Tomato WRKY81 acts as a negative regulator for drought tolerance by modulating guard cell H2O2-mediated stomatal closure

WRKY transcription factors (TFs) are key regulators in numerous plant biological processes and responses to stresses. Although a group III tomato WRKY, SlWKRY81, is induced by some biotic stressors, its role in drought response remains largely unknown. Here, we unveiled a critical role of SlWKRY81 in regulation of drought response by using agronomic, bioinformatics, genetic and pharmacological approaches. Drought gradually increased the transcript levels of SlWRKY81 and impaired leaf water potential and membrane stability in tomato. Analysis of plant phenotypes revealed that silencing of SlWRKY81 in tomato enhanced tolerance to drought, while its overexpression in Arabidopsis resulted in an opposite phenotype. Notably, the enhanced drought tolerance in SlWRKY81-silenced tomato plants was closely associated with a rapid and increased stomatal closure. Furthermore, such stomatal response in the SlWRKY81-silenced plants was sensitive to abscisic acid alongside drought-induced enhanced accumulation of H2O2 in the guard cells. The results suggest that SlWRKY81 acts as a negative regulator of stomatal closure by suppressing SlRBOH1-derived H2O2 accumulation, which attenuates plant tolerance to drought. These results may have potential implications on improving plant drought tolerance through genetic manipulation.