Effector gene reshuffling involves dispensable mini-chromosomes in the wheat blast fungus

English version

Autoři: Zhao Peng ^aff001; Ely Oliveira-Garcia ^aff001; Guifang Lin ^aff001; Ying Hu ^aff001; Melinda Dalby ^aff001; Pierre Migeon ^aff001; Haibao Tang ^aff003; Mark Farman ^aff004; David Cook ^aff001; Frank F. White ^aff002; Barbara Valent ^aff001; Sanzhen Liu ^aff001
Působiště autorů: Department of Plant Pathology, Kansas State University, Manhattan, KS, United States of America ^aff001; Department of Plant Pathology, University of Florida, Gainesville, FL, United States of America ^aff002; Center for Genomics and Biotechnology and Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fujian, China ^aff003; Department of Plant Pathology, University of Kentucky, Lexington, KY, United States of America ^aff004
Vyšlo v časopise: Effector gene reshuffling involves dispensable mini-chromosomes in the wheat blast fungus. PLoS Genet 15(9): e32767. doi:10.1371/journal.pgen.1008272
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008272

Souhrn

Newly emerged wheat blast disease is a serious threat to global wheat production. Wheat blast is caused by a distinct, exceptionally diverse lineage of the fungus causing rice blast disease. Through sequencing a recent field isolate, we report a reference genome that includes seven core chromosomes and mini-chromosome sequences that harbor effector genes normally found on ends of core chromosomes in other strains. No mini-chromosomes were observed in an early field strain, and at least two from another isolate each contain different effector genes and core chromosome end sequences. The mini-chromosome is enriched in transposons occurring most frequently at core chromosome ends. Additionally, transposons in mini-chromosomes lack the characteristic signature for inactivation by repeat-induced point (RIP) mutation genome defenses. Our results, collectively, indicate that dispensable mini-chromosomes and core chromosomes undergo divergent evolutionary trajectories, and mini-chromosomes and core chromosome ends are coupled as a mobile, fast-evolving effector compartment in the wheat pathogen genome.

Klíčová slova:

Biology and life sciences – Organisms – Eukaryota – Plants – Grasses – Wheat – Rice – Fungi – Genetics – Genomics – Genome analysis – Sequence assembly tools – Mobile genetic elements – Transposable elements – Fungal genomics – Genetic elements – Fungal genetics – Computational biology – Mycology – Plant science – Plant pathology – Plant pathogens – Plant fungal pathogens – Rice blast fungus – Research and analysis methods – Animal studies – Experimental organism systems – Plant and algal models – Database and informatics methods – Bioinformatics – Sequence analysis – Sequence alignment

Zdroje

1. Cruz CD, Valent B (2017) Wheat blast disease: danger on the move. Tropical Plant Pathology 42: 210–222.

2. Kohli MM, Mehta YR, Guzman E, Viedma L, Cubilla LE (2011) Pyricularia blast—a threat to wheat cultivation. Czech Journal of Genetics and Plant Breeding 47: S130–S134.

3. Islam MT, Croll D, Gladieux P, Soanes DM, Persoons A, et al. (2016) Emergence of wheat blast in Bangladesh was caused by a South American lineage of Magnaporthe oryzae. BMC Biology 14: 84. doi: 10.1186/s12915-016-0309-7 27716181

4. Malaker PK, Barma NCD, Tiwari TP, W.J.Collis WJ, Duveiller E, et al. (2016) First report of wheat blast caused by Magnaporthe oryzae pathotype triticum in Bangladesh. Plant Disease 100: 2330

5. Mottaleb KA, Singh PK, Sonder K, Kruseman G, Tiwari TP, et al. (2018) Threat of wheat blast to South Asia’s food security: An ex-ante analysis. PLoS ONE 13: e0197555. doi: 10.1371/journal.pone.0197555 29782528

6. Gladieux P, Condon B, Ravel S, Soanes D, Nunes Maciel JL, et al. (2018) Gene flow between divergent cereal- and grass-specific lineages of the rice blast fungus Magnaporthe oryzae. mBio 9:e01219–17.

