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Auxin-induced degradation dynamics set the pace for lateral root development.

ABSTRACT: Auxin elicits diverse cell behaviors through a simple nuclear signaling pathway initiated by degradation of Aux/IAA co-repressors. Our previous work revealed that members of the large Arabidopsis Aux/IAA family exhibit a range of degradation rates in synthetic contexts. However, it remained an unresolved issue whether differences in Aux/IAA turnover rates played a significant role in plant responses to auxin. Here, we use the well-established model of lateral root development to directly test the hypothesis that the rate of auxin-induced Aux/IAA turnover sets the pace for auxin-regulated developmental events. We did this by generating transgenic plants expressing degradation rate variants of IAA14, a crucial determinant of lateral root initiation. Progression through the well-established stages of lateral root development was strongly correlated with the engineered rates of IAA14 turnover, leading to the conclusion that Aux/IAAs are auxin-initiated timers that synchronize developmental transitions.

SUBMITTER: Guseman JM

PROVIDER: S-EPMC4352979 | biostudies-literature |

REPOSITORIES: biostudies-literature

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SLR/IAA14-dependent auxin induced lateral root initiation

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Noncanonical auxin signaling regulates cell division pattern during lateral root development.

Project description:In both plants and animals, multiple cellular processes must be orchestrated to ensure proper organogenesis. The cell division patterns control the shape of growing organs, yet how they are precisely determined and coordinated is poorly understood. In plants, the distribution of the phytohormone auxin is tightly linked to organogenesis, including lateral root (LR) development. Nevertheless, how auxin regulates cell division pattern during lateral root development remains elusive. Here, we report that auxin activates Mitogen-Activated Protein Kinase (MAPK) signaling via transmembrane kinases (TMKs) to control cell division pattern during lateral root development. Both TMK1/4 and MKK4/5-MPK3/6 pathways are required to properly orient cell divisions, which ultimately determine lateral root development in response to auxin. We show that TMKs directly and specifically interact with and phosphorylate MKK4/5, which is required for auxin to activate MKK4/5-MPK3/6 signaling. Our data suggest that TMK-mediated noncanonical auxin signaling is required to regulate cell division pattern and connect auxin signaling to MAPK signaling, which are both essential for plant development.

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Project description:Lateral root (LR) formation promotes plant resistance, whereas high-level ethylene induced by abiotic stress will inhibit LR emergence. Considering that local auxin accumulation is a precondition for LR generation, auxin-induced genes inhibiting ethylene synthesis may thus be important for LR development. Here, we found that auxin response factor 4 (SaARF4) in Sedum alfredii Hance could be induced by auxin. The overexpression of SaARF4 decreased the LR number and reduced the vessel diameters. Meanwhile, the auxin distribution mode was altered in the root tips and PIN expression was also decreased in the overexpressed lines compared with the wild-type (WT) plants. The overexpression of SaARF4 could reduce ethylene synthesis, and thus, the repression of ethylene production decreased the LR number of WT and reduced PIN expression in the roots. Furthermore, the quantitative real-time PCR, chromatin immunoprecipitation sequencing, yeast one-hybrid, and dual-luciferase assay results showed that SaARF4 could bind the promoter of 1-aminocyclopropane-1-carboxylate oxidase 4 (SaACO4), associated with ethylene biosynthesis, and could downregulate its expression. Therefore, we concluded that SaARF4 induced by auxin can inhibit ethylene biosynthesis by repressing SaACO4 expression, and this process may affect auxin transport to delay LR development.

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PRH1 mediates ARF7-LBD dependent auxin signaling to regulate lateral root development in Arabidopsis thaliana.

Project description:The development of lateral roots in Arabidopsis thaliana is strongly dependent on signaling directed by the AUXIN RESPONSE FACTOR7 (ARF7), which in turn activates LATERAL ORGAN BOUNDARIES DOMAIN (LBD) transcription factors (LBD16, LBD18 and LBD29). Here, the product of PRH1, a PR-1 homolog annotated previously as encoding a pathogen-responsive protein, was identified as a target of ARF7-mediated auxin signaling and also as participating in the development of lateral roots. PRH1 was shown to be strongly induced by auxin treatment, and plants lacking a functional copy of PRH1 formed fewer lateral roots. The transcription of PRH1 was controlled by the binding of both ARF7 and LBDs to its promoter region.

| S-EPMC7006904 | biostudies-literature

Hydrogen Gas Is Involved in Auxin-Induced Lateral Root Formation by Modulating Nitric Oxide Synthesis.

