Skip to main content
Log in

Genome-wide Identification and Expression Analyses of RPP13-like Genes in Barley

  • Original Article
  • Published:
BioChip Journal Aims and scope Submit manuscript

Abstract

Plants have evolved a series of mechanisms to resist pathogens infection. The nucleotide-binding site and leucine-rich repeat (NBS-LRR) family contains the largest number of plant disease resistance genes in plants. Recognition of Peronospora Parasitica 13-like (RPP13-like) genes belong to this superfamily and play important roles in the resistance of various plant diseases including the downy mildew caused by Peronospora parasitica. In this study, 21 RPP13-like genes were identified in barley via bioinformatics. These genes all contained CC, NB-ARC and LRR domains. The physical and chemical properties, chromosome locations, gene structures, protein motifs, 3D protein structures, and microarray based expression dynamics of these genes, as well as their phylogenetic relationship with other plant species were analyzed. Non-expression of MLOC_19262.1 was detected without pathogen infection. When barley was inoculated with the powdery mildew pathogenic fungus, the expression of MLOC_ 19262.1 reached a very high level, suggesting that this gene is an important and promising candidate resistance gene for further study. The two RPP13-like genes, MLOC_57007.2 and MLOC_5059.1 may be involved in barley regular or abiotic stress induced physiological metabolism in specific tissues or at specific developmental stages; furthermore, these functions may be associated with specific domains. These findings provided evidence for the functional diversity of plant pathogen resistance genes and will be helpful for the future characterization of the PRR13-like gene subfamily.

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

Similar content being viewed by others

References

  1. Jones, J.D. & Dang, I.J. The plant immune system. Nature 444, 323–329 (2006).

    Article  CAS  PubMed  Google Scholar 

  2. Li, B., Meng, X.Z., Shan, L.B. & He, P. Transcriptional regulation of pattern-triggered immunity in plants. Cell Host & Microbe. 19, 641–650 (2016).

    Article  CAS  Google Scholar 

  3. Allen, R.L. et al. Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science 306, 1957–1960 (2004).

    Article  CAS  PubMed  Google Scholar 

  4. Dodds, P.N. & Schwechheimer, C.A. Breakdown in defense signaling. Plant Cell 14, 5–8 (2002).

    Article  Google Scholar 

  5. Wang, X.S., Wu, W.R., Jin, G.L. & Zhu, J. Genomewide identification of R genes and exploitation of candidate RGA markers in rice. Chinese Sci. Bull. 50, 1120–1125 (2005).

    Article  Google Scholar 

  6. Dodds, P.N., Lawrence, G.J. & Ellis, J.G. Six amino acid changes confined to the leucine-rich repeat β-Strand/β-turn motif determine the difference between the P and P2 rust resistance specificities in flax. Plant Cell 13, 163–178 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Crute, L.R. & Pink, D.A. Genetics and utilization of pathogen resistance in plants. Plant Cell 8, 1747–1755 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Bittner-eddy, P.D., Crute, L.R., Holub, E.B. & Beynon, J.L. RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J. 21, 177–188 (2000).

    Article  CAS  PubMed  Google Scholar 

  9. Boyes, D.C., Nam, J. & Dangl, J.L. The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. PNAS 95, 15849–15854 (1998).

    Article  CAS  PubMed  Google Scholar 

  10. Rose, L.E. et al. The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana. Genetics. 166, 1517–1527 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Jia, Y.L., McAdams, S.A., Bryan, G.T., Hershey, H.P. & Valent, B. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19, 4004–4014 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Amin, N., Ali, B., Muzaffar, S., Majeed, I. & Sayeed, N. Symptoms, pathogen biology and control of downy mildew of brassica. J. Biosphere. 2, 6–9 (2013).

    Google Scholar 

  13. Bittner-Eddy, P.D. et al. Genetic and physical mapping of the RPP13 locus, in Arabidopsis, responsible for specific recognition of several Peronospora parasitica (downy mildew) isolates. Mol. Plant Microbe. In. 12, 792–802 (1999).

    Article  CAS  Google Scholar 

  14. Liang, Y. et al. Genome-wide identifcation, structural analysis and new insights into late embryogenesis abundant (LEA) gene family formation pattern in Brassica napus. Sci. Rep. 6, 24265 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Martin, G.B., Bogdanove, A.J. & Sessa, G. Understanding the functions of plant disease resistance proteins. Annu. Rev. Plant. Biol. 54, 23–61 (2003).

    Article  CAS  PubMed  Google Scholar 

  16. Bittner-eddy, P.D. & Beynon, J.L. The Arabidopsis downy mildew resistance gene, RPP13-Nd, functions independently of NDR1 and EDS1 and does not require the accumulation of salicylic acid. Mol. Plant Microbe. In. 14, 416–421 (2001).

    Article  CAS  Google Scholar 

  17. Wan, H. et al. Genome-wide analysis of NBS-encoding disease resistance genes in Cucumis sativus and phylogenetic study of NBS-encoding genes in Cucurbitaceae crops. BMC Genomics 14, 109 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Pandey, S.P. & Somssich, I.E. The Role of WRKY transcription factors in plant immunity. Plant Physiol. 150, 1648–1655 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Song, X.M. et al. Genome-wide analysis of the GRAS gene family in Chinese cabbage (Brassica ra-passp. pekinensis). Genomics 14, 135–146 (2014).

