Skip to main content
SpringerLink
Log in

OsWRKY24, a blast-disease responsive transcription factor, positively regulates rice disease resistance

  • Host Responses
  • Published:
Journal of General Plant Pathology Aims and scope Submit manuscript

Abstract

WRKYs are plant-specific transcription factors that play important roles in disease response. Here, we showed that a WRKY gene in rice, OsWRKY24, was upregulated in response to inoculation with rice blast fungus Pyricularia oryzae. Its expression was also induced by wounding. Green fluorescent protein-fused OsWRKY24 localized to nuclei in rice epidermal cells, and OsWRKY24 had transactivation activity in yeast cells. In addition, functional repression of OsWRKY24 through a chimeric repressor (OsWRKY24-SRDX) greatly increased susceptibility to P. oryzae. These results indicate that OsWRKY24 is a transcriptional activator that positively regulates disease resistance in rice.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Bagnaresi P, Biselli C, Orrù L, Urso S, Crispino L, Abbruscato P, Piffanelli P, Lupotto E, Cattivelli L, Valè G (2012) Comparative transcriptome profiling of the early response to Magnaporthe oryzae in durable resistant vs susceptible rice (Oryza sativa L.) genotypes. PLoS One 7:e51609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406

    Article  CAS  PubMed  Google Scholar 

  • Cheng H, Liu H, Deng Y, Xiao J, Li X, Wang S (2015) The WRKY45-2 WRKY13 WRKY42 transcriptional regulatory cascade is required for rice resistance to fungal pathogen. Plant Physiol 167:1087–1099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chujo T, Takai R, Akimoto-Tomiyama C, Ando S, Minami E, Nagamura Y, Kaku H, Shibuya N, Yasuda M, Nakashita H, Umemura K, Okada A, Okada K, Nojiri H, Yamane H (2007) Involvement of the elicitor-induced gene OsWRKY53 in the expression of defense-related genes in rice. Biochim Biophys Acta 1769:497–505

    Article  CAS  PubMed  Google Scholar 

  • Chujo T, Miyamoto K, Shimogawa T, Shimizu T, Otake Y, Yokotani N, Nishizawa Y, Shibuya N, Nojiri H, Yamane H, Minami E, Okada K (2013) OsWRKY28, a PAMP-responsive transrepressor, negatively regulates innate immune responses in rice against rice blast fungus. Plant Mol Biol 82:23–37

    Article  CAS  PubMed  Google Scholar 

  • Chujo T, Miyamoto K, Ogawa S, Masuda Y, Shimizu T, Kishi-Kaboshi M, Takahashi A, Nishizawa Y, Minami E, Nojiri H, Yamane H, Okada K (2014) Overexpression of phosphomimic mutated OsWRKY53 leads to enhanced blast resistance in rice. PLoS One 9:e98737

    Article  PubMed  PubMed Central  Google Scholar 

  • Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206

    Article  CAS  PubMed  Google Scholar 

  • Fukushima S, Mori M, Sugano S, Takatsuji H (2016) Transcription factor WRKY62 plays a role in pathogen defense and hypoxia-responsive gene expression in rice. Plant Cell Physiol 57:2541–2551

    Article  CAS  PubMed  Google Scholar 

  • Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34:733–739

    Article  CAS  PubMed  Google Scholar 

  • Hood EE, Gelvin SB, Melchers LS, Hoekema A (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res 2:208–218

    Article  CAS  Google Scholar 

  • Ishihama N, Yoshioka H (2012) Post-translational regulation of WRKY transcription factors in plant immunity. Curr Opin Plant Biol 15:431–437

    Article  CAS  PubMed  Google Scholar 

  • Jach G, Binot E, Frings S, Luxa K, Schell J (2001) Use of red fluorescent protein from Discosoma sp. (dsRED) as a reporter for plant gene expression. Plant J 28:483–491

    Article  CAS  PubMed  Google Scholar 

  • Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 345:646–651

    Article  CAS  PubMed  Google Scholar 

  • Kim SH, Oikawa T, Kyozuka J, Wong HL, Umemura K, Kishi-Kaboshi M, Takahashi A, Kawano Y, Kawasaki T, Shimamoto K (2012) The bHLH Rac Immunity1 (RAI1) is activated by OsRac1 via OsMAPK3 and OsMAPK6 in rice immunity. Plant Cell Physiol 53:740–754

    Article  CAS  PubMed  Google Scholar 

  • Lan A, Huang J, Zhao W, Peng Y, Chen Z, Kang D (2013) A salicylic acid-induced rice (Oryza sativa L.) transcription factor OsWRKY77 is involved in disease resistance of Arabidopsis thaliana. Plant Biol 15:452–461

