The Role of Radical Burst in Plant Defense Responses to Necrotrophic Fungi

doi:10.1016/S1671-2927(00)8659

Journal of Integrative Agriculture ›› 2012, Vol. 12 ›› Issue (8): 1305-1312.DOI: 10.1016/S1671-2927(00)8659

The Role of Radical Burst in Plant Defense Responses to Necrotrophic Fungi

Mahesh S Kulye, LIU Hua, QIU De-wen

Key Laboratory of Integrated Pest Management in Crops, Ministry of Agriculture/Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China

收稿日期:2011-10-08 出版日期:2012-08-01 发布日期:2012-09-09
通讯作者: Correspondence QIU De-wen, E-mail: qiudewen@caas.net.cn
作者简介:Mahesh S Kulye, E-mail: kulyemahesh@gmail.com
基金资助:
This work was supported by the National High Technology Research and Development Program of China (2011AA10A205).

The Role of Radical Burst in Plant Defense Responses to Necrotrophic Fungi

Mahesh S Kulye, LIU Hua, QIU De-wen

Key Laboratory of Integrated Pest Management in Crops, Ministry of Agriculture/Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China

Received:2011-10-08 Online:2012-08-01 Published:2012-09-09
Contact: Correspondence QIU De-wen, E-mail: qiudewen@caas.net.cn
About author:Mahesh S Kulye, E-mail: kulyemahesh@gmail.com
Supported by:
This work was supported by the National High Technology Research and Development Program of China (2011AA10A205).

摘要/Abstract

摘要： Necrotrophic fungi, being the largest class of fungal plant pathogens, pose a serious economic problem to crop production. Nitric oxide (NO) is an essential regulatory molecule in plant immunity in synergy with reactive oxygen species (ROS). Most experimental data available on the roles of NO and ROS during plant-pathogen interactions are from studies of infections by potential biotrophic pathogens, including bacteria and viruses. However, there are several arguments about the role of ROS in defense responses during plants and necrotrophic pathogens interaction and little is known about the role of NO as a counterpart of ROS in disease resistance to necrotrophic pathogens. This review focuses on the recent knowledge about the role of oxidative burst in plant defense response to necrotrophic fungi.

关键词: nitric oxide, mitogen-activated protein kinase, necrotrophic fungi, programmed cell death reactive oxygen species

Abstract: Necrotrophic fungi, being the largest class of fungal plant pathogens, pose a serious economic problem to crop production. Nitric oxide (NO) is an essential regulatory molecule in plant immunity in synergy with reactive oxygen species (ROS). Most experimental data available on the roles of NO and ROS during plant-pathogen interactions are from studies of infections by potential biotrophic pathogens, including bacteria and viruses. However, there are several arguments about the role of ROS in defense responses during plants and necrotrophic pathogens interaction and little is known about the role of NO as a counterpart of ROS in disease resistance to necrotrophic pathogens. This review focuses on the recent knowledge about the role of oxidative burst in plant defense response to necrotrophic fungi.

Key words: nitric oxide, mitogen-activated protein kinase, necrotrophic fungi, programmed cell death reactive oxygen species

Mahesh S Kulye, LIU Hua, QIU De-wen. The Role of Radical Burst in Plant Defense Responses to Necrotrophic Fungi[J]. Journal of Integrative Agriculture, 2012, 12(8): 1305-1312.

参考文献

[1]Adhikari T B, Bai J, Meinhardt S W, Gurung S, Myrfield M, Patel J, Ali S, Gudmestad N C, Rasmussen J B. 2009. Tsn1-mediated host responses to ToxA from Pyrenophora tritici-repentis. Molecular Plant-Microbe Interactions, 22, 1056-1068.

[2]Asai S, Mase K,Yoshioka H. 2010. Role of nitric oxide and reactive oxide species in disease resistance to necrotrophic pathogens. Plant Signaling and Behavior, 5, 872-874.

