM (2015) Plant stem cell maintenance by transcriptional cross-regulation of related receptor kinases. Development, 142(6), 1043-9. PMCID:PMC4360179. PMID:25758219. doi:10.1242/dev.119677.
The CLAVATA3 (CLV3)-CLAVATA1 (CLV1) ligand-receptor kinase pair negatively regulates shoot stem cell proliferation in plants. clv1 null mutants are weaker in phenotype than clv3 mutants, but the clv1 null phenotype is enhanced by mutations in the related receptor kinases BARELY ANY MERISTEM 1, 2 and 3 (BAM1, 2 and 3). The basis of this genetic redundancy is unknown. Here, we demonstrate that the apparent redundancy in the CLV1 clade is in fact due to the transcriptional repression of BAM genes by CLV1 signaling. CLV1 signaling in the rib meristem (RM) of the shoot apical meristem is necessary and sufficient for stem cell regulation. CLV3-CLV1 signaling in the RM represses BAM expression in wild-type Arabidopsis plants. In clv1 mutants, ectopic BAM expression in the RM partially complements the loss of CLV1. BAM regulation by CLV1 is distinct from CLV1 regulation of WUSCHEL, a proposed CLV1 target gene. In addition, quadruple receptor mutants are stronger in phenotype than clv3, pointing to the existence of additional CLV1/BAM ligands. These data provide an explanation for the genetic redundancy seen in the CLV1 clade and reveal a novel feedback operating in the control of plant stem cells.
Melnyk, CW, Meyerowitz, EM (2015) Plant grafting. Curr. Biol., 25(5), R183-8. PMID:25734263. doi:10.1016/j.cub.2015.01.029.
Since ancient times, people have cut and joined together plants of different varieties or species so they would grow as a single plant - a process known as grafting (Figures 1 and 2). References to grafting appear in the Bible, ancient Greek and ancient Chinese texts, indicating that grafting was practised in Europe, the Middle East and Asia by at least the 5(th) century BCE. It is unknown where or how grafting was first discovered, but it is likely that natural grafting, the process by which two plants touch and fuse limbs or roots in the absence of human interference (Figure 3), influenced people's thinking. Such natural grafts are generally uncommon, but are seen in certain species, including English ivy. Parasitic plants, such as mistletoe, that grow and feed on often unrelated species may have also contributed to the development of grafting as a technique, as people would have observed mistletoe growing on trees such as apples or poplars.
Zhou, Y, Liu, X, Engstrom, EM, Nimchuk, ZL, Pruneda-Paz, JL, Tarr, PT, Yan, A, Kay, SA, Meyerowitz, EM (2015) Control of plant stem cell function by conserved interacting transcriptional regulators. Nature, 517(7534), 377-80. PMCID:PMC4297503. PMID:25363783. doi:10.1038/nature13853.
Plant stem cells in the shoot apical meristem (SAM) and root apical meristem are necessary for postembryonic development of aboveground tissues and roots, respectively, while secondary vascular stem cells sustain vascular development. WUSCHEL (WUS), a homeodomain transcription factor expressed in the rib meristem of the Arabidopsis SAM, is a key regulatory factor controlling SAM stem cell populations, and is thought to establish the shoot stem cell niche through a feedback circuit involving the CLAVATA3 (CLV3) peptide signalling pathway. WUSCHEL-RELATED HOMEOBOX 5 (WOX5), which is specifically expressed in the root quiescent centre, defines quiescent centre identity and functions interchangeably with WUS in the control of shoot and root stem cell niches. WOX4, expressed in Arabidopsis procambial cells, defines the vascular stem cell niche. WUS/WOX family proteins are evolutionarily and functionally conserved throughout the plant kingdom and emerge as key actors in the specification and maintenance of stem cells within all meristems. However, the nature of the genetic regime in stem cell niches that centre on WOX gene function has been elusive, and molecular links underlying conserved WUS/WOX function in stem cell niches remain unknown. Here we demonstrate that the Arabidopsis HAIRY MERISTEM (HAM) family of transcription regulators act as conserved interacting cofactors with WUS/WOX proteins. HAM and WUS share common targets in vivo and their physical interaction is important in driving downstream transcriptional programs and in promoting shoot stem cell proliferation. Differences in the overlapping expression patterns of WOX and HAM family members underlie the formation of diverse stem cell niche locations, and the HAM family is essential for all of these stem cell niches. These findings establish a new framework for the control of stem cell production during plant development.


Qi, J, Wang, Y, Yu, T, Cunha, A, Wu, B, Vernoux, T, Meyerowitz, E, Jiao, Y (2014) Auxin depletion from leaf primordia contributes to organ patterning. Proc. Natl. Acad. Sci. U.S.A., , . PMID:25512543. doi:10.1073/pnas.1421878112.
Stem cells are responsible for organogenesis, but it is largely unknown whether and how information from stem cells acts to direct organ patterning after organ primordia are formed. It has long been proposed that the stem cells at the plant shoot apex produce a signal, which promotes leaf adaxial-abaxial (dorsoventral) patterning. Here we show the existence of a transient low auxin zone in the adaxial domain of early leaf primordia. We also demonstrate that this adaxial low auxin domain contributes to leaf adaxial-abaxial patterning. The auxin signal is mediated by the auxin-responsive transcription factor MONOPTEROS (MP), whose constitutive activation in the adaxial domain promotes abaxial cell fate. Furthermore, we show that auxin flow from emerging leaf primordia to the shoot apical meristem establishes the low auxin zone, and that this auxin flow contributes to leaf polarity. Our results provide an explanation for the hypothetical meristem-derived leaf polarity signal. Opposite to the original proposal, instead of a signal derived from the meristem, we show that a signaling molecule is departing from the primordium to the meristem to promote robustness in leaf patterning.
Zhou, Y, Liu, X, Engstrom, EM, Nimchuk, ZL, Pruneda-Paz, JL, Tarr, PT, Yan, A, Kay, SA, Meyerowitz, EM (2014) Control of plant stem cell function by conserved interacting transcriptional regulators. Nature, PMID:25363783. doi:10.1038/nature13853.
Plant stem cells in the shoot apical meristem (SAM) and root apical meristem are necessary for postembryonic development of aboveground tissues and roots, respectively, while secondary vascular stem cells sustain vascular development. WUSCHEL (WUS), a homeodomain transcription factor expressed in the rib meristem of the Arabidopsis SAM, is a key regulatory factor controlling SAM stem cell populations, and is thought to establish the shoot stem cell niche through a feedback circuit involving the CLAVATA3 (CLV3) peptide signalling pathway. WUSCHEL-RELATED HOMEOBOX 5 (WOX5), which is specifically expressed in the root quiescent centre, defines quiescent centre identity and functions interchangeably with WUS in the control of shoot and root stem cell niches. WOX4, expressed in Arabidopsis procambial cells, defines the vascular stem cell niche. WUS/WOX family proteins are evolutionarily and functionally conserved throughout the plant kingdom and emerge as key actors in the specification and maintenance of stem cells within all meristems. However, the nature of the genetic regime in stem cell niches that centre on WOX gene function has been elusive, and molecular links underlying conserved WUS/WOX function in stem cell niches remain unknown. Here we demonstrate that the Arabidopsis HAIRY MERISTEM (HAM) family of transcription regulators act as conserved interacting cofactors with WUS/WOX proteins. HAM and WUS share common targets in vivo and their physical interaction is important in driving downstream transcriptional programs and in promoting shoot stem cell proliferation. Differences in the overlapping expression patterns of WOX and HAM family members underlie the formation of diverse stem cell niche locations, and the HAM family is essential for all of these stem cell niches. These findings establish a new framework for the control of stem cell production during plant development.
Sampathkumar, A, Krupinski, P, Wightman, R, Milani, P, Berquand, A, Boudaoud, A, Hamant, O, Jönsson, H, Meyerowitz, EM (2014) Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. Elife, 3, e01967. PMCID:PMC3985187. PMID:24740969. doi:10.7554/eLife.01967.
Although it is a central question in biology, how cell shape controls intracellular dynamics largely remains an open question. Here, we show that the shape of Arabidopsis pavement cells creates a stress pattern that controls microtubule orientation, which then guides cell wall reinforcement. Live-imaging, combined with modeling of cell mechanics, shows that microtubules align along the maximal tensile stress direction within the cells, and atomic force microscopy demonstrates that this leads to reinforcement of the cell wall parallel to the microtubules. This feedback loop is regulated: cell-shape derived stresses could be overridden by imposed tissue level stresses, showing how competition between subcellular and supracellular cues control microtubule behavior. Furthermore, at the microtubule level, we identified an amplification mechanism in which mechanical stress promotes the microtubule response to stress by increasing severing activity. These multiscale feedbacks likely contribute to the robustness of microtubule behavior in plant epidermis. DOI:
Sampathkumar, A, Yan, A, Krupinski, P, Meyerowitz, EM (2014) Physical forces regulate plant development and morphogenesis. Curr. Biol., 24(10), R475-83. PMCID:PMC4049271. PMID:24845680. doi:10.1016/j.cub.2014.03.014.
Plant cells in tissues experience mechanical stress not only as a result of high turgor, but also through interaction with their neighbors. Cells can expand at different rates and in different directions from neighbors with which they share a cell wall. This in connection with specific tissue shapes and properties of the cell wall material can lead to intricate stress patterns throughout the tissue. Two cellular responses to mechanical stress are a microtubule cytoskeletal response that directs new wall synthesis so as to resist stress, and a hormone transporter response that regulates transport of the hormone auxin, a regulator of cell expansion. Shape changes in plant tissues affect the pattern of stresses in the tissues, and at the same time, via the cellular stress responses, the pattern of stresses controls cell growth, which in turn changes tissue shape, and stress pattern. This feedback loop controls plant morphogenesis, and explains several previously mysterious aspects of plant growth.
Wellmer, F, Bowman, JL, Davies, B, Ferrándiz, C, Fletcher, JC, Franks, RG, Graciet, E, Gregis, V, Ito, T, Jack, TP, Jiao, Y, Kater, MM, Ma, H, Meyerowitz, EM, Prunet, N, Riechmann, JL (2014) Flower development: open questions and future directions. Methods Mol. Biol., 1110, 103-24. PMID:24395254. doi:10.1007/978-1-4614-9408-9_5.
Almost three decades of genetic and molecular analyses have resulted in detailed insights into many of the processes that take place during flower development and in the identification of a large number of key regulatory genes that control these processes. Despite this impressive progress, many questions about how flower development is controlled in different angiosperm species remain unanswered. In this chapter, we discuss some of these open questions and the experimental strategies with which they could be addressed. Specifically, we focus on the areas of floral meristem development and patterning, floral organ specification and differentiation, as well as on the molecular mechanisms underlying the evolutionary changes that have led to the astounding variations in flower size and architecture among extant and extinct angiosperms.
Nimchuk, Z., Zhou, Y. and Meyerowitz, E.M. (2014) Little peptides with big roles: regulation of apical meristems by CLE peptides. Annual Plant Reviews, Peptide Signals in Plants, eds. G. Pearce and A. Huffaker, Wiley-Blackwell, in press.
Abstract, when available, will be posted here.


