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Transgenic Expression of a Functional Fragment of Harpin Protein Hpa1 in Wheat Represses English Grain Aphid Infestation |
XU Man-yu, ZHOU Ting, ZHAO Yan-ying, LI Jia-bao, XU Heng, DONG Han-song , ZHANG Chun-ling |
National Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education/College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, P.R.China |
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摘要 The harpin protein Hpa1 produced by the rice bacterial blight pathogen promotes plant growth and induces plant resistance to pathogens and insect pests. The region of 10-42 residues (Hpa110-42) in the Hpa1 sequence is critical as the isolated Hpa110-42 fragment is 1.3-7.5-fold more effective than the full length in inducing plant growth and resistance. Here we report that transgenic expression of Hpa110-42 in wheat induces resistance to English grain aphid, a dominant species of wheat aphids. Hpa110-42-induced resistance is effective to inhibit the aphid behavior in plant preference at the initial colonization stage and repress aphid performances in the reproduction, nymph growth, and instar development on transgenic plants. The resistance characters are correlated with enhanced expression of defense-regulatory genes (EIN2, PP2-A, and GSL10) and consistent with induced expression of defense response genes (Hel, PDF1.2, PR-1b, and PR-2b). As a result, aphid infestations are alleviated in transgenic plants. The level of Hpa110-42-induced resistance in regard to repression of aphid infestations is equivalent to the effect of chemical control provided by an insecticide. These results suggested that the defensive role of Hpa110-42 can be integrated into breeding germplasm of the agriculturally significant crop with a great potential of the agricultural application.
Abstract The harpin protein Hpa1 produced by the rice bacterial blight pathogen promotes plant growth and induces plant resistance to pathogens and insect pests. The region of 10-42 residues (Hpa110-42) in the Hpa1 sequence is critical as the isolated Hpa110-42 fragment is 1.3-7.5-fold more effective than the full length in inducing plant growth and resistance. Here we report that transgenic expression of Hpa110-42 in wheat induces resistance to English grain aphid, a dominant species of wheat aphids. Hpa110-42-induced resistance is effective to inhibit the aphid behavior in plant preference at the initial colonization stage and repress aphid performances in the reproduction, nymph growth, and instar development on transgenic plants. The resistance characters are correlated with enhanced expression of defense-regulatory genes (EIN2, PP2-A, and GSL10) and consistent with induced expression of defense response genes (Hel, PDF1.2, PR-1b, and PR-2b). As a result, aphid infestations are alleviated in transgenic plants. The level of Hpa110-42-induced resistance in regard to repression of aphid infestations is equivalent to the effect of chemical control provided by an insecticide. These results suggested that the defensive role of Hpa110-42 can be integrated into breeding germplasm of the agriculturally significant crop with a great potential of the agricultural application.
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Received: 18 October 2013
Accepted:
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Fund: This study was supported by the Programme of Introducing Talents of Discipline to Universities, Ministry of Education of China (111 Project). |
Corresponding Authors:
ZHANG Chun-ling, Tel: +86-25-84399057, E-mail: zhangcl@njau.edu.cn
E-mail: zhangcl@njau.edu.cn
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About author: XU Man-yu, Tel: +86-25-84399005, E-mail: xu_manyu@163.com |
Cite this article:
XU Man-yu, ZHOU Ting, ZHAO Yan-ying, LI Jia-bao, XU Heng, DONG Han-song , ZHANG Chun-ling.
2014.
Transgenic Expression of a Functional Fragment of Harpin Protein Hpa1 in Wheat Represses English Grain Aphid Infestation. Journal of Integrative Agriculture, 13(12): 2565-2576.
