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Selective auxin agonists induce specific AUX/IAA protein degradation to modulate plant development

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Abstract
Auxin phytohormones control most aspects of plant development through a complex and interconnected signaling network. In the presence of auxin, AUXIN/INDOLE-3-ACETIC ACID (AUX/IAA) transcriptional repressors are targeted for degradation by the SKP1-CULLIN1-F-BOX (SCF) ubiquitin-protein ligases containing TRANSPORT INHIBITOR RESISTANT 1/AUXIN SIGNALING F-BOX (TIR1/AFB). CULLIN1-neddylation is required for SCFTIR1/AFB functionality, as exemplified by mutants deficient in the NEDD8-activating enzyme subunit AUXIN-RESISTANT 1 (AXR1). Here, we report a chemical biology screen that identifies small molecules requiring AXR1 to modulate plant development. We selected four molecules of interest, RubNeddin 1 to 4 (RN1 to -4), among which RN3 and RN4 trigger selective auxin responses at transcriptional, biochemical, and morphological levels. This selective activity is explained by their ability to consistently promote the interaction between TIR1 and a specific subset of AUX/IAA proteins, stimulating the degradation of particular AUX/IAA combinations. Finally, we performed a genetic screen using RN4, the RN with the greatest potential for dissecting auxin perception, which revealed that the chromatin remodeling ATPase BRAHMA is implicated in auxin-mediated apical hook development. These results demonstrate the power of selective auxin agonists to dissect auxin perception for plant developmental functions, as well as offering opportunities to discover new molecular players involved in auxin responses.
Keywords
auxin, chemical biology, hormone perception, prohormone, selective agonist

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Citation

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Chicago
Vain, Thomas, Sara Raggi, Noel Ferro, Deepak Kumar Barange, Martin Kieffer, Qian Ma, Siamsa M. Doyle, et al. 2019. “Selective Auxin Agonists Induce Specific AUX/IAA Protein Degradation to Modulate Plant Development.” Proceedings of the National Academy of Sciences 116 (13): 6463–6472.
APA
Vain, T., Raggi, S., Ferro, N., Barange, D. K., Kieffer, M., Ma, Q., Doyle, S. M., et al. (2019). Selective auxin agonists induce specific AUX/IAA protein degradation to modulate plant development. Proceedings of the National Academy of Sciences, 116(13), 6463–6472.
Vancouver
1.
Vain T, Raggi S, Ferro N, Barange DK, Kieffer M, Ma Q, et al. Selective auxin agonists induce specific AUX/IAA protein degradation to modulate plant development. Proceedings of the National Academy of Sciences. Proceedings of the National Academy of Sciences; 2019;116(13):6463–72.
MLA
Vain, Thomas et al. “Selective Auxin Agonists Induce Specific AUX/IAA Protein Degradation to Modulate Plant Development.” Proceedings of the National Academy of Sciences 116.13 (2019): 6463–6472. Print.
@article{8611170,
  abstract     = {Auxin phytohormones control most aspects of plant development through a complex and interconnected signaling network. In the presence of auxin, AUXIN/INDOLE-3-ACETIC ACID (AUX/IAA) transcriptional repressors are targeted for degradation by the SKP1-CULLIN1-F-BOX (SCF) ubiquitin-protein ligases containing TRANSPORT INHIBITOR RESISTANT 1/AUXIN SIGNALING F-BOX (TIR1/AFB). CULLIN1-neddylation is required for SCFTIR1/AFB functionality, as exemplified by mutants deficient in the NEDD8-activating enzyme subunit AUXIN-RESISTANT 1 (AXR1). Here, we report a chemical biology screen that identifies small molecules requiring AXR1 to modulate plant development. We selected four molecules of interest, RubNeddin 1 to 4 (RN1 to -4), among which RN3 and RN4 trigger selective auxin responses at transcriptional, biochemical, and morphological levels. This selective activity is explained by their ability to consistently promote the interaction between TIR1 and a specific subset of AUX/IAA proteins, stimulating the degradation of particular AUX/IAA combinations. Finally, we performed a genetic screen using RN4, the RN with the greatest potential for dissecting auxin perception, which revealed that the chromatin remodeling ATPase BRAHMA is implicated in auxin-mediated apical hook development. These results demonstrate the power of selective auxin agonists to dissect auxin perception for plant developmental functions, as well as offering opportunities to discover new molecular players involved in auxin responses.},
  author       = {Vain, Thomas and Raggi, Sara and Ferro, Noel and Barange, Deepak Kumar and Kieffer, Martin and Ma, Qian and Doyle, Siamsa M. and Thelander, Mattias and Pa\v{r}{\'i}zkov{\'a}, Barbora and Nov{\'a}k, Ond\v{r}ej and Ismail, Alexandre and Enquist, Per-Anders and Rigal, Adeline and \unmatched{0141}angowska, Ma\unmatched{0142}gorzata and Ramans Harborough, Sigurd and Zhang, Yi and Ljung, Karin and Callis, Judy and Almqvist, Fredrik and Kepinski, Stefan and Estelle, Mark and Pauwels, Laurens and Robert, St{\'e}phanie},
  issn         = {0027-8424},
  journal      = {Proceedings of the National Academy of Sciences},
  number       = {13},
  pages        = {6463--6472},
  publisher    = {Proceedings of the National Academy of Sciences},
  title        = {Selective auxin agonists induce specific AUX/IAA protein degradation to modulate plant development},
  url          = {http://dx.doi.org/10.1073/pnas.1809037116},
  volume       = {116},
  year         = {2019},
}

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