Shapiro, BE, Meyerowitz, EM, Mjolsness, E (2013) Using cellzilla for plant growth simulations at the cellular level. Front Plant Sci, 4, 408. PMCID:PMC3797531. PMID:24137172. doi:10.3389/fpls.2013.00408.
Cellzilla is a two-dimensional tissue simulation platform for plant modeling utilizing Cellerator arrows. Cellerator describes biochemical interactions with a simplified arrow-based notation; all interactions are input as reactions and are automatically translated to the appropriate differential equations using a computer algebra system. Cells are represented by a polygonal mesh of well-mixed compartments. Cell constituents can interact intercellularly via Cellerator reactions utilizing diffusion, transport, and action at a distance, as well as amongst themselves within a cell. The mesh data structure consists of vertices, edges (vertex pairs), and cells (and optional intercellular wall compartments) as ordered collections of edges. Simulations may be either static, in which cell constituents change with time but cell size and shape remain fixed; or dynamic, where cells can also grow. Growth is controlled by Hookean springs associated with each mesh edge and an outward pointing pressure force. Spring rest length grows at a rate proportional to the extension beyond equilibrium. Cell division occurs when a specified constituent (or cell mass) passes a (random, normally distributed) threshold. The orientation of new cell walls is determined either by Errera's rule, or by a potential model that weighs contributions due to equalizing daughter areas, minimizing wall length, alignment perpendicular to cell extension, and alignment perpendicular to actual growth direction.
Li, W, Zhou, Y, Liu, X, Yu, P, Cohen, JD, Meyerowitz, EM (2013) LEAFY controls auxin response pathways in floral primordium formation. Sci Signal, 6(270), ra23. PMID:23572147. doi:10.1126/scisignal.2003937.
The transcription factor LEAFY is a master regulator of flowering and of flower development. It acts as a component of a switch that mediates the transition from the vegetative to the reproductive phase of plant development. Auxin is a plant hormone with many different roles in plant growth, including the induction of new primordia of both leaves and flowers at the shoot apex. We report that LEAFY acts in part by controlling the auxin response pathway in new primordia. Therefore, regulation of flower development by transcriptional master regulators and hormonal control of morphogenesis appear to be interacting processes. We found that hormone perception not only controls but is also controlled by the transcriptional signals that create plant form.
Zhang, X, Zhou, Y, Ding, L, Wu, Z, Liu, R, Meyerowitz, EM (2013) Transcription repressor HANABA TARANU controls flower development by integrating the actions of multiple hormones, floral organ specification genes, and GATA3 family genes in Arabidopsis. Plant Cell, 25(1), 83-101. PMCID:PMC3584552. PMID:23335616. doi:10.1105/tpc.112.107854..
Plant inflorescence meristems and floral meristems possess specific boundary domains that result in proper floral organ separation and specification. HANABA TARANU (HAN) encodes a boundary-expressed GATA3-type transcription factor that regulates shoot meristem organization and flower development in Arabidopsis thaliana, but the underlying mechanism remains unclear. Through time-course microarray analyses following transient overexpression of HAN, we found that HAN represses hundreds of genes, especially genes involved in hormone responses and floral organ specification. Transient overexpression of HAN also represses the expression of HAN and three other GATA3 family genes, HANL2 (HAN-LIKE 2), GNC (GATA, NITRATE-INDUCIBLE, CARBON-METABOLISM-INVOLVED), and GNL (GNC-LIKE), forming a negative regulatory feedback loop. Genetic analysis indicates that HAN and the three GATA3 family genes coordinately regulate floral development, and their expression patterns are partially overlapping. HAN can homodimerize and heterodimerize with the three proteins encoded by these genes, and HAN directly binds to its own promoter and the GNC promoter in vivo. These findings, along with the fact that constitutive overexpression of HAN produces an even stronger phenotype than the loss-of-function mutation, support the hypothesis that HAN functions as a key repressor that regulates floral development via regulatory networks involving genes in the GATA3 family, along with genes involved in hormone action and floral organ specification.
Sugimoto, K, Meyerowitz, EM (2013) Regeneration in Arabidopsis tissue culture. Methods Mol. Biol., 959, 265-75. PMID:23299682. doi:10.1007/978-1-62703-221-6_18.
An entire Arabidopsis plant can be regenerated from a small piece of tissue by two sequential hormonal treatments in tissue culture. Currently this in vitro regeneration system is a good system to study the mechanism by which plants show regenerative plasticity. Also, it is useful to test the hormone sensitivity of plants and to propagate sterile lines in Arabidopsis. Here we describe a standard protocol for regenerating Arabidopsis plants in tissue culture, and for preparing and observing samples using confocal microscopy to study cells during regeneration.


Bowman, JL, Smyth, DR, Meyerowitz, EM (2012) The ABC model of flower development: then and now. Development, 139(22), 4095-8. PMID:23093420. doi:10.1242/dev.083972.
In 1991, we published a paper in Development that proposed the ABC model of flower development, an early contribution to the genetic analysis of development in plants. In this, we used a series of homeotic mutants, and double and triple mutants, to establish a predictive model of organ specification in developing flowers. This model has served as the basis for much subsequent work, especially towards understanding seed plant evolution. Here, we discuss several aspects of this story, that could be a much longer one. One surprising conclusion is that materials and methods that might have led to similar work, and to the same model, were available 100 years before our experiments, belying the belief that progress in biology necessarily comes from improvements in methods, rather than in concepts.
Roeder, AH, Cunha, A, Ohno, CK, Meyerowitz, EM (2012) Cell cycle regulates cell type in the Arabidopsis sepal. Development, 139(23), 4416-27. PMID:23095885. doi:10.1242/dev.082925.
The formation of cellular patterns during development requires the coordination of cell division with cell identity specification. This coordination is essential in patterning the highly elongated giant cells, which are interspersed between small cells, in the outer epidermis of the Arabidopsis thaliana sepal. Giant cells undergo endocycles, replicating their DNA without dividing, whereas small cells divide mitotically. We show that distinct enhancers are expressed in giant cells and small cells, indicating that these cell types have different identities as well as different sizes. We find that members of the epidermal specification pathway, DEFECTIVE KERNEL1 (DEK1), MERISTEM LAYER1 (ATML1), Arabidopsis CRINKLY4 (ACR4) and HOMEODOMAIN GLABROUS11 (HDG11), control the identity of giant cells. Giant cell identity is established upstream of cell cycle regulation. Conversely, endoreduplication represses small cell identity. These results show not only that cell type affects cell cycle regulation, but also that changes in the cell cycle can regulate cell type.
Segonzac, C, Nimchuk, ZL, Beck, M, Tarr, PT, Robatzek, S, Meyerowitz, EM, Zipfel, C (2012) The shoot apical meristem regulatory peptide CLV3 does not activate innate immunity. Plant Cell, 24(8), 3186-92. PMCID:PMC3462624. PMID:22923673. doi:10.1105/tpc.111.091264.
The Arabidopsis thaliana leucine-rich repeat receptor kinase FLAGELLIN SENSING2 (FLS2) is required for the recognition of bacterial flagellin in innate immunity. Recently, FLS2 was proposed to act as a multispecific receptor recognizing unrelated exogenous and endogenous peptide ligands, including CLAVATA3 (CLV3), a key regulator of shoot meristem stem cell production. Here, we report experimental evidence demonstrating that FLS2 does not recognize CLV3 and that the shoot apical meristem is immune to bacteria independently of CLV3 perception.
Roeder, AH, Cunha, A, Burl, MC, Meyerowitz, EM (2012) A computational image analysis glossary for biologists. Development, 139(17), 3071-80. PMID:22872081. doi:10.1242/dev.076414.
Recent advances in biological imaging have resulted in an explosion in the quality and quantity of images obtained in a digital format. Developmental biologists are increasingly acquiring beautiful and complex images, thus creating vast image datasets. In the past, patterns in image data have been detected by the human eye. Larger datasets, however, necessitate high-throughput objective analysis tools to computationally extract quantitative information from the images. These tools have been developed in collaborations between biologists, computer scientists, mathematicians and physicists. In this Primer we present a glossary of image analysis terms to aid biologists and briefly discuss the importance of robust image analysis in developmental studies.
Chickarmane, VS, Gordon, SP, Tarr, PT, Heisler, MG, Meyerowitz, EM (2012) Cytokinin signaling as a positional cue for patterning the apical-basal axis of the growing Arabidopsis shoot meristem. Proc. Natl. Acad. Sci. U.S.A., 109(10), 4002-7. PMCID:PMC3309735. PMID:22345559. doi:10.1073/pnas.1200636109.
The transcription factor WUSCHEL (WUS) acts from a well-defined domain within the Arabidopsis thaliana shoot apical meristem (SAM) to maintain a stem cell niche. A negative-feedback loop involving the CLAVATA (CLV) signaling pathway regulates the number of WUS-expressing cells and provides the current paradigm for the homeostatic maintenance of stem cell numbers. Despite the continual turnover of cells in the SAM during development, the WUS domain remains patterned at a fixed distance below the shoot apex. Recent work has uncovered a positive-feedback loop between WUS function and the plant hormone cytokinin. Furthermore, loss of function of the cytokinin biosynthetic gene, LONELY GUY (LOG), results in a wus-like phenotype in rice. Herein, we find the Arabidopsis LOG4 gene is expressed in the SAM epidermis. We use this to develop a computational model representing a growing SAM to suggest the plausibility that apically derived cytokinin and CLV signaling, together, act as positional cues for patterning the WUS domain within the stem cell niche. Furthermore, model simulations backed by experimental data suggest a previously unknown negative feedback between WUS function and cytokinin biosynthesis in the Arabidopsis SAM epidermis. These results suggest a plausible dynamic feedback principle by which the SAM stem cell niche is patterned.
Cunha, A, Tarr, PT, Roeder, AH, Altinok, A, Mjolsness, E, Meyerowitz, EM (2012) Computational analysis of live cell images of the Arabidopsis thaliana plant. Methods Cell Biol., 110, 285-323. PMID:22482954. doi:10.1016/B978-0-12-388403-9.00012-6.
Quantitative studies in plant developmental biology require monitoring and measuring the changes in cells and tissues as growth gives rise to intricate patterns. The success of these studies has been amplified by the combined strengths of two complementary techniques, namely live imaging and computational image analysis. Live imaging records time-lapse images showing the spatial-temporal progress of tissue growth with cells dividing and changing shape under controlled laboratory experiments. Image processing and analysis make sense of these data by providing computational ways to extract and interpret quantitative developmental information present in the acquired images. Manual labeling and qualitative interpretation of images are limited as they don't scale well to large data sets and cannot provide field measurements to feed into mathematical and computational models of growth and patterning. Computational analysis, when it can be made sufficiently accurate, is more efficient, complete, repeatable, and less biased. In this chapter, we present some guidelines for the acquisition and processing of images of sepals and the shoot apical meristem of Arabidopsis thaliana to serve as a basis for modeling. We discuss fluorescent markers and imaging using confocal laser scanning microscopy as well as present protocols for doing time-lapse live imaging and static imaging of living tissue. Image segmentation and tracking are discussed. Algorithms are presented and demonstrated together with low-level image processing methods that have proven to be essential in the detection of cell contours. We illustrate the application of these procedures in investigations aiming to unravel the mechanical and biochemical signaling mechanisms responsible for the coordinated growth and patterning in plants.


