Transcriptome analysis of the Brassica napus–Leptosphaeria maculans pathosystem identifies receptor, signaling and structural genes underlying plant resistance

Plant Journal

Volumn 90, Issue 3, 2017, Pages 573-586

  Becker, Michael G ^a   Zhang, Xuehua ^a   Walker, Philip L ^a   Wan, Joey C ^a   Millar, Jenna L ^a   Khan, Deirdre ^a   Granger, Matthew J ^a   Cavers, Jacob D ^a   Chan, Ainsley C ^a   Fernando, Dilantha W G ^a   Belmonte, Mark F ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

blackleg; Brassica napus; laser microdissection; Leptosphaeria maculans; resistance; RNA sequencing; transcriptome

Indexed keywords

ELECTRIC RESISTANCE; MICRODISSECTION; PLANTS (BOTANY); POLYMERASE CHAIN REACTION; RNA;

BLACKLEG; BRASSICA NAPUS; LASER MICRO DISSECTIONS; LEPTOSPHAERIA MACULANS; RNA SEQUENCING; TRANSCRIPTOMES;

GENES;

GENES; NUCLEIC ACIDS; PATHOGENS; PLANTS;

ASCOMYCETES; DISEASE RESISTANCE; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; POLYMERASE CHAIN REACTION; QUANTITATIVE TRAIT LOCUS; RAPESEED;

ASCOMYCOTA; BRASSICA NAPUS; DISEASE RESISTANCE; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES; POLYMERASE CHAIN REACTION; QUANTITATIVE TRAIT LOCI;

EID: 85016635481     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13514     Document Type: Article