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Alonso J M, Hirayama T, Roman G, Nourizadeh S, Ecker JR. 1999. EIN2, a bifunctional transducer of ethylene andstress responses in Arabidopsis. Science, 284, 2148-2152Chen L, Long J, Zhang S S, Qu S, Yin Q, Qian J, Wu X, SunF, Wu T, Cheng Z, Beer S V, Dong H. 2008a. A fragmentof the Xanthomonas oryzae pv. oryzicola harpin HpaGXoocreduces disease and increases yield of rice in extensivegrower plantings. Phytopathology, 98, 792-802Chen L, Qian J, Qu S P, Long J Y, Yin Q, Zhang CL, Wu X J,Sun F, Wu T Q, Beer S V, Dong H. 2008b. Identificationof specific fragments of HpaGXooc, a harpin protein fromXanthomonas oryzae pv. oryzicola, that induce diseaseresistance and enhanced growth in rice. Phytopathology,98, 781-791Dangl J L, Dietrich R A, Richberg M H. 1996. Death don’thave no mercy: Cell death programs in plant-microbeinteractions. The Plant Cell, 8, 1793-1807Dinant S, Clark A M, Zhu Y, Vilaine F, Palauqui J C, KusiakC, Thompson G A. 2003. Diversity of the superfamily ofphloem lectins (phloem protein 2) in angiosperms. PlantPhysiology, 131, 114-128Dong H, Delaney T P, Bauer D W, Beer S V. 1999. Harpininduces disease resistance in Arabidopsis through thesystemic acquired resistance pathway mediated by salicylicacid and the NIM1 gene. The Plant Journal, 20, 207-215Dong H P, Peng J L, Bao Z L, Meng X D, Bonasera J M, ChenG Y, Beer SV, Dong H. 2004. Downstream divergenceof the ethylene signaling pathway for harpin-stimulatedArabidopsis growth and insect defense. Plant Physiology,136, 3628-3638Dong H P, Yu H Q, Bao Z L, Guo X J, Peng J L, Yao Z, ChenG Y, Dong H. 2005. The ABI2-dependent abscisic acidsignalling controls HrpN-induced drought tolerance inArabidopsis. Planta, 221, 313-327Fu M Q, Xu M Y, Zhou T, Wang D F, Tian S, Han B, Dong HS, Zhang C L. 2014. Transgenic expression of a functionalfragment of harpin protein Hpa1 in wheat induces thephloem-based defense to English grain aphid. Journal ofExperimental Botany, 65, 1439-1543He S Y, Huang H C, Collmer A. 1993. Pseudomonas syringaepv. syringae harpinPss: A protein that is secreted via the Hrppathway and elicits the hypersensitive response in plants.Cell, 73, 1255-1266de Ilarduya O M, Xie Q G, Kaloshian I. 2003. Aphid-induceddefense responses in Mi-1-mediated compatible andincompatible tomato interactions Molecular Plant-Microbe Interactions, 16, 699-708Jung C, Seo J S, Han SW, Koo Y J, Kim C H, Song S I, NahmB H, Choi Y D, Cheong J J. 2008. Overexpression ofAtMYB44 enhances stomatal closure to confer abiotic stresstolerance in transgenic Arabidopsis. Plant Physiology,146, 623-635Jung C, Shim J S, Seo J S, Lee H Y, Kim C H, Choi Y D,Cheong J J. 2010. Non-specific phytohormonal inductionof AtMYB44 and suppression of jasmonate-responsive geneactivation in Arabidopsis thaliana. Molecular and CellularBiochemistry, 29, 71-76Kehr J. 2006. Phloem sap proteins: Their identities andpotential roles in the interaction between plants andphloem-feeding insects. Journal of Experimental Botany,57, 767-774Kim J F, Beer S V. 2000. Hrp genes and harpins of Erwiniaamylovora: A decade of discovery. In: Vanneste J L, ed.,Fire Blight and its Causative Agent, Erwinia Amylovora.CAB International, Wallingford, UK. pp. 141-162Li X J, Wang D F, Cai H S, Liu C L, Dong H, Zhang C L.2014. Transgenic expression of an active fragment of theharpin protein Hpa1 in wheat reduces Fusarium head blight.Acta Phytophylogica Sinica, 1, 25-34 (in Chinese)Liu F Q, Liu H X, Jia Q, Guo X J, Zhang S J, Wu X J, Song F,Dong H. 2006. The internal glycine-rich motif and cysteinesuppress several effects of the HpaGXooc protein