Wagner, D, Meyerowitz, EM (2011) Switching on Flowers: Transient LEAFY Induction Reveals Novel Aspects of the Regulation of Reproductive Development in Arabidopsis. Front Plant Sci, 2, 60. PMCID:PMC3355602. PMID:22639600. doi:10.3389/fpls.2011.00060.
DEVELOPMENTAL FATE DECISIONS IN CELL POPULATIONS FUNDAMENTALLY DEPEND ON AT LEAST TWO PARAMETERS: a signal that is perceived by the cell and the intrinsic ability of the cell to respond to the signal. The same regulatory logic holds for phase transitions in the life cycle of an organism, for example the switch to reproductive development in flowering plants. Here we have tested the response of the monocarpic plant species Arabidopsis thaliana to a signal that directs flower formation, the plant-specific transcription factor LEAFY (LFY). Using transient steroid-dependent LEAFY (LFY) activation in lfy null mutant Arabidopsis plants, we show that the plant's competence to respond to the LFY signal changes during development. Very early in the life cycle, the plant is not competent to respond to the signal. Subsequently, transient LFY activation can direct primordia at the flanks of the shoot apical meristem to adopt a floral fate. Finally, the plants acquire competence to initiate the flower-patterning program in response to transient LFY activation. Similar to a perennial life strategy, we did not observe reprogramming of all primordia after perception of the transient signal, instead only a small number of meristems responded, followed by reversion to the prior developmental program. The ability to initiate flower formation and to direct flower patterning in response to transient LFY upregulation was dependent on the known direct LFY target APETALA1 (AP1). Prolonged LFY or activation could alter the developmental gradient and bypass the requirement for AP1. Prolonged high AP1 levels, in turn, can also alter the plants' competence. Our findings shed light on how plants can fine-tune important phase transitions and developmental responses.
Romanel, E, Das, P, Amasino, RM, Traas, J, Meyerowitz, E, Alves-Ferreira, M (2011) Reproductive Meristem22 is a unique marker for the early stages of stamen development. Int. J. Dev. Biol., 55(6), 657-64. PMID:21948714. doi:10.1387/ijdb.113340er.
Stamens undergo a very elaborate development program that gives rise not only to many specific tissue types, but also to the male gametes. The specification of stamen identity is coordinated by a group of homeotic genes such as APETALA3 (AP3) and PISTILLATA (PI), AGAMOUS (AG) and SEPALLATA (SEP1-4) genes. Genome-wide transcriptomic comparisons between floral buds of wild-type and ap3 mutants led to the identification of the REM22 gene, which is expressed in the early stages of stamen development. This gene is member of the plant-specific B3 DNA-binding superfamily. In this work, we dissect the spatio-temporal expression pattern of REM22 during the early stages of stamen development. To this end, both in situ hybridization analyses as well as in vivo fluorescence strategies were employed. At stage 4 of flower development, REM22 is expressed exclusively in those undifferentiated cells of the floral meristem that will give rise to the stamen primordia. At stage 5, REM22 expression is restricted to the epidermal and the subepidermal layers of anther primordia. Later, this expression is confined to the middle layer and the differentiating tapetal cells. After stage 10 when all the tissues of the anther have differentiated, REM22 expression is no longer detectable. Furthermore, we examined the pREM22::GUS-GFP marker line in an inducible system where the ectopic AG function is used to promote microsporogenesis. The data support the idea that REM22 expression is a useful marker to study the early stages of stamen development.
Nimchuk, ZL, Tarr, PT, Meyerowitz, EM (2011) An evolutionarily conserved pseudokinase mediates stem cell production in plants. Plant Cell, 23(3), 851-4. PMCID:PMC3082267. PMID:21398569. doi:10.1105/tpc.110.075622.
Sequence comparisons, biochemical experiments, and studies with mutants in transgenic plants show that the Arabidopsis protein CORYNE, currently thought to be a kinase that acts as part of a receptor kinase complex, is likely to be a pseudokinase and not a kinase.
Roeder, AH, Tarr, PT, Tobin, C, Zhang, X, Chickarmane, V, Cunha, A, Meyerowitz, EM (2011) Computational morphodynamics of plants: integrating development over space and time. Nat. Rev. Mol. Cell Biol., 12(4), 265-73. PMID:21364682. doi:10.1038/nrm3079.
The emerging field of computational morphodynamics aims to understand the changes that occur in space and time during development by combining three technical strategies: live imaging to observe development as it happens; image processing and analysis to extract quantitative information; and computational modelling to express and test time-dependent hypotheses. The strength of the field comes from the iterative and combined use of these techniques, which has provided important insights into plant development.
Nimchuk, ZL, Tarr, PT, Ohno, C, Qu, X, Meyerowitz, EM (2011) Plant stem cell signaling involves ligand-dependent trafficking of the CLAVATA1 receptor kinase. Curr. Biol., 21(5), 345-52. PMCID:PMC3072602. PMID:21333538. doi:10.1016/j.cub.2011.01.039.
Cell numbers in above-ground meristems of plants are thought to be maintained by a feedback loop driven by perception of the glycopeptide ligand CLAVATA3 (CLV3) by the CLAVATA1 (CLV1) receptor kinase and the CLV2/CORYNE (CRN) receptor-like complex. CLV3 produced in the stem cells at the meristem apex limits the expression level of the stem cell-promoting homeodomain protein WUSCHEL (WUS) in the cells beneath, where CLV1 and WUS RNA are localized. WUS downregulation nonautonomously reduces stem cell proliferation. Overexpression of CLV3 eliminates the stem cells, causing meristem termination, and loss of CLV3 function allows meristem overproliferation. There are many questions regarding the CLV3/CLV1 interaction, including where in the meristem it occurs, how it is regulated, and how it is that a large range of CLV3 concentrations gives no meristem size phenotype.


Sugimoto, K, Gordon, SP, Meyerowitz, EM (2011) Regeneration in plants and animals: dedifferentiation, transdifferentiation, or just differentiation? Trends Cell Biol., 21(4), 212-8. PMID:21236679. doi:10.1016/j.tcb.2010.12.004.
The textbooks and literature of plant biology indicate that plant cells are totipotent, and that regeneration occurs via dedifferentiation, by which the cell and its descendents recapitulate earlier stages of development. However, recent work on the generation of callus, a presumed undifferentiated or dedifferentiated and disorganized cellular mass, indicates that the cells of callus are neither, and that callus forms predominantly from a pre-existing population of stem cells. Recent work in animal regeneration, for example in salamander limbs, also indicates that previous assumptions about the extent of dedifferentiation and pluripotency in animals are in need of critical reassessment. We review here some of these data, compare plant and animal regeneration, and argue that the importance of dedifferentiation and plasticity in regenerating systems is due for reevaluation.
Jaillais, Y, Hothorn, M, Belkhadir, Y, Dabi, T, Nimchuk, ZL, Meyerowitz, EM, Chory, J (2011) Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor. Genes Dev., 25(3), 232-7. PMCID:PMC3034898. PMID:21289069. doi:10.1101/gad.2001911.
Receptor tyrosine kinases control many critical processes in metazoans, but these enzymes appear to be absent in plants. Recently, two Arabidopsis receptor kinases--BRASSINOSTEROID INSENSITIVE 1 (BRI1) and BRI1-ASSOCIATED KINASE1 (BAK1), the receptor and coreceptor for brassinosteroids--were shown to autophosphorylate on tyrosines. However, the cellular roles for tyrosine phosphorylation in plants remain poorly understood. Here, we report that the BRI1 KINASE INHIBITOR 1 (BKI1) is tyrosine phosphorylated in response to brassinosteroid perception. Phosphorylation occurs within a reiterated [KR][KR] membrane targeting motif, releasing BKI1 into the cytosol and enabling formation of an active signaling complex. Our work reveals that tyrosine phosphorylation is a conserved mechanism controlling protein localization in all higher organisms.
Álvarez-Buylla, E.R., Ambrose, B.A., Flores-Sandoval, E., Vergara-Silva, F., Englund, M., Garay-Arroyo, A., García-Ponce, B., de la Torre-Bárcena, E., Espinosa-Matías, Martínez, E., Pińeyro-Nelson, A., Engström, P., Meyerowitz, E.M. (2010) B-function expression in the flower center underlies the homeotic phenotype of Lacandonia schismatica (Triuridaceae). Plant Cell 22, 3543-3559. PMCID: PMC3015125. doi: 10.1105/tpc.111.230160.
Intercellular signaling is essential for the coordination of growth and development in higher plants. Although hundreds of putative receptors have been identified in Arabidopsis (Arabidopsis thaliana), only a few families of extracellular signaling molecules have been discovered, and their biological roles are largely unknown. To expand our insight into the developmental processes potentially regulated by ligand-mediated signal transduction pathways, we undertook a systematic expression analysis of the members of the Arabidopsis CLAVATA3/ESR-RELATED (CLE) small signaling polypeptide family. Using reporter constructs, we show that the CLE genes have distinct and specific patterns of promoter activity. We find that each Arabidopsis tissue expresses at least one CLE gene, indicating that CLE-mediated signaling pathways are likely to play roles in many biological processes during the plant life cycle. Some CLE genes that are closely related in sequence have dissimilar expression profiles, yet in many tissues multiple CLE genes have overlapping patterns of promoter-driven reporter activity. This observation, plus the general absence of detectable morphological phenotypes in cle null mutants, suggest that a high degree of functional redundancy exists among CLE gene family members. Our work establishes a community resource of CLE-related biological materials and provides a platform for understanding and ultimately manipulating many different plant signaling systems.
Jun, J, Fiume, E, Roeder, AH, Meng, L, Sharma, VK, Osmont, KS, Baker, C, Ha, CM, Meyerowitz, EM, Feldman, LJ, Fletcher, JC (2010) Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis. Plant Physiol., 154(4), 1721-36. PMCID:PMC2996011. PMID:20884811. doi:10.1104/pp.110.163683.
Intercellular signaling is essential for the coordination of growth and development in higher plants. Although hundreds of putative receptors have been identified in Arabidopsis (Arabidopsis thaliana), only a few families of extracellular signaling molecules have been discovered, and their biological roles are largely unknown. To expand our insight into the developmental processes potentially regulated by ligand-mediated signal transduction pathways, we undertook a systematic expression analysis of the members of the Arabidopsis CLAVATA3/ESR-RELATED (CLE) small signaling polypeptide family. Using reporter constructs, we show that the CLE genes have distinct and specific patterns of promoter activity. We find that each Arabidopsis tissue expresses at least one CLE gene, indicating that CLE-mediated signaling pathways are likely to play roles in many biological processes during the plant life cycle. Some CLE genes that are closely related in sequence have dissimilar expression profiles, yet in many tissues multiple CLE genes have overlapping patterns of promoter-driven reporter activity. This observation, plus the general absence of detectable morphological phenotypes in cle null mutants, suggest that a high degree of functional redundancy exists among CLE gene family members. Our work establishes a community resource of CLE-related biological materials and provides a platform for understanding and ultimately manipulating many different plant signaling systems.
Jiao, Y, Meyerowitz, EM (2010) Cell-type specific analysis of translating RNAs in developing flowers reveals new levels of control. Mol. Syst. Biol., 6, 419. PMCID:PMC2990639. PMID:20924354. doi:10.1038/msb.2010.76.
Determining both the expression levels of mRNA and the regulation of its translation is important in understanding specialized cell functions. In this study, we describe both the expression profiles of cells within spatiotemporal domains of the Arabidopsis thaliana flower and the post-transcriptional regulation of these mRNAs, at nucleotide resolution. We express a tagged ribosomal protein under the promoters of three master regulators of flower development. By precipitating tagged polysomes, we isolated cell type-specific mRNAs that are probably translating, and quantified those mRNAs through deep sequencing. Cell type comparisons identified known cell-specific transcripts and uncovered many new ones, from which we inferred cell type-specific hormone responses, promoter motifs and coexpressed cognate binding factor candidates, and splicing isoforms. By comparing translating mRNAs with steady-state overall transcripts, we found evidence for widespread post-transcriptional regulation at both the intron splicing and translational stages. Sequence analyses identified structural features associated with each step. Finally, we identified a new class of noncoding RNAs associated with polysomes. Findings from our profiling lead to new hypotheses in the understanding of flower development.
Hamant, O., Meyerowitz, E.M. and Traas, J. (2011) Is cell polarity under mechanical control in plants? Plant Signaling and Behavior 6, 137-137. PMCID: PMC3122027. PMID: 21258209 doi: 10.4161/psb.6.1.14269
Plant cells experience a tremendous amount of mechanical stress caused by turgor pressure. Because cells are glued to their neighbors by the middle lamella, supracellular patterns of physical forces are emerging during growth, usually leading to tension in the epidermis. Cortical microtubules have been shown to reorient in response to these mechanical stresses, and to resist them, indirectly via their impact on the anisotropic structure of the cell wall. In a recent study, we show that the polar localization of the auxin efflux carrier PIN1 can also be under the control of physical forces, thus linking cell growth rate and anisotropy by a common mechanical signal. Because of the known impact of auxin on the stiffness of the cell wall, this suggests that the mechanical properties of the extracellular matrix play a crucial signaling role in morphogenesis, notably controlling the polarity of the cell, as observed in animal systems.
Heisler, MG, Hamant, O, Krupinski, P, Uyttewaal, M, Ohno, C, Jönsson, H, Traas, J, Meyerowitz, EM (2010) Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biol., 8(10), e1000516. PMCID:PMC2957402. PMID:20976043. doi:10.1371/journal.pbio.1000516.
Morphogenesis during multicellular development is regulated by intercellular signaling molecules as well as by the mechanical properties of individual cells. In particular, normal patterns of organogenesis in plants require coordination between growth direction and growth magnitude. How this is achieved remains unclear. Here we show that in Arabidopsis thaliana, auxin patterning and cellular growth are linked through a correlated pattern of auxin efflux carrier localization and cortical microtubule orientation. Our experiments reveal that both PIN1 localization and microtubule array orientation are likely to respond to a shared upstream regulator that appears to be biomechanical in nature. Lastly, through mathematical modeling we show that such a biophysical coupling could mediate the feedback loop between auxin and its transport that underlies plant phyllotaxis.
Roeder, AH, Chickarmane, V, Cunha, A, Obara, B, Manjunath, BS, Meyerowitz, EM (2010) Variability in the control of cell division underlies sepal epidermal patterning in Arabidopsis thaliana. PLoS Biol., 8(5), e1000367. PMCID:PMC2867943. PMID:20485493. doi:10.1371/journal.pbio.1000367..
How growth and proliferation are precisely controlled in organs during development and how the regulation of cell division contributes to the formation of complex cell type patterns are important questions in developmental biology. Such a pattern of diverse cell sizes is characteristic of the sepals, the outermost floral organs, of the plant Arabidopsis thaliana. To determine how the cell size pattern is formed in the sepal epidermis, we iterate between generating predictions from a computational model and testing these predictions through time-lapse imaging. We show that the cell size diversity is due to the variability in decisions of individual cells about when to divide and when to stop dividing and enter the specialized endoreduplication cell cycle. We further show that altering the activity of cell cycle inhibitors biases the timing and changes the cell size pattern as our model predicts. Models and observations together demonstrate that variability in the time of cell division is a major determinant in the formation of a characteristic pattern.
Kaufmann, K, Wellmer, F, Muiño, JM, Ferrier, T, Wuest, SE, Kumar, V, Serrano-Mislata, A, Madueño, F, Krajewski, P, Meyerowitz, EM, Angenent, GC, Riechmann, JL (2010) Orchestration of floral initiation by APETALA1. Science, 328(5974), 85-9. PMID:20360106. doi:10.1126/science.1185244.
The MADS-domain transcription factor APETALA1 (AP1) is a key regulator of Arabidopsis flower development. To understand the molecular mechanisms underlying AP1 function, we identified its target genes during floral initiation using a combination of gene expression profiling and genome-wide binding studies. Many of its targets encode transcriptional regulators, including known floral repressors. The latter genes are down-regulated by AP1, suggesting that it initiates floral development by abrogating the inhibitory effects of these genes. Although AP1 acts predominantly as a transcriptional repressor during the earliest stages of flower development, at more advanced stages it also activates regulatory genes required for floral organ formation, indicating a dynamic mode of action. Our results further imply that AP1 orchestrates floral initiation by integrating growth, patterning, and hormonal pathways.
Cunha, AL, Roeder, AH, Meyerowitz, EM (2010) Segmenting the sepal and shoot apical meristem of Arabidopsis thaliana. Conf Proc IEEE Eng Med Biol Soc, 2010, 5338-42. PMID:21096072. doi:10.1109/IEMBS.2010.5626342.
We present methods for segmenting the sepal and shoot apical meristem of the Arabidopsis thaliana plant. We propose a mathematical morphology pipeline and a modified numerical scheme for the active contours without edges algorithm to extract the geometry and topology of plant cells imaged using confocal laser scanning microscopy. We demonstrate our methods in typical images used in the studies of cell endoreduplication and hormone transport and show that in practice they produce highly accurate results requiring little human intervention to cope with image aberrations.
Chickarmane, V, Roeder, AH, Tarr, PT, Cunha, A, Tobin, C, Meyerowitz, EM (2010) Computational morphodynamics: a modeling framework to understand plant growth. Annu Rev Plant Biol, 61, 65-87. PMID:20192756. doi:10.1146/annurev-arplant-042809-112213.
Computational morphodynamics utilizes computer modeling to understand the development of living organisms over space and time. Results from biological experiments are used to construct accurate and predictive models of growth. These models are then used to make novel predictions that provide further insight into the processes involved, which can be tested experimentally to either confirm or rule out the validity of the computational models. This review highlights two fundamental challenges: (a) to understand the feedback between mechanics of growth and chemical or molecular signaling, and (b) to design models that span and integrate single cell behavior with tissue development. We review different approaches to model plant growth and discuss a variety of model types that can be implemented to demonstrate how the interplay between computational modeling and experimentation can be used to explore the morphodynamics of plant development.
Sugimoto, K, Jiao, Y, Meyerowitz, EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev. Cell, 18(3), 463-71. PMID:20230752. doi:10.1016/j.devcel.2010.02.004.
Unlike most animal cells, plant cells can easily regenerate new tissues from a wide variety of organs when properly cultured. The common elements that provide varied plant cells with their remarkable regeneration ability are still largely unknown. Here we describe the initial process of Arabidopsis in vitro regeneration, where a pluripotent cell mass termed callus is induced. We demonstrate that callus resembles the tip of a root meristem, even if it is derived from aerial organs such as petals, which clearly shows that callus formation is not a simple reprogramming process backward to an undifferentiated state as widely believed. Furthermore, callus formation in roots, cotyledons, and petals is blocked in mutant plants incapable of lateral root initiation. It thus appears that the ectopic activation of a lateral root development program is a common mechanism in callus formation from multiple organs.


