Growth regulation tailors plant development to its environment. A showcase is response to gravity, where shoots bend up and roots down 1 . This paradox is based on opposite effects of the phytohormone auxin, which promotes cell expansion in shoots, while inhibiting it in roots via a yet unknown cellular mechanism 2 . Here, by combining micro uidics, live imaging, genetic engineering and phosphoproteomics in Arabidopsis thaliana, we advance our understanding how auxin inhibits root growth. We show that auxin activates two distinct, antagonistically acting signalling pathways that converge on the rapid regulation of the apoplastic pH, a causative growth determinant. Cell surface-based TRANSMEMBRANE KINASE1 (TMK1) interacts with and mediates phosphorylation and activation of plasma membrane H + -ATPases for apoplast acidi cation, while intracellular canonical auxin signalling promotes net cellular H + -in ux, causing apoplast alkalinisation. The simultaneous activation of these two counteracting mechanisms poises the root for a rapid, ne-tuned growth modulation while navigating complex soil environment. MainAuxin, a major growth regulator in plants, acts oppositely in shoots and roots. In shoots, canonical/intracellular auxin TRANSPORT INHIBITOR RESPONSE1 (TIR1)/AUXIN-SIGNALING F-BOX (AFB) receptors by downstream transcriptional regulation activate H + -pumps to acidify the apoplast a promote cell elongation 3,4 , in accordance with the Acid Growth Theory, which postulates that low apoplastic pH promotes growth 5 . In roots of many species including Arabidopsis, auxin inhibits growth. These contrasting responses are the basis for positive versus negative bending of roots and shoots in response to gravity and light 1 . The inhibitory auxin effect in roots also involves TIR1/AFB receptors but its rapid timing points towards an unknown non-transcriptional signalling branch 6 . Besides, a cell surface-based pathway involving TMK1 regulates development 7 , including differential growth in the apical hook 8 , while its role in auxin-regulated root growth remains unclear. Hence, the auxin signalling mechanism and the downstream processes for regulating root growth remain elusive.In this study, we revealed antagonistic action of intracellular TIR1/AFB and cell surface TMK1 auxin signalling converging on regulation of apoplastic pH, which we con rm as the key cellular mechanism allowing immediate and sensitive root growth regulation. Growth inhibition correlates with H + -in uxAuxin rapidly inhibits root growth through a non-transcriptional branch of TIR1/AFB signalling 6 . Although several cellular processes, including cortical microtubule (CMT) reorientation 9,10 , vacuolar fragmentation 11 and apoplastic pH changes [12][13][14] have been implicated, the causal mechanism remains unidenti ed.
In this review, we summarize the different biosynthesis-related pathways that contribute to the regulation of endogenous auxin in plants. We demonstrate that all known genes involved in auxin biosynthesis also have a role in root formation, from the initiation of a root meristem during embryogenesis to the generation of a functional root system with a primary root, secondary lateral root branches and adventitious roots. Furthermore, the versatile adaptation of root development in response to environmental challenges is mediated by both local and distant control of auxin biosynthesis. In conclusion, auxin homeostasis mediated by spatial and temporal regulation of auxin biosynthesis plays a central role in determining root architecture.
Highlights d SA modulates root development independently of NPR1mediated canonical signaling d SA attenuates growth through crosstalk with the auxin transport network d SA upregulates the phosphorylation status of PIN auxin efflux carriers through PP2A d SA directly targets A subunits of PP2A, inhibiting the activity of the complex
Wound-induced adventitious root (AR) formation is a requirement for plant survival upon root damage inflicted by pathogen attack, but also during the regeneration of plant stem cuttings for clonal propagation of elite plant varieties. Yet, adventitious rooting also takes place without wounding. This happens for example in etiolated Arabidopsis thaliana hypocotyls, in which AR initiate upon de-etiolation or in tomato seedlings, in which AR initiate upon flooding or high water availability. In the hypocotyl AR originate from a cell layer reminiscent to the pericycle in the primary root (PR) and the initiated AR share histological and developmental characteristics with lateral roots (LRs). In contrast to the PR however, the hypocotyl is a determinate structure with an established final number of cells. This points to differences between the induction of hypocotyl AR and LR on the PR, as the latter grows indeterminately. The induction of AR on the hypocotyl takes place in environmental conditions that differ from those that control LR formation. Hence, AR formation depends on differentially regulated gene products. Similarly to AR induction in stem cuttings, the capacity to induce hypocotyl AR is genotype-dependent and the plant growth regulator auxin is a key regulator controlling the rooting response. The hormones cytokinins, ethylene, jasmonic acid, and strigolactones in general reduce the root-inducing capacity. The involvement of this many regulators indicates that a tight control and fine-tuning of the initiation and emergence of AR exists. Recently, several genetic factors, specific to hypocotyl adventitious rooting in A. thaliana, have been uncovered. These factors reveal a dedicated signaling network that drives AR formation in the Arabidopsis hypocotyl. Here we provide an overview of the environmental and genetic factors controlling hypocotyl-born AR and we summarize how AR formation and the regulating factors of this organogenesis are distinct from LR induction.
