小麦赤霉病抗性机理研究进展

doi:10.3864/j.issn.0578-1752.2016.08.005

摘要/Abstract

摘要： 赤霉病（Fusarium head blight，FHB）是小麦最主要的病害之一，严重影响小麦生产安全和食品安全，研究小麦赤霉病抗性机理对于解决小麦赤霉病这一世界性难题具有重要意义。根据对赤霉病的抗性表现形式，将小麦赤霉病抗性分为五个大类，分别为抗侵入（Type I）、抗扩展（Type II）、籽粒抗感染（Type III）、耐病性（Type Ⅳ）和抗毒素积累（Type V）。小麦赤霉病的抗性机理可以分为形态机制和生理机制，形态抗性机制是被动的，株高、抽穗期、花期长短、花药挤出程度、有芒无芒、穗长、穗密度、颖壳张开程度和穗部蜡质程度等形态特征均可能与赤霉病抗侵染特性有关。细胞学研究表明，病原菌侵染后抗病品种可迅速从细胞结构和生理生化方面产生防卫反应，通过乳突、胞壁沉积物的形成以及木质素、硫堇、富含羟脯氨酸糖蛋白和水解酶类等的增长来协同抵御病菌在体内的扩展。在植物复杂的信号途径中，水杨酸（SA）、茉莉酸（JA）和乙烯（ET）3种信号途径在植物抵御病原菌入侵中的作用最为重要，SA和ET信号途径对小麦赤霉病抗性方面的作用目前还存在一定争议，而JA信号途径在小麦赤霉病抗性中积极作用已经被多数研究者所证实。迄今为止，人类定位了200个以上不同类型的抗赤霉病QTL位点，这些位点分布于所有的小麦染色体，其中的22个QTL位点被不同的作图群体所定位，包括2个定位在3BS和6BS染色体上稳定的抗扩展位点Fhb1和Fhb2，以及2个定位在4B和5A染色体上的抗侵染位点Fhb4和Fhb5。在受到病原菌侵染后，植物会产生一系列复杂的信号途径激活应答反应，诱导抗病相关基因的表达，进而引起蛋白以及代谢水平的变化，抵御病原菌的侵袭，研究表明，病程相关蛋白基因、抗菌肽基因、转录因子基因、脱毒相关蛋白基因以及其他赤霉病抗性相关基因均参与了小麦赤霉病抗性提高的过程。随着生物工程技术和生物信息技术的迅猛发展，将来可利用图位克隆技术分离抗赤霉病主效基因，并在全基因组关联分析和各种组学技术的基础上，从全基因组和基因调控网络水平上研究小麦赤霉病抗性机理，以期在更深层次上理解小麦赤霉病的抗性机理。

关键词: 小麦, 赤霉病, QTL定位, 植物信号, 抗病基因

Abstract: Fusarium head blight (FHB) is one of the most important diseases of wheat worldwide, which poses a serious threat to wheat production and food safety. According to the form of wheat resistance to FHB, the resistance types can be divided into five categories: resistance against initial infection (Type I), resistance to pathogen spreading in infected tissue (Type II), resistance to kernel infection(Type III), tolerance(Type Ⅳ) and resistance to toxins in ears by decomposing them(Type V). Resistance mechanism types are usually classified into either morphological or physiological, and the morphological resistance mechanism is synonymous with passive. Wheat morphological characteristics including plant height, heading date and flowering duration, anther extrusion, presence or absence of awns, ear length and density, flower opening width and waxy surfaces on ear tissue may be related to resistance against initial infection. Cytological studies showed that the resistant varieties infected by pathogen can make rapidly defense response by the cell structure, physiological and biochemical responses. The formation of thick-layered appositions and papillae and the increase of lignin, thionins, hydroxyproline-rich glycoproteins and hydrolytic enzymes are cooperated to resist the pathogen development in the resistant varieties. In the complex plant signaling pathways, three signaling pathways including salicylic acid (SA), jasmonic acid (SA) and ethylene (ET) play the most important role in the antifungal response of plant. The role of SA and ET signaling pathways in wheat resistance to FHB is still in controversy, and the positive role of JA signaling pathway has been confirmed by most of the researchers. So far, it is found that more than 200 FHB resistance quantitative trait loci (QTLs) are distributed on all 21 wheat chromosomes, among them 22 QTLs were mapped by different mapping populations, including two stable Type I sites Fhb1 and Fhb2 locating on chromosome 3BS and 6BS, respectively, and two stable Type II sites Fhb3 and Fhb4 locating on chromosome 4B and 5A, respectively. When infected by the plant will produce a series of complex signaling pathway to activate resistant response, and induce the expression of defense-related genes, thereby causing protein and metabolic changes to resist the invasion of pathogen. Studies have indicated that the pathogenesis-related genes, antimicrobial peptide genes, transcription factor genes, detoxification-related genes and other FHB resistance genes are involved in the process of wheat resistance to FHB. In the future, major genes controlling FHB resistance can be cloned by map-based cloning technology, and based on genome-wide association studies and various omics techniques, the mechanism of wheat FHB resistance will be studied on whole genome and gene regulatory network level. This paper can provide a reference for the related research on resistance mechanism to FHB in wheat.

