Recent advances in the Zymoseptoria tritici–wheat interaction: Insights from pathogenomics

Frontiers in Plant Science

Volumn 6, Issue FEB, 2015, Pages

  McDonald, Megan C ^a   McDonald, Bruce A ^b   Solomon, Peter S ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b ETH ZURICH   (Switzerland)

Author keywords

Comparative genomics; Effector; Mycosphaerella graminicola; Necrotroph; RNA seq; Wheat pathogen

Indexed keywords

MYCOSPHAERELLA GRAMINICOLA; TRITICUM AESTIVUM;

EID: 84925081236     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00102     Document Type: Review

References (41)

1. Banke, S., Peschon, A., and McDonald, B. A. (2004). Phylogenetic analysis of globally distributed Mycosphaerella graminicola populations based on three DNA sequence loci. Fungal Genet. Biol. 41, 226-238. doi: 10.1016/j.fgb.2003.09.006
2. Brading, P. A., Verstappen, E. C. P., Kema, G. H. J., and Brown, J. K. M. (2002). A gene-for-gene relationship between wheat and Mycosphaerella graminicola, the Septoria tritici blotch pathogen. Phytopathology 92, 439-445. doi: 10.1094/PHYTO.2002.92.4.439
3. Brunner, P. C., Torriani, S. F. F., Croll, D., Stukenbrock, E. H., and McDonald, B. A. (2013). Coevolution and life cycle specialization of plant cell wall degrading enzymes in a hemibiotrophic pathogen. Mol. Biol. Evol. 30, 1337-1347. doi: 10.1093/molbev/mst041
4. Chartrain, L., Sourdille, P., Bernard, M., and Brown, J. K. M. (2009). Identification and location of Stb9, a gene for resistance to Septoria tritici blotch in wheat cultivars Courtot and Tonic. Plant Pathol. 58, 547-555. doi: 10.1111/j.1365-3059.2008.02013.x
5. Cools, H. J., and Fraaije, B. A. (2008). Are azole fungicides losing ground against Septoria wheat disease? Resistance mechanisms in Mycosphaerella graminicola. Pest Manag. Sci. 64, 681-684. doi: 10.1002/ps.1568
6. Cowger, C., Hoffer, M. E., and Mundt, C. C. (2000). Specific adaptation by Mycosphaerella graminicola to a resistant wheat cultivar. Plant Pathol. 49, 445-451. doi: 10.1046/j.1365-3059.2000.00472.x
7. Croll, D., and McDonald, B. A. (2011). The accessory genome as a cradle for adaptive evolution in pathogens. PLoS Pathog. 8:e1002608. doi: 10.1371/journal.ppat.1002608
8. Croll, D., Zala, M., and McDonald, B. A. (2013). Breakage-fusion-bridge cycles and large insertions contribute to the rapid evolution of accessory chromosomes in a fungal pathogen. PLoS Genet. 9:e1003567. doi: 10.1371/journal.pgen.1003567
9. Davey, J. W., Hohenlohe, P. A., Etter, P. D., Boone, J. Q., Catchen, J. M., and Blaxter, M. L. (2011). Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat. Rev. Genet. 12, 499-510. doi: 10.1038/nrg3012
10. Deller, S., Hammond-Kosack, K. E., and Rudd, J. J. (2011). The complex interactions between host immunity and non-biotrophic fungal pathogens of wheat leaves. J. Plant Physiol. 168, 63-71. doi: 10.1016/j.jplph.2010.05.024
11. Duncan, K. E., and Howard, R. J. (2000). Cytological analysis of wheat infection by the leaf blotch pathogenMycosphaerella graminicola. Mycol. Res. 104, 1074-1082. doi: 10.1017/S0953756299002294
12. Esquerré-Tugayé, M.-T., Boudart, G., and Dumas, B. (2000). Cell wall degrading enzymes, inhibitory proteins, and oligosaccharides participate in the molecular dialogue between plants and pathogens. Plant Physiol. Biochem. 38, 157-163. doi: 10.1016/S0981-9428(00)00161-3
13. Flicek, P., Amode, M. R., Barrell, D., Beal, K., Billis, K., Brent, S., et al. (2014). Ensembl 2014. Nucleic Acids Res. 42, D749-D755. doi: 10.1093/nar/gkt1196
