Skip to main content
SpringerLink
Log in

Comparative Transcriptome Analysis of Rice Resistant and Susceptible Genotypes to Xanthomonas oryzae pv. oryzae Identifies Novel Genes to Control Bacterial Leaf Blight

  • Original Paper
  • Published:
Molecular Biotechnology Aims and scope Submit manuscript

Abstract

The bacterial leaf blight in rice caused by Xanthomonas oryzae pv. oryzae (Xoo) affects crop losses worldwide. In spite of developing resistant varieties by introgressing different Xa genes, the occurrence of diseases is evident. Here we report identification of several genes that are associated with improved plant immunity against Xoo in a resistant genotype BPT-5204 in comparison with susceptible genotype TN-1. The RNA sequencing information was developed to identify the genes that could provide durable resistance in rice. Xoo-resistant rice genotype BPT-5204 with Xa 5, 13 and 21 genes is compared with sensitive Taichung Native 1 (TN-1) to identify the genetic pathways and gene networks involved in resistance mechanisms. The higher levels of salicylic acid resulted in upregulation of many pathogenesis-related (PR) and redox protein encoding transcripts which resulted in higher hypersensitive response in BPT-5204. Many Serine/threonine protein kinase, leucine-rich repeat (LRR) transmembrane protein kinase, protein kinase family genes, Wall-associated kinase (WAK) were upregulated that resulted in activation of bZIP, WRKY, MYB, DOF and HSFs transcription factors that are associated with improved plant immunity. The study provided roles of many genes and their associated plant immunity pathways that can be used for developing resistant rice cultivars.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Liu, W., Liu, J., Triplett, L., Leach, J. E., & Wang, G.-L. (2014). Novel insights into rice innate immunity against bacterial and fungal pathogens. Annual Review of Phytopathology, 52, 213–241.

    Article  CAS  Google Scholar 

  2. Bogdanove, A. J., Schornack, S., & Lahaye, T. (2010). TAL effectors: Finding plant genes for disease and defense. Current Opinion in Plant Biology, 13(4), 394–401.

    Article  CAS  Google Scholar 

  3. ZhiYuan, J., ChunLian, W., & KaiJun, Z. (2018). Rice routes of countering Xanthomonas oryzae. International Journal of Molecular Sciences, 19(10), 3008.

    Article  Google Scholar 

  4. Suh, J. P., Jeung, J. U., Noh, T. H., Cho, Y. C., Park, S. H., Park, H. S., Shin, M. S., Kim, C. K., & Jena, K. K. (2013). Development of breeding lines with three pyramided resistance genes that confer broad-spectrum bacterial blight resistance and their molecular analysis in rice. Rice, 6(1), 5.

    Article  PubMed Central  Google Scholar 

  5. Kottapalli, K. R., Narasu, M. L., & Jena, K. K. (2010). Effective strategy for pyramiding three bacterial blight resistance genes into fine grain rice cultivar, Samba Mahsuri, using sequence tagged site markers. Biotechnology Letters, 2(7), 989–996.

    Article  Google Scholar 

  6. Singh, A. K., Gopalakrishnan, S., Singh, V. P., Prabhu, K. V., Mohapatra, T., Singh, N. K., Sharma, T. R., Nagarajan, M., Vinod, K. K., Singh, D., et al. (2011). Marker assisted selection: A paradigm shift in Basmati breeding. Indian Journal of Genetics and Plant Breeding, 71(2), 1–9.

    Google Scholar 

  7. Zhang, S., Song, W. Y., Chen, L., Ruan, D., Taylor, N., Ronald, P., Beachy, R., & Fauquet, C. (1998). Transgenic elite Indica rice varieties, resistant to Xanthomonas oryzae pv. oryzae. Molecular Breeding, 4, 551–558.

    Article  CAS  Google Scholar 

  8. Tu, J., Ona, I., Zhang, Q., Mew, T. W., Khush, G. S., & Datta, S. K. (1998). Transgenic rice variety ‘IR72’ with Xa21 is resistant to bacterial blight. Theoretical and Applied Genetics, 97, 31–36.

