Modelling meristem development in plants

Meristems continually supply new cells for post-embryonic plant development and coordinate the initiation of new organs, such as leaves and flowers. Meristem function is regulated by a large and interconnected dynamic system that includes transcription networks, intercellular protein signalling, polarized transport of hormones and a constantly changing cellular topology. Mathematical modelling, in which the dynamics of a system are simulated using explicitly defined interactions, can serve as a powerful tool for examining the expected behaviour of such a system given our present knowledge and assumptions. Modelling can also help to investigate new hypotheses in silico both to validate ideas and to obtain inspiration for new experiments. Several recent studies have used new molecular data together with modelling and computational techniques to investigate meristem function

The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue development

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 C2H2-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

Pattern formation during de novo assembly of the Arabidopsis shoot meristem

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

PIN-FORMED1 polarity in the plant shoot epidermis is insensitive to the polarity of neighboring cells

At the Arabidopsis shoot apex, epidermal cells are planar-polarized along an axis marked by the asymmetric localization patterns of several proteins including PIN-FORMED1 (PIN1), which facilitates the directional efflux of the plant hormone auxin to pattern phyllotaxis. While PIN1 polarity is known to be regulated non -cell autonomously via the MONOPTEROS (MP) transcription factor, how this occurs has not been determined. Here, we use mosaic expression of the serine threonine kinase PINOID (PID) to test whether PIN1 polarizes according to the polarity of neighboring cells. Our findings reveal that PIN1 is insensitive to the po-larity of PIN1 in neighboring cells arguing against auxin flux or extracellular auxin concentrations acting as a polarity cue, in contrast to previous model proposals

Auxin Acts through MONOPTEROS to Regulate Plant Cell Polarity and Pattern Phyllotaxis.

The periodic formation of plant organs such as leaves and flowers gives rise to intricate patterns that have fascinated biologists and mathematicians alike for hundreds of years [1]. The plant hormone auxin plays a central role in establishing these patterns by promoting organ formation at sites where it accumulates due to its polar, cell-to-cell transport [2-6]. Although experimental evidence as well as modeling suggest that feedback from auxin to its transport direction may help specify phyllotactic patterns [7-12], the nature of this feedback remains unclear [13]. Here we reveal that polarization of the auxin efflux carrier PIN-FORMED 1 (PIN1) is regulated by the auxin response transcription factor MONOPTEROS (MP) [14]. We find that in the shoot, cell polarity patterns follow MP expression, which in turn follows auxin distribution patterns. By perturbing MP activity both globally and locally, we show that localized MP activity is necessary for the generation of polarity convergence patterns and that localized MP expression is sufficient to instruct PIN1 polarity directions non-cell autonomously, toward MP-expressing cells. By expressing MP in the epidermis of mp mutants, we further show that although MP activity in a single-cell layer is sufficient to promote polarity convergence patterns, MP in sub-epidermal tissues helps anchor these polarity patterns to the underlying cells. Overall, our findings reveal a patterning module in plants that determines organ position by orienting transport of the hormone auxin toward cells with high levels of MP-mediated auxin signaling. We propose that this feedback process acts broadly to generate periodic plant architectures.The research leading to these results received funding from the Australian Research Council (M.G.H.) and European Research Council under the European Union’s Seventh Framework Programme ( FP/2007-2013 )/ERC grant agreement 261081 (M.G.H.). The work was also supported by the European Molecular Biology Laboratory (N.B., C.O., and M.G.H.), EMBL International PhD Programme (N.B.), Gatsby Charitable Foundation ( GAT3395/PR4 ) (H.J.), and Swedish Research Council ( VR2013-4632 ) (H.J.).This is the final version of the article. It first appeared from Elsevier (Cell Press) via https://doi.org/10.1016/j.cub.2016.09.04

Quantitative analysis of auxin sensing in leaf primordia argues against proposed role in regulating leaf dorsoventrality

Dorsoventrality in leaves has been shown to depend on the pre-patterned expression of KANADI and HD-ZIPIII genes within the plant shoot apical meristem (SAM). However, it has also been proposed that asymmetric auxin levels within initiating leaves help establish leaf polarity, based in part on observations of the DII auxin sensor. By analyzing and quantifying the expression of the R2D2 auxin sensor, we find that there is no obvious asymmetry in auxin levels during Arabidopsis leaf development. We further show that the mDII control sensor also exhibits an asymmetry in expression in developing leaf primordia early on, while it becomes more symmetric at a later developmental stage as reported previously. Together with other recent findings, our results argue against the importance of auxin asymmetry in establishing leaf polarity

Cell type boundaries organize plant development

In plants the dorsoventral boundary of leaves defines an axis of symmetry through the centre of the organ separating the top (dorsal) and bottom (ventral) tissues. Although the positioning of this boundary is critical for leaf morphogenesis, how the boundary is established and how it influences development remains unclear. Using live-imaging and perturbation experiments we show that leaf orientation, morphology and position are pre-patterned by HD-ZIPIII and KAN gene expression in the shoot, leading to a model in which dorsoventral genes coordinate to regulate plant development by localizing auxin response between their expression domains. However we also find that auxin levels feedback on dorsoventral patterning by spatially organizing HD-ZIPIII and KAN expression in the shoot periphery. By demonstrating that the regulation of these genes by auxin also governs their response to wounds, our results also provide a parsimonious explanation for the influence of wounds on leaf dorsoventrality.The EMM laboratory is supported by funds from the Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation (through grant GBMF3406). The research leading to these results received funding from the Australian Research Council (MGH) and European Research Council under the European Union’s Seventh Framework Programme (FP/2007–2013)/ERC Grant Agreement n. 261081 (MGH), as well as the People Programme (Marie Curie Actions) under REA grant agreement n. 255089 (PS). The work was also supported by: the European Molecular Biology Laboratory (XY, MPC, CO, PS, NB, HR and MGH); the EMBL International PhD Programme (XY, NB and MPC); Gatsby Charitable Foundation (GAT3395/PR4) (HJ) and Swedish Research Council (VR2013-4632) (HJ)

Calcium signals are necessary to establish auxin transporter polarity in a plant stem cell niche

In plants mechanical signals pattern morphogenesis through the polar transport of the hormone auxin and through regulation of interphase microtubule (MT) orientation. To date, the mechanisms by which such signals induce changes in cell polarity remain unknown. Through a combination of time-lapse imaging, and chemical and mechanical perturbations, we show that mechanical stimulation of the SAM causes transient changes in cytoplasmic calcium ion concentration (Ca^(2+)) and that transient Ca^(2+) response is required for downstream changes in PIN-FORMED 1 (PIN1) polarity. We also find that dynamic changes in Ca^(2+) occur during development of the SAM and this Ca^(2+) response is required for changes in PIN1 polarity, though not sufficient. In contrast, we find that Ca^(2+) is not necessary for the response of MTs to mechanical perturbations revealing that Ca^(2+) specifically acts downstream of mechanics to regulate PIN1 polarity response