Plant Sex Chromosomes and Breeding Systems
Plants have evolved a wide array of mechanisms to control with whom they mate, which is among the most important factors to ensure that progeny are fit. Many of these breeding systems reduce the probability of inbreeding, which can lower fitness relative to outbred progeny. Our lab has conducted in-depth investigations of the genetics and ecology of two breeding systems - gynodioecy, wherein individuals within a species are either female or hermaphrodites, and dioecy, wherein individuals are male or female. Our current work is primarily focused on the evolution of sex chromosomes which control sex determination in dioecious plants.
Evolution of Sex Chromosomes in the Salicaceae
Theory predicts that the evolution of gender dimorphism and the evolution of sex chromosomes should be intertwined; yet few biological systems are poised to test these predictions. Our research is developing the Salicaceae as a premier biological system to comprehensively understand sex chromosome evolution in plants, including changes in the location and size of the sex determination region (SDR), the influence of sexual antagonism and gender dimorphism, and how plant gender dimorphism has cascading influences on different trophic levels. Populus (poplars, aspens, cottonwoods) and Salix (willows) are sister genera in the Salicaceae. They are dioecious with sex chromosomes, a rarity among plant genera. Species in these genera also exhibit gender dimorphism, which can influence arthropod diversity. The two genera are among the most dynamic biological systems with regard to changes in the location of the sex determination region and which sex is heterogametic. Many more changes in the heterogametic sex and location of the SDR may have occurred in these genera, but sex determination in large portions of their diversity remains unstudied.
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Our research aims to unify and integrate how the interplay among functional, genetic, and phylogenetic aspects of biodiversity is influencing the evolutionary outcomes of sex determination in Populus and Salix. With colleagues in our US-China Joint Lab, we are conducting a comprehensive survey of gender dimorphism for defense and volatile chemistry in Populus and Salix, and determining how gender dimorphism influences pollinator attraction, herbivore feeding preferences, and overall arthropod community structure. We also are mapping the SDR locations in a suite of 16 new Salix and Populus species, determine if these regions contain defense and volatile chemistry loci consistent with their theoretical influence on movement of the SDR, and investigating predicted population genomic patterns of sex chromosome divergence caused by interactions between gender dimorphic and sexually antagonistic loci with the SDR. Finally, we are developing and integrating robust phylogenies of Populus, Salix, and close outgroup genera within the Salicaceae in order to understand how many times the SDR has moved in this taxonomic group, how the SDR has changed in size and composition, and whether movement of the SDR correlates with the inability to hybridize.
Representative Publications:
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Sanderson, B., L. Wang, Z.-Q. Wu, P. Tiffin and M.S. Olson. 2018. Sexual dimorphism and sex-biased gene expression in Populus balsamifera. New Phytologist. http://onlinelibrary.wiley.com/10.1111/(ISSN)1469-8137
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Olson, M.S., J.L. Hamrick, and R.C. Moore. 2016. Breeding systems, mating systems, and gender determination in angiosperm trees. In: A. Groover and Q. Cronk, eds. Comparative and Evolutionary Genomics of Angiosperm Trees. Springer.
Ecological Genetics of Gynodioecy in Silene vulgaris
Gynodioecy is a breeding system wherein female and hermaphrodite individuals coexist in populations. In S. vulgaris female result from male-sterility factors carried in the mitochondrial genome (cytoplasmic male sterility, CMS), whereas hermaphodites carry male-sterility factors, but also carry a male-fertility restorer in the nuclear genome. Inheritance of sex expression is determined by the combination of CMS factors and male fertility restorer genes that an individual carries. Across a series of studies we have shown that mitochondrial diversity in natural populations is extremely high, likely reflecting a high diversity of CMS types. We also have shown that seed fitness of both females and hermaphrodites is frequency dependent, and hermaphrodite selfing rates are negatively frequency dependent. Finally, we have identified chimeric genes in the mitochondria that are candidates for CMS genes. We plant to continue to explore the genetics of this fascinating and complex breeding system and encourage students interested in this topic to contact us.
Representative Publications:
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Stone, J.D. and M. S. Olson. 2018. Pollination context alters female advantage in gynodioecious Silene vulgaris. Journal of Evolutionary Biology 31:111-122.
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Štorchová H., K. Müller, S. Lau, and M.S. Olson. 2012. Mosaic origin of a complex chimeric mitochondrial gene in Silene vulgaris. PLoS ONE 7:e30401.
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Miyake, K. and M.S. Olson. 2009. Experimental evidence for frequency dependent self fertilization in gynodioecious plant, Silene vulgaris. Evolution 63:1644-1652
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Olson, M. S. and D. E. McCauley. 2002. Mitochondrial DNA diversity, population structure, and gender association in the gynodioecious plant Silene vulgaris. Evolution, 56:253-262.