Pan-genome analysis reveals conservation and diversification of the SWEET gene family in wheat

Abstract

SWEET (Sugars Will Eventually be Exported Transporter) proteins mediate sugar transport and play important roles in plant growth, development, source-sink allocation, and responses to environmental stimuli. However, the conservation and diversification of the SWEET gene family across the wheat pan-genome remain poorly understood. Here, we performed a systematic pan-genome analysis of the SWEET gene family across 19 hexaploid wheat (Triticum aestivum L.) accessions. A total of 1,594 SWEET genes were identified, with 77–90 members in individual genomes. Gene copies belonging to core, soft-core, dispensable, and private homologous groups accounted for 52.6%, 30.9%, 14.6%, and 1.9%, respectively, based on presence/absence variation (PAV), revealing a predominantly conserved genomic framework accompanied by a smaller accession-variable component. Phylogenetic, motif, chromosomal and synteny analyses further revealed extensive evolutionary and genomic conservation accompanied by localized diversification among family members. Extensive homeologous and inter-accession collinearity was observed, and most pairwise ortholog comparisons exhibited Ka/Ks ratios below 1, supporting predominant purifying selection on conserved SWEET coding sequences. Promoter analysis identified diverse putative cis-regulatory elements related to environmental, hormonal, and developmental regulation, while transcriptome profiling showed heterogeneous tissue- and stress-associated expression patterns among TaSWEET genes. qRT-PCR analysis further suggested distinct temporal responses of selected TaSWEET genes under cold and polyethylene glycol (PEG)-induced osmotic stress. TaSWEET47 overexpression significantly increased grain width, thousand-grain weight, and mature-grain starch content in two independent transgenic lines without significantly affecting grain length. Collectively, these results reveal gene-content, evolutionary, regulatory, and transcriptional diversification within a broadly conserved SWEET family framework.