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Gut-Associated Bacteria of Helicoverpa zea Indirectly Trigger Plant Defenses in Maize

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A Correction to this article was published on 13 June 2018

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Abstract

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.

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  • 13 June 2018

    The original version of this article unfortunately contained a mistake. Fig. 3 and Fig. 4a were identical and the original version of Fig. 4a had been accidentally replaced.

References

  • Acevedo FE, Rivera-Vega LJ, Chung SH, Ray S, Felton GW (2015) Cues from chewing insects - the intersection of DAMPs, HAMPs, MAMPs and effectors. Curr Opin Plant Biol 26:80–86

    Article  PubMed  CAS  Google Scholar 

  • Acevedo FE, Peiffer M, Tan CW, Stanley BA, Stanley A, Wang J, Jones AG, Hoover K, Rosa C, Luthe D, Felton GW (2017) Fall armyworm-associated gut bacteria modulate plant defense responses. Mol Plant-Microbe Interact 30:127–137

    Article  PubMed  CAS  Google Scholar 

  • Akman GE, Douglas AE (2009) Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proc R Soc B Biol Sci 276:987–991

    Article  CAS  Google Scholar 

  • Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949

    Article  CAS  Google Scholar 

  • Bede JC, Musser RO, Felton GW, Korth KL (2006) Caterpillar herbivory and salivary enzymes decrease transcript levels of Medicago truncatula genes encoding early enzymes in terpenoid biosynthesis. Plant Mol Biol 60:519–531

    Article  PubMed  CAS  Google Scholar 

  • Celorio-Mancera ML, Ytterberg AJ, Rutishauser D, Janz N, Zubarev RA (2015) Effect of host plant and immune challenge on the levels of chemosensory and odorant-binding proteins in caterpillar salivary glands. Insect Biochem Mol Biol 61:34–45

    Article  CAS  Google Scholar 

  • Chung SH, Rosa C, Scully ED, Peiffer M, Tooker JF, Hoover K, Luthe DS, Felton GW (2013) Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc Natl Acad Sci U S A 110:15728–15733

    Article  PubMed  PubMed Central  Google Scholar 

  • Clark EL, Karley AJ, Hubbard SF (2010) Insect endosymbionts: manipulators of insect herbivore trophic interactions? Protoplasma 244:25–51

    Article  PubMed  Google Scholar 

  • Diezel C, Von CC D, Gaquerel E, Baldwin IT (2009) Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiol 150:1576–1586

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dow M, Newman M, Roepenack EV (2000) The induction and modulation of plant defense responses by bacterial lipopolysaccharides. Annu Rev Phytopathol 38:241–261

    Article  PubMed  CAS  Google Scholar 

  • Eichenseer H, Mathews M, Bi JL, Murphy JB, Felton GW (1999) Salivary glucose oxidase: multifunctional roles for Helicoverpa zea? Arch Insect Biochem Physiol 109:99–109

    Article  Google Scholar 

  • Felton GW, Chung SH, Hernandez MGE, Louis J, Peiffer M, Tian D (2014) Herbivore oral secretions are the first line of protection against plant-induced defences. Pages 37–76 in Annual Plant Reviews, C. Voelckel and G. Jander, eds. Wiley

  • Hammer TJ, Janzen DH, Hallwachs W, Jaffe SP, Fierer N (2017) Caterpillars lack a resident gut microbiome. Proc Natl Acad Sci U S A 114:9641–9646

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hoffmann WA, Poorter H (2002) Avoiding bias in calculations of relative growth rate. Ann Bot 90:37–42

    Article  PubMed  PubMed Central  Google Scholar 

  • Hultmark D (1996) Insect lysozymes. In: Jollès P (ed) Lysozymes: model enzymes in biochemistry and biology. Birkhauser Verlag Basel, Switzerland, pp 87–102

    Chapter  Google Scholar 

  • Kohl KD, Dearing MD (2012) Experience matters: prior exposure to plant toxins enhances diversity of gut microbes in herbivores. Ecol Lett 15:1008–1015

    Article  PubMed  Google Scholar 

  • Kwakman PHS, te Velde AA, de Boer L, Speijer D, Vandenbroucke-Grauls CMJE, Zaat SAJ (2010) How honey kills bacteria. FASEB J 24:2576–2582

    Article  PubMed  CAS  Google Scholar 

  • Lemos FJ, Terra WR (1991) Digestion of bacteria and the role of midgut lysozyme in some insect larvae. Comp Biochem Physiol B 100:265–268

    Article  PubMed  CAS  Google Scholar 

  • Liu F, Cui L, Cox-Foster D, Felton GW (2004) Characterization of a salivary lysozyme in larval Helicoverpa zea. J Chem Ecol 30:2439–2457

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Louis J, Peiffer M, Ray S, Luthe DS, Felton GW (2013) Rapid report host-specific salivary elicitor (s) of European corn borer induce defenses in tomato and maize. New Phytol 199:66–73

    Article  PubMed  CAS  Google Scholar 

  • Mason CJ, Couture JJ, Raffa KF(2014) Plant-associated bacteria degrade defense chemicals and reduce their adverse effects on an insect defoliator. Oecologia 175:901–910

    Article  PubMed  Google Scholar 

  • Mohan S, Ma PW, Williams WP, Luthe DS (2008) A naturally occurring plant cysteine protease possesses remarkable toxicity against insect pests and synergizes Bacillus thuringiensis toxin. PLoS One 3:e1786

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moran NA, Russell JA, Koga R, Fukatsu T (2005) Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Appl Environ Microbiol 71:3302–3310

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy B, Felton GW (2002) Herbivory: caterpillar saliva beats plant defences. Nature 416:599–600