Key words: wheat; fusarium head blight, QTL location, plant signal, resistance genes

刘易科，佟汉文，朱展望，陈泠，邹娟，张宇庆，高春保. 小麦赤霉病抗性机理研究进展[J]. 中国农业科学, 2016, 49(8): 1476-1488.

LIU Yi-ke, TONG Han-wen, ZHU Zhan-wang, CHEN Ling, ZOU Juan, ZHANG Yu-qing, GAO Chun-bao. Progress in Research on Mechanism of Resistance to Fusarium Head Blight in Wheat[J]. Scientia Agricultura Sinica, 2016, 49(8): 1476-1488.

0
/ / 推荐

导出引用管理器 EndNote|Reference Manager|ProCite|BibTeX|RefWorks

链接本文: https://www.chinaagrisci.com/CN/10.3864/j.issn.0578-1752.2016.08.005

https://www.chinaagrisci.com/CN/Y2016/V49/I8/1476

参考文献

[1] Nopsa J F H, Baenziger P S, Eskridge K M, Peiris K M, Kamarange H S, Dowell F E, Harris S D, Wegulo S N. Differential accumulation of deoxynivalenol in two winter wheat cultivars varying in FHB phenotype response under field conditions. Canadian Journal of Plant Pathology, 2012, 34: 380-389.

[2] Bai G, Shaner G. Management and resistance in wheat and barley to Fusarium head blight 1. Annual Review of Phytopathology, 2004, 42: 135-161.

[3] Foroud N A, Eudes F. Trichothecenes in cereal grains. International Journal of Molecular Sciences, 2009, 10: 147-173.

[4] 程顺和, 张勇, 别同德, 高德荣, 张伯桥. 中国小麦赤霉病的危害及抗性遗传改良. 江苏农业学报, 2012, 28: 938-942.

Cheng S H, Zhang Y, Bie T D, Gao D R, Zhang B Q. Damage of wheat Fusarium head blight (FHB) epidemics and genetic improvement of wheat for scab resistance in China. Jiangsu Journal of Agricultural Sciences, 2012, 28: 938-942. (in Chinese)

[5] 刘易科. 小麦内标准基因的开发及抗赤霉病转基因小麦转录组分析[D]. 武汉: 华中农业大学, 2015.

Liu Y K. Development of an endogenous reference gene in wheat and transcriptome analyses of transgenic wheat resistant to Fusarium head blight [D]. Wuhan: Huazhong Agriculture University, 2015. (in Chinese)

[6] Ban T. Analysis of quantitative trait loci associated with resistance to Fusarium head blight caused by Fusarium graminearum Schwabe and of resistance mechanisms in wheat (Triticum aestivum L.). Breeding Science, 2000, 50: 131-137.

[7] Rudd J C, Horsley R D, McKendry A L, Elias E M. Host plant resistance genes for Fusarium head blight: Sources, mechanisms, and utility in conventional breeding systems. Crop Science, 2001, 41: 620-627.

[8] Gilsinger J, Kong L, Shen X, Ohm H. DNA markers associated with low Fusarium head blight incidence and narrow flower opening in wheat. Theoretical and Applied Genetics, 2005, 110: 1218-1225.

[9] Buerstmayr H, Adam G, Lemmens M. Resistance to head blight caused by Fusarium spp. in wheat. Disease Resistance in Wheat, 2012, 1: 236.

[10] Zhang X, Fu J, Hiromasa Y, Pan H, Bai G. Differentially expressed proteins associated with Fusarium head blight resistance in wheat. PloS One, 2013, 8: e82079.

[11] Van Eeuwijk E A, Mesterhazy A, Kling C I, Ruc-kenbauer P, Saur L, Buerstmayr H, Lemmens M, Keizer L C P, Maurin N, Snijders C H. Assessing non-specificity of resistance in wheat to head blight caused by inoculation with European stains of Fusarium culmorum, F. graminearum and M. nivale using a multiplicative model for interaction. Theoretical and Applied Genetics, 1995, 90: 221-228.

[12] Buerstmayr M, Buerstmayr H. Comparative mapping of quantitative trait loci for Fusarium head blight resistance and anther retention in the winter wheat population Capo×Arina. Theoretical and Applied Genetics, 2015: 1-12.

[13] Long X Y, Balcerzak M, Gulden S, Cao W Q, Fedak G, Wei Y M, Zheng Y L, Somers D, Ouellet D. Expression profiling identifies differentially expressed genes associated with the Fusarium head blight resistance QTL 2DL from the wheat variety Wuhan-1. Physiological and Molecular Plant Pathology, 2015, 90: 1-11.

