Skip to main content
SpringerLink
Log in

Wheat resistome in response to barley yellow dwarf virus infection

  • Original Paper
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

Barley yellow dwarf virus (BYDV) caused one of the most serious virus diseases of wheat (Triticum aestivum) worldwide. The wheat–Thinopyrum intermedium translocation line YW642 carries BYDV resistance gene Bdv2. To explore resistant wheat resistome in response to BYDV infection, we used Affymetrix GeneChip® Wheat Genome Arrays to analyze transcriptomes of YW642 and its susceptible parent Zhong8601 at 12 and 72 h postinoculation with BYDV compared to mock-inoculated controls. Relative to mock-inoculated control, 335 defense-related transcripts were upregulated in BYDV-inoculated YW642, among which 70 were upregulated only in BYDV-inoculated YW642 but not in BYDV-inoculated Zhong8601 through clustering analysis. Additional analysis using BYDV-inoculated Zhong8601 as reference revealed that 59 defense-related transcripts were upregulated in BYDV-inoculated YW642. Comparison of these upregulated defense transcripts obtained via the two analysis ways indicated that 19 overlapped defense-related transcripts were highly expressed in BYDV-inoculated YW642 relative to BYDV-inoculated Zhong8601 and mock-inoculated YW642, which likely are significant factors in Bdv2-mediated defense response to BYDV. High expression of some resistance homologous genes, pathogen-associated molecular pattern-triggered immunity-related genes, ABC transporter genes, pathogenesis-related protein genes, and genes in reactive oxygen species, phospholipid signaling, and jasmonic acid-signaling may contribute to Bdv2-mediated defense response to BYDV.

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

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29

    Article  PubMed  CAS  Google Scholar 

  • Ayala L, van Ginkel M, Khairallah M, Keller B, Henry M (2001) Expression of Thinopyrum intermedium-derived barley yellow dwarf virus resistance in elite bread wheat backgrounds. Phytopathology 91:55–62

    Article  PubMed  CAS  Google Scholar 

  • Bai S, Liu J, Chang C, Zhang L, Maekawa T, Wang Q, Xiao W, Liu Y, Chai J, Takken FL, Schulze-Lefert P, Shen QH (2012) Structure-function analysis of barley NLR immune receptor MLA10 reveals its cell compartment specific activity in cell death and disease resistance. PLoS Pathog 8:e1002752

    Article  PubMed  CAS  Google Scholar 

  • Banks PM, Davidson JL, Bariana H, Larkin PJ (1995a) Effects of barley yellow dwarf virus on the yield of winter wheat. Austr J Agric Res 46:935–946

    Article  Google Scholar 

  • Banks PM, Larkin PJ, Bariana HS, Lagudah ES, Appels R, Waterhouse PM, Brettel RIS, Chen X, Xu HJ, Xin ZY, Qian YT, Zhou XN, Cheng ZM, Zhou GH (1995b) The use of cell culture for subchromosomal introgressions of barley yellow dwarf virus resistance from Thinopyrum intermedium to wheat. Genome 38:395–405

    Article  PubMed  CAS  Google Scholar 

  • Bari R, Jones JD (2009) Role of plant hormones in plant defense responses. Plant Mol Biol 69:473–488

    Article  PubMed  CAS  Google Scholar 

  • Bernardo A, Bai GH, Guo PG, Xiao K, Guenzi AC, Ayoubi P (2007) Fusarium graminearum-induced changes in gene expression between Fusarium head blight-resistant and susceptible wheat cultivars. Funct Integ Genomics 7:69–77

    Article  CAS  Google Scholar 

  • Boddu J, Cho S, Kruger WM, Muehlbauer GJ (2006) Transcriptome analysis of the Barley–Fusarium graminearum interaction. Mol Plant–Microbe Interact 19:407–417

    Article  PubMed  CAS  Google Scholar 

  • Bolton MD, Kolmer JA, Xu WW, Garvin DF (2008) Lr34-mediated leaf rust resistance in wheat: transcript profiling reveals a high energetic demand supported by transient recruitment of multiple metabolic pathways. Mol Plant–Microbe Interact 21:1515–1527

    Article  PubMed  CAS  Google Scholar 

  • Caldo R, Nettleton D, Wise R (2004) Interaction-dependent gene expression in Mla-specified response to barley powdery mildew. Plant Cell 16:2513–2518

    Google Scholar 

  • Canonne J, Marino D, Jauneau A, Pouzet C, Briere C, Roby D, Rivas S (2011) The Xanthomonas type III effector XopD targets the Arabidopsis transcription factor AtMYB30 to suppress plant defence. Plant Cell 23:3498–3511

    Article  PubMed  CAS  Google Scholar 

  • Cao A, Xing L, Wang X, Yang X, Wang W, Sun Y, Qian C, Ni J, Chen Y, Liu D, Wang X, Chen P (2011) Serine/threonine kinase gene Stpk-V, a key member of powdery mildew resistance gene Pm21, confers powdery mildew resistance in wheat. Proc Natl Acad Sci USA 108:7727–7732

    Article  PubMed  CAS  Google Scholar 

  • Cauderon Y, Saigne B, Dauge M (1973) The resistance to wheat rust of Agropyron intermedium and its use in wheat improvement. Proc 4th Int Wheat Genet Symp, University of Missouri, Columbia, USA, pp. 401–407

  • Coram TE, Wang MN, Chen XM (2008) Transcriptome analysis of the wheat–Puccinia striiformis f.sp. tritici interaction. Mol Plant Pathol 8:157–169

    Article  Google Scholar 

  • D’Arcy CJ (1995) Symptomatology and host range of barley yellow dwarf. Barley yellow dwarf: 40 years of progress. APS Press, St. Paul, pp 9–28

