Seasonal gene-expression signatures of delayed fertilization in Fagaceae

Abstract In the family Fagaceae, fertilization is delayed by several weeks to one year after pollination, leading to one- or two-year fruiting species depending on whether fruiting occurs in the same or the next year after flowering. To investigate physiological responses underlying the regulation of delayed fertilization, we monitored seasonal changes in genome-wide gene expression in tissues including leaves and buds over two years under natural conditions in one- ( Quercus glauca ) and two-year fruiting species ( Lithocarpus edulis ). Genes associated with the responses to cold stress, photosynthesis, and cell proliferation, which are essential for survival and growth, showed highly conserved seasonal expression profiles regardless of species. However, seasonal expression profiles diverged between the one- and two-year fruiting species in genes associated with pollination, an important process contributing to the origin and maintenance of the reproductive barrier between plant species. By comparing seasonal progression of ovule development and gene expression in pistillate flowers, we revealed that ovules started developing after winter in the two-year fruiting species, which could be linked to the activation of genes involved in fertilization and female gametophyte development after winter. These findings suggest that the two-year fruiting species may have evolved a requirement of winter cold to prevent fertilization before winter and facilitate fertilization and embryo development in the following spring when temperature rises. This study offers new possibilities to explore the evolution of reproductive strategies in Fagaceae.