Unlike animals, whose body plans are set during embryo development, plants maintain the ability to initiate new organs throughout their life cycle. Auxin is a key regulator of almost all aspects of ...plant development, including morphogenesis and adaptive responses. Cellular auxin concentrations influence whether a cell will divide, grow, or differentiate, thereby contributing to organ formation, growth, and ultimately plant shape. Auxin gradients are established and maintained by a tightly regulated interplay between metabolism, signalling, and transport. Auxin is synthesised, stored, and inactivated by a multitude of parallel pathways that are all tightly regulated. Here we summarise the remarkable progress that has been achieved in identifying some key components of these pathways and the genetic complexity underlying their precise regulation.
In the Arabidopsis root meristem, the boundary between dividing and differentiating cells is positioned by active formation of a local auxin minima. Active auxin degradation, by its conjugation to amino acids, contributes to the formation of this auxin minimum. Therefore, auxin conjugation contributes to regulating meristem size and activity in roots.Auxin is locally produced in the Arabidopsis root quiescent centre. Both this local auxin biosynthesis and auxin transport are individually dispensable for root meristem maintenance.Auxin homeostasis is regulated in a complex manner. Metabolic profiling in combination with mathematical modelling of auxin metabolic pathways showed that auxin oxidation is more important for auxin homoeostasis at lower hormone concentrations, whereas auxin conjugation is most significant at high auxin levels.
Root branching is critical for plants to secure anchorage and ensure the supply of water, minerals, and nutrients. To date, research on root branching has focused on lateral root development in young ...seedlings. However, many other programs of postembryonic root organogénesis exist in angiosperms. In cereal crops, the majority of the mature root system is composed of several classes of adventitious roots that include crown roots and brace roots. In this Update, we initially describe the diversity of postembryonic root forms. Next, we review recent advances in our understanding of the genes, signals, and mechanisms regulating lateral root and adventitious root branching in the plant models Arabidopsis (Arabidopsis thaliana), maize (Zea mays), and rice (Oryza sativa). While many common signals, regulatory components, and mechanisms have been identified that control the initiation, morphogenesis, and emergence of new lateral and adventitious root organs, much more remains to be done. We conclude by discussing the challenges and opportunities facing root branching research.
Auxin is a key signal regulating plant growth and development. It is well established that auxin dynamics depend on the spatial distribution of efflux and influx carriers on the cell membranes. In ...this study, we employ a systems approach to characterise an alternative symplastic pathway for auxin mobilisation via plasmodesmata, which function as intercellular pores linking the cytoplasm of adjacent cells. To investigate the role of plasmodesmata in auxin patterning, we developed a multicellular model of the
root tip. We tested the model predictions using the DII-VENUS auxin response reporter, comparing the predicted and observed DII-VENUS distributions using genetic and chemical perturbations designed to affect both carrier-mediated and plasmodesmatal auxin fluxes. The model revealed that carrier-mediated transport alone cannot explain the experimentally determined auxin distribution in the root tip. In contrast, a composite model that incorporates both carrier-mediated and plasmodesmatal auxin fluxes re-capitulates the root-tip auxin distribution. We found that auxin fluxes through plasmodesmata enable auxin reflux and increase total root-tip auxin. We conclude that auxin fluxes through plasmodesmata modify the auxin distribution created by efflux and influx carriers.
Phosphate (P) is an essential macronutrient for plant growth. Roots employ adaptive mechanisms to forage for P in soil. Root hair elongation is particularly important since P is immobile. Here we ...report that auxin plays a critical role promoting root hair growth in Arabidopsis in response to low external P. Mutants disrupting auxin synthesis (taa1) and transport (aux1) attenuate the low P root hair response. Conversely, targeting AUX1 expression in lateral root cap and epidermal cells rescues this low P response in aux1. Hence auxin transport from the root apex to differentiation zone promotes auxin-dependent hair response to low P. Low external P results in induction of root hair expressed auxin-inducible transcription factors ARF19, RSL2, and RSL4. Mutants lacking these genes disrupt the low P root hair response. We conclude auxin synthesis, transport and response pathway components play critical roles regulating this low P root adaptive response.
Since colonizing land, plants have developed mechanisms to tolerate a broad range of abiotic stresses that include flooding, drought, high salinity, and nutrient limitation. Roots play a key role ...acclimating plants to these as their developmental plasticity enables them to grow toward more favorable conditions and away from limiting or harmful stresses. The phytohormone auxin plays a key role translating these environmental signals into developmental outputs. This is achieved by modulating auxin levels and/or signaling, often through cross talk with other hormone signals like abscisic acid (ABA) or ethylene. In our review, we discuss how auxin controls root responses to water, osmotic and nutrient-related stresses, and describe how the synthesis, degradation, transport, and response of this key signaling hormone helps optimize root architecture to maximize resource acquisition while limiting the impact of abiotic stresses.
To generate the various tissues and organs that build up the adult body, plants and animals require organized formative cell divisions and correct cell specification. In plants, these processes are ...controlled mainly by phytohormones and transcriptional networks. Recently, ligand-receptor-like kinase signalling pathways have been revealed as additional potentially crucial regulators of cell specification in plants. We review here the importance of such signalling cascades for plant growth and development, and we discuss, where possible, similarities to well-investigated cascades in animals.