in plants.Phytopathology, 96, 1052-1059Liu R X, Chen L, Jia Z H, Lü B B, Dong H. 2011. Transcriptionfactor AtMYB44 regulates induced expression ofthe ETHYLENE INSENSITIVE2 gene in Arabidopsisresponding to a harpin protein. Molecular Plant-MicrobeInteractions, 24, 377-389Liu R X, Lü B B, Wang X M, Zhang C L, Zhang S P,Qian J, Chen L, Shi H J, Dong H S. 2010. Thirty-seventranscription factor genes differentially respond to a harpinprotein and affect resistance to the green peach aphid inArabidopsis. Journal of Biosciences, 35, 435-450Lü B B, Li X J, Sun W W, Li L, Gao R, Zhu Q, Tian S M, FuM Q, Yu H L, Tang X M, Zhang C L. 2013. AtMYB44regulates resistance to the green peach aphid anddiamondback moth by activating EIN2-affected defensesin Arabidopsis. Plant Biology (Stuttg), 15, 841-850Lü B B, Sun W W, Zhang S P, Zhang C L, Qian J, Wang X M,Gao R, Dong H. 2010. HrpNEa-induced deterrent effect onphloem feeding of the green peach aphid Myzus persicaerequires AtGSL5 and AtMYB44 genes in Arabidopsisthaliana. Journal of Biosciences, 36, 123-137Miao W G, Wang X B, Li M, Song C F, Wang Y, Hu D W,Wang J S. 2010a. Genetic transformation of cotton with aharpin-encoding gene hpaXoo confers an enhanced defenseresponse against different pathogens through a primingmechanism. BMC Plant Biology, 10, 67.Miao W G, Wang X B, Song C F, Wang Y, Ren Y H, Wang JS. 2010b. Transcriptome analysis of Hpa1Xoo transformedcotton revealed constitutive expression of genes in multiplesignalling pathways related to disease resistance. Journalof Experimental Botany, 61, 4263-4275Mukhtar M S, Nishimura M T, Dangl J 2009. NPR1 in plantdefense: It’s not over ‘til it’s turned over. Cell, 137, 804-806Peng J L, Bao Z L, Ren H Y, Wang J S, Dong H. 2004.Expression of harpinXoo in transgenic tobacco inducespathogen defense in the absence of hypersensitiveresponse. Phytopathology, 94, 1048-1055Peng J L, Dong H, Dong H P, Delaney T P, Bonasera B M, Beer S V. 2003. Harpin-elicited hypersensitive cell death andpathogen resistance requires the NDR1 and EDS1 genes.Physiology Molecular Plant Pathology, 62, 317-326Qiao H, Chang K N, Yazaki J, Ecker J R. 2009. Interplaybetween ethylene, ETP1/ETP2 F-box proteins, anddegradation of EIN2 triggers ethylene responses inArabidopsis. Genes Development, 23, 512-521Qiao H, Shen Z, Huang S S, Schmitz R J, Urich M A, Briggs SP, Ecker J R. 2012. Processing and subcellular traffickingof ER-tethered EIN2 control response to ethylene gas.Science, 338, 390-393Read S M, Northcote D H. 1983. Subunit structure andinteractions of the phloem proteins of Cucurbita maxima(pumpkin). European Journal of Biochemistry, 134, 561-569Ren H Y, Gu G Y, Long J Y, Yin Q, Wu T Q, Song T, ZhangS J, Chen Z Y, Dong H. 2006a. Combinative effects of abacterial type-III effector and a biocontrol bacterium onrice growth and disease resistance. Journal of Biosciences,31, 617-627Ren H Y, Song T, Wu T Q, Sun L J, Liu Y X, Yang F F, ChenZ Y, Dong H. 2006b. Effects of a biocontrol bacteriumon transgenic rice plants expressing a bacterial type-IIIeffector. Annals of Microbiology, 56, 281-287Sang S L, Li X J, Gao R, You Z Z, Lü B B, Liu P Q, Ma QX, Dong H. 2012. Apoplastic and cytoplasmic locationof harpin protein Hpa1Xoo plays different roles in H2O2generation and pathogen resistance in Arabidopsis. PlantMolecular Biology, 79, 375-391Spoel S H, Mou Z, Tada Y, Spivey N W, Genschik P, Dong X.2009. Proteasome-mediated turnover of the transcriptioncoactivator NPR1 plays dual roles in regulating plantimmunity. Cell, 137, 860-872Stone B A, Clarke A E. 1992. Chemistry and physiology ofhigher plant 1,3-β-glucans (callose). In: Stone