Roles for polyploidy, circadian rhythms, and stress responses in hybrid vigor
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Hybrid plants and animals, like corn and the domestic dog, grow larger and more vigorously than their parents, a common phenomenon known as hybrid vigor or heterosis. In hybrids between Arabidopsis ecotypes or species (in allotetraploids), altered expression of circadian clock genes leads to increased starch and chlorophyll content and greater biomass. In plants and animals, circadian clock regulation plays a key role in optimizing metabolic pathways, increasing fitness, and controlling responses to biotic and abiotic stresses. In the allotetraploids, the increased level of heterosis is likely caused by interspecific hybridization as well as genome doubling. However, it is unknown how genome dosage and allelic effects influence heterosis, and whether additional clock output traits, such as stress responses, are altered in hybrids. In three related projects, the effects of genomic hybridization (including parent-of-origin effects) and genome dosage on heterosis were elucidated. In my first project, I found that although ploidy influenced many traits, including seed and cell size, biomass and circadian clock gene expression were most strongly influenced by hybridization. Additionally, parent-of-origin effects between reciprocal hybrids were frequently observed for many traits. In my second project, I described a unique role for RNA-directed DNA methylation (mainly CHH methylation) in mediating the parent-of-origin effect on expression of the circadian clock gene CCA1 in reciprocal hybrids. Altered CCA1 expression peaks were associated with heterosis of biomass accumulation in the reciprocal hybrids. Lastly, I used transcriptome sequencing in hybrids at different times of day to examine changes in downstream clock-regulated pathways. In the hybrids, many genes in photosynthetic pathways were upregulated, while many genes involved in biotic and abiotic stresses were repressed during the morning and afternoon, respectively. Additionally, natural variation between parents in stress-responsive gene expression was found to be crucial for producing vigorous hybrids. These conceptual advances increase the mechanistic understanding of heterosis, and may guide selection of parents for making better hybrids.