Testing genetic and evolutionary mechanisms of gamete signal divergence in Solanum

Indiana University, Bloomington IN

Investigators

Abstract

Differences between males and females in mating opportunities can result in unequal evolutionary pressures that are termed "sexual selection." While sexual selection is well studied in animals, its existence and evolution in plants is not well known. Understanding this process in plants can contribute to methods for crossing crops with their wild relatives, thereby allowing the transfer of useful wild traits into agricultural species. This research examines variation in chemical signals between male and female gametes (pollen and ovules) in several species in the genus Solanum, a group that includes important crop species: tomato, potato and eggplant. Chemical attraction between gametes is essential for reproduction in most plants and animals. The project will measure the effectiveness of gamete signals within and between species, identify the genetic and chemical causes of variation in signal attractiveness, and the consequences of this variation for patterns of fertilization success. These findings will generate new information about which signaling interactions are essential for fertilization, and greater understanding of why and how differences in male-female signaling interactions evolve. In addition, the project will involve graduate students, undergraduates, and high school students, including women and individuals from groups that are underrepresented in the sciences. The project addresses the mechanistic basis of divergence in gamete chemoattraction, including the specific causal molecular changes, the role of this divergence in reproductive barriers (gamete isolation) between species, and the ecological and reproductive conditions that influence rates of change in the attraction signal. Preliminary research in the wild tomato group (Solanum) shows that gamete recognition occurs via an ovule-secreted chemoattractant that causes growing pollen tubes to reorient towards conspecific female gametes. Specific combinations of heterospecific gametes show significantly reduced attraction, indicating divergence between some species in this ovule-secreted (female) signal. The proposed work will: quantify the association between divergence in ovule gene expression and gamete chemoattraction within and between a group of closely related species; identify the underlying molecular loci, characterize their patterns of molecular evolution across the clade, and associate sequence changes with functional behavioral divergence in gamete attraction; and, evaluate evidence that selection in general, and sexual selection specifically, is a driver of gamete signal evolution and therefore divergence in chemoattraction between species. The research uses a combination of semi in vivo behavioral assays that manipulate the identity of interacting gametic partners, targeted transgenic markers, functional manipulation, and molecular evolutionary analysis, each of which has already been developed or applied in this experimental system. The findings will provide a comprehensive empirical assessment of the relationship between molecular and functional divergence in gamete recognition molecules, across multiple closely related species. This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.