Integrative systems analysis reveals heat-induced functional divergence in cultivated and wild tomato genotypes

Abstract

Extreme heat events driven by global warming increasingly threaten the productivity of tomato ( Solanum lycopersicum L.). While thermotolerance is often evaluated through individual physiological traits, resilience emerges from coordinated, multi-level regulation across growth dynamics and cellular stress responses. Here, we analyzed a diverse and contrasting panel of cultivated and wild tomato genotypes to resolve multidimensional stress-response strategies. Morphological, physiological, and biochemical traits were systematically quantified and integrated using the Stress Tolerance Index (STI), Membership Function Value (MFV), and correlation network analysis. Heat exposure induced pronounced, genotype-dependent divergence in biomass retention, membrane stability, pigment integrity, osmotic adjustment, and antioxidant capacity. Sensitive accessions (e.g., S. chilense PI 251313) exhibited severe growth suppression, chlorophyll loss, and elevated lipid peroxidation. In contrast, the commercial cultivar S. lycopersicum cv. İksir maintained biomass and structural stability, whereas the wild accession S. pimpinellifolium PI 365957 displayed enhanced antioxidant coordination and membrane protection. Network analysis revealed a heat-induced shift from growth-centered regulation to a tightly interconnected stress-response module, with strong associations among proline, superoxide dismutase, and catalase. Multivariate integration consistently ranked S. lycopersicum cv. İksir and S. pimpinellifolium PI 365957 as the most thermotolerant genotypes at the vegetative stage under acute thermal stress (45 °C), highlighting complementary adaptive strategies across cultivated and wild backgrounds. Collectively, these findings establish thermotolerance as an emergent systems property and identify wild relatives as valuable reservoirs of coordinated stress-adaptive traits for climate-resilient tomato breeding.