Abstract
The bacterial pathogen Xanthomonas oryzae pv. oryzae (Xoo), belonging to Xanthomonas sp., causes one of the most destructive vascular diseases in rice worldwide, particularly in Asia and Africa. To better understand Xoo pathogenesis, we performed genome sequencing of the Korea race 1 strain DY89031 (J18) and analyzed the phylogenetic tree of 63 Xoo strains. We found that the rich diversity of evolutionary features is likely associated with the rice cultivation regions. Further, virulence effector proteins secreted by the type III secretion system (T3SS) of Xoo showed pathogenesis divergence. The genome of DY89031 shows a remarkable difference from that of the widely prevailed Philippines race 6 strain PXO99A, which is avirulent to rice Xa21, a well-known disease resistance (R) gene that can be broken down by DY89031. Interestingly, plant inoculation experiments with the PXO99A transformants expressing the DY89031 genes enabled us to identify additional TAL (transcription activator-like) and non-TAL effectors that may support DY89031-specific virulence. Characterization of DY89031 genome and identification of new effectors will facilitate the investigation of the rice-Xoo interaction and new mechanisms involved.
Similar content being viewed by others
References
Ahmad, S., Ranaghan, K.E., and Azam, S.S. (2019). Combating tigecycline resistant Acinetobacter baumannii: A leap forward towards multi-epitope based vaccine discovery. Eur J Pharm Sci 132, 1–17.
Alegria, M.C., Souza, D.P., Andrade, M.O., Docena, C., Khater, L., Ramos, C.H.I., da Silva, A.C.R., and Farah, C.S. (2005). Identification of new protein-protein interactions involving the products of the chromosome-and plasmid-encoded type IV secretion loci of the phytopathogen Xanthomonas axonopodis pv. citri. J Bacteriol 187, 2315–2325.
An, S.Q., Potnis, N., Dow, M., Vorhölter, F.J., He, Y.Q., Becker, A., Teper, D., Li, Y., Wang, N., Bleris, L., et al. (2020). Mechanistic insights into host adaptation, virulence and epidemiology of the phytopathogen Xanthomonas. FEMS Microbiol Rev 44, 1–32.
Antony, G., Zhou, J., Huang, S., Li, T., Liu, B., White, F., and Yang, B. (2010). Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. Plant Cell 22, 3864–3876.
Bartetzko, V., Sonnewald, S., Vogel, F., Hartner, K., Stadler, R., Hammes, U.Z., and Börnke, F. (2009). The Xanthomonas campestris pv. vesicatoria type III effector protein XopJ inhibits protein secretion: evidence for interference with cell wall-associated defense responses. MPMI 22, 655–664.
Bhasin, H., Bhatia, D., Raghuvanshi, S., Lore, J.S., Sahi, G.K., Kaur, B., Vikal, Y., and Singh, K. (2011). New PCR-based sequence-tagged site marker for bacterial blight resistance gene Xa38 of rice. Mol Breeding 30, 607–611.
Boch, J., and Bonas, U. (2010). Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu Rev Phytopathol 48, 419–436.
Bogdanove, A.J., Schornack, S., and Lahaye, T. (2010). TAL effectors: finding plant genes for disease and defense. Curr Opin Plant Biol 13, 394–401.
Chen, L.Q., Qu, X.Q., Hou, B.H., Sosso, D., Osorio, S., Fernie, A.R., and Frommer, W.B. (2012). Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335, 207–211.
Cianfanelli, F.R., Alcoforado Diniz, J., Guo, M., De Cesare, V., Trost, M., and Coulthurst, S.J. (2016). VgrG and PAAR proteins define distinct versions of a functional type VI secretion system. PLoS Pathog 12, e1005735.
da Silva, F.G., Shen, Y., Dardick, C., Burdman, S., Yadav, R.C., de Leon, A. L., and Ronald, P.C. (2003). Bacterial genes involved in type I secretion and sulfation are required to elicit the rice Xa21-mediated innate immune response. MPMI 17, 593–601.
Eom, J.S., Luo, D., Atienza-Grande, G., Yang, J., Ji, C., Thi Luu, V., Huguet-Tapia, J.C., Char, S.N., Liu, B., Nguyen, H., et al. (2019). Diagnostic kit for rice blight resistance. Nat Biotechnol 37, 1372–1379.
Deng, Y., Ning, Y., Yang, D.L., Zhai, K., Wang, G.L., and He, Z. (2020). Molecular Basis of disease resistance and perspectives on breeding strategies for resistance improvement in crops. Mol Plant 13, 1402–1419.
Fraikin, N., Goormaghtigh, F., and Van Melderen, L. (2020). Type II toxin-antitoxin systems: evolution and revolutions. J Bacteriol 202, e00763.
Furutani, A., Takaoka, M., Sanada, H., Noguchi, Y., Oku, T., Tsuno, K., Ochiai, H., and Tsuge, S. (2009). Identification of novel type III secretion effectors in Xanthomonas oryzae pv. oryzae. MPMI 22, 96–106.