7. Farman M, Peterson GL, Chen L, Starnes JH, Valent B, et al. (2017) The Lolium pathotype of Magnaporthe oryzae recovered from a single blasted wheat plant in the United States. Plant Disease 101: 684–692. doi: 10.1094/PDIS-05-16-0700-RE 30678560

8. Giraldo MC, Valent B (2013) Filamentous plant pathogen effectors in action. Nature Reviews Microbiology 11: 800–814. doi: 10.1038/nrmicro3119 24129511

9. Wang B, Ebbole DJ, Wang Z (2017) The arms race between Magnaporthe oryzae and rice: diversity and interaction of Avr and R genes. Journal of Integrative Agriculture 16: 2746–2760.

10. Liu WD, Liu JL, Triplett L, Leach JE, Wang GL (2014) Novel insights into rice innate immunity against bacterial and fungal pathogens. Annual Review of Phytopathology 52: 213–241. doi: 10.1146/annurev-phyto-102313-045926 24906128

11. Kang S, Sweigard JA, Valent B (1995) The PWL host specificity gene family in the blast fungus Magnaporthe grisea. Molecular Plant Microbe Interactions 8: 939–948. 8664503

12. Sweigard JA, Carroll AM, Kang S, Farrall L, Chumley FG, et al. (1995) Identification, cloning, and characterization of Pwl2, a gene for host species-specificity in the rice blast fungus. The Plant Cell 7: 1221–1233. doi: 10.1105/tpc.7.8.1221 7549480

13. Inoue Y, Vy TTP, Yoshida K, Asano H, Mitsuoka C, et al. (2017) Evolution of the wheat blast fungus through functional losses in a host specificity determinant. Science 357: 80–83. doi: 10.1126/science.aam9654 28684523

14. Kroj T, Chanclud E, Michel‐Romiti C, Grand X, Morel JB (2016) Integration of decoy domains derived from protein targets of pathogen effectors into plant immune receptors is widespread. New Phytologist 210: 618–626. doi: 10.1111/nph.13869 26848538

15. Raffaele S, Kamoun S (2012) Genome evolution in filamentous plant pathogens: why bigger can be better. Nature Reviews Microbiology 10: 417–430. doi: 10.1038/nrmicro2790 22565130

16. Bertazzoni S, Williams AH, Jones DA, Syme RA, Tan KC, et al. (2018) Accessories make the outfit: Accessory chromosomes and other dispensable DNA regions in plant-pathogenic fungi. Molecular Plant Microbe Interactions 31: 779–788. doi: 10.1094/MPMI-06-17-0135-FI 29664319

17. Valent B, Khang CH (2010) Recent advances in rice blast effector research. Current Opinion in Plant Biology 13: 434–441. doi: 10.1016/j.pbi.2010.04.012 20627803

18. Chuma I, Isobe C, Hotta Y, Ibaragi K, Futamata N, et al. (2011) Multiple translocation of the AVR-Pita effector gene among chromosomes of the rice blast fungus Magnaporthe oryzae and related species. PLoS Pathogens 7: e1002147. doi: 10.1371/journal.ppat.1002147 21829350

19. Luo CX, Yin LF, Ohtaka K, Kusaba M (2007) The 1.6Mb chromosome carrying the avirulence gene AvrPik in Magnaporthe oryzae isolate 84R-62B is a chimera containing chromosome 1 sequences. Mycological Research 111: 232–239. doi: 10.1016/j.mycres.2006.10.008 17188484

20. Mehrabi R, Mirzadi Gohari A, Kema GHJ (2017) Karyotype variability in plant-pathogenic fungi. Annual Review of Phytopathology 55: 483–503. doi: 10.1146/annurev-phyto-080615-095928 28777924

21. Soyer JL, Balesdent M-H, Rouxel T, Dean RA (2018) To B or not to B: a tale of unorthodox chromosomes. Current Opinion in Microbiology 46: 50–57. doi: 10.1016/j.mib.2018.01.012 29579575

22. Chuma I, Tosa Y, Taga M, Nakayashiki H, Mayama S (2003) Meiotic behavior of a supernumerary chromosome in Magnaporthe oryzae. Current Genetics 43: 191–198. doi: 10.1007/s00294-003-0390-7 12764669

23. Orbach MJ, Chumley FG, Valent B (1996) Electrophoretic karyotypes of Magnaporthe grisea pathogens of diverse grasses. Molecular Plant Microbe Interactions 9: 261–271.

