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Physical and metabolic consequences of Hessian fly infestation are more severe on nonhost Brachypodium distachyon than on host-plant resistant wheat

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Abstract

Physical and metabolic changes were compared between the model grass, Brachypodium distachyon, and the Hessian fly host plant, wheat, after infestation. B. distachyon was determined to be a nonhost, where 13 lines were resistant to all infestations tested, yet it responded with characteristics of both host-plant resistant wheat and susceptible wheat. Similar to resistant wheat, B. distachyon completed development with no seed yield penalty imposed by Hessian fly infestation. Wheat and B. distachyon exhibited some degree of leaf stunting, but only of the leaves that were actively growing while the larvae were attempting to feed. Since resistant wheat killed all larvae within 3–5 days after egg hatch, only the lower leaves were stunted. In compensation for leaf stunting, infested resistant wheat underwent precocious initiation and accelerated growth of the upper leaves once the larvae had died. In contrast, larvae survived, without growing, on B. distachyon for much longer, some up to 46 days after egg hatch when the plant was senescing; consequently, all leaves of B. distachyon exhibited stunting, but to a lesser degree than leaves of susceptible wheat where the insects complete their life cycle. Transcript profiling of eight key genes, known to respond to Hessian fly in either resistant or susceptible wheat, demonstrated that B. distachyon exhibited responses intermediate between the compatible and incompatible interactions of wheat as well as both type I and type II nonhost resistance.

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References

  • Agrios GN (1997) Plant diseases caused by Mollicutes: phytoplasmas and spiroplasmas. In: Agrios GN (ed) Plant pathology, 4th edn. Academic Press, New York, pp 457–470

    Google Scholar 

  • Altschul S, Gish W, Miller W, Myers E, Lipman D (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Anderson KG, Harris MO (2008) Leaf growth signals the onset of effective plant resistance against Hessian fly larvae. Entomol Exp Appl 128:184–195

    Article  Google Scholar 

  • Anderson KM, Kang Q, Reber J, Harris MO (2011) No fitness cost for wheat’s H-gene-mediated resistance to Hessian fly (Diptera: Cecidomyiidae). J Econ Entomol 104:1393–1405

    Article  PubMed  Google Scholar 

  • Baluch SD, Ohm HW, Shukle JT, Williams CE (2012) Obviation of wheat resistance to the Hessian fly through systemic induced susceptibility. J Econ Entomol 105:642–650

    Article  PubMed  Google Scholar 

  • Berzonsky WA, Ding H, Haley SD, Harris MO, Lamb RJ, McKenzie RI, Peairs FB, Porter DR, Ratcliffe RH, Shanowar TG (2003) Breeding wheat for resistance to insects. Plant Breed Rev 22:221–297

    Google Scholar 

  • Bragg JN, Wu J, Gordon SP, Guttman ME, Thilmony R, Lazo GR, Gu YQ, Vogel JP (2012) Generation and characterization of the Western regional Research Center Brachypodium T-DNA insertional mutant collection. PLoS ONE 7:e41916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Cartwright WB, Caldwell RM, Compton LE (1959) Response of resistant and susceptible wheat to Hessian fly attack. Agron J 51:529–531

    Article  Google Scholar 

  • Chen MS, Fellers JP, Zhu YC, Stuart JJ, Hulbert S, El-Bouhssini M, Liu X (2006) A super-family of genes coding for secreted salivary gland proteins from the Hessian fly, Mayetiola destructor. J. Insect Sci 6:12

    Article  PubMed Central  Google Scholar 

  • Fay PA, Hartnett DC, Knapp AK (1993) Increased photosynthesis and water potentials in Silphium integrifolium galled by cynipid wasps. Oecologia 93:114–120

    Article  PubMed  Google Scholar 

  • Fernandes GW, Negreiros D (2001) The occurrence and effectiveness of hypersensitive reaction against galling herbivores across host taxa. Ecol Entomol 26:46–55

    Article  Google Scholar 

  • Gagné RJ, Hatchett JH (1989) Instars of the Hessian fly (Diptera: Cecidomyiidae). Ann Entomol Soc Am 82:73–79