[3]Asai S, Ohta K, Yoshioka H. 2008. MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. The Plant Cell, 20, 1390-1406.

[4]Asai S, Yoshioka H. 2009. Nitric oxide as a partner of reactive oxygen species participates in disease resistance to necrotrophic pathogen Botrytis cinerea in Nicotiana benthamiana. Molecular Plant-Microbe Interactions, 22, 619-629.

[5]Asai S H, Yoshioka H. 2008. The role of radical burst via MAPK signaling in plant immunity. Plant Signaling and Behavior, 3, 920-922.

[6]Asselbergh B, Curvers K, Franca S C, Audenaert K, Vuylsteke M, van Breusegem F, Hofte M. 2007. Resistance to Botrytis cinerea in sitiens, an abscisic acid-deficient tomato mutant, involves timely production of hydrogen peroxide and cell wall modifications in the epidermis. Plant Physiology, 144, 1863-1877.

[7]van Baarlen P, Woltering E J, Staats M, van Kan J A L. 2007. Histochemical and genetic analysis of host and non-host interactions of Arabidopsis with three Botrytis species: An important role for cell death control. Molecular Plant Pathology, 8, 41-54.

[8]Besson-Bard A, Pugin A, Wendehenne D. 2008. New insights into nitric oxide signaling in plants. Annual Review of Plant Biology, 59, 21-39.

[9]Butt Y K C, Lum J H K, Lo S C L. 2003. Proteomic identification of plant proteins probed by mammalian nitric oxide synthase antibodies. Planta, 216, 762-771.

[10]Chassot C, Buchala A, Schoonbeek H, Métraux J P, Lamotte O. 2008. Wounding of Arabidopsis leaves causes a powerful but transient protection against Botrytis infection. The Plant Journal, 55, 555-567.

[11]Clarke A, Desikan R, Hurst R D, Hancock J T, Neill S J. 2000. NO way back: Nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. The Plant Journal, 24, 667-677.

[12]Collazo C, Chaco´n O, Borra´s O. 2006. Programmed cell death in plants resembles apoptosis of animals. Biotechnology and Applied Biochemistry, 23, 1-10.

[13]Crawford N M, Galli M, Tischner R, Heimer Y M, Okamoto M, Mack A. 2006. Response to Zemojtel et al: Plant nitric oxide synthase: back to square one. Trends in Plant Science, 11, 526-527.

[14]Curtis M J, Wolpert T J. 2004. The victorin-induced mitochondrial permeability transition precedes cell shrinkage and biochemical markers of cell death, and shrinkage occurs without loss of membrane integrity. The Plant Journal, 38, 244-259.

[15]Delledonne M. 2005. NO news is good news for plants. Current Opinion in Plant Biology, 8, 390-396.

[16]Delledonne M, Xia Y, Dixon R A, Lamb C. 1998. Nitric oxide functions as a signal in plant disease resistance. Nature, 394, 585-588.

[17]Delledonne M, Zeier J, Marocco A, Lamb C. 2001. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proceedings of the National Academy of Sciences of the United States of America, 98, 13454-13459.

[18]van Doorn W D, Woltering E. 2005. Many ways to exit? Cell deathcategories in plants. Trends in Plant Science, 10, 117-122.

[19]Elad Y. 1992. The use of antioxidants (free radical scavangers) to control grey mould (Botrytis cinerea) and white mould (Sclerotinia sclerotionumm) in various crops. Plant Pathology, 41, 417-426.

[20]Floryszak-Wieczorek J, Arasimowicz M, Milczarek G, Jelen H, Jackowiak H. 2007. Only an early nitric oxide burst and the following wave of secondary nitric oxide generation enhanced effective defence responses of pelargonium to a necrotrophic pathogen. New Phytologist, 175, 718-730.

[21]Garcia-Mata C, Lamattina L. 2003. Abscisic acid, nitric oxide and stomatal closure-Is nitrate reductase one of the missing links. Trends in Plant Science, 8, 20-26.