[14] Walter S, Nicholson P, Doohan F M. Action and reaction of host and pathogen during Fusarium head blight disease. New Phytologist, 2010, 185: 54-66.

[15] Schroeder H W, Christensen J J. Factors affecting resistance of wheat to scab caused by Gibberella zeae. Phytopathology, 1963, 53: 831-838.

[16] Mesterhazy A. Types and components of resistance to Fusarium head blight of wheat. Plant Breeding,1995, 114: 377-386.

[17] Miller J D, Young J C, Sampson D R. Deoxynivalenol and Fusarium head blight resistance in spring cereals. Journal of Phytopathology, 1985, 113: 359-367.

[18] Boutigny A L, Richard-Forget F, Barreau C. Natural mechanisms for cereal resistance to the accumulation of Fusarium trichothecenes. European Journal of Plant Pathology, 2008, 121: 411-423.

[19] Gilbert J, Tekauz A. Review: Recent developments in research on Fusarium head blight of wheat in Canada. Canadian Journal of Plant Pathology, 2000, 22: 1-8.

[20] Foroud N A. Investigating the molecular mechanisms of Fusarium head blight resistance in wheat [D]. Vancouver: University British Columbia, 2011.

[21] Mesterházy Á, Leonard K J, Bushnell W R. Breeding wheat for Fusarium head blight resistance in Europe. Fusarium Head Blight of Wheat and Barley, 2003: 211-240.

[22] Graham S, Browne R A. Anther extrusion and Fusarium head blight resistance in European wheat. Journal of Phytopathology, 2009, 157: 580-582.

[23] Schmolke M, Zimmermann G, Buerstmayr H, Schweizer G, Miedaner T, Korzun V, Ebmeyer E, Hartl L. Molecular mapping of Fusarium head blight resistance in the winter wheat population Dream/Lynx. Theoretical and Applied Genetics, 2005, 111: 747-756.

[24] Gautam P, Halley S, Stein J M. Contribution of primary spikes vs tillers to total deoxynivalenol in harvested grain of wheat and barley. American Journal of Agricultural and Biological Science, 2012, 7: 293-300.

[25] Draeger R, Gosman N, Steed A, Chandler E, Thomsett M, Srinivasachary, Schondelmaier J, Buerstmayr H, Lemmens M, Schmolke M, Mesterhazy A, Nicholson P. Identification of QTLs for resistance to Fusarium head blight, DON accumulation and associated traits in the winter wheat variety Arina. Theoretical and Applied Genetics, 2007, 115: 617-625.

[26] Liu S, Griffey C A, Hall M D, McKendry A L, Chen J L, Brooks W S, Brown-Guedira G, Sanford D V, Schmale D G. Molecular characterization of field resistance to Fusarium head blight in two US soft red winter wheat cultivars. Theoretical and Applied Genetics, 2013, 126: 2485-2498.

[27] He X Y, Singh P K, Schlang N, Duveiller E, Dreisigacker S, Payne T, He Z H. Characterization of Chinese wheat germplasm for resistance to Fusarium head blight at CIMMYT, Mexico. Euphytica, 2014, 195: 383-395.

[28] Chu C, Niu Z, Zhong S, Chao S, Friesen T, Halley S, Elias E M, Dong Y, Faris J D, Xu S S. Identification and molecular mapping of two QTLs with major effects for resistance to Fusarium head blight in wheat. Theoretical and Applied Genetics, 2011, 123: 1107-1119.

[29] Suzuki T, Sato M, Takeuchi T. Evaluation of the effects of five QTL regions on Fusarium head blight resistance and agronomic traits in spring wheat (Triticum aestivum L.). Breeding Science, 2012, 62: 11.

[30] Skinnes H, Tarkegne Y, Dieseth J, Bjørnstad A. Associations between anther extrusion and Fusarium head blight in European wheat. Cereal Research Communications, 2008, 36(Suppl.6): 223-231.

[31] Skinnes H, Semagn K, Tarkegne Y, Marøy A G, Bjørnstad A. The inheritance of anther extrusion in hexaploid wheat and its relationship to Fusarium head blight resistance and deoxynivalenol content. Plant Breeding, 2010, 129: 149-155.

[32] Buerstmayr M, Huber K, Heckmann J, Steiner B, Nelson J C, Buerstmayr H. Mapping of QTL for Fusarium head blight resistance and morphological and developmental traits in three backcross populations derived from Triticum dicoccum×Triticum durum. Theoretical and Applied Genetics, 2012, 125: 1751-1765.

[33] Lu Q, Lillemo M, Skinnes H, He X, Shi J, Ji F, Dong Y, Bjørns Å. Anther extrusion and plant height are associated with Type I resistance to Fusarium head blight in bread wheat line ‘Shanghai-3/Catbird’. Theoretical and Applied Genetics, 2013, 126: 317-334.

