Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Plant defence responses: conservation between models and crops

Jonathan P. Anderson A , Louise F. Thatcher A B and Karam B. Singh A C
+ Author Affiliations
- Author Affiliations

A CSIRO Plant Industry, Centre for environment and life sciences, Private bag 5, Wembley, WA 6913, Australia.

B Soil Science and Plant Nutrition, School of Earth and Geographical Sciences, The University of Western Australia, Crawley, WA 6009, Australia.

C Corresponding author. Email: Karam.Singh@csiro.au

Functional Plant Biology 32(1) 21-34 https://doi.org/10.1071/FP04136
Submitted: 4 August 2004  Accepted: 19 September 2004   Published: 21 January 2005

Abstract

Diseases of plants are a major problem for agriculture world wide. Understanding the mechanisms employed by plants to defend themselves against pathogens may lead to novel strategies to enhance disease resistance in crop plants. Much of the research in this area has been conducted with Arabidopsis as a model system, and this review focuses on how relevant the knowledge generated from this model system will be for increasing resistance in crop plants. In addition, the progress made using other model plant species is discussed. While there appears to be substantial similarity between the defence responses of Arabidopsis and other plants, there are also areas where significant differences are evident. For this reason it is also necessary to increase our understanding of the specific aspects of the defence response that cannot be studied using Arabidopsis as a model.

Keywords: ethylene, jasmonate, pathogen, pathogenesis related genes, plant defense signalling pathways, plant disease, salicylic acid.


Acknowledgments

We thank Drs Peter Dodds and Kemal Kazan for helpful comments on the manuscript, and members of the Singh laboratory for useful discussions. We apologise for not being able to cite several important references because of length limitations. Work on plant defence in the authors’ laboratory is supported in part by the Grains Research and Development Corporation (GRDC) and the Department of Education, Science and Training (DEST).


References


Agrawal GK, Rakwal R, Jwa NS, Agrawal VP (2001) Signalling molecules and blast pathogen attack activates rice OsPR1a and OsPR1b genes: a model illustrating components participating during defence / stress response. Plant Physiology and Biochemistry 39, 1095–1103.
Crossref | GoogleScholarGoogle Scholar | open url image1

Akimoto-Tomiyama C, Sakata K, Yazaki J, Nakamura K, Fujii F , et al. (2003) Rice gene expression in response to n-acetylchitooligosaccharide elicitor: comprehensive analysis by DNA microarray with randomly selected ESTs. Plant Molecular Biology 52, 537–551.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Alvarez ME (2000) Salicylic acid in the machinery of hypersensitive cell death and disease resistance. Plant Molecular Biology 44, 429–442.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Anand A, Zhou T, Trick HN, Gill BS, Bockus WW, Muthukrishnan S (2003a) 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, 1101–1111.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Anand A, Schmelz EA, Muthukrishnan S (2003b) Development of a lesion-mimic phenotype in a transgenic wheat line overexpressing genes for pathogenesis-related (PR) proteins is dependent on salicylic acid concentration. Molecular Plant–Microbe Interactions 16, 916–925.
PubMed |
open url image1

Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) Map kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977–983.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ayliffe MA, Steinau M, Park RF, Rooke L, Pacheco MG, Hulbert SH, Trick HN, Pryor AJ (2004) Aberrant mRNA processing of the maize Rp1-D rust resistance gene in wheat and barley. Molecular Plant–Microbe Interactions 17, 853–864.
PubMed |
open url image1

Azevedo C, Sadanandom A, Kitagawa K, Freialdenhoven A, Shirasu K, Schulze-Lefert P (2002) The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295, 2073–2076.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bai JF, Pennill LA, Ning JC, Lee SW, Ramalingam J , et al. (2002) Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Research 12, 1871–1884.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bassett CL, Artlip TS, Callahan AM (2002) Characterization of the peach homologue of the ethylene receptor, PpETR1, reveals some unusual features regarding transcript processing. Planta 215, 679–688.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bent AF, Yu IC (1999) Applications of molecular biology to plant disease and insect resistance. Advances in Agronomy 66, 251–292. open url image1

Bertini L, Leonardi L, Caporale C, Tucci M, Cascone N, Di Berardino I, Buonocore V, Caruso C (2003) Pathogen-responsive wheat PR4 genes are induced by activators of systemic acquired resistance and wounding. Plant Science 164, 1067–1078.
Crossref | GoogleScholarGoogle Scholar | open url image1

