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Maize Plants Recognize Herbivore-Associated Cues from Caterpillar Frass

Abstract

Caterpillar behaviors such as feeding, crawling, and oviposition are known to induce defenses in maize and other plant species. We examined plant defense responses to another important caterpillar behavior, their defecation. Fall armyworms (FAW, Spodoptera frugiperda), a major threat to maize (Zea mays), are voracious eaters and deposit copious amounts of frass in the enclosed whorl tissue surrounding their feeding site, where it remains for long periods of time. FAW frass is composed of molecules derived from the host plant, the insect itself, and associated microbes, and hence provides abundant cues that may alter plant defense responses. We observed that proteins from FAW frass initially induced wound-responsive defense genes in maize; however, a pathogenesis-related (pr) defense gene was induced as the time after application increased. Elicitation of pathogen defenses by frass proteins was correlated with increased herbivore performance and reduced fungal pathogen performance over time. These responses differ from the typical plant response to oral secretions of the FAW. The results pave the way for identification of protein molecule(s) from the excretion of an herbivore that elicits pathogen defense responses while attenuating herbivore defenses in plants.

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References

  • Alborn HT (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949

    Article  CAS  Google Scholar 

  • Alborn HT, Hansen TV, Jones TH, Bennett DC, Tumlinson JH, Schmelz EA, Teal PEA (2007) Disulfooxy fatty acids from the American bird grasshopper Schistocerca americana, elicitors of plant volatiles. Proc Natl Acad Sci U S A 104:12976–12981

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ankala A, Luthe DS, Williams WP, Wilkinson JR (2009) Integration of ethylene and jasmonic acid signaling pathways in the expression of maize defense protein Mir1-CP. Mol Plant-Microbe Interact 22:1555–1564

    Article  CAS  PubMed  Google Scholar 

  • Baldwin IT, Preston CA (1999) The eco-physiological complexity of plant responses to insect herbivores. Planta 208:137–145

    Article  CAS  Google Scholar 

  • Bass HW, Krawetz JE, OBrian GR, Zinselmeier C, Habben JE, Boston RS (2004) Maize ribosome-inactivating proteins (RIPs) with distinct expression patterns have similar requirements for proenzyme activation. J Exp Bot 55:2219–2233

    Article  CAS  PubMed  Google Scholar 

  • Bent AF, Mackey D (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45:399–436

    Article  CAS  PubMed  Google Scholar 

  • Bolwell GP, Wojtaszek P (1997) Mechanisms for the generation of reactive oxygen species in plant defence - a broad perspective. Physiol Mol Plant Pathol 51:347–366

    Article  CAS  Google Scholar 

  • Bonaventure G, VanDoorn A, Baldwin IT (2011) Herbivore-associated elicitors: FAC signaling and metabolism. Trends Plant Sci 16:294–299

    Article  CAS  PubMed  Google Scholar 

  • Bricchi I, Leitner M, Foti M, Mithöfer A, Boland W, Maffei ME (2010) Robotic mechanical wounding (MecWorm) versus herbivore-induced responses: Early signaling and volatile emission in Lima bean (Phaseolus lunatus L.). Planta 232:719–729

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Gonzales-Vigil E, Wilkerson CG, Howe GA (2007) Stability of plant defense proteins in the gut of insect herbivores. Plant Physiol 143:1954–1967

  • Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA (2005) Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proc Natl Acad Sci USA 102:19237–19242

  • Chuang WP, Herde M, Ray S, Castano-Dugue L, Howe GA, Luthe DS (2014a) Caterpillar attack triggers accumulation of the toxic maize protein RIP2. New Phytol 201:928–939

    Article  CAS  PubMed  Google Scholar 

  • Chuang WP, Ray S, Acevedo FE, Peiffer M, Felton GW, Luthe DS (2014b) Herbivore cues from the fall armyworm (Spodoptera frugiperda) larvae trigger direct defenses in maize. Mol Plant Microbe Interact 27:461–470

    Article  CAS  PubMed  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 Central  CAS  PubMed  Google Scholar 

  • Dempsey DA, Shah J, Klessig DF (1999) Salicylic acid and disease resistance in plants. CRC Crit Rev Plant Sci 18:547–575

    Article  CAS  Google Scholar 

  • Erb M, Flors V, Karlen D, de Lange E, Planchamp C, D’Alessandro M, Turlings TCJ, Ton J (2009) Signal signature of aboveground-induced resistance upon belowground herbivory in maize. Plant J 59:292–302

