Cytoplasmic male sterility

Occasionally, abnormal recombination events occur in plant mitochondrial DNA, and such events can sometimes result in the formation of novel protein coding sequences called open reading frames or ORFs. The expression of such ORFs can, in turn, result in the phenotype of male sterility, the inability of the plant to produce functional male gametes (pollen). Such cytoplasmic (for its mode of inheritance) male sterility, or CMS, is a very widespread trait in higher plants. Often, the trait is masked by the presence of nuclear genes termed restorers of fertility, or Rf genes that suppress the male sterility by reducing expression of the CMS-associated ORF. For this reason, CMS can often only be revealed through wide intraspecific or interspecific crosses. In other cases, the trait is revealed in nature via gynodioecy, a term used to refer to populations consisting of a mixture of female (i.e. male sterile) and hermaphroditic plants.

Normally, one would expect that the male sterility trait would be evolutionarily disadvantageous. Why then, is this trait encountered so frequently in flowering plants? Population biologists seeking an explanation for this phenomenon have proposed that a maternally inherited gene conferring male sterility can spread in a population provided adequate pollen is available from neighboring plants. Such populations would be gynodioecious. The continued spread of the male-sterile gene, however, would eventually limit the pollen available to the population, and create the selective pressure for the appearance of a restorer of fertility gene that would suppress the maternally inherited male sterility and restore pollen production. If the restorer gene spread to fixation in the population (i.e. it would be present in all individuals), the population would consist entirely of hermaphroditic individuals, even though many, perhaps all of these would contain a potentially male sterility causing mitochondrial gene. The repeated appearance of mitochondrial genes capable of causing male sterility, and the corresponding evolution of new nuclear restorer genes can be viewed as an “intragenomic arms race”: a cytoplasmic genetic element spreading at the expense of nuclear gene transmission, and the corresponding response of the nucleus with the evolution of a new restorer gene.

Diagram illustrating the population dynamics of cytoplasmic male sterility and nuclear fertility restoration as an intragenomic evolutionary arms race.

For more than 20 years, my laboratory has been studying the molecular and developmental biology of cytoplasmic male sterility as it occurs in Brassica napus, the plant species that is grown as canola, Canada’s major oilseed crop. We have identified the mitochondrial genes that specify the two different types of CMS native to this species (1, 2), and shown that these are highly similar in structure, suggesting a relatively recent evolutionary origin. In addition, we have mapped the restorer genes for these two types and shown that they appear to be alleles or haplotypes of a single nuclear locus (3, 4) again suggesting a recent evolutionary origin. These findings indicate that B. napus represents an ideal model for understanding the molecular features underlying the evolutionary dynamics of CMS-restorer gene co-evolution. We have, in addition, isolated and characterized the nuclear restorer gene termed Rfo (5), which specifically suppresses a form of CMS termed Ogura, that has been introduced from the related species, the radish Raphanus sativus.

Flowers of cytoplasmic male sterile (CMS, left) and male fertile Brassica napus plants. The CMS plant has small anthers which shed no pollen in comparison with the normal sized anthers in the male fertile plant.

Selected references from my laboratory, as cited above:
1. Singh, M. and Brown G.G. (1991). Suppression of cytoplasmic male sterility by nuclear genes alters expression of a novel mitochondrial gene region. Plant Cell 3:1349-1362.
2. L’Homme, Y., Stahl, R.J., Li, X.-Q., Hameed, A. and Brown, G.G. (1997). Brassica nap cytoplasmic male sterility is associated with expression of a mtDNA region containing a chimeric gene similar to the pol CMS-associated orf224 gene. Current Genet. 31: 325-335.
3. Brown, G.G. (1999). Unique aspects of cytoplasmic male sterility and nuclear fertility restoration in Brassica napus. J. Hered. 90: 351-356.
4. Li, X.-Q,, Jean, M., Landry, B.S. and Brown, G.G. (1998). Restorer genes for different forms of Brassica cytoplasmic male sterility map to a single nuclear locus that modifies transcripts of several mitochondrial genes. Proc. Natl. Acad. Sci. USA. 97: 10032-10037.
5. Brown, G.G. et al. (2003). The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. Plant J. 35: 262-272.