    Article  Google Scholar 

  • Garvin DF, Gu YQ, Hasterok R, Hazen SP, Jenkins G, Mockler TC, Mur LAJ, Vogel JP (2008) Development of genetic and genomic research resources for Brachypodium distachyon, a new model system for grass crop research. Crop Sci 48:S69–S84

    Article  Google Scholar 

  • Gill US, Lee S, Mysore KS (2015) Host versus nonhost resistance: distinct wars with similar arsenals. Phytopathology 105:580–587

    Article  PubMed  Google Scholar 

  • Giovanini MP, Saltzmann KD, Puthoff DP, Gonzalo M, Ohm HW, Williams CE (2007) A novel wheat gene encoding a putative chitin-binding lectin is associated with resistance against Hessian fly. Mol Plant Pathol 8:69–82

    Article  CAS  PubMed  Google Scholar 

  • Goethals K, Vereecke D, Jaziri M, Van Montagu M, Holsters M (2001) Leafy gall formation by Rhodococcus fascians. Annu Rev Phytopathol 39:27–52

    Article  CAS  PubMed  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 

  • Heath MC (1985) Implications of nonhost resistance for understanding host–parasite interactions. In: Groth JV, Bushnell WR (eds) Genetic basis of biochemical mechanisms of plant disease. APS Press, St Paul, pp 25–42

    Google Scholar 

  • Heath MC (2000) Nonhost resistance and nonspecific plant defenses. Curr Opin Plant Biol 3:315–319

    Article  CAS  PubMed  Google Scholar 

  • Huo N, Vogel JP, Lazo GR, You FM, Ma Y, McMahon S, Dvorak J, Anderson OD, Luo M-C, Gu YQ (2009) Structural characterization of Brachypodium genome and its syntenic relationship with rice and wheat. Plant Mol Biol 70:47–61

    Article  CAS  PubMed  Google Scholar 

  • Jankiewicz LS, Plich H, Antoszewski R (1970) Preliminary studies on the translocation of 14C-labelled assimilates and 32PO3 − towards the gall evoked by Cynips (Diplolepis) quercus-folii L. on oak leaves. Marcellia 36:163–172

    Google Scholar 

  • Kebrom TH, Spielmeyer W, Finnegan EJ (2013) Grasses provide new insights into regulation of shoot branching. Trends Plant Sci 18:41–48

    Article  CAS  PubMed  Google Scholar 

  • Keppler R, Rickman RW, Belford RK (1983) Leaf and tiller identification on wheat plants. Crop Sci 23:1002–1004

    Article  Google Scholar 

  • Kosma DK, Nemacheck JA, Jenks MA, Williams CE (2010) Changes in properties of wheat leaf cuticle during interactions with Hessian fly. Plant J 63:31–43

    CAS  PubMed  Google Scholar 

  • Lara MEB, Garcia M-CG, Fatima T, Ehneß R, Lee TK, Proels R, Tanner W, Roitsch T (2004) Extracellular invertase is an essential component of cytokinin mediated delay of senescence. Plant Cell 16:15–21

    Google Scholar 

  • Larson KC, Whitham TG (1991) Manipulation of food resources by a gall-forming aphid: the physiology of sink–source interactions. Oecologia 88:15–21

    Article  PubMed  Google Scholar 

  • Li C, Chen MS, Chao S, Yu J, Bai G (2013) Identification of a novel gene, H34, in wheat using recombinant inbred lines and single nucleotide polymorphism markers. Theor Appl Genet 126:2065–2071

    Article  CAS  PubMed  Google Scholar 

  • Liu XM, Khajuria C, Li JR, Trick HN, Huang L, Gill BS, Reeck GR, Antony G, White FF, Chen MS (2013) Wheat Mds-1 encodes a heat-shock protein and governs susceptibility towards the Hessian fly gall midge. Nat Commun 4:2070

    PubMed  Google Scholar 

  • McColloch JW (1923) The Hessian fly in Kansas. Kans Agric Exp Stn Bull 11:96

    Google Scholar 

  • McDonald MJ, Ohm HW, Rinehart KD, Giovanini MP, Williams CE (2014) H33: a wheat gene providing Hessian fly resistance for the southeastern United States. Crop Sci 54:2045–2053

