Cytoplasmic Male Sterility and Fertility Restoration

Cytoplasmic male sterility (CMS), a condition under which a plant is unable to produce functional pollen, is widespread among higher plants. CMS systems represent a valuable tool in the production of hybrid seed in self-pollinating crop species, including maize, rice, cotton, and a number of vegetable crops. Hybrids often exhibit heterosis, more commonly known as hybrid vigor, whereby hybrid progeny exhibit superior growth characteristics relative to either of the parental lines. CMS systems can be of considerable value in facilitating efficient hybrid seed production. There is growing interest in improving hybrid technology both to help supply food for the world’s increasing population and to contribute to land conservation efforts. For example, the use of hybrid rice enabled China to reduce the total amount of land planted to rice from 36.5 Mha in 1975 to 30.5 Mha in 2000 while at the same time increasing total production from 128 to 189 million tons, representing a yield increase of 3.5 to 6.2 tons/ha (http://www.fao.org/ rice2004).Understanding themolecularbasis of CMS, as well as other hybrid production methods involving self-incompatibility and apomixis, is critical for continued improvements in hybrid technology. CMS is a maternally inherited trait that is often associated with unusual open reading frames (ORFs) found in mitochondrial genomes (Chase and Babay-Laughnan, 2004; Hanson and Bentolila, 2004). In many cases, it has been found that male fertility can be restored by nuclear-encoded fertility restorer (Rf) gene(s).CMS/Rfsystemstherefore are also of value in the study of interactions between nuclear and mitochondrial genomes. On the one hand, sterility results from mitochondrial genes causing cytoplasmic dysfunction, and on the other, fertility restoration relies on nuclear genes that suppress cytoplasmic dysfunction. CMS can arise spontaneously in breeding lines, as a result of wide crosses or the interspecific exchange of nuclear and cytoplasmic genomes, or following mutagenesis (Hanson and Bentolila, 2004). For example, CMS-WA (wild abortive) rice was developed in indica rice cultivars from a male-sterile plant found in a natural population of the wild rice Oryza rufipogon Griff. CMS-Boro II rice arose from a wide cross based on the cytoplasm of Chinsurah Boro II (O. sativa subsp indica) and the nucleus of Taichung 65 (subsp japonica). The well-known male-sterile Texas cytoplasm in maize arose spontaneously in a breeding line, and CMS-PET1 cytoplasm of sunflower arose from an interspecific cross between Helianthus petiolaris and H. annuus. There are a number of different types of CMS systems with distinct genetic features, both within and among different species, but key features that appear to be shared across different types are (1) CMS is associated with chimeric mitochondrial ORFs, and (2) fertility restoration is often associated with genes encoding pentatricopeptide repeat (PPR) proteins (Chase and Babay-Laughnan, 2004; Hanson and Bentolila, 2004). In this issue of The Plant Cell, Wang et al. (pages 676–687) describe details of the molecular basis of CMS and fertility restoration in the CMSBoro II system in rice, which are likely to have far-reaching implications for CMS systems in general. First, the authors show that the mitochondrial orf79 associated with CMS-Boro II encodes a cytotoxic peptide responsible for CMS, and second, they show that two PPR proteins encoded by the Rf-1 locus in the Boro II system block the production of this cytotoxic peptide by distinctmechanisms (endonucleolytic cleavage and degradation of the dicistronic mRNA). In the early 1990s, several groups reported that rice CMS-Boro II is associated with an abnormal copy of the mitochondrial gene apt6 (Kadowaki et al., 1990; Iwabuchi et al., 1993) that produces aberrant mRNA transcripts containing an additional ORF named orf79 (Akagi et al., 1994). Interestingly, in a number of well-characterized systems, CMS is associated with alterations in promoter regions and portions of coding regions of mitochondrial ATP synthase subunit genes, which raises the possibility that impaired ATP synthase activity could be a causal factor in the