Gordon, SP, Chickarmane, VS, Ohno, C, Meyerowitz, EM (2009) Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc. Natl. Acad. Sci. U.S.A., 106(38), 16529-34. PMCID:PMC2752578. PMID:19717465. doi:10.1073/pnas.0908122106.
A central unanswered question in stem cell biology, both in plants and in animals, is how the spatial organization of stem cell niches are maintained as cells move through them. We address this question for the shoot apical meristem (SAM) which harbors pluripotent stem cells responsible for growth of above-ground tissues in flowering plants. We find that localized perception of the plant hormone cytokinin establishes a spatial domain in which cell fate is respecified through induction of the master regulator WUSCHEL as cells are displaced during growth. Cytokinin-induced WUSCHEL expression occurs through both CLAVATA-dependent and CLAVATA-independent pathways. Computational analysis shows that feedback between cytokinin response and genetic regulators predicts their relative patterning, which we confirm experimentally. Our results also may explain how increasing cytokinin concentration leads to the first steps in reestablishing the shoot stem cell niche in vitro.
Graciet, E, Walter, F, Maoiléidigh, DO, Pollmann, S, Meyerowitz, EM, Varshavsky, A, Wellmer, F (2009) The N-end rule pathway controls multiple functions during Arabidopsis shoot and leaf development. Proc. Natl. Acad. Sci. U.S.A., 106(32), 13618-23. PMCID:PMC2726413. PMID:19620738. doi:10.1073/pnas.0906404106.
The ubiquitin-dependent N-end rule pathway relates the in vivo half-life of a protein to the identity of its N-terminal residue. This proteolytic system is present in all organisms examined and has been shown to have a multitude of functions in animals and fungi. In plants, however, the functional understanding of the N-end rule pathway is only beginning. The N-end rule has a hierarchic structure. Destabilizing activity of N-terminal Asp, Glu, and (oxidized) Cys requires their conjugation to Arg by an arginyl-tRNA-protein transferase (R-transferase). The resulting N-terminal Arg is recognized by the pathway's E3 ubiquitin ligases, called "N-recognins." Here, we show that the Arabidopsis R-transferases AtATE1 and AtATE2 regulate various aspects of leaf and shoot development. We also show that the previously identified N-recognin PROTEOLYSIS6 (PRT6) mediates these R-transferase-dependent activities. We further demonstrate that the arginylation branch of the N-end rule pathway plays a role in repressing the meristem-promoting BREVIPEDICELLUS (BP) gene in developing leaves. BP expression is known to be excluded from Arabidopsis leaves by the activities of the ASYMMETRIC LEAVES1 (AS1) transcription factor complex and the phytohormone auxin. Our results suggest that AtATE1 and AtATE2 act redundantly with AS1, but independently of auxin, in the control of leaf development.
Das, P, Ito, T, Wellmer, F, Vernoux, T, Dedieu, A, Traas, J, Meyerowitz, EM (2009) Floral stem cell termination involves the direct regulation of AGAMOUS by PERIANTHIA. Development, 136(10), 1605-11. PMID:19395638. doi:10.1242/dev.035436.
In Arabidopsis, the population of stem cells present in young flower buds is lost after the production of a fixed number of floral organs. The precisely timed repression of the stem cell identity gene WUSCHEL (WUS) by the floral homeotic protein AGAMOUS (AG) is a key part of this process. In this study, we report on the identification of a novel input into the process of floral stem cell regulation. We use genetics and chromatin immunoprecipitation assays to demonstrate that the bZIP transcription factor PERIANTHIA (PAN) plays a role in regulating stem cell fate by directly controlling AG expression and suggest that this activity is spatially restricted to the centermost region of the AG expression domain. These results suggest that the termination of floral stem cell fate is a multiply redundant process involving loci with unrelated floral patterning functions.
Harrison, CJ, Roeder, AH, Meyerowitz, EM, Langdale, JA (2009) Local cues and asymmetric cell divisions underpin body plan transitions in the moss Physcomitrella patens. Curr. Biol., 19(6), 461-71. PMID:19303301. doi:10.1016/j.cub.2009.02.050.
Land plants evolved from aquatic algae more than 450 million years ago. Algal sisters of land plants grow through the activity of apical initial cells that cleave either in one plane to generate filaments or in two planes to generate mats. Acquisition of the capacity for cell cleavage in three planes facilitated the formation of upright bushy body plans and enabled the invasion of land. Evolutionary transitions between filamentous, planar, and bushy growth are mimicked within moss life cycles.