•Modelling has helped to understand the complex network structure of single hormonal pathways, but has also provided insights into hormone activity at many levels.•We describe how multiple hormones ...have been incorporated into new models.•We explore future challenges in integrating different models.•We propose that future models need to be more realistic by capturing more geometrical, mechanical as well as biological data.
As our knowledge of the complexity of hormone homeostasis, transport, perception, and response increases, and their outputs become less intuitive, modelling is set to become more important. Initial modelling efforts have focused on hormone transport and response pathways. However, we now need to move beyond the network scales and use multicellular and multiscale modelling approaches to predict emergent properties at different scales. Here we review some examples where such approaches have been successful, for example, auxin–cytokinin crosstalk regulating root vascular development or a study of lateral root emergence where an iterative cycle of modelling and experiments lead to the identification of an overlooked role for PIN3. Finally, we discuss some of the remaining biological and technical challenges.
Auxin represents a key signal in plants, regulating almost every aspect of their growth and development. Major breakthroughs have been made dissecting the molecular basis of auxin transport, ...perception, and response. In contrast, how plants control the metabolism and homeostasis of the major form of auxin in plants, indole-3-acetic acid (IAA), remains unclear. In this paper, we initially describe the function of the Arabidopsis thaliana gene DIOXYGENASE FOR AUXIN OXIDATION 1 (AtDAO1). Transcriptional and translational reporter lines revealed that AtDAO1 encodes a highly root-expressed, cytoplasmically localized IAA oxidase. Stable isotope-labeled IAA feeding studies of loss and gain of function AtDAO1 lines showed that this oxidase represents the major regulator of auxin degradation to 2-oxoindole-3-acetic acid (oxIAA) in Arabidopsis. Surprisingly, AtDAO1 loss and gain of function lines exhibited relatively subtle auxin-related phenotypes, such as altered root hair length. Metabolite profiling of mutant lines revealed that disrupting AtDAO1 regulation resulted in major changes in steady-state levels of oxIAA and IAA conjugates but not IAA. Hence, IAA conjugation and catabolism seem to regulate auxin levels in Arabidopsis in a highly redundant manner. We observed that transcripts of AtDOA1 IAA oxidase and GH3 IAA-conjugating enzymes are auxin-inducible, providing a molecular basis for their observed functional redundancy. We conclude that the AtDAO1 gene plays a key role regulating auxin homeostasis in Arabidopsis, acting in concert with GH3 genes, to maintain auxin concentration at optimal levels for plant growth and development.
The hormone auxin is a key regulator of plant growth and development, and great progress has been made understanding auxin transport and signaling. Here, we show that auxin metabolism and homeostasis ...are also regulated in a complex manner. The principal auxin degradation pathways in Arabidopsis include oxidation by Arabidopsis thaliana gene DIOXYGENASE FOR AUXIN OXIDATION 1/2 (AtDAO1/2) and conjugation by Gretchen Hagen3s (GH3s). Metabolic profiling of dao1-1 root tissues revealed a 50% decrease in the oxidation product 2-oxoindole-3-acetic acid (oxIAA) and increases in the conjugated forms indole-3-acetic acid aspartic acid (IAA-Asp) and indole-3-acetic acid glutamic acid (IAA-Glu) of 438- and 240-fold, respectively, whereas auxin remains close to the WT. By fitting parameter values to a mathematical model of these metabolic pathways, we show that, in addition to reduced oxidation, both auxin biosynthesis and conjugation are increased in dao1-1. Transcripts of AtDAO1 and GH3 genes increase in response to auxin over different timescales and concentration ranges. Including this regulation of AtDAO1 and GH3 in an extended model reveals that auxin oxidation is more important for auxin homoeostasis at lower hormone concentrations, whereas auxin conjugation is most significant at high auxin levels. Finally, embedding our homeostasis model in a multicellular simulation to assess the spatial effect of the dao1-1 mutant shows that auxin increases in outer root tissues in agreement with the dao1-1 mutant root hair phenotype. We conclude that auxin homeostasis is dependent on AtDAO1, acting in concert with GH3, to maintain auxin at optimal levels for plant growth and development.
Lateral root organogenesis plays an essential role in elaborating plant root system architecture. In Arabidopsis, the AP2 family transcription factor PUCHI controls cell proliferation in lateral root ...primordia. To identify potential targets of PUCHI, we analyzed a time course transcriptomic dataset of lateral root formation. We report that multiple genes coding for very long chain fatty acid (VLCFA) biosynthesis enzymes are induced during lateral root development in a PUCHI-dependent manner. Significantly, several mutants perturbed in VLCFA biosynthesis show similar lateral root developmental defects as puchi-1. Moreover, puchi-1 roots display the same disorganized callus formation phenotype as VLCFA biosynthesis-deficient mutants when grown on auxin-rich callus-inducing medium. Lipidomic profiling of puchi-1 roots revealed reduced VLCFA content compared with WT. We conclude that PUCHI-regulated VLCFA biosynthesis is part of a pathway controlling cell proliferation during lateral root and callus formation.
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