Light triggers PILS-dependent reduction in nuclear auxin signalling for growth transition.
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ABSTRACT:
SUBMITTER: Beziat C
PROVIDER: S-EPMC5524181 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:BACKGROUND: The plant hormone auxin directs many aspects of plant growth and development. To understand the evolution of auxin signalling, we compared the genes encoding two families of crucial transcriptional regulators, AUXIN RESPONSE FACTOR (ARF) and AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA), among flowering plants and two non-seed plants, Physcomitrella patens and Selaginella moellendorffii. RESULTS: Comparative analysis of the P. patens, S. moellendorffii and Arabidopsis thaliana genomes suggests that the well-established rapid transcriptional response to auxin of flowering plants, evolved in vascular plants after their divergence from the last common ancestor shared with mosses. An N-terminally truncated ARF transcriptional activator is encoded by the genomes of P. patens and S. moellendorffii, and suggests a supplementary mechanism of nuclear auxin signalling, absent in flowering plants. Site-specific analyses of positive Darwinian selection revealed relatively high rates of synonymous substitution in the A. thaliana ARFs of classes IIa (and their closest orthologous genes in poplar) and Ib, suggesting that neofunctionalization in important functional regions has driven the evolution of auxin signalling in flowering plants. Primary auxin responsive gene families (GH3, SAUR, LBD) show different phylogenetic profiles in P. patens, S. moellendorffii and flowering plants, highlighting genes for further study. CONCLUSION: The genome of P. patens encodes all of the basic components necessary for a rapid auxin response. The spatial separation of the Q-rich activator domain and DNA-binding domain suggests an alternative mechanism of transcriptional control in P. patens distinct from the mechanism seen in flowering plants. Significantly, the genome of S. moellendorffii is predicted to encode proteins suitable for both methods of regulation.
| S-EPMC2708152 | biostudies-literature
Project description:Multiple internal and external signals modulate the metabolism, intercellular transport and signaling of the phytohormone auxin. Considering this complexity, it remains largely unknown how plant cells monitor and ensure the homeostasis of auxin responses. PIN-LIKES (PILS) intracellular auxin transport facilitators at the endoplasmic reticulum are suitable candidates to buffer cellular auxin responses because they limit nuclear abundance and signaling of auxin. We used forward genetics to identify gloomy and shiny pils (gasp) mutants that define the PILS6 protein abundance in a post-translational manner. Here, we show that GASP1 encodes an uncharacterized RING/U-box superfamily protein that impacts on auxin signaling output. The low auxin signaling in gasp1 mutants correlates with reduced abundance of PILS5 and PILS6 proteins. Mechanistically, we show that high and low auxin conditions increase and reduce PILS6 protein levels, respectively. Accordingly, non-optimum auxin concentrations are buffered by alterations in PILS6 abundance, consequently leading to homeostatic auxin output regulation. We envision that this feedback mechanism provides robustness to auxin-dependent plant development.
| S-EPMC9340555 | biostudies-literature
Project description:The phytohormone auxin contributes to virtually every aspect of the plant development. The spatiotemporal distribution of auxin depends on a complex interplay between auxin metabolism and intercellular auxin transport. Intracellular auxin compartmentalization provides another link between auxin transport processes and auxin metabolism. The PIN-LIKES (PILS) putative auxin carriers localize to the endoplasmic reticulum (ER) and contribute to cellular auxin homeostasis. PILS proteins regulate intracellular auxin accumulation, the rate of auxin conjugation and, subsequently, affect nuclear auxin signaling. Here, we investigate sequence diversification of the PILS family in Arabidopsis thaliana and provide insights into the evolution of these novel putative auxin carriers in plants. Our data suggest that PILS proteins are conserved throughout the plant lineage and expanded during higher plant evolution. PILS proteins diversified early during plant evolution into three clades. Besides the ancient Clade I encompassing non-land plant species, PILS proteins evolved into two clades. The diversification of Clade II and Clade III occurred already at the level of non-vascular plant evolution and, hence, both clades contain vascular and non-vascular plant species. Nevertheless, Clade III contains fewer non- and increased numbers of vascular plants, indicating higher importance of Clade III for vascular plant evolution. Notably, PILS proteins are distinct and appear evolutionarily older than the prominent PIN-FORMED auxin carriers. Moreover, we revealed particular PILS sequence divergence in Arabidopsis and assume that these alterations could contribute to distinct gene regulations and protein functions.