Shapiro, B.E., Jönsson, H., Sahlin, P., Heisler, M., Roeder, A., Burl, M., Meyerowitz, E.M. and E.D. Mjolsness (2008) Tessellations and Pattern Formation in Plant Growth and Development. In Tessellations in the Sciences: Virtues, Techniques and Applications of Geometric Tilings, eds. Van de Weijgaert, R., Vegter, G., Ritzerveld, J. and Icke, V., Springer-Verlag.
Abstract, when available, will be posted here.
Hamant, O, Heisler, MG, Jönsson, H, Krupinski, P, Uyttewaal, M, Bokov, P, Corson, F, Sahlin, P, Boudaoud, A, Meyerowitz, EM, Couder, Y, Traas, J (2008) Developmental patterning by mechanical signals in Arabidopsis. Science, 322(5908), 1650-5. PMID:19074340. doi:10.1126/science.1165594.
A central question in developmental biology is whether and how mechanical forces serve as cues for cellular behavior and thereby regulate morphogenesis. We found that morphogenesis at the Arabidopsis shoot apex depends on the microtubule cytoskeleton, which in turn is regulated by mechanical stress. A combination of experiments and modeling shows that a feedback loop encompassing tissue morphology, stress patterns, and microtubule-mediated cellular properties is sufficient to account for the coordinated patterns of microtubule arrays observed in epidermal cells, as well as for patterns of apical morphogenesis.
Jiao, Y, Riechmann, JL, Meyerowitz, EM (2008) Transcriptome-wide analysis of uncapped mRNAs in Arabidopsis reveals regulation of mRNA degradation. Plant Cell, 20(10), 2571-85. PMCID:PMC2590717. PMID:18952771. doi:10.1105/tpc.108.062786.
The composition of the transcriptome is determined by a balance between mRNA synthesis and degradation. An important route for mRNA degradation produces uncapped mRNAs, and this decay process can be initiated by decapping enzymes, endonucleases, and small RNAs. Although uncapped mRNAs are an important intermediate for mRNA decay, their identity and abundance have never been studied on a large scale until recently. Here, we present an experimental method for transcriptome-wide profiling of uncapped mRNAs that can be used in any eukaryotic system. We applied the method to study the prevalence of uncapped transcripts during the early stages of Arabidopsis thaliana flower development. Uncapped transcripts were identified for the majority of expressed genes, although at different levels. By comparing uncapped RNA levels with steady state overall transcript levels, our study provides evidence for widespread mRNA degradation control in numerous biological processes involving genes of varied molecular functions, implying that uncapped mRNA levels are dynamically regulated. Sequence analyses identified structural features of transcripts and cis-elements that were associated with different levels of uncapping. These transcriptome-wide profiles of uncapped mRNAs will aid in illuminating new regulatory mechanisms of eukaryotic transcriptional networks.
Li, D, Liu, C, Shen, L, Wu, Y, Chen, H, Robertson, M, Helliwell, CA, Ito, T, Meyerowitz, E, Yu, H (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev. Cell, 15(1), 110-20. PMID:18606145. doi:10.1016/j.devcel.2008.05.002.
Multiple genetic pathways act in response to developmental cues and environmental signals to promote the floral transition, by regulating several floral pathway integrators. These include FLOWERING LOCUS T (FT) and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1). We show that the flowering repressor SHORT VEGETATIVE PHASE (SVP) is controlled by the autonomous, thermosensory, and gibberellin pathways, and directly represses SOC1 transcription in the shoot apex and leaf. Moreover, FT expression in the leaf is also modulated by SVP. SVP protein associates with the promoter regions of SOC1 and FT, where another potent repressor FLOWERING LOCUS C (FLC) binds. SVP consistently interacts with FLC in vivo during vegetative growth and their function is mutually dependent. Our findings suggest that SVP is another central regulator of the flowering regulatory network, and that the interaction between SVP and FLC mediated by various flowering genetic pathways governs the integration of flowering signals.
Jones, AM, Chory, J, Dangl, JL, Estelle, M, Jacobsen, SE, Meyerowitz, EM, Nordborg, M, Weigel, D (2008) The impact of Arabidopsis on human health: diversifying our portfolio. Cell, 133(6), 939-43. PMCID:PMC3124625. PMID:18555767. doi:10.1016/j.cell.2008.05.040.
Studies of the model plant Arabidopsis thaliana may seem to have little impact on advances in medical research, yet a survey of the scientific literature shows that this is a misconception. Many discoveries with direct relevance to human health and disease have been elaborated using Arabidopsis, and several processes important to human biology are more easily studied in this versatile model plant.
Haswell, ES, Peyronnet, R, Barbier-Brygoo, H, Meyerowitz, EM, Frachisse, JM (2008) Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root. Curr. Biol., 18(10), 730-4. PMID:18485707. doi:10.1016/j.cub.2008.04.039.
In bacterial and animal systems, mechanosensitive (MS) ion channels are thought to mediate the perception of pressure, touch, and sound [1-3]. Although plants respond to a wide variety of mechanical stimuli, and although many mechanosensitive channel activities have been characterized in plant membranes by the patch-clamp method, the molecular nature of mechanoperception in plant systems has remained elusive [4]. Likely candidates are relatives of MscS (Mechanosensitive channel of small conductance), a well-characterized MS channel that serves to protect E. coli from osmotic shock [5]. Ten MscS-Like (MSL) proteins are found in the genome of the model flowering plant Arabidopsis thaliana[4, 6, 7]. MSL2 and MSL3, along with MSC1, a MscS family member from green algae, are implicated in the control of organelle morphology [8, 9]. Here, we characterize MSL9 and MSL10, two MSL proteins found in the plasma membrane of root cells. We use a combined genetic and electrophysiological approach to show that MSL9 and MSL10, along with three other members of the MSL family, are required for MS channel activities detected in protoplasts derived from root cells. This is the first molecular identification and characterization of MS channels in plant membranes.


Ito, T, Ng, KH, Lim, TS, Yu, H, Meyerowitz, EM (2007) The homeotic protein AGAMOUS controls late stamen development by regulating a jasmonate biosynthetic gene in Arabidopsis. Plant Cell, 19(11), 3516-29. PMCID:PMC2174883. PMID:17981996. doi:10.1105/tpc.107.055467.
The Arabidopsis thaliana floral homeotic gene AGAMOUS (AG) plays a central role in reproductive organ (stamen and carpel) development. AG RNA is expressed in the center of floral primordia from a time prior to the initiation of stamen and carpel primordia until late in flower development. While early AG expression acts in specification of stamens and carpels, the role, if any, of continued AG expression in later flower development is unknown. To examine the timing of AG action and its possible late-stage functions, we performed a series of time-course experiments using a transgenic line with inducible AG activity in an ag homozygous mutant background. We show that AG controls late-stage stamen development, including anther morphogenesis and dehiscence, as well as filament formation and elongation. We further show that AG coordinates late stamen maturation by controlling a biosynthetic gene of the lipid-derived phytohormone jasmonic acid (JA). Expression analysis and in vivo binding of AG indicate that AG directly regulates the transcription of a catalytic enzyme of JA, DEFECTIVE IN ANTHER DEHISCENCE1. Our results indicate that stamen identity and differentiation control by AG is achieved by the regulation of different transcriptional cascades in different floral stages, with organ specification induced early, followed by phytohormone biosynthesis to coordinate stamen maturation.
Alves-Ferreira, M, Wellmer, F, Banhara, A, Kumar, V, Riechmann, JL, Meyerowitz, EM (2007) Global expression profiling applied to the analysis of Arabidopsis stamen development. Plant Physiol., 145(3), 747-62. PMCID:PMC2048804. PMID:17905860. doi:10.1104/pp.107.104422.
To obtain detailed information about gene expression during stamen development in Arabidopsis (Arabidopsis thaliana), we compared, by microarray analysis, the gene expression profile of wild-type inflorescences to those of the floral mutants apetala3, sporocyteless/nozzle, and male sterile1 (ms1), in which different aspects of stamen formation are disrupted. These experiments led to the identification of groups of genes with predicted expression at early, intermediate, and late stages of stamen development. Validation experiments using in situ hybridization confirmed the predicted expression patterns. Additional experiments aimed at characterizing gene expression specifically during microspore formation. To this end, we compared the gene expression profiles of wild-type flowers of distinct developmental stages to those of the ms1 mutant. Computational analysis of the datasets derived from this experiment led to the identification of genes that are likely involved in the control of key developmental processes during microsporogenesis. We also identified a large number of genes whose expression is prolonged in ms1 mutant flowers compared to the wild type. This result suggests that MS1, which encodes a putative transcriptional regulator, is involved in the stage-specific repression of these genes. Lastly, we applied reverse genetics to characterize several of the genes identified in the microarray experiments and uncovered novel regulators of microsporogenesis, including the transcription factor MYB99 and a putative phosphatidylinositol 4-kinase.
Gordon, SP, Heisler, MG, Reddy, GV, Ohno, C, Das, P, Meyerowitz, EM (2007) Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development, 134(19), 3539-48. PMID:17827180. doi:10.1242/dev.010298.
Most multicellular organisms have a capacity to regenerate tissue after wounding. Few, however, have the ability to regenerate an entire new body from adult tissue. Induction of new shoot meristems from cultured root explants is a widely used, but poorly understood, process in which apical plant tissues are regenerated from adult somatic tissue through the de novo formation of shoot meristems. We characterize early patterning during de novo development of the Arabidopsis shoot meristem using fluorescent reporters of known gene and protein activities required for shoot meristem development and maintenance. We find that a small number of progenitor cells initiate development of new shoot meristems through stereotypical stages of reporter expression and activity of CUP-SHAPED COTYLEDON 2 (CUC2), WUSCHEL (WUS), PIN-FORMED 1 (PIN1), SHOOT-MERISTEMLESS (STM), FILAMENTOUS FLOWER (FIL, also known as AFO), REVOLUTA (REV), ARABIDOPSIS THALIANA MERISTEM L1 LAYER (ATML1) and CLAVATA 3 (CLV3). Furthermore, we demonstrate a functional requirement for WUS activity during de novo shoot meristem initiation. We propose that de novo shoot meristem induction is an easily accessible system for the study of patterning and self-organization in the well-studied model organism Arabidopsis.
Michniewicz, M, Zago, MK, Abas, L, Weijers, D, Schweighofer, A, Meskiene, I, Heisler, MG, Ohno, C, Zhang, J, Huang, F, Schwab, R, Weigel, D, Meyerowitz, EM, Luschnig, C, Offringa, R, Friml, J (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell, 130(6), 1044-56. PMID:17889649. doi:10.1016/j.cell.2007.07.033.
In plants, cell polarity and tissue patterning are connected by intercellular flow of the phytohormone auxin, whose directional signaling depends on polar subcellular localization of PIN auxin transport proteins. The mechanism of polar targeting of PINs or other cargos in plants is largely unidentified, with the PINOID kinase being the only known molecular component. Here, we identify PP2A phosphatase as an important regulator of PIN apical-basal targeting and auxin distribution. Genetic analysis, localization, and phosphorylation studies demonstrate that PP2A and PINOID both partially colocalize with PINs and act antagonistically on the phosphorylation state of their central hydrophilic loop, hence mediating PIN apical-basal polar targeting. Thus, in plants, polar sorting by the reversible phosphorylation of cargos allows for their conditional delivery to specific intracellular destinations. In the case of PIN proteins, this mechanism enables switches in the direction of intercellular auxin fluxes, which mediate differential growth, tissue patterning, and organogenesis.
Reddy, GV, Gordon, SP, Meyerowitz, EM (2007) Unravelling developmental dynamics: transient intervention and live imaging in plants. Nat. Rev. Mol. Cell Biol., 8(6), 491-501. PMID:17522592. doi:10.1038/nrm2188.
Plant development is dynamic in nature. This is exemplified in developmental patterning, in which roots and shoots rapidly elongate while simultaneously giving rise to precisely positioned new organs over a time course of minutes to hours. In this Review, we emphasize the insights gained from simultaneous use of live imaging and transient perturbation technologies to capture the dynamic properties of plant processes.
Sieber, P, Wellmer, F, Gheyselinck, J, Riechmann, JL, Meyerowitz, EM (2007) Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness. Development, 134(6), 1051-60. PMID:17287247. doi:10.1242/dev.02817.
In plants, members of microRNA (miRNA) families are often predicted to target the same or overlapping sets of genes. It has thus been hypothesized that these miRNAs may act in a functionally redundant manner. This hypothesis is tested here by studying the effects of elimination of all three members of the MIR164 family from Arabidopsis. It was found that a loss of miR164 activity leads to a severe disruption of shoot development, in contrast to the effect of mutation in any single MIR164 gene. This indicates that these miRNAs are indeed functionally redundant. Differences in the expression patterns of the individual MIR164 genes imply, however, that redundancy among them is not complete, and that these miRNAs show functional specialization. Furthermore, the results of molecular and genetic analyses of miR164-mediated target regulation indicate that miR164 miRNAs function to control the transcript levels, as well as the expression patterns, of their targets, suggesting that they might contribute to developmental robustness. For two of the miR164 targets, namely CUP-SHAPED COTYLEDON1 (CUC1) and CUC2, we provide evidence for their involvement in the regulation of growth and show that their derepression in miR164 loss-of-function mutants is likely to account for most of the mutant phenotype.
Carlsson, J, Lagercrantz, U, Sundström, J, Teixeira, R, Wellmer, F, Meyerowitz, EM, Glimelius, K (2007) Microarray analysis reveals altered expression of a large number of nuclear genes in developing cytoplasmic male sterile Brassica napus flowers. Plant J., 49(3), 452-62. PMID:17217466. doi:10.1111/j.1365-313X.2006.02975.x.
To gain new insights into the mechanism underlying cytoplasmic male sterility (CMS), we compared the nuclear gene expression profiles of flowers of a Brassica napus CMS line with that of the fertile B. napus maintainer line using Arabidopsis thaliana flower-specific cDNA microarrays. The CMS line used has a B. napus nuclear genome, but has a rearranged mitochondrial (mt) genome consisting of both B. napus and A. thaliana DNA. Gene expression profiling revealed that a large number of genes differed in expression between the two lines. For example, nuclear genes coding for proteins that are involved in protein import into organelles, genes expressed in stamens and pollen, as well as genes implicated in either cell-wall remodeling or architecture, were repressed in the CMS line compared with B. napus. These results show that the mt genome of the CMS line strongly influences nuclear gene expression, and thus reveal the importance of retrograde signalling between the mitochondria and the nucleus. Furthermore, flowers of the CMS line are characterized by a replacement of stamens with carpelloid organs, and thus partially resemble the APETALA3 (AP3) and PISTILLATA (PI) mutants. In accordance with this phenotype, AP3 expression was downregulated in the stamens, shortly before these organs developed carpelloid characteristics, even though it was initiated correctly. Repression of PI succeeded that of AP3 and might be a consequence of a loss of AP3 activity. These results suggest that AP3 expression in stamens depends on proper mt function and a correct nuclear-mt interaction, and that mt alterations cause the male sterility phenotype of the CMS line.