Project description:Metabolism of molecular hydrogen (H?) in bacteria and algae has been widely studied, and it has attracted increasing attention in the context of animals and plants. However, the role of endogenous H? in lateral root (LR) formation is still unclear. Here, our results showed that H?-induced lateral root formation is a universal event. Naphthalene-1-acetic acid (NAA; the auxin analog) was able to trigger endogenous H? production in tomato seedlings, and a contrasting response was observed in the presence of N-1-naphthyphthalamic acid (NPA), an auxin transport inhibitor. NPA-triggered the inhibition of H? production and thereafter lateral root development was rescued by exogenously applied H?. Detection of endogenous nitric oxide (NO) by the specific probe 4-amino-5-methylamino-2',7'-difluorofluorescein diacetate (DAF-FM DA) and electron paramagnetic resonance (EPR) analyses revealed that the NO level was increased in both NAA- and H?-treated tomato seedlings. Furthermore, NO production and thereafter LR formation induced by auxin and H? were prevented by 2-4-carboxyphenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO; a specific scavenger of NO) and the inhibitor of nitrate reductase (NR; an important NO synthetic enzyme). Molecular evidence confirmed that some representative NO-targeted cell cycle regulatory genes were also induced by H?, but was impaired by the removal of endogenous NO. Genetic evidence suggested that in the presence of H?, Arabidopsis mutants nia2 (in particular) and nia1 (two nitrate reductases (NR)-defective mutants) exhibited defects in lateral root length. Together, these results demonstrated that auxin-induced H? production was associated with lateral root formation, at least partially via a NR-dependent NO synthesis.

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| S-SCDT-EMBOJ-2019-101928 | biostudies-other

Strigolactones and auxin cooperate to regulate lateral root development in response to nitrate

Project description:In maize, nitrate regulates root development thanks to the coordinated action of many players. In this study, the involvement of SLs and auxin as putative downstream components of the nitrate regulation of lateral root development was investigated. To this aim, the endogenous SL content of maize root in response to nitrate availability was assessed by means of LC-MS/MS and measurements of lateral root density in the presence of analogues or inhibitors of auxin and strigolactones were performed. Furthermore, un untargeted RNA-seq based approach was used to better characterize the participation of auxin and strigolacotones to the transcriptional signature of maize root response to nitrate. Our results suggested that N deprivation toughly induces zealactone and carlactonoic acid biosynthesis in maize root, to a higher extent if compared to P-deprived roots. Moreover, data on lateral root density led to hypothesise the existence of both auxin-dependent and auxin-independent effects of nitrate on LR development. In addition, the inhibition of SL biosynthesis seems to participate to the auxin-dependent induction of LR, but the involvement of further downstream unknown components cannot be ruled out.

2021-04-11 | GSE162411 | GEO

Fine control of aerenchyma and lateral root development through AUX/IAA- and ARF-dependent auxin signaling.

Project description:Lateral roots (LRs) are derived from a parental root and contribute to water and nutrient uptake from the soil. Auxin/indole-3-acetic acid protein (AUX/IAA; IAA) and auxin response factor (ARF)-mediated signaling are essential for LR formation. Lysigenous aerenchyma, a gas space created by cortical cell death, aids internal oxygen transport within plants. Rice (Oryza sativa) forms lysigenous aerenchyma constitutively under aerobic conditions and increases its formation under oxygen-deficient conditions; however, the molecular mechanisms regulating constitutive aerenchyma (CA) formation remain unclear. LR number is reduced by the dominant-negative effect of a mutated AUX/IAA protein in the iaa13 mutant. We found that CA formation is also reduced in iaa13 We have identified ARF19 as an interactor of IAA13 and identified a lateral organ boundary domain (LBD)-containing protein (LBD1-8) as a target of ARF19. IAA13, ARF19, and LBD1-8 were highly expressed in the cortex and LR primordia, suggesting that these genes function in the initiation of CA and LR formation. Restoration of LBD1-8 expression recovered aerenchyma formation and partly recovered LR formation in the iaa13 background, in which LBD1-8 expression was reduced. An auxin transport inhibitor suppressed CA and LR formation, and a natural auxin stimulated CA formation in the presence of the auxin transport inhibitor. Our findings suggest that CA and LR formation are both regulated through AUX/IAA- and ARF-dependent auxin signaling. The initiation of CA formation lagged that of LR formation, which indicates that the formation of CA and LR are regulated differently by auxin signaling during root development in rice.

| S-EPMC6789968 | biostudies-literature

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