Plant cytoplasmic male sterility: long-standing questions, practical issues and the evolution of restorer-of-fertility genes

Cytoplasmic male sterility (CMS) is a well-studied mitochondrion-encoded trait in plants. The recent discovery of CMS in the freshwater snail Physa acuta has broadened the known distribution of this trait and is likely to stimulate new discussions between plant and animal researchers. In this review we focus on naturally occurring CMS in beet (Beta vulgaris) to highlight key topics in plant CMS and stimulate further study. Plant CMS is associated with a hydrophobic protein that is unique to CMS mitochondria. CMS plants characteristically develop morphologically aberrant mitochondria lacking proper internal structure in tissues surrounding male gametes (the tapetum). Such mitochondrial abnormalities resemble dysfunctional mitochondria in yeast and mammal. From the perspective of mitochondrial quality control, their persistence raises the question of why they are not degraded but instead accumulate. Mathematical models suggest an increased rate of mitochondrial damage and/or reduced efficiency in degrading damaged mitochondria. The CMS phenotype varies from completely sterile to nearly male fertile. This can be explained by the action of the nuclear suppressor gene restorer-of-fertility (Rf) which may possess multiple alleles differing in strength and environmental sensitivity. Comparative analyses of Rf genes revealed molecular signatures consistent with an evolutionary arms race among different Rf types. Some researchers have even proposed that Rf evolution preceded the emergence of the corresponding CMS mitochondria.