24. Talbot NJ, Salch YP, Ma M, Hamer JE (1993) Karyotypic variability within clonal lineages of the rice blast fungus, Magnaporthe grisea. Applied and Environmental Microbiology 59: 585–593. 16348876

25. Yoshida K, Saunders DG, Mitsuoka C, Natsume S, Kosugi S, et al. (2016) Host specialization of the blast fungus Magnaporthe oryzae is associated with dynamic gain and loss of genes linked to transposable elements. BMC Genomics 17: 370. doi: 10.1186/s12864-016-2690-6 27194050

26. Cruz CD, Peterson GL, Bockus WW, Kankanala P, Dubcovsky J, et al. (2016) The 2NS translocation from Aegilops ventricosa confers resistance to the Triticum Pathotype of Magnaporthe oryzae. Crop Science 56: 990–1000. doi: 10.2135/cropsci2015.07.0410 27814405

27. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, et al. (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434: 980–986. doi: 10.1038/nature03449 15846337

28. Starnes JH, Thornbury DW, Novikova OS, Rehmeyer CJ, Farman ML (2012) Telomere-targeted retrotransposons in the rice blast fungus Magnaporthe oryzae: agents of telomere instability. Genetics 191: 389–406. doi: 10.1534/genetics.111.137950 22446319

29. Bao J, Chen M, Zhong Z, Tang W, Lin L, et al. (2017) PacBio sequencing reveals transposable element as a key contributor to genomic plasticity and virulence variation in Magnaporthe oryzae. Molecular Plant 10: 1465–1468. doi: 10.1016/j.molp.2017.08.008 28838703

30. Zhang S, Wang L, Wu W, He L, Yang X, et al. (2015) Function and evolution of Magnaporthe oryzae avirulence gene AvrPib responding to the rice blast resistance gene Pib. Scientific Reports 5: 11642. doi: 10.1038/srep11642 26109439

31. Li W, Wang B, Wu J, Lu G, Hu Y, et al. (2009) The Magnaporthe oryzae avirulence gene AvrPiz-t encodes a predicted secreted protein that triggers the immunity in rice mediated by the blast resistance gene Piz-t. Molecular Plant Microbe Interactions 22: 411–420. doi: 10.1094/MPMI-22-4-0411 19271956

32. Mosquera G, Giraldo MC, Khang CH, Coughlan S, Valent B (2009) Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1-4 as biotrophy-associated secreted proteins in rice blast disease. Plant Cell 21: 1273–1290. doi: 10.1105/tpc.107.055228 19357089

33. Tosa Y, Osue J, Eto Y, Oh HS, Nakayashiki H, et al. (2005) Evolution of an avirulence gene, AVR1-CO39, concomitant with the evolution and differentiation of Magnaporthe oryzae. Mol Plant Microbe Interact 18: 1148–1160. doi: 10.1094/MPMI-18-1148 16353550

34. Zheng Y, Zheng W, Lin F, Zhang Y, Yi Y, et al. (2011) AVR1-CO39 is a predominant locus governing the broad avirulence of Magnaporthe oryzae 2539 on cultivated rice (Oryza sativa L.). Mol Plant Microbe Interact 24: 13–17. doi: 10.1094/MPMI-10-09-0240 20879839

35. Brown DW, Busman M, Proctor RH (2014) Fusarium verticillioides SGE1 is required for full virulence and regulates expression of protein effector and secondary metabolite biosynthetic genes. Mol Plant Microbe Interact 27: 809–823. doi: 10.1094/MPMI-09-13-0281-R 24742071