[22]Gechev T S, Gadjev I Z, Hille J. 2004. An extensive microarray analysis of ALL-toxin-induced cell death in Arabidopsis thaliana brings new insight into the complexity of programmed cell death in plants. Cellular and Molecular Life Sciences, 61, 1185-1197.

[23]Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology, 43, 205-227.

[24]Govrin E, Levine A. 2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Current Biology, 10, 751-757.

[25]Govrin E M, Rachmilevitch S, Tiwari B S, Solomon M, Levine A. 2006. An elicitor from Botrytis cinerea induces the hypersensitive response in Arabidopsis thaliana and other plants and promotes the gray mold disease. Phytopathology, 96, 299-307.

[26]Guo F Q, Okamoto M, Crawford N M. 2003. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science, 302, 100-103.

[27]Hammond-Kosack K E, Parker J E. 2003. Deciphering plantpathogen communication: fresh perspectives for molecular resistance breeding. Current Opinion in Biotechnology, 14, 177-193.

[28]He Y, Tang R H, Hao Y, Stevens R D, Cook C W, Ahn S M, Jing L, Yang Z, Chen L, Guo F, et al. 2004. Nitric oxide represses the Arabidopsis floral transition. Science, 305, 1968-1971.

[29]Jin H, Liu Y, Yang K Y, Kim C Y, Baker B, Zhang S. 2003. Function of a mitogen-activated protein kinase pathway in N gene mediated resistance in tobacco. The Plant Journal, 33, 719-731.

[30]Jones J D G, Dangl J L. 2006. The plant immune system. Nature, 444, 323-329.

[31]van Kan J A L. 2006. Licensed to kill: the lifestyle of necrotrophic plant pathogen. Trends in Plant Science, 11, 247-253.

[32]Kobayashi M, Kawakita K, Maeshima M, Doke N, Yoshioka H. 2006. Subcellular localization of strboh proteins and NADPH-dependent O2-generating activity in potato tuber tissues. Journal of Experimental Botany, 57, 1373-1379.

[33]Kunz C, Vandelle E, Rolland S, Poinssot B, Bruel C, Cimerman A, Zotti C, Moreau E, Vedel R, Pugin A, et al. 2006. Characterization of a new, nonpathogenic mutant of Botrytis cinerea with impaired plant colonization capacity. New Phytologist, 170, 537-550.

[34]Kuroyangi M, Yamada K, Hatsugai N, Kondo M, Nishimura M, Hara-Nishimura L. 2005. Vacuolar processing enzyme is essential for mycotoxin-induced cell death in Arabidopsis thaliana. Journal of Biological Chemistry, 280, 32914-32920.

[35]Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M. 2009. NO signals in the haze: nitric oxide signalling in plant defence. Current Opinion of Plant Biology, 12, 451-458.

[36]Manning V A, Chu A L, Steeves J E, Wolpert T J, Ciuffetti L M. 2009. A host-selective toxin of Pyrenophora triticirepentis, Ptr ToxA, induces photosystem changes and reactive oxygen species accumulation in sensitive wheat. Molecular Plant-Microbe Interactions, 22, 665-676.

[37]Moreau M, Lee G I, Wang Y, Crane B R, Klessig D F. 2008. AtNOS/A1 is a functional Arabidopsis thaliana cGTPase and not a nitric oxide synthase. Journal of Biological Chemistry, 283, 32957-32967.

[38]Nakagami H, Pitzschke A, Hirt H. 2005. Emerging MAP kinase pathways in plant stress signalling. Trends in Plant Science, 10, 339-346.

[39]Narusaka Y, Narusaka M, Seki M, Ishida J, Shinozaki K, Nan Y, Park P, Shiraishi T, Kobayashi M. 2005. Cytological and molecular analyses of non-host resistance of Arabidopsis thaliana to Alternaria alternata. Molecular Plant Pathology, 6, 615-627.

