Skip to main content
SpringerLink
Log in

Role of OsNPR1 in rice defense program as revealed by genome-wide expression analysis

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

NPR1 is a central regulator of salicylic-acid (SA)-mediated defense signaling in Arabidopsis. Here, we report the characterization of OsNPR1, an Oryzae sativa (rice) ortholog of NPR1, focusing on its role in blast disease resistance and identification of OsNPR1-regulated genes. Blast resistance tests using OsNPR1 knockdown and overexpressing rice lines demonstrated the essential role of OsNPR1 in benzothiadiazole (BTH)-induced blast resistance. Genome-wide transcript profiling using OsNPR1-knockdown lines revealed that 358 genes out of 1,228 BTH-upregulated genes and 724 genes out of 1,069 BTH-downregulated genes were OsNPR1-dependent with respect to BTH responsiveness, thereby indicating that OsNPR1 plays a more vital role in gene downregulation. The OsNPR1-dependently downregulated genes included many of those involved in photosynthesis and in chloroplast translation and transcription. Reduction of photosynthetic activity after BTH treatment and its negation by OsNPR1 knockdown were indeed reflected in the changes in Fv/Fm values in leaves. These results imply the role of OsNPR1 in the reallocation of energy and resources during defense responses. We also examined the OsNPR1-dependence of SA-mediated suppression of ABA-induced genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Statistical Soc B57:289–300

    Google Scholar 

  • Blanco F, Salinas P, Cecchini N, Jordana X, Van Hummelen P, Alvarez M, Holuigue L (2009) Early genomic responses to salicylic acid in Arabidopsis. Plant Mol Biol 70:79–102

    Article  CAS  PubMed  Google Scholar 

  • Cao H, Bowling SA, Gordon AS, Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583–1592

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Chern M, Fitzgerald HA, Canlas PE, Navarre DA, Ronald PC (2005) Overexpression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light. Mol Plant-Microbe Interact 18:511–520

    Article  CAS  PubMed  Google Scholar 

  • Conrath U, Pieterse CM, Mauch-Mani B (2002) Priming in plant-pathogen interactions. Trends Plant Sci 7:210–216

    Article  CAS  PubMed  Google Scholar 

  • Delaney TP, Friedrich L, Ryals JA (1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci USA 92:6602–6606

    Article  CAS  PubMed  Google Scholar 

  • Despres C, Chubak C, Rochon A, Clark R, Bethune T, Desveaux D, Fobert PR (2003) The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell 15:2181–2191

    Article  CAS  PubMed  Google Scholar 

  • Fan W, Dong X (2002) In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis. Plant Cell 14:1377–1389

    Article  CAS  PubMed  Google Scholar 

  • 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. Mol Plant-Microbe Interact 17:140–151

    Article  CAS  PubMed  Google Scholar 

  • Gene-Ontology-Consortium (2006) The Gene Ontology (GO) project in 2006. Nucleic Acids Res 34:D322–D326

    Article  Google Scholar 

  • Gorlach J, Volrath S, Knauf-Beiter G, Hengy G, Beckhove U, Kogel KH, Oostendorp M, Staub T, Ward E, Kessmann H, Ryals J (1996) Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8:629–643

    Article  CAS  PubMed  Google Scholar 

  • Harris MA, Clark J, Ireland A, Lomax J, Ashburner M, Foulger R, Eilbeck K, Lewis S, Marshall B, Mungall C, Richter J, Rubin GM, Blake JA, Bult C, Dolan M, Drabkin H, Eppig JT, Hill DP, Ni L, Ringwald M, Balakrishnan R, Cherry JM, Christie KR, Costanzo MC, Dwight SS, Engel S, Fisk DG, Hirschman JE, Hong EL, Nash RS, Sethuraman A, Theesfeld CL, Botstein D, Dolinski K, Feierbach B, Berardini T, Mundodi S, Rhee SY, Apweiler R, Barrell D, Camon E, Dimmer E, Lee V, Chisholm R, Gaudet P, Kibbe W, Kishore R, Schwarz EM, Sternberg P, Gwinn M, Hannick L, Wortman J, Berriman M, Wood V, De la Cruz N, Tonellato P, Jaiswal P, Seigfried T, White R (2004) The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 32:D258–D261

    Article  CAS  PubMed  Google Scholar 

  • Heidel AJ, Dong X (2006) Fitness benefits of systemic acquired resistance during Hyaloperonospora parasitica infection in Arabidopsis thaliana. Genetics 173:1621–1628

