Genetic analysis of phenotypic plasticity identifies BBX6 as the candidate gene for maize adaptation to temperate regions

INTRODUCTION: Climate changes pose a significant threat to crop adaptation and production. Dissecting the genetic basis of phenotypic plasticity and uncovering the responsiveness of regulatory genes to environmental factors can significantly contribute to the improvement of climate- resilience in crops. METHODS: We established a BC1F3:4 population using the elite inbred lines Zheng58 and PH4CV and evaluated plant height (PH) across four environments characterized by substantial variations in environmental factors. Then, we quantified the correlation between the environmental mean of PH (the mean performance in each environment) and the environmental parameters within a specific growth window. Furthermore, we performed GWAS analysis of phenotypic plasticity, and identified QTLs and candidate gene that respond to key environment index. After that, we constructed the coexpression network involving the candidate gene, and performed selective sweep analysis of the candidate gene. RESULTS: We found that the environmental parameters demonstrated substantial variation across the environments, and genotype by environment interaction contributed to the variations of PH. Then, we identified PTT(35-48) (PTT is the abbreviation for photothermal units), the mean PTT from 35 to 48 days after planting, as the pivotal environmental index that closely correlated with environmental mean of PH. Leveraging the slopes of the response of PH to both the environmental mean and PTT(35-48), we successfully pinpointed QTLs for phenotypic plasticity on chromosomes 1 and 2. Notably, the PH4CV genotypes at these two QTLs exhibited positive contributions to phenotypic plasticity. Furthermore, our analysis demonstrated a direct correlation between the additive effects of each QTL and PTT(35-48). By analyzing transcriptome data of the parental lines in two environments, we found that the 1009 genes responding to PTT(35-48) were enriched in the biological processes related to environmental sensitivity. BBX6 was the prime candidate gene among the 13 genes in the two QTL regions. The coexpression network of BBX6 contained other genes related to flowering time and photoperiod sensitivity. Our investigation, including selective sweep analysis and genetic differentiation analysis, suggested that BBX6 underwent selection during maize domestication. DISCUSSION: Th is research substantially advances our understanding of critical environmental factors influencing maize adaptation while simultaneously provides an invaluable gene resource for the development of climate-resilient maize hybrid varieties.