Pangenome and transcriptome analyses reveal extensive diversity and breeding signatures in the oat GDSL-esterase/lipase gene family

Abstract

Lipolytic enzymes play critical roles in plant development, growth, and stress responses. In oat (Avena sativa), they are of particular interest because lipid hydrolysis contributes to rancidity and reduced grain quality, yet little is known about genomic variation in oat lipolytic enzymes. Here, we investigated genomic and expression diversity of the GDSL-esterase/lipase gene family using pangenome, transcriptome, and genome-wide association analyses. Across 22 A. sativa and two A. sterilis genome assemblies, we identified 7,775 GDSL genes (~324 per assembly), revealing wide conservation of ancestral orthologs alongside extensive copy-number variation among homoeologs and paralogs. Transcriptome profiling across 20 genotypes and six tissues demonstrated preferential expression in embryo and root, with tissue-specific patterns highlighting candidates for specific functions, such as seed lipid metabolism. Associations with structural variants further uncovered candidate mutations underlying expression variation among accessions. Comparisons of cultivated and wild oat detected loci with signatures of breeding-based selection, suggesting that GDSL genes have contributed to diversification of the cultivated gene pool. Using 629 whole-genome sequenced accessions, we also identified associations between GDSL regions and agronomic traits, particularly plant height and effective tiller number. Several regions showed patterns consistent with selection, highlighting candidate loci for further investigation of agronomic variation. Together, our results reveal substantial genomic and transcriptional diversity within the oat GDSL gene family and identify candidate genes and genomic regions for improving seed quality and agronomic performance. More broadly, our study demonstrates how pangenomic resources can be used to investigate gene-family diversity and function in complex polyploid crops.