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Chen F, Sun L, Zhang Z, Yang Y, He Z (2006) Expression profiling of rice genes in early defense responses to blast and bacterial blight pathogens using cDNA microarray. Physiol Mol Plant Pathol 68:51–60

    Article  CAS  Google Scholar 

  • Liu X, Bai X, Wang X, Chu C (2007) OsWRKY71, a rice transcription factor, is involved in rice defense response. J Plant Physiol 164:969–979

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Chen X, Liu J, Ye J, Guo Z (2012) The rice ERF transcription factor OsERF922 negatively regulates resistance to Magnaporthe oryzae and salt tolerance. J Exp Bot 63:3899–3911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Chen X, Liang X, Zhou X, Yang F, Liu J, He SY, Guo Z (2016) Alternative splicing of rice WRKY62 and WRKY76 transcription factor genes in pathogen defense. Plant Physiol 171:1427–1442

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mao G, Meng X, Liu Y, Zheng Z, Chen Z, Zhang S (2011) Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23:1639–1653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mosquera G, Giraldo MC, Khang CH, Coughlan S, Valent B (2009) Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1-4 as biotrophy-associated secreted proteins in rice blast disease. Plant Cell 21:1273–1290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakayama A, Fukushima S, Goto S, Matsushita A, Shimono M, Sugano S, Jiang CJ, Akagi A, Yamazaki M, Inoue H, Takatsuji H (2013) Genome-wide identification of WRKY45-regulated genes that mediate benzothiadiazole-induced defense responses in rice. BMC Plant Biol 13:150

    Article  PubMed  PubMed Central  Google Scholar 

  • Nishizawa Y, Mochizuki S, Yokotani N, Nishmura T, Minami E (2016) Molecular and cellular analysis of the biotrophic interaction between rice and Magnaporthe oryzae—exploring situations in which the blast fungus controls the infection. Physiol Mol Plant Pathol 95:70–76

    Article  CAS  Google Scholar 

  • Niwa Y, Hirano T, Yoshimoto K, Shimizu M, Kobayashi H (1999) Non-invasive quantitative detection and applications of non-toxic, S65T-type green fluorescent protein in living plants. Plant J 18:455–463

    Article  CAS  PubMed  Google Scholar 

  • Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng Y, Bartley LE, Chen X, Dardick C, Chern M, Ruan R, Canlas PE, Ronald PC (2008) OsWRKY62 is a negative regulator of basal and Xa21-mediated defense against Xanthomonas oryzae pv. oryzae in rice. Mol Plant 1:446–458

    Article  CAS  PubMed  Google Scholar 

  • Peng X, Hu Y, Tang X, Zhou P, Deng X, Wang H, Guo Z (2012) Constitutive expression of rice WRKY30 gene increases the endogenous jasmonic acid accumulation, PR gene expression and resistance to fungal pathogens in rice. Planta 236:1485–1498

    Article  CAS  PubMed  Google Scholar 

  • Ross CA, Liu Y, Shen QJ (2007) The WRKY gene family in rice (Oryza sativa). J Integr Plant Biol 49:827–842

    Article  CAS  Google Scholar 

  • Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258

    Article  CAS  PubMed  Google Scholar 

  • Ryu HS, Han M, Lee SK, Cho JI, Ryoo N, Heu S, Lee YH, Bhoo SH, Wang GL, Hahn TR, Jeon JS (2006) A comprehensive expression analysis of the WRKY gene superfamily in rice plants during defense response. Plant Cell Rep 25:836–847

    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  PubMed Central  Google Scholar 

  • Sun L, Zhang H, Li D, Huang L, Hong Y, Ding XS, Nelson RS, Zhou X, Song F (2013) Functions of rice NAC transcriptional factors, ONAC122 and ONAC131, in defense responses against Magnaporthe grisea. Plant Mol Biol 81:41–56

    Article  CAS  PubMed  Google Scholar 

  • Talbot NJ (2003) On the trail of a cereal killer: exploring the biology of Magnaporthe grisea. Annu Rev Microbiol 57:177–202

    Article  CAS  PubMed  Google Scholar 

  • Tanabe S, Yokotani N, Nagata T, Fujisawa Y, Jiang CJ, Abe K, Ichikawa H, Mitsuda N, Ohme-Takagi M, Nishizawa Y, Minami E (2014) Spatial regulation of defense-related genes revealed by expression analysis using dissected tissues of rice leaves inoculated with Magnaporthe oryzae. J Plant Physiol Pathol 2:1000135

    Article  Google Scholar 

  • Tanaka W, Toriba T, Ohmori Y, Yoshida A, Kawai A, Mayama-Tsuchida T, Ichikawa H, Mitsuda N, Ohme-Takagi M, Hirano HY (2012) The YABBY gene TONGARI-BOUSHI1 is involved in lateral organ development and maintenance of meristem organization in the rice spikelet. Plant Cell 24:80–95