Wellmer, F, Alves-Ferreira, M, Dubois, A, Riechmann, JL, Meyerowitz, EM (2006) Genome-wide analysis of gene expression during early Arabidopsis flower development. PLoS Genet., 2(7), e117. PMCID:PMC1523247. PMID:16789830. doi:10.1371/journal.pgen.0020117
Detailed information about stage-specific changes in gene expression is crucial for the understanding of the gene regulatory networks underlying development. Here, we describe the global gene expression dynamics during early flower development, a key process in the life cycle of a plant, during which floral patterning and the specification of floral organs is established. We used a novel floral induction system in Arabidopsis, which allows the isolation of a large number of synchronized floral buds, in conjunction with whole-genome microarray analysis to identify genes with differential expression at distinct stages of flower development. We found that the onset of flower formation is characterized by a massive downregulation of genes in incipient floral primordia, which is followed by a predominance of gene activation during the differentiation of floral organs. Among the genes we identified as differentially expressed in the experiment, we detected a significant enrichment of closely related members of gene families. The expression profiles of these related genes were often highly correlated, indicating similar temporal expression patterns. Moreover, we found that the majority of these genes is specifically up-regulated during certain developmental stages. Because co-expressed members of gene families in Arabidops is frequently act in a redundant manner, these results suggest a high degree of functional redundancy during early flower development, but also that its extent may vary in a stage-specific manner.
Ponomaryov, D., Omelianchuk, N.A., Mironova, V., Kolchanov, N., Mjolsness, E. and Meyerowitz, E. (2006) A program method of constructing ontology of phenotypic abnormalities for Arabidopsis thaliana. Proc. Fifth Intl. Conf. on Bioinformatics of Genome Regulation and Structure 2, 231-234.
Abstract, when available, will be posted here.
Ponomaryov, D., Omelianchuk, N.A., Kolchanov, N., Mjolsness, E. and Meyerowitz, E. (2006) Semantically rich ontology of anatomical structure and development for Arabidopsis thaliana L. Proc. Fifth Intl. Conf. on Bioinformatics of Genome Regulation and Structure 2, 227-230.
Abstract, when available, will be posted here.
Omelianchuk, N.A., Mironova, V.V., Poplavsky, A.S., Pavlov, K.S., Savinskaya, S.A., Podkolodny, N.L., Mjolsness, E.D., Meyerowitz, E.M., and Kolchanov, N.A. (2006) AGNS (Arabidopsis GeneNet Supplementary DataBase), Release 3.0. Proc. Fifth Intl. Conf. on Bioinformatics of Genome Regulation and Structure 2, 223-226.
Abstract, when available, will be posted here.
Long, JA, Ohno, C, Smith, ZR, Meyerowitz, EM (2006) TOPLESS regulates apical embryonic fate in Arabidopsis. Science, 312(5779), 1520-3. PMID:16763149. doi:10.1126/science.1123841.
The embryos of seed plants develop with an apical shoot pole and a basal root pole. In Arabidopsis, the topless-1 (tpl-1) mutation transforms the shoot pole into a second root pole. Here, we show that TPL resembles known transcriptional corepressors and that tpl-1 acts as a dominant negative mutation for multiple TPL-related proteins. Mutations in the putative coactivator HISTONE ACETYLTRANSFERASE GNAT SUPERFAMILY1 suppress the tpl-1 phenotype. Mutations in HISTONE DEACETYLASE19, a putative corepressor, increase the penetrance of tpl-1 and display similar apical defects. These data point to a transcriptional repression mechanism that prevents root formation in the shoot pole during Arabidopsis embryogenesis.
McAbee, JM, Hill, TA, Skinner, DJ, Izhaki, A, Hauser, BA, Meister, RJ, Venugopala Reddy, G, Meyerowitz, EM, Bowman, JL, Gasser, CS (2006) ABERRANT TESTA SHAPE encodes a KANADI family member, linking polarity determination to separation and growth of Arabidopsis ovule integuments. Plant J., 46(3), 522-31. PMID:16623911. doi:10.1111/j.1365-313X.2006.02717.x.
The Arabidopsis aberrant testa shape (ats) mutant produces a single integument instead of the two integuments seen in wild-type ovules. Cellular anatomy and patterns of marker gene expression indicate that the single integument results from congenital fusion of the two integuments of the wild type. Isolation of the ATS locus showed it to encode a member of the KANADI (KAN) family of putative transcription factors, previously referred to as KAN4. ATS was expressed at the border between the two integuments at the time of their initiation, with expression later confined to the abaxial layer of the inner integument. In an inner no outer (ino) mutant background, where an outer integument does not form, the ats mutation led to amorphous inner integument growth. The kan1kan2 double mutant exhibits a similar amorphous growth of the outer integument without affecting inner integument growth. We hypothesize that ATS and KAN1/KAN2 play similar roles in the specification of polarity in the inner and outer integuments, respectively, that parallel the known roles of KAN proteins in promoting abaxial identity during leaf development. INO and other members of the YABBY gene family have been hypothesized to have similar parallel roles in outer integument and leaf development. Together, these two hypotheses lead us to propose a model for normal integument growth that also explains the described mutant phenotypes.
Jönsson, H, Heisler, MG, Shapiro, BE, Meyerowitz, EM, Mjolsness, E (2006) An auxin-driven polarized transport model for phyllotaxis. Proc. Natl. Acad. Sci. U.S.A., 103(5), 1633-8. PMCID:PMC1326488. PMID:16415160. doi:10.1073/pnas.0509839103.
Recent studies show that plant organ positioning may be mediated by localized concentrations of the plant hormone auxin. Auxin patterning in the shoot apical meristem is in turn brought about by the subcellular polar distribution of the putative auxin efflux mediator, PIN1. However, the question of what signals determine PIN1 polarization and how this gives rise to regular patterns of auxin concentration remains unknown. Here we address these questions by using mathematical modeling combined with confocal imaging. We propose a model that is based on the assumption that auxin influences the polarization of its own efflux within the meristem epidermis. We show that such a model is sufficient to create regular spatial patterns of auxin concentration on systems with static and dynamic cellular connectivities, the latter governed by a mechanical model. We also optimize parameter values for the PIN1 dynamics by using a detailed auxin transport model, for which parameter values are taken from experimental estimates, together with a template consisting of cell and wall compartments as well as PIN1 concentrations quantitatively extracted from confocal data. The model shows how polarized transport can drive the formation of regular patterns.
Omelyanchuk, N., Mironova, V., Poplavsky, A., Podkolodny, N., Kolchanov, N., Mjolsness, E., and Meyerowitz, E. (2006) AGNS - A database on expression of Arabidopsis genes, in Bioinformatics of Genome Regulation and Structure II, Springer, New York, pp. 433-442. doi:10.1007/0-387-29455-4_41
Abstract, when available, will be posted here.
Gor, V., Shapiro, B.E., Jönsson, H., Heisler, M., Reddy, G.V., Meyerowitz, E.M., and Mjolsness, E. (2006) A software architecture for developmental modeling in plants: The computable plant project, in Bioinformatics of Genome Regulation and Structure II, Springer, New York, pp. 345-354. doi:10.1007/0-387-29455-4_33
Abstract, when available, will be posted here.
Haswell, ES, Meyerowitz, EM (2006) MscS-like proteins control plastid size and shape in Arabidopsis thaliana. Curr. Biol., 16(1), 1-11. PMID:16401419. doi:10.1016/j.cub.2005.11.044.
Mechanosensitive (MS) ion channels provide a mechanism for the perception of mechanical stimuli such as sound, touch, and osmotic pressure. The bacterial MS ion channel MscS opens in response to increased membrane tension and serves to protect against cellular lysis during osmotic downshock. MscS-like proteins are found widely in bacterial and archaeal species and have also been identified in fission yeast and plants. None of the eukaryotic members of the family have yet been characterized.


Vijayraghavan, U., Prasad, K. and Meyerowitz, E.M. (2005) Specification and maintenance of the floral meristem: interactions between positively acting promoters of flowering and negative regulators. Current Science 89, 1835-1843.
Abstract, when available, will be posted here.
Heisler, MG, Ohno, C, Das, P, Sieber, P, Reddy, GV, Long, JA, Meyerowitz, EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol., 15(21), 1899-911. PMID:16271866. doi:10.1016/j.cub.2005.09.052.
Plants produce leaf and flower primordia from a specialized tissue called the shoot apical meristem (SAM). Genetic studies have identified a large number of genes that affect various aspects of primordium development including positioning, growth, and differentiation. So far, however, a detailed understanding of the spatio-temporal sequence of events leading to primordium development has not been established.
Reddy, GV, Meyerowitz, EM (2005) Stem-cell homeostasis and growth dynamics can be uncoupled in the Arabidopsis shoot apex. Science, 310(5748), 663-7. PMID:16210497. doi:10.1126/science.1116261.
The shoot apical meristem (SAM) is a collection of stem cells that resides at the tip of each shoot and provides the cells of the shoot. It is divided into functional regions. The central zone (CZ) at the tip of the meristem is the domain of expression of the CLAVATA3 (CLV3) gene, encoding a putative ligand for a transmembrane receptor kinase, CLAVATA1, active in cells of the rib meristem (RM), located just below the CZ. We show here that CLV3 restricts its own domain of expression (the CZ) by preventing differentiation of peripheral zone cells (PZ), which surround the CZ, into CZ cells and restricts overall SAM size by a separate, long-range effect on cell division rate.
Jönsson, H, Heisler, M, Reddy, GV, Agrawal, V, Gor, V, Shapiro, BE, Mjolsness, E, Meyerowitz, EM (2005) Modeling the organization of the WUSCHEL expression domain in the shoot apical meristem. Bioinformatics, 21 Suppl 1, i232-40. PMID:15961462. doi:10.1093/bioinformatics/bti1036.
The above-ground tissues of higher plants are generated from a small region of cells situated at the plant apex called the shoot apical meristem. An important genetic control circuit modulating the size of the Arabidopsis thaliana meristem is a feed-back network between the CLAVATA3 and WUSCHEL genes. Although the expression patterns for these genes do not overlap, WUSCHEL activity is both necessary and sufficient (when expressed ectopically) for the induction of CLAVATA3 expression. However, upregulation of CLAVATA3 in conjunction with the receptor kinase CLAVATA1 results in the downregulation of WUSCHEL. Despite much work, experimental data for this network are incomplete and additional hypotheses are needed to explain the spatial locations and dynamics of these expression domains. Predictive mathematical models describing the system should provide a useful tool for investigating and discriminating among possible hypotheses, by determining which hypotheses best explain observed gene expression dynamics.
Baker, CC, Sieber, P, Wellmer, F, Meyerowitz, EM (2005) The early extra petals1 mutant uncovers a role for microRNA miR164c in regulating petal number in Arabidopsis. Curr. Biol., 15(4), 303-15. PMID:15723790. doi:10.1016/j.cub.2005.02.017.
MicroRNAs (miRNAs) are small 20-25 nucleotide non-protein-coding RNAs that negatively regulate expression of genes in many organisms, ranging from plants to humans. The MIR164 family of miRNAs in Arabidopsis consists of three members that share sequence complementarity to transcripts of NAC family transcription factors, including CUP-SHAPED COTYLEDON1 (CUC1) and CUC2. CUC1 and CUC2 are redundantly required for the formation of boundaries between organ primordia. The analysis of transgenic plants that either overexpress miR164a or miR164b or express a miRNA-resistant version of CUC1 or CUC2 has shown that miRNA regulation of CUC1 and CUC2 is necessary for normal flower development. A loss-of-function allele of MIR164b did not result in a mutant phenotype, possibly because of functional redundancy among the three members of the MIR164 family.


