Systemic acquired resistance, NPR1, and pathogenesis-related genes in wheat and barley
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摘要
In Arabidopsis, systemic acquired resistance(SAR) is established beyond the initial infection by a pathogen or is directly induced by treatment with salicylic acid(SA) or its functional analogs, 2,6-dichloroisonicotinic acid(INA) and benzothiadiazole(BTH). NPR1 protein is considered the master regulator of SAR in both SA signal sensing and transduction. In wheat(Triticum aestivum) and barley(Hordeum vulgare), both pathogen infection and BTH treatment can induce broad-spectrum resistance to various diseases, including powdery mildew, leaf rust, Fusarium head blight, etc. However, three different types of SAR-like responses including acquired resistance(AR), systemic immunity(SI), and BTH-induced resistance(BIR) seem to be achieved by activating different gene pathways. Recent research on wheat and barley NPR1 homologs in AR and SI has provided the initial clue for understanding the mechanism of SAR in these two plant species. In this review, the specific features of AR, SI, and BIR in wheat and barley were summarized and compared with that of SAR in model plants of Arabidopsis and rice. Research updates on downstream genes of SAR, including pathogenesis-related(PR) and BTH-induced genes, were highlighted.
In Arabidopsis, systemic acquired resistance(SAR) is established beyond the initial infection by a pathogen or is directly induced by treatment with salicylic acid(SA) or its functional analogs, 2,6-dichloroisonicotinic acid(INA) and benzothiadiazole(BTH). NPR1 protein is considered the master regulator of SAR in both SA signal sensing and transduction. In wheat(Triticum aestivum) and barley(Hordeum vulgare), both pathogen infection and BTH treatment can induce broad-spectrum resistance to various diseases, including powdery mildew, leaf rust, Fusarium head blight, etc. However, three different types of SAR-like responses including acquired resistance(AR), systemic immunity(SI), and BTH-induced resistance(BIR) seem to be achieved by activating different gene pathways. Recent research on wheat and barley NPR1 homologs in AR and SI has provided the initial clue for understanding the mechanism of SAR in these two plant species. In this review, the specific features of AR, SI, and BIR in wheat and barley were summarized and compared with that of SAR in model plants of Arabidopsis and rice. Research updates on downstream genes of SAR, including pathogenesis-related(PR) and BTH-induced genes, were highlighted.
In Arabidopsis, systemic acquired resistance(SAR) is established beyond the initial infection by a pathogen or is directly induced by treatment with salicylic acid(SA) or its functional analogs, 2,6-dichloroisonicotinic acid(INA) and benzothiadiazole(BTH). NPR1 protein is considered the master regulator of SAR in both SA signal sensing and transduction. In wheat(Triticum aestivum) and barley(Hordeum vulgare), both pathogen infection and BTH treatment can induce broad-spectrum resistance to various diseases, including powdery mildew, leaf rust, Fusarium head blight, etc. However, three different types of SAR-like responses including acquired resistance(AR), systemic immunity(SI), and BTH-induced resistance(BIR) seem to be achieved by activating different gene pathways. Recent research on wheat and barley NPR1 homologs in AR and SI has provided the initial clue for understanding the mechanism of SAR in these two plant species. In this review, the specific features of AR, SI, and BIR in wheat and barley were summarized and compared with that of SAR in model plants of Arabidopsis and rice. Research updates on downstream genes of SAR, including pathogenesis-related(PR) and BTH-induced genes, were highlighted.
引文
Ahmed S M,Liu P,Xue Q,Ji C,Qi T,Guo J,Guo J,Kang Z.2017.TaDIR1-2,a wheat ortholog of lipid transfer protein AtDIR1 contributes to negative regulation of wheat resistance against Puccinia striiformis f.sp.tritici.Frontiers in Plant Science,8,521.
Anand A,Zhou T,Trick H N,Gill B S,Bockus W W,Muthukrishnan S.2003.Greenhouse and field testing of transgenic wheat plants stably expressing genes for thaumatin-like protein,chitinase and glucanase against Fusarium graminearum.Journal of Experimental Botany,54,1101.
Bai W,Chern M,Ruan D,Canlas P E,Sze-To W H,Ronald PC.2011.Enhanced disease resistance and hypersensitivity to BTH by introduction of an NH1/OsNPR1 paralog.Plant Biotechnology Journal,9,205-215.
Be?er K,Jarosch B,Langen G,Kogel K-H.2000.Expression analysis of genes induced in barley after chemical activation reveals distinct disease resistance pathways.Molecular Plant Pathology,1,277-286.
Bertini L,Leonardi L,Caporale C,Tucci M,Cascone N,Berardino I D,Buonocore V,Caruso C.2003.Pathogenresponsive wheat PR4 genes are induced by activators of systemic acquired resistance and wounding.Plant Science,164,1067-1078.
Cantu D,Yang B,Ruan R,Li K,Menzo V,Fu D,Chern M,Ronald P C,Dubcovsky J.2013.Comparative analysis of protein-protein interactions in the defense response of rice and wheat.BMC Genomics,14,166.
Cao H,Bowling S A,Gordon A S,Dong X.1994.Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance.The Plant Cell,6,1583.