    Article  Google Scholar 

  • Miyoshi K, Ahn B-O, Kawakatsu T, Ito Y, Itoh J-I, Nagato Y, Kurata N (2004) PLASTOCHROME1, a timekeeper of leaf initiation in rice, encodes cytochrome P450. Proc Natl Acad Sci USA 101:875–880

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mysore KS, Ryu CM (2004) Nonhost resistance: How much do we know? Trends Plant Sci 9:97–104

    Article  CAS  PubMed  Google Scholar 

  • Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noble WB, Suneson CA (1943) Differentiation of the two genetic factors for resistance to Hessian fly in Dawson wheat. J Agric Res 67:27–32

    Google Scholar 

  • Patterson FL, Maas FB, Foster JE, Ratcliffe RH, Cambron SE, Safranski SG, Taylor PL, Ohm HW (1994) Registration of eight Hessian fly resistant common winter wheat germplasm lines (Carol, Erin, Flynn, Iris, Joy, Karen, Lola, and Molly). Crop Sci 34:315–316

    Article  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Robinson RJ, Miller BS, Mitchell HL, Mussman HC, Johnson JA, Jones ET (1960) Chloroplast number in leaves of normal wheat plants and those infested with Hessian fly or treated with maleic hydrazide. J Econ Entomol 53:560–562

    Article  CAS  Google Scholar 

  • Rohfritsch O (2005) Gall making. In: Goodman R (ed) Encyclopedia of plant and crop science. Marcel Dekker Inc., New York, pp 1021–1022

    Google Scholar 

  • Saltzmann KD, Giovanini MP, Zheng C, Williams CE (2008) Virulent Hessian fly larvae manipulate the free amino acid content of host wheat plants. J Chem Ecol 34:1401–1410

    Article  CAS  PubMed  Google Scholar 

  • Santos J, Silveira F, Fernandes G (2008) Long term oviposition preference and larval performance of Schizomyia macrocapillata (Diptera: Cecidomyiidae) on larger shoots of its host plant Bauhinia brevipes (Fabaceae). Evol Ecol 22:123–137

    Article  Google Scholar 

  • Sardesai N, Nemacheck JA, Subramanyam S, Williams CE (2005) Identification and mapping of H32, a new wheat gene conferring resistance to Hessian fly. Theor Appl Genet 111:1167–1173

    Article  CAS  PubMed  Google Scholar 

  • Senthil-Kumar M, Mysore KS (2013) Nonhost resistance against bacterial pathogens: retrospectives and prospects. Ann Rev Phytopathol 51:407–427

    Article  CAS  Google Scholar 

  • Shukle RH, Grover PB Jr, Mocelin G (1992) Responses of susceptible and resistant wheat associated with Hessian fly (Diptera: Cecidomyiidae) infestation. Environ Entomol 21:845–853

    Article  Google Scholar 

  • Shukle RH, Subramanyam S, Saltzmann KA, Williams CE (2010) Ultrastructural changes in the midguts of Hessian fly larvae feeding on resistant wheat. J Insect Physiol 56:754–760

    Article  CAS  PubMed  Google Scholar 

  • Shukle RH, Subramanyam S, Williams CE (2012) Effects of antinutrient proteins on Hessian fly (Diptera: Cecidomyiidae) larvae. J Insect Physiol 58:41–48

    Article  CAS  PubMed  Google Scholar 

  • Sosa O, Gallun RL (1973) Purification of races B and C of the Hessian fly by genetic manipulation. Ann Entomol Soc Am 66:1065–1070

    Article  Google Scholar 

  • Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522

    Article  Google Scholar 

  • Subramanyam S, Sardesai N, Puthoff DP, Meyer JM, Nemacheck JA, Gonzalo M, Williams CE (2006) Expression of two wheat defense-response genes, Hfr-1 and Wci-1, under biotic and abiotic stresses. Plant Sci 170:90–103