Brown RL, Kazan K, McGrath KC, Maclean DJ, Manners JM (2003) A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis. Plant Physiology 132, 1020–1032.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Buttner M, Singh KB (1997) Arabidopsis thaliana ethylene-responsive element binding protein (AtEBP), an ethylene-inducible, GCC box DNA-binding protein interacts with an OCS element binding protein. Proceedings of the National Academy of Sciences USA 94, 5961–5966.
Crossref | GoogleScholarGoogle Scholar | open url image1

Caldo RA, Nettleton D, Wise RP (2004) Interaction-dependent gene expression in Mla-specified response to barley powdery mildew Plant Cell 16, 2514–2528.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chandra S, Martin GB, Low PS (1996) The Pto kinase mediates a signaling pathway leading to the oxidative burst in tomato. Proceedings of the National Academy of Sciences USA 93, 13 393–13 397.
Crossref | GoogleScholarGoogle Scholar | open url image1

Chen WP, Chen PD, Liu DJ, Kynast R, Friebe B, Velazhahan R, Muthukrishnan S, Gill BS (1999) Development of wheat scab symptoms is delayed in transgenic wheat plants that constitutively express a rice thaumatin-like protein gene. Theoretical and Applied Genetics 99, 755–760.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cheong YH, Moon BC, Kim JK, Kim CY, Kim MC , et al. (2003) BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor. Plant Physiology 132, 1961–1972.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fischer U, Dronge-Laser W (2004) Overexpression of NtERF5, a new member of the tobacco ethylene response transcription factor family enhances resistance to Tobacco mosaic virus Molecular Plant–Microbe Interactions 17, 1162–1171.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chern MS, Fitzgerald HA, Yadav RC, Canlas PE, Dong XN, Ronald PC (2001) Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis. The Plant Journal 27, 101–113.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E , et al. (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425, 973–977.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dervinis C, Clark DG, Barrett JE, Nell TA (2000) Effect of pollination and exogenous ethylene on accumulation of ETR1 homologue transcripts during flower petal abscission in geranium (Pelargonium × hortorum L.H. Bailey). Plant Molecular Biology 42, 847–856.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dodds PN, Lawrence GJ, Catanzariti AM, Ayliffe MA, Ellis JG (2004) The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. The Plant Cell 16, 755–768.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ekengren SK, Liu YL, Schiff M, Dinesh-Kumar SP, Martin GB (2003) Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. The Plant Journal 36, 905–917.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Elliott C, Zhou FS, Spielmeyer W, Panstruga R, Schulze-Lefert P (2002) Functional conservation of wheat and rice Mlo orthologs in defense modulation to the powdery mildew fungus. Molecular Plant–Microbe Interactions 15, 1069–1077.
PubMed |
open url image1

El-Sharkawy I, Jones B, Li ZG, Lelievre JM, Pech JC, Latche A (2003) Isolation and characterization of four ethylene perception elements and their expression during ripening in pears (Pyrus communis L.) with / without cold requirement. Journal of Experimental Botany 54, 1615–1625.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive detection system for the most conserved domain of the bacterial flagellin. The Plant Journal 18, 265–276.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fitzgerald HA, Chern MS, Navarre R, Ronald PC (2004) Overexpression of (At)NPR1 in rice leads to a BTH- and environment-induced lesion-mimic / cell death phenotype. Molecular Plant–Microbe Interactions 17, 140–151.
PubMed |
open url image1

Friedrich L, Moyer M, Ward E, Ryals J (1991) Pathogenesis-related protein-4 is structurally homologous to the carboxy-terminal domains of hevein, Win-1 and Win-2. Molecular and General Genetics 230, 113–119.
Crossref | PubMed |
open url image1

Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proceedings of the National Academy of Sciences USA 98, 373–378.
Crossref | GoogleScholarGoogle Scholar | open url image1

Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. The Plant Cell 12, 393–404.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J (1993) Requirement of salicylic-acid for the induction of systemic acquired-resistance. Science 261, 754–756. open url image1