    Article  CAS  PubMed  Google Scholar 

  • Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Felton GW, Tumlinson JH (2008) Plant-insect dialogs: complex interactions at the plant-insect interface. Curr Opin Plant Biol 11:457–463

    Article  CAS  PubMed  Google Scholar 

  • Helms AM, De Moraes CM, Tooker JF, Mescher MC (2013) Exposure of Solidago altissima plants to volatile emissions of an insect antagonist (Eurosta solidaginis) deters subsequent herbivory. Proc Natl Acad Sci U S A 110:199–204

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hilfiker O, Groux R, Bruessow F, Kiefer K, Zeier J, Reymond (2014) Insect eggs induce a systemic acquired resistance in Arabidopsis. Plant J 80:1085–1094

    Article  CAS  PubMed  Google Scholar 

  • Hilker M, Meiners T (2006) Early herbivore alert: insect eggs induce plant defense. J Chem Ecol 32:1379–1397

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    Article  CAS  PubMed  Google Scholar 

  • Kim J, Tooker JF, Luthe DS, DeMoraes CM, Felton GW (2012) Insect eggs can enhance wound response in plants: a study system of tomato Solanum lycopersicum L. and Helicoverpa zea Boddie. PLoS One 7, e37420

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Korth KL, Dixon RA (1997) Evidence for chewing insect-specific molecular events distinct from a general wound response in leaves. Plant Physiol 115:1299–1305

    PubMed Central  CAS  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mattiacci L, Dicke M, Posthumus MA (1995) Beta-glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proc Natl Acad Sci U S A 92:2036–2040

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McCloud ES, Baldwin IT (1997) Herbivory and caterpillar regurgitants amplify the wound-induced increases in jasmonic acid but not nicotine in Nicotiana sylvestris. Planta 203:430–435

    Article  CAS  Google Scholar 

  • Mithöfer A, Boland W (2008) Recognition of herbivory-associated molecular patterns. Plant Physiol 146:825–831

    Article  PubMed Central  PubMed  Google Scholar 

  • Mithöfer A, Wanner G, Boland W (2005) Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol 137:1160–1168

    Article  PubMed Central  PubMed  Google Scholar 

  • Mohan S, Ma PWK, 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 Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Musser RO, Cipollini DF, Hum-Musser SM, Williams SA, Brown JK, Felton GW (2005) Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in solanaceous plants. Arch Insect Biochem Physiol 58:128–137

    Article  CAS  PubMed  Google Scholar 

  • Panstruga R, Dodds PN (2009) Terrific protein traffic: the mystery of effector protein delivery by filamentous plant pathogens. Science 324:748–750

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Peiffer M, Tooker JF, Luthe DS, Felton GW (2009) Plants on early alert: glandular trichomes as sensors for insect herbivores. New Phytol 184:644–656

    Article  CAS  PubMed  Google Scholar 

  • Ritchie SW, Hanway JJ, Benson GO (1986) How a corn plant develops. Iowa State University of Science and Technology Cooperative Extension Service Special Report 48 (Revised), Ames, IA, U.S.A.

  • Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343

    Article  CAS  PubMed  Google Scholar 

  • Salinovich O, Montelaro RC (1986) Reversible staining and peptide mapping of proteins transferred to nitrocellulose after separation by sodium dodecylsulfate-polyacrylamide gel electrophoresis. Anal Biochem 156:341–347

    Article  CAS  PubMed  Google Scholar 

  • Schäfer M, Fischer C, Meldau S, Seebald E, Oelmüller R, Baldwin IT (2011) Lipase activity in insect oral secretions mediates defense responses in Arabidopsis. Plant Physiol 156:1520–1534

    Article  PubMed Central  PubMed  Google Scholar 

  • Schmelz EA, Engelberth J, Alborn HT, O’Donnell P, Sammons M, Toshima H, Tumlinson JH (2003) Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc Natl Acad Sci U S A 100:10552–10557

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schmelz EA, Engelberth J, Tumlinson JH, Block A, Alborn HT (2004) The use of vapor phase extraction in metabolic profiles of phytohormones and other metabolites. Plant J 39:790–808

    Article  CAS  PubMed  Google Scholar 

  • Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J, Chourey PS, Alborn HT, Teal PEA (2006) Fragments of ATP synthase mediate plant perception of insect attack. Proc Natl Acad Sci U S A 103:8894–8899