Increasing drought and diminishing freshwater supplies have stimulated interest in developing small molecules that can be used to control transpiration. Receptors for the plant hormone abscisic acid (ABA) have emerged as key targets for this application, because ABA controls the apertures of stomata, which in turn regulate transpiration. Here, we describe the rational design of cyanabactin, an ABA receptor agonist that preferentially activates Pyrabactin Resistance 1 (PYR1) with low nanomolar potency. A 1.63 Å X-ray crystallographic structure of cyanabactin in complex with PYR1 illustrates that cyanabactin's arylnitrile mimics ABA's cyclohexenone oxygen and engages the tryptophan lock, a key component required to stabilize activated receptors. Further, its sulfonamide and 4-methylbenzyl substructures mimic ABA's carboxylate and C6 methyl groups, respectively. Isothermal titration calorimetry measurements show that cyanabactin's compact structure provides ready access to high ligand efficiency on a relatively simple scaffold. Cyanabactin treatments reduce Arabidopsis whole-plant stomatal conductance and activate multiple ABA responses, demonstrating that its in vitro potency translates to ABA-like activity in vivo. Genetic analyses show that the effects of cyanabactin, and the previously identified agonist quinabactin, can be abolished by the genetic removal of PYR1 and PYL1, which form subclade A within the dimeric subfamily III receptors. Thus, cyanabactin is a potent and selective agonist with a wide spectrum of ABA-like activities that defines subfamily IIIA receptors as key target sites for manipulating transpiration.
In many plants, the asymmetric division of the zygote sets up the apical-basal axis of the embryo. Unlike animals, plant zygotes are transcriptionally active, implying that plants have evolved specific mechanisms to control transcriptional activation of patterning genes in the zygote. In Arabidopsis, two pathways have been found to regulate zygote asymmetry: YODA (YDA) mitogen-activated protein kinase (MAPK) signaling, which is potentiated by sperm-delivered mRNA of the SHORT SUSPENSOR (SSP) membrane protein, and up-regulation of the patterning gene WOX8 by the WRKY2 transcription factor. How SSP/YDA signaling is transduced into the nucleus and how these pathways are integrated have remained elusive. Here we show that paternal SSP/YDA signaling directly phosphorylates WRKY2, which in turn leads to the up-regulation of WOX8 transcription in the zygote. We further discovered the transcription factors HOMEODOMAIN GLABROUS11/12 (HDG11/12) as maternal regulators of zygote asymmetry that also directly regulate WOX8 transcription. Our results reveal a framework of how maternal and paternal factors are integrated in the zygote to regulate embryo patterning.
SignificanceThis study identifies and outlines a nontranscriptional branch of the canonical GA signaling pathway that redirects protein traffic from the vacuolar degradation route to the plasma membrane. As a result, the amount of receptors and transporters, such as PIN transporters for the plant hormone auxin, is functionally regulated at the cell surface. The identified branching occurs at the level of DELLA proteins that, besides transcriptional regulation, also target the microtubule (MT) network and protein trafficking. In this work, we provide multiple lines of evidence that DELLA proteins act via their interacting partners Prefoldins and that a downstream MT/CLASP1 module regulates the activity of the retromer complex that directs protein trafficking at the intersection of the vacuolar and recycling pathways.
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