Modeling auxin transport and plant development

The plant hormone auxin plays a critical role in plant development. Central to its function is its distribution in plant tissues, which is, in turn, largely shaped by intercellular polar transport processes. Auxin transport relies on diffusive uptake as well as carrier-mediated transport via influx and efflux carriers. Mathematical models have been used to both refine our theoretical understanding of these processes and to test new hypotheses regarding the localization of efflux carriers to understand auxin patterning at the tissue level. Here we review models for auxin transport and how they have been applied to patterning processes, including the elaboration of plant vasculature and primordium positioning. Second, we investigate the possible role of auxin influx carriers such as AUX1 in patterning auxin in the shoot meristem. We find that AUX1 and its relatives are likely to play a crucial role in maintaining high auxin levels in the meristem epidermis. We also show that auxin influx carriers may play an important role in stabilizing auxin distribution patterns generated by auxin-gradient type models for phyllotaxis

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

Tessellations and Pattern Formation in Plant Growth and Development

The shoot apical meristem (SAM) is a dome-shaped collection of cells at the apex of growing plants from which all above-ground tissue ultimately derives. In Arabidopsis thaliana (thale cress), a small flowering weed of the Brassicaceae family (related to mustard and cabbage), the SAM typically contains some three to five hundred cells that range from five to ten microns in diameter. These cells are organized into several distinct zones that maintain their topological and functional relationships throughout the life of the plant. As the plant grows, organs (primordia) form on its surface flanks in a phyllotactic pattern that develop into new shoots, leaves, and flowers. Cross-sections through the meristem reveal a pattern of polygonal tessellation that is suggestive of Voronoi diagrams derived from the centroids of cellular nuclei. In this chapter we explore some of the properties of these patterns within the meristem and explore the applicability of simple, standard mathematical models of their geometry.Comment: Originally presented at: "The World is a Jigsaw: Tessellations in the Sciences," Lorentz Center, Leiden, The Netherlands, March 200

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

Raman vibrational dynamics of hydrated ions in the low-frequency spectral region

The hydration structure of ions in aqueous environments can have a significant influence on their chemical and biological properties. Due to its inherent dynamical character, determination of the hydration shell around dissolved ions has proved challenging, mainly so for cations such as sodium and potassium which form diffuse and dynamic hydrating structures. The low frequency polarized Raman spectrum, as retrieved by time resolved isotropic optical Kerr effect measurements, is sensitive to structural fluctuations and can reveal information about ion-water interactions through their Raman active vibrational modes. Here we study a series of mixtures of sodium, potassium and lithium hydroxide solutions by changing cation concentration pairwise (namely, sodium/potassium or sodium/lithium) while keeping constant the hydroxide concentration. The hydroxide-water hydrogen bond vibration, which produces a well-defined isotropic Raman mode, appears at higher frequencies from the cation-water Raman active vibrations. In addition to previously reported lithium-water low frequency vibrations, clear spectral features could be resolved from the concentration studies and assigned to sodium-water hydration shell vibrations. However, potassium related low frequency spectral features remain elusive. The same method was applied to mixtures of the same cations with a halide anion (chloride) in order to rule out any specific features related to the dissolved hydroxide anion. Comparison between halide and hydroxide measurements confirmed the presence of the cation modes and further revealed a low frequency spectral feature related to hydroxide induced changes in water polarizability