Synchronization of proline, ascorbate and oxidative stress pathways under the combination of salinity and heat in tomato plants

Adverse environmental conditions have a devastating impact on plant productivity. In nature, multiple abiotic stresses occur simultaneously, and plants have evolved unique responses to cope against this combination of stresses. Here, we coupled genome-wide transcriptional profiling and untargeted metabolomics with physiological and biochemical analyses to characterize the effect of salinity and heat applied in combination on the metabolism of tomato plants. Our results demonstrate that this combination of stresses causes a unique reprogramming of metabolic pathways, including changes in the expression of 1388 genes and the accumulation of 568 molecular features. Pathway enrichment analysis of transcript and metabolite data indicated that the proline and ascorbate pathways act synchronously to maintain cellular redox homeostasis, which was supported by measurements of enzymatic activity and oxidative stress markers. We also identified key transcription factors from the basic Leucine Zipper Domain (bZIP), Zinc Finger Cysteine-2/Histidine-2 (C2H2) and Trihelix families that are likely regulators of the identified up-regulated genes under salinity + heat combination. Our results expand the current understanding of how plants acclimate to environmental stresses in combination and unveil the synergy between key cellular metabolic pathways for effective ROS detoxification. Our study opens the door to elucidating the different signaling mechanisms for stress tolerance.Acknowledgments This work was supported by the Ministry of Economy and Competitiveness from Spain (Grant No. PGC2018-09573-B-100) to R.M.R (Murcia, Spain), by the Ministry of Science, Innovation and Universities of Spain (Grant No. FPU16/05265) to M.L-D. (Murcia, Spain) and by start-up funds from the College of Agricultural and Environmental Sciences and the Department of Plant Sciences (UC Davis) to B.B-U (Davis, CA, United States