Neofunctionalization of Mitochondrial Proteins and Incorporation into Signaling Networks in Plants

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.

Joint inhibition of mitochondrial complex IV and alternative oxidase by genetic or chemical means represses chloroplast transcription in Arabidopsis

“…Strikingly, many defencerelated genes were highly induced, including pathogenesisrelated PR1, PR4, PDF1.2b and phytoalexin deficient PAD3. Also, many known target genes of ANAC017, including AOX1a, UGT74E2, At2g04050 and At2g41730 were highly induced, indicating that the mitochondrial retrograde signalling via ANAC017 was activated in the rps10 mutant [9,10,40]. A gene ontology analysis confirmed that among the up-regulated genes common to P2 and P3, those related to pathogen response, stress response, abscisic acid signalling and glucosinolate biosynthesis were overrepresented (electronic supplementary material, table S5).…”

Retrograde signals from mitochondria reprogramme skoto-morphogenesis in Arabidopsis thaliana via alternative oxidase 1a

“…These data emphasize the strong similarity in the gene-expression profiles of rpoTmp plants that differ for developmental stages and growth conditions. Remarkably, among the common up DEGs, 20 genes encode mitochondrial localized proteins and at least nine genes are induced by mitochondrial dysfunction and transcriptionally regulated by mitochondrial retrograde signaling, as AT12CYS2 [11], NDB4 [11], five different DUF 295 organellar genes [35] and UPOX that is an hallmark of oxidative stress [37]. All these data pointed to the presence of a strong mitochondrial stress in rpoTmp plants and prompted us to explore the possibility that defects in mitochondrial respiration are at the origin of the observed skoto-morphogenetic alteration.…”

Regulation of Three Key Kinases of Brassinosteroid Signaling Pathway

“…In addition to its role in BIN2 degradation, the Kelch repeat-mediated KIB1-BIN2 interaction blocked the BIN2-BZR1 binding, thus further reducing the BIN2 phosphorylation activity [ 28 ]. It remains to be determined whether proteasome-mediated degradation is an evolutionally conserved mechanism in other plant species to regulate the phosphorylation activity of BIN2 homologs given a recent discovery of restricted distribution of KIB1 and its homologs in the Brassicaceae family and their extremely low expression in vegetative tissues [ 210 ]. It is interesting to note that the proteasome-mediated GSK3 degradation was previously shown to be induced by glucocorticoid in mammalian cells although the identity of a GSK3-interacting E3 ubiquitin ligase remains unknown [ 211 ].…”