Gut-Associated Bacteria of Helicoverpa zea Indirectly Trigger Plant Defenses in Maize
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Insect-associated microbes can contribute to the physiological and ecological functions of insects. Despite a few examples in beetles and piercing-sucking insects, the varied mechanisms of how insect-associated bacteria mediate plant-insect interactions are still not fully understood. The polyphagous herbivore Helicoverpa zea is a major agricultural pest that harbors certain microbes in their digestive systems. Enterobacter ludwigii is one of the gut-associated bacteria identified from field-collected caterpillars, and it has been shown to indirectly induce defenses in the dicot plant tomato by triggering the biosynthesis of salivary elicitors, but there are no clear mechanisms to show how gut microbes alter these salivary cues and how a different host plant responds to these inducible elicitors. Here, we conducted a series of assays to determine whether infection with E. ludwigii affects H. zea larval growth, immunity, and salivary responses and thus influences induced defenses of maize to herbivory. Inoculating lab-reared caterpillars with E. ludwigii, did not significantly affect the growth of caterpillars, but two immunity-related genes glucose oxidase (GOX) and lysozyme (LYZ) were more highly expressed in both salivary glands and midguts compared with MgCl2 solution-treated caterpillars. Oral elicitors were evaluated for their role in triggering maize-specific defense responses. Our results show that saliva and its main component protein glucose oxidase (GOX) from E. ludwigii-inoculated caterpillars played a role in inducing maize anti-herbivore responses. These findings provide a novel concept that introducing bacteria to an herbivore may be an important approach to pest control through alteration of insect immune responses and thus indirect induction of plant resistance.
KeywordsGut bacteria Induced defense Symbiosis Microbiome Immunity Saliva Glucose oxidase
Many thanks to two anonymous reviewers and Michelle Peiffer and Rongrong Xue for providing very constructive comments for the manuscript. This research was supported by the National Science Foundation Grant (IOS-1256326), United States Department of Agriculture (AFRI 2017-67013-26596) awarded to G.W.F., C.R. and K.H., Research Project of Department of Education of Fujian for Young and Middle-age teachers (JAT170155), Talent Programs of Fujian Agriculture and Forestry University (KXJQ17013), Natural Science Foundation of Fujian Province (2018 J01712) and the National Natural Science Foundation of China (31701855) awarded to J.W.
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