Caruso C,Bertini L,Tucci M,Caporale C,Leonardi L,Saccardo F,Bressan R A,Veronese P,Buonocore V.1999.Isolation and characterisation of wheat cDNA clones encoding PR4proteins.DNA Sequence the Journal of DNA Sequencing&Mapping,10,301.
Caruso C,Bertini L,Tucci M,Caporale C,Nobile M,Leonardi L,Buonocore V.2001.Recombinant wheat antifungal PR4proteins expressed in Escherichia coli.Protein Expression and Purification,23,380-388.
Chen H,Chen J,Li M,Chang M,Xu K,Shang Z,Zhao Y,Palmer I,Zhang Y,McGill J,Alfano J R,Nishimura M T,Liu F,Fu Z Q.2017.A bacterial Type III effector targets the master regulator of salicylic acid signaling,NPR1,to subvert plant immunity.Cell Host&Microbe,22,777-788.
Chen Z,Iyer S,Caplan A,Klessig D F,Fan B.1997.Differential accumulation of salicylic acid and salicylic acid-sensitive catalase in different rice tissues.Plant Physiology,114,193.
Chern M,Fitzgerald H A,Canlas P E,Navarre D A,Ronald P C.2005.Overexpression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light.Molecular Plant-Microbe Interactions,18,511-520.
Chern M S,Fitzgerald H A,Yadav R C,Canlas P E,Dong X,Ronald P C.2001.Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis.Plant Journal for Cell and Molecular Biology,27,101-113.
Christensen A B,Cho B H,N?sby M,Gregersen P L,Brandt J,Madriz-Orde?ana K,Collinge D B,Thordal-Christensen H.2002.The molecular characterization of two barley proteins establishes the novel PR-17 family of pathogenesis-related proteins.Molecular Plant Pathology,3,135-144.
Colebrook E H,Creissen G,Mcgrann G R,Dreos R,Lamb C,Boyd L A.2012.Broad-spectrum acquired resistance in barley induced by the Pseudomonas pathosystem shares transcriptional components with Arabidopsis systemic acquired resistance.Molecular Plant-Microbe Interactions,25,658-667.
Custers J H H V,Harrison S J,Sela-Buurlage M B,Deventer E V,Lageweg W,Howe P W,Meijs P J V D,Ponstein A S,Simons B H,Melchers L S.2004.Isolation and characterisation of a class of carbohydrate oxidases from higher plants,with a role in active defence.The Plant Journal,39,147.
Delaney T P,Friedrich L,Ryals J A.1995.Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance.Proceedings of the National Academy of Sciences of the United States of America,92,6602.
Després C,Chubak C,Rochon A,Clark R,Bethune T,Desveaux D,Fobert P R.2003.The Arabidopsis NPR1disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1.The Plant Cell,15,2181-2191.
Dey S,Wenig M,Langen G,Sharma S,Kugler K G,Knappe C,Hause B,Bichlmeier M,Babaeizad V,Imani J.2014.Bacteria-triggered systemic immunity in barley is associated with WRKY and ETHYLENE RESPONSIVE FACTORs but not with salicylic acid.Plant Physiology,166,2133-2151.
Elhamid M I A,Makboul H E,Sedik M Z,Ismail I M,Ibrahim MA.2010.Cloning,expression and antifungal activity of an endochitinase gene derived from barley(Hordeum vulgare).Research Journal of Agriculture and Biological Sciences,6,356-363.
Epple P,Apel K,Bohlmann H.1995.An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins.Plant Physiology,109,813.
Ferreira R B,Monteiro S,Freitas R,Santos C N,Chen Z,Batista L M,Duarte J,Borges A,Teixeira A R.2007.The role of plant defence proteins in fungal pathogenesis.Molecular Plant Pathology,8,677.
Fu Z Q,Dong X.2013.Systemic acquired resistance:Turning local infection into global defense.Annual Review of Plant Biology,64,839-863.
Fu Z Q,Yan S,Saleh A,Wang W,Ruble J,Oka N,Mohan R,Spoel S H,Tada Y,Zheng N,Dong X.2012.NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants.Nature,486,228.
Gaddour K,Vicentecarbajosa J,Lara P,Isabellamoneda I,Díaz I,Carbonero P.2001.A constitutive cystatin-encoding gene from barley(Icy)responds differentially to abiotic stimuli.Plant Molecular Biology,45,599-608.
Gamir J,Darwiche R,Van’T Hof P,Choudhary V,Stumpe M,Schneiter R,Mauch F.2017.The sterol-binding activity of PATHOGENESIS-RELATED PROTEIN 1 reveals the mode of action of an antimicrobial protein.The Plant Journal,89,502-509.
Gao C,Kou X,Li H,Zhang J,Saad A,Liao Y.2013.Inverse effects of Arabidopsis NPR1 gene on fusarium seedling blight and fusarium head blight in transgenic wheat.Plant Pathology,62,383-392.
Gao L,Wang S,Li X Y,Wei X J,Zhang Y J,Wang H Y,Liu D Q.2015.Expression and functional analysis of a pathogenesisrelated protein 1 gene,TcLr19PR1,involved in wheat resistance against leaf rust fungus.Plant Molecular Biology Reporter,33,797-805.
