Andrea Case
Ph.D. 2002, McGill University
September 2003 - July 2005
Currently: Assistant Professor, Kent State University.
Genomic coevolution in plants: An investigation of cytoplasmic male sterility and nuclear fertility restoration in Mimulus guttatus
The subdivision of the eukaryotic genome into cytoplasmic and nuclear components favors intergenomic integration and cooperation at the molecular level. Cells (and nuclear genomes) depend on the metabolic processes of mitochondria (mt) and chloroplasts (cp) for survival and reproduction, while the smaller cytoplasmic genomes rely on nuclear components (enzymes, transcription regulators, etc.) to carry out their critical functions.
The process of intergenomic coevolution and integration is of particular interest in plants for two reasons: 1) plants must co-ordinate three rather than two separate genomic components, and 2) plant mt contain a large number of detrimental expressed open reading frames that must be continuously counteracted by nuclear elements. The best-known example of this intergenomic coevolution in plants is cytoplasmic male sterility and nuclear fertility restoration (CMS; Frank 1989, Hanson 1991, Schnable and Wise 1998, Budar et al. 2003, Hanson and Bentolila 2004).
The disruption of pollen development by CMS has been documented in over 150 plant species to date and may be ubiquitous in flowering plants (Schnable and Wise 1998, Hanson and Bentolila 2004). CMS is always associated with chimeric genes in the mt genome, which are always accompanied by nuclear genes capable of restoring male fertility (Rf). Much of what we understand about CMS/Rf molecular genetics comes from hermaphroditic crop species. We have a very limited understanding of the historical patterns or population genetics of CMS/Rf in populations of wild hermaphroditic species.
I have taken a genetic approach to identify molecular variation and population structure of a CMS gene in a wild hermaphroditic plant, Mimulus guttatus. The expression of this CMS gene in hybrids results in malformed anther morphology and a complete lack of pollen production (Fig. 1). Further crossing experiments support the existence of a dominant Rf allele, which is currently being mapped (L. Fishman, pers. comm.).
The distribution of this CMS gene among M. guttatus populations will provide insight into several critical questions about the evolutionary dynamics of cyto-nuclear interactions.
- How often do novel CMS genes arise and how fast do they spread within populations? If the mitochondrial rearrangements creating these genes are frequent, we should expect each CMS gene to be localized to a small geographic area, perhaps individual populations. Rapid fixation of CMS/Rf within populations would indicate strong selection and would contribute to local distribution if the rate of spread exceeds the rate of seed flow to other populations.
- What factors limit or promote their spread between populations? CMS genes can only disperse through seed, while nuclear restorers can also spread through pollen. The invasion of either CMS or Rf into populations depends on their direct fitness effects in the presence or absence of the other partner.
The first step in addressing these questions directly is identifying the CMS gene and screen for its presence among multiple populations of Mimulus.
Significance of the proposed research This research project will enlighten our understanding of the evolutionary dynamics of cyto- nuclear interactions, and the process of intergenomic coevolution. Cytoplasmic male sterility represents an easily observed phenotype stemming from a lack of compatibility and integration between nuclear and mitochondrial genomes. The nature of selection on such interactions in natural populations is presently unknown, and depends a great deal on the fitness effects of these interactions as well as their prevalence-how often new players evolve and how frequently they interact via gene flow.
Literature Cited
Budar, F., P. Touzet, and R. De Paepe. 2003. The nucleo-mitochondrial conflict in cytoplasmic male steriles revisited. Genetica 117:3-16.
Frank, S.A. 1989. The evolutionary dynamics of cytoplasmic male sterility. Am. Nat. 133:345-376.
Hanson, M.R. 1991. Plant mitochondrial mutations and male sterility. Ann. Rev. Genet. 25:461-486.
Hanson, M.R. and S. Bentolila 2004. Interactions of mitochondrial and nuclear genes that affect male gametophyte development. The Plant Cell 16:S154-S169.
Palmer, J.D., K.L. Adams, Y. Cho, C.L. Parkinson, Y-L. Qiu, and K. Song. 2000. Dynamic evolution of plant mitochondrial gemones: Mobile genes and introns and highly variable mutation rates. PNAS 97:6960-6966.
Schnable, P.S. & R.P. Wise 1998. The molecular basis of cytoplasmic male sterility and fertility restoration. Tr. Pl. Sci. 3:175-180.