Goff SA, Ricke D, Lan TH, Presting G, Wang RL , et al. (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296, 92–100.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gu YQ, Wildermuth MC, Chakravarthy S, Loh YT, Yang CM, He XH, Han Y, Martin GB (2002) Tomato transcription factors Pti4, Pti5, and Pti6 activate defense responses when expressed in Arabidopsis. The Plant Cell 14, 817–831.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Halterman DA, Wise RP (2004) A single-amino acid substitution in the sixth leucine-rich repeat of barley MLA6 and MLA13 alleviates dependence on RAR1 for disease resistance signalling The Plant Journal 38, 215–226.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hatakeyama K, Ishiguro S, Okada K, Takasaki T, Hinata K (2003) Antisense inhibition of a nuclear gene, BrDAD1, in Brassica causes male sterility that is restorable with jasmonic acid treatment. Molecular Breeding 11, 325–336.
Crossref | GoogleScholarGoogle Scholar | open url image1

Heath MC (2000) Hypersensitive response-related death. Plant Molecular Biology 44, 321–334.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hennin C, Diederichsen E, Hofte M (2001) Local and systemic resistance to fungal pathogens triggered by an AVR9-mediated hypersensitive response in tomato and oilseed rape carrying the Cf-9 resistance gene. Physiological and Molecular Plant Pathology 59, 287–295.
Crossref | GoogleScholarGoogle Scholar | open url image1

Horvath DP, Schaffer R, West M, Wisman E (2003) Arabidopsis microarrays identify conserved and differentially expressed genes involved in shoot growth and development from distantly related plant species. The Plant Journal 34, 125–134.
Crossref | PubMed |
open url image1

Hwang BK, Heitefuss R (1992) Induced resistance of spring barley to Erisyphe graminus f. sp. hordei. Phytopathology 103, 41–47. open url image1

Jorgensen JH (1996) Effect of three suppressors on the expression of powdery mildew resistance in barley. Genome 39, 492–498. open url image1

Jwa NS, Agrawal GK, Rakwal R, Park CH, Agrawal VP (2001) Molecular cloning and characterization of a novel jasmonate inducible pathogenesis-related class 10 protein gene, jiospr10, from rice (Oryza sativa L.) seedling leaves. Biochemical and Biophysical Research Communications 286, 973–983.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kang Z, Huang LL, Buchenauer H (2003) Subcellular localization of chitinase and beta-1,3-glucanase in compatible and incompatible interactions between wheat and Puccinia striiformis f. sp tritici. Zeitschrift Fur Pflanzenkrankheiten Und Pflanzenschutz-Journal of Plant Diseases and Protection 110, 170–183. open url image1

Kim JH, Lee JH, Joo S, Kim WT (1999) Ethylene regulation of an ERS1 homolog in mung bean seedlings. Physiologia Plantarum 106, 90–97.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kim JA, Agrawal GK, Rakwal R, Han KS, Kim KN, Yun CH, Heo SG, Park SY, Lee YH, Jwa NS (2003) Molecular cloning and mRNA expression analysis of a novel rice (Oryza sativa L.) MAPK kinase kinase, OsEDR1, an ortholog of Arabidopsis AtEDR1, reveal its role in defense / stress signalling pathways and development. Biochemical and Biophysical Research Communications 304, 215–216.
Crossref | GoogleScholarGoogle Scholar | open url image1

Knoester M, Hennig J, van Loon LC, Bol JF, Linthorst HJM (1997) Isolation and characterization of a tobacco cDNA encoding an ETR1 homolog (Accession No. AF022727). Plant Physiology 115, 1731. open url image1

Kobayashi Y, Yamada M, Kobayashi I, Kunoh H (1997) Actin microfilaments are required for the expression of non-host resistance in higher plants. Plant and Cell Physiology 38, 725–733. open url image1

Koczyk G, Chelkowski J (2003) An assessment of the resistance gene analogues of Oryza sativa ssp. japonica: Their presence and structure. Cellular and Molecular Biology Letters 8, 963–972.
PubMed |
open url image1