Garcíaolmedo F,Molina A,Segura A,Moreno M.1995.The defensive role of nonspecific lipid-transfer proteins in plants.Trends in Microbiology,3,72.
Girhepuje P V,Shinde G B.2010.Transgenic tomato plants expressing a wheat endochitinase gene demonstrate enhanced resistance to Fusarium oxysporum f.sp.lycopersici.Plant Cell Tissue and Organ Culture,105,243-251.
Gregersen P L,Thordalchristensen H,Forster H,Collinge D B.1997.Differential gene transcript accumulation in barley leaf epidermis and mesophyll in response to attack by Blumeria graminis f.sp.hordei(syn.Erysiphe graminis f.sp.hordei).Physiological and Molecular Plant Pathology,51,85-97.
G?rlach J,Volrath S,Knaufbeiter G,Hengy G,Beckhove U,Kogel K H,Oostendorp M,Staub T,Ward E,Kessmann H.1996.Benzothiadiazole,a novel class of inducers of systemic acquired resistance,activates gene expression and disease resistance in wheat.The Plant Cell,8,629-643.
Hafez Y M,Soliman N K,Saber M M,Imbabi I A,Abdelaziz A S.2014.Induced resistance against Puccinia triticina,the causal agent of wheat leaf rust by chemical inducers.Egyptian Journal of Pest Control,24,173-181.
JordáL,Conejero V,Vera P.2000.Characterization of P69Eand P69F,two differentially regulated genes encoding new members of the subtilisin-like proteinase family from tomato plants.Plant Physiology,122,67-73.
Kang Z,Buchenauer H.2002.Immunocytochemical localization ofβ-1,3-glucanase and chitinase in Fusarium culmoruminfected wheat spikes.Physiological and Molecular Plant Pathology,60,141-153.
Kirubakaran S I,Begum S M,Ulaganathan K,Sakthivel N.2008.Characterization of a new antifungal lipid transfer protein from wheat.Plant Physiology and Biochemistry,46,918.
Li W L,Faris J D,Muthukrishnan S,Liu D J,Chen P D,Gill B S.2001.Isolation and characterization of novel cDNA clones of acidic chitinases and beta-1,3-glucanases from wheat spikes infected by Fusarium graminearum.Theoretical and Applied Genetics,102,353-362.
Li X Y,Gao L,Zhang W H,Liu J K,Zhang Y J,Wang H Y,Liu D Q.2015.Characteristic expression of wheat PR5 gene in response to infection by the leaf rust pathogen,Puccinia triticina.Journal of Plant Interactions,10,132-141.
Liu B,Xue X,Cui S,Zhang X,Han Q,Zhu L,Liang X,Wang X,Huang L,Chen X.2010.Cloning and characterization of a wheat beta-1,3-glucanase gene induced by the stripe rust pathogen Puccinia striiformis f.sp.tritici.Molecular Biology Reports,37,1045.
Loon L C V,Rep M,Pieterse C M J.2006.Significance of inducible defense-related proteins in infected plants.Annual Review of Phytopathology,44,135.
Lu S,Faris J D,Sherwood R,Friesen T L,Edwards M C.2014.A dimeric PR-1-type pathogenesis-related protein interacts with ToxA and potentially mediates ToxA-induced necrosis in sensitive wheat.Molecular Plant Pathology,15,650.
Lu Y,Zhang Z Y,Ren L J,Liu B Y,Liao Y,Xu H J,Du L P,Ma H X,Ren Z L,Jing J X.2009.Molecular analyses on Rs-AFP2 transgenic wheat plants and their resistance to Rhizoctonia cerealis.Acta Agronomica Sinica,35,640-646.
Makandar R,Essig J S,Schapaugh M A,Trick H N,Shah J.2006.Genetically engineered resistance to Fusarium head blight in wheat by expression of Arabidopsis NPR1.Molecular Plant-Microbe Interactions,19,123-129.
Molina A,García-Olmedo F.1993.Developmental and pathogen-induced expression of three barley genes encoding lipid transfer proteins.The Plant Journal,4,983.
Molina A,García-Olmedo F.1997.Enhanced tolerance to bacterial pathogens caused by the transgenic expression of barley lipid transfer protein LTP2.The Plant Journal,12,669-675.
Molina A,G?rlach J,Volrath S,Ryals J.1999.Wheat genes encoding two types of PR-1 proteins are pathogen inducible,but do not respond to activators of systemic acquired resistance.Molecular Plant-Microbe Interactions,12,53-58.
Moreau M,Tian M,Klessig D F.2012.Salicylic acid binds NPR3and NPR4 to regulate NPR1-dependent defense responses.Cell Research,22,1631.
Mou Z,Fan W,Dong X.2003.Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes.Cell,113,935.
Nakayama A,Fukushima S,Goto S,Matsushita A,Shimono M,Sugano S,Jiang C J,Akagi A,Yamazaki M,Inoue H.2013.Genome-wide identification of WRKY45-regulated genes that mediate benzothiadiazole-induced defense responses in rice.BMC Plant Biology,13,150.
