biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 64:551-560, 2020 | DOI: 10.32615/bp.2020.024

Genes for defense response to Plasmodiophora brassicae during late infection in small spheroid galls of Brassica rapa

H. YANG1,2, X.Y. FANG2, X.L. WANG2, J. ZHENG2, C.L. YI2, J. FAN1, S. YUAN3, J. SHANG2, I.Y. HUANG2, W.M. WANG1,*
1 Rice Research Institute and Research Center for Major Crop Diseases, Sichuan Agricultural University, Chengdu 611130, P.R. China
2 College of Agronomy, Sichuan Agricultural University, Chengdu 611130, P.R. China
3 College of Resources, Sichuan Agricultural University, Chengdu 611130, P.R. China

Plasmodiophora brassicae is a biotrophic pathogen causing clubroots of cruciferous crops. The Brassica rapa accession T1-145 has an ability to produce small spheroid galls (SSGs), which represent neither a fully compatible interaction nor a complete resistance. To explore the defense response in SSGs induced by P. brassicae infection, global transcriptome profiling SSGs was performed at different time points. By comparing gene expression patterns, we identified many defense related genes. The first group included genes encoding receptor-like protein/kinases, such as cysteine-rich receptor-like protein kinases, receptor-like proteins, phloem intercalated with xylem/tracheary element differentiation inhibitory factor receptor (PXY/TDR), PXY-correlated 1, wall-associated kinases, nuclear shuttle protein-interacting kinase, lectin receptor-like kinases, and flagelin-sensitive 2, which might activate a basal defense. The second group involved robust effector-triggered immunity response genes such as resistance to leptosphaeria maculans 1B, constitutive shade-avoidance 1, target of avirulence B operation 1, ribosomal protein of the small subunit 6, resistance to Pseudomonas maculicola 1-interacting protein 4, enhanced disease resistance 2L, and recognition of Peronospora parasitica 13-like protein 4. The third group included genes encoding secondary cell wall formation related protein/s, a nodulin-like protein, a germin-like protein, a jacalin-related lectin, a defensin-like protein, tumor inhibitors, and sugars will eventually be exported transporter, which might contribute to quantitative resistance against P. brassicae. The gene expressions were the highest at the late stage of infection. To our knowledge, it is the first report on exploring defense response genes during SSG occurrence by a transcriptome analysis. Our data would provide useful information to further explore molecular mechanisms of the incomplete resistance.

Keywords: biotrophic pathogen, effector-triggered immunity, gene expression patterns, receptor-like protein/kinases.

Received: July 29, 2019; Revised: January 9, 2020; Accepted: February 10, 2020; Published online: August 11, 2020  Show citation

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YANG, H., FANG, X.Y., WANG, X.L., ZHENG, J., YI, C.L., FAN, J., ... WANG, W.M. (2020). Genes for defense response to Plasmodiophora brassicae during late infection in small spheroid galls of Brassica rapa. Biologia plantarum64, Article 551-560. https://doi.org/10.32615/bp.2020.024
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References

