Dynamic effects of interacting genes underlying rice flowering-time phenotypic plasticity and global adaptation

Abstract

Phenotypic variation of living organisms is shaped by genetics, environment, and their interaction. Understanding phenotypic plasticity under natural conditions is hindered by the apparently complex environment and the interacting genes and pathways. Herein, we report findings from the dissection of rice flowering-time plasticity in a genetic mapping population grown in natural long-day field environments. Genetic loci harboring four genes originally discovered for their photoperiodic effects (Hd1, Hd2, Hd5, and Hd6) were found to differentially respond to temperature at the early growth stage to jointly determine flowering time. The effects of these plasticity genes were revealed with multiple reaction norms along the temperature gradient. Coupling genomics and the environmental index, accurate performance predictions were obtained. Next, we examined the allelic variation in the four flowering-time genes across the diverse accessions from the 3,000 Rice Genomes Project, and constructed haplotypes at both individual-gene and multi-gene levels. The geographic distribution of haplotypes revealed their preferential adaptation to different temperature zones. Regions with lower temperature were dominated by haplotypes sensitive to temperature changes, while the equatorial region had a majority of haplotypes that are less responsive to temperature. Integrating knowledge from genomics, gene cloning and functional characterization, and environment quantification, we proposed a conceptual model with multiple levels of reaction norms to help bridge the gaps among individual gene discovery, field-level phenotypic plasticity, and genomic diversity and adaptation.