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Multicentric origin and diversification of atp6-orf79-like structures reveal mitochondrial gene flows in Oryza rufipogon and Oryza sativa.

ABSTRACT: Cytoplasmic male sterility (CMS) is a widely used genetic tool in modern hybrid rice breeding. Most genes conferring rice gametophytic CMS are homologous to orf79 and co-transcribe with atp6. However, the origin, differentiation and flow of these mitochondrial genes in wild and cultivated rice species remain unclear. In this study, we performed de novo assembly of the mitochondrial genomes of 221 common wild rice (Oryza rufipogon Griff.) and 369 Asian cultivated rice (Oryza sativa L.) accessions, and identified 16 haplotypes of atp6-orf79-like structures and 11 orf79 alleles. These homologous structures were classified into 4 distinct groups (AO-I, AO-II, AO-III and AO-IV), all of which were observed in O. rufipogon but only AO-I was detected in O. sativa, causing a decrease in the frequency of atp6-orf79-like structures from 19.9% to 8.1%. Phylogenetic and biogeographic analyses revealed that the different groups of these gametophytic CMS-related genes in O. rufipogon evolved in a multicentric pattern. The geographical origin of the atp6-orf79-like structures was further traced back, and a candidate region in north-east of Gangetic Plain on the Indian Peninsula (South Asia) was identified as the origin centre of AO-I. The orf79 alleles were detected in all three cytoplasmic types (Or-CT0, Or-CT1 and Or-CT2) of O. rufipogon, but only two alleles (orf79a and orf79b) were observed in Or-CT0 type of O. sativa, while no orf79 allele was found in other types of O. sativa. Our results also revealed that the orf79 alleles in cultivated rice originated from the wild rice population in South and South-East Asia. In addition, strong positive selection pressure was detected on the sequence variations of orf79 alleles, and a special evolutionary strategy was noted in these gametophytic CMS-related genes, suggesting that their divergence could be beneficial to their survival in evolution.

SUBMITTER: He W

PROVIDER: S-EPMC7513716 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe cytoplasmic male sterility (CMS) of rice is caused by chimeric mitochondrial DNA (mtDNA) that is maternally inherited in the majority of multicellular organisms. Wild rice (Oryza rufipogon Griff.) has been regarded as the ancestral progenitor of Asian cultivated rice (Oryza sativa L.). To investigate the distribution of original CMS source, and explore the origin of gametophytic CMS gene, a total of 427 individuals with seventeen representative populations of O. rufipogon were collected in from Dongxiang of Jiangxi Province to Sanya of Hainan Province, China, for the PCR amplification of atp6, orfH79 and B-atp6-orfH79, respectively.ResultsThe B-atp6-orfH79 and its variants (B-atp6-GSV) were detected in five among seventeen populations (i.e. HK, GZ, PS, TL and YJ) through PCR amplification, which could be divided into three haplotypes, i.e., BH1, BH2, and BH3. The BH2 haplotype was identical to B-atp6-orfH79, while the BH1 and BH3 were the novel haplotypes of B-atp6-GSV. Combined with the high-homology sequences in GenBank, a total of eighteen haplotypes have been revealed, only with ten haplotypes in orfH79 and its variants (GSV) that belong to three species (i.e. O. rufipogon, Oryza nivara and Oryza sativa). Enough haplotypes clearly demonstrated the uniform structural characteristics of the B-atp6-orfH79 as follows: except for the conserved sequence (671 bp) composed of B-atp6 (619 bp) and the downstream followed the B-atp6 (52 bp, DS), and GSV sequence, a rich variable sequence (VS, 176 bp) lies between the DS and GSV with five insertion or deletion and more than 30 single nucleotide polymorphism. Maximum likelihood analysis showed that eighteen haplotypes formed three clades with high support rate. The hierarchical analysis of molecular variance (AMOVA) indicated the occurrence of variation among all populations (FST = 1; P < 0.001), which implied that the chimeric structure occurred independently. Three haplotypes (i.e., H1, H2 and H3) were detected by the primer of orfH79, which were identical to the GVS in B-atp6-GVS structure, respectively. All seventeen haplotypes of the orfH79, belonged to six species based on our results and the existing references. Seven existed single nucleotide polymorphism in GSV section can be translated into eleven various amino acid sequences.ConclusionsGenerally, this study, indicating that orfH79 was always accompanied by the B-atp6, not only provide two original CMS sources for rice breeding, but also confirm the uniform structure of B-atp-orfH79, which contribute to revealing the origin of rice gametophytic CMS genes, and the reason about frequent recombination of mitochondrial DNA.

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Multicentric origin and diversification of atp6-orf79-like structures reveal mitochondrial gene flows in Oryza rufipogon and Oryza sativa.

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