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Neofunctionalization of mitochondrial proteins and incorporation into signaling networks in plants

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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 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.
Keywords
mitochondria, evolution, retrograde signaling, stress, neofunctionalization, GENES-ENCODING MITOCHONDRIAL, NAC TRANSCRIPTION FACTOR, RETROGRADE REGULATION, ARABIDOPSIS-THALIANA, LIGASE COMPLEX, ORIGIN, EVOLUTIONARY, GENOME, SUBUNITS, RECEPTOR

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  • Supplemental Table II. DUF295 mito RNAseq+DAP-seq+knn300.xlsx
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  • Supplemental Table III. DUF295 RNAseq counts.xlsx
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  • Supplemental Table IV. DUF295 HIMs vs transcripts.xlsx
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  • Supplemental Table V. Phylostratic coexpression.xls
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  • Supplemental Table I. AT4G25920 Y2H interaction partners 2.xlsx
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Citation

Please use this url to cite or link to this publication:

MLA
Lama, Sbatie, et al. “Neofunctionalization of Mitochondrial Proteins and Incorporation into Signaling Networks in Plants.” MOLECULAR BIOLOGY AND EVOLUTION, vol. 36, no. 5, 2019, pp. 974–89.
APA
Lama, S., Broda, M., Abbas, Z., Vaneechoutte, D., Belt, K., Säll, T., … Van Aken, O. (2019). Neofunctionalization of mitochondrial proteins and incorporation into signaling networks in plants. MOLECULAR BIOLOGY AND EVOLUTION, 36(5), 974–989.
Chicago author-date
Lama, Sbatie, Martyna Broda, Zahra Abbas, Dries Vaneechoutte, Katharina Belt, Torbjörn Säll, Klaas Vandepoele, and Olivier Van Aken. 2019. “Neofunctionalization of Mitochondrial Proteins and Incorporation into Signaling Networks in Plants.” MOLECULAR BIOLOGY AND EVOLUTION 36 (5): 974–89.
Chicago author-date (all authors)
Lama, Sbatie, Martyna Broda, Zahra Abbas, Dries Vaneechoutte, Katharina Belt, Torbjörn Säll, Klaas Vandepoele, and Olivier Van Aken. 2019. “Neofunctionalization of Mitochondrial Proteins and Incorporation into Signaling Networks in Plants.” MOLECULAR BIOLOGY AND EVOLUTION 36 (5): 974–989.
Vancouver
1.
Lama S, Broda M, Abbas Z, Vaneechoutte D, Belt K, Säll T, et al. Neofunctionalization of mitochondrial proteins and incorporation into signaling networks in plants. MOLECULAR BIOLOGY AND EVOLUTION. 2019;36(5):974–89.
IEEE
[1]
S. Lama et al., “Neofunctionalization of mitochondrial proteins and incorporation into signaling networks in plants,” MOLECULAR BIOLOGY AND EVOLUTION, vol. 36, no. 5, pp. 974–989, 2019.
@article{8611458,
  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 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.},
  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},
  journal      = {MOLECULAR BIOLOGY AND EVOLUTION},
  keywords     = {mitochondria,evolution,retrograde signaling,stress,neofunctionalization,GENES-ENCODING MITOCHONDRIAL,NAC TRANSCRIPTION FACTOR,RETROGRADE REGULATION,ARABIDOPSIS-THALIANA,LIGASE COMPLEX,ORIGIN,EVOLUTIONARY,GENOME,SUBUNITS,RECEPTOR},
  language     = {eng},
  number       = {5},
  pages        = {974--989},
  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},
}

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