Comparative transcriptomic and proteomic analyses of hypoxia response in wild and cultivated tomato roots.

Abstract

Background: Hypoxia significantly impairs tomato productivity and yield. Although cultivated tomato varieties (Solanum lycopersicum) are generally sensitive to low-oxygen conditions, their wild relatives (Solanum habrochaites) display substantially lower sensitivity. To elucidate the molecular mechanisms underlying these contrasting phenotypes, as well as the impact of positive selection and protein-protein interactions of differentially expressed genes (DEGs) and proteins (DEPs), we conducted transcriptomic and proteomic analyses of root samples from a wild tomato accession, T178 (S. habrochaites), and a cultivated tomato variety, Fenzhenzhu (S. lycopersicum, FZZ).

Results: Compared with cultivated seedlings, wild tomato seedlings exhibited markedly reduced sensitivity to hypoxia, as demonstrated by lower growth inhibition and higher membership function values under low-oxygen conditions. In T178, 2,351 DEGs were identified (1,238 upregulated and 1,113 downregulated), whereas in FZZ, 2,931 DEGs were detected (1,326 upregulated and 1,605 downregulated). Heatmap clustering and functional enrichment analysis revealed significant differences in transcriptional regulation between T178 and FZZ under hypoxia. Specifically, among the unique DEGs in T178, genes related to carbohydrate metabolism were significantly upregulated, whereas genes associated with single-organism metabolic processes were downregulated. In contrast, among the unique DEGs in FZZ, genes related to DNA-templated transcription were significantly upregulated, whereas genes associated with protein phosphorylation were downregulated. Proteomic analysis identified 544 and 493 DEPs in T178 and FZZ, respectively, with T178 DEPs predominantly linked to metabolic flexibility and antioxidant responses, whereas both sets were enriched in similar metabolic pathways. Further positive selection analyses emphasized the adaptive evolution of hypoxic responses in wild and cultivated tomatoes, exemplified by T178, which harbors 1,289 positively selected genes linked to carbon metabolism and energy homeostasis, underscoring its adaptation to low-oxygen environments. Moreover, protein-protein interaction (PPI) network analyses revealed distinct adaptive strategies in T178 and FZZ. By analyzing the gene and protein networks of FZZ and T178 under hypoxic conditions, we inferred that T178 enhances hypoxia adaptation by forming more independent small modules and multilevel regulatory networks, whereas FZZ relies on a few large modules with limited functional diversity, resulting in weaker hypoxia tolerance.

Conclusions: Our results demonstrated that the molecular response mechanisms to hypoxia differ substantially between wild and cultivated tomatoes, with wild tomatoes showing more distinctive and effective adaptations. The differentially regulated genes identified in this study represent promising targets for future research and breeding efforts aimed at improving hypoxia tolerance in tomatoes.