Gao, M.J., and He, Z.H. (2013). Studies on innate immunity in rice (in Chinese). Sci Sin Vitae 43, 1016–1029.
Gerlach, R.G., and Hensel, M. (2007). Protein secretion systems and adhesins: the molecular armory of Gram-negative pathogens. Int J Med Microbiol 297, 401–415.
Gonzalez, C., Szurek, B., Manceau, C., Mathieu, T., Séré, Y., and Verdier, V. (2007). Molecular and pathotypic characterization of new Xanthomonas oryzae strains from West Africa. MPMI 20, 534–546.
Hutin, M., Sabot, F., Ghesquière, A., Koebnik, R., and Szurek, B. (2015). A knowledge-based molecular screen uncovers a broad-spectrum OsSWEET14 resistance allele to bacterial blight from wild rice. Plant J 84, 694–703.
Ji, C., Ji, Z., Liu, B., Cheng, H., Liu, H., Liu, S., Yang, B., and Chen, G. (2020). Xa1 allelic R genes activate rice blight resistance suppressed by interfering TAL effectors. Plant Commun 1, 100087.
Ji, Z., Ji, C., Liu, B., Zou, L., Chen, G., and Yang, B. (2016). Interfering TAL effectors of Xanthomonas oryzae neutralize R-gene-mediated plant disease resistance. Nat Commun 7, 13435.
Jiang, G., Liu, D., Yin, D., Zhou, Z., Shi, Y., Li, C., Zhu, L., and Zhai, W. (2020a). A rice NBS-ARC gene conferring quantitative resistance to bacterial blight is regulated by a pathogen effector-inducible miRNA. Mol Plant 13, 1752–1767.
Jiang, N., Yan, J., Liang, Y., Shi, Y., He, Z., Wu, Y., Zeng, Q., Liu, X., and Peng, J. (2020b). Resistance genes and their interactions with bacterial blight/leaf streak pathogens (Xanthomonas oryzae) in rice (Oryza sativa L.)—an updated review. Rice 13, 3.
Jones, J.D.G., and Dangl, J.L. (2006). The plant immune system Nature 444, 323–329.
Kim, J.G., Li, X., Roden, J.A., Taylor, K.W., Aakre, C.D., Su, B., Lalonde, S., Kirik, A., Chen, Y., Baranage, G., et al. (2009). Xanthomonas T3S effector XopN suppresses PAMP-triggered immunity and interacts with a tomato atypical receptor-like kinase and TFT1. Plant Cell 21, 1305–1323.
Kurtz, S., Phillippy, A., Delcher, A.L., Smoot, M., Shumway, M., Antonescu, C., and Salzberg, S.L. (2004). Versatile and open software for comparing large genomes. Genome Biol 5, R12.
Lee, B.M., Park, Y.J., Park, D.S., Kang, H.W., Kim, J.G., Song, E.S., Park, I.C., Yoon, U.H., Hahn, J.H., Koo, B.S., et al. (2005). The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Res 33, 577–586.
Li, W., Deng, Y., Ning, Y., He, Z., and Wang, G.L. (2020). Exploiting broad-spectrum disease resistance in crops: From molecular dissection to breeding. Annu Rev Plant Biol 71, 575–603.
Mew, T.W. (1987). Current status and future prospects of research on bacterial blight of rice. Annu Rev Phytopathol 25, 359–382.
Miller, J.C., Tan, S., Qiao, G., Barlow, K.A., Wang, J., Xia, D.F., Meng, X., Paschon, D.E., Leung, E., Hinkley, S.J., et al. (2011). A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29, 143–148.
Niño-Liu, D.O., Ronald, P.C., and Bogdanove, A.J. (2006). Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol Plant Pathol 7, 303–324.
Ochiai, H., Inoue, Y., Takeya, M., Sasaki, A., and Kaku, H. (2005). Genome sequence of Xanthomonas oryzae pv. oryzae suggests contribution of large numbers of effector genes and insertion sequences to its race diversity. JARQ 39, 275–287.
Pfeilmeier, S., Caly, D.L., and Malone, J.G. (2016). Bacterial pathogenesis of plants: future challenges from a microbial perspective. Mol Plant Pathol 17, 1298–1313.
Pruitt, R.N., Schwessinger, B., Joe, A., Thomas, N., Liu, F., Albert, M., Robinson, M.R., Chan, L.J.G., Luu, D.D., Chen, H., et al. (2015). The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium. Sci Adv 1, e1500245.
Qin, J., Zhou, X., Sun, L., Wang, K., Yang, F., Liao, H., Rong, W., Yin, J., Chen, H., Chen, X., et al. (2018). The Xanthomonas effector XopK harbours E3 ubiquitin-ligase activity that is required for virulence. New Phytol 220, 219–231.
Salzberg, S.L., Sommer, D.D., Schatz, M.C., Phillippy, A.M., Rabinowicz, P.D., Tsuge, S., Furutani, A., Ochiai, H., Delcher, A.L., Kelley, D., et al. (2008). Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC Genomics 9, 204.