[34] Kubo K, Kawada N, Fujita M, Hatta K, Oda S, Nakajima T. Effect of cleistogamy on Fusarium head blight resistance in wheat. Breeding Science, 2010, 60: 405-411.

[35] Kubo K, Kawada N, Fujita M. Evaluation of Fusarium head blight resistance in wheat and the development of a new variety by integrating type I and II resistance. Japan Agricultural Research Quarterly, 2013, 47: 9-19.

[36] Kang Z S, Huang L L, Buchenauer H, Han Q M, Jiang X L. Cytology of infection process of Fusarium graminearum on wheat spikes. Acta Phytopathologica Sinica, 2004, 34: 329-335.

[37] Zhang X, Lee T, Dufresne M, Liu T, Lu W, Yu D, Ma H. Infection of green fluorescence protein-tagged Fusarium graminearum on wheat and barley spikes. Cereal Research Communications, 2008, 36(Suppl.6): 465-469.

[38] Kang Z, Buchenauer H. Ultrastructural and immunocytochemical investigation of pathogen development and host responses in resistant and susceptible wheat spikes infected by Fusarium culmorum. Physiological and Molecular Plant Pathology, 2000, 57: 255-268.

[39] Kang Z, Buchenauer H. Immunocytochemical localization of beta-1, 3-glucanase and chitinase in Fusarium culmorum-infected wheat spikes. Physiological and Molecular Plant Pathology, 2002, 60: 141-153.

[40] Kang Z, Buchenauer H. Immunocytochemical localization of cell wall-bound thionins and hydroxyproline-rich glycoproteins in fusarium culmorum-infected wheat spikes. Journal of Phytopathology, 2003, 151: 120-129.

[41] Kang Z, Buchenauer H, Huang L, Han Q, Zhang H. Cytological and immunocytochemical studies on responses of wheat spikes of the resistant Chinese cv. Sumai 3 and the susceptible cv. Xiaoyan 22 to infection by Fusarium graminearum. European Journal of Plant Pathology, 2008, 120: 383-396.

[42] Lionetti V, Giancaspro A, Fabri E, GioveS L, Reem N, Zabotina O A, Blanco A, Gadaleta A, Bellincampi D. Cell wall traits as potential resources to improve resistance of durum wheat against Fusarium graminearum. BMC Plant Biology, 2015, 15: 6.

[43] Li G, Yen Y. Jasmonate and ethylene signaling pathway may mediate Fusarium head blight resistance in wheat. Crop Science, 2008, 48: 1888-1896.

[44] Ding L N, Xu H B, Yi H Y, Yang L M, Kong Z X, Zhang L X, Xue S L, Jia H Y, Ma Z Q. Resistance to hemi-biotrophic Fusarium graminearum infection is associated with coordinated and ordered expression of diverse defense signaling pathways. PloS One, 2011, 6: e19008.

[45] Foroud N A, Ouellet T, Laroche A, Oosterveen B, Jordan M C, Ellis B E, Eudes F. Differntial transcriptomic analysis of three wheat genotypes reveal different host response pathways associated with Fusarium head blight and trichothecene resistance. Plant Pathology, 2012, 61: 296-314.

[46] Makandar R, Nalam V, Chaturvedi R, Jeannotte R, Sparks A A, Shah J. Involvement of salicylate and jasmonates signaling pathways in Arabidopsis interaction with Fusarium graminearum. Molecular Plant-Microbe Interactions, 2010, 23: 861-870.

[47] Makandar R, Nalam V J, Lee H, Trick H N, Dong Y, Shah J. Salicylic acid regulates basal resistance to Fusarium head blight in wheat.Molecular Plant-Microbe Interactions, 2012,25: 431-439.

[48] Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology, 2005, 43: 205-207.

[49] Jansen C, Von Wettstein D, Schafer W, Kogel K H, Felk A, Maier F J. Infection patterns in barley and wheat spikes inoculated with wild- type and trichodiene synthase gene disrupted Fusarium graminearum. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102: 16892-16897.

[50] Rocheleau H J, Zheng W, Gulden S, Xu R, Wang L, Ouellet T. Comparative gene expression pro?ling of major plant hormone pathways during infection by Fusarium graminearum//Ouellet T, Leger D. Proceedings of the Sixth Canadian Workshop on Fusarium Head Blight. Ottawa, ON, Canada, 2009.

[51] Gottwald S, Samans B, Lück S, Friedt W. Jasmonate and ethylene dependent defence gene expression and suppression of fungal virulence factors: Two essential mechanisms of Fusarium head blight resistance in wheat? BMC Genomics, 2012, 13: 369.

