1887

Abstract

is a fungal pathogen that causes leaf mould of tomato. The reference genome of this pathogen was released in 2012 but its high repetitive DNA content prevented a contiguous assembly and further prohibited the analysis of its genome architecture. In this study, we combined third generation sequencing technology with the Hi-C chromatin conformation capture technique, to produce a high-quality and near complete genome assembly and gene annotation of a Race 5 isolate of . The resulting genome assembly contained 67.17 Mb organized into 14 chromosomes (Chr1-to-Chr14), all of which were assembled telomere-to-telomere. The smallest of the chromosomes, Chr14, is only 460 kb in size and contains 25 genes that all encode hypothetical proteins. Notably, PCR assays revealed that Chr14 was absent in 19 out of 24 isolates of a world-wide collection of , indicating that Chr14 is dispensable. Thus, is currently the second species of Capnodiales shown to harbour dispensable chromosomes. The genome of Race 5 is 49.7 % repetitive and contains 14 690 predicted genes with an estimated completeness of 98.9%, currently one of the highest among the Capnodiales. Genome structure analysis revealed a compartmentalized architecture composed of gene-dense and repeat-poor regions interspersed with gene-sparse and repeat-rich regions. Nearly 39.2 % of the Race 5 genome is affected by Repeat-Induced Point (RIP) mutations and evidence of RIP leakage toward non-repetitive regions was observed in all chromosomes, indicating the RIP plays an important role in the evolution of this pathogen. Finally, 345 genes encoding candidate effectors were identified in Race 5, with a significant enrichment of their location in gene-sparse regions, in accordance with the ‘two-speed genome’ model of evolution. Overall, the new reference genome of presents several notable features and is a valuable resource for studies in plant pathogens.

Funding
This study was supported by the:
  • University of California, Davis (Award Dean’s Distinguished Graduate Fellowship (DDGF) program)
    • Principle Award Recipient: AlexZanella Zaccaron
  • USDA-NIFA (Award CA-D-PPA-2185-H)
    • Principle Award Recipient: IoannisStergiopoulos
  • Directorate for Biological Sciences (Award 1557995)
    • Principle Award Recipient: IoannisStergiopoulos
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2022-04-26
2024-05-13
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References

  1. Haridas S, Albert R, Binder M, Bloem J, LaButti K et al. 101 Dothideomycetes genomes: A test case for predicting lifestyles and emergence of pathogens. Stud Mycol 2020; 96:141–153 [View Article] [PubMed]
    [Google Scholar]
  2. Salzberg SL, Yorke JA. Beware of mis-assembled genomes. Bioinformatics 2005; 21:4320–4321 [View Article] [PubMed]
    [Google Scholar]
  3. Treangen TJ, Salzberg SL. Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat Rev Genet 2011; 13:36–46 [View Article] [PubMed]
    [Google Scholar]
  4. Castanera R, López-Varas L, Borgognone A, LaButti K, Lapidus A et al. Transposable elements versus the fungal genome: impact on whole-genome architecture and transcriptional profiles. PLoS Genet 2016; 12:e1006108 [View Article] [PubMed]
    [Google Scholar]
  5. Guo X, Zhang R, Li Y, Wang Z, Ishchuk OP et al. Understand the genomic diversity and evolution of fungal pathogen Candida glabrata by genome-wide analysis of genetic variations. Methods 2020; 176:82–90 [View Article] [PubMed]
    [Google Scholar]