[40]Park P, Ikeda K-I. 2008. Ultrastructural analysis of responses of host and fungal cells during plant infection. Journal of General Plant Pathology, 74, 2-14.

[41]Pedley K F, Martin G B. 2005. Role of mitogen-activated protein kinases in plant immunity. Current Opinion in Plant Biology, 8, 541-547.

[42]Ren D, Liu Y, Yang K Y, Han L, Mao G, Glazebrook J, Zhang S. 2008. A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 105, 5638-5643.

[43]Repka V. 2006. Early defense responses induced by two distinct elicitors derived from a Botrytis cinerea in grapevine leaves and cell suspensions. Biologia Plantarum, 50, 94-106.

[44]Romeis T, Piedras P, Zhang S, Klessig D F, Hirt H, Jones J D G. 1999. Rapid Avr9-and Cf9-dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. The Plant Cell, 11, 273-287.

[45]Romero-Puertas M C, Campostrini N, Matte A, Righetti P G, Perazolli M, Zolla L, Roepstorff P, Delledonne M. 2008. Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. Proteomics, 8, 1459-1469.

[46]Rudd J J, Keon J, Hammond-Kosack K E. 2008. The wheat mitogen-activated protein kinases TaMPK3 and TaMPK6 are differentially regulated at multiple levels during compatible disease interactions with Mycosphaerella graminicola. Plant Physiology, 147, 802-815.

[47]Seo S, Sano H, Ohashi Y. 1999. Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco mitogen activated protein kinase. The Plant Cell, 11, 289-298.

[48]Simon-Plas F, Elmayan T, Blein J P. 2002. The plasma membrane oxidase Ntrboh D is responsible for AOS production in elicited tobacco cells. The Plant Journal, 31, 137-147.

[49]Sudhamsu J, Lee G I, Klessig D F, Crane B R. 2008 The structure of YqeH: An AtNOS1/AtNOA1 ortholog that couples GTP hydrolysis to molecular recognition. Journal of Biological Chemistry, 283, 32968-32978.

[50]Tiedemann A V. 1997. Evidence for a primary role of active oxygen species in induction of host cell death during infection of bean leaves with Botrytis cinerea. Physiological and Molecular Plant Pathology, 50, 151-166.

[51]Thomma B P H J, Tierens K F M, Penninckx I A M A, Mauch-Mani B, Broekaert W F, Cammue B P A. 2001. Different micro-organisms differentially induce Arabidopsis disease response pathways. Plant Physiology and Biochemistry, 39, 673-680.

[52]Torres M A, Dangl J L, Jones J D G. 2002. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proceedings of the National Academy of Sciences of the United States of America, 99, 517-522.

[53]Torres M A, Jones J D G, Dangl J L. 2005. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nature Genetics, 37, 1130-1134.

[54]Torres M A, Jones J D G, Dangl J L. 2006. Reactive oxygen species signaling in response to pathogens. Plant Physiology, 141, 373-378.

[55]Wendehenne D, Durner J, Klessig D F. 2004. Nitric oxide: A new player in plant signalling and defence responses. Current Opinion in Plant Biology, 7, 449-455.

[56]Yoshioka H, Asai S, Yoshioka M, Kobayashi M. 2009. Molecular mechanisms of generation for nitric oxide and reactive oxygen species, and role of the radical burst in plant immunity. Molecules and Cells, 28, 321-329.

[57]Yoshioka H, Sugie K, Park H J, Maeda H, Tsuda N, Kawakita K, Doke N. 2001. Induction of plant gp91 phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato. Molecular Plant-Microbe Interactions, 14, 725-736.

[58]Yoshioka H, Numata N, Nakajima K, Katou S, Kawakita K, Rowland O, Jones J D G, Doke N. 2003. Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. The Plant Cell, 15, 706-718.

[59]Zago E, Morsa S, Dat J F, Alard P, Ferrarini A, Inze D, Delledonne M, van Breusegem F. 2006. Nitric oxideand hydrogen peroxide responsive gene regulation during cell death induction in tobacco. The Plant Physiology, 141, 404-411.

