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Hessian fly larval attack triggers elevated expression of disease resistance dirigent-like protein-encoding gene, HfrDrd, in resistant wheat

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Abstract

Dirigent proteins regulate coupling of monolignol plant phenols to generate the cell wall polymers lignins and lignans that are involved in structural fortification and defense against pathogens and pests. In this study, we report the temporal expression of a putative Hessian fly-responsive disease resistance dirigent-like protein-encoding gene, HfrDrd, in wheat. HfrDrd transcript abundance was quantified under biotic stresses imposed by Hessian fly, bird cherry-oat aphid, barley and cereal yellow dwarf virus, fall army worm and silverleaf white fly, after mechanical wounding, as well as during treatment with signaling elicitors. Quantitative transcriptional analysis indicated increased abundance of HfrDrd mRNA in both susceptible and resistant wheat after Hessian fly attack. However, within 24 h, resistant wheat accumulated 2.5- to >20-fold higher HfrDrd mRNA levels than the susceptible wheat. The increase in transcripts as early as 2 h after egg hatch suggested a role for HfrDrd in early defense against Hessian fly larvae. HfrDrd transcript abundance was not responsive to exogenous application of plant defense-signaling pathway molecules, salicylic acid, methyl jasmonate or abscisic acid. Lack of HfrDrd response during other wheat–insect interactions or mechanical wounding indicated that HfrDrd is not a general stress-responsive gene, but is specific to the defense mechanisms responding to probing by Hessian fly larvae.

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References

  • Afzal AH, Natarajan A, Saini N, Iqbal JM, Geisler M, El Shemy HA, Mungur R, Willmitzer L, Lightfoot DA (2009) The nematode resistance allele at the rhg1 locus alters the proteome and primary metabolism of soybean roots. Plant Physiol 151:1264–1280

    Article  PubMed  CAS  Google Scholar 

  • Asano J, Chiba K, Tada M, Yoshii T (1996) Antiviral activity of lignans and they gllysosides from Justicia procumbens. Phytochemistry 42:713–717

    Article  PubMed  CAS  Google Scholar 

  • Atta-ur-Rahman AM, Choudhary MI, Habib-ur-Rahman KMH (1995) Antifungal arlytetralin lignans from leaves of Podophyllum hexandrum. Phytochemistry 40:427–431

    Article  CAS  Google Scholar 

  • Burlat V, Kwon M, Davin LB, Lewis NG (2001) Dirigent proteins and dirigent sites in lignifying tissues. Phytochemistry 57:883–897

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Chen M-S, Zhao HX, Zhu YC, Scheffler B, Liu X, Liu X, Hulbert S, Stuart JJ (2008) Analysis of transcripts and protein expressed in the salivary glands of Hessian fly (Mayetiola destructor) larvae. J Insect Physiol 54:1–16

    Article  PubMed  CAS  Google Scholar 

  • Damaj MB, Kumpatla SP, Emani C, Beremand PD, Avutu S, Reddy AS, Rathore KS, Buenrostro-Nava MT, Curtis IS, Thomas TL, Mirkov TE (2010) Sugarcane DIRIGENT and O-methyltransferase promoters confer stem-regulated gene expression in diverse monocots. Planta 231:1439–1458

    Article  PubMed  CAS  Google Scholar 

  • Davin LB, Lewis NG (2000) Dirigent proteins and dirigent sites explain the mystery of specificity of radical precursor coupling in lignin and lignin biosynthesis. Plant Physiol 123:453–461

    Article  PubMed  CAS  Google Scholar 

  • Davin LB, Wang H-B, Crowell AL, Bedgar DL, Martin DM, Sarkansen S, Lewis NG (1997) Stereoselective bimolecular phenoxy radical coupling by an auxiliary (dirigent) protein without an active center. Science 275:362–366

    Article  PubMed  CAS  Google Scholar 

  • Day SH, Chiu NY, Won SJ, Lin CN (1999) Cytotoxic lignans of Justicia ciliate. J Nat Prod 62:1056–1058

    Article  PubMed  CAS  Google Scholar 

  • Flor HH (1946) Genetics of pathogenicity in Melamspora lini. J Agric Res 73:335

    Google Scholar 

  • Fung RWM, Gonzalo M, Fekete C, Kovacs L, He Y, Marsh E, McIntyre M, Schachtman DP, Qiu W (2008) Powdery mildew induces defense-oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine. Plant Physiol 146:236–249

