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Neofunctionalization of Mitochondrial Proteins and Incorporation into Signaling Networks in Plants

Lama, Sbatie LU ; Broda, Martyna; Abbas, Zahra; Vaneechoutte, Dries; Belt, Katharina; Säll, Torbjörn LU ; Vandepoele, Klaas and Van Aken, Olivier LU (2019) In Molecular biology and evolution 36(5). p.974-989
Abstract

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... (More)

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.

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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
evolution, mitochondria, neofunctionalization, retrograde signaling, stress
in
Molecular biology and evolution
volume
36
issue
5
pages
16 pages
publisher
Oxford University Press
external identifiers
  • scopus:85065679721
ISSN
0737-4038
DOI
10.1093/molbev/msz031
language
English
LU publication?
yes
id
23cc3875-2aa6-4b5b-8ef2-7f5f8ef9a5ff
date added to LUP
2019-05-28 12:00:11
date last changed
2019-06-19 04:14:02
@article{23cc3875-2aa6-4b5b-8ef2-7f5f8ef9a5ff,
  abstract     = {<p>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.</p>},
  author       = {Lama, Sbatie and Broda, Martyna and Abbas, Zahra and Vaneechoutte, Dries and Belt, Katharina and Säll, Torbjörn and Vandepoele, Klaas and Van Aken, Olivier},
  issn         = {0737-4038},
  keyword      = {evolution,mitochondria,neofunctionalization,retrograde signaling,stress},
  language     = {eng},
  number       = {5},
  pages        = {974--989},
  publisher    = {Oxford University Press},
  series       = {Molecular biology and evolution},
  title        = {Neofunctionalization of Mitochondrial Proteins and Incorporation into Signaling Networks in Plants},
  url          = {http://dx.doi.org/10.1093/molbev/msz031},
  volume       = {36},
  year         = {2019},
}