Evolution of the basic Helix-Loop-Helix transcription factor SPATULA and its role in gynoecium development.

ALCATRAZ Amborella trichopoda Arabidopsis thaliana Nymphaea thermarum Petunia axillaris SPATULA angiosperm basic Helix-Loop-Helix carpel carpel margin meristem flower gynoecium

Journal

Annals of botany
ISSN: 1095-8290
Titre abrégé: Ann Bot
Pays: England
ID NLM: 0372347

Informations de publication

Date de publication:
26 Aug 2024
Historique:
received: 28 03 2024
medline: 26 8 2024
pubmed: 26 8 2024
entrez: 26 8 2024
Statut: aheadofprint

Résumé

SPATULA (SPT) encodes a basic Helix-Loop-Helix transcription factor in Arabidopsis thaliana that functions in the development of the style, stigma and replum tissues, all of which arise from the carpel margin meristem (CMM) of the gynoecium. Here, we use a comparative approach to investigate the evolutionary history of SPT and identify changes that potentially contributed to its role in gynoecium development. We investigate SPT's molecular and functional evolution using phylogenetic reconstruction, yeast-2-hybrid analyses of protein-protein interactions, microarray-based analyses of protein-DNA interactions, plant transformation assays, RNA in-situ hybridization, and in-silico analyses of promoter sequences. We demonstrate the SPT lineage to have arisen at the base of euphyllophytes from a clade of potentially light-regulated transcription factors through gene duplication followed by the loss of an Active Phytochrome Binding (APB) domain. We also clarify the more recent evolutionary history of SPT and its paralog ALCATRAZ (ALC), which appear to have arisen through a large-scale duplication within Brassicales. We find that SPT orthologs from diverse groups of seed plants share strikingly similar capacities for protein-protein and protein-DNA interactions, and that SPT coding regions from a wide taxonomic range of plants are able to complement loss-of-function spt mutations in transgenic Arabidopsis. However, the expression pattern of SPT appears to have evolved significantly within angiosperms, and we identify structural changes in SPT's promoter region that correlate with the acquisition of high expression levels in tissues arising from the CMM in Brassicaeae. We conclude that changes to SPT's expression pattern made a major contribution to the evolution of its developmental role in the gynoecium of Brassicaeae. By contrast, the main biochemical capacities of SPT, as well as many of its immediate transcriptional targets, appear to have been conserved at least since the base of living angiosperms.

Sections du résumé

BACKGROUND AND AIMS OBJECTIVE
SPATULA (SPT) encodes a basic Helix-Loop-Helix transcription factor in Arabidopsis thaliana that functions in the development of the style, stigma and replum tissues, all of which arise from the carpel margin meristem (CMM) of the gynoecium. Here, we use a comparative approach to investigate the evolutionary history of SPT and identify changes that potentially contributed to its role in gynoecium development.
METHODS METHODS
We investigate SPT's molecular and functional evolution using phylogenetic reconstruction, yeast-2-hybrid analyses of protein-protein interactions, microarray-based analyses of protein-DNA interactions, plant transformation assays, RNA in-situ hybridization, and in-silico analyses of promoter sequences.
KEY RESULTS RESULTS
We demonstrate the SPT lineage to have arisen at the base of euphyllophytes from a clade of potentially light-regulated transcription factors through gene duplication followed by the loss of an Active Phytochrome Binding (APB) domain. We also clarify the more recent evolutionary history of SPT and its paralog ALCATRAZ (ALC), which appear to have arisen through a large-scale duplication within Brassicales. We find that SPT orthologs from diverse groups of seed plants share strikingly similar capacities for protein-protein and protein-DNA interactions, and that SPT coding regions from a wide taxonomic range of plants are able to complement loss-of-function spt mutations in transgenic Arabidopsis. However, the expression pattern of SPT appears to have evolved significantly within angiosperms, and we identify structural changes in SPT's promoter region that correlate with the acquisition of high expression levels in tissues arising from the CMM in Brassicaeae.
CONCLUSIONS CONCLUSIONS
We conclude that changes to SPT's expression pattern made a major contribution to the evolution of its developmental role in the gynoecium of Brassicaeae. By contrast, the main biochemical capacities of SPT, as well as many of its immediate transcriptional targets, appear to have been conserved at least since the base of living angiosperms.

Identifiants

pubmed: 39183603
pii: 7741035
doi: 10.1093/aob/mcae140
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© The Author(s) 2024. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.

Auteurs

Ana C Rivarola-Sena (AC)

Laboratoire Reproduction et Développement des Plantes (CNRS UMR 5667), Ecole Normale Supérieure de Lyon, 69364 Lyon Cedex 7, France.

Aurélie C Vialette (AC)

Laboratoire Reproduction et Développement des Plantes (CNRS UMR 5667), Ecole Normale Supérieure de Lyon, 69364 Lyon Cedex 7, France.

Amélie Andres-Robin (A)

Laboratoire Reproduction et Développement des Plantes (CNRS UMR 5667), Ecole Normale Supérieure de Lyon, 69364 Lyon Cedex 7, France.

Pierre Chambrier (P)

Laboratoire Reproduction et Développement des Plantes (CNRS UMR 5667), Ecole Normale Supérieure de Lyon, 69364 Lyon Cedex 7, France.

Loïc Bideau (L)

Laboratoire Reproduction et Développement des Plantes (CNRS UMR 5667), Ecole Normale Supérieure de Lyon, 69364 Lyon Cedex 7, France.

Jose Manuel Franco-Zorrilla (JM)

Centro Nacional de Biotecnología-Consejo Superior de Investigaciones Científicas, C/Darwin3, 28049 Madrid, Spain.

Charles P Scutt (CP)

Laboratoire Reproduction et Développement des Plantes (CNRS UMR 5667), Ecole Normale Supérieure de Lyon, 69364 Lyon Cedex 7, France.

Classifications MeSH