[60]Zaninotto F, La Camera S, Polverari A, Delledonne M. 2006. Cross talk between reactive nitrogen and oxygen species during the hypersensitive disease resistance response. Plant Physiology, 141, 379-383.

[61]Zeidler D, Zahringer U, Gerber I, Dubery I, Hartung T, Bors W, Hutzler P, Durner J. 2004. Innate immunity in Arabidopsis thaliana: Lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proceedings of the National Academy of Sciences of the United States of America, 101, 15811-15816.

[62]Zemojtel T, Frohlich A, Palmieri M C, Kolanczyk M, Mikula I, Wyrwicz L S, Wanker E E, Mundlos S, Vingron M, Martasek P, et al. 2006. Plant nitric oxide synthase: A never-ending story? Trends in Plant Science, 11, 524-525.

[63]Zhang S, Klessig D F. 1997. Salicylic acid activates a 48 kD MAP kinase in tobacco. The Plant Cell, 9, 809-824.

[64]Zhang S, Liu Y, Klessig D F. 2000. Multiple levels of tobacco WIPK activation during the induction of cell death by fungal elicitins. The Plant Journal, 23, 339-347.

[65]Zhang Z, Feechan A, Pedersen C, Newman M A, Qiu J L, Olesen K L, Thordal-Christensen H. 2007. A SNAREprotein has opposing functions in penetration resistance and defense signaling pathways. The Plant Journal, 49, 302-312.

[66]Zhao M G, Tian Q Y, Zhang W H. 2007. Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiology, 144, 206-217.

The Role of Radical Burst in Plant Defense Responses to Necrotrophic Fungi

The Role of Radical Burst in Plant Defense Responses to Necrotrophic Fungi

PDF

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 6

编辑推荐

Metrics

[1]	LIU Yu-chen, WANG Juan, SU Pei-ying, MA Chun-mei , ZHU Shu-hua. Effect of Nitric Oxide on the Interaction Between Mitochondrial Malate Dehydrogenase and Citrate Synthase[J]. Journal of Integrative Agriculture, 2014, 13(12): 2616-2624.
[2]	ZHAO Xiu-feng, CHEN Lin, Muhammad I A Rehmani, WANG Qiang-sheng, WANG Shao-hua, HOU Pengfu, LI Gang-hua , DING Yan-feng. Effect of Nitric Oxide on Alleviating Cadmium Toxicity in Rice (Oryza sativa L.)[J]. Journal of Integrative Agriculture, 2013, 12(9): 1540-1550.
[3]	GUO Jun-xiang, CHEN Er-ying, YIN Yan-ping, WANG Ping, LI Yong, CHEN Xiao-guang, WU Guanglei. Nitric Oxide Content in Wheat Leaves and Its Relation to Programmed Cell Death of Main Stem and Tillers Under Different Nitrogen Levels[J]. Journal of Integrative Agriculture, 2013, 12(2): 239-250.
[4]	DONG Yu-xiu, WANG Xiu-feng , CUI Xiu-min. Exogenous Nitric Oxide Involved in Subcellular Distribution and Chemical Forms of Cu2+ Under Copper Stress in Tomato Seedlings[J]. Journal of Integrative Agriculture, 2013, 12(10): 1783-1790.
[5]	LIU Jing, HOU Zhi-hui, LIU Guo-hua, HOU Li-xia, LIU Xin. Hydrogen Sulfide May Function Downstream of Nitric Oxide in Ethylene- Induced Stomatal Closure in Vicia faba L.[J]. Journal of Integrative Agriculture, 2012, 12(10): 1644-1653.
[6]	LIU Li-qin, DONG Yu, GUAN Jun-feng. Effects of Nitric Oxide on the Quality and Pectin Metabolism of Yali Pears During Cold Storage[J]. Journal of Integrative Agriculture, 2011, 10(7): 1125-1133.