    Article  CAS  Google Scholar 

  20. Caldo, R.A., Nettleton, D., Peng, J. & Wise, R.P. Stage-specific suppression of basal defense discriminates barley plants containing fast and delayed-acting Mla powdery mildew resistance alleles. Mol. Plant Microbe. In. 19, 939–947 (2006).

    Article  CAS  Google Scholar 

  21. Hruz, T. et al. Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv. Bioinform. 420747, 35–39 (2008).

    Google Scholar 

  22. Muñoz-Amatriaín, M. et al. Transcriptome analysis of a barley breeding program examines gene expression diversity and reveals target genes for malting quality improvement. BMC Genomics 11, 1–15 (2010).

    Article  CAS  Google Scholar 

  23. Abebe, T., Melmaiee, K., Berg, V. & Wise, R.P. Drought response in the spikes of barley: gene expression in the lemma, palea, awn, and seed. Func. Integr. Genomic. 10, 191–205 (2010).

    Article  CAS  Google Scholar 

  24. Gómez-Porras, J.L., Riaño-Pachón, D.M., Dreyer, I., Mayer, J.E. & Mueller-Roeber, B. Genome-wide analysis of ABA-responsive elements ABRE and CE3 reveals divergent patterns in Arabidopsis and rice. BMC Genomics 8, 260 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Goldsbrough, A.P., Albrecht, H. & Stratford, R. Salicylic acid inducible binding of a tobacco nuclear protein to a 10 bp sequence which is highly conserved amongst stress-inducible genes. Plant J. 3, 563–571 (1993).

    Article  CAS  PubMed  Google Scholar 

  26. Tan, C.M. et al. OsPOP5, a prolyl oligopeptidase family gene from rice confers abiotic stress tolerance in Escherichia coli. Int. J. Mol. Sci. 14, 20204–20219 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Zhang, X.L., Yang, Z.P., Zhang, J. & Zhang, L.G. Ectopic expression of BraYAB1-702, a member of YABBY gene family in Chinese cabbage, causes leaf curling, inhibition of development of shoot apical meristem and flowering stage delaying in Arabidopsis thaliana. Int. J. Mol. Sci. 14, 14872–14891 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Pellegrineschi, A. et al. Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47, 493–500 (2004).

    Article  CAS  PubMed  Google Scholar 

  29. Bent, A.F. Plant disease resistance genes: function meets structure. The Plant Cell 8, 1757–1771 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Brown, N.J. et al. Independent and parallel recruitment of preexisting mechanisms underlying C4 photosynthesis. Science 331, 1436–1439 (2011).

    Article  CAS  PubMed  Google Scholar 

  31. Wilkinson, S. & Davies, W.J. Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant, Cell & Environ. 33, 510–525 (2010).

    Article  CAS  Google Scholar 

  32. Umezawa, T. et al. Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol. 51, 1821–1839 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Nakashima, K. et al. Transcriptional regulation of ABI3-and ABA-responsive genes including RD29B and RD29A in seeds, germinating embryos, and seedlings of Arabidopsis. Plant. Mol. Biol. 60, 51–68 (2006).

    Article  CAS  PubMed  Google Scholar 

  34. Hobo, T., Asada, M., Kowyama, Y. & Hottori, T. ACGTcontaining abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. Plant J. 19, 679–689 (1999).

    Article  CAS  PubMed  Google Scholar 

  35. Yanagisawa, S. Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. Plant J. 21, 281–288 (2000).

    Article  CAS  PubMed  Google Scholar 

  36. Rejeb, I.B., Pastor, V. & Mauch-Mani, B. Plant responses to simultaneous biotic and abiotic stress: molecular mechanisms. Plants 3, 458–475 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Ramegowda, V. & Senthil-Kumar, M. The interactive effects of simultaneous biotic and abiotic stresses on plants: mechanistic understanding from drought and pathogen combination. J. Plant Physiol. 176, 47–54 (2015).

    Article  CAS  PubMed  Google Scholar 

  38. Rojas, C.M., Senthil-Kumar, M., Tzin, V. & Mysore, K.S. Regulation of primary plant metabolism during plant-pathogen interactions and its contribution to plant defense. Front. Plant Sci. 5, 1–12 (2014).

    Article  CAS  Google Scholar 

  39. Goodstein, D.M. et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, 1178–1186 (2012).

    Article  CAS  Google Scholar 

  40. Gasteiger, E. et al. Protein identification and analysis tools in the ExPASy server. Method. Mol. Biology 112, 531–552 (1999).

    Google Scholar 

  41. Lin, Y.X. et al. Genome-wide identification, classification and analysis of heat shock transcription factor family in maize. BMC Genomics 12, 1–14 (2011).

    Article  CAS  Google Scholar 

  42. Bailey, T.L. et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37, w202–w208 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Källberg, M. et al. Template-based protein structure modeling using the RaptorX web server. Nat. Protoc. 7, 1511–1522 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Lovell, S.C. et al. Structure validation by Cα geometry: φ,ψ and Cβ deviation. Proteins: Structure Function & Bioinformatics 50, 437–450 (2003).

    Article  CAS  Google Scholar 

  45. Deng, W., Wang, Y., Liu, Z., Cheng, H. & Xue, Y. HemI: a toolkit for illustrating heatmaps. Plos One 9, e111988–e111988 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Lescot, M. et al. PlantCARE: a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 30, 325–327 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zheng Liu.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheng, J., Fan, H., Li, L. et al. Genome-wide Identification and Expression Analyses of RPP13-like Genes in Barley. BioChip J 12, 102–113 (2018). https://doi.org/10.1007/s13206-017-2203-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13206-017-2203-y

Keywords

Navigation