Comparative Analysis of Environment-Responsive Alternative Splicing in the Inflorescences of Cultivated and Wild Tomato Species

Abstract

Cultivated tomato (Solanum lycopersicum) is bred for fruit production in optimized environments, in contrast to harsh environments where their ancestral relatives thrive. The process of domestication and breeding has profound impacts on the phenotypic plasticity of plant development and the stress response. Notably, the alternative splicing (AS) of precursor message RNA (pre-mRNA), which is one of the major factors contributing to transcriptome complexity, is responsive to developmental cues and environmental change. To determine a possible association between AS events and phenotypic plasticity, we investigated environment-responsive AS events in the inflorescences of cultivated tomato and its ancestral relatives S. pimpinellifolium. Despite that similar AS frequencies were detected in the cultivated tomato variety Moneymaker and two S. pimpinellifolium accessions under the same growth conditions, 528 genes including splicing factors showed differential splicing in the inflorescences of plants grown in open fields and plastic greenhouses in the Moneymaker variety. In contrast, the two S. pimpinellifolium accessions, LA1589 and LA1781, had 298 and 268 genes showing differential splicing, respectively. Moreover, seven heat responsive genes showed opposite expression patterns in response to changing growth conditions between Moneymaker and its ancestral relatives. Accordingly, there were eight differentially expressed splice variants from genes involved in heat response in Moneymaker. Our results reveal distinctive features of AS events in the inflorescences between cultivated tomato and its ancestral relatives, and show that AS regulation in response to environmental changes is genotype dependent.