Zhao, Y, Medrano, L, Ohashi, K, Fletcher, JC, Yu, H, Sakai, H, Meyerowitz, EM (2004) HANABA TARANU is a GATA transcription factor that regulates shoot apical meristem and flower development in Arabidopsis. Plant Cell, 16(10), 2586-600. PMCID:PMC520957. PMID:15367721. doi:10.1105/tpc.104.024869.
We have isolated a new mutant, hanaba taranu (han), which affects both flower and shoot apical meristem (SAM) development in Arabidopsis thaliana. Mutants have fused sepals and reduced organ numbers in all four whorls, especially in the 2nd (petal) and 3rd (stamen) whorls. han meristems can become flatter or smaller than in the wild type. HAN encodes a GATA-3-like transcription factor with a single zinc finger domain. HAN is transcribed at the boundaries between the meristem and its newly initiated organ primordia and at the boundaries between different floral whorls. It is also expressed in vascular tissues, developing ovules and stamens, and in the embryo. han interacts strongly with clavata (clv) mutations (clv1, clv2, and clv3), resulting in highly fasciated SAMs, and we find that WUS expression is altered in han mutants from early embryogenesis. In addition, HAN is ectopically expressed both in clv1 and clv3 mutants. We propose that HAN is normally required for establishing organ boundaries in shoots and flowers and for controlling the number and position of WUS-expressing cells. Ectopic HAN expression causes growth retardation, aberrant cell division patterns, and loss of meristem activity, suggesting that HAN is involved in controlling cell proliferation and differentiation.
Ito, T, Wellmer, F, Yu, H, Das, P, Ito, N, Alves-Ferreira, M, Riechmann, JL, Meyerowitz, EM (2004) The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature, 430(6997), 356-60. PMID:15254538. doi:10.1038/nature02733.
The Arabidopsis homeotic gene AGAMOUS (AG) is necessary for the specification of reproductive organs (stamens and carpels) during the early steps of flower development. AG encodes a transcription factor of the MADS-box family that is expressed in stamen and carpel primordia. At later stages of development, AG is expressed in distinct regions of the reproductive organs. This suggests that AG might function during the maturation of stamens and carpels, as well as in their early development. However, the developmental processes that AG might control during organogenesis and the genes that are regulated by this factor are largely unknown. Here we show that microsporogenesis, the process leading to pollen formation, is induced by AG through activation of the SPOROCYTELESS gene (SPL, also known as NOZZLE,NZZ), a regulator of sporogenesis. Furthermore, we demonstrate that SPL can induce microsporogenesis in the absence of AG function, suggesting that AG controls a specific process during organogenesis by activating another regulator that performs a subset of its functions.
Reddy, GV, Heisler, MG, Ehrhardt, DW, Meyerowitz, EM (2004) Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana. Development, 131(17), 4225-37. PMID:15280208. doi:10.1242/dev.01261.
Precise knowledge of spatial and temporal patterns of cell division, including number and orientation of divisions, and knowledge of cell expansion, is central to understanding morphogenesis. Our current knowledge of cell division patterns during plant and animal morphogenesis is largely deduced from analysis of clonal shapes and sizes. But such an analysis can reveal only the number, not the orientation or exact rate, of cell divisions. In this study, we have analyzed growth in real time by monitoring individual cell divisions in the shoot apical meristems (SAMs) of Arabidopsis thaliana. The live imaging technique has led to the development of a spatial and temporal map of cell division patterns. We have integrated cell behavior over time to visualize growth. Our analysis reveals temporal variation in mitotic activity and the cell division is coordinated across clonally distinct layers of cells. Temporal variation in mitotic activity is not correlated to the estimated plastochron length and diurnal rhythms. Cell division rates vary across the SAM surface. Cells in the peripheral zone (PZ) divide at a faster rate than in the central zone (CZ). Cell division rates in the CZ are relatively heterogeneous when compared with PZ cells. We have analyzed the cell behavior associated with flower primordium development starting from a stage at which the future flower comprises four cells in the L1 epidermal layer. Primordium development is a sequential process linked to distinct cellular behavior. Oriented cell divisions, in primordial progenitors and in cells located proximal to them, are associated with initial primordial outgrowth. The oriented cell divisions are followed by a rapid burst of cell expansion and cell division, which transforms a flower primordium into a three-dimensional flower bud. Distinct lack of cell expansion is seen in a narrow band of cells, which forms the boundary region between developing flower bud and the SAM. We discuss these results in the context of SAM morphogenesis.
Wagner, D, Wellmer, F, Dilks, K, William, D, Smith, MR, Kumar, PP, Riechmann, JL, Greenland, AJ, Meyerowitz, EM (2004) Floral induction in tissue culture: a system for the analysis of LEAFY-dependent gene regulation. Plant J., 39(2), 273-82. PMID:15225291. doi:10.1111/j.1365-313X.2004.02127.x.
We have developed a versatile floral induction system that is based on ectopic overexpression of the transcription factor LEAFY (LFY) in callus. During shoot regeneration, flowers or floral organs are formed directly from root explants without prior formation of rosette leaves. Morphological and reporter gene analyses show that leaf-like structures are converted to floral organs in response to LFY activity. Thus, increased levels of LFY activity are sufficient to bypass normal vegetative development and to direct formation of flowers in tissue culture. We found that about half of the cultured cells respond to inducible LFY activity with a rapid upregulation of the known direct target gene of LFY, APETALA1 (AP1). This dramatic increase in the number of LFY-responsive cells compared to whole plants suggested that the tissue culture system could greatly facilitate the analysis of LFY-dependent gene regulation by genomic approaches. To test this, we monitored the gene expression changes that occur in tissue culture after activation of LFY using a flower-specific cDNA microarray. Induction of known LFY target genes was readily detected in these experiments. In addition, several other genes were identified that had not been implicated in signaling downstream of LFY before. Thus, the floral induction system is suitable for the detection of low abundance transcripts whose expression is controlled in an LFY-dependent manner.
Wellmer, F, Riechmann, JL, Alves-Ferreira, M, Meyerowitz, EM (2004) Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell, 16(5), 1314-26. PMCID:PMC423218. PMID:15100403. doi:10.1105/tpc.021741.
We have compared the gene expression profiles of inflorescences of the floral homeotic mutants apetala1, apetala2, apetala3, pistillata, and agamous with that of wild-type plants using a flower-specific cDNA microarray and a whole genome oligonucleotide array. By combining the data sets from the individual mutant/wild type comparisons, we were able to identify a large number of genes that are, within flowers, predicted to be specifically or at least predominantly expressed in one type of floral organ. We have analyzed the expression patterns of several of these genes by in situ hybridization and found that they match the predictions that were made based on the microarray experiments. Moreover, genes with known floral organ-specific expression patterns were correctly assigned by our analysis. The vast majority of the identified transcripts are found in stamens or carpels, whereas few genes are predicted to be expressed specifically or predominantly in sepals or petals. These findings indicate that spatially limited expression of a large number of genes is part of flower development and that its extent differs significantly between the reproductive organs and the organs of the perianth.
Yu, H, Ito, T, Zhao, Y, Peng, J, Kumar, P, Meyerowitz, EM (2004) Floral homeotic genes are targets of gibberellin signaling in flower development. Proc. Natl. Acad. Sci. U.S.A., 101(20), 7827-32. PMCID:PMC419691. PMID:15128937. doi:10.1073/pnas.0402377101.
Gibberellins (GAs) are a class of plant hormones involved in the regulation of flower development in Arabidopsis. The GA-deficient ga1-3 mutant shows retarded growth of all floral organs, especially abortive stamen development that results in complete male sterility. Until now, it has not been clear how GA regulates the late-stage development of floral organs after the establishment of their identities within floral meristems. Various combinations of null mutations of DELLA proteins can gradually rescue floral defects in ga1-3. In particular, the synergistic effect of rga-t2 and rgl2-1 can substantially restore flower development in ga1-3. We find that the transcript levels of floral homeotic genes APETALA3 (AP3), PISTILLATA (PI), and AGAMOUS (AG) are immediately upregulated in young flowers of ga1-3 upon GA treatment. Using a steroid-inducible activation of RGA, we further demonstrated that these floral homeotic genes are transcriptionally repressed by RGA activity in young flowers whereas the expression of LEAFY (LFY) and APETALA1 (AP1) is not substantially affected. In addition, we observed the partial rescue of floral defects in ga1-3 by overexpression of AG. Our results indicate that GA promotes the expression of floral homeotic genes by antagonizing the effects of DELLA proteins, thereby allowing continued flower development.
Ohno, CK, Reddy, GV, Heisler, MG, Meyerowitz, EM (2004) The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue development. Development, 131(5), 1111-22. PMID:14973281. doi:10.1242/dev.00991.
Important goals in understanding leaf development are to identify genes involved in pattern specification, and also genes that translate this information into cell types and tissue structure. Loss-of-function mutations at the JAGGED (JAG) locus result in Arabidopsis plants with abnormally shaped lateral organs including serrated leaves, narrow floral organs, and petals that contain fewer but more elongate cells. jag mutations also suppress bract formation in leafy, apetala1 and apetala2 mutant backgrounds. The JAG gene was identified by map-based cloning to be a member of the zinc finger family of plant transcription factors and encodes a protein similar in structure to SUPERMAN with a single C(2)H(2)-type zinc finger, a proline-rich motif and a short leucine-rich repressor motif. JAG mRNA is localized to lateral organ primordia throughout the plant but is not found in the shoot apical meristem. Misexpression of JAG results in leaf fusion and the development of ectopic leaf-like outgrowth from both vegetative and floral tissues. Thus, JAG is necessary for proper lateral organ shape and is sufficient to induce the proliferation of lateral organ tissue.
Yu, H, Ito, T, Wellmer, F, Meyerowitz, EM (2004) Repression of AGAMOUS-LIKE 24 is a crucial step in promoting flower development. Nat. Genet., 36(2), 157-61. PMID:14716314. doi:10.1038/ng1286.
Flower development begins as floral meristems arise in succession on the flank of the inflorescence meristem. Floral meristem identity genes LEAFY (LFY) and APETALA1 (AP1) promote establishment and maintenance of floral identity in newly formed floral primordia. Without their activity, the floral primordia develop with inflorescence characteristics. The underlying molecular-genetic mechanism is unknown. Here we show that these phenotypes are due in large part to the ectopic expression of AGAMOUS-LIKE 24 (AGL24), a central regulator of floral meristem identity. We present evidence that AGL24 is an early target of transcriptional repression by LFY and AP1. Without such repression, continued AGL24 expression in floral meristems is sufficient to cause floral reversion regardless of the activation of floral organ identity genes. This indicates that LFY and AP1 promote floral development not only by positively regulating genes activated in flower development, but also by repressing AGL24, a promoter of inflorescence fate.
Jönsson, H., Shapiro, B. E., Meyerowitz, E. M. and E. Mjolsness (2004) Modeling plant development with gene regulation networks including signaling and cell division. In R. Hofestaedt and N. Kolchanov (Eds.) Bioinformatics of Genome Regulation and Structure, Kluwer, Boston, pp. 311-318.
Abstract, when available, will be posted here.


