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.

BackgroundRelatively little is known about the genomic basis and evolution of wood-feeding in beetles. We undertook genome sequencing and annotation, gene expression assays, studies of plant cell wall degrading enzymes, and other functional and comparative studies of the Asian longhorned beetle, Anoplophora glabripennis, a globally significant invasive species capable of inflicting severe feeding damage on many important tree species. Complementary studies of genes encoding enzymes involved in digestion of woody plant tissues or detoxification of plant allelochemicals were undertaken with the genomes of 14 additional insects, including the newly sequenced emerald ash borer and bull-headed dung beetle.ResultsThe Asian longhorned beetle genome encodes a uniquely diverse arsenal of enzymes that can degrade the main polysaccharide networks in plant cell walls, detoxify plant allelochemicals, and otherwise facilitate feeding on woody plants. It has the metabolic plasticity needed to feed on diverse plant species, contributing to its highly invasive nature. Large expansions of chemosensory genes involved in the reception of pheromones and plant kairomones are consistent with the complexity of chemical cues it uses to find host plants and mates.ConclusionsAmplification and functional divergence of genes associated with specialized feeding on plants, including genes originally obtained via horizontal gene transfer from fungi and bacteria, contributed to the addition, expansion, and enhancement of the metabolic repertoire of the Asian longhorned beetle, certain other phytophagous beetles, and to a lesser degree, other phytophagous insects. Our results thus begin to establish a genomic basis for the evolutionary success of beetles on plants.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-1088-8) contains supplementary material, which is available to authorized users.

Manipulation of host behavior by parasites and pathogens has been widely observed, but the basis for these behaviors has remained elusive. Gypsy moths infected by a baculovirus climb to the top of trees to die, liquefy, and "rain" virus on the foliage below to infect new hosts. The viral gene that manipulates climbing behavior of the host was identified, providing evidence of a genetic basis for the extended phenotype.

The aromatic polymer lignin protects plants from most forms of microbial attack. Despite the fact that a significant fraction of all lignocellulose degraded passes through arthropod guts, the fate of lignin in these systems is not known. Using tetramethylammonium hydroxide thermochemolysis, we show lignin degradation by two insect species, the Asian longhorned beetle (Anoplophora glabripennis) and the Pacific dampwood termite (Zootermopsis angusticollis). In both the beetle and termite, significant levels of propyl side-chain oxidation (depolymerization) and demethylation of ring methoxyl groups is detected; for the termite, ring hydroxylation is also observed. In addition, culture-independent fungal gut community analysis of A. glabripennis identified a single species of fungus in the Fusarium solani/Nectria haematococca species complex. This is a soft-rot fungus that may be contributing to wood degradation. These results transform our understanding of lignin degradation by wood-feeding insects.Asian longhorned beetle ͉ Pacific dampwood termite ͉ TMAH thermochemolysis ͉ Anoplophora glabripennis ͉ Zootermopsis angusticollis L ignin plays a central role in carbon cycling on Earth. Its heterogeneous structure imparts plants with structural rigidity and also serves to protect cellulose and hemicellulose from degradation (1). Most of what is known about lignin biodegradation is from pure culture studies with filamentous basidiomycete fungi, known as white-rot and brown-rot decay. Although both white-rot and brown-rot fungal degradation have been characterized, much more is known about the white-rot system (2, 3). White-rot fungi simultaneously degrade the three major components of the plant cell wall: lignin, cellulose, and hemicellulose. Analysis of white-rot-degraded wood shows that the reactions in lignin: (i) are oxidative, (ii) involve demethylation (or demethoxylation), (iii) include side-chain oxidation at C ␣ , and (iv) involve propyl side-chain cleavage between C ␣ and C ␤ (Fig. 1) (4). In contrast to white-rot fungi, brown-rot fungi are able to circumvent the lignin barrier, removing the hemicellulose and cellulose with only minor modification to the lignin. Consequently, lignin remains a major component of the degraded plant cell wall (5). The remaining lignin is demethylated on aryl methoxy groups and contains a greater number of ring hydroxyl groups (6).Little is known about lignin degradation in complex ecosystems, such as insect guts, where a consortium of microbes may be involved in degradation rather than just a single species. Although cellulose degradation in insect guts is well documented (7,8), the fate of lignin has not clearly been demonstrated (9, 10), and it is widely accepted that insect gut systems do not have the capacity to degrade lignin (10). Although the majority of previous reports suggest that many wood-feeding insects overcome the lignin barrier by feeding on predegraded wood (11) or through exosymbiotic relationships with wood-degrading fungi (12, 13), there are species of insects...

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