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

PLoS One. 2024 Sep 27;19(9):e0308551. doi: 10.1371/journal.pone.0308551. eCollection 2024.

Abstract

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.

MeSH terms

  • Beta vulgaris* / genetics
  • DNA, Mitochondrial / genetics
  • Genes, Mitochondrial
  • Genes, Plant
  • Genome, Mitochondrial
  • Mitochondria / genetics
  • Phylogeny*
  • Plant Infertility* / genetics
  • Polymorphism, Single Nucleotide

Substances

  • DNA, Mitochondrial

Grants and funding

This study was financially supported by the Japan Society for the Promotion of Science, Grant-in-Aid for Scientific Research, in the form of grants (21H02159 and 24K01726) received by HM, KK, and TK. This study was also financially supported by the Japan Society for the Promotion of Science, Grant-in-Aid for Scientific Research, in the form of a grant (22K05569) received by HM and KK. This study was also financially supported by the Japan Society for the Promotion of Science, Grant-in-Aid for Scientific Research, in the form of a grant (JP22H04925 (PAGS)) received by AT, HT, KK, and TK. This study was also financially supported by the Japan Society for the Promotion of Science, Grant-in-Aid for Scientific Research, in the form of a grant (22H02267) received by YK, KK, and TK. No additional external funding was received for this study. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.