    Article  PubMed  CAS  Google Scholar 

  • Musser RO, Kwon HS, Williams SA, White JC, Romano MA, Holt SM, Bradbury S, Brown JK, Felton GW (2005) Evidence that caterpillar labial saliva suppresses infectivity of potential bacterial pathogens. Arch Insect Biochem Physiol 58:138–144

    Article  PubMed  CAS  Google Scholar 

  • Ohashi K, Natori S, Kubo T (1999) Expression of amylase and glucose oxidase in the hypopharyngeal gland with an age-dependent role change of the worker honeybee (Apis mellifera L.). Eur J Biochem 265:127–133

    Article  PubMed  CAS  Google Scholar 

  • Peiffer M, Felton GW (2005) The host plant as a factor in the synthesis and secretion of salivary glucose oxidase in larval Helicoverpa zea. Arch Insect Biochem Physiol 58:106–113

    Article  PubMed  CAS  Google Scholar 

  • Peiffer M, Felton GW (2009) Do caterpillars secrete “oral secretions”? J Chem Ecol 35:326–335

    Article  PubMed  CAS  Google Scholar 

  • Qi J, Sun G, Wang L, Zhao C, Hettenhausen C, Schuman MC, Baldwin IT, Li J, Song J, Liu Z, Xu G, Lu X, Wu J (2016) Oral secretions from Mythimna separata insects specifically induce defence responses in maize as revealed by high-dimensional biological data. Plant Cell Environ 39:1749–1766

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ray S, Gaffor I, Acevedo FE, Helms A, Chuang WP, Tooker J, Felton GW, Luthe DS (2015) Maize plants recognize herbivore-associated cues from caterpillar frass. J Chem Ecol 41:781–792

    Article  PubMed  CAS  Google Scholar 

  • Ray S, Basu S, Rivera-Vega LJ, Acevedo FE, Louis J, Felton GW, Luthe DS (2016) Lessons from the far end: Caterpillar frass-induced defenses in maize, rice, cabbage, and tomato. J Chem Ecol 42:1130–1141

    Article  PubMed  CAS  Google Scholar 

  • Rivera-Vega LJ, Acevedo FE, Felton GW (2017) Genomics of Lepidoptera saliva reveals function in herbivory. Curr Opin Insect Sci 19:61–69

    Article  PubMed  Google Scholar 

  • Schittko U, Preston CA, Baldwin IT (2000) Eating the evidence? Manduca sexta larvae cannot disrupt specific jasmonate induction in Nicotiana attenuata by rapid consumption. Planta 210:343–346

    Article  PubMed  CAS  Google Scholar 

  • Schmelz EA (2015) Impacts of insect oral secretions on defoliation-induced plant defense. Curr Opin Insect Sci 9:7–15

    Article  Google Scholar 

  • Staudacher H, Kaltenpoth M, Breeuwer JAJ, Menken SB, Heckel DG, Groot AT (2016) Variability of bacterial communities in the moth Heliothis virescens indicates transient association with the host. PLoS One 11:e0154514

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tang Q, Hu Y, Kang L, Wang CZ (2012a) Archives of insect biochemistry and physiology characterization of glucose-induced glucose oxidase gene and protein expression in Helicoverpa armigera larvae. Arch Insect Biochem Physiol 79:104–119

    Article  PubMed  CAS  Google Scholar 

  • Tang X, Freitak D, Vogel H, Ping L, Shao Y, Cordero EA, Andersen G, Westermann M, Heckel D, Boland W (2012b) Complexity and variability of gut commensal microbiota in polyphagous lepidopteran larvae. PLoS One 7:e36978

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tian D, Peiffer M, Shoemaker E, Tooker J, Haubruge E, Francis F, Luthe DS, Felton GW (2012) Salivary glucose oxidase from caterpillars mediates the induction of rapid and delayed-induced defenses in the tomato plant. PLoS One 7:e36168

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang J, Peiffer M, Rosa C, Zeng R, Felton GW (2017) Helicoverpa zea gut-associated bacteria indirectly induce defenses in tomato through mediating salivary elicitor(s). New Phytol 214:1294–1306

    Article  PubMed  CAS  Google Scholar 

  • Wu S, Peiffer M, Luthe DS, Felton GW (2012) ATP hydrolyzing salivary enzymes of caterpillars suppress plant defenses. PLoS One 7:e41947

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xiang H, Wei G, Jia S, Huang J, Miao X, Zhou Z, Zhao L, Huang YP (2006) Microbial communities in the larval midgut of laboratory and field populations of cotton bollworm ( Helicoverpa armigera ). Can J Microbiol 52:1085–1092

    Article  PubMed  CAS  Google Scholar 

  • Zhu F, Poelman EH, Dicke M (2015) Insect herbivore-associated organisms affect plant responses to herbivory. New Phytol 204:315–321

    Article  Google Scholar 

  • Zong N, Wang C (2004) Induction of nicotine in tobacco by herbivory and its relation to glucose oxidase activity in the labial gland of three noctuid caterpillars. Chin Sci Bull 49:1596–1601

    CAS  Google Scholar 

Download references

Acknowledgments

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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Correspondence to Jie Wang.

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The original version of this article was revised: The original version of this article unfortunately contained a mistake. Figure 3 and figure 4a were identical and the original version of figure 4a had been accidentally replaced. The correct version of figure 4a can be found below.

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Wang, J., Yang, M., Song, Y. et al. Gut-Associated Bacteria of Helicoverpa zea Indirectly Trigger Plant Defenses in Maize. J Chem Ecol 44, 690–699 (2018). https://doi.org/10.1007/s10886-018-0970-0

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