Kosugi S, Ohashi Y (2000) Cloning and DNA-binding properties of a tobacco ethylene-insensitive3 (EIN3) homolog. Nucleic Acids Research 28, 960–967.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kuhlmann M, Horvay K, Strathmann A, Heinekamp T, Fischer U, Bottner S, Droge-Laser W (2003) The alpha-helical D1 domain of the tobacco bZIP transcription factor BZI-1 interacts with the ankyrin-repeat protein ANK1 and is important for BZI-1 function, both in auxin signaling and pathogen response. Journal of Biological Chemistry 278, 8786–8794.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kumar D, Klessig DF (2000) Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene, and jasmonic acid. Molecular Plant–Microbe Interactions 13, 347–351.
PubMed |
open url image1

Kumar D, Klessig DF (2003) High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity. Proceedings of the National Academy of Sciences USA 100, 16 101–16 106.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17, 1244–1245.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lahaye T, Hartmann S, Topsch S, Freialdenhoven A, Yano M, Schulze-Lefert P (1998) High-resolution genetic and physical mapping of the Rar1 locus in barley. Theoretical and Applied Genetics 97, 526–534.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lashbrook CC, Tieman DM, Klee HJ (1998) Differential regulation of the tomato ETR gene family throughout plant development. The Plant Journal 15, 243–252.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lawton K, Ward E, Payne G, Moyer M, Ryals J (1992) Acidic and basic class-III chitinase messenger-RNA accumulation in response to TMV infection of tobacco. Plant Molecular Biology 19, 735–743.
Crossref | PubMed |
open url image1

Leclercq J, Adams-Phillips LC, Zegzouti H, Jones B, Latche A, Giovannoni JJ, Pech JC, Bouzayen M (2002) LeCTR1, a tomato CTR1-like gene, demonstrates ethylene signaling ability in Arabidopsis and novel expression patterns in tomato. Plant Physiology 130, 1132–1142.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lee JH, Kim WT (2003) Molecular and biochemical characterization of VR-EILs encoding mung bean ETHYLENE INSENSITIVE3-LIKE proteins. Plant Physiology 132, 1475–1488.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lee MW, Qi M, Yang YO (2001) A novel jasmonic acid-inducible rice Myb gene associates with fungal infection and host cell death. Molecular Plant–Microbe Interactions 14, 527–535.
PubMed |
open url image1

Li L, Zhao YF, McCaig BC, Wingerd BA, Wang JH, Whalon ME, Pichersky E, Howe GA (2004) The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. The Plant Cell 16, 126–143.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lin W-C, Lu C-F, Wu J-W, Cheng M-L, Lin Y-M, Yang N-S, Black L, Green SK, Weng J-W, Cheng C-P (2004) Transgenic tomato plants expressing the Arabidopsis NPR1 gene display enhanced resistance to a spectrum of fungal and bacterial diseases. Transgenic research 13, 567–581.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lindsey K, Casson S, Chilley P (2002) Peptides: new signalling molecules in plants. Trends in Plant Science 7, 78–83.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Liu Y, Schiff M, Marathe R, Dinesh-Kumar SP (2002a) Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. The Plant Journal 30, 415–429.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Liu Y, Schiff M, Serino G, Deng XW, Dinesh-Kumar SP (2002b) Role of SCF ubiquitin-ligase and the COP9 signalosome in the N gene-mediated resistance response to tobacco mosaic virus. The Plant Cell 14, 1483–1496.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ma QH, Wang XM (2003) Characterization of an ethylene receptor homologue from wheat and its expression during leaf senescence. Journal of Experimental Botany 54, 1489–1490.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic-acid — a likely endogenous signal in the resistance response of tobacco to viral-infection. Science 250, 1002–1004. open url image1

Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nature Genetics 26, 403–410.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Martinez-Abarca F, Herrera-Cervera JA, Bueno P, Sanjuan J, Bisseling T, Olivares J (1998) Involvement of salicylic acid in the establishment of the Rhizobium meliloti – alfalfa symbiosis. Molecular Plant–Microbe Interactions 11, 153–155. open url image1

Martinez PG, Gomez RL, Gomez-Lim MA (2001) Identification of an ETR1-homologue from mango fruit expressing during fruit ripening and wounding. Journal of Plant Physiology 158, 101–108. open url image1