  1. Alcázar, R., Von Reth, M., Bautor, J., Chae, E., Weigel, D., Koornneef, M., Parker, J.E.: Analysis of a plant complex resistance gene locus underlying immune-related hybrid incompatibility and its occurrence in nature. - PLoS Genet. 10: e1004848, 2014. Go to original source...
  2. Audic, S., Claverie, J.M.: The significance of digital gene expression profiles. - Genome Res. 7: 986-995, 1997. Go to original source...
  3. Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D., Butler, H., Cherry, J.M.: Geneontology: tool for the unification of biology. - Nat. Genet. 25: 25-29, 2000. Go to original source...
  4. Chen, J., Pang, W., Chen, B., Zhang, C., Piao, Z.: Transcriptome analysis of Brassica rapa near-isogenic lines carrying clubroot-resistant and -susceptible alleles in response to Plasmodiophora brassicae during early infection. - Front Plant Sci. 6: 1183, 2016. Go to original source...
  5. Ciaghi, S., Schwelm, A., Neuhauser, S.: Transcriptomic response in symptomless roots of clubroot infected kohlrabi (Brassica oleracea var. gongylodes) mirrors resistant plants. - BMC Plant Biol. 19: 288, 2019. Go to original source...
  6. Crisp, P., Crute, I.R., Sutherland, R.A., Angell, S.M., Bloo, R.K.: The exploitation of genetic resources of Brassica oleracea in breeding for resistance to clubroot Plasmodiophora brassicae. - Euphytica 42: 215-226, 1989. Go to original source...
  7. Delteil, A., Gobbato, E., Cayrol, B., Estevan, J., Michel-Romiti, C., Dievart, A.: Several wall- associated kinases participate positively and negatively in basal defense against rice blast fungus. - BMC Plant Biol. 16: 17, 2016. Go to original source...
  8. Denancé, N., Ranocha, P., Oria, N., Barlet, X., Rivière, M.P., Yadeta, K.A.: Arabidopsis wat1 (walls are thin1)-mediated resistance to the bacterial vascular pathogen, Ralstonia solanacearum, is accompanied by cross-regulation of salicylic acid and tryptophan metabolism. - Plant J. 73: 225-239, 2013. Go to original source...
  9. Devos, S., Laukens, K., Deckers, P., Van Der Straeten, D., Beeckman, T., Inzé, D., Van Onckelen, H., Witters, E., Prinsen, E.: A hormone and proteome approach to picturing the initial metabolic events during Plasmodiophora brassicae infection on Arabidopsis. -Mol. Plant Microbe Interact. 19: 1431-1443, 2006. Go to original source...
  10. Eitas, T.K., Nimchuk, Z.L., Dangl, J.L.: Arabidopsis TAO1 is a TIR-NB-LRR protein that contributes to disease resistance induced by the Pseudomonas syringae effector AvrB. - Proc. nat. Acad. Sci. USA 105: 6475-6480, 2008. Go to original source...
  11. Gamas, P., De Billy, F., Truchet, G.: Symbiosis-specific expression of two Medicago truncatula nodulin genes, MtN1 and MtN13, encoding products homologous to plant defense proteins. - Mol. Plant Microbe Interact. 11: 393-403, 1998. Go to original source...
  12. Holtz, M.D., Hwang, S.F., Strelkov, S.E.: Genotyping of Plasmodiophora brassicae reveals the presence of disinct populations. - BMC Genomics 19: 254, 2018. Go to original source...
  13. Hu, Q., Min, L., Yang, X., Jin, S., Zhang, L., Li, Y.: Laccase GhLac1 modulates broad-spectrum biotic stress tolerance via DAMP-triggered immunity. - Plant Physiol. 176: 1808-1823, 2017. Go to original source...
  14. Ji, R., Zhao, L., Xing, M., Shen, X., Bi, Q., Peng, S., Feng, H.: Infection of Plasmodiophora brassicae in Chinese cabbage. - Genet. mol. Res. 13: 10976-10982, 2014. Go to original source...
  15. Jubault, M., Lariagon, C., Taconnat, L., Renou, J.P., Gravot, A., Delourme, R., Manzanares- Dauleux, M.J.: Partial resistance to clubroot in Arabidopsis is based on changes in the host primary metabolism and targeted cell division and expansion capacity. - Funct. integr. Genomics 13: 191-205, 2013. Go to original source...
  16. Kageyama, K., Asano, T.: Life cycle of Plasmodiophora brassicae. - J. Plant Growth Regul. 28: 203-211, 2009. Go to original source...