References (57)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403–410.
2. Anders, S. and Huber, W. (2010) Differential expression analysis for sequence count data. Genome Biol. 11, R106.
3. Belmonte, M.F., Kirkbride, R.C., Stone, S.L. et al. (2013) Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed. Proc. Natl Acad. Sci. USA, 110, E435–E444.
4. Bhardwaj, A.R., Joshi, G., Kukreja, B. et al. (2015) Global insights into high temperature and drought stress regulated genes by RNA-Seq in economically important oilseed crop Brassica juncea. BMC Plant Biol. 15, 9.
5. Bigeard, J., Colcombet, J. and Hirt, H. (2015) Signaling mechanisms in pattern-triggered immunity (PTI). Mol. Plant, 8, 521–539.
6. Bohman, S., Staal, J., Thomma, B.P.H.J., Wang, M. and Dixelius, C. (2004) Characterisation of an Arabidopsis-Leptosphaeria maculans pathosystem: resistance partially requires camalexin biosynthesis and is independent of salicylic acid, ethylene and jasmonic acid signalling. Plant J. 37, 9–20.
7. Bolger, A.M., Lohse, M. and Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114–2120.
8. Bu, Q., Jiang, H., Li, C.-B., Zhai, Q., Zhang, J., Wu, X., Sun, J., Xie, Q. and Li, C. (2008) Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. Cell Res. 18, 756–767.
9. Cawly, J., Cole, A.B., Király, L., Qiu, W. and Schoelz, J.E. (2005) The plant gene CCD1 selectively blocks cell death during the hypersensitive response to Cauliflower mosaic virus infection. Mol. Plant-Microbe Interact. 18, 212–219.
10. Chalhoub, B., Denoeud, F., Liu, S. et al. (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science, 345, 950–953. Available at: http://www.sciencemag.org/cgi/doi/10.1126/science.1253435.
11. Chan, A. and Belmonte, M. (2013) Histological and ultrastructural changes in canola (Brassica napus) funicular anatomy during the seed lifecycle. Botany, 91, 671–679.
12. Chan, A.C., Khan, D., Girard, I.J., Becker, M.G., Millar, J.L., Sytnik, D. and Belmonte, M.F. (2016) Tissue-specific laser microdissection of the Brassica napus funiculus improves gene discovery and spatial identification of biological processes. J. Exp. Bot. 67, erw179.
13. Clay, N.K., Adio, A.M., Denoux, C., Jander, G. and Ausubel, F.M. (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science, 323, 95–101.
14. Dangl, J.L., Horvath, D.M. and Staskawicz, B.J. (2013) Pivoting the plant immune system from dissection to deployment. Science, 341, 746–751.
15. Denancé, N., Sánchez-Vallet, A., Goffner, D. and Molina, A. (2013) Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front. Plant Sci. 4, 1–12.
16. Ellinger, D., Naumann, M., Falter, C., Zwikowics, C., Jamrow, T., Manisseri, C., Somerville, S.C. and Voigt, C.A. (2013) Elevated early callose deposition results in complete penetration resistance to Powdery Mildew in Arabidopsis. Plant Physiol. 161, 1433–1444.
17. Fitt, B.D.L., Brun, H., Barbetti, M.J. and Rimmer, S.R. (2006) World-wide importance of phoma stem canker (Leptosphaeria maculans and L. biglobosa) on oilseed Rape (Brassica napus). Eur. J. Plant Pathol. 114, 3–15.
18. Flor, H.H. (1971) Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9, 275–296.
19. Frerigmann, H. and Gigolashvili, T. (2014) MYB34, MYB51, and MYB122 distinctly regulate indolic glucosinolate biosynthesis in Arabidopsis thaliana. Mol. Plant, 7, 814–828.
20. Haddadi, P., Ma, L., Wang, H. and Borhan, M.H. (2016) Genome-wide transcriptomic analyses provide insights into the lifestyle transition and effector repertoire of Leptosphaeria maculans during the colonization of Brassica napus seedlings. Mol. Plant Pathol. 7, 1196–1210.
21. Hiruma, K., Fukunaga, S., Bednarek, P., Pislewska-Bednarek, M., Watanabe, S., Narusaka, Y., Shirasu, K. and Takano, Y. (2013) Glutathione and tryptophan metabolism are required for Arabidopsis immunity during the hypersensitive response to hemibiotrophs. Proc. Natl Acad. Sci. USA, 110, 9589–9594.
22. Jones, J.D.G. and Dangl, J.L. (2006) The plant immune system. Nature, 444, 323–329.
23. Kabbage, M., Williams, B. and Dickman, M.B. (2013) Cell death control: the interplay of apoptosis and autophagy in the pathogenicity of Sclerotinia sclerotiorum. PLoS Pathog. 9, e1003287.
24. Kaliff, M., Staal, J., Myrenås, M. and Dixelius, C. (2007) ABA is required for Leptosphaeria maculans resistance via ABI1- and ABI4-dependent signaling. Mol. Plant-Microbe Interact. 20, 335–345.
25. Kumar, R., Ichihashi, Y., Kimura, S., Chitwood, D.H., Headland, L.R., Peng, J., Maloof, J.N. and Sinha, N.R. (2012) A high-throughput method for Illumina RNA-Seq library preparation. Front. Plant Sci. 3, 1–10.
26. Larkan, N.J., Lydiate, D.J., Parkin, I.A.P., Nelson, M.N., Epp, D.J., Cowling, W., Rimmer, S.R. and Borhan, M.H. (2013) The Brassica napus blackleg resistance gene LepR3 encodes a receptor-like protein triggered by the Leptosphaeria maculans effector AVRLM1. New Phytol. 197, 595–605.
27. Larkan, N.J., Ma, L. and Borhan, M.H. (2015) The Brassica napus receptor-like protein RLM2 is encoded by a second allele of the LepR3/Rlm2 blackleg resistance locus. Plant Biotechnol. J. 13, 983–992.
28. Le, M.H., Cao, Y., Zhang, X.C. and Stacey, G. (2014) LIK1, a CERK1-interacting kinase, regulates plant immune responses in Arabidopsis. PLoS ONE, 9, e102245.
29. Li, S., Fu, Q., Chen, L., Huang, W. and Yu, D. (2011) Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta, 233, 1237–1252.