McDowell JM, Dangl JL (2000) Signal transduction in the plant immune response. Trends in Biochemical Sciences 25, 79–82.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Menke FLH, Champion A, Kijne JW, Memelink J (1999) A novel jasmonate- and elicitor-responsive element in the periwinkle secondary metabolite biosynthetic gene Str interacts with a jasmonate- and elicitor-inducible AP2-domain transcription factor, ORCA2. EMBO Journal 18, 4455–4463.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mita S, Kawamura S, Asai T (2002) Regulation of the expression of a putative ethylene receptor, PeERS2, during the development of passion fruit (Passiflora edulis). Physiologia Plantarum 114, 271–280.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mithofer A (2002) Suppression of plant defence in rhizobia-legume symbiosis. Trends in Plant Science 7, 440–444.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mysore KS, Crasta OR, Tuori RP, Folkerts O, Swirsky PB, Martin GB (2002) Comprehensive transcript profiling of Pto- and Prf-mediated host defense responses to infection by Pseudomonas syringae pv. tomato. The Plant Journal 32, 299–315.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mysore KS, Ryu CM (2004) Non-host resistance: how much do we know? Trends in Plant Science 9, 97–104.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Niggeweg R, Thurow C, Weigel R, Pfitzner U, Gatz C (2000) Tobacco TGA factors differ with respect to interaction with NPR1, activation potential and DNA-binding properties. Plant Molecular Biology 42, 775–788.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nuhse TS, Peck SC, Hirt H, Boller T (2000) Microbial elicitors induce activation and dual phosphorylation of the Arabidopsis thaliana MAPK 6. Journal of Biological Chemistry 275, 7521–7526.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. The Plant Cell 7, 173–182.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ohta M, Ohme Takagi M, Shinshi H (2000) Three ethylene-responsive transcription factors in tobacco with distinct transactivation functions. The Plant Journal 22, 29–38.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ohta M, Matsui K, Hiratsu K, Shinshi H, Ohme-Takagi M (2001) Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. The Plant Cell 13, 1959–1968.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Papadopoulou K, Melton RE, Leggett M, Daniels MJ, Osbourn AE (1999) Compromised disease resistance in saponin-deficient plants. Proceedings of the National Academy of Sciences USA 96, 12 923–12 928.
Crossref | GoogleScholarGoogle Scholar | open url image1

Payne G, Parks TD, Burkhart W, Dincher S, Ahl P, Metraux JP, Ryals J (1988a) Isolation of the genomic clone for pathogenesis-related protein-1a from Nicotiana tabacum cv xanthi-nc. Plant Molecular Biology 11, 89–94.
Crossref |
open url image1

Payne G, Middlesteadt W, Williams S, Desai N, Parks TD, Dincher S, Carnes M, Ryals J (1988b) Isolation and nucleotide sequence of a novel cDNA clone encoding the major form of pathogenesis-related protein-R. Plant Molecular Biology 11, 223–224.
Crossref |
open url image1

Payne G, Ahl P, Moyer M, Harper A, Beck J, Meins F, Ryals J (1990a) Isolation of complementary-DNA clones encoding pathogenesis-related protein-P and protein-Q, 2 acidic chitinases from tobacco. Proceedings of the National Academy of Sciences USA 87, 98–102. open url image1

Payne G, Ward E, Gaffney T, Goy PA, Moyer M, Harper A, Meins F, Ryals J (1990b) Evidence for a 3rd structural class of beta-1,3-glucanase in tobacco. Plant Molecular Biology 15, 797–808.
Crossref | PubMed |
open url image1

Peart JR, Cook G, Feys BJ, Parker JE, Baulcombe DC (2002) An EDS1 orthologue is required for N-mediated resistance against tobacco mosaic virus. The Plant Journal 29, 569–579.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Peterhansel C, Freialdenhoven A, Kurth J, Kolsch R, Schulze Lefert P (1997) Interaction analyses of genes required for resistance responses to powdery mildew in barley reveal distinct pathways leading to leaf cell death. The Plant Cell 9, 1397–1409.
Crossref | PubMed |
open url image1

Piedras P, Hammond-Kosack KE, Harrison K, Jones JDG (1998) Rapid, Cf-9- and Avr9-dependent production of active oxygen species in tobacco suspension cultures. Molecular Plant–Microbe Interactions 11, 1155–1166. open url image1

