Skip to main content
Log in

Comprehensive analysis of VQ motif-containing gene expression in rice defense responses to three pathogens

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Expression levels of rice VQ motif-containing genes in response to pathogen infection vary among pathogens, and some of the genes are co-expressed with defense-response WRKY genes.

Abstract

Recent studies have revealed that some VQ (FxxxVQxLTG) motif-containing proteins in plants partner with WRKY transcription factors to participate in their functions. Accumulating information suggests that WRKY proteins play important roles in the response of rice plants to pathogen infection. However, the functions of rice VQ motif-containing proteins are unknown. To explore whether VQ motif-containing proteins are involved in defense against pathogens in rice, we performed a comprehensive expression analysis of the genes for these proteins. The rice VQ motif-containing family consists of 40 genes, all of which encode proteins harboring a 21-amino acid VQ-containing motif, which in turn contains the known VQ motif. On the basis of their phylogenetic relationships and tissue-specific and developmental stage-specific expression characteristics, we transcriptionally analyzed 13 representative genes in rice responses to three pathogens: Xanthomonas oryzae pv. oryzae, which causes bacterial blight disease; X. oryzae pv. oryzicola, which causes bacterial streak disease; and Magnaporthe oryzae, which causes fungal blast disease. The expression of some of the genes changed markedly in response to infection by at least one of the pathogen species, and some of the genes also showed markedly different expression in resistant and susceptible reactions. In addition, some defense-responsive VQ motif-containing genes were co-expressed with defense-response WRKY genes. These results provide a new perspective on the putative roles of rice VQ motif-containing proteins and their putative WRKY partners in rice–pathogen interactions.

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

Access this article

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
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

ETI:

Effector-triggered immunity

LRR:

Leucine-rich repeat

M. oryzae :

Magnaporthe oryzae

MR :

Major disease resistance

NB-ARC:

Nucleotide-binding adaptor shared by APAF-1, R proteins, and CED-4

PRR:

Pattern recognition receptor

PTI:

Pattern-triggered immunity

R:

Resistance

Xoc :

Xanthomonas oryzae pv. oryzicola

Xoo :

Xanthomonas oryzae pv. oryzae

VQC:

VQ-containing

References

  • Agarwal P, Reddy MP, Chikara J (2011) WRKY: its structure, evolutionary relationship, DNA-binding selectivity, role in stress tolerance and development of plants. Mol Biol Rep 38:3883–3896

    Article  CAS  PubMed  Google Scholar 

  • Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NH, Zhu S, Qiu JL, Micheelsen P, Rocher A, Petersen M, Newman MA, Bjorn Nielsen H, Hirt H, Somssich I, Mattsson O, Mundy J (2005) The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J 24:2579–2589

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–W373

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen C, Chen Z (2002) Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogen-induced Arabidopsis transcription factor. Plant Physiol 129:706–716

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen H, Wang S, Zhang Q (2002) New gene for bacterial blight resistance in rice located on chromosome 12 identified from Minghui 63, an elite restorer line. Phytopathology 92:750–754

    CAS  PubMed  Google Scholar 

  • Chen H, Wang S, Xing Y, Xu C, Hayes PM, Zhang Q (2003) Comparative analyses of genomic locations and race specificities of loci for quantitative resistance to Pyricularia grisea in rice and barley. Proc Natl Acad Sci USA 100:2544–2549

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cheng Y, Zhou Y, Yang Y, Chi YJ, Zhou J, Chen JY, Wang F, Fan B, Shi K, Zhou YH, Yu JQ, Chen Z (2012) Structural and functional analysis of VQ motif-containing proteins in Arabidopsis as interacting proteins of WRKY transcription factors. Plant Physiol 159:810–825

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chi Y, Yang Y, Zhou Y, Zhou J, Fan B, Yu JQ, Chen Z (2013) Protein–protein interactions in the regulation of WRKY transcription factors. Mol Plant 6:287–300

    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

    CAS  PubMed  Google Scholar 

  • Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51:21–37

    CAS  PubMed  Google Scholar 

  • Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442

    PubMed  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    CAS  PubMed  Google Scholar 

  • Hu Y, Chen L, Wang H, Zhang L, Wang F, Yu D (2013) Arabidopsis transcription factor WRKY8 functions antagonistically with its interacting partner VQ9 to modulate salinity stress tolerance. Plant J 74:730–745

    CAS  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    CAS  PubMed  Google Scholar 

  • Kim DY, Kwon SI, Choi C, Lee H, Ahn I, Park SR, Bae SC, Lee SC, Hwang DJ (2013) Expression analysis of rice VQ genes in response to biotic and abiotic stresses. Gene 529:208–214

    CAS  PubMed  Google Scholar 

  • Kou Y, Wang S (2010) Broad-spectrum and durability: understanding of quantitative disease resistance. Curr Opin Plant Biol 13:181–185

    CAS  PubMed  Google Scholar 

  • Kou Y, Wang S (2012) Toward an understanding of the molecular basis of quantitative disease resistance in rice. J Biotechnol 159:283–290

    CAS  PubMed  Google Scholar 

  • Kou Y, Wang S (2013) Bacterial blight resistance in rice. In: Varshney RK, Tuberosa R (eds) Translational genomics for crop breeding: volume 1, biotic stress. Wiley, Hoboken, pp 11–30

