Pangenomic analysis identifies structural variation associated with heat tolerance in pearl millet

Pearl millet is an important cereal crop worldwide and shows superior heat tolerance. Here, we developed a graph-based pan-genome by assembling ten chromosomal genomes with one existing assembly adapted to different climates worldwide and captured 424,085 genomic structural variations (SVs). Comparative genomics and transcriptomics analyses revealed the expansion of the RWP-RK transcription factor family and the involvement of endoplasmic reticulum (ER)-related genes in heat tolerance. The overexpression of one RWP-RK gene led to enhanced plant heat tolerance and transactivated ER-related genes quickly, supporting the important roles of RWP-RK transcription factors and ER system in heat tolerance. Furthermore, we found that some SVs affected the gene expression associated with heat tolerance and SVs surrounding ER-related genes shaped adaptation to heat tolerance during domestication in the population. Our study provides a comprehensive genomic resource revealing insights into heat tolerance and laying a foundation for generating more robust crops under the changing climate. A graph-based pan-genome constructed using de novo genome assemblies of ten pearl millet accessions adapted to different climates worldwide identifies structural variations and their contribution to heat tolerance in pearl millet.

Automated summary

A graph-based pan-genome, developed from ten pearl millet chromosomal genomes and one existing assembly, identifies 424,085 genomic structural variations. Comparative genomics and transcriptomics analyses highlight the role of RWP-RK transcription factors and endoplasmic reticulum (ER)-related genes in heat tolerance. Overexpression of an RWP-RK gene enhances plant heat tolerance and activates ER-related genes, indicating their importance in heat tolerance. Structural variations influence gene expression associated with heat tolerance and contribute to the adaptation of pearl millet during domestication. This study provides a comprehensive genomic resource for understanding heat tolerance and improving crop resilience to changing climates.