  17. Kim, S.H., Son, G.H., Bhattacharjee, S., Kim, H.J., Nam, J.C., Nguyen, P.D.: The Arabidopsis immune adaptor SRFR1 interacts with TCP transcription factors that redundantly contribute to effector-triggered immunity. - Plant J. 78: 978-789, 2014. Go to original source...
  18. La Camera, S., Balague, C., Gobel, C., Geoffroy, P., Legrand, M., Feussner, I., Roby, D., Heitz, T.: The Arabidopsis patatin-like protein 2 (PLP2) plays an essential role in cell death execution and differentially affects biosynthesis of oxylipins and resistance to pathogens. - Mol Plant Microbe Interact. 22: 469-481, 2009. Go to original source...
  19. Li. K., Hegarty, J., Zhang, C., Wan, A., Wu, J., Guedira, G.B.: Fine mapping of barley locus Rps6 conferring resistance to wheat stripe rust. - Theor. appl. Genet. 129: 845-859, 2016. Go to original source...
  20. Li, Y., Wang, Y., Zhang, H., Zhang, Q., Zhai, H., Liu, Q., He, S.: The plasma membrane-localized sucrose transporter IbSWEET10 contributes to the resistance of sweet potato to Fusarium oxysporum. - Front Plant Sci. 8: 197, 2017. Go to original source...
  21. Li, H., Li, X., Xuan, Y., Jiang, J., Wei, Y., Piao, Z.: Genome wide identification and expression profiling of SWEET genes family reveals its role during Plasmodiophora brassicae induced formation of clubroot in Brassica rapa. - Front Plant Sci. 9: 207, 2018. Go to original source...
  22. Liu, Q., Yang, J., Yan, S., Zhang, S., Zhao, J., Wang, W.: The germin-like protein OsGLP2-1 enhances resistance to fungal blast and bacterial blight in rice. - Plant mol. Biol. 92: 411-423, 2016. Go to original source...
  23. Ludwig-Müller, J.: Auxin homeostasis, signaling, and interaction with other growth hormones during the clubroot disease of Brassicaceae. - Plant Signal Behav. 9: e28593, 2014. Go to original source...
  24. Luo, X., Xu, N., Huang, J., Gao, F., Zou, H., Boudsocq, M.: A lectin receptor- like kinase mediates pattern-triggered salicylic acid signaling. - Plant Physiol. 174: 2501-2514, 2017. Go to original source...
  25. Mugford, S.T., Qi, X., Bakht, S., Hill, L., Wegel, E., Hughes, RK.: A serine carboxypeptidase- like acyltransferase is required for synthesis of antimicrobial compounds and disease resistance in oats. - Plant Cell 21: 2473-2484, 2009. Go to original source...
  26. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L., Wold, B.: Mapping and quantifying mammalian transcriptomes by RNA-Seq. - Nat. Methods 5: 621-628, 2008. Go to original source...
  27. Osaki, K., Tanaka, S., Ito, S.: Pathogenicity of Plasmodiophora brassicae populations from small, spheroid, resistant-type clubroot galls on roots of clubroot-resistant cultivars of Chinese cabbage (Brassica rapa L. subsp. pekinensis). - J. gen. Plant Pathol. 74: 242-245, 2008. Go to original source...
  28. Peng, Y., Huang, Y., Liu, Z.L., Yang, H., Shang, J.: Occurrence and morphology of small spheroid galls on clubroot-resistant Chinese cabbage. - Eur. J. Plant Pathol. 145: 591-599, 2016. Go to original source...
  29. Piao, Z.Y., Ramchiary, N., Lim, Y.P.: Genetics of clubroot resistance in Brassica species. - J. Plant Growth Regul. 28: 252-264, 2009. Go to original source...
  30. Pitino, M., Armstrong, C.M., Duan, Y.: Rapid screening for citrus canker resistance employing pathogen-associated molecular pattern-triggered immunity responses. - Hort. Res. 2: 15042, 2015. Go to original source...
  31. Rennie, D.C., Manolii, V.P., Plishka, M., Strelkov, S.E.: Histological analysis of spindle and spheroid root galls caused by Plasmodiophora brassicae. - Eur. J. Plant Pathol. 135: 771-781, 2013. Go to original source...
  32. Santos, A. A., Lopes, K.V.G., Apfata, J.A.C., Fontes, E.P.: NSP-interacting kinase, NIK: a transducer of plant defence signalling. - J. exp. Bot. 14: 3839-3845, 2010. Go to original source...
  33. Schwelm, A., Fogelqvist, J., Knaust, A., Jülke, S., Lilja, T., Bonilla-Rosso, G.: The Plasmodiophora brassicae genome reveals insights in its life cycle and ancestry of chitin synthases. - Sci. Rep. 5: 11153, 2015. Go to original source...