| S-EPMC3470039 | biostudies-literature
Project description:Arabidopsis thaliana shoot branching is inhibited by a low red light to far red light ratio (R:FR, an indicator of competition), and by loss of phytochrome B function. Prior studies have shown that phytochrome B deficiency suppresses bud growth by elevating systemic auxin signalling, and that increasing the R:FR promotes the growth of buds suppressed by low R:FR by inhibiting bud abscisic acid (ABA) accumulation and signalling. Here, systemic auxin signalling and bud ABA signalling were examined in the context of rapid bud responses to an increased R:FR. Increasing the R:FR promoted the growth of buds inhibited by a low R:FR within 6 h. Relative to a low R:FR, bud ABA accumulation and signalling in plants given a high R:FR showed a sustained decline within 3 h, prior to increased growth. Main stem auxin levels and signalling showed a weak, transient response. Systemic effects and those localised to the bud were further examined by decapitating plants maintained either under a low R:FR or provided with a high R:FR. Increasing the R:FR promoted bud growth before decapitation, but decapitated plants eventually formed longer branches. The data suggest that rapid responses to an increased R:FR may be mediated by changes in bud ABA physiology, although systemic auxin signalling is necessary for sustained bud repression under a low R:FR.
| S-EPMC5444464 | biostudies-literature
Project description:Arabidopsis plants transfer information from the leaf tip to the petiole base to induce adaptive upward leaf movement upon neighbour detection through Far-Red light enrichment in the leaf tip. To determine how a distally derived signal can specifically regulate growth in the abaxial petiole we analysed the transcriptome in the leaf tip and abaxial-adaxially split petiole sections during the first hours of far-red enrichment.
2022-12-20 | GSE218944 | GEO
Project description:The phytohormone auxin is the information carrier in a plethora of developmental and physiological processes in plants1. It has been firmly established that canonical, nuclear auxin signalling acts through regulation of gene transcription2. Here, we combined microfluidics, live imaging, genetic engineering and computational modelling to reanalyse the classical case of root growth inhibition3 by auxin. We show that Arabidopsis roots react to addition and removal of auxin by extremely rapid adaptation of growth rate. This process requires intracellular auxin perception but not transcriptional reprogramming. The formation of the canonical TIR1/AFB-Aux/IAA co-receptor complex is required for the growth regulation, hinting to a novel, non-transcriptional branch of this signalling pathway. Our results challenge the current understanding of root growth regulation by auxin and suggest another, presumably non-transcriptional, signalling output of the canonical auxin pathway.
| S-EPMC6104345 | biostudies-literature
Project description:Auxin is an important regulator of plant ontogenies including embryo development and the exogenous application of this phytohormone has been found to be necessary for the induction of the embryogenic response in plant explants that have been cultured in vitro. However, in the present study, we show that treatment of Arabidopsis explants with trichostatin A (TSA), which is a chemical inhibitor of histone deacetylases, induces somatic embryogenesis (SE) without the exogenous application of auxin. We found that the TSA-treated explants generated somatic embryos that developed efficiently on the adaxial side of the cotyledons, which are the parts of an explant that are involved in auxin-induced SE. A substantial reduction in the activity of histone deacetylase (HDAC) was observed in the TSA-treated explants, thus confirming a histone acetylation-related mechanism of the TSA-promoted embryogenic response. Unexpectedly, the embryogenic effect of TSA was lower on the auxin-supplemented media and this finding further suggests an auxin-related mechanism of TSA-induced SE. Congruently, we found a significantly increased content of indolic compounds, which is indicative of IAA and an enhanced DR5::GUS signal in the TSA-treated explants. In line with these results, two of the YUCCA genes (YUC1 and YUC10), which are involved in auxin biosynthesis, were found to be distinctly up-regulated during TSA-induced SE and their expression was colocalised with the explant sites that are involved in SE. Beside auxin, ROS were extensively accumulated in response to TSA, thereby indicating that a stress-response is involved in TSA-triggered SE. Relevantly, we showed that the genes encoding the transcription factors (TFs) that have a regulatory function in auxin biosynthesis including LEC1, LEC2, BBM, and stress responses (MYB118) were highly up-regulated in the TSA-treated explants. Collectively, the results provide several pieces of evidence about the similarities between the molecular pathways of SE induction that are triggered by TSA and 2,4-D that involve the activation of the auxin-responsive TF genes that have a regulatory function in auxin biosynthesis and stress responses. The study suggests the involvement of histone acetylation in the auxin-mediated release of the embryogenic program of development in the somatic cells of Arabidopsis.