  6. Möller M, Habig M, Freitag M, Stukenbrock EH. Extraordinary Genome Instability and Widespread Chromosome Rearrangements During Vegetative Growth. Genetics 2018; 210:517–529 [View Article] [PubMed]
    [Google Scholar]
  7. Muszewska A, Steczkiewicz K, Stepniewska-Dziubinska M, Ginalski K. Transposable elements contribute to fungal genes and impact fungal lifestyle. Sci Rep 2019; 9:1–10 [View Article] [PubMed]
    [Google Scholar]
  8. Plissonneau C, Benevenuto J, Mohd-Assaad N, Fouché S, Hartmann FE et al. Using population and comparative genomics to understand the genetic basis of effector-driven fungal pathogen evolution. Front Plant Sci 2017; 8:119 [View Article] [PubMed]
    [Google Scholar]
  9. Covo S. Genomic Instability in Fungal Plant Pathogens. Genes (Basel) 2020; 11:E421 [View Article] [PubMed]
    [Google Scholar]
  10. Miyauchi S, Kiss E, Kuo A, Drula E, Kohler A et al. Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits. Nat Commun 2020; 11:1–17 [View Article] [PubMed]
    [Google Scholar]
  11. Möller M, Stukenbrock EH. Evolution and genome architecture in fungal plant pathogens. Nat Rev Microbiol 2017; 15:756–771 [View Article] [PubMed]
    [Google Scholar]
  12. Houben A, Banaei-Moghaddam AM, Klemme S, Timmis JN. Evolution and biology of supernumerary B chromosomes. Cell Mol Life Sci 2014; 71:467–478 [View Article] [PubMed]
    [Google Scholar]
  13. Bertazzoni S, Williams AH, Jones DA, Syme RA, Tan K-C et al. Accessories Make the Outfit: Accessory Chromosomes and Other Dispensable DNA Regions in Plant-Pathogenic Fungi. Mol Plant Microbe Interact 2018; 31:779–788 [View Article] [PubMed]
    [Google Scholar]
  14. Goodwin SB, M’barek SB, Dhillon B, Wittenberg AHJ, Crane CF et al. Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet 2011; 7:e1002070 [View Article]
    [Google Scholar]
  15. Li J, Fokkens L, van Dam P, Rep M. Related mobile pathogenicity chromosomes in Fusarium oxysporum determine host range on cucurbits. Mol Plant Pathol 2020; 21:761–776 [View Article] [PubMed]
    [Google Scholar]
  16. Ma L-J, van der Does HC, Borkovich KA, Coleman JJ, Daboussi M-J et al. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 2010; 464:367–373 [View Article] [PubMed]
    [Google Scholar]
  17. Tsuge T, Harimoto Y, Akimitsu K, Ohtani K, Kodama M et al. Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata. FEMS Microbiol Rev 2013; 37:44–66 [View Article] [PubMed]
    [Google Scholar]
  18. Wang M, Fu H, Shen X-X, Ruan R, Rokas A et al. Genomic features and evolution of the conditionally dispensable chromosome in the tangerine pathotype of Alternaria alternata. Mol Plant Pathol 2019; 20:1425–1438 [View Article] [PubMed]
    [Google Scholar]
  19. Witte TE, Villeneuve N, Boddy CN, Overy DP. Accessory Chromosome-Acquired Secondary Metabolism in Plant Pathogenic Fungi: The Evolution of Biotrophs Into Host-Specific Pathogens. Front Microbiol 2021; 12:664276 [View Article] [PubMed]
    [Google Scholar]
  20. van Dam P, Fokkens L, Ayukawa Y, van der Gragt M, Ter Horst A et al. A mobile pathogenicity chromosome in Fusarium oxysporum for infection of multiple cucurbit species. Sci Rep 2017; 7:1–15 [View Article] [PubMed]
    [Google Scholar]
  21. Wijayawardene NN, Hyde KD, Rajeshkumar KC, Hawksworth DL, Madrid H et al. Notes for genera: Ascomycota. Fungal Divers 2017; 86:1–594 [View Article]
    [Google Scholar]
  22. Hane JK, Rouxel T, Howlett BJ, Kema GHJ, Goodwin SB et al. A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biol 2011; 12:1–16 [View Article] [PubMed]