Rasori A, Ruperti B, Bonghi C, Tonutti P, Ramina A (2002) Characterization of two putative ethylene receptor genes expressed during peach fruit development and abscission. Journal of Experimental Botany 53, 2333–2339.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ren D, Yang H, Zhang S (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. Journal of Biological Chemistry 277, 559–565.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rieu I, Mariani C, Weterings K (2003) Expression analysis of five tobacco EIN3 family members in relation to tissue-specific ethylene responses. Journal of Experimental Botany 54, 2239–2244.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ronald PC, Salmeron JM, Carland FM, Staskawicz BJ (1992) The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto resistance gene. Journal of Bacteriology 174, 1604–1611.
PubMed |
open url image1

Sakamoto A, Minami M, Huh GH, Iwabuchi M (1993) The putative zinc-finger protein wzf1 interacts with a cis-acting element of wheat histone genes. European Journal of Biochemistry 217, 1049–1056.
PubMed |
open url image1

Schenk PM, Kazan K, Manners JM, Anderson JP, Simpson RS, Wilson IW, Somerville S, Maclean DJ (2003) Systemic gene expression in Arabidopsis during an incompatible interaction with Alternaria brassicicola. Plant Physiology 132, 999–1010.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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. Proceedings of the National Academy of Sciences USA 97, 11 655–11 660.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schweizer P, Hunziker W, Mosinger E (1989) Complementary DNA cloning, in vitro transcription and partial sequence analysis of messenger RNA from winter wheat (Triticum aestivum L.) with induced resistance to Erysiphe graminis f. sp. tritici. Plant Molecular Biology 12, 643–654.
Crossref |
open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Shetty NP, Kristensen BK, Newman MA, Moller K, Gregersen PL, Jorgensen HJL (2003) Association of hydrogen peroxide with restriction of Septoria tritici in resistant wheat. Physiological and Molecular Plant Pathology 62, 333–346.
Crossref | GoogleScholarGoogle Scholar | open url image1

Shirasu K, Lahaye T, Tan MW, Zhou FS, Azevedo C, Schulze-Lefert P (1999) A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell 99, 355–366.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Silverman P, Seskar M, Kanter D, Schweizer P, Metraux JP, Raskin I (1995) Salicylic-acid in rice — biosynthesis, conjugation, and possible role. Plant Physiology 108, 633–639.
PubMed |
open url image1

Smith JA, Metraux J-P (1991) Pseudomonas syringae pv. syringae induces systemic acquired resistance to Pyricularia oryzae in rice. Physiological and Molecular Plant Pathology 39, 451–461.
Crossref |
open url image1

Song F, Goodman RM (2001) Activity of nitric oxide is dependent on, but is partially required for function of, salicylic acid in the signalling pathway in tobacco systemic acquired resistance. Molecular Plant–Microbe Interactions 14, 1458–1462.
PubMed |
open url image1

Suzuki K, Suzuki N, Ohme-Takagi M, Shinshi H (1998) Immediate early induction of mRNAs for ethylene-responsive transcription factors in tobacco leaf strips after cutting. The Plant Journal 15, 657–665.
Crossref | GoogleScholarGoogle Scholar | open url image1

Suzuki K (2002) MAP kinase cascades in elicitor signal transduction. Journal of Plant Research 115, 237–244.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tai TH, Dahlbeck D, Clark ET, Gajiwala P, Pasion R, Whalen MC, Stall RE, Staskawicz BJ (1999) Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proceedings of the National Academy of Sciences USA 96, 14153–14158.
Crossref | GoogleScholarGoogle Scholar | open url image1

Terajima Y, Nukui H, Kobayashi A, Fujimoto S, Hase S, Yoshioka T, Hashiba T, Satoh S (2001) Molecular cloning and characterization of a cDNA for a novel ethylene receptor, NT-ERS1, of tobacco (Nicotiana tabacum L.). Plant and Cell Physiology 42, 308–313.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Thaler JS, Owen B, Higgins VJ (2004) The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiology 135, 530–538.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Thatcher L, Anderson JP, Singh KB (2004) Plant defence responses: what have we learnt from Arabidopsis?  31, 1–19. open url image1

Thilmony RL, Chen ZT, Bressan RA, Martin GB (1995) Expression of the tomato Pto Gene in tobacco enhances resistance to Pseudomonas syringae pv tabaci expressing AvrPto. The Plant Cell 7, 1529–1536.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch Mani B, Vogelsang R, Cammue BPA, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proceedings of the National Academy of Sciences USA 95, 15 107–15 111.
Crossref | GoogleScholarGoogle Scholar | open url image1