Oostendorp M,Kunz W,Dietrich B,Staub T.2001.Induced disease resistance in plants by chemicals.European Journal of Plant Pathology,107,19-28.
Quilis J,Pe?as G,Messeguer J,Brugidou C,Segundo B S.2008.The Arabidopsis AtNPR1 inversely modulates defense responses against fungal,bacterial,or viral pathogens while conferring hypersensitivity to abiotic stresses in transgenic rice.Molecular Plant-Microbe Interactions,21,1215-1231.
Reiss E,Horstmann C.2001.Drechslera teres-infected barley(Hordeum vulgare L.)leaves accumulate eight isoforms of thaumatin-like proteins.Physiological and Molecular Plant Pathology,58,183-188.
Ryals J,Weymann K,Lawton K,Friedrich L,Ellis D,Steiner H Y,Johnson J,Delaney T P,Jesse T,Vos P.1997.The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B.The Plant Cell,9,425.
Schweizer P,Schlagenhauf E,Schaffrath U,Dudler R.1999.Different patterns of host genes are induced in rice by Pseudomonas syringae,a biological inducer of resistance,and the chemical inducer benzothiadiazole(BTH).European Journal of Plant Pathology,105,659-665.
Sels J,Mathys J,Coninck B M A D,Cammue B P A,Bolle MF C D.2008.Plant pathogenesis-related(PR)proteins:Afocus on PR peptides.Plant Physiology and Biochemistry,46,941-950.
Shah J,Tsui F,Klessig D F.1997.Characterization of a salicylic acid-insensitive mutant(sai1)of Arabidopsis thaliana,identified in a selective screen utilizing the SA-inducible expression of the tms2 gene.Molecular Plant-Microbe Interactions,10,69.
Shimono M,Sugano S,Nakayama A,Jiang C J,Ono K,Toki S,Takatsuji H.2007.Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance.The Plant Cell,19,2064-2076.
Shin S,Mackintosh C A,Lewis J,Heinen S J,Radmer L,Dillmacky R,Baldridge G D,Zeyen R J,Muehlbauer GJ.2008.Transgenic wheat expressing a barley class IIchitinase gene has enhanced resistance against Fusarium graminearum.Journal of Experimental Botany,59,2371-2378.
Silverman P,Seskar M,Schweizer P,Métraux J P,Raskin I.1995.Salicylic acid in rice:Niosynthesis,conjugation,and possible role.Plant Physiology,108,633.
Smith J A,Métraux J P.1991.Pseudomonas syringae pv.syringae induces systemic resistance to Pyricularia oryzae in rice.Physiological and Molecular Plant Pathology,39,451-461.
Sock J,Rohringer,Kang Z.1990.Extracellularβ-1,3-glucanases in stem rust-affected and abiotically stressed wheat leaves:Immunocytochemical localization of the enzyme and detection of multiple forms in gels by activity staining with dye-labeled laminarin.Plant Physiology,94,1376-1389.
Steinerlange S,Fischer A,Boettcher A,Rouhara I,Liedgens H,Schmelzer E,Knogge W.2003.Differential defense reactions in leaf tissues of barley in response to infection by Rhynchosporium secalis and to treatment with a fungal avirulence gene product.Molecular Plant-Microbe Interactions,16,893.
Sun H,Du S C,Kim N H,Kim D S,Hwang B K.2014.Pathogenesis-related protein 4b interacts with leucine-rich repeat protein1 to suppress PR4b-triggered cell death and defense response in pepper.Plant Journal for Cell and Molecular Biology,77,521-533.
Terras F R,Eggermont K,Kovaleva V,Raikhel N V,Osborn RW,Kester A,Rees S B,Torrekens S,Van L F,Vanderleyden J.1995.Small cysteine-rich antifungal proteins from radish:Their role in host defense.The Plant Cell,7,573.
Thordal-Christensen H,Brandt J,Cho B H,Rasmussen S K,Gregersen P L,Smedegaard-Petersen V,Collinge D B.1992.cDNA cloning and characterization of two barley peroxidase transcripts induced differentially by the powdery mildew fungus Erysiphe graminis.Physiological and Molecular Plant Pathology,40,395-409.
Vallélianbindschedler L,Métraux J P,Schweizer P.1998.Salicylic acid accumulation in barley is pathogen specific but not required for defense-gene activation.Molecular Plant-Microbe Interactions,11,702-705.
Wang B,Sun Y,Song N,Zhao M,Liu R,Feng H,Wang X,Kang Z.2017.Puccinia striiformis f.sp.tritici microRNA-like RNA 1(Pst-milR1),an important pathogenicity factor of Pst,impairs wheat resistance to Pst by suppressing the wheat pathogenesis-related 2 gene.New Phytologist,215,338-350.
Wang X,Tang C,Deng L,Cai G,Liu X,Liu B,Han Q,Buchenauer H,Wei G,Han D.2010.Characterization of a pathogenesis-related thaumatin-like protein gene TaPR5from wheat induced by stripe rust fungus.Physiologia Plantarum,139,27-38.
