Multi-omics-based insights into tomato adaptation to multifactorial stress combination
Lidia S. Pascual, Enrique Serna, Abdul Ghani, Zhen Lyu, Manish Sridhar Immadi, Trupti Joshi, Mohit Verma, José Luís Rambla, Aurelio Gómez‐Cadenas, Ron Mittler, Sara I. Zandalinas
Abstract
Multifactorial stress combination (MFSC) is emerging as a major constraint to crop productivity under different climate change scenarios. While the physiological impacts of MFSC have been previously characterized in different plant species, the molecular and metabolic effects of MFSC remain poorly defined. Here, we used an integrative multi-omics approach to dissect the response of tomato (Solanum lycopersicum) plants to an MFSC of up to 6 low-intensity abiotic stressors. Our analysis uncovered a complexity-dependent molecular program in tomato. Transcriptomic analysis identified a core set of 194 transcripts commonly altered across all stress conditions, along with 155 transcription factors (TFs) specifically regulated under high-complexity conditions (4-, 5-, and 6-stress combinations). Focusing on heat-associated MFSC responses, we identified 103 transcripts uniquely responsive to these conditions, including 2 TFs (Zinc finger TF 32 and a B3 family protein) that may act as master regulators of all heat-associated MFSCs. Metabolomic profiling revealed a pronounced reprogramming of primary metabolism under MFSC, marked by decreased levels of tricarboxylic acid intermediates and accumulation of sugars, γ-aminobutyric acid, and branched-chain amino acids, suggesting a trade-off that favors osmoprotection and redox homeostasis over energy-intensive processes. Comparative analyses across tomato, Arabidopsis, Chlamydomonas, rice, and soybean highlighted a conserved molecular signature associated with MFSC. Integrated omics correlation analysis uncovered functional links among phytohormone signaling, photosynthetic efficiency, and key MFSC-related transcripts and metabolic hubs. Together, we reveal a coordinated and complexity-dependent molecular program in tomato, offering insights into plant adaptation to MFSC and identifying candidate regulatory and metabolic markers for engineering climate-resilient crops.