    [Google Scholar]
  23. Ohm RA, Feau N, Henrissat B, Schoch CL, Horwitz BA et al. Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog 2012; 8:e1003037 [View Article] [PubMed]
    [Google Scholar]
  24. Dong S, Raffaele S, Kamoun S. The two-speed genomes of filamentous pathogens: waltz with plants. Curr Opin Genet Dev 2015; 35:57–65 [View Article] [PubMed]
    [Google Scholar]
  25. Raffaele S, Kamoun S. Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol 2012; 10:417–430 [View Article] [PubMed]
    [Google Scholar]
  26. Stergiopoulos I, de Wit PJGM. Fungal effector proteins. Annu Rev Phytopathol 2009; 47:233–263 [View Article] [PubMed]
    [Google Scholar]
  27. Dutheil JY, Mannhaupt G, Schweizer G, M K Sieber C, Münsterkötter M et al. A Tale of Genome Compartmentalization: The Evolution of Virulence Clusters in Smut Fungi. Genome Biol Evol 2016; 8:681–704 [View Article] [PubMed]
    [Google Scholar]
  28. Navarrete F, Grujic N, Stirnberg A, Saado I, Aleksza D et al. The Pleiades are a cluster of fungal effectors that inhibit host defenses. PLoS Pathog 2021; 17:e1009641 [View Article] [PubMed]
    [Google Scholar]
  29. Gan P, Hiroyama R, Tsushima A, Masuda S, Shibata A et al. Telomeres and a repeat-rich chromosome encode effector gene clusters in plant pathogenic Colletotrichum fungi. Environ Microbiol 2021; 23:6004–6018 [View Article] [PubMed]
    [Google Scholar]
  30. Tsushima A, Gan P, Kumakura N, Narusaka M, Takano Y et al. Genomic Plasticity Mediated by Transposable Elements in the Plant Pathogenic Fungus Colletotrichum higginsianum. Genome Biol Evol 2019; 11:1487–1500 [View Article] [PubMed]
    [Google Scholar]
  31. Depotter JRL, Shi-Kunne X, Missonnier H, Liu T, Faino L et al. Dynamic virulence-related regions of the plant pathogenic fungus Verticillium dahliae display enhanced sequence conservation. Mol Ecol 2019; 28:3482–3495 [View Article] [PubMed]
    [Google Scholar]
  32. Grandaubert J, Lowe RGT, Soyer JL, Schoch CL, Van de Wouw AP et al. Transposable element-assisted evolution and adaptation to host plant within the Leptosphaeria maculans-Leptosphaeria biglobosa species complex of fungal pathogens. BMC Genomics 2014; 15:1–27 [View Article] [PubMed]
    [Google Scholar]
  33. Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP et al. Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat-induced point mutations. Nat Commun 2011; 2:1–10 [View Article]
    [Google Scholar]
  34. Frantzeskakis L, Kusch S, Panstruga R. The need for speed: compartmentalized genome evolution in filamentous phytopathogens. Mol Plant Pathol 2019; 20:3–7 [View Article] [PubMed]
    [Google Scholar]
  35. Croll D, McDonald BA. The accessory genome as a cradle for adaptive evolution in pathogens. PLoS Pathog 2012; 8:e1002608 [View Article] [PubMed]
    [Google Scholar]
  36. Schrader L, Schmitz J. The impact of transposable elements in adaptive evolution. Mol Ecol 2019; 28:1537–1549 [View Article] [PubMed]
    [Google Scholar]
  37. Iida Y, van’t Hof P, Beenen H, Mesarich C, Kubota M et al. Novel Mutations Detected in Avirulence Genes Overcoming Tomato Cf Resistance Genes in Isolates of a Japanese Population of Cladosporium fulvum. PLoS One 2015; 10:e0123271 [View Article] [PubMed]
    [Google Scholar]
  38. Stergiopoulos I, De Kock MJD, Lindhout P, De Wit PJGM. Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution. Mol Plant Microbe Interact 2007; 20:1271–1283 [View Article] [PubMed]