36. Kanzaki H, Yoshida K, Saitoh H, Fujisaki K, Hirabuchi A, et al. (2012) Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions. Plant Journal 72: 894–907. doi: 10.1111/j.1365-313X.2012.05110.x 22805093

37. Gladyshev E (2017) Repeat-induced point mutation and other genome defense mechanisms in fungi. Microbiology Spectrum 5: doi: 10.1128/microbiolspec.FUNK-0042-2017 28721856

38. Ikeda K, Nakayashiki H, Kataoka T, Tamba H, Hashimoto Y, et al. (2002) Repeat-induced point mutation (RIP) in Magnaporthe grisea: implications for its sexual cycle in the natural field context. Molecular Microbiology 45: 1355–1364. doi: 10.1046/j.1365-2958.2002.03101.x 12207702

39. Nakayashiki H, Nishimoto N, Ikeda K, Tosa Y, Mayama S (1999) Degenerate MAGGY elements in a subgroup of Pyricularia grisea: a possible example of successful capture of a genetic invader by a fungal genome. Molecular and General Genetics 261: 958–966. doi: 10.1007/s004380051044 10485287

40. Hane JK, Oliver RP (2008) RIPCAL: a tool for alignment-based analysis of repeat-induced point mutations in fungal genomic sequences. BMC Bioinformatics 9: 478. doi: 10.1186/1471-2105-9-478 19014496

41. Coleman JJ, Rounsley SD, Rodriguez-Carres M, Kuo A, Wasmann CC, et al. (2009) The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genetics 5: e1000618. doi: 10.1371/journal.pgen.1000618 19714214

42. Ma L-J, van der Does HC, Borkovich KA, Coleman JJ, Daboussi M-J, et al. (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367–373. doi: 10.1038/nature08850 20237561

43. Croll D, Zala M, McDonald BA (2013) Breakage-fusion-bridge cycles and large insertions contribute to the rapid evolution of accessory chromosomes in a fungal pathogen. PLoS Genetics 9: 20.

44. Goodwin SB, Ben M'Barek S, Dhillon B, Wittenberg AHJ, Crane CF, et al. (2011) Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genetics 7: e1002070. doi: 10.1371/journal.pgen.1002070 21695235

45. Balesdent MH, Fudal I, Ollivier B, Bally P, Grandaubert J, et al. (2013) The dispensable chromosome of Leptosphaeria maculans shelters an effector gene conferring avirulence towards Brassica rapa. New Phytol 198: 887–898. doi: 10.1111/nph.12178 23406519

46. Moller M, Stukenbrock EH (2017) Evolution and genome architecture in fungal plant pathogens. Nature Reviews Microbiology 15: 756–771. doi: 10.1038/nrmicro.2017.76 28781365

47. Vanheule A, Audenaert K, Warris S, van de Geest H, Schijlen E, et al. (2016) Living apart together: crosstalk between the core and supernumerary genomes in a fungal plant pathogen. BMC Genomics 17: 670. doi: 10.1186/s12864-016-2941-6 27552804

48. Daverdin G, Rouxel T, Gout L, Aubertot JN, Fudal I, et al. (2012) Genome structure and reproductive behaviour influence the evolutionary potential of a fungal phytopathogen. PLoS Pathogens 8: 15.

49. Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP, et al. (2011) Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations. Nature Communications 2: 202. doi: 10.1038/ncomms1189 21326234

50. Faino L, Seidl MF, Shi-Kunne X, Pauper M, van den Berg GC, et al. (2016) Transposons passively and actively contribute to evolution of the two-speed genome of a fungal pathogen. Genome Research 26: 1091–1100. doi: 10.1101/gr.204974.116 27325116

51. Khang CH, Park SY, Lee YH, Valent B, Kang S (2008) Genome organization and evolution of the AVR-Pita avirulence gene family in the Magnaporthe grisea species complex. Molecular Plant Microbe Interactions 21: 658–670. doi: 10.1094/MPMI-21-5-0658 18393625

52. Orbach MJ, Farrall L, Sweigard JA, Chumley FG, Valent B (2000) A telomeric avirulence gene AVR-Pita determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell 12: 2019–2032. doi: 10.1105/tpc.12.11.2019 11090206

53. Habig M, Kema GH, Holtgrewe Stukenbrock E (2018) Meiotic drive of female-inherited supernumerary chromosomes in a pathogenic fungus. Elife 7.