    Article  CAS  PubMed  Google Scholar 

  • Heidel AJ, Clarke JD, Antonovics J, Dong X (2004) Fitness costs of mutations affecting the systemic acquired resistance pathway in Arabidopsis thaliana. Genetics 168:2197–2206

    Article  CAS  PubMed  Google Scholar 

  • Ishizaki Y, Tsunoyama Y, Hatano K, Ando K, Kato K, Shinmyo A, Kobori M, Takeba G, Nakahira Y, Shiina T (2005) A nuclear-encoded sigma factor, Arabidopsis SIG6, recognizes sigma-70 type chloroplast promoters and regulates early chloroplast development in cotyledons. Plant J 42:133–144

    Article  CAS  PubMed  Google Scholar 

  • Jiang CJ, Shimono M, Sugano S, Kojima M, Yazawa K, Yoshida R, Inoue H, Hayashi N, Sakakibara H, Takatsuji H (2010) Abscisic acid interacts antagonistically with salicylic acid signaling pathway in rice-Magnaporthe grisea interaction. Mol Plant-Microbe Interact 23:791–798

    Article  CAS  PubMed  Google Scholar 

  • Johnson C, Boden E, Arias J (2003) Salicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis. Plant Cell 15:1846–1858

    Article  CAS  PubMed  Google Scholar 

  • Kanamaru K, Nagashima A, Fujiwara M, Shimada H, Shirano Y, Nakabayashi K, Shibata D, Tanaka K, Takahashi H (2001) An Arabidopsis sigma factor (SIG2)-dependent expression of plastid-encoded tRNAs in chloroplasts. Plant Cell Physiol 42:1034–1043

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32:D277–D280

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484

    Article  CAS  PubMed  Google Scholar 

  • Kasai K, Kawagishi-Kobayashi M, Teraishi M, Ito Y, Ochi K, Wakasa K, Tozawa Y (2004) Differential expression of three plastidial sigma factors, OsSIG1, OsSIG2A, and OsSIG2B, during leaf development in rice. Biosci Biotechnol Biochem 68:973–977

    Article  CAS  PubMed  Google Scholar 

  • Kinkema M, Fan W, Dong X (2000) Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12:2339–2350

    Article  CAS  PubMed  Google Scholar 

  • Lawton KA, Friedrich L, Hunt M, Weymann K, Delaney T, Kessmann H, Staub T, Ryals J (1996) Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J 10:71–82

    Article  CAS  PubMed  Google Scholar 

  • Lerdau M (1992) Future discounts and resource-allocation in plants. Funct Ecology 6:371–375

    Article  Google Scholar 

  • Miki D, Shimamoto K (2004) Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol 45:490–495

    Article  CAS  PubMed  Google Scholar 

  • Miki D, Itoh R, Shimamoto K (2005) RNA silencing of single and multiple members in a gene family of rice. Plant Physiol 138:1903–1913

    Article  CAS  PubMed  Google Scholar 

  • Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944

    Article  CAS  PubMed  Google Scholar 

  • Nettleton D (2006) A discussion of statistical methods for design and analysis of microarray experiments for plant scientists. Plant Cell 18:2112–2121

    Article  CAS  PubMed  Google Scholar 

  • Qi M, Yang Y (2002) Quantification of Magnaporthe grisea during infection of rice plants using real-time polymerase chain reaction and northern blot/phosphoimaging analyses. Phytopathology 92:870–876

    Article  CAS  PubMed  Google Scholar 

  • Quilis J, Penas G, Messeguer J, Brugidou C, San Segundo B (2008) The Arabidopsis AtNPR1 inversely modulates defense responses against fungal, bacterial, or viral pathogens while conferring hypersensitivity to abiotic stresses in transgenic rice. Mol Plant-Microbe Interact 21:1215–1231

    Article  CAS  PubMed  Google Scholar 

  • Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809–1819

    Article  CAS  PubMed  Google Scholar 

  • Schloles J (1992) Photosynthesis: cellular and tissue aspects in diseased leaves. In: Ayres P (ed) Pests and pathogens. Bios Scientific Publishers, Oxford, pp 85–106

    Google Scholar 

  • Shah J, Tsui F, Klessig DF (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. Mol Plant-Microbe Interact 10:69–78

    Article  CAS  PubMed  Google Scholar 

  • Shimizu T, Satoh K, Kikuchi S, Omura T (2007) The repression of cell wall- and plastid-related genes and the induction of defense-related genes in rice plants infected with Rice dwarf virus. Mol Plant-Microbe Interact 20:247–254

    Article  CAS  PubMed  Google Scholar 

  • Shimono M, Sugano S, Nakayama A, Jiang CJ, Ono K, Toki S, Takatsuji H (2007) Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19:2064–2076

