Genome Sequencing and Comparative Genomics of the Broad Host-Range Pathogen AG8

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The fungus Rhizoctonia solani is divided into several sub-species which cause disease in a range of plant species that includes most major agriculture, forestry and bioenergy species. This study focuses on sub-species AG8 which causes disease of cereals, canola and legumes, and compares its genome to other R. solani sub-species and a wide range of fungal and non-fungal species. R. solani is unusual in that it can possess more than one nucleus per cell. The multiple nuclei and sequence mutations between them made assembly of its genome challenging, and required novel techniques. We observed signs that DNA sequences originating from multiple nuclei in AG8 exhibit a high frequency of single nucleotide polymorphisms (SNPs) and more SNP diversity than most fungal populations. These SNP mutations also have similarities to repeat-induced point mutations (RIP). Moreover in AG8, RIP-like SNPs are not restricted to intergenic regions but are also widely observed in gene-coding regions. This is novel as RIP has previously only been reported in repetitive DNA of distantly-related fungi that have only a single nucleus per cell. We generated a list of 308 genes with similar properties to known plant-disease proteins, in which we found higher rates of non-synonymous mutations than normal.

Vyšlo v časopise: Genome Sequencing and Comparative Genomics of the Broad Host-Range Pathogen AG8. PLoS Genet 10(5): e32767. doi:10.1371/journal.pgen.1004281
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004281

Souhrn

Zdroje

1. Sneh B, Burpee L, Ogoshi A, editors(1991) Identification of Rhizoctonia species. St. Paul, Minnesota, USA: APS Press.

2. PaulitzTC (2006) Low input no-till cereal production in the Pacific Northwest of the US: The challenges of root diseases. Eur J Plant Pathol 115 : 271–281.

3. AndersonJP, SinghKB (2011) Interactions of Arabidopsis and M. truncatula with the same pathogens differ in dependence on ethylene and ethylene response factors. Plant Signal Behav 6 : 551–552.

4. BellDK, SumnerDR (1982) Virulence of Rhizoctonia solani Ag-2 Type-1 and Type-2 and Ag-4 from Peanut Seed on Corn, Sorghum, Lupine, Snapbean, Peanut and Soybean. Phytopathology 72 : 947–948.

5. SumnerDR, BellDK (1982) Crop-Rotation and Yield Loss in Corn in Soil Infested with Rhizoctonia solani Ag-2 and Ag-4. Phytopathology 72 : 361–362.

6. BradleyCA, HartmanGL, NelsonRL, MuellerDS, PedersenWL (2001) Response of ancestral soybean lines and commercial cultivars to Rhizoctonia root and hypocotyl rot. Plant Dis 85 : 1091–1095.

7. KluthC, BuhreC, VarrelmannM (2010) Susceptibility of intercrops to infection with Rhizoctonia solani AG 2-2 IIIB and influence on subsequently cultivated sugar beet. Plant Pathol 59 : 683–692.

8. KluthC, VarrelmannM (2010) Maize genotype susceptibility to Rhizoctonia solani and its effect on sugar beet crop rotations. Crop Prot 29 : 230–238.

9. GarciaVG, OncoMAP, SusanVR (2006) Review. Biology and systematics of the form genus Rhizoctonia. Span J Agric Res 4 : 55–79.

10. SharonM, KuninagaS, MyakumachiM, SnehB (2006) The advancing identification and classification of Rhizoctonia spp. using molecular and biotechnological methods compared with the classical anastomosis grouping. Mycoscience 47 : 299–316.

11. MurrayGM, BrennanJP (2009) Estimating disease losses to the Australian wheat industry. Australas Plant Pathol 38 : 558–570.

12. MurrayGM, BrennanJP (2010) Estimating disease losses to the Australian barley industry. Australas Plant Pathol 39 : 85–96.

13. SchroederKL, ShettyKK, PaulitzTC (2011) Survey of Rhizoctonia spp. from wheat soils in the US and determination of pathogenicity on wheat and barley. Phytopathology 101: S161–S161.

14. SweetinghamMW, CruickshankRH, WongDH (1986) Pectic zymograms and taxonomy and pathogenicity of the Ceratobasidiaceae. Mycol Res 86 : 305–311.

15. Sweetingham MW, MacNish GC, editors(1994) Rhizoctonia Isolation, Identification and Pathogenicity: A Laboratory Manual. 2nd ed. South Perth, WA, Australia: Department of Agriculture.

16. AndersonJP, LichtenzveigJ, GleasonC, OliverRP, SinghKB (2010) The B-3 ethylene response factor MtERF1-1 mediates resistance to a subset of root pathogens in Medicago truncatula without adversely affecting symbiosis with rhizobia. Plant Physiol 154 : 861–873.