    Google Scholar 

  • Lai Z, Li Y, Wang F, Cheng Y, Fan B, Yu JQ, Chen Z (2011) Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in plant defense. Plant Cell 23:3824–3841

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li H, Wang S (2013) Disease resistance. In: Jorgenson R (ed) Plant genetics and genomics: crops and models, Zhang Q, Wing RA (eds) Vol 5: Genetics and genomics of rice. Springer, Heidelberg, pp 161–175

  • 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

    CAS  PubMed  Google Scholar 

  • Ouyang Y, Huang X, Lu Z, Yao J (2012) Genomic survey, expression profile and co-expression network analysis of OsWD40 family in rice. BMC Genom 13:100

    CAS  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Petersen K, Qiu JL, Lutje J, Fiil BK, Hansen S, Mundy J, Petersen M (2010) Arabidopsis MKS1 is involved in basal immunity and requires an intact N-terminal domain for proper function. PLoS One 5:e14364

    CAS  PubMed Central  PubMed  Google Scholar 

  • Qiu D, Xiao J, Ding X, Xiong M, Cai M, Cao Y, Li X, Xu C, Wang S (2007) OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol Plant Microbe Interact 20:492–499

    CAS  PubMed  Google Scholar 

  • Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, Thorgrimsen S, Palma K, Suarez-Rodriguez MC, Sandbech-Clausen S, Lichota J, Brodersen P, Grasser KD, Mattsson O, Glazebrook J, Mundy J, Petersen M (2008) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27:2214–2221

    CAS  PubMed Central  PubMed  Google Scholar 

  • Qiu D, Xiao J, Xie W, Cheng H, Li X, Wang S (2009) Exploring transcriptional signaling mediated by OsWRKY13, a potential regulator of multiple physiological processes in rice. BMC Plant Biol 9:74

    PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Rushton DL, Tripathi P, Rabara RC, Lin J, Ringler P, Boken AK, Langum TJ, Smidt L, Boomsma DD, Emme NJ, Chen X, Finer JJ, Shen QJ, Rushton PJ (2012) WRKY transcription factors: key components in abscisic acid signalling. Plant Biotechnol J 10:2–11

    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

    CAS  PubMed  Google Scholar 

  • Schaad NW, Wang ZK, Di M, McBeath J, Peterson GL, Bonde MR (1996) An improved infiltration technique to test the pathogenicity of Xanthomonas oryzae pv. oryzae in rice seedlings. Seed Sci Technol 24:449–456

    Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shen X, Liu H, Yuan B, Li X, Xu C, Wang S (2011) OsEDR1 negatively regulates rice bacterial resistance via activation of ethylene biosynthesis. Plant, Cell Environ 34:179–191

    CAS  Google Scholar 

  • Sun X, Cao Y, Yang Z, Xu C, Li X, Wang S, Zhang Q (2004) Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encoding a LRR receptor kinase-like protein. Plant J 37:517–527

    CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tao Z, Liu H, Qiu D, Zhou Y, Li X, Xu C, Wang S (2009) A pair of allelic WRKY genes play opposite roles in rice-bacteria interactions. Plant Physiol 151:936–948

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thomma BP, Nurnberger T, Joosten MH (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang A, Garcia D, Zhang H, Feng K, Chaudhury A, Berger F, Peacock WJ, Dennis ES, Luo M (2010a) The VQ motif protein IKU1 regulates endosperm growth and seed size in Arabidopsis. Plant J 63:670–679

    CAS  PubMed  Google Scholar 

  • Wang L, Xie W, Chen Y, Tang W, Yang J, Ye R, Liu L, Lin Y, Xu C, Xiao J, Zhang Q (2010b) A dynamic gene expression atlas covering the entire life cycle of rice. Plant J 61:752–766

    CAS  PubMed  Google Scholar 

  • Wen N, Chu Z, Wang S (2003) Three types of defense-responsive genes are involved in resistance to bacterial blight and fungal blast diseases in rice. Mol Genet Genomics 269:331–339

    CAS  PubMed  Google Scholar 

  • Xiang Y, Cao Y, Xu C, Li X, Wang S (2006) Xa3, conferring resistance for rice bacterial blight and encoding a receptor kinase-like protein, is the same as Xa26. Theor Appl Genet 113:1347–1355

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xu X, Chen C, Fan B, Chen Z (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell 18:1310–1326

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang H, Wang S (2013) Rice versus Xanthomonas oryzae pv. oryzae: a unique pathosystem. Curr Opin Plant Biol 16:188–195

    PubMed  Google Scholar 

  • Zhou B, Qu S, Liu G, Dolan M, Sakai H, Lu G, Bellizzi M, Wang GL (2006) The eight amino-acid differences within three leucine-rich repeats between Pi2 and Piz-t resistance proteins determine the resistance specificity to Magnaporthe grisea. Mol Plant Microbe Interact 19:1216–1228

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National Program on the Development of Basic Research in China (2012CB114005) and the National Program of High Technology Development of China (2012AA10A303).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shiping Wang.

Additional information

Communicated by Kang Chong.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 87 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, N., Li, X., Xiao, J. et al. Comprehensive analysis of VQ motif-containing gene expression in rice defense responses to three pathogens. Plant Cell Rep 33, 1493–1505 (2014). https://doi.org/10.1007/s00299-014-1633-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-014-1633-4

Keywords

Navigation