Ito, T., Sakai, H. and Meyerowitz, E.M. (2003) Whorl specific expression of the SUPERMAN gene of Arabidopsis is mediated by cis elements in the transcribed region. Curr. Biol. 13, 1524-1530. PMID:12956955. doi:10.1016/S0960-9822(03)00612-2
The SUPERMAN (SUP) gene of Arabidopsis is involved in controlling cell proliferation in stamen and carpel primordia and in ovules during flower development. The SUP gene encodes a transcription factor with a C2H2-type zinc finger motif, a serine/proline-rich domain, a basic domain, and a leucine-zipper-like domain and is expressed in a very limited region in stamen primordia and in the developing ovary during flower development. The SUP gene is susceptible to methylation, resulting in epigenetic gene silencing. To understand how the SUP gene is expressed spatially and temporally in its restricted domain, and why methylation of the transcribed region affects early-stage SUP expression, we have identified the SUP cis regulatory elements by characterizing SUP gene fusions. These studies show that the SUP gene has discrete upstream promoter elements required for expression in stamen primordia in early stages and in the ovary in later stages. The promoter activity for stamen primordia is modulated by several positive and negative elements located in the transcribed and translated regions. Several regulatory elements in the transcribed region correlate with the areas of the gene that are heavily methylated in epigenetic alleles; these data provide a possible explanation of how methylation of the transcribed region represses transcription.
Jönsson, H., Shapiro, B. E., Meyerowitz, E. M. and E. Mjolsness (2003). Signaling in Multicellular Models of Plant Development. In S. Kumar and P.J. Bentley (Eds.) On Growth, Form, and Computers, Academic Press, London, UK, pp. 156-161. doi:10.1016/B978-012428765-5/50041-4
This chapter describes how a model framework with interaction and signaling between cells is a powerful tool to investigate the behavior of various parts of a developmental system. The model can be used to falsify or discard hypotheses and also to introduce and test new ones. The shoot apical meristem (SAM) is the source of the complete part of a plant above ground. Arabidopsis thaliana has become a model system for dicot plants, and it has a SAM of about 103 cells. It retains this size and its almost half-spherical shape throughout the post-embryonic life of the plant. The SAM can be divided into cytologically defined zones where the central zone is at the very apex, the peripheral zone is on the sides, and the rib meristem is in the central parts of the meristem. An interesting property of the SAM is that it is self-organizing. The chapter shows how the introduced model framework is valuable as a tool when evaluating a developmental system. It suggests possible explanations of experimental data in the SAM, including hypotheses open for verification. In the model framework, a gene is only an extra variable and an interaction is a parameter in the differential equations. The simulations presented in this chapter need only a couple of minutes to finish on a typical personal computer (IGHz AMD processor). Hence, the framework provides a tractable method to refine new hypotheses in silico for future verification in vivo.
Somerville, C.R. and Meyerowitz, E.M. (eds.) The Arabidopsis Book. American Society of Plant Biologists, Rockville, 2003, doi: 10.1199/tab.9999.
Abstract, when available, will be posted here.
Shapiro, BE, Levchenko, A, Meyerowitz, EM, Wold, BJ, Mjolsness, ED (2003) Cellerator: extending a computer algebra system to include biochemical arrows for signal transduction simulations. Bioinformatics, 19(5), 677-8. PMID:12651737. doi:12651737.
Cellerator describes single and multi-cellular signal transduction networks (STN) with a compact, optionally palette-driven, arrow-based notation to represent biochemical reactions and transcriptional activation. Multi-compartment systems are represented as graphs with STNs embedded in each node. Interactions include mass-action, enzymatic, allosteric and connectionist models. Reactions are translated into differential equations and can be solved numerically to generate predictive time courses or output as systems of equations that can be read by other programs. Cellerator simulations are fully extensible and portable to any operating system that supports Mathematica, and can be indefinitely nested within larger data structures to produce highly scaleable models.
Vergara-Silva, F., Espinosa-Matías, S., Ambrose, B.A., Vázquez-Santana, S., Martínez-Mena, A., Márquez-Guzmán, J., Martínez, E., Meyerowitz, E.M. and Alvarez-Buylla, E.R. (2003) Inside-out flowers characteristic of Lacandonia schismatica evolved at least before its divergence from its putative sister taxon, Triuris brevistylis. Int. J. Plant Sci. 164, 345-357. doi:10.1086/368235
Lacandonia schismatica, a mycoheterotrophic, hermaphroditic monocotyledon endemic to the Lacandon rain forest of southeast Mexico, is the only flowering plant for which a spatial inversion (heterotopy, complete homeosis) of the reproductive floral whorls (stamens and carpels) is known to occur in natural populations. In order to investigate if this autapomorphic inside?out arrangement of the reproductive organs is fixed in natural populations, we have undertaken extensive and intensive fieldwork spanning several years to locate new populations in addition to the type locality. In parallel, we have also searched for natural variation in floral organ arrangement in Triuris brevistylis, a closely related dioecious triurid that is found in nearby areas of the Lacandon forest. We have found that a small proportion of L. schismatica inflorescences bear unisexual flowers of both sexes, as well as bisexual flowers with differences in the number of reproductive organs. However, in all bisexual flowers, the stamens were always central and the carpels peripheral to them. More important, we have also found that a few T. brevistylis individuals have bisexual flowers with altered positions of stamens and carpels. Among these, flowers with an inside?out L. schismatica?like floral organ arrangement were observed. We document our findings with scanning electron micrographs, histological sections, and dissection microscope views. The information presented implies that the developmental?genetic mechanism putatively responsible for homeotic/heterotopic transformations involving floral reproductive organs in the two triurid species originated at least before these taxa diverged from each other. The Mexican triurids may be an example in which the molecular evolutionary events causally related to a major morphological change in plants can best be understood at the microevolutionary scale.


Vishnevetsky, M. and Meyerowitz, E.M. (2002) Molecular control of flower development. In Breeding for Ornamentals: Classical and Molecular Approaches, ed. A. Vainstein, Kluwer Academic, Dordrecht, pp. 239-252.
Abstract, when available, will be posted here.
Long, J., Woody, S., Poethig, S., Meyerowitz, E.M. and Barton, M.K. (2002) Transformation of shoots into roots in Arabidopsis embryos mutant at the TOPLESS locus. Development 129, 2797-2806. PMID:12050130.
We describe a novel phenotype in Arabidopsis embryos homozygous for the temperature-sensitive topless-1 mutation. This mutation causes the transformation of the shoot pole into a root. Developing topless embryos fail to express markers for the shoot apical meristem (SHOOT MERISTEMLESS and UNUSUAL FLORAL ORGANS) and the hypocotyl (KNAT1). By contrast, the pattern of expression of root markers is either duplicated (LENNY, J1092) or expanded (SCARECROW). Shifts of developing topless embryos between permissive and restrictive temperatures show that apical fates (cotyledons plus shoot apical meristem) can be transformed to basal fates (root) as late as transition stage. As the apical pole of transition stage embryos shows both morphological and molecular characteristics of shoot development, this demonstrates that the topless 1 mutation is capable of causing structures specified as shoot to be respecified as root. Finally, our experiments fail to show a clear link between auxin signal transduction and topless-1 mutant activity: the development of the apical root in topless mutant individuals is not dependent on the activity of the predicted auxin response factor MONOPTEROS nor is the expression of DR5, a proposed 'auxin maximum reporter', expanded in the apical domain of topless embryos.
Meyerowitz, EM (2002) Plants compared to animals: the broadest comparative study of development. Science, 295(5559), 1482-5. PMID:11859185. doi:10.1126/science.1066609.
If the last common ancestor of plants and animals was unicellular, comparison of the developmental mechanisms of plants and animals would show that development was independently invented in each lineage. And if this is the case, comparison of plant and animal developmental processes would give us a truly comparative study of development, which comparisons merely among animals, or merely among plants, do not-because in each of these lineages, the fundamental mechanisms are similar by descent. Evidence from studies of developmental mechanisms in both kingdoms, and data from genome-sequencing projects, indicate that development evolved independently in the lineages leading to plants and to animals.
Wagner, D, Meyerowitz, EM (2002) SPLAYED, a novel SWI/SNF ATPase homolog, controls reproductive development in Arabidopsis. Curr. Biol., 12(2), 85-94. PMID:11818058. doi:11818058.
The plant-specific transcriptional activator LEAFY (LFY) is a central regulator of the transition to reproductive development in Arabidopsis. LFY has a second, later role in the induction of floral homeotic gene expression. Available data suggests that, while LFY activity is controlled via interaction with tissue-specific coactivators, other mechanisms exist that regulate LFY activity, the identity of which are not known.


Kishimoto, N., Sakai, H., Jackson, J., Jacobsen, S.E., Meyerowitz, E.M., Dennis, E.S. and Finnegan, E.J. (2001) Site specificity of the Arabidopsis METI DNA methyltransferase demonstrated through hypermethylation of the superman locus. Plant Mol. Biol. 46, 171-183. PMID:11442057. doi:10.1023/A:1010636222327.
Plants with low levels of DNA methylation show a range of developmental abnormalities including homeotic transformation of floral organs. Two independent DNA METHYLTRANSFERASEI (METI) antisense transformants with low levels of DNA methylation had flowers with increased numbers of stamens which resembled flowers seen on the loss-of-function superman (sup) mutant plants and on transgenic plants that ectopically express APETALA3 (AP3). These METI antisense plants have both increased and decreased methylation in and around the sup gene, compared with untransformed controls. DNA from the antisense plants was demethylated at least 4 kb upstream of the sup gene, while there was dense methylation around the start of transcription and within the coding region of this gene; these regions were unmethylated in control DNA. Methylation within the sup gene was correlated with an absence of SUP transcripts. The pattern and density of methylation was heterogeneous among different DNA molecules from the same plant, with some molecules being completely unmethylated. Methylcytosine occurred in asymmetric sites and in symmetric CpA/TpG but rarely in CpG dinucleotides in the antisense plants. In contrast, segregants lacking the METI antisense construct and epimutants with a hypermethylated allele of sup (clark kent 3), both of which have active METI genes, showed a higher frequency of methylation of CpG dinucleotides and of asymmetric cytosines. We conclude that METI is the predominant CpG methyltransferase and directly or indirectly affects asymmetric methylation.
Meyerowitz, EM (2001) Prehistory and history of Arabidopsis research. Plant Physiol., 125(1), 15-9. PMCID:PMC1539315. PMID:11154286. doi:10.1104/pp.125.1.1.
The earliest non-taxonomic appearance of Arabidopsis in the literature of botany appears to be a paper by Alexander Braun in 1873, describing a mutant plant found in a field near Berlin (7). The mutation was almost certainly in theAGAMOUS gene, now well known as one of the floral ABC regulators and cloned in 1990 (54). The next notable appearance of Arabidopsis in the experimental literature was in 1907, when Friedrich Laibach (1885-1967), a student in Strasburger's laboratory in Bonn, published an account of the chromosome number of several plants. He was attempting to find a plant with a small number of large chromosomes to be used in experiments to determine the individuality of chromosomes (23). Arabidopsis was not such a plant: the chromosomes are very small. The next relevant appearance of Arabidopsis was in a 1935 paper that resulted from a Russian expedition to find a plant that could be used in genetics and cytogenetics, as Drosophila was then used (15, 51). Although the small chromosome number (incorrectly stated by Titova to be a haploid no. of three; Laibach had correctly counted five in 1907) and rapid time to flowering were considered useful features, the small size of the plant and its parts were considered a disadvantage, as was the inability to distinguish different chromosome pairs. It does not appear that Arabidopsis was ever used in the laboratory by Titova and her colleagues.


Ziegelhoffer, EC, Medrano, LJ, Meyerowitz, EM (2000) Cloning of the Arabidopsis WIGGUM gene identifies a role for farnesylation in meristem development. Proc. Natl. Acad. Sci. U.S.A., 97(13), 7633-8. PMCID:PMC16597. PMID:10840062. doi:10.1073/pnas.130189397.
Control of cellular proliferation in plant meristems is important for maintaining the correct number and position of developing organs. One of the genes identified in the control of floral and apical meristem size and floral organ number in Arabidopsis thaliana is WIGGUM. In wiggum mutants, one of the most striking phenotypes is an increase in floral organ number, particularly in the sepals and petals, correlating with an increase in the width of young floral meristems. Additional phenotypes include reduced and delayed germination, delayed flowering, maturation, and senescence, decreased internode elongation, shortened roots, aberrant phyllotaxy of flowers, aberrant sepal development, floral buds that open precociously, and occasional apical meristem fasciation. As a first step in determining a molecular function for WIGGUM, we used positional cloning to identify the gene. DNA sequencing revealed that WIGGUM is identical to ERA1 (enhanced response to abscisic acid), a previously identified farnesyltransferase beta-subunit gene of Arabidopsis. This finding provides a link between protein modification by farnesylation and the control of meristem size. Using in situ hybridization, we examined the expression of ERA1 throughout development and found it to be nearly ubiquitous. This extensive expression domain is consistent with the pleiotropic nature of wiggum mutants and highlights a broad utility for farnesylation in plant growth and development.


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Reviews & book chapters 1984-2000

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