    Google Scholar 

  • De Jong CF, Laxalt AM, Bargmann BO, de Wit PJ, Joosten MH, Munnik T (2004) Phosphatidic acid accumulation is an early response in the Cf-4/Avr4 interaction. Plant J 39:1–12

    Article  PubMed  Google Scholar 

  • Dhondt S, Geoffroy P, Stelmach BA, Legrand M, Heitz T (2000) Soluble phospholipase A2 activity is induced before oxylipin accumulation in tobacco mosaic virus-infected tobacco leaves and iscontributed by patatin-like enzymes. Plant J 23:431–440

    Article  PubMed  CAS  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11:539–548

    Article  PubMed  CAS  Google Scholar 

  • Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868

    Article  PubMed  CAS  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–332

    Article  PubMed  CAS  Google Scholar 

  • Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA 105:7100–7105

    Article  PubMed  CAS  Google Scholar 

  • Larkin PJ, Banks PM, Lagudah ES, Appels R, Chen X, Xin ZY, Ohm HW, McIntosh RA (1995) Disomic Thinopyrum intermedium addition lines in wheat with barley yellow dwarf virus resistance and with rust resistances. Genome 38:385–394

    Article  PubMed  CAS  Google Scholar 

  • Laxalt AM, Munnik T (2002) Phospholipid signalling in plant defense. Curr Opin Plant Biol 5:332–338

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R (2004) JASMONATE-insensitive1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defence responses in Arabidopsis. Plant Cell 16:1938–1950

    Article  PubMed  CAS  Google Scholar 

  • Sharma H, Gill B, Uyemoto J (1984) High levels of resistance in Agropyron species to barley yellow dwarf and wheat streak mosaic viruses. Phytopathol Z 110:143–147

    Article  Google Scholar 

  • Sharma H, Ohm L, Goulart R, Lister R, Appels R, Benlhabib O (1995) Introgression and characterization of barley yellow dwarf virus resistance from Thinopyrum intermedium into wheat. Genome 38:406–413

    Article  PubMed  CAS  Google Scholar 

  • Soosaar JL, Burch-Smith TM, Dinesh-Kumar SP (2005) Mechainsms of plant resistance to viruses. Nat Rev Microbiol 3:789–798

    Article  PubMed  CAS  Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100:9440–9445

    Article  PubMed  CAS  Google Scholar 

  • Viemann D, Goebeler M, Schmid S, Klimmek K, Sorg C, Ludwig S, Roth J (2004) Transcriptional profiling of IKK2/NF-κB- and p38 MAP kinase-dependent gene expression in TNF-α-stimulated primary human endothelial cells. Blood 103:3365–3373

    Article  PubMed  CAS  Google Scholar 

  • Vinatzer BA, Patocchi A, Gianfranceschi L, Tartarini S, Zhang HB, Gessler C, Sansavini S (2001) Apple (Malus sp.) contains receptor-like genes homologous to the Cf resistance gene family of tomato with a cluster of such genes co-segregating with Vf apple scab resistance. Mol Plant Microbe Interact 14:508–515

    Article  PubMed  CAS  Google Scholar 

  • Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 322:681–692

    PubMed  CAS  Google Scholar 

  • Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094

    Article  PubMed  CAS  Google Scholar 

  • Xin ZY, Xu HJ, Chen X, Lin ZS, Zhou GH, Qian YT, Chen ZM, Larkin PJ, Banks PM, Apples R, Clarke B, Brettell RIS (1991) Development of common wheat germplasm resistant to barley yellow dwarf virus by biotechnology. Sci China Ser B 34(9):1055–1062

    Google Scholar 

  • Xin ZY, Zhang ZY, Chen X, Lin ZS, Ma YZ, Xu HJ, Banks PM, Larkin PJ (2001) Development and characterization of common wheat–Thinopyrum intermedium translocation lines with resistance to barley yellow dwarf virus. Euphytica 119:161–165

    Article  CAS  Google Scholar 

  • Zhang ZY, Xin ZY, Ma YZ, Chen X, Xu QF, Lin ZS (1999) Mapping of a BYDV resistance gene from Thinopyrum intermedium in wheat background by molecular markers. Sci China Ser C 42:663–668

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors are very grateful to Professor Zhiyong Xin, Drs. Xiu’e Wang, and Xuening Wei for their nice help. This study was supported by the National “863” programs (2012AA10A309 and 2006AA100102).

Author information

Authors and Affiliations

  1. The National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops of the Agriculture Ministry, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing, 100081, China

    Xindong Wang, Liang Chen, Dan Zhao & Zengyan Zhang

  2. State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, China

    Yan Liu & Xifeng Wang

Authors
  1. Xindong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dan Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xifeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zengyan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zengyan Zhang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

Primers of transcripts and reference genes for qRT-PCR (DOC 146 kb)

Table S2

Comparisons of data obtained by GeneChip and qRT-PCR (DOC 82 kb)

Table S3

Raw data from microarray analyses were identified as differentially expressed probe sets in excel format. p ≤ 0.001, FDR ≤ 0.05 in excel format. (XLS 1.13 MB)

Table S4

Functional annotations and functional categories for differentially expressed transcripts s in excel format (XLS 256 kb)

Table S5

Raw data from RB relative to SB were identified as differentially expressed transcripts in excel format (XLS 142 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, X., Liu, Y., Chen, L. et al. Wheat resistome in response to barley yellow dwarf virus infection. Funct Integr Genomics 13, 155–165 (2013). https://doi.org/10.1007/s10142-013-0309-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-013-0309-4

Keywords

Search

Navigation