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Insight into Types I and II nonhost resistance using expression patterns of defense-related genes in tobacco

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Abstract

Plants protect themselves against pathogens using a range of response mechanisms. There are two categories of nonhost resistance: Type I, which does not result in visible cell death; and Type II, which entails localized programmed cell death (or hypersensitive response) in response to nonhost pathogens. The genes responsible for these two systems have not yet been intensively investigated at the molecular level. Using tobacco plants (Nicotiana tabacum), we compared expression of 12 defense-related genes between a Type I (Xanthomonas axonopodis pv. glycines 8ra) nonhost interaction, and two Type II (Pseudomonas syringae pv. syringae 61 and P. syringae pv. phaseolicola NPS3121) nonhost interactions, as well as those expressed during R gene-mediated resistance to Tobacco mosaic virus. In general, expression of most defense-related genes during R gene-mediated resistance was activated 48 h after challenge by TMV; the same genes were upregulated as early as 9 h after infiltration by nonhost pathogens. Surprisingly, X. axonopodis pv. glycines (Type I) elicited the same set of defense-related genes as did two pathovars of P. syringae, despite the absence of visible cell death. In two examples of Type II nonhost interactions, P. syringae pv. phaseolicola NPS3121 produced an expression profile more closely resembling that of X. axonopodis pv. glycines 8ra, than that of P. syringae pv. syringae 61. These results suggest that Type I nonhost resistance may act as a mechanism providing a more specific and active defense response against a broad range of potential pathogens.

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Abbreviations

Ng-CDM1 :

Nicotiana glutinosa-cell death marker1

MAPK:

Mitogen-activated protein kinase

Nt-hsr203J :

Nicotiana tabacum-hypersensitive response related203J

Nt-hin1 :

Nicotiana tabacum-harpin induced1

References

  • Abramovitch RB, Martin GB (2004) Strategies used by bacterial pathogens to suppress plant defenses. Curr Opin Plant Biol 7:356–364

    Article  PubMed  CAS  Google Scholar 

  • Agrios GN (1997) Plant pathology, 4th edn. Academic, London

    Google Scholar 

  • Alfano JR, Collmer A (1996) Bacterial pathogens in plants: life up against the wall. Plant Cell 8:1683–1698

    Article  PubMed  CAS  Google Scholar 

  • Choi D, Kim HM, Yun HK, Park JA, Kim WT, Bok SH (1996) Molecular cloning of a metallothionein-like gene from Nicotiana glutinosa L. and its induction by wounding and tobacco mosaic virus infection. Plant Physiol 112:353–359

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK Jr, Bent AF (2000) The Arabidopsis dnd1 “defense, no death” gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci USA 97:9323–9328

    Article  PubMed  CAS  Google Scholar 

  • Dangl JL, Dietrich RA, Richberg MH (1996) Death don’t have no mercy: cell death programs in plant–microbe interactions. Plant Cell 8:1793–1807

    Article  PubMed  CAS  Google Scholar 

  • Espinosa A, Alfano JR (2004) Disabling surveillance: bacterial type III secretion system effectors that suppress innate immunity. Cell Microbiol 11:1027–1040

    Article  CAS  Google Scholar 

  • Fink W, Liefland M, Mendgen K (1990) Comparison of various stress responses in oat in compatible and nonhost resistant interactions with rust fungi. Physiol Mol Plant Pathol 37:309–321

    Article  CAS  Google Scholar 

  • Flor HH (1971) The current status of the gene for gene concept. Annu Rev Phytopathol 9:275–276

    Article  Google Scholar 

  • Goodman RN, Novacky AJ (1994) The hypersensitive reaction in plants to pathogens: a resistance phenomenon. American Phytopathological Society, APS press, St. Paul

  • Gopalan S, Wei W, He SY (1996) hrp gene-dependant induction of hin1: a plant gene activated rapidly by both harpins and the avrPto gene mediated signal. Plant J 10:591–600

    Article  PubMed  CAS  Google Scholar 

  • Heath M.C (2000) Nonhost resistance and nonspecific plant defenses. Curr Opin Plant Biol 3:315–319