    Article  CAS  Google Scholar 

  9. Yoshimura, S., Yamanouchi, U., Katayose, Y., Toki, S., Wang, Z. X., Kono, I., Kurata, N., Yano, M., Iwata, N., & Sasaki, T. (1998). Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proceedings of the National Academy of Sciences of the United States of America, 95(4), 1663–1668.

    Article  CAS  PubMed Central  Google Scholar 

  10. Hwang, S. H., Sl, K., Jang, J. Y., Fang, I. L., Lee, H., Choi, C., Park, S., Ahn, I., Bae, S., & Hwang, D. J. (2016). OsWRKY51, a rice transcription factor, functions as a positive regulator in defense response against Xanthomonas oryzae pv. oryzae. Plant Cell Reports, 35, 1975–1985.

    Article  CAS  Google Scholar 

  11. Wang, C., Tariq, R., Ji, Z., Wei, Z., Zheng, K., Mishra, R., & Zhao, K. (2019). Transcriptome analysis of a rice cultivar reveals the differentially expressed genes in response to wild and mutant mutant strains of Xanthomonas oryzae pv. oryzae. Scientific Reports, 9, 3757.

    Article  PubMed Central  Google Scholar 

  12. Cheng, X. J., He, B., Chen, L., Xiao, S. Q., Fu, J., Chen, Y., Yu, T. Q., Cheng, Z. Q., & Feng, H. (2016). Transcriptome analysis confers a complex disease resistance network in wild rice Oryza meyeriana against Xanthomonas oryzae pv. oryzae. Scientific Reports, 6, 38215.

    Article  CAS  PubMed Central  Google Scholar 

  13. Djedatin, G., Ndjiondjop, M.-N., Sanni, A., Lorieux, M., Verdier, V., & Ghesquiere, A. (2016). Identification of novel major and minor QTLs associated with Xanthomonas oryzae pv. oryzae (African strains) resistance in rice (Oryza sativa L.). Rice, 9, 18.

    Article  PubMed Central  Google Scholar 

  14. Ke, Y., Hui, S., & Yuan, M. (2017). Xanthomonas oryzae pv. oryzae inoculation and growth rate on rice by leaf clipping method. Bio-Protocol, 7, 1–7.

    Article  Google Scholar 

  15. Defraia, C. T., Schmelz, E. A., & Mou, Z. (2008). A rapid biosensor-based method for quantification of free and glucose-conjugated salicylic acid. Plant Methods, 4, 1–11.

    Article  Google Scholar 

  16. Rio, D. C., Ares, M. J., Hannon, G. J., & Nilsen, T. W. (2010). Purification of RNA using TRIzol (TRI reagent). Cold Spring Harbor Protocols, pdb.prot5439.

  17. Pertea, M., Pertea, G. M., Antonescu, C. M., Chang, T. C., Mendell, J. T., & Salzberg, S. L. (2015). StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature Biotechnology, 33(3), 290–295.

    Article  CAS  PubMed Central  Google Scholar 

  18. Liu, L., Mei, Q., Yu, Z., Sun, T., Zhang, Z., & Chen, M. (2013). An integrative bioinformatics framework for genome-scale multiple level network reconstruction of rice. Journal of Integrative Bioinformatics, 10(2), 223.

    Article  Google Scholar 

  19. Du, Z., Zhou, X., Ling, Y., Zhang, Z., & Su, Z. (2010). agriGO: A GO analysis toolkit for the agricultural community. Nucleic Acids Research, 38(Web Server issue), W64–W70.

  20. Thimm, O., Bläsing, O., Gibon, Y., Nagel, A., Meyer, S., Krüger, P., Selbig, J., Müller, L. A., Rhee, S. Y., & Stitt, M. (2004). MAPMAN: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant Journal, 37(6), 914–939.

    Article  CAS  Google Scholar 

  21. Tsuda, K., & Katagiri, F. (2010). Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Current Opinion in Plant Biology, 13(4), 459–465.