    Article  CAS  PubMed  Google Scholar 

  • Shobbar ZS, Oane R, Gamuyao R, De Palma J, Malboobi MA, Karimzadeh G, Javaran MJ, Bennett J (2008) Abscisic acid regulates gene expression in cortical fiber cells and silica cells of rice shoots. New Phytol 178:68–79

    Article  CAS  PubMed  Google Scholar 

  • Silverman P, Seskar M, Kanter D, Schweizer P, Metraux JP, Raskin I (1995) Salicylic acid in rice: biosynthesis, conjugation, and possible role. Plant Physiol 108:633–639

    CAS  PubMed  Google Scholar 

  • Somssich IE, Hahlbrock K (1998) Pathogen defence in plants—a paradigm of biological complexity. Trends Plant Sci 3:86–90

    Article  Google Scholar 

  • Spoel SH, Mou Z, Tada Y, Spivey NW, Genschik P, Dong X (2009) Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137:860–872

    Article  CAS  PubMed  Google Scholar 

  • Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H (2006) Early infection of scutellum tissue with Agrobacterium allows high speed transformation of rice. Plant J 47:969–976

    Article  CAS  PubMed  Google Scholar 

  • van Hulten M, Pelser M, van Loon LC, Pieterse CM, Ton J (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci USA 103:5602–5607

    Article  PubMed  Google Scholar 

  • Wang D, Amornsiripanitch N, Dong X (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog 2:e123

    Article  PubMed  Google Scholar 

  • Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol 17:1784–1790

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Qi M, Mei C (2004) Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J 40:909–919

    Article  CAS  PubMed  Google Scholar 

  • Yasuda M, Ishikawa A, Jikumaru Y, Seki M, Umezawa T, Asami T, Maruyama-Nakashita A, Kudo T, Shinozaki K, Yoshida S, Nakashita H (2008) Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell 20:1678–1692

    Article  CAS  PubMed  Google Scholar 

  • Yuan Y, Zhong S, Li Q, Zhu Z, Lou Y, Wang L, Wang J, Wang M, Li Q, Yang D, He Z (2007) Functional analysis of rice NPR1-like genes reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotechnol J 5:313–324

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Fan W, Kinkema M, Li X, Dong X (1999) Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc Natl Acad Sci USA 96:6523–6528

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Ministry of Agriculture, Forestry, and Fisheries of Japan (Green Technology Project, IP-4006, and Genomics for Agricultural Innovation, PMI-0008). We are grateful for the excellent technical support provided by Ms. M. Ishikawa and Ms. T. Yasuhara. We thank Prof. K. Shimamoto for providing the RNAi vector pANDA; Dr. S. Toki and Ms. K. Ono, for technical advice; and Mr. T. Numa, for advice on microarray data analysis. We also thank the Rice Genome Resource Center at NIAS for the use of the rice microarray analysis system, as well as Dr. Y. Nagamura and Ms. R. Motoyama for their technical support.

Author information

Author notes

  1. Masaki Shimono

    Present address: Department of Plant Pathology, Michigan State University, 107 Center for Integrated Plant Systems, East Lansing, MI, 48824-1311, USA

  2. Akira Nakayama

    Present address: Maebashi Institute of Technology, Maebashi, Gunma, 371-0816, Japan

Authors and Affiliations

  1. Plant Disease Resistance Research Unit, Division of Plant Sciences, National Institute of Agrobiological Sciences, 2-1-2 Kannondai, Tsukuba, Ibaraki, 305-8602, Japan

    Shoji Sugano, Chang-Jie Jiang, Katsumi Yazawa, Nagao Hayashi, Masaki Shimono, Akira Nakayama & Hiroshi Takatsuji

  2. Photobiology and Photosynthesis Research Unit, Division of Plant Sciences, National Institute of Agrobiological Sciences, Kannondai 2-1-2, Tsukuba, Ibaraki, 305-8602, Japan

    Shin-Ichi Miyazawa, Chisato Masumoto & Mitsue Miyao

Authors
  1. Shoji Sugano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chang-Jie Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shin-Ichi Miyazawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chisato Masumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Katsumi Yazawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nagao Hayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Masaki Shimono
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Akira Nakayama
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Mitsue Miyao
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hiroshi Takatsuji
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroshi Takatsuji.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sugano, S., Jiang, CJ., Miyazawa, SI. et al. Role of OsNPR1 in rice defense program as revealed by genome-wide expression analysis. Plant Mol Biol 74, 549–562 (2010). https://doi.org/10.1007/s11103-010-9695-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-010-9695-3

Keywords

Search

Navigation