Wang X,Yang B,Li K,Kang Z,Cantu D,Dubcovsky J.2016.Aconserved Puccinia striiformis protein interacts with wheat NPR1 and reduces induction of pathogenesis-related genes in response to pathogens.Molecular Plant-Microbe Interactions,29,977.
Xu G,Yuan M,Ai C,Liu L,Zhuang E,Karapetyan S,Wang S,Dong X.2017.uORF-mediated translation allows engineered plant disease resistance without fitness costs.Nature,545,491-494.
Yu C L,Kreuzaler F,Fischer R,Reisener H J,Tiburzy R.1994.Characterization of a wheat class Ib chitinase gene differentially induced in isogenic lines by infection with Puccinia graminis.Plant Science,103,177-187.
Yu G,Zhang X,Yao J,Zhou M P,Ma H.2017.Resistance against fusarium head blight in transgenic wheat plants expressing the ScNPR1 gene.Journal of Phytopathology,165,223-231.
Zhang W J,Pedersen C,Kwaaitaal M,Gregersen P L,M?rch S M,Hanisch S,Kristensen A,Fuglsang A T,Collinge D B,Thordal-Christensen H.2012.Interaction of barley powdery mildew effector candidate CSEP0055 with the defence protein PR17c.Molecular Plant Pathology,13,1110-1119.
Zheng Q F,Dong X.2013.Systemic acquired resistance:Turning local infection into global defense.Annual Review of Plant Biology,64,839.
Zhou F,Collinge D B,Thordal-Christensen H.1998.Molecular characterization of the oxalate oxidase involved in the response of barley to the powdery mildew fungus.Plant Physiology,117,33.
Zhu X,Li Z,Xu H,Zhou M,Du L,Zhang Z.2012.Overexpression of wheat lipid transfer protein gene TaLTP5 increases resistances to Cochliobolus sativus and Fusarium graminearum in transgenic wheat.Functional and Integrative Genomics,12,481.
Anand A,Zhou T,Trick H N,Gill B S,Bockus W W,Muthukrishnan S.2003.Greenhouse and field testing of transgenic wheat plants stably expressing genes for thaumatin-like protein,chitinase and glucanase against Fusarium graminearum.Journal of Experimental Botany,54,1101.
Bai W,Chern M,Ruan D,Canlas P E,Sze-To W H,Ronald PC.2011.Enhanced disease resistance and hypersensitivity to BTH by introduction of an NH1/OsNPR1 paralog.Plant Biotechnology Journal,9,205-215.
Be?er K,Jarosch B,Langen G,Kogel K-H.2000.Expression analysis of genes induced in barley after chemical activation reveals distinct disease resistance pathways.Molecular Plant Pathology,1,277-286.
Bertini L,Leonardi L,Caporale C,Tucci M,Cascone N,Berardino I D,Buonocore V,Caruso C.2003.Pathogenresponsive wheat PR4 genes are induced by activators of systemic acquired resistance and wounding.Plant Science,164,1067-1078.
Cantu D,Yang B,Ruan R,Li K,Menzo V,Fu D,Chern M,Ronald P C,Dubcovsky J.2013.Comparative analysis of protein-protein interactions in the defense response of rice and wheat.BMC Genomics,14,166.
Cao H,Bowling S A,Gordon A S,Dong X.1994.Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance.The Plant Cell,6,1583.
Caruso C,Bertini L,Tucci M,Caporale C,Leonardi L,Saccardo F,Bressan R A,Veronese P,Buonocore V.1999.Isolation and characterisation of wheat cDNA clones encoding PR4proteins.DNA Sequence the Journal of DNA Sequencing&Mapping,10,301.
Caruso C,Bertini L,Tucci M,Caporale C,Nobile M,Leonardi L,Buonocore V.2001.Recombinant wheat antifungal PR4proteins expressed in Escherichia coli.Protein Expression and Purification,23,380-388.
Chen H,Chen J,Li M,Chang M,Xu K,Shang Z,Zhao Y,Palmer I,Zhang Y,McGill J,Alfano J R,Nishimura M T,Liu F,Fu Z Q.2017.A bacterial Type III effector targets the master regulator of salicylic acid signaling,NPR1,to subvert plant immunity.Cell Host&Microbe,22,777-788.
Chen Z,Iyer S,Caplan A,Klessig D F,Fan B.1997.Differential accumulation of salicylic acid and salicylic acid-sensitive catalase in different rice tissues.Plant Physiology,114,193.
Chern M,Fitzgerald H A,Canlas P E,Navarre D A,Ronald P C.2005.Overexpression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light.Molecular Plant-Microbe Interactions,18,511-520.
Chern M S,Fitzgerald H A,Yadav R C,Canlas P E,Dong X,Ronald P C.2001.Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis.Plant Journal for Cell and Molecular Biology,27,101-113.
Christensen A B,Cho B H,N?sby M,Gregersen P L,Brandt J,Madriz-Orde?ana K,Collinge D B,Thordal-Christensen H.2002.The molecular characterization of two barley proteins establishes the novel PR-17 family of pathogenesis-related proteins.Molecular Plant Pathology,3,135-144.