    Article  CAS  Google Scholar 

  • Subramanyam S, Smith DE, Clemens JC, Webb MA, Sardesai N, Williams CE (2008) Functional characterization of HFR1, a high-mannose N-glycan-specific wheat lectin induced by Hessian fly. Plant Physiol 146:1412–1426

    Article  Google Scholar 

  • Subramanyam S, Sardesai N, Minocha S, Zheng C, Shukle RH, Williams CE (2015) Hessian fly larval feeding triggers enhanced polyamine levels in susceptible wheat but not resistant wheat. BMC Plant Biol 15:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Sumit R (2013) Investigation of the Arabidopsis nonhost resistance mechanism against the soybean pathogen, Phytophthora sojae. Dissertation, Iowa State University

  • The International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763–768

    Article  Google Scholar 

  • Thole V, Worland B, Wright J, Bevan MW, Vain P (2010) Distribution and characterization of more than 1000 T-DNA tags in the genome of Brachypodium distachyon community standard line Bd21. Plant Biotechnol J 8:734–747

    Article  CAS  PubMed  Google Scholar 

  • Vogel JP, Bragg J (2009) Brachypodium distachyon, a new model for Triticeae. In: Feuillet C, Muehlbauer G (eds) Genetics and genomics of the Triticeae. Plant genetics and genomics: crops and models, vol 7. Springer, Berlin, pp 427–449

    Chapter  Google Scholar 

  • Vogel JP, Hill TA (2008) High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3. Plant Cell Rep 27:471–478

    Article  CAS  PubMed  Google Scholar 

  • Vogel JP, Garvin DF, Leong OM, Hayden DM (2006) Agrobacterium-mediated transformation and inbred line development in the model grass Brachypodium distachyon. Plant Cell Tissue Organ Cult 84:100179–100191

    Article  Google Scholar 

  • Waggoner PE, Berger RD (1987) Defoliation, disease, and growth. Phytopathology 77:393–398

    Google Scholar 

  • Walters DR (2000) Polyamines in plant-microbe interactions. Physiol Mol Plant Pathol 57:137–146

    Article  CAS  Google Scholar 

  • Walters DR (2003) Polyamines and plant disease. Phytochem 64:97–107

    Article  CAS  Google Scholar 

  • Walters DR, McRoberts N, Fitt BDL (2008) Are green islands red herrings? Significance of green islands in plant interactions with pathogens and pests. Biol Rev 83:79–102

    Article  PubMed  Google Scholar 

  • Williams CE, Collier CC, Nemacheck JA, Liang C, Cambron SE (2002) A lectin-like wheat gene responds systemically to attempted feeding by avirulent first-instar Hessian fly larvae. J Chem Ecol 28:1411–1428

    Article  CAS  PubMed  Google Scholar 

  • Williams CE, Collier CC, Sardesai N, Ohm HW, Cambron SE (2003) Phenotypic assessment and mapped markers for H31, a new wheat gene conferring resistance to Hessian fly (Diptera: Cecidomyiidae). Theor Appl Genet 107:1516–1523

    Article  CAS  PubMed  Google Scholar 

  • Williams CE, Nemacheck JA, Shukle JT, Subramanyam S, Saltzmann K, Shukle RH (2011) Induced epidermal permeability modulates resistance and susceptibility of wheat seedlings to herbivory by Hessian fly larvae. J Exp Botany 62:4521–4531

    Article  CAS  Google Scholar 

  • Xu SS, Chu CG, Harris MO, Williams CE (2011) Comparative analysis of genetic background in eight near-isogenic wheat lines with different H genes conferring resistance to Hessian fly. Genome 54:81–89