14. Goodwin, S. B. (2007). Back to basics and beyond: increasing the level of resistance to Septoria tritici blotch in wheat. Australas. Plant Pathol. 36, 532-538. doi: 10.1071/AP07068
15. Goodwin, S. B., M'Barek, S. B., Dhillon, B., Wittenberg, A. H. J., Crane, C. F., Hane, J. K., et al. (2011). Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet. 7:e1002070. doi: 10.1371/journal.pgen.1002070
16. Goudemand, E., Laurent, V., Duchalais, L., Tabib Ghaffary, S. M., Kema, G. H. J., Lonnet, P., et al. (2013). Association mapping and meta-analysis: two complementary approaches for the detection of reliable Septoria tritici blotch quantitative resistance in bread wheat (Triticum aestivum L.). Mol. Breed. 32, 563-584. doi: 10.1007/s11032-013-9890-4
17. Hammond-Kosack, K., and Rudd, J. (2008). Plant resistance signaling hijacked by a necrotrophic fungal pathogen.Plant Signal. Behav. 3, 993-995. doi: 10.4161/psb.6292
18. Jørgensen, L. N., Hovmøller, M. S., Hansen, J. G., Lassen, P., Clark, B., Bayles, R., et al. (2014). IPM Strategies and Their dilemmas including an introduction to www.eurowheat.org. J. Integr. Agric. 13, 265-281. doi: 10.1016/S2095-3119(13)60646-2
19. Kellner, R., Bhattacharyya, A., Poppe, S., Hsu, T. Y., Brem, R. B., and Stukenbrock, E. H. (2014). Expression profiling of the wheat pathogen Zymoseptoria tritici reveals genomic patterns of transcription and host-specific regulatory programs. Genome Biol. Evol. 6, 1353-1365. doi: 10.1093/gbe/evu101
20. Kema, G., Yu, D., Rijkenberg, F., Shaw, M. W., and Baayen, R. P. (1996). Histology of the pathogenesis ofMycosphaerella graminicola in wheat. Phytopathology 86, 777-786. doi: 10.1094/Phyto-86-777
21. Kema, G. H., Verstappen, E. C., and Waalwijk, C. (2000). Avirulence in the wheat Septoria tritici leaf blotch fungusMycosphaerella graminicola is controlled by a single locus. Mol. Plant Microbe Interact. 13, 1375-1379. doi: 10.1094/MPMI.2000.13.12.1375
22. Keon, J., Antoniw, J., Carzaniga, R., Deller, S., Ward, J. L., Baker, J. M., et al. (2007). Transcriptional adaptation ofMycosphaerella graminicola to programmed cell death (PCD) of its susceptible wheat host. Mol. Plant Microbe Interact. 20, 178-193. doi: 10.1094/MPMI-20-2-0178
23. Keon, J., Rudd, J. J., Antoniw, J., Skinner, W., Hargreaves, J., and Hammond-Kosack, K. (2005). Metabolic and stress adaptation by Mycosphaerella graminicola during sporulation in its host revealed through microarray transcription profiling. Mol. Plant Pathol. 6, 527-540. doi: 10.1111/j.1364-3703.2005.00304.x
24. Lee, W.-S., Rudd, J. J., Hammond-Kosack, K. E., and Kanyuka, K. (2014). Mycosphaerella graminicola LysM effector-mediated stealth pathogenesis subverts recognition through both CERK1 and CEBiP homologues in wheat.Mol. Plant Microbe Interact. 27, 236-243. doi: 10.1094/MPMI-07-13-0201-R
25. Lendenmann, M. H., Croll, D., Stewart, E. L., and McDonald, B. A. (2014). Quantitative trait locus mapping of melanization in the plant pathogenic fungus Zymoseptoria tritici. G (Bethesda) 4, 2519-2533. doi: 10.1534/g3.114.015289
26. Ma, L.-J., van der Does, H. C., Borkovich, K. A., Coleman, J. J., Daboussi, M.-J., Di Pietro, A., et al. (2010). Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464, 367-373. doi: 10.1038/nature08850
27. Marshall, R., Kombrink, A., Motteram, J., Loza-Reyes, E., Lucas, J., Hammond-Kosack, K. E., et al. (2011). Analysis of two in planta expressed LysM effector homologs from the fungus Mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat. Plant Physiol. 156, 756-769. doi: 10.1104/pp.111.176347
