Functional analysis of regA paralog rlsD in Volvox carteri.

RNA‐seq Volvox carteri cell differentiation evolution regA resource limitation transcription factor

Journal

The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397

Informations de publication

Date de publication:
22 Oct 2024
Historique:
revised: 14 08 2024
received: 15 09 2023
accepted: 28 09 2024
medline: 22 10 2024
pubmed: 22 10 2024
entrez: 22 10 2024
Statut: aheadofprint

Résumé

Volvox carteri is an excellent system for investigating the origins of cell differentiation because it possesses just two cell types, reproductive gonidia and motile somatic cells, which evolved relatively recently. The somatic phenotype depends on the regA gene, which represses cell growth and reproduction, preventing cells expressing it from growing large enough to become gonidia. regA encodes a putative transcription factor and was generated in an undifferentiated ancestor of V. carteri through duplication of a progenitor gene whose ortholog in V. carteri is named rlsD. Here we analyze the function of rlsD through knockdown, overexpression, and RNA-seq experiments, to gain clues into the function of a member of an understudied putative transcription factor family and to obtain insight into the origins of cell differentiation in the volvocine algae. rlsD knockdown was lethal, while rlsD overexpression dramatically reduced gonidial growth. rlsD overexpression led to differential expression of approximately one-fourth of the genome, with repressed genes biased for those typically overexpressed in gonidia relative to somatic cells, and upregulated genes biased toward expression in soma, where regA expression is high. Notably, rlsD overexpression affects accumulation of transcripts for genes/Pfam domains involved in ribosome biogenesis, photosynthetic light harvesting, and sulfate generation, functions related to organismal growth, and responses to resource availability. We also found that in the wild type, rlsD expression is induced by light deprivation. These findings are consistent with the idea that cell differentiation in V. carteri evolved when a resource-responsive, growth-regulating gene was amplified, and a resulting gene duplicate was co-opted to repress growth in a constitutive, spatial context.

Identifiants

pubmed: 39436924
doi: 10.1111/tpj.17081
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National Science Foundation
ID : NSF-EFRI 1332344
Organisme : National Science Foundation
ID : NSF-MCB 1715894
Organisme : NIH HHS
ID : NIH P20 GM103418
Pays : United States

Informations de copyright

© 2024 Society for Experimental Biology and John Wiley & Sons Ltd.

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Auteurs

Berenice Jiménez-Marín (B)

Division of Biology, Kansas State University, 239E Chalmers Hall, Manhattan, 66506, Kansas, USA.

José A Ortega-Escalante (JA)

Department of Biological Sciences, UMBC, 1000 Hilltop Circle, Baltimore, 21250, Maryland, USA.

Antariksh Tyagi (A)

Division of Biology, Kansas State University, 239E Chalmers Hall, Manhattan, 66506, Kansas, USA.

Jundhi Seah (J)

Department of Biological Sciences, UMBC, 1000 Hilltop Circle, Baltimore, 21250, Maryland, USA.

Bradley J S C Olson (BJSC)

Division of Biology, Kansas State University, 239E Chalmers Hall, Manhattan, 66506, Kansas, USA.

Stephen M Miller (SM)

Department of Biological Sciences, UMBC, 1000 Hilltop Circle, Baltimore, 21250, Maryland, USA.

Classifications MeSH