Effect of Feeding Stage and Density of Whiteflies on Subsequent Aphid Performance on Tobacco Plants

Abstract

Bemisia tabaci Middle East-Asia Minor 1 (MEAM1) is a cosmopolitan, highly polyphagous agricultural pest, which has the capacity to displace other native insect herbivores. Here, equipped with an integrated approach, the effect of developmental stages and feeding density of whiteflies on Myzus persicae performance in tobacco plants are investigated. Bioassay results showed that B. tabaci nymphs, but not adult, pre-infestation significantly reduced survival and fecundity of M. persicae, and the strongest resistance to M. persicae was detected at the medium density (9–10 nymphs/cm2). Neither low nor high feeding density of B. tabaci nymphs triggered visible resistance to aphids. However, no significant results were detected in salicylate-deficient NahG plants after B. tabaci nymph infestation. In addition to performance distinctions, hormone quantification and qPCR results revealed very different effects for nymph and adult whitefly stages on the defense responses in tobacco. B. tabaci nymph infestation significantly increased SA accumulation and SA-responsive genes (PR-1a, PR-2a) expression but suppressed JA-regulated responses. In contrast, tobacco plants responded to adult infestation by slightly increasing in both SA- and JA-regulated defenses. Furthermore, higher transcription level of Bt56, coding gene of a secretory salivary effector, was recorded in nymphs vs. adults, while silencing of Bt56 by virus-induced gene silencing (VIGS) partly impaired the aphid resistance induced by B. tabaci nymphs. These results proved that the induction of tobacco defense responses varied with the feeding stages of whiteflies: nymphs of B. tabaci, but not adults, induced a defense response against aphids, with a density threshold for this induced resistance.