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Feeding by Hessian Fly (Mayetiola destructor [Say]) Larvae on Wheat Increases Levels of Fatty Acids and Indole-3-Acetic Acid but not Hormones Involved in Plant-Defense Signaling

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Abstract

Gall-inducing insects exert a unique level of control over the physiology of their host plants. This control can extend to host–plant defenses so that some, if not most, gall-inducing species appear to avoid or modify host plant defenses to effect production of their gall. Included among gall insects is Hessian fly (Mayetiola destructor [Say], Diptera: Cecidomyiidae), a damaging pest of wheat (Triticum aestivum L.) and an emerging model system for studying plant–insect interactions. We studied the dynamics of some defense-related phytohormones and associated fatty acids during feeding of first instar Hessian fly larvae on a susceptible variety of wheat. We found that Hessian fly larvae significantly elevated in their host plants’ levels of linolenic and linoleic acids, fatty acids that may be nutritionally beneficial. Hessian fly larvae also elevated levels of indole-3-acetic acid (IAA), a phytohormone hypothesized to be involved in gall formation, but not the defense-related hormones jasmonic (JA) and salicylic acids. Moreover, we detected in Hessian fly-infested plants a significant negative relationship between IAA and JA that was not present in control plants. Our results suggest that Hessian fly larvae may induce nutritionally beneficial changes while concomitantly altering phytohormone levels, possibly to facilitate plant-defense avoidance.

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References

  • Allison SD, Schultz JC (2005) Biochemical responses of chestnut oak to a galling cynipid. J Chem Ecol 31:151–166

    Article  PubMed  CAS  Google Scholar 

  • Buntin GD (1999) Hessian fly (Diptera: Cecidomyiidae) injury and loss of winter wheat grain yield and quality. J Econ Entomol 92:1190–1197

    Google Scholar 

  • Byers RA, Gallun RL (1972) Ability of Hessian fly to stunt winter wheat. 1. Effect of larval feeding on elongation of leaves. J Econ Entomol 65:955–958

    Google Scholar 

  • Cervantes DE, Eigenbrode SD, Ding HJ, Bosque-Pérez NA (2002) Oviposition responses by Hessian fly, Mayetiola destructor, to wheats varying in surface waxes. J Chem Ecol 28:193–210

    Article  PubMed  CAS  Google Scholar 

  • Chang CL, Vargas RI (2007) Addition of wheat germ oil to a liquid larval diet for rearing improved quality oriental fruit flies (Diptera: Tephritidae). J Econ Entomol 100:322–326

    Article  PubMed  CAS  Google Scholar 

  • Dadd RH (1977) Qualitative requirements and utilization of nutrients: insects. In: Rechcigl M Jr (ed) Handbook series in nutrition and food. Section D: nutritional requirements, vol 1. CRC Press, Cleveland, pp 305–346

    Google Scholar 

  • Davies PJ (2004) The plant hormones: their nature, occurrence, and functions. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action! Kluwer Academic Publishers, Dordrecht, pp 1–15

  • del Rio-Celestino M, Font R, de Haro-Bailón A (2008) Distribution of fatty acids in edible organs and seed fractions of borage (Borago officinalis L.). J Sci Food Agric 88:248–255

    Article  CAS  Google Scholar 

  • Downer RGH (1985) Lipid metabolism. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 10. Pergamon Press, Oxford, pp 77–114

    Google Scholar 

  • Farmer EE, Ryan CA (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4:129–134

    Article  PubMed  CAS  Google Scholar 

  • Harris MO, Stuart JJ, Mohan M, Nair S, Lamb RJ, Rohfritsch O (2003) Grasses and gall midges: plant defense and insect adaptation. Ann Rev Entomol 48:549–577

    Article  CAS  Google Scholar 

  • Harris MO, Freeman TP, Rohfritsch O, Anderson KG, Payne SA, Moore JA (2006) Virulent Hessian fly (Diptera: Cecidomyiidae) larvae induce a nutritive tissue during compatible interactions with wheat. Ann Entomol Soc Am 99:305–316

    Article  Google Scholar 

  • Hartley SE (1998) The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall former? Oecologia 113:492–501

    Article  Google Scholar 

  • Harwood JL, Russell NJ (1983) Lipids in plants and microbes. George Allen and Unwin, London, p 162

    Google Scholar 

  • Hatchett JH, Kreitner GL, Elzinga RJ (1990) Larval mouthparts and feeding mechanism of the Hessian fly (Diptera: Cecidomyiidae). Ann Entomol Soc Am 83:1137–1147

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago, p 319

    Google Scholar 

  • Koo AJ, Howe GA (2009) The wound hormone jasmonate. Phytochemistry 70:1571–1580

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Bai J, Zhu L, Liu X, Weng N, Reese JC, Harris M, Stuart JJ, Chen M (2007) Differential gene expression of H9 and H13 wheat genotypes during attack by virulent and avirulent Hessian fly (Mayetiola destructor) larvae. J Chem Ecol 33:2171–2194

    Article  PubMed  CAS  Google Scholar 

  • Nyman T, Julkunen-Tiitto R (2000) Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proc Natl Acad Sci USA 97:13184–13187

