Evolution of the Auxin Response Factors from charophyte ancestors.

Auxin is a major developmental regulator in plants and the acquisition of a transcriptional response to auxin likely contributed to developmental innovations at the time of water-to-land transition. Auxin Response Factors (ARFs) Transcription Factors (TFs) that mediate auxin-dependent transcriptiona...

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Main Authors: Raquel Martin-Arevalillo, Emmanuel Thévenon, Fanny Jégu, Thomas Vinos-Poyo, Teva Vernoux, François Parcy, Renaud Dumas
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-09-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1008400
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author Raquel Martin-Arevalillo
Emmanuel Thévenon
Fanny Jégu
Thomas Vinos-Poyo
Teva Vernoux
François Parcy
Renaud Dumas
author_facet Raquel Martin-Arevalillo
Emmanuel Thévenon
Fanny Jégu
Thomas Vinos-Poyo
Teva Vernoux
François Parcy
Renaud Dumas
author_sort Raquel Martin-Arevalillo
collection DOAJ
description Auxin is a major developmental regulator in plants and the acquisition of a transcriptional response to auxin likely contributed to developmental innovations at the time of water-to-land transition. Auxin Response Factors (ARFs) Transcription Factors (TFs) that mediate auxin-dependent transcriptional changes are divided into A, B and C evolutive classes in land plants. The origin and nature of the first ARF proteins in algae is still debated. Here, we identify the most 'ancient' ARF homologue to date in the early divergent charophyte algae Chlorokybus atmophyticus, CaARF. Structural modelling combined with biochemical studies showed that CaARF already shares many features with modern ARFs: it is capable of oligomerization, interacts with the TOPLESS co-repressor and specifically binds Auxin Response Elements as dimer. In addition, CaARF possesses a DNA-binding specificity that differs from class A and B ARFs and that was maintained in class C ARF along plants evolution. Phylogenetic evidence together with CaARF biochemical properties indicate that the different classes of ARFs likely arose from an ancestral proto-ARF protein with class C-like features. The foundation of auxin signalling would have thus happened from a pre-existing hormone-independent transcriptional regulation together with the emergence of a functional hormone perception complex.
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spelling doaj.art-4c1c6e81e1ae40da9bdbf1d0466dd5352022-12-21T22:36:24ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042019-09-01159e100840010.1371/journal.pgen.1008400Evolution of the Auxin Response Factors from charophyte ancestors.Raquel Martin-ArevalilloEmmanuel ThévenonFanny JéguThomas Vinos-PoyoTeva VernouxFrançois ParcyRenaud DumasAuxin is a major developmental regulator in plants and the acquisition of a transcriptional response to auxin likely contributed to developmental innovations at the time of water-to-land transition. Auxin Response Factors (ARFs) Transcription Factors (TFs) that mediate auxin-dependent transcriptional changes are divided into A, B and C evolutive classes in land plants. The origin and nature of the first ARF proteins in algae is still debated. Here, we identify the most 'ancient' ARF homologue to date in the early divergent charophyte algae Chlorokybus atmophyticus, CaARF. Structural modelling combined with biochemical studies showed that CaARF already shares many features with modern ARFs: it is capable of oligomerization, interacts with the TOPLESS co-repressor and specifically binds Auxin Response Elements as dimer. In addition, CaARF possesses a DNA-binding specificity that differs from class A and B ARFs and that was maintained in class C ARF along plants evolution. Phylogenetic evidence together with CaARF biochemical properties indicate that the different classes of ARFs likely arose from an ancestral proto-ARF protein with class C-like features. The foundation of auxin signalling would have thus happened from a pre-existing hormone-independent transcriptional regulation together with the emergence of a functional hormone perception complex.https://doi.org/10.1371/journal.pgen.1008400
spellingShingle Raquel Martin-Arevalillo
Emmanuel Thévenon
Fanny Jégu
Thomas Vinos-Poyo
Teva Vernoux
François Parcy
Renaud Dumas
Evolution of the Auxin Response Factors from charophyte ancestors.
PLoS Genetics
title Evolution of the Auxin Response Factors from charophyte ancestors.
title_full Evolution of the Auxin Response Factors from charophyte ancestors.
title_fullStr Evolution of the Auxin Response Factors from charophyte ancestors.
title_full_unstemmed Evolution of the Auxin Response Factors from charophyte ancestors.
title_short Evolution of the Auxin Response Factors from charophyte ancestors.
title_sort evolution of the auxin response factors from charophyte ancestors
url https://doi.org/10.1371/journal.pgen.1008400
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