Colebrook E H,Creissen G,Mcgrann G R,Dreos R,Lamb C,Boyd L A.2012.Broad-spectrum acquired resistance in barley induced by the Pseudomonas pathosystem shares transcriptional components with Arabidopsis systemic acquired resistance.Molecular Plant-Microbe Interactions,25,658-667.
Custers J H H V,Harrison S J,Sela-Buurlage M B,Deventer E V,Lageweg W,Howe P W,Meijs P J V D,Ponstein A S,Simons B H,Melchers L S.2004.Isolation and characterisation of a class of carbohydrate oxidases from higher plants,with a role in active defence.The Plant Journal,39,147.
Delaney T P,Friedrich L,Ryals J A.1995.Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance.Proceedings of the National Academy of Sciences of the United States of America,92,6602.
Després C,Chubak C,Rochon A,Clark R,Bethune T,Desveaux D,Fobert P R.2003.The Arabidopsis NPR1disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1.The Plant Cell,15,2181-2191.
Dey S,Wenig M,Langen G,Sharma S,Kugler K G,Knappe C,Hause B,Bichlmeier M,Babaeizad V,Imani J.2014.Bacteria-triggered systemic immunity in barley is associated with WRKY and ETHYLENE RESPONSIVE FACTORs but not with salicylic acid.Plant Physiology,166,2133-2151.
Elhamid M I A,Makboul H E,Sedik M Z,Ismail I M,Ibrahim MA.2010.Cloning,expression and antifungal activity of an endochitinase gene derived from barley(Hordeum vulgare).Research Journal of Agriculture and Biological Sciences,6,356-363.
Epple P,Apel K,Bohlmann H.1995.An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins.Plant Physiology,109,813.
Ferreira R B,Monteiro S,Freitas R,Santos C N,Chen Z,Batista L M,Duarte J,Borges A,Teixeira A R.2007.The role of plant defence proteins in fungal pathogenesis.Molecular Plant Pathology,8,677.
Fu Z Q,Dong X.2013.Systemic acquired resistance:Turning local infection into global defense.Annual Review of Plant Biology,64,839-863.
Fu Z Q,Yan S,Saleh A,Wang W,Ruble J,Oka N,Mohan R,Spoel S H,Tada Y,Zheng N,Dong X.2012.NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants.Nature,486,228.
Gaddour K,Vicentecarbajosa J,Lara P,Isabellamoneda I,Díaz I,Carbonero P.2001.A constitutive cystatin-encoding gene from barley(Icy)responds differentially to abiotic stimuli.Plant Molecular Biology,45,599-608.
Gamir J,Darwiche R,Van’T Hof P,Choudhary V,Stumpe M,Schneiter R,Mauch F.2017.The sterol-binding activity of PATHOGENESIS-RELATED PROTEIN 1 reveals the mode of action of an antimicrobial protein.The Plant Journal,89,502-509.
Gao C,Kou X,Li H,Zhang J,Saad A,Liao Y.2013.Inverse effects of Arabidopsis NPR1 gene on fusarium seedling blight and fusarium head blight in transgenic wheat.Plant Pathology,62,383-392.
Gao L,Wang S,Li X Y,Wei X J,Zhang Y J,Wang H Y,Liu D Q.2015.Expression and functional analysis of a pathogenesisrelated protein 1 gene,TcLr19PR1,involved in wheat resistance against leaf rust fungus.Plant Molecular Biology Reporter,33,797-805.
Garcíaolmedo F,Molina A,Segura A,Moreno M.1995.The defensive role of nonspecific lipid-transfer proteins in plants.Trends in Microbiology,3,72.
Girhepuje P V,Shinde G B.2010.Transgenic tomato plants expressing a wheat endochitinase gene demonstrate enhanced resistance to Fusarium oxysporum f.sp.lycopersici.Plant Cell Tissue and Organ Culture,105,243-251.
Gregersen P L,Thordalchristensen H,Forster H,Collinge D B.1997.Differential gene transcript accumulation in barley leaf epidermis and mesophyll in response to attack by Blumeria graminis f.sp.hordei(syn.Erysiphe graminis f.sp.hordei).Physiological and Molecular Plant Pathology,51,85-97.
G?rlach J,Volrath S,Knaufbeiter G,Hengy G,Beckhove U,Kogel K H,Oostendorp M,Staub T,Ward E,Kessmann H.1996.Benzothiadiazole,a novel class of inducers of systemic acquired resistance,activates gene expression and disease resistance in wheat.The Plant Cell,8,629-643.
Hafez Y M,Soliman N K,Saber M M,Imbabi I A,Abdelaziz A S.2014.Induced resistance against Puccinia triticina,the causal agent of wheat leaf rust by chemical inducers.Egyptian Journal of Pest Control,24,173-181.
JordáL,Conejero V,Vera P.2000.Characterization of P69Eand P69F,two differentially regulated genes encoding new members of the subtilisin-like proteinase family from tomato plants.Plant Physiology,122,67-73.
Kang Z,Buchenauer H.2002.Immunocytochemical localization ofβ-1,3-glucanase and chitinase in Fusarium culmoruminfected wheat spikes.Physiological and Molecular Plant Pathology,60,141-153.
