Skip to main content
SpringerLink
Log in

CC-NBS-LRR-Type R Proteins for Rice Blast Commonly Interact with Specific WRKY Transcription Factors

  • Brief Communication
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Rice blast resistance caused by Resistance (R) genes, most of which encode coiled-coil (CC), nucleotide-binding (NB), and leucine-rich-repeat (LRR) domains, is race-specific. Panicle blast 1 (Pb1) is a panicle blast resistance gene that confers a durable non-race-specific blast resistance to rice. Despite being non-R, Pb1 also encodes a CC-NB-LRR protein. Pb1 specifically interacts with rice WRKY45, a transcription factor (TF) in the rice salicylic acid signaling pathway, through its CC domain, and that this interaction is important for the blast resistance conferred by Pb1. Additionally, barley MLA10, an R protein for Blumeria graminis, specifically interacts with HvWRKY1/2. Here, we investigated whether the blast resistance between conferred by R genes and non-R Pb1 genes is mediated by their interaction with WRKY TFs. We performed targeted yeast two-hybrid and glutathione S-transferase (GST)-pull-down assays, which showed that all the five rice R proteins of the CC-NB-LRR type tested, Pi36, Pib, Pita, Pit, and Piz-t, interacted with WRKY45 and WRKY66 through their CC domains. However, elicitor-triggered immunity due to these R genes was not affected by the knockdown of these WRKY genes. The results suggest that R proteins can potentially transduce defense signals by interacting with WRKY TFs but the potentials are masked by HR-mediated elicitor-triggered immunity responses.

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

References

  • Akagi A, Fukushima S, Okada K, Jiang CJ, Yoshida R, Nakayama A, Shimono M, Sugano S, Yamane H, Takatsuji H (2014) WRKY45-dependent priming of diterpenoid phytoalexin biosynthesis in rice and the role of cytokinin in triggering the reaction. Plant Mol Biol 86(1-2):171–183. doi:10.1007/s11103-014-0221-x

    Article  CAS  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(5):199–206

    Article  CAS  PubMed  Google Scholar 

  • Hayashi N, Inoue H, Kato T, Funao T, Shirota M, Shimizu T, Kanamori H, Yamane H, Hayano-Saito Y, Matsumoto T, Yano M, Takatsuji H (2010) Durable panicle blast-resistance gene Pb1 encodes an atypical CC-NBS-LRR protein and was generated by acquiring a promoter through local genome duplication. Plant J 64(3):498–510. doi:10.1111/j.1365-313X.2010.04348.x

    Article  CAS  PubMed  Google Scholar 

  • Horisue M (1986) Development of near-isogenic lines of cultivar Nipponbare, Kanto IL1 to 14, harboring different blast resistance genes. Newslett Natl Agricul Res Center 2:30–36

    Google Scholar 

  • Inoue H, Hayashi N, Matsushita A, Liu X, Nakayama A, Sugano S, Jiang CJ, Takatsuji H (2013) Blast resistance of CC-NB-LRR protein Pb1 is mediated by WRKY45 through protein-protein interaction. Proc Natl Acad Sci U S A 110(23):9577–9582. doi:10.1073/pnas.1222155110

    Article  CAS  PubMed  PubMed Central  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(6):791–798. doi:10.1094/MPMI-23-6-0791

    Article  CAS  PubMed  Google Scholar 

  • Matsushita A, Inoue H, Goto S, Nakayama A, Sugano S, Hayashi N, Takatsuji H (2012) The nuclear ubiquitin proteasome degradation affects WRKY45 function in the rice defense program. Plant J:(in press)

  • Miki D, Shimamoto K (2004) Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol 45(4):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(4):1903–1913

    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(1):150. doi:10.1186/1471-2229-13-150

    Article  PubMed  PubMed Central  Google Scholar 

  • Nozawa A, Nanamiya H, Miyata T, Linka N, Endo Y, Weber AP, Tozawa Y (2007) A cell-free translation and proteoliposome reconstitution system for functional analysis of plant solute transporters. Plant Cell Physiol 48(12):1815–1820. doi:10.1093/pcp/pcm150

    Article  CAS  PubMed  Google Scholar 

  • Okuyama Y, Kanzaki H, Abe A, Yoshida K, Tamiru M, Saitoh H, Fujibe T, Matsumura H, Shenton M, Galam DC, Undan J, Ito A, Sone T, Terauchi R (2011) A multifaceted genomics approach allows the isolation of the rice Pia-blast resistance gene consisting of two adjacent NBS-LRR protein genes. Plant J 66(3):467–479. doi:10.1111/j.1365-313X.2011.04502.x

