Abstract

The silverleaf whitefly Bemisia tabaci is an important and invasive crop pest in many countries. Previous laboratory studies with Arabidopsis demonstrated that B. tabaci can suppress jasmonic acid (JA) defenses and thereby enhance B. tabaci performance. Whether B. tabaci can suppress JA-regulated host plant defenses in field is unknown. In the present study, we found that, relative to wild-type (WT) tomato plants, transgenic tomato mutants that activated JA defenses (35s::prosys) or impaired JA defenses (spr-2 and def-1) did not affect the survival or reproduction of B. tabaci adults in growth chamber experiments. In contrast, tomato mutants that activated JA defenses slowed B. tabaci nymphal development, while mutants that impaired JA defenses accelerated nymphal development. These effects of JA defenses on nymphal development were also documented under semi-field conditions. Changes in the expression of defense genes and in the production of phytohormones indicated that B. tabaci adults can suppress JA-dependent defenses after infestation for >72 h. The suppression of JA was correlated with the induction of salicylic acid (SA) in B. tabaci-infested leaves under laboratory and under semi-field conditions. If SA signaling was blocked, JA accumulation increased in infested leaves and B. tabaci nymphal development was delayed. These results indicate that, although JA signaling helps in mediating tomato responses against B. tabaci nymphs, B. tabaci can inhibit JA biosynthesis and its action in an SA-dependent manner.

Highlights

  • Plants have various defenses against herbivores, and some defenses are induced

  • Our data show that the reproduction and survival of B. tabaci adults were unaffected by impairment of jasmonic acid (JA) defenses or constitutive activation of JA defenses (35s::prosys; Figure 1)

  • The development of B. tabaci nymphs, was significantly accelerated by impairment of JA defenses and was substantially slowed by constitutive activation or artificial induction of JA defenses (Figure 2). These results are consistent with previous findings that impairment of JA defenses in Arabidopsis accelerates the development of B. tabaci nymphs (Zarate et al, 2007; Zhang et al, 2013b), and that activation of JA defenses in tomato slows nymphal development (SánchezHernández et al, 2006)

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Summary

Introduction

Plants have various defenses against herbivores, and some defenses are induced. Induced plant defenses include the production of antibiotic or antixenotic metabolites that directly influence herbivore performance and behavior (Bleeker et al, 2009; Luan et al, 2013), and the release of volatiles that indirectly recruit parasitoids or predators to infested plants and that thereby indirectly affect herbivores (Turlings et al, 1990; Kessler and Baldwin, 2001; Dicke et al, 2009). The jasmonic acid (JA) signaling pathway is especially important in mediating induced plant defenses against herbivores (Ament et al, 2004; Kessler et al, 2004; Thaler et al, 2012), salicylic acid (SA) and ethylene (ET) signaling pathways are important in some cases (Penninckx et al, 1998; Zhang et al, 2013b). For example, JA regulates the expression of defense-related. Manipulating Plant Defenses genes (Farmer et al, 1992) and the emission of herbivore-induced volatiles that may attract natural enemies (Ament et al, 2004). The butterfly Pieris brassicae, for example, utilizes egg-derived elicitors to inhibit the expression of JA-regulated defense genes in Arabidopsis (Bruessow et al, 2010). The leafhopper Macrosteles quadrilineatus suppresses JA defenses via an effector derived from a vectored phytoplasma, resulting in increased performance of its larvae (Sugio et al, 2011)

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