Kirubakaran S I,Begum S M,Ulaganathan K,Sakthivel N.2008.Characterization of a new antifungal lipid transfer protein from wheat.Plant Physiology and Biochemistry,46,918.
Li W L,Faris J D,Muthukrishnan S,Liu D J,Chen P D,Gill B S.2001.Isolation and characterization of novel cDNA clones of acidic chitinases and beta-1,3-glucanases from wheat spikes infected by Fusarium graminearum.Theoretical and Applied Genetics,102,353-362.
Li X Y,Gao L,Zhang W H,Liu J K,Zhang Y J,Wang H Y,Liu D Q.2015.Characteristic expression of wheat PR5 gene in response to infection by the leaf rust pathogen,Puccinia triticina.Journal of Plant Interactions,10,132-141.
Liu B,Xue X,Cui S,Zhang X,Han Q,Zhu L,Liang X,Wang X,Huang L,Chen X.2010.Cloning and characterization of a wheat beta-1,3-glucanase gene induced by the stripe rust pathogen Puccinia striiformis f.sp.tritici.Molecular Biology Reports,37,1045.
Loon L C V,Rep M,Pieterse C M J.2006.Significance of inducible defense-related proteins in infected plants.Annual Review of Phytopathology,44,135.
Lu S,Faris J D,Sherwood R,Friesen T L,Edwards M C.2014.A dimeric PR-1-type pathogenesis-related protein interacts with ToxA and potentially mediates ToxA-induced necrosis in sensitive wheat.Molecular Plant Pathology,15,650.
Lu Y,Zhang Z Y,Ren L J,Liu B Y,Liao Y,Xu H J,Du L P,Ma H X,Ren Z L,Jing J X.2009.Molecular analyses on Rs-AFP2 transgenic wheat plants and their resistance to Rhizoctonia cerealis.Acta Agronomica Sinica,35,640-646.
Makandar R,Essig J S,Schapaugh M A,Trick H N,Shah J.2006.Genetically engineered resistance to Fusarium head blight in wheat by expression of Arabidopsis NPR1.Molecular Plant-Microbe Interactions,19,123-129.
Molina A,García-Olmedo F.1993.Developmental and pathogen-induced expression of three barley genes encoding lipid transfer proteins.The Plant Journal,4,983.
Molina A,García-Olmedo F.1997.Enhanced tolerance to bacterial pathogens caused by the transgenic expression of barley lipid transfer protein LTP2.The Plant Journal,12,669-675.
Molina A,G?rlach J,Volrath S,Ryals J.1999.Wheat genes encoding two types of PR-1 proteins are pathogen inducible,but do not respond to activators of systemic acquired resistance.Molecular Plant-Microbe Interactions,12,53-58.
Moreau M,Tian M,Klessig D F.2012.Salicylic acid binds NPR3and NPR4 to regulate NPR1-dependent defense responses.Cell Research,22,1631.
Mou Z,Fan W,Dong X.2003.Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes.Cell,113,935.
Nakayama A,Fukushima S,Goto S,Matsushita A,Shimono M,Sugano S,Jiang C J,Akagi A,Yamazaki M,Inoue H.2013.Genome-wide identification of WRKY45-regulated genes that mediate benzothiadiazole-induced defense responses in rice.BMC Plant Biology,13,150.
Oostendorp M,Kunz W,Dietrich B,Staub T.2001.Induced disease resistance in plants by chemicals.European Journal of Plant Pathology,107,19-28.
Quilis J,Pe?as G,Messeguer J,Brugidou C,Segundo B S.2008.The Arabidopsis AtNPR1 inversely modulates defense responses against fungal,bacterial,or viral pathogens while conferring hypersensitivity to abiotic stresses in transgenic rice.Molecular Plant-Microbe Interactions,21,1215-1231.
Reiss E,Horstmann C.2001.Drechslera teres-infected barley(Hordeum vulgare L.)leaves accumulate eight isoforms of thaumatin-like proteins.Physiological and Molecular Plant Pathology,58,183-188.
Ryals J,Weymann K,Lawton K,Friedrich L,Ellis D,Steiner H Y,Johnson J,Delaney T P,Jesse T,Vos P.1997.The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B.The Plant Cell,9,425.
Schweizer P,Schlagenhauf E,Schaffrath U,Dudler R.1999.Different patterns of host genes are induced in rice by Pseudomonas syringae,a biological inducer of resistance,and the chemical inducer benzothiadiazole(BTH).European Journal of Plant Pathology,105,659-665.
Sels J,Mathys J,Coninck B M A D,Cammue B P A,Bolle MF C D.2008.Plant pathogenesis-related(PR)proteins:Afocus on PR peptides.Plant Physiology and Biochemistry,46,941-950.
Shah J,Tsui F,Klessig D F.1997.Characterization of a salicylic acid-insensitive mutant(sai1)of Arabidopsis thaliana,identified in a selective screen utilizing the SA-inducible expression of the tms2 gene.Molecular Plant-Microbe Interactions,10,69.
Shimono M,Sugano S,Nakayama A,Jiang C J,Ono K,Toki S,Takatsuji H.2007.Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance.The Plant Cell,19,2064-2076.