    Article  PubMed  CAS  Google Scholar 

  • Huang HC, Schuurink R, Denny TP, Atkinson MM, Baker CJ, Yucel I Hutcheson SW, Collmer A (1988) Molecular cloning of a Pseudomonas syringae pv. syringae gene cluster that enables Pseudomonas fluorescens to elicit the hypersensitive response in tobacco plants. J Bacteriol 170:4748–4756

    PubMed  CAS  Google Scholar 

  • Hwang I, Lim SM, Shaw PD (1992) Cloning and characterization of pathogenicity genes from Xanthomonas campestris pv. glycines. J Bacteriol 174:1923–1931

    PubMed  CAS  Google Scholar 

  • Jakobek JL, Lindgren PB (1993) Generalized induction of defense responses in bean is not correlated with the induction of the hypersensitive reaction. Plant Cell 5:49–56

    Article  PubMed  CAS  Google Scholar 

  • Kamoun S (2001) Nonhost resistance to Phytophthora: novel prospects for a classical problem. Curr Opin Plant Biol 4:295–300

    Article  PubMed  CAS  Google Scholar 

  • Kamoun S, van West P, Vleeshouwers VG, de Groot KE, Govers F (1998) Resistance of Nicotiana benthamiana to Phytophthora infestans is mediated by the recognition of the elicitor protein INF1. Plant Cell 10:1413–1426

    Article  PubMed  CAS  Google Scholar 

  • Kang M-K, Park K-S, Choi D (1998) Coordinated expression of defense-related genes by TMV infection or salicylic acid treatment in tobacco. Mol Cells 8:388–392

    PubMed  CAS  Google Scholar 

  • Kang L, Li J, Zhao T, Xiao F, Tang X, Thilmony R, He S, Zhou JM (2003) Interplay of the Arabidopsis nonhost resistance gene NHO1 with bacterial virulence. Proc Natl Acad Sci USA 100:3519–3524

    Article  PubMed  CAS  Google Scholar 

  • Klement Z, Bozso Z, Ott PG, Kecskes ML, Rudolph K (1999) Symptomless resistant response instead of the hypersensitive reaction in tobacco leaves after infiltration of heterologous pathovars of Pseudomonas syringae. J Phytopathol 147:467–475

    Article  CAS  Google Scholar 

  • Lindgren PB, Peet RC, Panopulow NJ (1986) Gene cluster of Pseudomanas syringae pv. phaseolicola controls pathogenicity of bean plants and hypersensitivity on nonhost plant. J Bacteriol 168:512–522

    PubMed  CAS  Google Scholar 

  • Mysore KS, Ryu C-M (2004) Nonhost resistance: how much do we know? Trends Plant Sci 9:97–104

    Article  PubMed  CAS  Google Scholar 

  • Nürnberger T, Brunner F, Kemmerling B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198:249–266

    Article  PubMed  Google Scholar 

  • Nürnberger T, Lipka V (2005) Non-host resistance in plants: new insights into an old phenomenon. Mol Plant Pathol 6:335–345

    Article  Google Scholar 

  • Oh S-K, Cheong J-J, Hwang I, Choi D (1999) Similarities of tobacco mosaic virus-induced hypersensitive cell death and copper-induced abiotic cell death in tobacco. Plant Pathol J 15:8–13

    Google Scholar 

  • Oh S-K, Park JM, Joung YH, Lee S, Chung E, Kim S-Y, Yu SH, Choi D (2005) A plant EPF-type zinc-finger protein, CaPIF1, involves in defense against pathogens. Mol Plant Pathol 6:269–285

    Article  CAS  Google Scholar 

  • Park K-S, Suh MC, Cheong J-J, Choi D (1999) Isolation of defense-related genes from Nicotiana glutinosa infected by tobacco mosaic virus using a modified differential screening. Plant Pathol J 15:295–301

    Google Scholar 

  • Peart JR, Lu R, Sadanandom A, Malcuit I, Moffett P, Brice DC, Schauser L, Jaggard DA, Xiao S, Coleman MJ, Dow M, Jones JD, Shirasu K, Baulcombe DC (2002) Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proc Natl Acad Sci USA 99:10865–10869