30. Lorang, J.M., Sweat, T.A. and Wolpert, T.J. (2007) Plant disease susceptibility conferred by a “resistance” gene. Proc. Natl Acad. Sci. USA, 104, 14861–14866.
31. Lowe, R.G.T., Cassin, A., Grandaubert, J., Clark, B.L., Van De Wouw, A.P., Rouxel, T. and Howlett, B.J. (2014) Genomes and transcriptomes of partners in plant–fungal-interactions between canola (Brassica napus) and two Leptosphaeria species. PLoS ONE, 9, e103098.
32. Luna, E., Pastor, V., Robert, J., Flors, V., Mauch-Mani, B. and Ton, J. (2011) Callose deposition: a multifaceted plant defense response. Mol. Plant-Microbe Interact. 24, 183–193.
33. Marcroft, S.J., Van de Wouw, A.P., Salisbury, P.A., Potter, T.D. and Howlett, B.J. (2012) Effect of rotation of canola (Brassica napus) cultivars with different complements of blackleg resistance genes on disease severity. Plant. Pathol. 61, 934–944.
34. Meng, X. and Zhang, S. (2013) MAPK cascades in plant disease resistance signaling. Annu. Rev. Phytopathol. 51, 245–266.
35. Millar, J.L., Becker, M.G. and Belmonte, M.F. (2015) Laser microdissection of plant tissues. In Plant Microtechniques and Protocols (Yeung, E.C.T., Stasolla, C., Sumner, M.J. and Huang, B.Q., eds). Cham: Springer International Publishing, pp. 337–350.
36. Mishra, A.K., Sharma, K. and Misra, R.S. (2012) Elicitor recognition, signal transduction and induced resistance in plants. J. Plant Interact. 7, 95–120.
37. Mithen, R.F., Lewis, B.G. and Fenwick, G.R. (1986) In vitro activity of glucosinolates and their products against Leptosphaeria maculans. Trans. Br. Mycol. Soc. 87, 433–440.
38. Mortazavi, A., Williams, B.A., Mccue, K., Schaeffer, L. and Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods, 5, 1–8.
39. Mugford, S.G., Yoshimoto, N., Reichelt, M. et al. (2009) Disruption of adenosine-5′-phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites. Plant Cell Online, 21, 910–927.
40. Nakao, M., Nakamura, R., Kita, K., Inukai, R. and Ishikawa, A. (2011) Non-host resistance to penetration and hyphal growth of Magnaporthe oryzae in Arabidopsis. Sci. Rep. 1, 171.
41. Orlando, D.A., Brady, S.M., Koch, J.D., Dinneny, R. and Benfey, P.N. (2009) Manipulating large-scale arabidopsis microarray expression data: identifying dominant expression patterns and biological process enrichment. In Plant Systems Biology (Belostotsky, D.A., ed). Totowa, NJ: Humana Press, pp. 57–77.
42. Pedras, M.S.C., Yaya, E.E. and Glawischnig, E. (2011) The phytoalexins from cultivated and wild crucifers: chemistry and biology. Nat. Prod. Rep. 28, 1381–1405.
43. Rao, M.V., Lee, H., Creelman, R.A., Mullet, J.E. and Davis, K.R. (2000) Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell, 12, 1633–1646.
44. Rieu, I. and Powers, S.J. (2009) Real-time quantitative RT-pcr: design, calculations, and statistics. Plant Cell Online, 21, 1031–1033.
45. Rouxel, T., Penaud, A., Pinochet, X., Brun, H., Gout, L., Delourme, R., Schmit, J. and Balesdent, M.H. (2003) A 10-year survey of populations of Leptosphaeria maculans in France indicates a rapid adaptation towards the Rlm1 resistance gene of oilseed rape. Eur. J. Plant Pathol. 109, 871–881.
46. Šašek, V., Nováková, M., Jind, B., Bóka, K., Valentová, O. and Burketová, L. (2012) Recognition of avirulence gene AvrLm1 from hemibiotrophic ascomycete Leptosphaeria maculans triggers salicylic acid and ethylene signaling in Brassica napus. Mol. Plant-Microbe Interact. 25, 1238–1250.
47. Schiffer, R., Görg, R., Jarosch, B., Beckhove, U., Bahrenberg, G., Kogel, K. and Schulze-Lefert, P. (1997) Tissue dependence and differential cordycepin sensitivity of race-specific resistance responses in the barley-powdery mildew interaction. Mol. Plant-Microbe Interact. 10, 830–839.
48. Staal, J., Kaliff, M., Bohman, S. and Dixelius, C. (2006) Transgressive segregation reveals two Arabidopsis TIR-NB-LRR resistance genes effective against Leptosphaeria maculans, causal agent of blackleg disease. Plant J. 46, 218–230.
49. Staal, J., Kaliff, M., Dewaele, E., Persson, M. and Dixelius, C. (2008) RLM3, a TIR domain encoding gene involved in broad-range immunity of Arabidopsis to necrotrophic fungal pathogens. Plant J. 55, 188–200.
50. Stotz, H.U., Mitrousia, G.K., de Wit, P.J.G.M. and Fitt, B.D.L. (2014) Effector-triggered defence against apoplastic fungal pathogens. Trends Plant Sci. 19, 491–500.
51. Thomma, B.P.H.J., Numberger, N. and Joosten, M.H.A.J. (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell, 23, 4–15.
52. Trapnell, C., Roberts, A., Goff, L. et al. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578.
53. Tsuda, K. and Katagiri, F. (2010) Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr. Opin. Plant Biol. 13, 459–465.
54. Van de Wouw, A.P., Cozijnsen, A.J., Hane, J.K., Brunner, P.C., McDonald, B.A., Oliver, R.P. and Howlett, B.J. (2010) Evolution of linked avirulence effectors in Leptosphaeria maculans is affected by genomic environment and exposure to resistance genes in host plants. PLoS Pathog. 6, e1001180.
55. Wang, Y.H. (2008) How effective is T-DNA insertional mutagenesis in Arabidopsis? J. Biochem. Technol. 1, 11–20.
56. Zhang, X., Peng, G., Kutcher, H.R., Balesdent, M.H., Delourme, R. and Fernando, W.G.D. (2016) Breakdown of Rlm3 resistance in the Brassica napus–Leptosphaeria maculans pathosystem in western Canada. Eur. J. Plant Pathol. 145(3), 659–674.
57. Zheng, Z., Mosher, S.L., Fan, B., Klessig, D.F. and Chen, Z. (2007) Functional analysis of Arabidopsis WRKY25 transcription factor in plant defense against Pseudomonas syringae. BMC Plant Biol. 7, 2.