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect-plant biology, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Schwartzberg EG, Tumlinson JH (2014) Aphid honeydew alters plant defence responses. Funct Ecol 28:386–394

    Article  Google Scholar 

  • Shanmugam V, Ronen M, Shalaby S, Larkov O, Rachamim Y, Hadar R, Rose MS, Carmeli S, Horwitz BA, Lev S (2010) The fungal pathogen Cochliobolus heterostrophus responds to maize phenolics: novel small molecule signals in a plant-fungal interaction. Cell Microbiol 12:1421–1434

    Article  CAS  PubMed  Google Scholar 

  • Shivaji R, Camas A, Ankala A, Engelberth J, Tumlinson JH, Williams WP, Wilkinson JR, Luthe DS (2010) Plants on constant alert: elevated levels of jasmonic acid and jasmonate-induced transcripts in caterpillar-resistant maize. J Chem Ecol 36:179–191

    Article  CAS  PubMed  Google Scholar 

  • Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270

    Article  CAS  PubMed  Google Scholar 

  • Tian D, Peiffer M, Shoemaker E, Tooker JF, 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 Central  CAS  PubMed  Google Scholar 

  • Tooker JF, de Moraes CM (2006) Jasmonate in Lepidopteran larvae. J Chem Ecol 32:2321–2326

    Article  CAS  PubMed  Google Scholar 

  • Tooker JF, Peiffer M, Luthe DS, Felton GW (2010) Trichomes as sensors: detecting activity on the leaf surface. Plant Signal Behav 5:73–75

    Article  PubMed Central  PubMed  Google Scholar 

  • Van der Does D, Leon-Reyes A, Koornneef A, Van Verk MC, Rodengurg N, Pauwels L, Goossens A, Körbes AP, Memelink J, Ritsema T, Van Wees SCM, Pierterse CMJ (2013) Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell 25:744–761

    Article  PubMed Central  PubMed  Google Scholar 

  • Van der Linde K, Hemetsberger C, Kastner C, Kaschani R, van der Hoorn RAL, Kumlehn J, Doehlemann G (2012) A maize cystatin suppresses host immunity by inhibiting apoplastic cysteine proteases. Plant Cell Online 24:1285–1300

    Article  Google Scholar 

  • Van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162

    Article  PubMed  Google Scholar 

  • VanDoorn A, de Vries M, Kant M, Schuurink R (2015) Whiteflies glycosylate salicylic acid and secrete the conjugate via their honeydew. J Chem Ecol 41:52–58

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Weiss MR (2003) Good housekeeping: why do shelter-dwelling caterpillars fling their frass? Ecol Lett 6:361–370

    Article  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 Central  CAS  PubMed  Google Scholar 

  • Yan Y, Christensen S, Isakeit T, Engelberth J, Meeley R, Hayward A, Emery RJN, Kolomiets MV (2012) Disruption of OPR7 and OPR8 reveals the versatile functions of jasmonic acid in maize development and defense. Plant Cell Online 24:1420–1436

    Article  CAS  Google Scholar 

  • Yoder OC (1988) Cochliobolus heterostrophus, cause of southern corn leaf blight. Genetics of plant pathogenic fungi. Academic, London, pp 93–112

    Book  Google Scholar 

  • Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Dr. Rebecca Boston for sending us antibody for Rip2 protein in maize. We also thank the insight of Nate McCarthey in Dr. Jim Tumlinson’s lab for the phytohormone analyses. We thank Dr. Elizabeth Bosak for letting us use the wounding tool. The author also acknowledges Dr. Kelli Hoover’s lab for help in quantifying RNA samples with Nanodrop (Thermo Fisher Scientific). We appreciate the comments of Dr SeungHo Chung in the preparation of this manuscript. We thank Susan Wolf at USDA-ARS (MSU), for providing the FAW eggs.

Funding

This work was supported by grants from USDA NIFA (2010-65105-20639 and 2011-67013-30352) awarded to D.S.L and G.W.F.

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Correspondence to Dawn S. Luthe.

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Ray, S., Gaffor, I., Acevedo, F.E. et al. Maize Plants Recognize Herbivore-Associated Cues from Caterpillar Frass. J Chem Ecol 41, 781–792 (2015). https://doi.org/10.1007/s10886-015-0619-1

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