Plant Virus Differentially Alters the Plant's Defense Response to Its Closely Related Vectors

Shi, Xiaolu; Pan, Huipeng; Xie, Wen; Wu, Qingjun; Wang, Shaoli; Liu, Yang; Fang, Yong; Chen, Gong; Gao, Xiwu; Zhang, Youjun

doi:10.1371/journal.pone.0083520

Cited by 41 publications

(52 citation statements)

References 62 publications

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“…A previous study demonstrated that exogenous SA application led to increased SA levels in tomato plants (Shi et al . ). Increased titres of SA ingested by whiteflies, or changes in phloem resulting from increased SA, potentially affect within‐host symbiont titres.…”

Section: Methodsmentioning

confidence: 97%

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

et al. 2015

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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.

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Section: Methodsmentioning

confidence: 97%

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

et al. 2015

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“…Our latest study showed that SA content was always higher in leaves infested with viruliferous B than with viruliferous Q5. Furthermore, the relative gene expression associated with SA signaling was increased by the feeding of viruliferous B but not by the feeding of viruliferous Q5. Zhang et al (2012)27 demonstrated that co-infection of the begomovirus tomato yellow leaf curl China virus (TYLCCNV) and its betasatellite can repress JA-regulated defenses of tobacco against invasive whiteflies and accelerate population increases of the insects.…”

mentioning

confidence: 85%

Bemisia tabaci Q carrying tomato yellow leaf curl virus strongly suppresses host plant defenses

Shi

Pan

Zhang

et al. 2014

Sci Rep

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The concurrence of tomato yellow leaf curl virus (TYLCV) with the spread of its vector Bemisia tabaci Q rather than B in China suggests a more mutualistic relationship between TYLCV and Q. Here, we investigated the hypothesis that viruliferous B and Q have different effects on plant defenses. We found the fecundity of nonviruliferous B, nonviruliferous Q, viruliferous Q and viruliferous B was 11.080, 12.060, 10.760, and 11.220 respectively on plants previously attacked by the other biotype, however, on their respective noninfested control leaves fecundity was 12.000, 10.880, 9.760, and 8.020 respectively. Only viruliferous B had higher fecundity on viruliferous Q-infested plants than on control plants. The longevity of viruliferous B showed the same phenomenon. At 1 d infestion, the jasmonic acid content in leaves noninfested and in leaves infested with nonviruliferous B, nonviruliferous Q, viruliferous B and viruliferous Q was 407.000, 281.333, 301.333, 266.667 and 134.000 ng/g FW, respectively. The JA content was lowest in viruliferous Q-infested leaves. The proteinase inhibitor activity and expression of JA-related upstream gene LOX and downstream gene PI II showed the same trend. The substantial suppression of host defenses by Q carrying TYLCV probably enhances the spread of Q and TYLCV in China.

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“…Indeed, differing persistence times might be a major explanation for the observation that manipulation effects are more frequently reported for intermediate than for final hosts, at least as long as all hosts are animals (Holmes and Bethel, 1972). Plant pathogens, by contrast, require mobile vectors for their dispersal among their immobile final hosts and, therefore, frequently manipulate the quality of their host plant for the vectors (Belliure et al, 2010;Mauck et al, 2010Mauck et al, , 2014aLuan et al, 2013;Shi et al, 2013) as well as the feeding decisions that are taken by their vectors (Stafford et al, 2011;Ingwell et al, 2012;Mann et al, 2012;Fang et al, 2013;Rajabaskar et al, 2014). These changes can be very fine-tuned: for example, plant viruses with a persistent mode of transmission require vectors to feed for a prolonged period of time on infected hosts and, thus, usually tend to improve the quality of the host plants for the vectors.…”

Section: Why Don't All Parasites Manipulate?mentioning

confidence: 99%

Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts

Heil

2016

Front. Ecol. Evol.

109

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Parasites must overcome host immunity and change hosts for dispersal. Therefore, seemingly odd behaviors of parasitized animals, like those exhibited by "Zombie ants" or the "fatal attraction" of mammals to their predators, have been explained as the extended phenotype of parasites that manipulate their hosts for transmission enhancement. Manipulation has evolved in all major phylogenetic lineages of parasites but is not ubiquitous. In fact, the real frequency and relevance of manipulation is still matter of debate. Here, I highlight some of the most pertinent questions that arise if we aim at a broader understanding of the ecological relevance and evolutionary trajectory of manipulating parasites. Why are more parasites with a trophic mode of transmission manipulating their host than horizontally transmitted parasites? Why are the causal agents of sexually transmitted diseases (STDs) so rarely reported to manipulate their host? Why do parasites of animals usually manipulate their intermediate host, whereas many pathogens of plants manipulate their final host and then cause a "fatal attraction" of herbivores to the already infected plant? How can we distinguish manipulation effects from adaptive host responses to parasitization? Does manipulation cause a cost to certain parasites that can select against the evolution of manipulation? More emphasis should be put on direct comparisons among parasites of animals, plants, and humans. Manipulation for transmission enhancement should be studied in concert with manipulation for host immunity suppression, the molecular mechanisms that control the manipulation effect need to be deciphered, and we should test for alternative explanations for the observed phenotypic changes. Finally, we should quantify transmission rates and net fitness for manipulating and non-manipulating parasites, in ecologically realistic setups, to identify the forces that select against the evolution of manipulation. Ultimately, parasite net fitness represents the relevant outcome of any manipulation effect.Keywords: immunity, malaria, partner manipulation, pathogen, plant-enemy interaction, STDs, toxoplasmosis "FATAL ATTRACTION" AND MANIPULATING PARASITES Parasites represent a ubiquitous aspect in the life of multicellular organisms (Wood and Johnson, 2015) and most, if not all, of us have experienced how strongly an infection can interfere with our normal activities and well-being. Therefore, it might not appear to be too surprising when parasitized hosts exhibit behavioral alterations (see Glossary) as compared to healthy conspecifics.

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Plant Virus Differentially Alters the Plant's Defense Response to Its Closely Related Vectors

Cited by 41 publications

References 62 publications

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

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

Bemisia tabaci Q carrying tomato yellow leaf curl virus strongly suppresses host plant defenses

Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts

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