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Selective auxin agonists induce specific AUX/IAA protein degradation to modulate plant development
Umeå University, Faculty of Science and Technology, Department of Chemistry. Chemical Biology Umeå, Chemical Biology Consortium Sweden.
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2019 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 116, no 13, p. 6463-6472Article in journal (Refereed) Published
Abstract [en]

The plant hormone auxin coordinates almost all aspects of plant development. Throughout plant life, the expression of hundreds of genes involved in auxin regulation is orchestrated via several combinatorial and cell-specific auxin perception systems. An effective approach to dissect these complex pathways is the use of synthetic molecules that target specific processes of auxin activity. Here, we describe synthetic auxins, RubNeddins (RNs), which act as selective auxin agonists. The RN with the greatest potential for dissecting auxin perception was RN4, which we used to reveal a role for the chromatin remodeling ATPase BRAHMA in apical hook development. Therefore, the understanding of RN mode of action paves the way to dissecting specific molecular components involved in auxin-regulated developmental processes.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.

Place, publisher, year, edition, pages
Washington: Proceedings of the National Academy of Sciences of the United States of America (PNAS) , 2019. Vol. 116, no 13, p. 6463-6472
Keywords [en]
auxin, chemical biology, selective agonist, prohormone, hormone perception
National Category
Biochemistry and Molecular Biology
Identifiers
URN: urn:nbn:se:umu:diva-157293DOI: 10.1073/pnas.1809037116ISI: 000462382800094PubMedID: 30850516OAI: oai:DiVA.org:umu-157293DiVA, id: diva2:1296170
Funder
Swedish Research Council, 2013-4632Swedish Research Council, 2016-00768VinnovaKnut and Alice Wallenberg FoundationStiftelsen Olle Engkvist ByggmästareThe Kempe FoundationsCarl Tryggers foundation NIH (National Institute of Health), NIH GM43644Available from: 2019-03-14 Created: 2019-03-14 Last updated: 2019-04-12Bibliographically approved

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Barange, Deepak KumarEnquist, Per-AndersAlmqvist, Fredrik

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