Neofunctionalization of Mitochondrial Proteins and Incorporation into Signaling Networks in Plants.


Journal

Molecular biology and evolution
ISSN: 1537-1719
Titre abrégé: Mol Biol Evol
Pays: United States
ID NLM: 8501455

Informations de publication

Date de publication:
01 05 2019
Historique:
pubmed: 3 4 2019
medline: 2 7 2019
entrez: 3 4 2019
Statut: ppublish

Résumé

Because of their symbiotic origin, many mitochondrial proteins are well conserved across eukaryotic kingdoms. It is however less obvious how specific lineages have obtained novel nuclear-encoded mitochondrial proteins. Here, we report a case of mitochondrial neofunctionalization in plants. Phylogenetic analysis of genes containing the Domain of Unknown Function 295 (DUF295) revealed that the domain likely originated in Angiosperms. The C-terminal DUF295 domain is usually accompanied by an N-terminal F-box domain, involved in ubiquitin ligation via binding with ASK1/SKP1-type proteins. Due to gene duplication, the gene family has expanded rapidly, with 94 DUF295-related genes in Arabidopsis thaliana alone. Two DUF295 family subgroups have uniquely evolved and quickly expanded within Brassicaceae. One of these subgroups has completely lost the F-box, but instead obtained strongly predicted mitochondrial targeting peptides. We show that several representatives of this DUF295 Organellar group are effectively targeted to plant mitochondria and chloroplasts. Furthermore, many DUF295 Organellar genes are induced by mitochondrial dysfunction, whereas F-Box DUF295 genes are not. In agreement, several Brassicaceae-specific DUF295 Organellar genes were incorporated in the evolutionary much older ANAC017-dependent mitochondrial retrograde signaling pathway. Finally, a representative set of DUF295 T-DNA insertion mutants was created. No obvious aberrant phenotypes during normal growth and mitochondrial dysfunction were observed, most likely due to the large extent of gene duplication and redundancy. Overall, this study provides insight into how novel mitochondrial proteins can be created via "intercompartmental" gene duplication events. Moreover, our analysis shows that these newly evolved genes can then be specifically integrated into relevant, pre-existing coexpression networks.

Identifiants

pubmed: 30938771
pii: 5342043
doi: 10.1093/molbev/msz031
pmc: PMC6501883
doi:

Substances chimiques

DNA, Bacterial 0
F-Box Proteins 0
Mitochondrial Proteins 0
Plant Proteins 0
T-DNA 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

974-989

Informations de copyright

© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

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Auteurs

Sbatie Lama (S)

Department of Biology, Lund University, Lund, Sweden.

Martyna Broda (M)

ARC Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Australia.

Zahra Abbas (Z)

ARC Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Australia.

Dries Vaneechoutte (D)

Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium.
VIB Center for Plant Systems Biology, Ghent, Belgium.

Katharina Belt (K)

ARC Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Australia.
CSIRO, Floreat, WA, Australia.

Torbjörn Säll (T)

Department of Biology, Lund University, Lund, Sweden.

Klaas Vandepoele (K)

Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium.
VIB Center for Plant Systems Biology, Ghent, Belgium.

Olivier Van Aken (O)

Department of Biology, Lund University, Lund, Sweden.

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Classifications MeSH