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.

Epigenetic differences between wild and cultivated grapevines highlight the contribution of DNA methylation during crop domestication

“…In grapevines, alternative splicing has been linked to phenotypic specificities and distinct adaptive capacities by enabling a diverse range of proteins to be produced [ 63 ]. Several studies suggest that crop domestication has selected alternative splicing variation linked to desired traits, such as flower production [ 64 ], anthocyanin accumulation [ 65 ] or cell wall degradation in fruits [ 66 ]. Research highlighted in a study on pear ( Pyrus pyrifolia ) revealed how domestication has led to changes in the alternative splicing of genes that contribute to the fruit traits such as sugar metabolism, acid metabolism, stone cell formation, and fruit firmness [ 66 ].…”

“…Research highlighted in a study on pear ( Pyrus pyrifolia ) revealed how domestication has led to changes in the alternative splicing of genes that contribute to the fruit traits such as sugar metabolism, acid metabolism, stone cell formation, and fruit firmness [ 66 ]. Similarly, comparative analyses between wild and cultivated tomato species have shown that domestication impacts environment-responsive alternative splicing in the inflorescences, suggesting a role in adaptability and phenotypic diversity [ 64 ]. In the spiny Solanum group, a study identified a DFR gene where alternative splicing, influenced by a natural promoter variant, plays a crucial role in anthocyanin accumulation, a trait selectively enhanced during domestication [ 65 ].…”

RNA-seq analysis reveals transcriptome reprogramming and alternative splicing during early response to salt stress in tomato root

“…In tomato, around 65% of the annotated protein-coding genes possess multiple transcript isoforms ( Clark et al., 2019 ). Alternative splicing changes have been reported in tomato plants grown under phytotron vs greenhouse conditions ( Wang et al., 2017 ), in inflorescences of cultivated and wild tomato species ( Zhou et al., 2022 ), during fruit development regulation ( Sun and Xiao, 2015 ; Wang et al., 2016 ), pollen responses to heat stress ( Keller et al., 2017 ), tomato responses to drought stress ( Lee et al., 2020 ), water deficit stress ( Ruggiero et al., 2022 ), low nitrate stress ( Ruggiero et al., 2022 ), phosphate starvation ( Tian et al., 2021 ), and response to the fungal infection by Trichoderma harzianum ( De Palma et al., 2019 ). Based on these studies, differential alternative splicing (DAS) was found to be tissue-specific, developmental stage-related or stress-responsive condition.…”

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“…In tomato, around 65% of the annotated protein-coding genes possess multiple transcript isoforms (Clark et al, 2019). Alternative splicing changes have been reported in tomato plants grown under phytotron vs greenhouse conditions (Wang et al, 2017), in inflorescences of cultivated and wild tomato species (Zhou et al, 2022), during fruit development regulation (Sun and Xiao, 2015;Wang et al, 2016), pollen responses to heat stress (Keller et al, 2017), tomato responses to drought stress (Lee et al, 2020), water deficit stress (Ruggiero et al, 2022), low nitrate stress (Ruggiero et al, 2022), phosphate starvation (Tian et al, 2021), and response to the fungal infection by Trichoderma harzianum (De Palma et al, 2019). Based on these studies, differential alternative splicing (DAS) was found to be tissuespecific, developmental stage-related or stress-responsive condition.…”

“…On the other hand, RI event was reported to be the most frequent event induced by salt stress in Arabidiopsis (Ding et al, 2014b), wheat (Liu et al, 2018), cotton (Zhu et al, 2018) and Barley (Fu et al, 2019), while A3SS was the mostly affected AS events in rice by salt stress (Fu et al, 2019). Given that the differences in AS profiles are related to tissue type, stress condition and genotype (Gan et al, 2011;Vitulo et al, 2014;Martıń et al, 2021;Zhou et al, 2022), the differences on the alternative splicing preference induced by salt may contribute to the evolutionary adaptation process in tomato.…”