Vector and virus induce plant responses that benefit a non-vector herbivore

Belliure, Belén; Sabelis, Maurice W.; Janssen, Arne

doi:10.1016/j.baae.2009.09.004

Cited by 38 publications

(40 citation statements)

References 35 publications

(51 reference statements)

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“…The positive response of insects on virus-infected plants can extend to other insects as well. TSWV infection and/or thrip damage affects spider mites; the spider mites do better on plants inoculated with virus via thrips, but thrip damage without virus does not have a negative effect on the spider mites, as it does on the thrips, rather the spider mites do better on these plants as well (Belliure et al, 2010). Thrips infected with TSWV change their feeding behavior in comparison to uninfected thrips: males feed more, and importantly probe more in a way that does not damage the plant cell, the type of probing that is required for virus transmission.…”

Section: Transmission By Thripsmentioning

confidence: 95%

Plants, viruses and the environment: Ecology and mutualism

2015

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Since the discovery of Tobacco mosaic virus nearly 120 years ago, most studies on viruses have focused on their roles as pathogens. Virus ecology takes a different look at viruses, from the standpoint of how they affect their hosts׳ interactions with the environment. Using the framework of symbiotic relationships helps put the true nature of viruses into perspective. Plants clearly have a long history of relationships with viruses that have shaped their evolution. In wild plants viruses are common but usually asymptomatic. In experimental studies plant viruses are sometimes mutualists rather than pathogens. Virus ecology is closely tied to the ecology of their vectors, and the behavior of insects, critical for transmission of many plant viruses, is impacted by virus-plant interactions. Virulence is probable not beneficial for most host-virus interactions, hence commensal and mutualistic relationships are almost certainly common, in spite of the paucity of literature on beneficial viruses.

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Section: Transmission By Thripsmentioning

confidence: 95%

Plants, viruses and the environment: Ecology and mutualism

2015

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“…Development of Spodoptera exigua caterpillars was greater on TMV-infected tomato plants than on control plants [12]. Pepper plants infected with Tomato spotted wilt virus (TSWV) harbored greater populations of a non-vector arthropod, the twospotted spider mite, Tetranychusurticae Koch (Acari: Tetranychidae) than uninfected plants [13]. On the other hand, TSWV infection reduced fecundity and longevity of whiteflies on TSWV-infected pepper plants [14].…”

Section: Introductionmentioning

confidence: 99%

Tomato Spotted Wilt Virus Benefits a Non-Vector Arthropod, Tetranychus Urticae, by Modulating Different Plant Responses in Tomato

et al. 2013

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The interaction between plant viruses and non-vector arthropod herbivores is poorly understood. However, there is accumulating evidence that plant viruses can impact fitness of non-vector herbivores. In this study, we used oligonucleotide microarrays, phytohormone, and total free amino acid analyses to characterize the molecular mechanisms underlying the interaction between Tomato spotted wilt virus (TSWV) and a non-vector arthropod, twospotted spider mite ( Tetranychusurticae ), on tomato plants, Solanum lycopersicum . Twospotted spider mites showed increased preference for and fecundity on TSWV-infected plants compared to mock-inoculated plants. Transcriptome profiles of TSWV-infected plants indicated significant up-regulation of salicylic acid (SA)-related genes, but no apparent down-regulation of jasmonic acid (JA)-related genes which could potentially confer induced resistance against TSM. This suggests that there was no antagonistic crosstalk between the signaling pathways to influence the interaction between TSWV and spider mites. In fact, SA- and JA-related genes were up-regulated when plants were challenged with both TSWV and the herbivore. TSWV infection resulted in down-regulation of cell wall-related genes and photosynthesis-associated genes, which may contribute to host plant susceptibility. There was a three-fold increase in total free amino acid content in virus-infected plants compared to mock-inoculated plants. Total free amino acid content is critical for arthropod nutrition and may, in part, explain the apparent positive indirect effect of TSWV on spider mites. Taken together, these data suggest that the mechanism(s) of increased host suitability of TSWV-infected plants to non-vector herbivores is complex and likely involves several plant biochemical processes.

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“…(Mouritsen and Poulin, 2003) What are the consequences for plant viruses when a virus-induced enhancement in phloem quality and its "public advertisement" via odors are exploited by non-vector insects that have similar nutritional requirements to those of the vectors? (Belliure et al, 2010;Mauck et al, 2014b) Parasites might reduce these costs by limiting the manipulation of their intermediate host to the developmental phase in which they are infectious to their definitive host (Dianne et al, 2011) but still, the net success of this strategy depends on the ratio of hosts to non-hosts in the current environment. The hijacking of manipulation effects by other species (Mouritsen and Poulin, 2003) can potentially have strong negative feedback effects on the parasite.…”

Section: Why Don't All Parasites Manipulate?mentioning

confidence: 99%

“…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.

106

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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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Vector and virus induce plant responses that benefit a non-vector herbivore

Cited by 38 publications

References 35 publications

Plants, viruses and the environment: Ecology and mutualism

Plants, viruses and the environment: Ecology and mutualism

Tomato Spotted Wilt Virus Benefits a Non-Vector Arthropod, Tetranychus Urticae, by Modulating Different Plant Responses in Tomato

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

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