Shared weapons of blood- and plant-feeding insects: Surprising commonalities for manipulating hosts

Guiguet, Antoine; Dubreuil, Géraldine; Harris, M. O.; Appel, Heidi M.; Schultz, Jack C.; Pereira, Marcos H.; Giron, David

doi:10.1016/j.jinsphys.2015.12.006

Cited by 48 publications

(41 citation statements)

References 304 publications

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“…proteinaceous effectors, phytohormones or phytohormone analogs secreted with the saliva) with those offered by microbes, as has been observed in other plant-herbivore and plant-plant parasitic nematode interactions (e.g. Favery et al, this issue; Guiguet et al, this issue; Harris et al, 2015; Kazan and Lyons, 2014; Zhang et al, this issue; Zhao et al, this issue). Future field-based experiments such as those described by Humphrey et al (2014) and O’Connor et al (2014) will allow us to gauge the extent and relevance of these associations.…”

Section: Discussionmentioning

confidence: 88%

Pseudomonas syringae enhances herbivory by suppressing the reactive oxygen burst in Arabidopsis

Groen

Humphrey

Chevasco

et al. 2016

Journal of Insect Physiology

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Plant-herbivore interactions have evolved in the presence of plant-colonizing microbes. These microbes can have important third-party effects on herbivore ecology, as exemplified by drosophilid flies that evolved from ancestors feeding on plant-associated microbes. Leaf-mining flies in the genus Scaptomyza, which is nested within the paraphyletic genus Drosophila, show strong associations with bacteria in the genus Pseudomonas, including Pseudomonas syringae. Adult females are capable of vectoring these bacteria between plants and larvae show a preference for feeding on P. syringae-infected leaves. Here we show that Scaptomyza flava larvae can also vector P. syringae to and from feeding sites, and that they not only feed more, but also develop faster on plants previously infected with P. syringae. Our genetic and physiological data show that P. syringae enhances S. flava feeding on infected plants at least in part by suppressing anti-herbivore defenses mediated by reactive oxygen species.

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Section: Discussionmentioning

confidence: 88%

Pseudomonas syringae enhances herbivory by suppressing the reactive oxygen burst in Arabidopsis

Groen

Humphrey

Chevasco

et al. 2016

Journal of Insect Physiology

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“…The inhibition of root growth has been identified as part of the ‘third danger signal’ in plant responses to herbivory (Guiguet et al . ), but it is unknown whether this type of response can be triggered specifically by an insect endosymbiont. The influence of H. defensa on root mass represents a new function of insect endosymbionts and as a result demands future research to elucidate the mechanism.…”

Section: Discussionmentioning

confidence: 99%

“…Hamiltonella defensa has been associated with suppression of whiteflyinduced plant defences in tomato (Su et al 2015) which provides evidence of potential effectors generated by or modified by Hamiltonella defensa. The inhibition of root growth has been identified as part of the 'third danger signal' in plant responses to herbivory (Guiguet et al 2016), but it is unknown whether this type of response can be triggered specifically by an insect endosymbiont. The influence of H. defensa on root mass represents a new function of insect endosymbionts and as a result demands future research to elucidate the mechanism.…”

Section: Discussionmentioning

confidence: 99%

Plant and insect microbial symbionts alter the outcome of plant–herbivore–parasitoid interactions: implications for invaded, agricultural and natural systems

et al. 2016

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Summary Understanding how soil microbial communities influence plant interactions with other organisms, and how this varies with characteristics of the interacting organisms, is important for multiple systems. Solanum spp. are a suitable model for trophic interactions in studies of agricultural and natural systems and can also provide useful corollaries in invaded systems. This study examined the influence of soil mutualist arbuscular mycorrhizal (AM) fungi on growth of different Solanum types fed on by the potato aphid, Macrosiphum euphorbiae, in relation to the presence of the aphid facultative endosymbiont Hamiltonella defensa. Four Solanum types comprising two wild species, S. berthaultii and S. polyadenum, and two accessions of S. tuberosum, were grown with or without AM fungi and infested with one of four clonal lines of a single M. euphorbiae genotype (two with and two without H. defensa). Two experiments were conducted to (i) characterize plant responses to AM fungi and aphids and (ii) assess whether soil AM fungi could influence the success of the parasitoid wasp Aphidius ervi when attacking aphids reared on each Solanum type. In both experiments, similar patterns of plant biomass were observed in relation to AM fungal and aphid treatments. Solanum biomass depended on plant type and aphid infection with H. defensa. Plants exposed to aphids harbouring H. defensa had smaller root biomass, and therefore total plant biomass, compared to plants infested with H. defensa‐free aphids. M. euphorbiae performance varied with aphid clonal line, Solanum type and the presence of AM fungi. Parasitoid success, measured as the proportion of aphids from which a wasp emerged, was highest from aphids that had fed on plants colonized by AM fungi, although this result also varied with Solanum type and aphid clonal line. Synthesis. The presence of soil AM fungi, combined with within‐species plant and insect variation in key traits, can have subtle – but significant – effects on plant fitness and insect success. This study highlights the importance of exploring genotypic variation in plant and pest responses to soil microbiota to identify suitable biocontrol options.

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“…Because plants are sessile, many pathogens of plants use the same strategies for their transmission as the agents of vectorborne human diseases (Guiguet et al, 2016) and, for example, change the behavior of their vectors to enhance transmission from infected to healthy plants hosts (Stafford et al, 2011;Ingwell et al, 2012;Rajabaskar et al, 2014), alter the emission of volatile organic compounds (VOCs) from the infected host (Mauck et al, 2010), or enhance the nutritional quality of the infected plant for herbivores that serve as their vectors (Fang et al, 2013;Luan et al, 2013;Shi et al, 2014). One of the most intriguing examples is Cucumber mosaic virus: the bouquet of VOCs emitted by infected plants is altered, making the plants more attractive to the aphids that vector this virus, even though the nutritional quality of infected plants is lower (Mauck et al, 2010).…”

Section: "Fatal Attraction" When the Host Is A Plantmentioning

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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Shared weapons of blood- and plant-feeding insects: Surprising commonalities for manipulating hosts

Cited by 48 publications

References 304 publications

Pseudomonas syringae enhances herbivory by suppressing the reactive oxygen burst in Arabidopsis

Pseudomonas syringae enhances herbivory by suppressing the reactive oxygen burst in Arabidopsis

Plant and insect microbial symbionts alter the outcome of plant–herbivore–parasitoid interactions: implications for invaded, agricultural and natural systems

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

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