  34. Siemens, J., Keller, I., Sarx, J., Kunz, S., Schuller, A., Nagel, W., Schmülling, T., Parniske, M., Ludwig-Müller, J.: Transcriptome analysis of Arabidopsis clubroots indicate a key role for cytokinins in disease development. - Mol. Plant Microbe Interact. 19: 480-494, 2006. Go to original source...
  35. Sun, X., Greenwood, D.R., Templeton, M.D., Libich, D.S., McGhie, T.K., Xue, B.: The intrinsically disordered structural platform of the plant defence hub protein RPM1-interacting protein 4 provides insights into its mode of action in the host-pathogen interface and evolution of the nitrate-induced domain protein family. - FEBS J. 281: 3955-3979, 2014. Go to original source...
  36. Suwabe, K., Tsukazaki, H., Iketani, H., Hatakeyama, K., Kondo, M.: Simple sequence repeat-based comparative genomics between Brassica rapa and Arabidopsis thaliana: the genetic origin of clubroot resistance. - Genetics 173: 309-319, 2006. Go to original source...
  37. Tanaka, S., Ito, S.: Pathogenic and genetic diversity in Plasmodiophora brassicae (clubroot) from Japan. - J. gen. Plant Pathol. 79: 297-306, 2013. Go to original source...
  38. Timmermann, T., Armijo, G., Donoso, R., Seguel, A., Holuigue, L., González, B.: Paraburkholderia phytofirmans PsJN protects Arabidopsis thaliana against a virulent strain of Pseudomonas syringae through the activation of induced resistance. - Mol. Plant Microbe Interact. 30: 215-230, 2017. Go to original source...
  39. Trapnell, C., Pachter, L., Salzberg, S.L.: TopHat: discovering splice junctions with RNA-Seq. - Bioinformatics 25: 1105-1111, 2009. Go to original source...
  40. Van Loon, L.C., Van Strien, E.A.: The families of pathogenesis-related proteins: their activities, and comparative analysis of PR-1 type proteins. - Physiol. mol. Plant Pathol. 55: 85-97, 1999. Go to original source...
  41. Wang, J., Kucukoglu, M., Zhang, L., Chen, P., Decker, D., Nilsson, O.: The Arabidopsis LRR-RLK, PXC1, is a regulator of secondary wall formation correlated with the TDIF-PXY/TDR-WOX4 signaling pathway. - BMC Plant Biol. 13: 94, 2013. Go to original source...
  42. Wang, J.P., Xu, Y.P., Munyampundu, J.P., Liu, T.Y., Cai, X.Z.: Calcium-dependent protein kinase (CDPK) and CDPK-related kinase (CRK) gene families in tomato: genome-wide identification and functional analyses in disease resistance. - Mol. Genet. Genomics 291: 661-676, 2016. Go to original source...
  43. Wang, L., Feng, Z., Wang, X.: DEGseq: an R package for identifying differentially expressed genes from RNA-seq data[J]. - Bioinformatics 26: 136-138, 2010. Go to original source...
  44. Williams, P.H.: A system for the determination of races of Plasmodiophora brassicae that infect cabbage and rutabaga. - Phytopathology 56: 624-626, 1996.
  45. Wu, J., Mao, X., Cai, T., Luo, J., Wei, L.: KOBAS server: a web-based platform for automated annotation and pathway identification. - Nucl. Acids Res. 34: 720-724, 2006. Go to original source...
  46. Xue, S., Cao, T., Howard, R.J., Hwang, S.F., Strelkov, S.E.: Isolation and variation in virulence of single-spore isolates of Plasmodiophora brassicae from Canada. - Plant Dis. 92: 456-462, 2008. Go to original source...
  47. Young, M.D., Wakefield, M.J., Smyth, G.K., Oshlack, A.: Gene ontology analysis for RNA-seq: accounting for selection bias. - Genome Biol. 11: 1-12, 2010. Go to original source...
  48. Zhang, H., Hong, Y., Huang, L., Liu, S., Tian, L., Dai, Y., Cao, Z., Huang, L., Li, D., Song, F.: Virus-induced gene silencing-based functional analyses revealed the involvement of several putative trehalose-6- phosphate synthase /phosphatase genes in disease resistance against Botrytis cinerea and Pseudomonas syringae pv. tomato DC3000 in tomato. - Front Plant Sci. 7: 1176, 2016. Go to original source...
  49. Zhao, Y., Bi, K., Gao, Z., Chen, T., Liu, H., Xie, J., Cheng, J., Fu, Y., Jiang, D.: Transcriptome analysis of Arabidopsis thaliana in response to Plasmodiophora brassicae during early infection. - Front. Microbiol. 8: 673, 2017. Go to original source...