Antagonistic and auxin-dependent phosphoregulation of columella PIN proteins controls lateral root gravitropic setpoint angle in Arabidopsis

Roychoudhry, Suruchi; Sageman-Furnas, Katelyn; Wolverton, Chris; Hl, Goodman; Grones, Peter; Mullen, Jack L.; Hangarter, Roger P.; Friml, Jiřı́; Kepinski, Stefan

doi:10.1101/594838

Cited by 5 publications

(14 citation statements)

References 53 publications

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“…1C). Since the effect of auxin and CK in governing GSA is already explored (Rosquete et al 2013(Rosquete et al , 2018Roychoudhry et al 2013Roychoudhry et al , 2019Waidmann et al 2019), we wanted to identify the role of other hormones in modulating this response. The Arabidopsis WT seedlings did not display any changes in branching angle when grown in brassinosteroids (BR), gibberellic acid (GA 3 ), 1-aminocyclopropane-1-carboxylic acid (ACC) or abscisic acid (ABA) (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…In plants, phytohormones have profound effects on determining GSA. For example, as mentioned above, recent findings have identified the fundamental role of auxin in governing the GSA of shoot branches and LRs of Arabidopsis thaliana and other vascular plants, such as rice and beans (Rosquete et al 2013;Rosquete, Waidmann & Kleine-Vehn 2018;Roychoudhry, Del Bianco, Kieffer & Kepinski 2013;Roychoudhry et al 2017Roychoudhry et al , 2019.…”

Section: Introductionmentioning

confidence: 91%

“…Auxin transport and signalling lies downstream to MeJA-mediated modulation of branching angle. Recent reports have shed light on the role of PIN auxin efflux activity and the TIR1/AFB-Aux/IAA-ARF-dependent auxin signalling module for the establishment of GSA in young LRs (Rosquete et al 2013(Rosquete et al , 2018Roychoudhry et al 2013Roychoudhry et al , 2019. We, therefore, assessed the involvement of auxin transport and signalling to govern this physiological response.…”

Section: Arabidopsismentioning

confidence: 99%

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Jasmonic Acid coordinates with Light, Glucose and Auxin signalling in Regulating Branching Angle ofArabidopsisLateral Roots

Sharma

Jamsheer

et al. 2020

Preprint

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The role of jasmonates (JAs) in root growth and development and plants response to external stimuli is already known. However, its role in lateral root (LR) development remains perplexing. Our work identifies methyl jasmonate (MeJA) as a crucial phytohormone in determining the branching angle of Arabidopsis LRs. MeJA inclines the LRs to a more vertical orientation which was dependent on JAR1-COI1-MYC2,3,4 signalling. Our work highlights the dual role of light acting with MeJA in governing the LR angle. Glucose (Glc), produced by light mediated photosynthesis induces wider branching angles. Combining physiological and molecular assays, we reveal that Glc antagonizes the MeJA response via HEXOKINASE1 (HXK1) mediated signalling and by stabilizing JAZ9. Moreover, physiological assays using auxin mutants; binding of MYC2 on the promoters of auxin biosynthetic gene CYP79B2 and LAZY2 and asymmetric distribution of DR5::GFP and PIN2::GFP pinpoints the role of an intact auxin machinery required by MeJA for vertical growth of LRs. We also demonstrate that light perception through PHYTOCHROMES (PHYA and PHYB) and LONG HYPOCOTYL5 (HY5) are indispensable for inducing vertical angles by MeJA. Thus, our investigation highlights antagonism between light and Glc signalling and how they interact with JA-auxin signals to optimize the branching angle of LRs.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 91%

Section: Arabidopsismentioning

confidence: 99%

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Jasmonic Acid coordinates with Light, Glucose and Auxin signalling in Regulating Branching Angle ofArabidopsisLateral Roots

Sharma

Jamsheer

et al. 2020

Preprint

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“…In addition, PP2A proteins dephosphorylate PIN1 proteins, leading to their basal location (Costa et al, 2020). Other studies have also shown that PIN3 and PIN7 proteins expressed in the columella region have their subcellular location at the root, and this varies according to the orientation of the gravitational field (Roychoudhry et al, 2019). Furthermore, the dynamic distribution of the PIN proteins on different sides of cells (transcytosis) is responsible for rapid changes in the polarity of the PIN protein, which allows auxin efflux to be quickly redirected in response to environmental signals (Costa et al, 2020;Qi et al, 2020).…”