B A, ClarkeA E, eds., Chemistry and Biology of 1,3-β-glucans. LaTrobe University Press, Bundoora, Australia. pp. 365-429Taketa S, Yuo T, Tonooka T, Tsumuraya Y, Inagaki Y,Haruyama N, Larroque O, Jobling S A. 2012. Functionalcharacterization of barley betaglucanless mutantsdemonstrates a unique role for CslF6 in (1,3;1,4)-β-Dglucanbiosynthesis. Journal of Experimental Botany, 63,381-392Tjallingii W F. 1987. Electrical recording of stylet penetrationactivities. In: Minks A K, Harrewijn P, eds., Aphids: TheirBiology, Natural Enemies and Control. Vol 2B. Elsevier,Amsterdam. pp. 95-108Tjallingii W F. 2006. Salivary secretions by aphids interactingwith proteins of phloem wound responses. Journal ofExperimental Botany, 57, 739-745Voigt C A, Schäfer W, Salomon S. 2006. A comprehensiveview on organ-specific callose synthesis in wheat (Triticumaestivum L.): Glucan synthase-like gene expression, callosesynthase activity, callose quantification and deposition.Plant Physiology & Biochemistry, 44, 242-247de Vos M, Jander G. 2009. Myzus persicae (green peachaphid) salivary components induce defence responsesin Arabidopsis thaliana. Plant, Cell & Environment, 32,1548-1560Wang X Y, Song C F, Miao W G, Ji Z L, Wang X, Zhang Y,Zhang J H, Hu J S, Borth W, Wang J S. 2008. Mutationsin the N-terminal coding region of the harpin protein Hpa1from Xanthomonas oryzae cause loss of hypersensitivereaction induction in tobacco. Applied Microbiology andBiotechnology, 81, 359-369Wei Z M, Lacy R J, Zumoff C H, Bauer D W, He S Y, CollmerA, Beer S V. 1992. Harpin, elicitor of the hypersensitiveresponse produced by the plant pathogen Erwiniaamylovora. Science, 257, 85-88Will T, van Bel A J. 2008. Induction as well as suppression:How aphid saliva may exert opposite effects on plantdefense. Plant Signaling & Behavior, 3, 427-430Will T, van Bel A J E. 2006. Physical and chemical interactionsbetween aphids and plants. Journal of ExperimentalBotany, 57, 729-737Wu X J, Wu T, Long J Y, Yin Q, Zhang Y, Chen L, LiangY, Liu R X, Gao T, Dong H. 2007. Productivity andbiochemical properties of green tea in response to abacterial type-III effector protein and its variants. Journalof Biosciences, 32, 1119-1132Yang M, Qin B P, Liu C L, Cai H S, Wang Z L, Liang Y C,Yin Y P. 2013. The molecular identification of transgenicHpa110-42 wheat and resistance evaluation on FusariumHead Blight Scientia Agricultura Sinica, 46, 657-667 (in Chinese)Yu I C, Parker J, Bent A F. 1998. Gene-for-gene diseaseresistance without the hypersensitive response inArabidopsis dnd1 mutant. Proceedings of the NationalAcademy of Sciences of the United States of America, 95,7819-7824Zhang C L, Shi H J, Chen L, Wang X M, Lü B B, Zhang SP, Liang Y, Liu R X, Qian J, Sun W W, You Z Z, DongH. 2011a. Harpin-induced expression and transgenicoverexpression of the phloem protein gene AtPP2-A1 inArabidopsis repress phloem feeding of the green peachaphid Myzus persicae. BMC Plant Biology, 11, 11.Zhang C L, Xiao S, Li W, Feng W, Li J, Wu Z, Gao X, LiuF, Shao M. 2011b. Overexpression of a Harpin-encodinggene hrf1 in rice enhances drought tolerance. Journal ofExperimental Botany, 62, 4229-4238Zhang C L, Fu M Q, Xu H, Dong H. 2012. Transcriptionalregulation of Arabidopsis phloem defenses as a paradigm toexplore molecular mechanism underlying wheat resistanceto aphids. Jounal of Nanjing Agricultural University, 35,113-124. ( in Chinese)Zhu W G, Magbanua M M, White F F. 2000. Identificationof two novel hpaG-associated genes in the hpaG genecluster of Xanthomonas oryzae pv. oryzae. Journal ofBacteriology, 182, 1844-1853. |
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