Regulation of AUXIN RESPONSE FACTOR condensation and nucleo-cytoplasmic partitioning

Jing, Hongwei; Korasick, David A.; Emenecker, Ryan; Morffy, Nicholas; Wilkinson, Edward G.; Powers, Samantha K.; Strader, Lucia C.

doi:10.1038/s41467-022-31628-2

Cited by 35 publications

(32 citation statements)

References 23 publications

(36 reference statements)

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“…To address if ARF7 accumulates exclusively due to autophagy deficiency, we also treated seedlings with the proteasome inhibitor with MG132 (Fig 1A-C) and observed that simultaneous inhibition of both degradation pathways leads to further accumulation of ARF7. These results indicate that ARF7 proteostasis is dependent on autophagy and the proteasome and are in agreement with data by Jing et al , (2022), in what concerns proteasomal participation in ARFs turnover. Because ARF7 often works together with ARF19 during regulation of root architecture, we also enquired about autophagy’s role during ARF19 turnover.…”

Section: Resultssupporting

confidence: 92%

“…It is possible that autophagy inhibition leads to ARF7 accumulation which may induce supersaturation (Mcswiggen et al , 2019) and cause ARF7 condensation in the cytoplasm (Fig 1 & 3). Recent reports (Powers et al , 2019; Jing et al , 2022) have linked ARFs condensation with decreased auxin responsiveness, therefore, the disruption of protein degradation pathways we report here causes ARF7 levels to increase, promoting cytoplasmic aggregation and consequent reduced auxin responsiveness. While our data provides an indication that the mobilization of ARF7 to cytoplasmic foci might be part of a mechanisms aimed at adjusting ARF7 abundance and auxin responsiveness, more experiments are needed to fully understand this process.…”

Section: Discussionmentioning

confidence: 49%

“…Here, we show how autophagy modulates ARF7 and ARF19 turnover and this can be carried selectively through NBR1 (Fig 1 & 2). We and others (Jing et al, 2022) have shown that MG132 treatment also causes ARF7 to accumulate, which suggests proteasomal activity also regulates this TF turnover.…”

Section: Discussionmentioning

confidence: 67%

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NBR1-mediated selective autophagy of ARF7 modulates root branching

Ebstrup

Ansboel

Chevalier

et al. 2022

Preprint

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Auxin is a critical hormone involved in growth and developmental regulation in plants. For instance, auxin dictates the roots architecture via the Auxin Response Factor (ARF) family of transcription factors, which control different aspects of lateral roots (LR) formation. In Arabidopsis, ARF7 is essential for the correct definition of LRs pre-branch sites (PBS) through an oscillatory mechanism controlling gene expression. Moreover, ARF7 also plays a pivotal role during the decision making necessary to initiate LR formation. Despite the relevance of ARF7 to this process, there is a surprising lack of knowledge about how proteostasis of ARF7 is regulated and how this impacts its function during root architecture patterning. Here, we show that ARF7 accumulates in autophagy mutants, localizes to autophagosomes and it is targeted for degradation through selective autophagy via the cargo adaptor NBR1. Moreover, we report that rhythmic changes to ARF7 abundance are a whole plant process and require functional autophagy to occur. Surprisingly, autophagy deficiency does not seem to impact PBS establishment but affects LR formation; this might be explained by the fact that autophagy mainly seems to regulate ARF7 abundance in mature root tissue but only play an accessory role in younger root tissue. In conclusion we report a novel role for autophagy during plant development, through the selective degradation of ARF7 to optimize root branching

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Section: Resultssupporting

confidence: 92%

Section: Discussionmentioning

confidence: 49%

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NBR1-mediated selective autophagy of ARF7 modulates root branching

Ebstrup

Ansboel

Chevalier

et al. 2022

Preprint

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“…The purified His-IAA17 recombinant proteins were used to immunize mice and rabbits, respectively. Immunoblot analysis was performed as described previously 31,32 . Total plant proteins were prepared by grinding seedlings in liquid nitrogen and then extracted in lysis buffer (50 mM Tris-HCl, pH 8.0, 150 mM NaCl, 1% (v/v) Nonidet P-40, 0.5% (w/v) sodium deoxycholate, 0.1% (w/v) SDS and 1 mM phenylmethylsulfonyl fluoride (PMSF), and 1% (v/v) protease inhibitors cocktail (Sigma-Aldrich, P9599).…”

Section: Methodsmentioning

confidence: 99%

S-nitrosylation of Aux/IAA protein represses auxin signaling

Jing¹,

Yang²,

Feng

et al. 2022

Preprint

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Auxin plays crucial roles in nearly every aspect of plant growth and development. Auxin signaling activation is mediated through degradation of Auxin/INDOLE-3-ACETIC ACID (Aux/IAA) family. Nitric oxide (NO) regulates diverse cellular bioactivities through S-nitrosylation of target protein at specific cysteine residues. NO-auxin interplay has an important role in regulation plant growth. However, little is known about the molecular mechanism of how NO effects Aux/IAA proteins stability. Here we show that NO negatively regulates the IAA17 protein stability to repress auxin signaling. We found that NO directly inhibits IAA17 protein degradation. S-nitrosylation of IAA17 at Cys-70 represses the TIR-IAA17 co-receptor interaction to attenuate auxin responsiveness. Our data suggest a model in which S-nitrosylation of IAA17 at Cys-70 negatively regulates auxin signaling to effect plant development, providing a mechanism for redox-phytohormones networks.

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“…Some ARFs undergo phase conversion to form cytoplasmic protein condensates in cells that have ceased active growth so that the auxin response may be developmentally regulated (52). Identi cation of Auxin Response Factor F-Box1 (AFF1) suggested ARF condensation as a major mechanism to regulate transcriptional activity (53). Based on available genetic and genomic data, a network of transcriptional repressors has been proposed to explain how class A activators of the ARF family are regulated (54).…”

Section: Introductionmentioning

confidence: 99%

Defining in vivo transcriptional responses to auxin

Xie¹,

Huang

Song

et al. 2022

Preprint

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The plant hormone auxin regulates many aspects of the plant life cycle through a series of transcriptional responses mediated by Auxin Response Factors (ARFs). However, thus far, it has not been possible to identify in vivo DNA binding sites for most of ARFs leading to a major gap in our understanding of these master regulatory transcription factors. Here we identify the DNA binding profiles for several ARFs as well as Aux/IAA proteins (IAAs), repressors of the response to auxin that heterodimerize with ARFs, using ChIP-seq. As expected, the common target genes of all tested ARFs are highly enriched in known auxin-responsive genes, each containing the motif K(T/G)GTCBB(T/G/C) with a core GTC and a non-A flanking sequence. Unexpectedly, genome-wide ARF binding sites are strongly associated with Aux/IAA ChIP-seq peaks, providing evidence that the Aux/IAA-ARF complex may control auxin transcriptional responses directly on the promoters of hormone-responsive genes. Additionally, we find that ABA response genes are also primary targets of an ARF10-IAA19 module and that a putative repressor ARF(ARF10) binds the same set of targets as activator ARFs. Finally, although ARFs have previously been reported to have strict spacing between their motifs when assayed in vitro, we observe that conservation of the spacing of ARF binding motifs is less rigid when assayed in planta.

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Regulation of AUXIN RESPONSE FACTOR condensation and nucleo-cytoplasmic partitioning

Cited by 35 publications

References 23 publications

NBR1-mediated selective autophagy of ARF7 modulates root branching

NBR1-mediated selective autophagy of ARF7 modulates root branching

S-nitrosylation of Aux/IAA protein represses auxin signaling

Defining in vivo transcriptional responses to auxin

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