    Article  PubMed  CAS  Google Scholar 

  • Raman A, Schaefer CW, Withers TM (2005) Galls and gall-inducing arthropods: an overview of their biology, ecology and evolution. In: Raman A, Schaefer CW, Withers TM (eds) Biology, ecology, and evolution of gall-inducing arthropods. Science Publishers, Inc., Enfield, pp 1–33

    Google Scholar 

  • Saniewski M, Ueda J, Miyamoto K (2002) Relationships between jasmonates and auxin in regulation of some physiological processes in higher plants. Acta Physiol Plant 24:211–220

    Article  CAS  Google Scholar 

  • Sardesai N, Subramanyam S, Nemacheck JA, Williams CE (2005) Modulation of defense-response gene expression in wheat during Hessian fly larval feeding. J Plant Interact 1:39–50

    Article  CAS  Google Scholar 

  • SAS Institute (2003) SAS/STAT user’s guide for personal computers, release 9. SAS Institute, Cary

    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 USA 100:10552–10557

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Smiley RW, Gourlie J, Whittaker R, Easley S, Kidwell K (2004) Economic impact of Hessian fly (Diptera: Cecidomyiidae) on spring wheat in Oregon and additive yield losses with Fusarium crown rot and lesion nematode. J Econ Entomol 97:397–408

    Article  PubMed  Google Scholar 

  • Smith CM, Liu X, Wang LJ, Liu X, Chen MS, Starkey S, Bai J (2010) Aphid feeding activates expression of a transcriptome of oxyplin-based defense signals in wheat involved in resistance to herbivory. J Chem Ecol 36:260–276

    Article  PubMed  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W. H. Freeman, New York, p 887

    Google Scholar 

  • Stuart JJ, Hatchett JH (1987) Morphogenesis and cytology of the salivary glands of the Hessian fly, Mayetiola destructor (Diptera: Cecidomyiidae). Ann Entomol Soc Am 80:475–482

    Google Scholar 

  • Tooker JF, De Moraes CM (2007) Feeding by Hessian fly [Mayetiola destructor (Say)] larvae does not induce plant indirect defences. Ecol Entomol 32:153–161

    Article  Google Scholar 

  • Tooker JF, De Moraes CM (2008) Gall insects and indirect plant defenses: a case of active manipulation? Plant Signal Behav 3:503–504

    Article  PubMed  Google Scholar 

  • Tooker JF, De Moraes CM (2009) A gall-inducing caterpillar species increases essential fatty acid content of its host plant without concomitant increases in phytohormone levels. Mol Plant Microbe Interact 22:551–559

    Article  PubMed  CAS  Google Scholar 

  • Tooker JF, Hanks LM (2004) Stereochemistry of host plant monoterpenes as mate location cues for the gall wasp Antistrophus rufus. J Chem Ecol 30:473–477

    Article  PubMed  CAS  Google Scholar 

  • Tooker JF, Koenig WA, Hanks LM (2002) Altered host plant volatiles are proxies for sex pheromones in the gall wasp Antistrophus rufus. Proc Natl Acad Sci USA 99:15486–15491

    Article  PubMed  CAS  Google Scholar 

  • Tooker JF, Rohr JR, Abrahamson WG, De Moraes CM (2008) Gall insects can avoid and alter indirect plant defenses. New Phytol 178:657–671

    Article  PubMed  CAS  Google Scholar 

  • van Hulten M, Pelser M, Van Loon LC, Pieterse CMJ, Ton J (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci USA 103:5602–5607

    Article  PubMed  Google Scholar 

  • von Dahl CC, Baldwin IT (2004) Methyl jasmonate and cis-jasmone do not dispose of the herbivore-induced jasmonate burst in Nicotiana attenuata. Physiol Plant 120:474–481

    Article  Google Scholar 

  • Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216

    PubMed  CAS  Google Scholar 

  • Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421

    Article  Google Scholar 

  • Zhu L, Liu X, Chen MS (2010) Differential accumulation of phytohormones in wheat seedlings attacked by avirulent and virulent Hessian fly (Diptera: Cecidomyiidae) larvae. J Econ Entomol 103:178–185

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank J. Saunders and C. Wagner for logistical support, E. Bogus for technical assistance, B. Banks for H. virescens eggs, and M. Tooker for drawing Fig. 1. Our Hessian fly colony was established with the generous assistance of N. Bosque-Perez and D. Schotzko (University of Idaho). The project was supported by the David and Lucile Packard Foundation, the Beckman Foundation, the DuPont Young Investigator grant, the National Science Foundation (NSF CAREER no. 0643966), and the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service (#2002-35302-12375 [CMDM]; #2006-01823 [JFT]).

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  1. Department of Entomology, The Pennsylvania State University, 501 ASI Building, University Park, PA, 16802-3508, USA

    John F. Tooker & Consuelo M. De Moraes

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  1. John F. Tooker
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  2. Consuelo M. De Moraes
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Correspondence to John F. Tooker.

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Tooker, J.F., De Moraes, C.M. Feeding by Hessian Fly (Mayetiola destructor [Say]) Larvae on Wheat Increases Levels of Fatty Acids and Indole-3-Acetic Acid but not Hormones Involved in Plant-Defense Signaling. J Plant Growth Regul 30, 158–165 (2011). https://doi.org/10.1007/s00344-010-9177-5

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  • DOI: https://doi.org/10.1007/s00344-010-9177-5

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