Schulze, S., Kay, S., Büttner, D., Egler, M., Eschen-Lippold, L., Hause, G., Krüger, A., Lee, J., Müller, O., Scheel, D., et al. (2012). Analysis of new type III effectors from Xanthomonas uncovers XopB and XopS as suppressors of plant immunity. New Phytol 195, 894–911.
Sinha, D., Gupta, M.K., Patel, H.K., Ranjan, A., and Sonti, R.V. (2013). Cell wall degrading enzyme induced rice innate immune responses are suppressed by the type 3 secretion system effectors XopN, XopQ, XopX and XopZ of Xanthomonas oryzae pv. oryzae. PLoS ONE 8, e75867.
Song, C., and Yang, B. (2010). Mutagenesis of 18 type III effectors reveals virulence function of XopZPXO99 in Xanthomonas oryzae pv. oryzae. MPMI 23, 893–902.
Song, W.Y., Wang, G.L., Chen, L.L., Kim, H.S., Pi, L.Y., Holsten, T., Gardner, J., Wang, B., Zhai, W.X., Zhu, L.H., et al. (1995). A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270, 1804–1806.
Souza, D.P., Andrade, M.O., Alvarez-Martinez, C.E., Arantes, G.M., Farah, C.S., and Salinas, R.K. (2011). A component of the Xanthomonadaceae type IV secretion system combines a VirB7 motif with a N0 domain found in outer membrane transport proteins. PLoS Pathog 7, e1002031.
Streubel, J., Pesce, C., Hutin, M., Koebnik, R., Boch, J., and Szurek, B. (2013). Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. New Phytol 200, 808–819.
Timilsina, S., Potnis, N., Newberry, E.A., Liyanapathiranage, P., Iruegas-Bocardo, F., White, F.F., Goss, E.M., and Jones, J.B. (2020). Xanthomonas diversity, virulence and plant-pathogen interactions. Nat Rev Microbiol 18, 415–427.
Wang, J., and Chai, J. (2020). Molecular actions of NLR immune receptors in plants and animals. Sci China Life Sci 63, 1303–1316.
Wang, J., Chern, M., and Chen, X. (2020). Structural dynamics of a plant NLR resistosome: transition from autoinhibition to activation. Sci China Life Sci 63, 617–619.
Wang, W., Mauleon, R., Hu, Z., Chebotarov, D., Tai, S., Wu, Z., Li, M., Zheng, T., Fuentes, R.R., Zhang, F., et al. (2018). Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature 557, 43–49.
Wu, X.M., Li, Y.R., Zou, L.F., and Chen, G.Y. (2007). Gene-for-gene relationships between rice and diverse avrBs3/pthA avirulence genes in Xanthomonas oryzae pv. oryzae. Plant Pathol 56, 26–34.
Yang, B., Sugio, A., and White, F.F. (2006). Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc Natl Acad Sci USA 103, 10503–10508.
Yang, D.L., Li, Q., Deng, Y.W., Lou, Y.G., Wang, M.Y., Zhou, G.X., Zhang, Y.Y., and He, Z.H. (2008). Altered disease development in the eui mutants and Eui overexpressors indicates that gibberellins negatively regulate rice basal disease resistance. Mol Plant 1, 528–537.
Zhang, B., Zhang, H., Li, F., Ouyang, Y., Yuan, M., Li, X., Xiao, J., and Wang, S. (2020). Multiple alleles encoding atypical NLRs with unique central tandem repeats in rice confer resistance to Xanthomonas oryzae pv. oryzae. Plant Commun 1, 100088.
Zhou, J., Peng, Z., Long, J., Sosso, D., Liu, B., Eom, J.S., Huang, S., Liu, S., Vera Cruz, C., Frommer, W.B., et al. (2015). Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J 82, 632–643.
Acknowledgements
This work was supported by Chinese Academy of Sciences (XDB27040201) and the National Natural Science Foundation of China (3181101746). We would like to thank Prof. Jianlong Xu (Institute of Crop Sciences, CAAS) for providing rice germplasm resources, Prof. Gongyou Chen (Shanghai Jiao Tong University) for providing Xoo strains, Prof. Yiwen Deng for rice disease evaluation, Dr. Zeling Xu (South China Agricultural University) for helping with the genome sequencing analysis.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Compliance and ethics The author(s) declare that they have no conflict of interest.
Electronic supplementary material
11427_2020_1917_MOESM7_ESM.docx
Genome sequencing of bacterial blight pathogen DY89031 reveals its diverse virulence and origins of Xanthomonas oryzae pv. oryzae strains
Rights and permissions
About this article
Cite this article
Chen, F., Yan, B., Gong, X. et al. Genome sequencing of the bacterial blight pathogen DY89031 reveals its diverse virulence and origins of Xanthomonas oryzae pv. oryzae strains. Sci. China Life Sci. 64, 2175–2185 (2021). https://doi.org/10.1007/s11427-020-1917-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-020-1917-x