    Article  PubMed  CAS  Google Scholar 

  • Peart JR, Mestre P, Lu R, Malcuit I. Baulcombe DC (2005) NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against Tobacco Mosaic Virus. Curr Biol 15:968–973

    Article  PubMed  CAS  Google Scholar 

  • Pedley KF, Martin GB (2003) Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato. Ann Rev Phytopathol 41:215–243

    Article  CAS  Google Scholar 

  • Pontier D, Godiard L, Marco Y, Roby D (1994) hsr203J, a tobacco gene whose activation is rapid, highly localized and specific for incompatible plant pathogen interactions. Plant J 5:507–521

    Article  PubMed  CAS  Google Scholar 

  • Pontier D, Tronchet M, Rogowsky P, Lam E, Roby D (1998) Activation of hsr203, a plant gene expressed during incompatible plant–pathogen interactions, is correlated with programmed cell death. Mol Plant Microbe Interact 11:544–554

    Article  PubMed  CAS  Google Scholar 

  • Rivas S, Thomas CM (2005) Molecular interactions between tomato and the leaf mold pathogen Cladosporium fulvum. Annu Rev Phytopathol 43:395–436

    Article  PubMed  CAS  Google Scholar 

  • Ryu C-M, Anand A, Kang L, Mysore KS (2004) Agrodrench: a novel and effective agroinoculation method for virus-induced gene silencing in roots and diverse Solanaceous species. Plant J 40:322–331

    Article  PubMed  CAS  Google Scholar 

  • Suh MC, Oh S-K, Kim Y-C, Pai H-S, Choi D (2003) Expression of a novel tobacco gene, NgCDM1, is preferentially associated with pathogen-induced cell death. Physiol Mol Plant Pathol 6:227–235

    Article  CAS  Google Scholar 

  • Tang X, Frederick RD, Zhou J, Halterman DA, Jia Y, Martin GB (1996) Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274:2060–2063

    Article  PubMed  CAS  Google Scholar 

  • Tao Y, Xie Z, Chen W, Glazebrook J, Chang H-S, Han B, Zhu T, Zou G, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–330

    Article  PubMed  CAS  Google Scholar 

  • Thordal-Christensen H. (2003) Fresh insights into processes of nonhost resistance. Curr Opin Plant Biol 6:351–357

    Article  PubMed  CAS  Google Scholar 

  • Whitham S, Denesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B. 1994. The product of the tobacco mosaic resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78:1101–1115

    Article  PubMed  CAS  Google Scholar 

  • Yun HK, Yi SY, Kim SU, Son KH, Yu SH, Bok SH, Choi D (1996) Molecular cloning and induction of beta-1,3-glucanase gene from Nicotiana glutinosa L. Mol Cells 6:422–428

    CAS  Google Scholar 

  • Yun HK, Yi SY, Yu S-H, Choi D (1999) Cloning of a pathogenesis-related protein-1 gene from Nicotiana glutinosa L. and its salicylic acid-independent induction by copper and β-amonobutyric acid. J Plant Physiol 154:327–333

    CAS  Google Scholar 

  • Yun BW, Atkinson HA, Gaborit C, Greenland A, Read ND, Pallas JA, Loake GJ (2003) Loss of actin cytoskeletal function and EDS1 activity, in combination, severely compromises nonhost resistance in Arabidopsis against wheat powdery mildew. Plant J 34:768–777

    Article  PubMed  CAS  Google Scholar 

  • Zeidler D, Zähringer 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. Proc Natl Acad Sci USA 101:15811–15816

    Article  PubMed  CAS  Google Scholar 

  • Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Ingyu Hwang (Department of Plant Pathology, Seoul National University) for providing three bacterial strains, and Li Kang and Kiran Mysore for critical reading of our manuscript. This research was supported by grants from the Plant Diversity Research Center (PDRC) and the Crop Functional Genomics Center (CFGC) of the 21st Century Frontier Research Program, funded by Ministry of Science and Technology (MOST).

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Correspondence to Choong-Min Ryu.

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Oh, SK., Lee, S., Chung, E. et al. Insight into Types I and II nonhost resistance using expression patterns of defense-related genes in tobacco. Planta 223, 1101–1107 (2006). https://doi.org/10.1007/s00425-006-0232-1

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