Integrated phenomic and genomic analyses unveil modes of altered phenotypic plasticity during wheat improvement

Wheat has a critical role in global food security. During the improvement of wheat from landraces to cultivars, a suite of traits has been modified for higher yields. However, changing patterns of wheat in response to different environmental conditions, or phenotypic plasticity, during this improvement remain to be elucidated. We measure 17 agronomic traits for 406 wheat accessions consisting of landraces and cultivars in 10 environments. Analyses reveal varied contributions from genotype and environment to phenotypic variation across the evaluated traits. Using environmental indices identified by Critical Environmental Regressor through Informed Search (CERIS), we model the phenotypic values across environments of each accession with two reaction-norm parameters (intercept and slope). Genome Wide Association Studies (GWAS) identify loci significantly associated with variation in the two parameters, including Ppd-D1 and two Green Revolution genes (Rht-D1 and Rht-B1). Compared with the corresponding wild-type allele, Rht-D1b alters intercept and slope of more traits than Rht-B1b. Among nine possible modes of phenotypic plasticity change from landraces to cultivars, three predominant modes account for 88% of evaluated traits. Generally, two reaction-norm parameters decrease simultaneously for plant architecture traits but increase simultaneously for yield component traits. We systematically evaluate phenome-wide wheat phenotypic plasticity. Two reaction-norm parameters based on specific environmental indices capture varied degrees of phenotypic plasticity for each trait across wheat accessions. Two Green Revolution genes have different effect spectra in altering phenome-wide phenotypic plasticity. By incorporating the evolutionary dimension, we reveal dominant modes of phenotypic plasticity change during wheat improvement.