Thomma BPHJ, Eggermont K, Broekaert WF, Cammue BPA (2000) Disease development of several fungi on Arabidopsis can be reduced by treatment with methyl jasmonate. Plant Physiology and Biochemistry 38, 421–427.
Crossref | GoogleScholarGoogle Scholar | open url image1

Thomma BPHJ, Cammue BPA, Thevissen K (2002) Plant defensins. Planta 216, 193–202.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Thordal-Christensen H (2003) Fresh insights into processes of non-host resistance. Current Opinion in Plant Biology 6, 351–357.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tieman DM, Taylor MG, Ciardi JA, Klee HJ (2000) The tomato ethylene receptors NR and LeETR4 are negative regulators of ethylene response and exhibit functional compensation within a multigene family. Proceedings of the National Academy of Sciences USA 97, 5663–5668.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tieman DM, Ciardi JA, Taylor MG, Klee HJ (2001) Members of the tomato LeEIL (EIN3-like) gene family are functionally redundant and regulate ethylene responses throughout plant development. The Plant Journal 26, 47–58.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Van der Hoorn RAL, Laurent F, Roth R, De Wit P (2000) Agroinfiltration is a versatile tool that facilitates comparative analyses of Avr9 / Cf-9-induced and Avr4 / Cf-4-induced necrosis. Molecular Plant–Microbe Interactions 13, 439–446.
PubMed |
open url image1

van der Fits L, Memelink J (2001) The jasmonate-inducible AP2 / ERF-domain transcription factor ORCA3 activates gene expression via interaction with a jasmonate-responsive promoter element. The Plant Journal 25, 43–53.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ward ER, Payne GB, Moyer MB, Williams SC, Dincher SS , et al. (1991) Differential regulation of beta-1,3-glucanase messenger-RNAs in response to pathogen infection. Plant Physiology 96, 390–397. open url image1

Wei F, Gobelman-Werner K, Morroll SM, Kurth J, Mao L, Wing R, Leister D, Schulze-Lefert P, Wise RP (1999) The Mla (powdery mildew) resistance cluster is associated with three NBSLRR gene families and suppressed recombination within a 300-kb DNA interval on chromosome 5S (1Hs) of barley. Genetics 153, 1929–1948.
PubMed |
open url image1

Whitham S, McCormick S, Baker B (1996) The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato. Proceedings of the National Academy of Sciences USA 93, 8776–8781.
Crossref | GoogleScholarGoogle Scholar | open url image1

Xiao SY, Charoenwattana P, Holcombe L, Turner JG (2003) The Arabidopsis genes RPW8.1 and RPW8.2 confer induced resistance to powdery mildew diseases in tobacco. Molecular Plant–Microbe Interactions 16, 289–294.
PubMed |
open url image1

Yan JQ, Wang J, Zhang H (2002) An ankyrin repeat-containing protein plays a role in both disease resistance and antioxidation metabolism. The Plant Journal 29, 193–202.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yang KY, Liu YD, Zhang SQ (2001) Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proceedings of the National Academy of Sciences USA 98, 741–746.
Crossref | GoogleScholarGoogle Scholar | open url image1

Yau CP, Wang LJ, Yu MD, Zee SY, Yip WK (2004) Differential expression of three genes encoding an ethylene receptor in rice during development, and in response to indole-3-acetic acid and silver ions. Journal of Experimental Botany 55, 547–556.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yu J, Hu SN, Wang J, Wong GKS, Li SG , et al. (2002) A draft sequence of the rice genome (Oryza sativa L.ssp indica). Science 296, 79–92.
Crossref | PubMed |
open url image1

Zhang SQ, Klessig DF (1998) The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK. Proceedings of the National Academy of Sciences USA 95, 7225–7230.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zhou DB, Kalaitzis P, Mattoo AK, Tucker ML (1996) The mRNA for an ETR1 homologue in tomato is constitutively expressed in vegetative and reproductive tissues. Plant Molecular Biology 30, 1331–1338.
Crossref | PubMed |
open url image1

Zhou JM, Tang XY, Martin GB (1997) The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO Journal 16, 3207–3218.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1