Microbial Symbionts in Insects Influence Down-Regulation of Defense Genes in Maize

Barr, Kelli L.; Hearne, Leonard B.; Briesacher, Sandra; Clark, Thomas L.; Davis, Georgia

doi:10.1371/journal.pone.0011339

Cited by 118 publications

(117 citation statements)

References 48 publications

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“…As this sequence of events is specifically triggered by disruption of the symbiosis rather than anthelminthic chemotherapy per se, wOo could be considered a defensive mutualist. This phenotype is now well recognized for Wolbachia in arthropods, and a precedent involving manipulation of the immune system of a third party exists for an insect pest of maize (Barr et al 2010). Moreover, in L. sigmodontis, successful migration of the infective larvae is also associated with immunomodulation of mammalian effector cells by Wolbachia (Specht et al 2011).…”

Section: Discussionmentioning

confidence: 96%

Analysis of gene expression from theWolbachiagenome of a filarial nematode supports both metabolic and defensive roles within the symbiosis

et al. 2012

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The a-proteobacterium Wolbachia is probably the most prevalent, vertically transmitted symbiont on Earth. In contrast with its wide distribution in arthropods, Wolbachia is restricted to one family of animal-parasitic nematodes, the Onchocercidae. This includes filarial pathogens such as Onchocerca volvulus, the cause of human onchocerciasis, or river blindness. The symbiosis between filariae and Wolbachia is obligate, although the basis of this dependency is not fully understood. Previous studies suggested that Wolbachia may provision metabolites (e.g., haem, riboflavin, and nucleotides) and/or contribute to immune defense. Importantly, Wolbachia is restricted to somatic tissues in adult male worms, whereas females also harbor bacteria in the germline. We sought to characterize the nature of the symbiosis between Wolbachia and O. ochengi, a bovine parasite representing the closest relative of O. volvulus. First, we sequenced the complete genome of Wolbachia strain wOo, which revealed an inability to synthesize riboflavin de novo. Using RNA-seq, we also generated endobacterial transcriptomes from male soma and female germline. In the soma, transcripts for membrane transport and respiration were up-regulated, while the gonad exhibited enrichment for DNA replication and translation. The most abundant Wolbachia proteins, as determined by geLC-MS, included ligands for mammalian Toll-like receptors. Enzymes involved in nucleotide synthesis were dominant among metabolism-related proteins, whereas the haem biosynthetic pathway was poorly represented. We conclude that Wolbachia may have a mitochondrion-like function in the soma, generating ATP for its host. Moreover, the abundance of immunogenic proteins in wOo suggests a role in diverting the immune system toward an ineffective antibacterial response.

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Section: Discussionmentioning

confidence: 96%

Analysis of gene expression from theWolbachiagenome of a filarial nematode supports both metabolic and defensive roles within the symbiosis

et al. 2012

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“…In maize roots, larvae of the western corn rootworm (D. virgifera virgifera) inhibited the induction of defense gene expression, which was not observed when insects were treated with the antibiotic tetracycline (13). The authors reported that larvae with Wolbachia infection suppressed plant-defense-related gene transcripts, although the effect of suppression on insect performance was not examined.…”

Section: Discussionmentioning

confidence: 99%

“…In addition, symbionts can influence plant-insect interactions (12,13). Symbiotic bacteria may allow some herbivores to expand the range of available host plants.…”

mentioning

confidence: 99%

“…Wolbachia-infected leaf miners (Phyllonorycter blancardella) elicit a green-island phenotype in apple, preserving photosynthetically active tissues in senescent leaves, and in turn, increase leaf miner performance (12). In maize roots, Wolbachia in western corn rootworms (Diabrotica virgifera virgifera) may suppress defense gene expression (13), although this is disputed (15). Despite a few examples, the role of insect symbionts as elicitors or effectors in modifying plant-insect interactions has received scant attention.…”

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confidence: 99%

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Herbivore exploits orally secreted bacteria to suppress plant defenses

Chung¹,

Rosa²,

Scully

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

381

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Significance The role of herbivore-associated microbes in modifying plant defenses has received scant attention. The Colorado potato beetle secretes symbiotic bacteria to wounds to manipulate plant defenses. The bacteria elicit salicylic acid (SA)-regulated defenses, and because SA signaling often negatively cross-talks with jasmonate signaling, plants are unable to fully activate their jasmonate-mediated resistance against the herbivore. From the plants’ perspective, they recognize herbivores not as such, but as microbial threats. We identified the specific bacteria from the beetle secretions and also characterized one of the bacterial effectors responsible for defense suppression. This clever, deceptive strategy for suppressing defenses has not been previously documented. Our results add a significant, unique concept to plant–insect interactions and how herbivores hijack plant defense signaling.

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“…Recent studies in the western corn rootworm ( Diabrotica virgifera virgifera ) and the tomato psyllid ( Bactericera cockerelli ) have found higher concentrations of endosymbionts correlate with reduced expression of plant defensive pathways (Barr et al. 2010; Casteel et al. 2012).…”

Section: Discussionmentioning

confidence: 99%

Stress‐induced changes in abundance differ among obligate and facultative endosymbionts of the soybean aphid

Enders

Miller

2016

Ecology and Evolution

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Bacterial endosymbionts can drive evolutionary novelty by conferring adaptive benefits under adverse environmental conditions. Among aphid species there is growing evidence that symbionts influence tolerance to various forms of stress. However, the extent to which stress inflicted on the aphid host has cascading effects on symbiont community dynamics remains poorly understood. Here we simultaneously quantified the effect of host‐plant induced and xenobiotic stress on soybean aphid (Aphis glycines) fitness and relative abundance of its three bacterial symbionts. Exposure to soybean defensive stress (Rag1 gene) and a neurotoxic insecticide (thiamethoxam) substantially reduced aphid composite fitness (survival × reproduction) by 74 ± 10% and 92 ± 2%, respectively, which in turn induced distinctive changes in the endosymbiont microbiota. When challenged by host‐plant defenses a 1.4‐fold reduction in abundance of the obligate symbiont Buchnera was observed across four aphid clonal lines. Among facultative symbionts of Rag1‐stressed aphids, Wolbachia abundance increased twofold and Arsenophonus decreased 1.5‐fold. A similar pattern was observed under xenobiotic stress, with Buchnera and Arsenophonus titers decreasing (1.3‐fold) and Wolbachia increasing (1.5‐fold). Furthermore, variation in aphid virulence to Rag1 was positively correlated with changes in Arsenophonus titers, but not Wolbachia or Buchnera. A single Arsenophonus multi‐locus genotype was found among aphid clonal lines, indicating strain diversity is not primarily responsible for correlated host‐symbiont stress levels. Overall, our results demonstrate the nature of aphid symbioses can significantly affect the outcome of interactions under stress and suggests general changes in the microbiome can occur across multiple stress types.

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Microbial Symbionts in Insects Influence Down-Regulation of Defense Genes in Maize

Cited by 118 publications

References 48 publications

Analysis of gene expression from theWolbachiagenome of a filarial nematode supports both metabolic and defensive roles within the symbiosis

Analysis of gene expression from theWolbachiagenome of a filarial nematode supports both metabolic and defensive roles within the symbiosis

Herbivore exploits orally secreted bacteria to suppress plant defenses

Stress‐induced changes in abundance differ among obligate and facultative endosymbionts of the soybean aphid

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