[52] Xiao J, Jin X, Jia X, Wang H, Cao A, Zhao W, Pei H, Xue Z, He L, Chen Q, Wang X. Transcriptome-based discovery of pathways and genes related to resistance against Fusarium head blight in wheat landrace Wangshuibai. BMC Genomics, 2013, 14: 197.

[53] Makandar R, Essig J S, Schapaugh M A, Trick H N, Shah J. Genetically engineered resistance to Fusarium head blight in wheat by expression of Arapidopsis NPR1. Molecular Plant-Microbe Interactions, 2006, 19: 123-129.

[54] 马信. 小麦抗赤霉病相关基因的克隆及功能分析[D]. 泰安: 山东农业大学, 2014.

Ma X. Cloning and function analysis of FHB resistance--related genes from wheat [D]. Taian: Shandong Agricultural University, 2014. (in Chinese)

[55] Robert-Seilaniantz A, Grant M, Jones J D G. Hormone crosstalk in plant disease and defense: More than just jasmonate-salicylate antagonism. Annual Review of Phytopathology, 2011, 49: 317-343.

[56] Xue Y J, Tao L, Yang Z M. Aluminum-induced cell wall peroxidase activity and lignin synthesis are differentially regulated by jasmonate and nitric oxide. Journal of Agricultural and Food Chemistry, 2008, 56: 9676-9684.

[57] Jia H, Cho S, Muehlbauer G J. Transcriptome analysis of a wheat near-isogenic line pair carrying Fusarium head blight-resistant and-susceptible alleles. Molecular Plant-Microbe Interactions, 2009, 22: 1366-1378.

[58] Bleecker A B, Kende H. Ethylene: A gaseous signal molecule in plants. Annual Review of Cell and Developmental Biology, 2000, 16: 1-18.

[59] Bent A F, Innes R W, Ecker J R, Staskawicz B J. Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomona and Xanthomonas pathogens.Molecular Plant-Microbe Interactions, 1992, 5: 372-378.

[60] Hoffman T, Schmidt J S, Zheng X, Bent A F. Isolation of ethylene-insensitive soybean mutants that are altered in pathogen susceptibility and gene-for-gene disease resistance. Plant Physiology, 1999, 119: 935-950.

[61] Thomma B P H J, Eggermont K, Tierens K F J, Broekaert W F. Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiology, 1999, 121: 1093-1101.

[62] Gillespie M E, Brandt A S, Scofield S R. Ethylene-signaling is essential for basal resistance to Fusarium head blight in wheat// 2012 National Fusarium Head Blight Forum. Orlando, FL. ASAP Printing, Inc. 2012: 135.

[63] Chen X, Steed A, Travella S, Keller B, Nicholson P. Fusarium graminearum exploits ethylene signaling to colonize dicotyledonous and monocotyledonous plants. New Phytologist, 2009, 182: 975-983.

[64] Buerstmayr H, Ban T, Anderson J A. QTL mapping and marker- assisted selection for Fusarium head blight resistance in wheat: A review. Plant Breeding, 2009, 128: 1-26.

[65] Cativelli M, Lewis S, Appendino M L. A Fusarium head blight resistance quantitative trait locus on chromosome 7D of the spring wheat cultivar Catbird. Crop Science, 2013, 53: 1464-1471.

[66] Garvin D F, Porter H, Blankenheim Z J, Chao S, Dill-Macky R. A spontaneous segmental deletion from chromosome arm 3DL enhances Fusarium head blight resistance in wheat. Genome, 2015, 58: 479-488.

[67] Bonin C M, Kolb F L. Resistance to Fusarium head blight and kernel damage in a winter wheat recombinant inbred line population. Crop Science, 2009, 49: 1304-1312.

[68] Lin F, Kong Z X, Zhu H L, Xue S L, Wu J Z, Tian D G, Wei J B, Zhang C Q, Ma Z Q. Mapping QTL associated with resistance to Fusarium head blight in the Nanda2419×Wangshuibai population: I. Type II resistance. Theoretical and Applied Genetics, 2004, 109: 1504-1511.

[69] Zhou W, Kolb F L, Yu J, Bai G, Boze L K, Domier L L. Molecular characterization of Fusarium head blight resistance in Wangshuibai with simple sequence repeat and amplified fragment length polymorphism markers. Genome, 2004, 47: 1137-1143.

[70] Somers D J, Fedak G, Savard M. Molecular mapping of novel genes controlling Fusarium head blight resistance and deoxynivalenol accumulation in spring wheat. Genome, 2003, 46: 555-564.

[71] Cuthbert P A, Somers D J, Thomas J, Cloutier S, Brulé-Babel A. Fine mapping Fhb1, a major gene controlling Fusarium head blight resistance in bread wheat (Triticum aestivum L.). Theoretical and Applied Genetics, 2006, 112: 1465-1472.

[72] Pumphrey M O, Bemardo R, Anderson J A. Validating the Fhb1 QTL for Fusarium head blight resistance in near-isogenic wheat lines developed from breeding population. Crop Science, 2007, 47: 200-206.

