Abstract
Rice sheath blight, caused by Rhizoctonia solani is one of the major diseases of rice. The pathogen infects rice plants directly through stomata or using lobate appressoria and hyphal masses called infection cushions. The infection structures were normally found at 36 h post-inoculation. During infection, the pathogenesis-related genes, PR1b and PBZ1 were induced in rice plants. To identify rice genes induced early in the defense response, suppression subtractive hybridization (SSH) was used to generate a cDNA library enriched for transcripts differentially expressed during infection by R. solani. After differential screening by membrane-based hybridization and subsequent confirmation by reverse Northern blot analysis, selected clones were sequenced. Fifty unique cDNA clones were found and assigned to five different functional categories. Most of the genes were not previously identified as being induced in response to pathogens. We examined expression of 100 rice genes induced by infection with Magnaporthe grisea, Xanthomonas oryzae pv. oryze (Xoo) and X. oryzae pv. oryzicola (Xooc). Twenty-five of them were found to be differentially expressed after the sheath blight infection, suggesting overlap of defense responses to different fungal and bacterial pathogens infection.
Similar content being viewed by others
References
Agrawal GK, Iwahashi H, Rakwal R (2003) Rice MAPKs. Biochem Biophys Res Commun 302:171–180
Arcuri F, Papa S, Meini A, Carducci A, Romagnoli R, Bianchi L, Riparbelli MG, Sanchez JC, Palmi M, Tosi P, Cintorino M (2005) The translationally controlled tumor protein is a novel calcium binding protein of the human placenta and regulates calcium handling in trophoblast cells. Biol Reprod 73:745–751
Austin MJ, Muskett P, Kahn K, Feys BJ, Jones JD, Parker JE (2002) Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295:2077–2080
Bonmann JM, Khush GS, Nelson RJ (1992) Breeding rice for resistance to pests. Annu Rev Phytopathol 30:507–523
Bovie C, Ongena M, Thonart P, Dommes J (2004) Cloning and expression analysis of cDNAs corresponding to genes activated in cucumber showing systemic acquired resistance after BTH treatment. BMC Plant Biol 4:15
Cans C, Passer BJ, Shalak V, Nancy-Portebois V, Crible V, Amzallag N, Allanic D, Tufino R, Argentini M, Moras D, Fiucci G, Goud B, Mirande M, Amson R, Telerman A (2003) Translationally controlled tumor protein acts as a guanine nucleotide dissociation inhibitor on the translation elongation factor eEF1A. Proc Natl Acad Sci USA 100:13892–13897
Chang C, Shockey JA (1999) The ethylene-response pathway: signal perception to gene regulation. Curr Opin Plant Biol 2:352–358
Chen S, Vaghchhipawala Z, Li W, Asard H, Dickman MB (2004) Tomato phospholipid hydroperoxide glutathione peroxidase inhibits cell death induced by Bax and oxidative stresses in yeast and plants. Plant Physiol 135:1630–1641
Chern MS, Fitzgerald HA, Yadav RC, Canlas PE, Dong X, Ronald PC (2001) Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis. Plant J 27:101–113
Chern MS, Fitzgerald HA, Canlas PE, Navarre DA, Ronald PC (2005a) Overexpression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light. Mol Plant Microbe Interact 18:511–520
Chern MS, Canlas PE, Fitzgerald HA, Ronald PC (2005b) Rice NRR, a negative regulator of disease resistance, interacts with Arabidopsis NPR1 and rice NH1. Plant J 43:623–631
Conklin PL, Last RL (1995) Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiol 109:203–212
Culley DE, Horovitz D, Hadwiger LA (1995) Molecular characterization of disease-resistance response gene DRR206-d from Pisum sativum (L.). Plant Physiol 107:301–302
Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 14:826–833
Denby KJ, Kumar P, Kliebenstein DJ (2004) Identification of Botrytis cinerea susceptibility loci in Arabidopsis thaliana. Plant J 38:473–486
Devoto A, Muskett PR, Shirasu K (2003) Role of ubiquitination in the regulation of plant defence against pathogens. Curr Opin Plant Biol 6:307–311
Dreher K, Callis J (2007) Ubiquitin, hormones and biotic stress in plants. Ann Bot 99:787–822
Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209
Etheridge N, Chen YF, Schaller GE (2005) Dissecting the ethylene pathway of Arabidopsis. Brief Funct Genomic Proteomic 3:372–381
Freemont PS (2000) Ubiquitination: RING for destruction? Curr Biol 10:R84–R87