Section: Auxin Transport and Distributionmentioning

confidence: 99%

“…In nodular roots of Elaeagnus umbellata, the gene EuNOD-ARP1 (Auxin Repressed Protein) was identified, which encodes a cytosolic protein with a higher level of expression in the zone of nodule fixation in roots than in leaves (Kim et al, 2007). Studies have reported the influence of strigolactone signalling on auxin transport, where mutants of Arabidopsis with high expression of the auxin efflux transporters PIN1 and PIN3 showed increased auxin transport capacity, indicating that strigolactones act directly on apical dominance and repress auxin transport, which prevents auxin synthesized in the lateral shoots from being transferred to the main stem (Banasiak et al, 2019;Roychoudhry et al, 2019;Zwiewka et al, 2019). Expression analysis showed that 48 genes are co-regulated by auxin and brassinosteroid (BR), including SAUR (SMALL AUXIN UP-REGULATED RNAs), Aux/IAA, and GH3 (GRETCHEN HAGEN3) (Hirano et al, 2017;Spartz et al, 2017).…”

Section: Gene Expression Regulated By Auxinmentioning

confidence: 99%

Auxin and its role in plant development: structure, signalling, regulation and response mechanisms

2021

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Auxins are plant hormones that play a central role in controlling plant growth and development across different environmental conditions. Even at low concentrations, auxins can regulate gene expression through specific transcription factors and proteins that are modulated to environmental responses in the signalling cascade. Auxins are synthesized in tissues with high cell division activity and distributed by specific transmembrane proteins that regulate efflux and influx. This review presents recent advances in understanding the biosynthetic pathways, both dependent and independent of tryptophan, highlighting the intermediate indole compounds (indole-3-acetamide, indole-3-acetaldoxime, indole-3-pyruvic acid and tryptamine) and the key enzymes for auxin biosynthesis, such as YUCs and TAAs. In relation to the signalling cascade, it has been shown that auxins influence gene expression regulation by the connection between synthesis and distribution. Moreover, the molecular action of the auxin response factors and auxin/indole-3-acetic acid transcription factors with the F-box TIR1/AFB auxin receptors regulates gene expression. In addition, the importance of microRNAs in the auxin signalling pathway and their influence on plant plasticity to environmental fluctuations is also demonstrated. Finally, this review describes the chemical and biological processes involving auxins in plants.

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Antigravitropic PIN polarization maintains non-vertical growth in lateral roots

Roychoudhry,

Sageman-Furnas,

Wolverton

et al. 2023

Nat. Plants

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Lateral roots are typically maintained at non-vertical angles with respect to gravity. These gravitropic setpoint angles are intriguing because their maintenance requires that roots are able to effect growth response both with and against the gravity vector, a phenomenon previously attributed to gravitropism acting against an antigravitropic offset mechanism. Here we show how the components mediating gravitropism in the vertical primary root—PINs and phosphatases acting upon them—are reconfigured in their regulation such that lateral root growth at a range of angles can be maintained. We show that the ability of Arabidopsis lateral roots to bend both downward and upward requires the generation of auxin asymmetries and is driven by angle-dependent variation in downward gravitropic auxin flux acting against angle-independent upward, antigravitropic flux. Further, we demonstrate a symmetry in auxin distribution in lateral roots at gravitropic setpoint angle that can be traced back to a net, balanced polarization of PIN3 and PIN7 auxin transporters in the columella. These auxin fluxes are shifted by altering PIN protein phosphoregulation in the columella, either by introducing PIN3 phosphovariant versions or via manipulation of levels of the phosphatase subunit PP2A/RCN1. Finally, we show that auxin, in addition to driving lateral root directional growth, acts within the lateral root columella to induce more vertical growth by increasing RCN1 levels, causing a downward shift in PIN3 localization, thereby diminishing the magnitude of the upward, antigravitropic auxin flux.

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Antagonistic and auxin-dependent phosphoregulation of columella PIN proteins controls lateral root gravitropic setpoint angle in Arabidopsis

Cited by 5 publications

References 53 publications

Jasmonic Acid coordinates with Light, Glucose and Auxin signalling in Regulating Branching Angle ofArabidopsisLateral Roots

Jasmonic Acid coordinates with Light, Glucose and Auxin signalling in Regulating Branching Angle ofArabidopsisLateral Roots

Auxin and its role in plant development: structure, signalling, regulation and response mechanisms

Antigravitropic PIN polarization maintains non-vertical growth in lateral roots

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