[73] Anderson J A, Stack R W, Liu S, Waldron B L, Fjeld A D, Coyne C. DNA markers for Fusarium head blight resistance QTLs its two wheat populations. Theoretical and Applied Genetics, 2001, 102: 1164-1168.

[74] Yang Z, Gilbert J, Fedak G, Somers D J. Genetic characterization of QTL associated with resistance to Fusarium head blight in a doubled-haploid spring wheat population. Genome, 2005, 48: 187-196.

[75] Shen X, Zhou M, Lu W, Ohm H. Detection of Fusarium head blight resistance QTL in a wheat population using bulked segregant analysis. Theoretical and Applied Genetics, 2003, 106: 1041-1047.

[76] Cuthbert P A, Somers D J, Brulé-Babel A. Mapping of Fhb2 on chromosome 6BS: A gene controlling Fusarium head blight field resistance in bread wheat (Triticum aestivum L.). Theoretical and Applied Genetics, 2007, 114: 429-437.

[77] Liu S, Abate Z A, Lu H, Musket T, Davis G L, McKendry A L. QTL associated with Fusarium head blight resistance in the soft red winter wheat Ernie. Theoretical and Applied Genetics,2007, 115: 417-427.

[78] Jayatilake D V, Bai G H, Dong Y H. A novel quantitative trait locus for Fusarium head blight resistance in chromosome 7A of wheat. Theoretical and Applied Genetics, 2011, 122: 1189-1198.

[79] Zhang X, Bai G, Bockus W, Ji X, Pan H. Quantitative trait loci for Fusarium head blight resistance in US hard winter wheat cultivar Heyne. Crop Science, 2012, 52: 1187-1194.

[80] Qi L L, Pumphrey M O, Friebe B, Chen P D, Gill B S. Molecular cytogenetic characterization of alien introgressions with gene Fhb3 for resistance to Fusarium head blight disease of wheat. Theoretical and Applied Genetics, 2008, 117: 1155-1166.

[81] Zhang X, Shen X, Hao Y, Cai J, Ohm H W, Kong L. A genetic map of Lophopyrum ponticum chromosome 7E, harboring resistance genes to Fusarium head blight and leaf rust. Theoretical and Applied Genetics, 2011, 122: 263-270.

[82] Guo J, Zhang X, Hou Y, Cai J, Shen X, Zhou T, Xu H, Ohm H, Wang H, Li A, Han F, Wang H, Kong L. High-density mapping of the major FHB resistance gene Fhb7 derived from Thinopyrum ponticum and its pyramiding with Fhb1 by marker-assisted selection. Theoretical and Applied Genetics, 2015, 128: 2301-2316.

[83] Buerstmayr H, Steiner B, Hartl L, Griesser M, Angerer N, Lengauer D, Miedaner T, Schneider B, Lemmens M. Molecular mapping of QTLs for Fusarium head blight resistance in spring wheat: II. Resistance to fungal penetration and spread. Theoretical and Applied Genetics, 2003, 107: 503-508.

[84] Steiner B, Lemmens M, Griesser M, Scholz U, Schondelmaier J, Buerstmayr H. Molecular mapping of resistance to Fusarium head blight in the spring wheat cultivar Frontana. Theoretical and Applied Genetics, 2004, 109: 215-224.

[85] Lin F, Xue S L, Zhang Z Z, Zhang C Q, Kong Z X, Yao G Q, Tian D G, Zhu H L, Li C J, Cao Y, Wei J B, Luo Q Y, Ma Z Q. Mapping QTL associated with resistance to Fusarium head blight in the Nanda2419×Wangshuibai population: II Type I resistance. Theoretical and Applied Genetics, 2006, 112: 528-535.

[86] Xue S, Li G, Jia H, Xu F, Lin F, Tang M, Wang Y, An X, Xu H, Zhang L, Kong Z, Ma Z. Fine mapping Fhb4, a major QTL conditioning resistance to Fusarium infection in bread wheat (Triticum aestivum L.). Theoretical and Applied Genetics, 2010, 121: 147-156.

[87] Xue S, Xu F, Tang M, Zhou Y, Li G, An X, Lin F, Xu H, Jia H, Zhang L, Kong Z, Ma Z. Precise mapping Fhb5, a major QTL conditioning resistance to Fusarium infection in bread wheat (Triticum aestivum L.). Theoretical and Applied Genetics, 2011, 123: 1055-1063.

[88] Liu S, Hall M D, Griffey C A, McKendry A L. Meta-analysis of QTL associated with Fusarium head blight resistance in wheat. Crop Science, 2009, 49: 1955-1968.

[89] Abate Z A, Liu S, McKendry A L. Quantitative trait loci associated with deoxynivalenol content and kernel quality in the soft red winter wheat ‘Ernie’. Crop Science, 2008, 48: 1408-1418.