54. Dong Y, Li Y, Zhao M, Jing M, Liu X, et al. (2015) Global genome and transcriptome analyses of Magnaporthe oryzae epidemic isolate 98–06 uncover novel effectors and pathogenicity-related genes, revealing gene gain and lose dynamics in genome evolution. PLoS Pathog 11: e1004801. doi: 10.1371/journal.ppat.1004801 25837042

55. Zhang MP, Zhang Y, Scheuring CF, Wu CC, Dong JJ, et al. (2012) Preparation of megabase-sized DNA from a variety of organisms using the nuclei method for advanced genomics research. Nature Protocols 7: 467–478. doi: 10.1038/nprot.2011.455 22343429

56. Clarke JD (2009) Cetyltrimethyl ammonium bromide (CTAB) DNA miniprep for plant DNA isolation. Cold Spring Harbor Protocols 2009: pdb.prot5177.

57. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH, et al. (2017) Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Research 27: 722–736. doi: 10.1101/gr.215087.116 28298431

58. Weisenfeld NI, Yin S, Sharpe T, Lau B, Hegarty R, et al. (2014) Comprehensive variation discovery in single human genomes. Nature Genetics 46: 1350–1355. doi: 10.1038/ng.3121 25326702

59. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W (2011) Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27: 578–579. doi: 10.1093/bioinformatics/btq683 21149342

60. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29: 644–U130. doi: 10.1038/nbt.1883 21572440

61. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, et al. (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29: 15–21. doi: 10.1093/bioinformatics/bts635 23104886

62. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15: 550. doi: 10.1186/s13059-014-0550-8 25516281

63. Benjamini Y, Hochberg Y (1995) Controlling the False Discovery Rate—a Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B-Methodological 57: 289–300.

64. Cantarel BL, Korf I, Robb SM, Parra G, Ross E, et al. (2008) MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Research 18: 188–196. doi: 10.1101/gr.6743907 18025269

65. Salamov AA, Solovyev VV (2000) Ab initio gene finding in Drosophila genomic DNA. Genome Research 10: 516–522. doi: 10.1101/gr.10.4.516 10779491

66. Parra G, Bradnam K, Ning Z, Keane T, Korf I (2009) Assessing the gene space in draft genomes. Nucleic Acids Research 37: 289–297. doi: 10.1093/nar/gkn916 19042974

67. Nielsen H (2017) Predicting secretory proteins with SignalP. Methods Mol Biology 1611: 59–73.

68. Olshen AB, Venkatraman ES, Lucito R, Wigler M (2004) Circular binary segmentation for the analysis of array-based DNA copy number data. Biostatistics 5: 557–572. doi: 10.1093/biostatistics/kxh008 15475419

69. Lee H, Lee M, Mohammed Ismail W, Rho M, Fox GC, et al. (2016) MGEScan: a Galaxy-based system for identifying retrotransposons in genomes. Bioinformatics 32: 2502–2504. doi: 10.1093/bioinformatics/btw157 27153595

70. Xu Z, Wang H (2007) LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Research 35: W265–268. doi: 10.1093/nar/gkm286 17485477

71. Ellinghaus D, Kurtz S, Willhoeft U (2008) LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics 9: 18. doi: 10.1186/1471-2105-9-18 18194517

72. Gremme G, Steinbiss S, Kurtz S (2013) GenomeTools: a comprehensive software library for efficient processing of structured genome annotations. IEEE/ACM Trans Comput Biol Bioinform 10: 645–656. doi: 10.1109/TCBB.2013.68 24091398

73. Bao W, Kojima KK, Kohany O (2015) Repbase Update, a database of repetitive elements in eukaryotic genomes. Mobile DNA 6: 11. doi: 10.1186/s13100-015-0041-9 26045719