    Article  CAS  PubMed  Google Scholar 

  • Zhao B, Lin X, Poland J, Trick H, Leach J, Hulbert S (2005) A maize resistance gene functions against bacterial streak disease in rice. Proc Natl Acad Sci USA 102:15383–15388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao C, Escalanta LN, Chen H, Benatti TR, Qu J, Chellapilla S, Waterhouse RM, Wheeler D, Andersson MN, Bao R, Batterton M, Behura SK, Blankenburg KP, Caragea D, Carolan JC, Coyle M, El-Bouhssini M, Francisco L, Friedrich M, Gill N, Grace T, Grimmelikhuijzen CJ, Han Y, Hause F, Herndon N, Holder M, Ioannidis P, Jackson L, Javaid M, Jhangiani SN, Johnson AJ, Kalra D, Korchina V, Kovar CL, Lara F, Lee SL, Liu X, Lofstedt C, Mata R, Mathew T, Muzny DM, Nagar S, Nazareth LV, Okwuonu G, Ongeri F, Perales L, Peterson BF, Pu L, Robertson HM, Schemerhorn BJ, Scherer SE, Shreve J, Simmons D, Subramanyam S, Thornton RL, Xue K, Weissenberger GM, Williams CE, Worley KC, Zhu D, Zhu Y, Harris MO, Shukle RH, Werren JH, Zdobnov EM, Chen M, Brown SJ, Stuart JJ, Richards S (2015) A massive expansion of effector genes underlies gall-formation in the wheat pest Mayetiola destructor. Curr Biol 25:613–620

    Article  CAS  PubMed  Google Scholar 

  • Zhu L, Liu X, Liu X, Jeannotte R, Reese JC, Harris M, Stuart JJ, Chen M-S (2008) Hessian fly (Mayetiola destructor) attack causes a dramatic shift in carbon and nitrogen metabolism in wheat. Mol Plant Microbe Interact 21:70–78

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was a joint contribution by the USDA Agricultural Research Service Crop Production and Pest Control Research Unit and Purdue University. Research was supported by USDA-CRIS Number 3602-22000-018-D. The authors wish to thank Sue Cambron (USDA-ARS) for maintaining Hessian fly stocks. Mention of a commercial or a proprietary product does not constitute endorsement or recommendation for its use by the USDA.

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    1. USDA-ARS Crop Production and Pest Control Research Unit, West Lafayette, IN, 47907, USA

      Andrea M. Hargarten, Jill A. Nemacheck, Brandon J. Schemerhorn & Christie E. Williams

    2. Department of Agronomy, Purdue University, West Lafayette, IN, 47907, USA

      Subhashree Subramanyam, Xiangye Xiao & Christie E. Williams

    3. Department of Entomology, Purdue University, West Lafayette, IN, 47907, USA

      Brandon J. Schemerhorn

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    1. Andrea M. Hargarten
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    Correspondence to Christie E. Williams.

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    Handling Editor: Chen-Zhu Wang.

    Andrea M. Hargarten and Jill A. Nemacheck contributed equally to this work.

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    11829_2017_9542_MOESM1_ESM.pdf

    Supplementary material 1 Hypersensitive response on B. distachyon. Ten DAH, seedlings were dissected to expose hypersensitive response at the crown where Biotype L larvae were attempting to feed. Scale bar represents 1 mm (PDF 110 kb)

    11829_2017_9542_MOESM2_ESM.pdf

    Supplementary material 2 Larval size on B. distachyon. Larvae were measured as in Fig. 1. Solid line represents the average size of larvae on H9-Iris wheat measured 8 DAH. Thin dashed lines above and below the solid line represent the largest and smallest larvae on H9-Iris. Thick dashed line represents the smallest larva measured on Newton wheat. 20% of larvae residing on B. distachyon were larger than the largest on H9-Iris wheat. Graphs were made in Microsoft Excel 2010 (PDF 90 kb)

    11829_2017_9542_MOESM3_ESM.pdf

    Supplementary material 3 Hessian fly infestation delayed B. distachyon senescence. In each photograph, two uninfested control pots are on the left and two infested pots are on the right. Each pot contains three plants (PDF 239 kb)

    Supplementary material 4 (PDF 12 kb)

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    Hargarten, A.M., Nemacheck, J.A., Subramanyam, S. et al. Physical and metabolic consequences of Hessian fly infestation are more severe on nonhost Brachypodium distachyon than on host-plant resistant wheat. Arthropod-Plant Interactions 11, 767–783 (2017). https://doi.org/10.1007/s11829-017-9542-4

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