    [Google Scholar]
  39. Wu J, Kou Y, Bao J, Li Y, Tang M et al. Comparative genomics identifies the Magnaporthe oryzae avirulence effector AvrPi9 that triggers Pi9-mediated blast resistance in rice. New Phytol 2015; 206:1463–1475 [View Article] [PubMed]
    [Google Scholar]
  40. McDonald MC, Taranto AP, Hill E, Schwessinger B, Liu Z et al. Transposon-Mediated Horizontal Transfer of the Host-Specific Virulence Protein ToxA between Three Fungal Wheat Pathogens. mBio 2019; 10:e01515-19 [View Article] [PubMed]
    [Google Scholar]
  41. Clutterbuck AJ. Genomic evidence of repeat-induced point mutation (RIP) in filamentous ascomycetes. Fungal Genet Biol 2011; 48:306–326 [View Article] [PubMed]
    [Google Scholar]
  42. Selker EU. Premeiotic instability of repeated sequences in Neurospora crassa. Annu Rev Genet 1990; 24:579–613 [View Article] [PubMed]
    [Google Scholar]
  43. Selker EU, Garrett PW. DNA sequence duplications trigger gene inactivation in Neurospora crassa. Proc Natl Acad Sci U S A 1988; 85:6870–6874 [View Article] [PubMed]
    [Google Scholar]
  44. Thomma BPHJ, VAN Esse HP, Crous PW, DE Wit PJGM. Cladosporium fulvum (syn. Passalora fulva), a highly specialized plant pathogen as a model for functional studies on plant pathogenic Mycosphaerellaceae. Mol Plant Pathol 2005; 6:379–393 [View Article] [PubMed]
    [Google Scholar]
  45. De Wit PJ, Joosten MH, Thomma BH, Stergiopoulos I. Gene for gene models and beyond: the Cladosporium fulvum-Tomato pathosystem. In Plant Relationships Springer; 2009 pp 135–156
    [Google Scholar]
  46. Joosten M, de Wit P. THE TOMATO-CLADOSPORIUM FULVUM INTERACTION: A Versatile Experimental System to Study Plant-Pathogen Interactions. Annu Rev Phytopathol 1999; 37:335–367 [View Article] [PubMed]
    [Google Scholar]
  47. van Kan JA, van den Ackerveken GF, de Wit PJ. Cloning and characterization of cDNA of avirulence gene avr9 of the fungal pathogen Cladosporium fulvum, causal agent of tomato leaf mold. Mol Plant Microbe Interact 1991; 4:52–59 [View Article] [PubMed]
    [Google Scholar]
  48. de Wit PJGM. Cladosporium fulvum Effectors: Weapons in the Arms Race with Tomato. Annu Rev Phytopathol 2016; 54:1–23 [View Article] [PubMed]
    [Google Scholar]
  49. de Wit PJGM, van der Burgt A, Ökmen B, Stergiopoulos I, Abd-Elsalam KA et al. The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genet 2012; 8:e1003088 [View Article] [PubMed]
    [Google Scholar]
  50. Eid J, Fehr A, Gray J, Luong K, Lyle J et al. Real-time DNA sequencing from single polymerase molecules. Science 2009; 323:133–138 [View Article] [PubMed]
    [Google Scholar]
  51. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009; 326:289–293 [View Article] [PubMed]
    [Google Scholar]
  52. Stergiopoulos I, Groenewald M, Staats M, Lindhout P, Crous PW et al. Mating-type genes and the genetic structure of a world-wide collection of the tomato pathogen Cladosporium fulvum. Fungal Genet Biol 2007; 44:415–429 [View Article] [PubMed]
    [Google Scholar]
  53. Jones A, Nagar R, Sharp A, Schwessinger B. High-molecular weight DNA extraction from challenging fungi using CTAB and gel purification v2 2019 [View Article]
    [Google Scholar]
  54. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH et al. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res 2017; 27:722–736 [View Article] [PubMed]
    [Google Scholar]
  55. Bushnell B. BBMap: a fast, accurate, splice-aware aligner Berkeley, CA: Lawrence Berkeley National Lab (LBNL); 2014