28. Mehrabi, R., Makhdoomi, A., and Jafar-Aghaie, M. (2014). Identification of new sources of resistance to Septoria tritici blotch caused by Zymoseptoria tritici. J. Phytopathol. 163, 84-90. doi: 10.1111/jph.12282
29. Mehrabi, R., Taga, M., and Kema, G. H. J. (2007). Electrophoretic and cytological karyotyping of the foliar wheat pathogen Mycosphaerella graminicola reveals many chromosomes with a large size range. Mycologia 99, 868-876. doi: 10.3852/mycologia.99.6.868
30. Miao, V. P., Covert, S. F., and VanEtten, H. D. (1991). A fungal gene for antibiotic resistance on a dispensable ("B") chromosome. Science 254, 1773-1776. doi: 10.1126/science.1763326
31. Orton, E. S., Deller, S., and Brown, J. K. M. (2011). Mycosphaerella graminicola: from genomics to disease control.Mol. Plant Pathol. 12, 413-424. doi: 10.1111/j.1364-3703.2010.00688.x
32. Rudd, J. J., Kanyuka, K., Hassani-Pak, K., Derbyshire, M., Andogabo, A., Devonshire, J., et al. (2015). Transcriptome and metabolite profiling the infection cycle of Zymoseptoria tritici on wheat (Triticum aestivum) reveals a biphasic interaction with plant immunity involving differential pathogen chromosomal contributions, and a variation on the hemibiotrophic lifestyle definition. Plant Physiol. doi: 10.1104/pp.114.255927 [Epub ahead of print].
33. Stukenbrock, E. H., Banke, S., Javan-Nikkhah, M., and McDonald, B. A. (2007). Origin and domestication of the fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation. Mol. Biol. Evol. 24, 398-411. doi: 10.1093/molbev/msl169
34. Stukenbrock, E. H., Bataillon, T., Dutheil, J. Y., Hansen, T. T., Li, R., Zala, M., et al. (2011). The making of a new pathogen: insights from comparative population genomics of the domesticated wheat pathogen Mycosphaerella graminicola and its wild sister species. Genome Res. 21, 2157-2166. doi: 10.1101/gr.118851.110
35. Stukenbrock, E. H., Jørgensen, F. G., Zala, M., Hansen, T. T., McDonald, B. A., and Schierup, M. H. (2010). Whole-genome and chromosome evolution associated with host adaptation and speciation of the wheat pathogenMycosphaerella graminicola. PLoS Genet. 6:e1001189. doi: 10.1371/journal.pgen.1001189
36. Tabib Ghaffary, S. M., Faris, J. D., Friesen, T. L., Visser, R. G. F., van der Lee, T. A. J., Robert, O., et al. (2012). New broad-spectrum resistance to Septoria tritici blotch derived from synthetic hexaploid wheat. Theor. Appl. Genet.124, 125-142. doi: 10.1007/s00122-011-1692-7
37. Torriani, S. F., Brunner, P. C., McDonald, B. A., and Sierotzki, H. (2009). QoI resistance emerged independently at least 4 times in European populations of Mycosphaerella graminicola. Pest Manag. Sci. 65, 155-162. doi: 10.1002/ps.1662
38. Torriani, S. F. F., Stukenbrock, E. H., Brunner, P. C., McDonald, B. A., and Croll, D. (2011). Evidence for extensive recent intron transposition in closely related fungi. Curr. Biol. 21, 2017-2022. doi: 10.1016/j.cub.2011.10.041
39. Vorwerk, S., Somerville, S., and Somerville, C. (2004). The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci. 9, 203-209. doi: 10.1016/j.tplants.2004.02.005
40. Wittenberg, A. H. J., van der Lee, T. A. J., Ben M'Barek, S., Ware, S. B., Goodwin, S. B., Kilian, A., et al. (2009). Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. PLoS ONE 4:e5863. doi: 10.1371/journal.pone.0005863
41. Yang, F., Li, W., and Jørgensen, H. J. L. (2013). Transcriptional reprogramming of wheat and the hemibiotrophic pathogen Septoria tritici during two phases of the compatible interaction. PLoS ONE 8:e816061. doi: 10.1371/journal.pone.0081606