    Article  PubMed  CAS  Google Scholar 

  • Gang, Costa MA, Fujita M, Dinkova-Kostova AT, Wang H-B, Burlat V, Martin W, Sarkanen S, Davin LB, Lewis NG (1999) Regiochemical control of monolignol radical coupling: a new paradigm for lignin and lignan biosynthesis. Chem Biol 6:143–151

    Article  PubMed  CAS  Google Scholar 

  • Gao CQ, Liu GF, Wang YC, Jiang J, Yang CP (2010) Cloning and analysis of dirigent-like protein in gene from Tamarix androssowii. Bull Bot Res 30:81–86

    CAS  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 again Hessian fly. Mol Plant Pathol 8:69–82

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  PubMed  CAS  Google Scholar 

  • Görlach J, Volrath S, Knauf-Beiter G, Hengy G, Beckhove U, Kogel KH, Oostendorp M, Staub T, Ward E, Kessmann H, Ryals J (1996) Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8:629–664

    PubMed  Google Scholar 

  • Guo J-L, Xu L-P, Fang J-P, Su Y-C, Fu H-Y, Que Y-X, Xu J-S (2012) A novel dirigent protein gene with highly stem-specific expression from sugarcane, response to drought, salt and oxidative stresses. Plant Cell Rep 31:1801–1812

    Article  CAS  Google Scholar 

  • Hadwiger LA, Chiang CC, Horovitz D (1992) Expression of disease resistance response genes in near-isogenic pea cultivars following challenge by Fusarium oxysporum race. Mol Plant Pathol 402:259–269

    Google Scholar 

  • Harmatha J, Dinan L (2003) Biological activities of lignans and stilbenoids associated with plant-insect chemical interaction. Phytochem Rev 2:231–330

    Article  Google Scholar 

  • Harper A, Kerr DJ, Gescher A, Chipman JK (1999) Antioxidant effects of isoflavanoids and lignans, and protection against DNA oxidation. Free Rad Res 31:149–160

    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 

  • Harris MO, Freeman TP, Anderson KG, Moore JA, Payne SA, Anderson KM, Rohfritsch O (2010) H gene-mediated resistance to Hessian fly exhibits features of penetration resistance to fungi. Phytopathology 100:279–289

    Article  PubMed  CAS  Google Scholar 

  • Hatchett JH, Gallun RL (1970) Genetics of the ability of the Hessian fly, Mayetiola destructor (Say), to survive on wheats having different genes for resistance. Ann Entomol Soc Am 63:1400–1407

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hückelhoven R (2007) Cell wall-associated mechanism of disease resistance and susceptibility. Annu Rev Phytopathol 45:101–127

    Article  PubMed  Google Scholar 

  • Klink VP, MacDonald M, Alkharouf N, Mathews BF (2005) Laser capture microdissection (LCM) and expression analyses of Glycine max (soybean) syncytium containing root regions formed by the plant pathogen Heterodera glycines (soybean cyst nematode). Plant Mol Biol 59:969–983

    Article  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  CAS  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

    PubMed  CAS  Google Scholar 

  • Kwon M, Davin LB, Lewis NG (2001) In situ hybridization and immunolocalization of lignan reductases in woody tissues: implications for heartwood formation and other forms of vascular tissue preservation. Phytochemistry 57:899–914

    Article  PubMed  CAS  Google Scholar 

  • Lee J, Parthier B, Lobler M (1996) Jasmonate signaling can be uncoupled from abscisic acid signaling in barley: identification of jasmonate-regulated transcripts which are not induced by abscisic acid. Planta 199:625–632

    Article  PubMed  CAS  Google Scholar 

  • Lippert D, Chowrira S, Ralph SG, Zhuang J, Aeschliman D, Ritland C, Ritland K, Bohlmann J (2007) Conifer defense against insects: proteome analysis of Sitka spruce (Picea sitchensis) bark induced by mechanical wounding or feeding by white pine weevils (Pissodes strobi). Proteomics 7:248–270

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Bai J, Zhu L, Liu X, Weng N, Reese JC, Harris MO, Stuart JJ, Chen M-S (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 

  • Liu X, Williams CE, Nemacheck JA, Wang H, Subramanyam S, Zheng C, Chen M-S (2010) Reactive oxygen species are involved in plant defense against a gall midge. Plant Physiol 152:985–999