    Article  CAS  PubMed  PubMed Central  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 

  • Wang H, Meng J, Peng X, Tang X, Zhou P, Xiang J, Deng X (2015) Rice WRKY4 acts as a transcriptional activator mediating defense responses toward Rhizoctonia solani, the causing agent of rice sheath blight. Plant Mol Biol 89:157–171

    Article  CAS  PubMed  Google Scholar 

  • Wei T, Ou B, Li J, Zhao Y, Guo D, Zhu Y, Chen Z, Gu H, Li C, Qin G, Qu LJ (2013) Transcriptional profiling of rice early response to Magnaporthe oryzae identified OsWRKYs as important regulators in rice blast resistance. PLoS One 8:e59720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao J, Cheng H, Li X, Xiao J, Xu C, Wang S (2013) Rice WRKY13 regulates cross talk between abiotic and biotic stress signaling pathways by selective binding to different cis-elements. Plant Physiol 163:1868–1882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie Z, Zhang ZL, Zou X, Huang J, Ruas P, Thompson D, Shen QJ (2005) Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells. Plant Physiol 137:176–189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokotani N, Sato Y, Tanabe S, Chujo T, Shimizu T, Okada K, Yamane H, Shimono M, Sugano S, Takatsuji H, Kaku H, Minami E, Nishizawa Y (2013) WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. J Exp Bot 64:5085–5097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokotani N, Tsuchida-Mayama T, Ichikawa H, Mitsuda N, Ohme-Takagi M, Kaku H, Minami E, Nishizawa Y (2014) OsNAC111, a blast disease-responsive transcription factor in rice, positively regulates the expression of defense-related genes. Mol Plant Microbe Interact 27:1027–1034

    Article  PubMed  Google Scholar 

  • Zhang J, Peng Y, Guo Z (2008) Constitutive expression of pathogen-inducible OsWRKY31 enhances disease resistance and affects root growth and auxin response in transgenic rice plants. Cell Res 18:508–521

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZL, Shin M, Zou X, Huang J, Ho TH, Shen QJ (2009) A negative regulator encoded by a rice WRKY gene represses both abscisic acid and gibberellins signaling in aleurone cells. Plant Mol Biol 70:139–151

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank former Prof. H. Naitoh (Akita Prefectural University, Japan) for providing P. oryzae isolate P91-15B. We also thank Dr. N. Ishii-Minami, Ms. E. Nakajima, Ms. M. Kouzai, and Mr. K. Nakajima for daily technical assistance and Dr. T. Tsuchida-Mayama, Dr. K. Abe, Ms. K. Iida-Okada, and Mr. A. Horikawa of NIAS, and Mr. T. Ishizuka and Ms. Y. Takiguchi of AIST and Mr. K. Sato of GreenSogna Inc. for generating SRDX rice lines. Japanese isolate Ina86-137 of P. oryzae (MAFF 101511) was supplied by NARO Genebank in Tsukuba, Japan. This research was supported by a grant to YN from the Japan Society for the Promotion of Science initiated by the Council for Science and Technology Policy (GS028) and also in part by grants from the Ministry of Agriculture, Forestry and Fisheries (Genomics for Agricultural Innovation, AMR0001 to HI and AMR0004 to MO-T and NM).

Author information

Author notes

  1. Naoki Yokotani

    Present address: Department of Technology Development Plant DNA Analysis Group, Kazusa DNA Research Institute, 2-6-7 Kazusa-Kamatari, Kisarazu, Chiba, 292-0818, Japan

Authors and Affiliations

  1. Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, 2-1-2 Kannondai, Tsukuba, Ibaraki, 305-8602, Japan

    Naoki Yokotani, Masahito Shikata, Hiroaki Ichikawa, Eiichi Minami & Yoko Nishizawa

  2. Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Higashi 1-1-1, Tsukuba, Ibaraki, 305-8562, Japan

    Nobutaka Mitsuda & Masaru Ohme-Takagi

  3. Institute for Environmental Research and Technology (IEST), Saitama University, Saitama, 338-8570, Japan

    Masaru Ohme-Takagi

Authors
  1. Naoki Yokotani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masahito Shikata
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hiroaki Ichikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nobutaka Mitsuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Masaru Ohme-Takagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eiichi Minami
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yoko Nishizawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yoko Nishizawa.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yokotani, N., Shikata, M., Ichikawa, H. et al. OsWRKY24, a blast-disease responsive transcription factor, positively regulates rice disease resistance. J Gen Plant Pathol 84, 85–91 (2018). https://doi.org/10.1007/s10327-018-0768-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10327-018-0768-5

Keywords

Search

Navigation