The C4 protein of tomato yellow leaf curl Sardinia virus primes drought tolerance in tomato through morphological adjustments

Viruses can interfere with the ability of plants to overcome abiotic stresses, indicating the existence of common molecular networksthat regulate stress responses. A begomovirus causing the tomato yellow leaf curl disease was recently shown to enhance heattolerance in tomato and drought tolerance in tomato and Nicotiana benthamiana and experimental evidence suggested that the virus encoded protein C4 is the main trigger of drought responses. However, the physiological andmolecular events underlying C4-induceddrought tolerance need further elucidation. In this study, transgenic tomato plants expressing the tomato yellow leaf curl Sardiniavirus (TYLCSV) C4 protein were subjected to severe drought stress, followed by recovery. Morphometric parameters, water potential,gas exchanges, and hormone contents in leaves weremeasured, in combination with molecular analysis of candidate genes involvedin stress response and hormone metabolism. Collected data proved that the expression of TYLCSV C4 positively affected the abilityof transgenic plants to tolerate water stress, by delaying the onset of stress-related features, improving the plant water use efficiencyand facilitating a rapid post-rehydration recovery. In addition, we demonstrated that specific anatomical and hydraulic traits, ratherthan biochemical signals, are the keynote of the C4-associated stress resilience. Our results provide novel insights into the biologyunderpinning drought tolerance in TYLCSV C4-expressing tomato plants, paving the way for further deepening the mechanismthrough which such proteins tune the plant-virus interaction.