    Article  PubMed  CAS  Google Scholar 

  • Page RD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 4:357–358

    Google Scholar 

  • Puthoff DP, Sardesai N, Subramanyam S, Nemacheck JA, Williams CE (2005) Hfr-2, a wheat cytolytic toxin-like gene, is up-regulated by virulent Hessian fly larval feeding. Mol Plant Pathol l6:411–423

    Article  Google Scholar 

  • Quentin M, Allasia V, Pegard A, Allais F, Ducrot P-H, Favery B, Levis C, Martinet S, Masur C, Ponchet M, Roby D, Schlaich NL, Jouanin L, Keller H (2009) Imbalanced lignin biosynthesis promotes the sexual reproduction of homothallic oomycete pathogens. PLoS Pathog 5:1–9

    Article  Google Scholar 

  • Rahman MM, Gray AI (2002) Antimicrobial constituents from the stem bark of Feronia limonia. Phytochemistry 59:73–77

    Article  PubMed  CAS  Google Scholar 

  • Ralph S, Park J-Y, Bohlmann J, Mansfield SD (2006) Dirigent proteins in conifer defense: gene discovery, phylogeny, and differential wound- and insect-induced expression of a family of DIR and DIR-like genes in spruce (Picea spp.). Plant Mol Biol 60:21–40

    Article  PubMed  CAS  Google Scholar 

  • Ralph SG, Jancsik S, Bohlmann J (2007) Dirigent proteins in conifer defense II: extended gene discovery, phylogeny, and constitutive and stress-induced gene expression in spruce (Picea spp.). Phytochemistry 68:1975–1991

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  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  PubMed  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 

  • Sears RG, Hatchett JH, Cox TS, Gill BS (1992) Registration of Hamlet, a Hessian fly resistant hard red winter wheat germplasm. Crop Sci 32:506

    Article  Google Scholar 

  • Shi H, Liu Z, Zhu L, Zhang C, Chen Y, Zhou Y, Li F, Li X (2012) Overexpression of cotton (Gossypium hirsutum) dirigent1 gene enhances lignification that blocks the spread of Verticillium dahliae. Acta Biochim Biophys Sin 44:555–564

    Article  PubMed  CAS  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 566:754–760

    Article  Google Scholar 

  • Smiley RW, Gourlie JA, Whittaker BG, Easley A, Kidwell KK (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 

  • 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

    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 DF, 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 larvae. Plant Physiol 147:1412–1426

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Piewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nuc Acids Res 25:4876–4882

    Article  CAS  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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wu J-X, Liu X, Zhang S, Zhu Y-C, Whiteworth RJ, Chen M-S (2008) Differential responses of wheat inhibitor-like genes to Hessian fly Mayetiola destructor, attacks during compatible and incompatible interactions. J Chem Ecol 34:1005–1012

    Article  PubMed  CAS  Google Scholar 

  • Wu RH, Wang LL, Wang Z, Shang HH, Liu X, Zhu Y, Qi DD, Deng X (2009) Cloning and expression analysis of a dirigent protein gene from the resurrection plant Boea hydrometrica. Prog Nat Sci 19:347–352

    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 gene conferring resistance to Hessian fly. Genome 54:81–89

    Article  PubMed  CAS  Google Scholar 

  • Zhu L, Zhang X, Tu L, Zeng F, Nie Y, Guo X (2007) Isolation and characterization of two novel dirigent-like genes highly induced in cotton (Gossypium barbadense and G. hirsutum) after infection by Verticillium dahliae. J Plant Pathol 89:41–45

    CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Zulak KG, Weljie AM, Vogel HJ, Facchiini PJ (2008) Quantitative 1H NMR metabolomics reveals extensive metabolic reprogramming of primary and secondary metabolism in elicitor-treated opium poppy cell cultures. BMC Plant Biol 8:5

    Article  PubMed  Google Scholar 

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Acknowledgments

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 3602-22000-016-D. The authors wish to thank Jill Nemacheck (USDA-ARS) for plant growth and tissue collections, Sue Cambron (USDA-ARS) for maintaining Hessian fly stocks, and Alisha Johnson (USDA-ARS) for assistance with phylogenetic analysis. Mention of commercial or proprietary product does not constitute endorsement or recommendation for its use by the USDA.

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Correspondence to Christie E. Williams.

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Subramanyam, S., Zheng, C., Shukle, J.T. et al. Hessian fly larval attack triggers elevated expression of disease resistance dirigent-like protein-encoding gene, HfrDrd, in resistant wheat. Arthropod-Plant Interactions 7, 389–402 (2013). https://doi.org/10.1007/s11829-013-9253-4

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