Trehalose induces tomato defenses and increases drought tolerance and bacterial wilt disease resistance

Abstract

AbstractRalstonia solanacearum causes plant bacterial wilt disease, leading to severe crop losses. Xylem sap from R. solanacearum-infected tomato is enriched in host produced trehalose. Water stressed plants accumulate the disaccharide trehalose, which increases drought tolerance via abscisic acid (ABA) signaling networks. Because infected plants have reduced water flow, we hypothesized that bacterial wilt physiologically mimics drought stress, which trehalose could mitigate. Transcriptomic responses of susceptible vs. resistant tomato plants to R. solanacearum infection revealed differential expression of drought-associated genes, including those involved in ABA and trehalose metabolism. ABA was enriched in xylem sap from R. solanacearum-infected plants. Treating roots with ABA lowered stomatal conductance and reduced R. solanacearum stem colonization. Treating roots with trehalose increased ABA in xylem sap and reduced plant water use by reducing stomatal conductance and temporarily improving water use efficiency. Further, trehalose-treated plants were more resistant to bacterial wilt disease. Trehalose treatment also upregulated expression of salicylic acid (SA)-dependent defense genes, increased xylem sap levels of SA and other antimicrobial compounds, and increased wilt resistance of SA-insensitive NahG tomato plants. Additionally, trehalose treatment increased xylem concentrations of jasmonic acid and related oxylipins. Together, these data show that exogenous trehalose reduced both water stress and bacterial wilt disease and triggered systemic resistance. This suite of responses revealed unexpected linkages between plant responses to biotic and abiotic stress and suggests that that R. solanacearum-infected tomato plants produce more trehalose to improve water use efficiency and increase wilt disease resistance. In turn, R. solanacearum degrades trehalose as a counter-defense.