A Reevaluation of Rice Mitochondrial Evolution Based on the Complete Sequence of Male-Fertile and Male-Sterile Mitochondrial Genomes

Bentolila, Stéphane; Стефанов, Стефан

doi:10.1104/pp.111.190231

Cited by 74 publications

(64 citation statements)

References 53 publications

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“…In plants, the large mitochondrial genomes contain more genes and putative ORFs; many of them are of unknown function. For example, in the mitochondrial genomes of O. rufipogon and O. sativa, besides the known functional genes, there are 32 and 21 putative genes (ORFs) of unknown function, respectively [21,27]. This study demonstrates that during the new gene origination process in the mitochondrial genomes, other non-CMS genes, together with the CMS genes, could also be generated.…”

Section: Discussionmentioning

confidence: 85%

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

Tang

Zheng

et al. 2016

Cell Res

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New gene origination is a major source of genomic innovations that confer phenotypic changes and biological diversity. Generation of new mitochondrial genes in plants may cause cytoplasmic male sterility (CMS), which can promote outcrossing and increase fitness. However, how mitochondrial genes originate and evolve in structure and function remains unclear. The rice Wild Abortive type of CMS is conferred by the mitochondrial gene WA352c (previously named WA352) and has been widely exploited in hybrid rice breeding. Here, we reconstruct the evolutionary trajectory of WA352c by the identification and analyses of 11 mitochondrial genomic recombinant structures related to WA352c in wild and cultivated rice. We deduce that these structures arose through multiple rearrangements among conserved mitochondrial sequences in the mitochondrial genome of the wild rice Oryza rufipogon, coupled with substoichiometric shifting and sequence variation. We identify two expressed but nonfunctional protogenes among these structures, and show that they could evolve into functional CMS genes via sequence variations that could relieve the self-inhibitory potential of the proteins. These sequence changes would endow the proteins the ability to interact with the nucleus-encoded mitochondrial protein COX11, resulting in premature programmed cell death in the anther tapetum and male sterility. Furthermore, we show that the sequences that encode the COX11-interaction domains in these WA352c-related genes have experienced purifying selection during evolution. We propose a model for the formation and evolution of new CMS genes via a "multi-recombination/protogene formation/functionalization" mechanism involving gradual variations in the structure, sequence, copy number, and function.

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Section: Discussionmentioning

confidence: 85%

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

Tang

Zheng

et al. 2016

Cell Res

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“…Quantitative RT-PCR was performed as described in ref. 69. All of the primers used for quantitative RT-PCR are given in SI Appendix, Table S3.…”

Section: Methodsmentioning

confidence: 99%

RIP1, a member of an Arabidopsis protein family, interacts with the protein RARE1 and broadly affects RNA editing

Bentolila¹,

Heller²,

Sun³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

214

266

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Transcripts of plant organelle genes are modified by cytidine-touridine (C-to-U) RNA editing, often changing the encoded amino acid predicted from the DNA sequence. Members of the PLS subclass of the pentatricopeptide repeat (PPR) motif-containing family are site-specific recognition factors for either chloroplast or mitochondrial C targets of editing. However, other than PPR proteins and the cis-elements on the organelle transcripts, no other components of the editing machinery in either organelle have previously been identified. The Arabidopsis chloroplast PPR protein Required for AccD RNA Editing 1 (RARE1) specifies editing of a C in the accD transcript. RARE1 was detected in a complex of >200 kDa. We immunoprecipitated epitope-tagged RARE1, and tandem MS/MS analysis identified a protein of unknown function lacking PPR motifs; we named it RNA-editing factor interacting protein 1 (RIP1). Yeast two-hybrid analysis confirmed RIP1 interaction with RARE1, and RIP1-GFP fusions were found in both chloroplasts and mitochondria. Editing assays for all 34 known Arabidopsis chloroplast targets in a rip1 mutant revealed altered efficiency of 14 editing events. In mitochondria, 266 editing events were found to have reduced efficiency, with major loss of editing at 108 C targets. Virusinduced gene silencing of RIP1 confirmed the altered editing efficiency. Transient introduction of a WT RIP1 allele into rip1 improved the defective RNA editing. The presence of RIP1 in a protein complex along with chloroplast editing factor RARE1 indicates that RIP1 is an important component of the RNA editing apparatus that acts on many chloroplast and mitochondrial C targets.nucleoid | RNA editosome | dual targeting P osttranscriptional C-to-U RNA editing occurs in plastid and plant mitochondrial transcripts. In a typical vascular plant, ∼30 C targets in chloroplasts and over 500 C targets in mitochondria are targeted for editing (1, 2). The majority of the editing events results in encoding of a different amino acid than the one predicted from the genomic sequence. The editing-encoded amino acid is usually more conserved relative to residues present in homologous proteins in other organisms than the genomically encoded amino acid. Because there is presently no known case in which useful genetic variation results from partial editing of a transcript population, the current concept is that editing is a correction mechanism for thymidine-to-cytidine (T-to-C) mutations that have arisen in plant organelle genomes (1,3,4).Little is known about the molecular apparatus that is responsible for recognizing the correct C target for editing and converting it to U, although plant mitochondrial RNA editing was discovered over 20 y ago (5-7). cis-Elements for recognition of editing sites have been identified proximal and 5′ to the nucleotide to be modified (8-10). As few as 22 nt in sequence surrounding the C target is sufficient to specify RNA editing (9). In 2005, a pentatricopeptide repeat (PPR) motif-containing protein termed CRR4 was discovered to ...

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“…(e.g. in rice; Bentolila & Stefanov 2012;Fujii, Kazama, Yamada, & Toriyama, 2010). This strategy has been validated in maize where the CMS genes were detected in CMS-T and CMS-S (Allen et al, 2007).…”

Section: Genome Evolution and Gynodioecymentioning

confidence: 99%

Mitochondrial Genome Evolution and Gynodioecy

Touzet¹

2012

Advances in Botanical Research

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A Reevaluation of Rice Mitochondrial Evolution Based on the Complete Sequence of Male-Fertile and Male-Sterile Mitochondrial Genomes

Cited by 74 publications

References 53 publications

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

RIP1, a member of an Arabidopsis protein family, interacts with the protein RARE1 and broadly affects RNA editing

Mitochondrial Genome Evolution and Gynodioecy

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