Shin S,Mackintosh C A,Lewis J,Heinen S J,Radmer L,Dillmacky R,Baldridge G D,Zeyen R J,Muehlbauer GJ.2008.Transgenic wheat expressing a barley class IIchitinase gene has enhanced resistance against Fusarium graminearum.Journal of Experimental Botany,59,2371-2378.
Silverman P,Seskar M,Schweizer P,Métraux J P,Raskin I.1995.Salicylic acid in rice:Niosynthesis,conjugation,and possible role.Plant Physiology,108,633.
Smith J A,Métraux J P.1991.Pseudomonas syringae pv.syringae induces systemic resistance to Pyricularia oryzae in rice.Physiological and Molecular Plant Pathology,39,451-461.
Sock J,Rohringer,Kang Z.1990.Extracellularβ-1,3-glucanases in stem rust-affected and abiotically stressed wheat leaves:Immunocytochemical localization of the enzyme and detection of multiple forms in gels by activity staining with dye-labeled laminarin.Plant Physiology,94,1376-1389.
Steinerlange S,Fischer A,Boettcher A,Rouhara I,Liedgens H,Schmelzer E,Knogge W.2003.Differential defense reactions in leaf tissues of barley in response to infection by Rhynchosporium secalis and to treatment with a fungal avirulence gene product.Molecular Plant-Microbe Interactions,16,893.
Sun H,Du S C,Kim N H,Kim D S,Hwang B K.2014.Pathogenesis-related protein 4b interacts with leucine-rich repeat protein1 to suppress PR4b-triggered cell death and defense response in pepper.Plant Journal for Cell and Molecular Biology,77,521-533.
Terras F R,Eggermont K,Kovaleva V,Raikhel N V,Osborn RW,Kester A,Rees S B,Torrekens S,Van L F,Vanderleyden J.1995.Small cysteine-rich antifungal proteins from radish:Their role in host defense.The Plant Cell,7,573.
Thordal-Christensen H,Brandt J,Cho B H,Rasmussen S K,Gregersen P L,Smedegaard-Petersen V,Collinge D B.1992.cDNA cloning and characterization of two barley peroxidase transcripts induced differentially by the powdery mildew fungus Erysiphe graminis.Physiological and Molecular Plant Pathology,40,395-409.
Vallélianbindschedler L,Métraux J P,Schweizer P.1998.Salicylic acid accumulation in barley is pathogen specific but not required for defense-gene activation.Molecular Plant-Microbe Interactions,11,702-705.
Wang B,Sun Y,Song N,Zhao M,Liu R,Feng H,Wang X,Kang Z.2017.Puccinia striiformis f.sp.tritici microRNA-like RNA 1(Pst-milR1),an important pathogenicity factor of Pst,impairs wheat resistance to Pst by suppressing the wheat pathogenesis-related 2 gene.New Phytologist,215,338-350.
Wang X,Tang C,Deng L,Cai G,Liu X,Liu B,Han Q,Buchenauer H,Wei G,Han D.2010.Characterization of a pathogenesis-related thaumatin-like protein gene TaPR5from wheat induced by stripe rust fungus.Physiologia Plantarum,139,27-38.
Wang X,Yang B,Li K,Kang Z,Cantu D,Dubcovsky J.2016.Aconserved Puccinia striiformis protein interacts with wheat NPR1 and reduces induction of pathogenesis-related genes in response to pathogens.Molecular Plant-Microbe Interactions,29,977.
Xu G,Yuan M,Ai C,Liu L,Zhuang E,Karapetyan S,Wang S,Dong X.2017.uORF-mediated translation allows engineered plant disease resistance without fitness costs.Nature,545,491-494.
Yu C L,Kreuzaler F,Fischer R,Reisener H J,Tiburzy R.1994.Characterization of a wheat class Ib chitinase gene differentially induced in isogenic lines by infection with Puccinia graminis.Plant Science,103,177-187.
Yu G,Zhang X,Yao J,Zhou M P,Ma H.2017.Resistance against fusarium head blight in transgenic wheat plants expressing the ScNPR1 gene.Journal of Phytopathology,165,223-231.
Zhang W J,Pedersen C,Kwaaitaal M,Gregersen P L,M?rch S M,Hanisch S,Kristensen A,Fuglsang A T,Collinge D B,Thordal-Christensen H.2012.Interaction of barley powdery mildew effector candidate CSEP0055 with the defence protein PR17c.Molecular Plant Pathology,13,1110-1119.
Zheng Q F,Dong X.2013.Systemic acquired resistance:Turning local infection into global defense.Annual Review of Plant Biology,64,839.
Zhou F,Collinge D B,Thordal-Christensen H.1998.Molecular characterization of the oxalate oxidase involved in the response of barley to the powdery mildew fungus.Plant Physiology,117,33.
Zhu X,Li Z,Xu H,Zhou M,Du L,Zhang Z.2012.Overexpression of wheat lipid transfer protein gene TaLTP5 increases resistances to Cochliobolus sativus and Fusarium graminearum in transgenic wheat.Functional and Integrative Genomics,12,481.