    [Google Scholar]
  56. Torriani SFF, Goodwin SB, Kema GHJ, Pangilinan JL, McDonald BA. Intraspecific comparison and annotation of two complete mitochondrial genome sequences from the plant pathogenic fungus Mycosphaerella graminicola. Fungal Genet Biol 2008; 45:628–637 [View Article] [PubMed]
    [Google Scholar]
  57. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018; 34:i884–i890 [View Article] [PubMed]
    [Google Scholar]
  58. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article] [PubMed]
    [Google Scholar]
  59. Faust GG, Hall IM. SAMBLASTER: fast duplicate marking and structural variant read extraction. Bioinformatics 2014; 30:2503–2505 [View Article] [PubMed]
    [Google Scholar]
  60. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article] [PubMed]
    [Google Scholar]
  61. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article] [PubMed]
    [Google Scholar]
  62. Dudchenko O, Batra SS, Omer AD, Nyquist SK, Hoeger M et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science 2017; 356:92–95 [View Article] [PubMed]
    [Google Scholar]
  63. Durand NC, Robinson JT, Shamim MS, Machol I, Mesirov JP et al. Juicebox Provides a Visualization System for Hi-C Contact Maps with Unlimited Zoom. Cell Syst 2016; 3:99–101 [View Article] [PubMed]
    [Google Scholar]
  64. Sedlazeck FJ, Rescheneder P, Smolka M, Fang H, Nattestad M et al. Accurate detection of complex structural variations using single-molecule sequencing. Nat Methods 2018; 15:461–468 [View Article] [PubMed]
    [Google Scholar]
  65. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES et al. Integrative genomics viewer. Nat Biotechnol 2011; 29:24–26 [View Article] [PubMed]
    [Google Scholar]
  66. Pedersen BS, Quinlan AR. Mosdepth: quick coverage calculation for genomes and exomes. Bioinformatics 2018; 34:867–868 [View Article] [PubMed]
    [Google Scholar]
  67. Flynn JM, Hubley R, Goubert C, Rosen J, Clark AG et al. RepeatModeler2 for automated genomic discovery of transposable element families. Proc Natl Acad Sci U S A 2020; 117:9451–9457 [View Article] [PubMed]
    [Google Scholar]
  68. van Wyk S, Harrison CH, Wingfield BD, De Vos L, van der Merwe NA et al. The RIPper, a web-based tool for genome-wide quantification of Repeat-Induced Point (RIP) mutations. PeerJ 2019; 7:e7447 [View Article] [PubMed]
    [Google Scholar]
  69. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods 2015; 12:357–360 [View Article] [PubMed]
    [Google Scholar]
  70. Pertea M, Pertea GM, Antonescu CM, Chang T-C, Mendell JT et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 2015; 33:290–295 [View Article] [PubMed]
    [Google Scholar]
  71. Cantarel BL, Korf I, Robb SMC, Parra G, Ross E et al. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 2008; 18:188–196 [View Article] [PubMed]
    [Google Scholar]
  72. Stanke M, Keller O, Gunduz I, Hayes A, Waack S et al. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res 2006; 34:W435–9 [View Article] [PubMed]
    [Google Scholar]
  73. Korf I. Gene finding in novel genomes. BMC Bioinformatics 2004; 5:1–9 [View Article] [PubMed]
    [Google Scholar]
  74. Keilwagen J, Hartung F, Grau J. GeMoMa: Homology-Based Gene Prediction Utilizing Intron Position Conservation and RNA-seq Data. Methods Mol Biol 2019; 1962:161–177 [View Article] [PubMed]
    [Google Scholar]
  75. Hoff KJ, Lomsadze A, Borodovsky M, Stanke M. Whole-Genome Annotation with BRAKER. Methods Mol Biol 2019; 1962:65–95 [View Article] [PubMed]