17. FoleyRC, GleasonCA, AndersonJP, HamannT, SinghKB (2013) Genetic and genomic analysis of Rhizoctonia solani interactions with Arabidopsis; evidence of resistance mediated through NADPH oxidases. PLoS ONE 8: e56814.

18. KamperJ, KahmannR, BolkerM, MaLJ, BrefortT, et al. (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444 : 97–101.

19. LaurieJD, AliS, LinningR, MannhauptG, WongP, et al. (2012) Genome comparison of barley and maize smut fungi reveals targeted loss of RNA silencing components and species-specific presence of transposable elements. Plant Cell 24 : 1733–1745.

20. SchirawskiJ, MannhauptG, MunchK, BrefortT, SchipperK, et al. (2010) Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330 : 1546–1548.

21. CantuD, SegoviaV, MacleanD, BaylesR, ChenX, et al. (2013) Genome analyses of the wheat yellow (stripe) rust pathogen Puccinia striiformis f. sp. tritici reveal polymorphic and haustorial expressed secreted proteins as candidate effectors. BMC Genomics 14 : 270.

22. DuplessisS, CuomoCA, LinYC, AertsA, TisserantE, et al. (2011) Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci U S A 108 : 9166–9171.

23. MondegoJM, CarazzolleMF, CostaGG, FormighieriEF, ParizziLP, et al. (2008) A genome survey of Moniliophthora perniciosa gives new insights into Witches' Broom Disease of cacao. BMC Genomics 9 : 548.

24. RiouxR, ManmathanH, SinghP, de los ReyesB, JiaYL, et al. (2011) Comparative analysis of putative pathogenesis-related gene expression in two Rhizoctonia solani pathosystems. Curr Genet 57 : 391–408.

25. LakshmanDK, AlkharoufN, RobertsDP, NatarajanSS, MitraA (2012) Gene expression profiling of the plant pathogenic basidiomycetous fungus Rhizoctonia solani AG 4 reveals putative virulence factors. Mycologia 104 : 1020–1035.

26. ZhengA, LinR, ZhangD, QinP, XuL, et al. (2013) The evolution and pathogenic mechanisms of the rice sheath blight pathogen. Nat Commun 4 : 1424.

27. WibbergD, JelonekL, RuppO, HennigM, EikmeyerF, et al. (2012) Establishment and interpretation of the genome sequence of the phytopathogenic fungus Rhizoctonia solani AG1-IB isolate 7/3/14. J Biotechnol 167 : 142–155.

28. Losada L, Pakala SB, Fedorova ND, Joardar V, Shabalina SA, et al.. (2014) Mobile elements and mitochondrial genome expansion in the soil fungus and potato pathogen Rhizoctonia solani AG-3. FEMS Microbiol Lett In Press.

29. CubetaMA, DeanRA, ThomasE, BaymanP, JabajiS, et al. (2009) Rhizoctonia solani genome project: providing insight into a link between beneficial and plant pathogenic fungi. Phytopathology 99: S166.

30. LiuTH, LinMJ, KoWH (2010) Factors affecting protoplast formation by Rhizoctonia solani. N Biotechnol 27 : 64–69.

31. RobinsonHL, DeaconJW (2001) Protoplast preparation and transient transformation of Rhizoctonia solani. Mycol Res 105 : 1295–1303.

32. YangHA, SivasithamparamK, ObrienPA (1993) Improved Method for Protoplast Regeneration of Rhizoctonia solani. Soil Biol Biochem 25 : 633–636.

33. HaneJK, OliverRP (2010) In silico reversal of repeat-induced point mutation (RIP) identifies the origins of repeat families and uncovers obscured duplicated genes. BMC Genomics 11 : 655.

34. KeijerJ, HoutermanPM, DullemansAM, KorsmanMG (1996) Heterogeneity in electrophoretic karyotype within and between anastomosis groups of Rhizoctonia solani. Mycol Res 100 : 789–797.

35. HaneJK, RouxelT, HowlettBJ, KemaGH, GoodwinSB, et al. (2011) A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biol 12: R45.

36. MaLJ, van der DoesHC, BorkovichKA, ColemanJJ, DaboussiMJ, et al. (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464 : 367–373.

37. MuszewskaA, Hoffman-SommerM, GrynbergM (2011) LTR Retrotransposons in Fungi. PLoS ONE 6: e29425.

38. PetersenTN, BrunakS, von HeijneG, NielsenH (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8 : 785–786.

39. HortonP, ParkKJ, ObayashiT, FujitaN, HaradaH, et al. (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35: W585–W587.

40. KallL, KroghA, SonnhammerELL (2004) A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338 : 1027–1036.

41. AlvianoCS, TravassosLR, SchauerR (1999) Sialic acids in fungi: A minireview. Glycoconj J 16 : 545–554.

42. MavromatisK, ChuK, IvanovaN, HooperSD, MarkowitzVM, et al. (2009) Gene Context Analysis in the Integrated Microbial Genomes (IMG) Data Management System. PLoS ONE 4: e7979.

