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Genetics of alternative splicing evolution during sunflower domestication

Significance Alternative splicing is a form of genetic regulation that enables the production of multiple proteins from a single gene. This study is one of the first to investigate variation in alternative splicing during a major evolutionary transition. We analyzed RNA from wild and domesticated sunflowers to examine differentiation in splice patterns during domestication. We identified divergent splice forms that may be involved in seed development, a major target of selection during domestication. Genetic mapping revealed that relatively few regulatory switches affecting many proteins have been altered in domesticated sunflowers. Our findings indicate that differences in splicing arose rapidly during a recent evolutionary transition and appear to contribute to adaptation and population divergence. Alternative splicing enables organisms to produce the diversity of proteins necessary for multicellular life by using relatively few protein-coding genes. Although differences in splicing have been identified among divergent taxa, the shorter-term evolution of splicing is understudied. The origins of novel splice forms, and the contributions of alternative splicing to major evolutionary transitions, are largely unknown. This study used transcriptomes of wild and domesticated sunflowers to examine splice differentiation and regulation during domestication. We identified substantial splicing divergence between wild and domesticated sunflowers, mainly in the form of intron retention. Transcripts with divergent splicing were enriched for seed-development functions, suggesting that artificial selection impacted splicing patterns. Mapping of quantitative trait loci (QTLs) associated with 144 differential splicing cases revealed primarily trans-acting variation affecting splicing patterns. A large proportion of identified QTLs contain known spliceosome proteins and are associated with splicing variation in multiple genes. Examining a broader set of wild and domesticated sunflower genotypes revealed that most differential splicing patterns in domesticated sunflowers likely arose from standing variation in wild Helianthus annuus and gained frequency during the domestication process. However, several domesticate-associated splicing patterns appear to be introgressed from other Helianthus species. These results suggest that sunflower domestication involved selection on pleiotropic regulatory alleles. More generally, our findings indicate that substantial differences in isoform abundances arose rapidly during a recent evolutionary transition and appear to contribute to adaptation and population divergence.