    Article  CAS  Google Scholar 

  22. Vemanna, R. S., Bakade, R., Bharti, P., Kumar, M. K. P., Sreeman, S. M., Senthil-Kumar, M., & Makarla, U. (2019). Cross-talk signaling in rice during combined drought and bacterial blight stress. Frontiers in Plant Science, 10, 193.

    Article  PubMed Central  Google Scholar 

  23. Kumar, S. V. (2016). Pyramiding of blast resistance genes in to elite rice cultivars.

  24. Yang, D.-L., Yang, Y., & He, Z. (2013). Roles of plant hormones and their interplay in rice immunity. Molecular Plant, 6, 675–685.

    Article  CAS  Google Scholar 

  25. Ponciano, G., Yoshikawa, M., Lee, J. L., Ronald, P. C., & Whalen, M. C. (2006). Pathogenesis-related gene expression in rice is correlated with developmentally controlled Xa21-mediated resistance against Xanthomonas oryzae pv. oryzae. Physiological and Molecular Plant Pathology, 69, 131–139.

    Article  CAS  Google Scholar 

  26. Narsai, R., Wang, C., Chen, J., Wu, J., Shou, H., & Whelan, J. (2013). Antagonistic, overlapping and distinct responses to biotic stress in rice (Oryza sativa) and interactions with abiotic stress. BMC Genomics, 14, 93.

    Article  CAS  PubMed Central  Google Scholar 

  27. Cheval, C., Aldon, D., Galaud, J. P., & Ranty, B. (2013). Calcium/calmodulin-mediated regulation of plant immunity. Biochimica et Biophysica Acta—Molecular Cell Research, 1833(7), 1766–1771.

    Article  CAS  Google Scholar 

  28. Mur, L. A. J., Kenton, P., Lloyd, A. J., Ougham, H., & Prats, E. (2008). The hypersensitive response; The centenary is upon us but how much do we know? Journal of Experimental Botany, 59(3), 501–520.

    Article  CAS  Google Scholar 

  29. Gullner, G., Komives, T., Király, L., & Schröder, P. (2018). Glutathione S-transferase enzymes in plant–pathogen interactions. Frontiers in plant science, 9, 1836.

    Article  PubMed Central  Google Scholar 

  30. Jones, J. D. G., & Dangl, J. L. (2006). The plant immune system. Nature, 444, 323–329.

    Article  CAS  Google Scholar 

  31. Dodds, P. N., & Rathjen, J. P. (2010). Plant immunity: Towards an integrated view of plant pathogen interactions. Nature Reviews Genetics, 11(8), 539–548.

    Article  CAS  Google Scholar 

  32. McHale, L., Tan, X., Koehl, P., & Michelmore, R. W. (2006). Plant NBS-LRR proteins: Adaptable guards. Genome Biology, 7(4), 212.

    Article  PubMed Central  Google Scholar 

  33. Tameling, W. I. L., Vossen, J. H., Albrecht, M., Lengauer, T., Berden, J. A., Haring, M. A., Cornelissen, B. J. C., & Takken, F. L. W. (2006). Mutations in the NB-ARC domain of I-2 that impair ATP hydrolysis cause autoactivation. Plant Physiology, 140(4), 1233–1245.

    Article  CAS  PubMed Central  Google Scholar 

  34. Oliva, R., Ji, C., Atienza-Grande, G., Huguet-Tapia, J. C., Perez-Quintero, A., Li, T., Eom, J. S., Li, C., Nguyen, H., Liu, B., et al. (2019). Broad-spectrum resistance to bacterial blight in rice using genome editing. Nature Biotechnology, 37(11), 1344–1350.

    Article  CAS  PubMed Central  Google Scholar 

  35. Ramu, V., Oh, S., Lee, H.-K., Nandety, R. S., Oh, Y., Lee, S., Nakashima, J., Tang, Y., Senthil-Kumar, M., & Mysore, K. S. (2020). A novel role of salt and drought induced RING 1 protein in modulating plant defense against hemibiotrophic and necrotrophic pathogens. Molecular Plant–Microbe Interactions: MPMI, 34(3), 297–308.