43. ZhaoZ, LiuH, WangC, XuJR (2013) Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 14 : 274.

44. CandyL, PeumansWJ, Menu-BouaouicheL, AstoulCH, Van DammeJ, et al. (2001) The Gal/GalNAc-specific lectin from the plant pathogenic basidiomycete Rhizoctonia solani is a member of the ricin-B family. Biochem Biophys Res Commun 282 : 655–661.

45. VachonV, LapradeR, SchwartzJL (2012) Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review. J Invertebr Pathol 111 : 1–12.

46. GrenierAM, DuportG, PagesS, CondemineG, RahbeY (2006) The phytopathogen Dickeya dadantii (Erwinia chrysanthemi 3937) is a pathogen of the pea aphid. Appl Environ Microbiol 72 : 1956–1965.

47. OlivaR, WinJ, RaffaeleS, BoutemyL, BozkurtTO, et al. (2010) Recent developments in effector biology of filamentous plant pathogens. Cell Microbiol 12 : 705–715.

48. KaleSD (2012) Oomycete and fungal effector entry, a microbial Trojan horse. New Phytol 193 : 874–881.

49. ClutterbuckAJ (2011) Genomic evidence of repeat-induced point mutation (RIP) in filamentous ascomycetes. Fungal Genet Biol 48 : 306–326.

50. Van de WouwAP, CozijnsenAJ, HaneJK, BrunnerPC, McDonaldBA, et al. (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.

51. HoodME, KatawczikM, GiraudT (2005) Repeat-induced point mutation and the population structure of transposable elements in Microbotryum violaceum. Genetics 170 : 1081–1089.

52. HornsF, PetitE, YocktengR, HoodME (2012) Patterns of repeat-induced point mutation in transposable elements of basidiomycete fungi. Genome Biol Evol 4 : 240–247.

53. NabelCS, ManningSA, KohliRM (2012) The curious chemical biology of cytosine: deamination, methylation, and oxidation as modulators of genomic potential. ACS Chem Biol 7 : 20–30.

54. MeerupatiT, AnderssonKM, FrimanE, KumarD, TunlidA, et al. (2013) Genomic mechanisms accounting for the adaptation to parasitism in nematode-trapping fungi. PLoS Genet 9: e1003909.

55. AuCH, CheungMK, WongMC, ChuAK, LawPT, et al. (2013) Rapid genotyping by low-coverage resequencing to construct genetic linkage maps of fungi: a case study in Lentinula edodes. BMC Res Notes 6 : 307.

56. HacquardS, KracherB, MaekawaT, VernaldiS, Schulze-LefertP, et al. (2013) Mosaic genome structure of the barley powdery mildew pathogen and conservation of transcriptional programs in divergent hosts. Proc Natl Acad Sci U S A 110: E2219–2228.

57. LinK, LimpensE, ZhangZ, IvanovS, SaundersDG, et al. (2014) Single Nucleus Genome Sequencing Reveals High Similarity among Nuclei of an Endomycorrhizal Fungus. PLoS Genet 10: e1004078.

58. OjedaDI, DhillonB, TsuiCK, HamelinRC (2013) Single-nucleotide polymorphism discovery in Leptographium longiclavatum, a mountain pine beetle-associated symbiotic fungus, using whole-genome resequencing. Mol Ecol Resour 14 : 401–410.

59. NeafseyDE, BarkerBM, SharptonTJ, StajichJE, ParkDJ, et al. (2010) Population genomic sequencing of Coccidioides fungi reveals recent hybridization and transposon control. Genome Res 20 : 938–946.

60. FreitagM, WilliamsRL, KotheGO, SelkerEU (2002) A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa. Proc Natl Acad Sci U S A 99 : 8802–8807.

61. MorrowCA, FraserJA (2013) Ploidy variation as an adaptive mechanism in human pathogenic fungi. Semin Cell Dev Biol 24 : 339–346.

62. KatariaHR, VermaPR, GisiU (1991) Variability in the Sensitivity of Rhizoctonia solani Anastomosis Groups to Fungicides. J Phytopathol 133 : 121–133.

63. MartinM (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal 17 : 10–12.

64. MagocT, SalzbergSL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27 : 2957–2963.

65. LiRQ, ZhuHM, RuanJ, QianWB, FangXD, et al. (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20 : 265–272.

66. BoetzerM, HenkelCV, JansenHJ, ButlerD, PirovanoW (2011) Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27 : 578–579.

67. HuangSF, ChenZL, HuangGR, YuT, YangP, et al. (2012) HaploMerger: Reconstructing allelic relationships for polymorphic diploid genome assemblies. Genome Res 22 : 1581–1588.