Fristensky B, Horovitz D, Hadwiger L (1988) cDNA sequences for pea disease resistance response genes. Plant Mol Biol 11:713–715
Gatzek S, Wheeler GL, Smirnoff N (2002) Antisense suppression of l-galactose dehydrogenase in Arabidopsis thaliana provides evidence for its role in ascorbate synthesis and reveals light modulated l-galactose synthesis. Plant J 31:541–553
Gepstein S, Sabehi G, Carp MJ, Hajouj T, Nesher MF, Yariv I, Dor C, Bassani M (2003) Large-scale identification of leaf senescence-associated genes. Plant J 36:629–642
Gesch RW, Boote KJ, Vu JC, Hartwell Allen L Jr, Bowes G (1998) Changes in growth CO2 result in rapid adjustments of ribulose-1, 5-bisphosphate carboxylase/oxygenase small subunit gene expression in expanding and mature leaves of rice. Plant Physiol 118:521–529
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Ann Rev Phytopathol 43:205–227
Gonzalez-Lamothe R, Tsitsigiannis DI, Ludwig AA, Panicot M, Shirasu K, Jones JD (2006) The U-box protein CMPG1 is required for efficient activation of defense mechanisms triggered by multiple resistance genes in tobacco and tomato. Plant Cell 18:1067–1083
Govrin EM, Levine A (2000). The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10:751–757
Hajduch M, Rakwal R, Agrawal GK, Yonekura M, Pretova A (2001) High-resolution two-dimensional electrophoresis separation of proteins from metal-stressed rice (Oryza sativa L.) leaves: drastic reductions/fragmentation of ribulose-1, 5-bisphosphate carboxylase/oxygenase and induction of stress-related proteins. Electrophoresis 22:2824–2831
Han CU, Lee CH, Jang KS, Choi GJ, Lim HK, Kim JC, Ahn S-N, Choi JE, Cha JS, Kim HT, Cho KY, Lee S-W (2004) Identification of rice genes induced in a rice blast-resistant mutant. Mol Cells 17:462–468
Jantasuriyarat C, Gowda M, Haller K, Hatfield J, Lu G, Stahlberg E, Zhou B, Li H, Kim H, Yu Y, Dean RA, Wing RA, Soderlund C, Wang G-L (2005) Large-scale identification of expressed sequence tags involved in rice and rice blast fungus interaction. Plant Physiol 138:105–115
Jung HW, Hwang BK (2000) Isolation, partial sequencing, and expression of pathogenesis-related cDNA genes from pepper leaves infected by Xanthomonas campestris pv. vesicatoria. Mol Plant Microbe Interact 13:136–142
Kang SG, Jeong HK, Suh HS (2004) Characterization of a new member of the glutathione peroxidase gene family in Oryza sativa. Mol Cells 17:23–28
Kawasaki T, Henmi K, Onstenk J, Hatakeyama S, Iwano M, Satoh H, Shimamoto K (1999) The small GTP-binding protein Rac is a regulator of cell death in plants. Proc Natl Acad Sci USA 96:10922–10926
Kim CY, Lee SH, Park HC, Bae CG, Cheong YH, Choi YJ, Han C, Lee SY, Lim CO, Cho MJ (2000) Identification of rice blast fungal elicitor-responsive genes by differential display analysis. Mol Plant Microbe Interact 13:470–474
Kim HS, Delaney TP (2002) Arabidopsis SON1 is an F-box protein that regulates a novel induced defense response independent of both salicylic acid and systemic acquired resistance. Plant Cell 14:1469–1482
Kim WY, Kim CY, Cheong NE, Choi YO, Lee KO, Lee SH, Park JB, Nakano A, Bahk JD, Cho MJ, Lee SY (1999) Characterization of two fungal-elicitor-induced rice cDNAs encoding functional homologues of the rab-specific GDP-dissociation inhibitor. Planta 210:143–149
Laxalt AM, Cassia RO, Sanllorenti PM, Madrid EA, Andreu AB, Daleo GR, Conde RD, Lamattina L (1996) Accumulation of cytosolic glyceraldehyde-3-phosphate dehydrogenase RNA under biological stress conditions and elicitor treatments in potato. Plant Mol Biol 30:961–972
Lee MW, Qi M, Yang Y (2001) A novel jasmonic acid-inducible rice myb gene associates with fungal infection and host cell death. Mol Plant Microbe Interact 14: 527–535
Lee WY, Hong JK, Kim CY, Chun HJ, Park HC, Kim JC, Yun D-J, Chung WS, Lee S-H, Lee SY, Cho MJ, Lim CO (2003) Over-expressed rice ADP-ribosylation factor 1 (RARF1) induces pathogenesis-related genes and pathogen resistance in tobacco plants. Physiol Plant 119:573–581
Liu XQ, Bai XQ, Qian Q, Wang XJ, Chen MS, Chu CC (2005) OsWRKY03, a rice transcriptional activator that functions in defense signaling pathway upstream of OsNPR1. Cell Res 15:593–603
Lu G, Jantasuriyarat C, Zhou B, Wang G-L (2004) Isolation and characterization of novel defense response genes involved in compatible and incompatible interactions between rice and Magnaporthe grisea. Theor Appl Genet 108:525–534