  • Park CJ, Ronald PC (2012) Cleavage and nuclear localization of the rice XA21 immune receptor. Nature Commun 3:920. doi:10.1038/ncomms1932

    Article  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(3):446–458. doi:10.1093/mp/ssn024

    Article  CAS  PubMed  Google Scholar 

  • Rairdan GJ, Collier SM, Sacco MA, Baldwin TT, Boettrich T, Moffett P (2008) The coiled-coil and nucleotide binding domains of the potato Rx disease resistance protein function in pathogen recognition and signaling. Plant Cell 20(3):739–751. doi:10.1105/tpc.107.056036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S, Keller B, Seki H, Ulker B, Somssich IE, Schulze-Lefert P (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315(5815):1098–1103

    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(6):2064–2076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimono M, Koga H, Akagi AYA, Hayashi N, Goto S, Sawada M, Kurihara T, Matsushita A, Sugano S, Jiang C-J, Kaku H, Inoue H, Takatsuji H (2012) Rice WRKY45 plays important roles in fungal and bacterial disease resistance. Mol Plant Pathol 13(1):83–94. doi:10.1111/j.1364-3703.2011.00732.x

    Article  CAS  PubMed  Google Scholar 

  • Takatsuji H (2014) Development of disease-resistant rice using regulatory components of induced disease resistance. Front Plant Sci 5. doi:10.3389/fpls.2014.00630

  • Takatsuji H, Jiang C-J, Sugano S (2010) Salicylic acid signaling pathway in rice and the potential applications of its regulators. JARQ 44(3):217–223

    Article  CAS  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 

  • Yuan B, Zhai C, Wang W, Zeng X, Xu X, Hu H, Lin F, Wang L, Pan Q (2011) The Pik-p resistance to Magnaporthe oryzae in rice is mediated by a pair of closely linked CC-NBS-LRR genes. Theor Appl Genet 122(5):1017–1028. doi:10.1007/s00122-010-1506-3

  • 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(1):176–189. doi:10.1104/pp. 104.054312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhai C, Lin F, Dong Z, He X, Yuan B, Zeng X, Wang L, Pan Q (2011) The isolation and characterization of Pik, a rice blast resistance gene which emerged after rice domestication. New Phytol 189(1):321–334. doi:10.1111/j.1469-8137.2010.03462.x

Download references

Acknowledgments

The work was supported by Grant-in-Aid for JSPS Fellows (21-09617), the grants from the Japanese Ministry of Agriculture, Forestry and Fisheries (Genomics for Agricultural Innovation, GMA0001 and PMI0008), and the National Natural Science Foundation of China (31370306).

Conflict of Interest

The authors declare that they have no competing interests.

Author information

Authors and Affiliations

  1. Disease Resistant Crops Research Unit, National Institute of Agrobiological Sciences, Kannondai 2-1-2, Tsukuba, 305-8602, Japan

    Xinqiong Liu, Haruhiko Inoue, Nagao Hayashi, Chang-Jie Jiang & Hiroshi Takatsuji

  2. Hubei Provincial Key Laboratory for Protection and Application of Special Plants in Wuling Area of China, College of Life Science, South-Central University for Nationalities, Wuhan, 430074, China

    Xinqiong Liu

Authors
  1. Xinqiong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Haruhiko Inoue
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nagao Hayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chang-Jie Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. 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

Below is the link to the electronic supplementary material.

Supplemental table 1

Primers for qRT-PCR. (DOC 27 kb)

Supplemental figure 1

Quantitative yeast two-hybrid assay between the R proteins and WRKY45. (PPT 119 kb)

Supplemental figure 2

Sequence alignment of the N-terminal domains of the WRKY proteins. (PPT 314 kb)

Supplemental figure 3

Sequence alignment of the CC domains in Pb1 and the R proteins. (PPT 88 kb)

Supplemental figure 4

Effects of WRKY45 knockdown on BTH-induced WRKY45 transcript levels. (PPT 195 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, X., Inoue, H., Hayashi, N. et al. CC-NBS-LRR-Type R Proteins for Rice Blast Commonly Interact with Specific WRKY Transcription Factors. Plant Mol Biol Rep 34, 533–537 (2016). https://doi.org/10.1007/s11105-015-0932-4

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-015-0932-4

Keywords

Search

Navigation