Mitochondrial phylogeny and distribution of cytoplasmic male sterility-associated genes in Beta vulgaris

• Published in: PloS one 2024-09, Vol.19 (9), p.e0308551
• Main Authors: Kubota, Keishi, Oishi, Mion, Taniguchi, Eigo, Akazawa, Akiho, Matsui, Katsunori, Kitazaki, Kazuyoshi, Toyoda, Atsushi, Toh, Hidehiro, Matsuhira, Hiroaki, Kuroda, Yosuke, Kubo, Tomohiko
• Format: Article
• Language: English
• Subjects: Analysis; Beets; Beta vulgaris; Beta vulgaris - genetics; Cluster analysis; Clustering; Cultivation; Cytochrome; Cytoplasmic male sterility; DNA, Mitochondrial - genetics; Gene frequency; Gene sequencing; Genes; Genes, Mitochondrial; Genes, Plant; Genetic aspects; Genome, Mitochondrial; Genomes; Genomics; Geographical distribution; Growth; Male sterility; Males; Mitochondria; Mitochondria - genetics; Mitochondrial DNA; Nucleotides; Phylogeny; Physiological aspects; Plant Infertility - genetics; Plants (botany); Polymorphism; Polymorphism, Single Nucleotide; Polypeptides; Principal components analysis; Single nucleotide polymorphisms; Software; Sugar beets
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0308551

Cytoplasmic male sterility (CMS) is a mitochondrial-encoded trait that confers reproductive defects in males but not in females or any vegetative function. Why CMS is so often found in plants should be investigated from the viewpoint of mitochondrial phylogeny. Beta vulgaris, including the wild subspecies maritima and cultivated subspecies vulgaris (e.g., sugar beet), is known to be mitochondrially polymorphic, from which multiple CMS mitochondria have been found, but their evolutionary relationship has been obscure. We first refined the B. vulgaris reference mitochondrial genome to conduct a more accurate phylogenetic study. We identified mitochondrial single-nucleotide polymorphic sites from 600 B. vulgaris accessions. Principal component analysis, hierarchical clustering analysis, and creation of a phylogenetic tree consistently suggested that B. vulgaris mitochondria can be classified into several groups whose geographical distribution tends to be biased toward either the Atlantic or Mediterranean coasts. We examined the distribution of CMS-associated mitochondrial genes from Owen, E- and G-type CMS mitochondria. About one-third of cultivated beets had Owen-type CMS, which reflects the prevalence of using Owen-type CMS in hybrid breeding. Occurrence frequencies for each of the three CMS genes in wild beet were less than 4%. CMS genes were tightly associated with specific mitochondrial groups that are phylogenetically distinct, suggesting their independent origin. However, homologous sequences of the Owen type CMS gene occurred in several different mitochondrial groups, for which an intricate explanation is necessary. Whereas the origin of cultivated beet had been presumed to be Greece, we found an absence of Owen-type mitochondria in Greek accessions.