    [Google Scholar]
  76. Ter-Hovhannisyan V, Lomsadze A, Chernoff YO, Borodovsky M. Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res 2008; 18:1979–1990 [View Article] [PubMed]
    [Google Scholar]
  77. Feng Y-Y, Ramu A, Cotto KC, Skidmore ZL, Kunisaki J et al. RegTools: integrated analysis of genomic and transcriptomic data for discovery of splicing variants in cancer. BioRxiv 2018; 436634: [View Article]
    [Google Scholar]
  78. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 2015; 31:3210–3212 [View Article] [PubMed]
    [Google Scholar]
  79. Medema MH, Blin K, Cimermancic P, de Jager V, Zakrzewski P et al. antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res 2011; 39:W339–46 [View Article] [PubMed]
    [Google Scholar]
  80. Zhang H, Yohe T, Huang L, Entwistle S, Wu P et al. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 2018; 46:W95–W101 [View Article] [PubMed]
    [Google Scholar]
  81. Rawlings ND, Waller M, Barrett AJ, Bateman A. MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 2014; 42:D503–9 [View Article] [PubMed]
    [Google Scholar]
  82. Saier MH Jr, Reddy VS, Tamang DG, Västermark A. The transporter classification database. Nucleic Acids Res 2014; 42:D251–8 [View Article] [PubMed]
    [Google Scholar]
  83. Almagro Armenteros JJ, Tsirigos KD, Sønderby CK, Petersen TN, Winther O et al. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol 2019; 37:420–423 [View Article] [PubMed]
    [Google Scholar]
  84. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001; 305:567–580 [View Article] [PubMed]
    [Google Scholar]
  85. Pierleoni A, Martelli PL, Casadio R. PredGPI: a GPI-anchor predictor. BMC Bioinformatics 2008; 9:1–11 [View Article] [PubMed]
    [Google Scholar]
  86. Sperschneider J, Gardiner DM, Dodds PN, Tini F, Covarelli L et al. EffectorP: predicting fungal effector proteins from secretomes using machine learning. New Phytol 2016; 210:743–761 [View Article] [PubMed]
    [Google Scholar]
  87. Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 2018; 34:3094–3100 [View Article] [PubMed]
    [Google Scholar]
  88. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010; 26:841–842 [View Article] [PubMed]
    [Google Scholar]
  89. Wickham H. ggplot2. In Ggplot2: Elegant Graphics for Data Analysis Cham: Springer-Verlag New York; 2016 [View Article]
    [Google Scholar]
  90. Yu G, Wang L-G, Han Y, He Q-Y. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 2012; 16:284–287 [View Article] [PubMed]
    [Google Scholar]
  91. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M et al. Versatile and open software for comparing large genomes. Genome Biol 2004; 5:1–9 [View Article] [PubMed]
    [Google Scholar]
  92. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R et al. Circos: an information aesthetic for comparative genomics. Genome Res 2009; 19:1639–1645 [View Article] [PubMed]
    [Google Scholar]
  93. Alonge M, Soyk S, Ramakrishnan S, Wang X, Goodwin S et al. RaGOO: fast and accurate reference-guided scaffolding of draft genomes. Genome Biol 2019; 20:1–17 [View Article] [PubMed]
    [Google Scholar]
  94. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 2014; 30:923–930 [View Article] [PubMed]
    [Google Scholar]
  95. Penouilh-Suzette C, Fourré S, Besnard G, Godiard L, Pecrix Y. A simple method for high molecular-weight genomic DNA extraction suitable for long-read sequencing from spores of an obligate biotroph oomycete. J Microbiol Methods 2020; 178:106054 [View Article] [PubMed]