[90] Islam M S, Brown-Guedira G, Sanford D V, Ohm H, Dong Y, McKendry A L. Novel QTL associated with the Fusarium head blight resistance in Truman soft red winter wheat. Euphytica, 2016, 207: 571-592.

[91] Pritsch C, Vance C P, Bushnell W R, Somers D A, Hohn T M, Muehlbauer G J. Systemic expression of defense response genes in wheat spikes as a response to Fusarium graminearum infection. Physiological and Molecular Plant Pathology, 2001, 58: 1-12.

[92] Li W L, Faris J D, Muthukrishnan S, Liu D J, Chen P D. Isolation and characterization of novel cDNA clones of acidic chitinases and β-1, 3-glucanases from wheat spikes infected by Fusarium graminearum. Theoretical and Applied Genetics, 2001, 102: 353-362.

[93] Pritsch C, Muehlbauer G J, Bushnell W R, Somers D A, Vance C P. Fungal development and induction of defense response genes during early infection of wheat spikes by Fusarium graminearum. Molecular Plant-Microbe Interactions, 2000, 13: 159-169.

[94] Chen W P, Chen P D, Liu D J, Kynast R, Friebe B, Velazhahan R, Muthukrishnan S, Gill B S. Development of wheat scab symptoms is delayed in transgenic wheat plants that constitutively express a rice thaumatin-like protein gene. Theoretical and Applied Genetics, 1999, 99: 755-760.

[95] Mackintosh C A, Lewis J, Radmer L E, Shin S, Heinen S J, Smith L A, Wyckoff M N, Dill-Macky R, Evans C K, Kravchenko S, Baldridge G D, Zeyen R J, Muehlbauer G J. Overexpression of defense response genes in transgenic wheat enhances resistance to Fusarium head blight. Plant Cell Report, 2007, 26: 479-488.

[96] Shin S, Mackintosh C A, Lewis J, Heinen S J, Radmer L, Dill-Macky R, Baldridge G D, Zeyen R J, Muehlbauer G J. Transgenic wheat expressing a barley class II chitinase gene has enhanced resistance against Fusarium graminearum. Journal of Experimental Botany, 2008, 59: 2371-2378.

[97] Cheng W, Li H P, Zhang J B, Du H J, Wei Q Y, Huang T, Yang P, Kong X W, LiaoY C. Tissue-specific and pathogen-inducible expression of a fusion protein containing a Fusarium-specific antibody and a fungal chitinase protects wheat against Fusarium pathogens and mycotoxins. Plant Biotechnology Journal, 2015, 13: 664-674.

[98] Zasloff M. Antimicrobial peptides of multicellular organisms. Nature, 2002, 415: 389-395.

[99] Zhu X L, Li Z, Xu H J, Zhou M P, Du L P, Zhang Z Y. Overexpression of wheat lipid transfer protein gene TaLTP5 increases resistance to Cochilobolus sativus and Fusarium graminearum in transgenic wheat. Functional & Integrative Genomics, 2012, 12: 481-488.

[100]Terras F R G, Goderis I J, Van Leuven F, Vanderleyden J, Cammue B P A, Broekaert W F. In vitro antifungal activity of a radish (Raphanus sativus L.) seed protein homologous to nonspecific lipid transfer proteins.Plant Physiology, 1992, 100: 1055-1058.

[101]Thevissen K, Warnecke D C, François I E, Leipelt M, Heinz E, Ott C, Zähringer U, Thomma B P, Ferket K K, Cammue B P. Defensins from insects and plants interact with fungal glucosylceramides.Journal of Biological Inorganic Chemistry, 2004, 279: 3900-3905.

[102]Li Z, Zhou M P, Zhang Z Y, Ren L J, Du L P, Zhang B Q, Xu H J, Xin Z Y. Expression of a radish defensin in transgenic wheat confers increased resistance to Fusarium graminearum and Rhizoctonia cerealis. Functional & Integrative Genomics, 2011, 11: 63-70.

[103]Eulgem T. Regulation of the Arabidopsis defense transcriptome. Trends in Plant Science, 2005, 10: 71-78.

[104]Jalali B L, Bhargava S, Kamble A. Signal transduction and transcriptional regulation of plant defense responses. Journal of Phytopathology, 2006, 154: 65-74.

[105]刘欣, 蔡士宾, 张伯桥, 周淼平, 路妍, 吴继中, 杜丽璞, 李斯深, 臧淑江, 张增艳. 抗纹枯病、赤霉病的转TaPIEP1基因小麦的分子鉴定与选育. 作物学报, 2011, 37: 1144-1150.

