Levels of gene expression underpin organismal phenotypes, but the nature of selection that acts on gene expression and its role in adaptive evolution remain unknown. In this project, we undertook two large-scale experiments where we assayed gene expression in rice (Oryza sativa) in both drought stress and salinity conditions, and used phenotypic selection analysis to estimate the type and strength of selection on the levels of more than 15,000 transcripts. The ability to estimate selection strengths provides insights into how selection can shape molecular traits at the core of gene action.

First, in a drought experiment, we found that variation in most transcripts appears (nearly) neutral or under very weak stabilizing selection in wet paddy conditions (with median standardized selection differentials near zero), but selection is stronger under drought conditions. Overall, more transcripts are conditionally neutral (2.83%) than are antagonistically pleiotropic (0.04%), and transcripts that display lower levels of expression and stochastic noise and higher levels of plasticity are under stronger selection. Selection strength was further weakly negatively associated with levels of cis-regulation and network connectivity9. Our multivariate analysis suggests that selection acts on the expression of photosynthesis genes, but that the efficacy of selection is genetically constrained under drought conditions10. Drought selected for earlier flowering and a higher expression of OsMADS18 (Os07g0605200), which encodes a MADS-box transcription factor and is a known regulator of early flowering—marking this gene as a drought-escape gene.

Second, we also used an integrative field dataset of rice grown in a normal wet paddy or subjected to moderate levels of salt stress to examine genome-wide patterns of gene expression variation under salinity stress conditions and to study their micro- and macroevolutionary dynamics. We find that at microevolutionary timescales, salinity stress induces increased selective pressure on gene expression. Further, we show that trans-eQTLs rather than cis-eQTLs are primarily associated with rice's response to salinity stress, potentially via a few master-regulators. Importantly, we show that cis- and trans-eQTLs are under different selection regimes, and that mating system may play a role in determining the selection profile for cis-eQTLs, but not trans-eQTLs, giving us insights into the macroevolutionary dynamics of gene expression variation. By examining genomic, transcriptomic, and phenotypic variation across a rice population, we gain insights into the molecular and genetic landscape underlying adaptive stress responses, which can be extended to other crops and other stresses.

Finally, we also conducted numerous other ancillary experiments that helped further illuminate rice biology.  We constructed the first fitness consequence map of rice by integrating single nucleotide polymorphism data (SNPs) with functional genomics and epigenomic marks to establish areas of the genome that were under varying levels of selection. We also examined the dispersal history of rice using genome information coupled with paleoclimate data, to role of environment in rice movement over the last 9,000 years.  Together, these and other studies helped advance our understanding of rice adaptation (and other plants) to varying environments, particularly stress environments.

Last Modified: 01/03/2024
Modified by: Michael D Purugganan