68. HuangXQ, MadanA (1999) CAP3: A DNA sequence assembly program. Genome Res 9 : 868–877.

69. AltschulSF, MaddenTL, SchafferAA, ZhangJH, ZhangZ, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 : 3389–3402.

70. LangmeadB, SalzbergSL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9 : 357–359.

71. McKennaA, HannaM, BanksE, SivachenkoA, CibulskisK, et al. (2010) The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20 : 1297–1303.

72. DanecekP, AutonA, AbecasisG, AlbersCA, BanksE, et al. (2011) The variant call format and VCFtools. Bioinformatics 27 : 2156–2158.

73. QuinlanAR, HallIM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26 : 841–842.

74. KurtzS, PhillippyA, DelcherAL, SmootM, ShumwayM, et al. (2004) Versatile and open software for comparing large genomes. Genome Biol 5: R12.

75. PriceAL, JonesNC, PevznerPA (2005) De novo identification of repeat families in large genomes. Bioinformatics 21: I351–I358.

76. Smit AFA, Hubley R, Green P (1996–2010) RepeatMasker Open-3.0. http://www.repeatmasker.org.

77. KohanyO, GentlesAJ, HankusL, JurkaJ (2006) Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics 7.

78. AbrusanG, GrundmannN, DeMesterL, MakalowskiW (2009) TEclass-a tool for automated classification of unknown eukaryotic transposable elements. Bioinformatics 25 : 1329–1330.

79. Haas BJ (2007–2011) TransposonPSI. http://transposonpsi.sourceforge.net.

80. JurkaJ, KapitonovVV, PavlicekA, KlonowskiP, KohanyO, et al. (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110 : 462–467.

81. TrapnellC, PachterL, SalzbergSL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25 : 1105–1111.

82. GrabherrMG, HaasBJ, YassourM, LevinJZ, ThompsonDA, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29 : 644–652.

83. MarcaisG, KingsfordC (2011) A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27 : 764–770.

84. HaasBJ, SalzbergSL, ZhuW, PerteaM, AllenJE, et al. (2008) Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biol 9: R7.

85. BorodovskyM, LomsadzeA (2011) Eukaryotic gene prediction using GeneMark.hmm-E and GeneMark-ES. Curr Protoc Bioinformatics Chapter 4 Unit 4.6.1-10.

86. WinnenburgR, BaldwinTK, UrbanM, RawlingsC, KohlerJ, et al. (2006) PHI-base: a new database for pathogen host interactions. Nucleic Acids Res 34: D459–D464.

87. HuangXQ, AdamsMD, ZhouH, KerlavageAR (1997) A tool for analyzing and annotating genomic sequences. Genomics 46 : 37–45.

88. LoweTM, EddySR (1997) tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25 : 955–964.

89. NawrockiEP, KolbeDL, EddySR (2009) Infernal 1.0: inference of RNA alignments. Bioinformatics 25 : 1335–1337.

90. LewisSE, SearleSM, HarrisN, GibsonM, LyerV, et al. (2002) Apollo: a sequence annotation editor. Genome Biol 3 research0082-0082.0014.

91. HusonDH, MitraS, RuscheweyhHJ, WeberN, SchusterSC (2011) Integrative analysis of environmental sequences using MEGAN4. Genome Res 21 : 1552–1560.

92. FinnRD, ClementsJ, EddySR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29–W37.

93. ParkBH, KarpinetsTV, SyedMH, LeuzeMR, UberbacherEC (2010) CAZymes Analysis Toolkit (CAT): Web service for searching and analyzing carbohydrate-active enzymes in a newly sequenced organism using CAZy database. Glycobiology 20 : 1574–1584.

94. KatohK, StandleyDM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30 : 772–780.

95. LechnerM, FindeissS, SteinerL, MarzM, StadlerPF, et al. (2011) Proteinortho: Detection of (co-)orthologs in large-scale analysis. BMC Bioinformatics 12 : 124.

96. StajichJE, BlockD, BoulezK, BrennerSE, ChervitzSA, et al. (2002) The Bioperl toolkit: Perl modules for the life sciences. Genome Res 12 : 1611–1618.

97. RiceP, LongdenI, BleasbyA (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16 : 276–277.

98. BaileyTL, BodenM, BuskeFA, FrithM, GrantCE, et al. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202–208.

99. CingolaniP, PlattsA, Wang leL, CoonM, NguyenT, et al. (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6 : 80–92.

100. RozenS, SkaletskyH (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132 : 365–386.

101. SchulerGD (1998) Electronic PCR: bridging the gap between genome mapping and genome sequencing. Trends Biotechnol 16 : 456–459.

102. AndersonJP, BadruzsaufariE, SchenkPM, MannersJM, DesmondOJ, et al. (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16 : 3460–3479.