Whitefly infestation on pepper plants elicits defence responses against bacterial pathogens in leaves and roots and changes the below-ground microflora

Abstract

Upon facing biotic stresses, plants orchestrate defence mechanisms via internal and external mechanisms that are mediated by signalling molecules such as salicylic acid, jasmonic acid, ethylene and various other volatile compounds. Although pathogen- and chemical-induced plant resistance has been studied extensively within the same plant compartment, the effects of above-ground (AG) insect-elicited plant defence on the resistance expression in roots and the below-ground (BG) microbial community are not well understood. We assessed the effect of AG whitefly (Bemisia tabaci) attack on the elicitation of induced resistance against a leaf pathogen, Xanthomonas axonopodis pv. vesicatoria, a soil-borne pathogen, Ralstonia solanacearum, and on BG modifications of the rhizosphere microflora in peppers (Capsicum annuum). Symptom development caused by the two bacterial pathogens on leaves and roots was significantly reduced in whitefly-exposed plants as compared to controls. A combined treatment with benzothiadiazole (BTH) and whitefly caused an additive effect on induced resistance, indicating that whitefly-induced plant defence can utilize salicylic acid (SA)-dependent signalling. To obtain further genetic evidence of this phenomenon, we evaluated the gene expression of Capsicum annuum pathogenesis-related protein (CaPR) 1, CaPR4, CaPR10 and Ca protease inhibitor II, and observed increased expression after BTH and/or whitefly treatment indicating that AG whitefly infestation elicited SA and jasmonic acid signalling in AG and BG. Since the expression pattern of PR genes in the roots differed, we assessed microbial diversity in plants treated with BTH and/or whitefly. In addition to eliciting BG defence responses, a whitefly infestation of the leaves augmented the population of root-associated Gram-positive bacteria and fungi, which may have positively affected plant growth and induced systemic resistance. Whitefly feeding reduced plant size, which usually occurs as a consequence of the high costs of direct resistance induction. Synthesis. Our results demonstrate that whitefly-induced resistance against bacterial pathogens can cross the AG-BG border and may cause further indirect benefits on future plant development, because it can positively affect the association or plant roots with putatively beneficial microorganisms.