| S-EPMC6146766 | biostudies-literature
Project description:Plants, although sessile, can reorient growth axes in response to changing environmental conditions. Phototropism and gravitropism represent adaptive growth responses induced by changes in light direction and growth axis orientation relative to gravitational direction, respectively. The nearly 80-year-old Cholodny-Went theory [Went, F. W. & Thimann, K. V. (1937) Phytohormones (Macmillan, New York)] predicts that formation of a gradient of the plant morphogen auxin is central to the establishment of tropic curvature. Loss of tropic responses in seedling stems of Arabidopsis thaliana mutants lacking the auxin-regulated transcriptional activator NPH4/ARF7 has further suggested that a gradient of gene expression represents an essential output from the auxin gradient. Yet the molecular identities of such output components, which are likely to encode proteins directly involved in growth control, have remained elusive. Here we report the discovery of a suite of tropic stimulus-induced genes in Brassica oleracea that are responsive to an auxin gradient and exhibit morphologically graded expression concomitant with, or before, observable curvature responses. These results provide compelling molecular support for the Cholodny-Went theory and suggest that morphologically graded transcription represents an important mechanism for interpreting tropically stimulated gradients of auxin. Intriguingly, two of the tropic stimulus-induced genes, EXPA1 and EXPA8, encode enzymes involved in cell wall extension, a response prerequisite for differential growth leading to curvatures, and are up-regulated before curvature in the flank that will elongate. This observation suggests that morphologically graded transcription likely leads to the graded expression of proteins whose activities can directly regulate the establishment and modulation of tropic curvatures.
| S-EPMC1324985 | biostudies-literature
Project description:Organogenesis of legume root nodules begins with the nodulation factor-dependent stimulation of compatible root cells to initiate divisions, signifying an early nodule primordium formation event. This is followed by cellular differentiation, including cell expansion and vascular bundle formation, and we previously showed that Lotus japonicus NF-YA1 is essential for this process, presumably by regulating three members of the SHORT INTERNODES/STYLISH (STY) transcription factor gene family. In this study, we used combined genetics, genomics and cell biology approaches to characterize the role of STY genes during root nodule formation and to test a hypothesis that they mediate nodule development by stimulating auxin signalling. We show here that L. japonicus STYs are required for nodule emergence. This is attributed to the NF-YA1-dependent regulatory cascade, comprising STY genes and their downstream targets, YUCCA1 and YUCCA11, involved in a local auxin biosynthesis at the post-initial cell division stage. An analogous NF-YA1/STY regulatory module seems to operate in Medicago truncatula in association with the indeterminate nodule patterning. Our data define L. japonicus and M. truncatula NF-YA1 genes as important nodule emergence stage-specific regulators of auxin signalling while indicating that the inductive stage and subsequent formation of early nodule primordia are mediated through an independent mechanism(s).
| S-EPMC7984406 | biostudies-literature
Project description:The second messenger cyclic guanosine 3',5'-monophosphate (cGMP) plays an important role in plant development and responses to stress. Recent studies indicated that cGMP is a secondary signal generated in response to auxin stimulation. cGMP also mediates auxin-induced adventitious root formation in mung bean and gravitropic bending in soybean. Nonetheless, the mechanism of the participation of cGMP in auxin signalling to affect these growth and developmental processes is largely unknown. In this report we provide evidence that indole-3-acetic acid (IAA) induces cGMP accumulation in Arabidopsis roots through modulation of the guanylate cyclase activity. Application of 8-bromo-cGMP (a cell-permeable cGMP derivative) increases auxin-dependent lateral root formation, root hair development, primary root growth, and gene expression. In contrast, inhibitors of endogenous cGMP synthesis block these processes induced by auxin. Data also showed that 8-bromo-cGMP enhances auxin-induced degradation of Aux/IAA protein modulated by the SCF(TIR1) ubiquitin-proteasome pathway. Furthermore, it was found that 8-bromo-cGMP is unable to directly influence the auxin-dependent TIR1-Aux/IAA interaction as evidenced by pull-down and yeast two-hybrid assays. In addition, we provide evidence for cGMP-mediated modulation of auxin signalling through cGMP-dependent protein kinase (PKG). Our results suggest that cGMP acts as a mediator to participate in auxin signalling and may govern this process by PKG activity via its influence on auxin-regulated gene expression and auxin/IAA degradation.
| S-EPMC3967089 | biostudies-literature