MacDonald SM, Rafnar T, Langdon J, Lichtenstein LM (1995) Molecular identification of an IgE-dependent histamine-releasing factor. Science 269:688–690
Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436
McElver J, Patton D, Rumbaugh M, Liu C, Yang LJ, Meinke D (2000) The TITAN5 gene of Arabidopsis encodes a protein related to the ADP ribosylation factor family of GTP binding proteins. Plant Cell 12:1379–1392
Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND (1999) Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J 20: 317–332
Midoh N, Iwate M (1996) Cloning and characterization of a probenazole-inducible gene for an intracellular pathogenesis-related protein in rice. Plant Cell Physiol 37:9–18
Mokranjac D, Neupert W (2005) Protein import into mitochondria. Biochem Soci Transact 33:1019–1023
Mou Z, He Y, Dai Y, Liu X, Li J (2000) Deficiency in fatty acid synthase leads to premature cell death and dramatic alterations in plant morphology. Plant Cell 12:405–417
Mouly A, Rumeau D, Esquerre-Tugaye M-T (1992) Differential accumulation of hydroxyproline-rich glycoprotein transcripts in sunflower plants infected with Sclerotinia sclerotiorum or treated with oxalic acid. Plant Sci 85:51–59
Mudgil Y, Singh B, Upadhyaya K, Sopory S, Reddy M (2002) Cloning and characterization of a cell cycle-regulated gene encoding Topoisomerase I from Nicotiana tabacum that is inducible by light, low temperature and abscisic acid. Mol Genet Genomics 267:380–390
Park AR, Cho SK, Yun UJ, Jin MY, Lee SH, Sachetto-Martins G, Park OK (2001) Interaction of the Arabidopsis receptor protein kinase Wak1 with a glycine-rich protein, AtGRP-3. J Biol Chem 276:26688–26693
Pei Y, Dong H, Li D (2002) Microarray analysis of rice gene expression specific induced by Xanthomonas oryzae pv. oryzae. J Agri Biotechnol 10:321–326
Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, Koncz C, Genschik P (2003) EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell 115:679–689
Qiu D, Xiao J, Ding X, Xiong M, Cai M, Cao Y, Li X, Xu C, Wang S (2007) OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol Plant Microbe Interact 20:492–4999
Quirino BF, Normanly J, Amasino RM (1999) Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogen-independent induction of defense-related genes. Plant Mol Biol 40:267–278
Rao Z, Dong H, Zhuang J, Chai R, Fan Y, Li D, Zheng K (2002) Analysis of gene expression profiles during host-Magnaporthe grisea interaction in a pair of near isogenic lines of rice. Acta Genet Sin 29:887–893
Rauyaree P, Choi W, Fang E, Blackmon B, Dean RA (2001) Genes expressed during early stages of rice infection with the rice blast fungus Magnaporthe grisea. Mol Plant Pathol 2:347–354
Ricard B, Rivoal J, Pradet A (1989) Rice cytosolic glyceraldehydes 3-phosphate dehydrogenase contains two subunits differentially regulated by anaerobiosis. Plant Mol Biol 12:131–139
Romeis T, Ludwig AA, Martin R, Jones JDG (2001) Calcium-dependent protein kinase plays an essential role in the plant defense response. EMBO J, 20:5556–5567
Roitsch T, Gonza´lez M-C (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9:606–613
Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steriner HY, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809–1819
Sachetto-Martins G, Franco LO, de Oliveira DE (2000) Plant glycine-rich proteins: a family or just proteins with a common motif? Biochim Biophys Acta 1492:1–14
Sachs MM, Subbaiah CC, Saab IN (1996) Anaerobic gene expression and flooding tolerance in maize. J Exp Bot 47:1–15
Sage-Ono K, Ono M, Harada H, Kamada H (1998) Dark-induced accumulation of mRNA for a homolog of translationally controlled tumor protein (TCTP) in Pharbitis. Plant Cell Physiol 39:357–360
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor
Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655–11660
Schweizer P, Buchala A, Dudler R, Metraux JP (1998) Induced systemic resistance in wounded rice plants. Plant J 14:475–481
Shen S, Jing Y, Kuang T (2003) Proteomics approach to identify wound-response related proteins from rice leaf sheath. Proteomics 3:527–535
Song WY, Wang G-L, Chen L-L, Kim H-S, Pi L-Y, Holsten T, Gardner J, Wang B, Zhai W-X, Zhu L-H, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806
Stepanova AN, Alonso JM (2005) Arabidopsis ethylene signaling pathway. Sci STKE 276:cm4
