The whitefly‐associated facultative symbiont Hamiltonella defensa suppresses induced plant defences in tomato

Abstract

Summary 1.Maternally inherited bacterial symbionts are present in many, if not most, insect species. While there is rapidly accumulating evidence that facultative, heritable symbionts often protect insect hosts from natural enemies, there have been few clear examples where facultative symbionts mediate herbivore-plant interactions. 2. The phloem-feeding whitefly, Bemisia tabaci, is a major agricultural pest that frequently harbours facultative symbionts, including Hamiltonella defensa. While H. defensa and other facultative symbionts have been shown to improve whitefly performance on particular food plants, no direct and specific roles for symbiont-mediated interactions with food plants have been identified. 3. Here, we conducted a series of assays to determine whether infection with H. defensa improved whitefly performance on tomato (Solanum lycopersicum) and whether this benefit was associated with symbiont effects on induced plant defences. Finally, we tested whether impacts on induced defences involved in the modulation of a salivary factor. 4. The downregulation of plant defences was associated with increased whitefly fecundity and survival. Feeding by H. defensa-infected whiteflies suppressed JA and JA-related anti-herbivore-induced defences in tomato relative to uninfected controls. That saliva-only treatments of damaged tomato leaves from H. defensa-infected whiteflies suppressed induced plant defences compared to saliva from uninfected controls, suggesting that elicitors in saliva were responsible. Characterization of the putative salivary factor(s) revealed they are likely small (< 3-kDa) and nonproteinaceous. 5. Interestingly, suppression of defences was not observed in SA-deficient NahG plants, indicating that suppression of JA-regulated defences depends on the SA signalling pathway. This finding reveals an intriguing example of the crosstalk between SA and JA signalling pathways and suggests that infection with facultative symbionts can result in the manipulation of induced plant defences to the benefit of the insect host and heritable symbiont. 6. Our results show that the bacterial symbiont H. defensa mediates whitefly-plant interactions by suppressing induced plant defences in tomato. This finding is among the first showing a direct role for facultative symbionts in mediating plant-herbivore interactions and demonstrates a novel tactic for insect herbivores to circumvent plant defences. Symbiont-mediated suppression of plant defences may enhance the deleterious effects of insect pests feeding on important crops.

Is there a role for symbiotic bacteria in plant virus transmission by insects?

“…In the H + strain, the performance benefit was shown to be the result of suppression of the anti-herbivore jasmonic acid plant defense pathway [107 ], data that provide unambiguous support for the hypothesis that symbiotic bacteria influence the plantinsect relationship. Excitingly, suppression of the jasmonic acid pathway was shown to be dependent on cross-talk with the anti-microbial salicylic acid signaling pathway [107 ]. Taken together, these data in the context of this simple model may explain how the Q biotype rapidly spread in China.…”

“…Tying this story back to the vector manipulation hypothesis, the Q biotype, which harbors Hamiltonella in China performs better on TYLCVinfected plants than the B biotype, which does not harbor Hamiltonella in China [100]. In the H + strain, the performance benefit was shown to be the result of suppression of the anti-herbivore jasmonic acid plant defense pathway [107 ], data that provide unambiguous support for the hypothesis that symbiotic bacteria influence the plantinsect relationship. Excitingly, suppression of the jasmonic acid pathway was shown to be dependent on cross-talk with the anti-microbial salicylic acid signaling pathway [107 ].…”

Transient Expression of Whitefly Effectors in Nicotiana benthamiana Leaves Activates Systemic Immunity Against the Leaf Pathogen Pseudomonas syringae and Soil-Borne Pathogen Ralstonia solanacearum

“…The identification of 6A10 as a large subunit ribosomal RNA of B. tabaci deserves further study. There are many examples of the secretion of effector proteins that modulate plant immunity in saliva from hemipterans including aphids and whitefly Will et al, 2013;Sharma et al, 2014;Su et al, 2015;Peng et al, 2016;Villarroel et al, 2016). For instance, the effector proteins C002, Mp1, and Mp2 from aphid promote fecundity, whereas Mp10 and Mp42 decrease fecundity (Bos et al, 2010;Pitino and Hogenhout, 2013).…”

“…Besides protein effectors, non-protein salivary factors can also act as effectors (Su et al, 2015). Bacterial rRNAs and plant DNA were recently shown to elicit SAR (Bhat and Ryu, 2016;Lee et al, 2016).…”

“…Our understanding of insect-mediated changes in the activation of plant immune responses is limited due to the lack of information on whitefly determinants that suppress or induce plant immune responses. To fill this knowledge gap, most studies on insect factors that modulate plant immunity have focused on the suppression of insect resistance rather than the induction of plant resistance responses such as systemic acquired resistance (SAR) (Kempema et al, 2007;Cooper et al, 2010;Su et al, 2012Su et al, , 2015. The effector proteins from pathogenic bacteria and fungi induce and suppress plant immunity via a well-known process described by the zigzag theory (Jones and Dangl, 2006).…”