    Article  Google Scholar 

  36. Pooja, S., Sweta, K., Mohanapriya, A., Sudandiradoss, C., Siva, R., Gothandam, K. M., & Babu, S. (2015). Homotypic clustering of OsMYB4 binding site motifs in promoters of the rice genome and cellular-level implications on sheath blight disease resistance. Gene, 561(2), 209–218.

    Article  CAS  Google Scholar 

  37. Cao, W. L., Chu, R. Z., Zhang, Y., Luo, J., Su, Y. Y., Xie, L. J., Zhang, H. S., Wang, J. F., & Bao, Y. M. (2015). OsJAMyb, a R2R3-type MYB transcription factor, enhanced blast resistance in transgenic rice. Physiological and Molecular Plant Pathology, 92, 154–160.

    Article  CAS  Google Scholar 

  38. Yin, Y., Zhu, Q., Dai, S., Lamb, C., & Beachy, R. N. (1997). RF2a, a bZIP transcriptional activator of the phloem-specific vice tungro bacilliform virus promoter, functions in vascular development. EMBO Journal, 16(17), 5247–5259.

    Article  CAS  Google Scholar 

  39. Nakashita, H., Yasuda, M., Nitta, T., Asami, T., Fujioka, S., Arai, Y., Sekimata, K., Takatsuto, S., Yamaguchi, I., & Yoshida, S. (2003). Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. The Plant Journal: For Cell and Molecular Biology, 33(5), 887–898.

    Article  CAS  Google Scholar 

  40. Liao, H., Xiao, X., Li, X., Chen, Y., Fu, X., Lin, D., Niu, X., Chen, Y., & He, C. (2016). OsBAK1 is involved in rice resistance to Xanthomonas oryzae pv. oryzae PXO99. Plant Biotechnology Reports, 10, 75–82.

    Article  Google Scholar 

  41. Li, D., Wang, L., Wang, M., Xu, Y.-Y., Luo, W., Liu, Y.-J., Xu, Z.-H., Li, J., & Chong, K. (2009). Engineering OsBAK1 gene as a molecular tool to improve rice architecture for high yield. Plant Biotechnology Journal, 7, 791–806.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by RCB core grant, Ramanujan fellowship (SB/S2/RJN-046/2016) to VSR. GP acknowledges CSIR-UGC fellowship.

Author information

Author notes

  1. Rahul Bakade, Kishor D. Ingole, Sanjay Deshpande and Garima Pal equally contributed to this study.

Authors and Affiliations

  1. Laboratory of Plant Functional Genomics, Regional Centre for Biotechnology, NCR Biotech Science Cluster, 3rd Milestone, Faridabad-Gurgaon Expressway, Faridabad, Haryana, 121 001, India

    Kishor D. Ingole, Sanjay Deshpande, Garima Pal, Saikat Bhattacharjee & Vemanna S. Ramu

  2. Department of Plant Pathology, University of Agricultural Sciences, GKVK, Bengaluru, 560065, India

    Rahul Bakade, Swathi S. Patil & M. K. Prasannakumar

Authors
  1. Rahul Bakade
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kishor D. Ingole
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sanjay Deshpande
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Garima Pal
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Swathi S. Patil
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Saikat Bhattacharjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. K. Prasannakumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Vemanna S. Ramu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vemanna S. Ramu.

Ethics declarations

Conflict of interest

Authors have no conflicts of interest.

Ethical Approval

Research involves rice plants and do not involve any human participants and/or animals.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bakade, R., Ingole, K.D., Deshpande, S. et al. Comparative Transcriptome Analysis of Rice Resistant and Susceptible Genotypes to Xanthomonas oryzae pv. oryzae Identifies Novel Genes to Control Bacterial Leaf Blight. Mol Biotechnol 63, 719–731 (2021). https://doi.org/10.1007/s12033-021-00338-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12033-021-00338-3

Keywords

Search

Navigation