Swiderski MR, Innes RW (2001) The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. Plant J 26:101–112
Takahashi A, Kawasaki T, Henmi K, ShiI K, Kodama O, Satoh H, Shimamoto K (1999) Lesion mimic mutants of rice with alterations in early signaling events of defense. Plant J 17:535–545
Takai R, Matsuda N, Nakano A, Hasegawa K, Akimoto C, Shibuya N, Minami E (2002) EL5, a rice N-acetylchitooligosaccharide elicitor-responsive RING-H2 finger protein, is a ubiquitin ligase which functions in vitro in co-operation with an elicitor-responsive ubiquitin-conjugating enzyme, OsUBC5b. Plant J 30:447–455
Thomma BP, Eggermont K, Tierens KF, Broekaert WF (1999) Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiol 121:1093–1102
Umeda M, Uchimiya H (1994) Differential transcript levels of genes associated with glycolysis and alcohol fermentation in rice plants (Oryza sativa L.) under submergence stress. Plant Physiol 106:1015–1022
Van Baarlen P, Woltering EJ, Staats M, Van Kan JA (2007) Histochemical and genetic analysis of host and non-host interactions of Arabidopsis with three Botrytis species: an important role for cell death control. Mol Plant Pathol 8: 41–54
Wan J, Dunning FM, Bent AF (2002) Probing plant–pathogen interactions and downstream defense signaling using DNA microarrays. Funct Integr Genomics 2:259–273
Wang Y, Zhang W, Cao J, McElroy D, Wu R (1992) Characterization of cis-acting elements regulating transcription from the promoter of a constitutively active rice actin gene. Mol Cell Biol 12:3399–3406
Woodger FJ, Gubler F, Pogson BJ, Jacobsen JV (2003) A Mak-like kinase is a repressor of GAMYB in barley aleurone. Plant J 33:707–717
Xiao F, Tang X, Zhou JM (2001) Expression of 35S Pto globally activates defense-related genes in tomato plants. Plant Physiol 126:1637–1645
Xiong L, Lee MW, Qi M, Yang Y (2001) Identification of defenserelated rice genes by suppression subtractive hybridization and differential screening. Mol Plant Microbe Interact 14:685–692
Xiong L, Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 15:745–759
Yanagisawa S, Izui K (1993) Molecular cloning of two DNA-binding proteins of maize that are structurally different but interact with the same sequence motif. J Biol Chem 268:16028–16036
Yang EJ, Oh YA, Lee ES, Park AR, Cho SK, Yoo YJ, Park OK (2003) Oxygen-evolving enhancer protein 2 is phosphorylated by glycine-rich protein 3/wall-associated kinase 1 in Arabidopsis. Biochem Biophys Res Commun 305:862–868
Yin Z, Chen J, Zeng L, Goh M, Leung H, Khush GS, Wang G-L (2000) Characterizing rice lesion mimic mutants and identifying a mutant with broad-spectrum resistance to rice blast and bacterial blight. Mol Plant Microbe Interact 13:869–876
Zeng LR, Vega-Sánchez ME, Zhu T, Wang GL (2006) Ubiquitination-mediated protein degradation and modification: an emerging theme in plant–microbe interactions. Cell Res 16:413–426
Zeng L-R, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, Xie Q, Nahm BH, Leung H, Wang G-L (2004) Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-Box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16:2795–2808
Zhang S, Klessig DF (2001) MAPK cascades in plant defense signaling. Trends Plant Sci. 6:520–527
Zhou B, Peng K, Chu Z, Wang S, Zhang Q (2002) The defense-responsive genes showing enhanced and repressed expression after pathogen infection in rice (Oryza stativa L). Sci China (Series C) 45:449–467
Zhou J-M, Loh Y-T, Bressan RA, Martin GB (1995) The tomato gene Pti1 encodes a serine-threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell 83:925–935
Acknowledgments
This research was supported by National Basic Research Program of China (Project No. 2006CB1019001), Commonweal Research Program of Agricultural Science of China (Project No. nyhyzx07-049) and Natural Science Foundation of Fujian Province of China (Project No. 2003F008). We thank Dr. Daniel Ebbole of Texas A & M University for his critical reading of the manuscript.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Communicated by M. Xu.
Chang-Jiang Zhao and Ai-Rong Wang contributed equally to this work.
Rights and permissions
About this article
Cite this article
Zhao, CJ., Wang, AR., Shi, YJ. et al. Identification of defense-related genes in rice responding to challenge by Rhizoctonia solani . Theor Appl Genet 116, 501–516 (2008). https://doi.org/10.1007/s00122-007-0686-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-007-0686-y