Liu X, Cai S B, Zhang B Q, Zhou X P, Lu Y, Wu J Z, Du L P, Li S S, Zang S J, Zhang Z Y. Molecular detection and identification of TaPIEP1 transgenic wheat with enhanced-resistance to sharp eyespot and Fusarium head blight. Acta Agronomica Sinica, 2011, 37: 1144-1150. (in Chinese)

[106] Yang P Z, Chen C N, Wang Z P, Fan B F, Chen Z X. A pathogen- and salicylic acid-induced WRKY DNA-binding activity recognizes the elicitor response element of the tobacco class I chitinase gene promoter. The Plant Journal, 1999, 18: 141-149.

[107]Eulgem T, Rushton P J, Robatzek S, Somssich I E. The WRKY superfamily of plant transcription factors. Trends in Plant Science, 2000, 5: 199-206.

[108]Kim C Y, Zhang S. Activation of a mitogen-activated protein kinase cascade induces WRKY family of transcription factors and defense genes in tobacco. The Plant Journal, 2004, 38: 142-151.

[109]Yamamoto S, Nakano T, Suzuki K, Shinshi H. Elicitor-induced activation of transcription via W box-related cis-acting elements from a basic chitinase gene by WRKY transcription factors in tobacco. Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression, 2004, 1679: 279-287.

[110]Bahrini I, Sugisawa M, Kikuchi R, Ogawa T, Kawahigashi H, Ban T, Handa H. Characterization of a wheat transcription factor, TaWRKY45, and its effect on Fusarium head blight resistance in transgenic wheat plants. Breeding Science, 2011, 61: 121-129.

[111]Gao C S, Kou X J, Li H P, Zhang J B, Saad A, Liao Y C. Inverse effects of Arabidopsis NPR1 gene on fusarium seedling blight and Fusarium head blight in transgenic wheat. Plant Pathology, 2013, 62: 383-392.

[112]Walter S, Brennan J M, Arunachalam C, Ansari K I, Hu X, Khan M R, Trognitz F, Trognitz B, Leonard G, Egan D, Doohan F M. Components of the gene network associated with genotype-dependent response of wheat to the Fusarium mycotoxins deoxynivalenol. Functional & Integrative Genomics, 2008, 8: 421-427.

[113]Ma L L, Shang Y, Cao A Z, Q Z J, Xing L P, Chen P D, Liu D J, Wang X E. Molecular cloning and charachterization of an up- regulated UDP-glucosyltransferase gene induced by DON from Triticum aestivum L. cv. Wangshuibai. Molecular Biology Reports, 2010, 37: 785-795.

[114]Zhou W, Kolb F L, Riechers D E. Identification of proteins induced or upregulated by Fusarium head blight infection in the spikes of hexaploid wheat (Triticum aestivum). Genome, 2005, 48: 770-780.

[115]Shang Y, Xiao J, Ma L L, Wang H Y, Qi Z J, Chen P D. Characterization of a PDR type transporter gene from wheat (Triticum aestivum L.). Chinese Science Bulletin, 2009, 54: 3249-3257.

[116]Theodoulou F L, Clark I M, He X L, Pallett K E, Cole D J, Hallahan D L. Co-induction of gluthatione-S-transferase and multidrug resistance associated protein by xenobiotics in wheat. Pest Management Science, 2003, 59: 202-214.

[117]Rea P A. Plant ATP-binding cassette transporters. Annual Review of Plant Biology, 2007, 58: 347-375.

[118]Gluck A, Endo Y, Wool I G. Ribosomal RNA identity elements for ricin A-chain recognition and catalysis:analysis with tetraloop mutants. Journal of Molecular Biology,1992, 226: 411-424.

[119]Balconi C, Lanzanova C, Conti E, Triulzi T, Forlani F, Cattaneo M, Lupotto E. Fusarium head blight evaluation in wheat transgenic plants expressing the maize b-32 antifungal gene. European Journal of Plant Pathology, 2007, 117: 129-140.

[120] Mohammadi M, Kazemi H. Changes in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusarium graminearum and induced resistance. Plant Science, 2002, 162: 491-498.

[121]Geddes J, Eudes F, Laroche A, Selinger L B. Differential expression of proteins in response to the interaction between the pathogen Fusarium graminearum and its host, Hordeum vulgare. Proteomics, 2008, 8: 545-554.

[122]Boddu J, Cho S, Muehlbauer G J. Transcriptome analysis of trichothecene-induced gene expression in barley. Molecular Plant-Microbe Interactions, 2007, 20: 1364-1375.

[123]Steiner B, Kurz H, Lemmens M, Buerstmayr H. Differential gene expression of related wheat lines with contrasting levels of head blight resistance after Fusarium graminearum inoculation. Theoretical and Applied Genetics, 2009, 118: 753-764.

[124]Ma X, Du X, Liu G, Yang Z, Hou W, Wang H, Feng D, Li A, Kong L. Cloning and characterization of a novel UDP-glycosyltransferase gene induced by DON from wheat. Journal of Integrative Agriculture, 2015, 14: 830-838.