    [Google Scholar]
  96. Varoquaux N, Liachko I, Ay F, Burton JN, Shendure J et al. Accurate identification of centromere locations in yeast genomes using Hi-C. Nucleic Acids Res 2015; 43:5331–5339 [View Article] [PubMed]
    [Google Scholar]
  97. Levan A, Fredga K, Sandberg AA. NOMENCLATURE FOR CENTROMERIC POSITION ON CHROMOSOMES. Hereditas 2009; 52:201–220 [View Article]
    [Google Scholar]
  98. van Wyk S, Wingfield BD, De Vos L, van der Merwe NA, Steenkamp ET. Genome-wide analyses of Repeat-Induced Point mutations in the Ascomycota. Front Microbiol 2021; 11:3625 [View Article]
    [Google Scholar]
  99. Collemare J, Griffiths S, Iida Y, Karimi Jashni M, Battaglia E et al. Secondary metabolism and biotrophic lifestyle in the tomato pathogen Cladosporium fulvum. PLoS One 2014; 9:e85877 [View Article] [PubMed]
    [Google Scholar]
  100. Lofgren LA, Uehling JK, Branco S, Bruns TD, Martin F et al. Genome-based estimates of fungal rDNA copy number variation across phylogenetic scales and ecological lifestyles. Mol Ecol 2019; 28:721–730 [View Article] [PubMed]
    [Google Scholar]
  101. Balesdent MH, Attard A, Kühn ML, Rouxel T. New avirulence genes in the phytopathogenic fungus Leptosphaeria maculans. Phytopathology 2002; 92:1122–1133 [View Article] [PubMed]
    [Google Scholar]
  102. Chang T-C, Salvucci A, Crous PW, Stergiopoulos I. Comparative genomics of the Sigatoka disease complex on banana suggests a link between parallel evolutionary changes in Pseudocercospora fijiensis and Pseudocercospora eumusae and increased virulence on the banana host. PLoS Genet 2016; 12:e1005904 [View Article] [PubMed]
    [Google Scholar]
  103. Frantzeskakis L, Kracher B, Kusch S, Yoshikawa-Maekawa M, Bauer S et al. Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen. BMC Genomics 2018; 19:381 [View Article] [PubMed]
    [Google Scholar]
  104. Torres DE, Oggenfuss U, Croll D, Seidl MF. Genome evolution in fungal plant pathogens: looking beyond the two-speed genome model. Fungal Biol Rev 2020; 34:136–143 [View Article]
    [Google Scholar]
  105. Lorrain C, Oggenfuss U, Croll D, Duplessis S, Stukenbrock E. Transposable elements in fungi: coevolution with the host genome shapes, genome architecture, plasticity and adaptation. In Zaragoza Ó, Casadevall A. eds Encyclopedia of Mycology Oxford: Elsevier; 2021 pp 142–155
    [Google Scholar]
  106. Oggenfuss U, Badet T, Wicker T, Hartmann FE, Singh NK et al. A population-level invasion by transposable elements triggers genome expansion in a fungal pathogen. Genomics 2020 [View Article]
    [Google Scholar]
  107. Mesarich CH, Griffiths SA, Burgt A, Ökmen B, Beenen HG et al. Transcriptome sequencing uncovers the Avr5 avirulence gene of the tomato leaf mold pathogen Cladosporium fulvum. Mol Plant Microbe Interact 2014; 27:846–857 [View Article]
    [Google Scholar]
  108. Ackerveken GF V, De Wit PJ. Molecular analysis of the avirulence gene avr9 of the fungal tomato pathogen Cladosporium fulvum fully supports the gene-for-gene hypothesis. Plant J 1992; 2:359–366
    [Google Scholar]
  109. Westerink N, Brandwagt BF, de Wit P, Joosten M. Cladosporium fulvum circumvents the second functional resistance gene homologue at the Cf-4 locus (Hcr9-4E) by secretion of a stable avr4E isoform. Mol Microbiol 2004; 54:533–545 [View Article]
    [Google Scholar]
  110. Mesarich CH, Ӧkmen B, Rovenich H, Griffiths SA, Wang C et al. Specific hypersensitive response-associated recognition of new apoplastic effectors from Cladosporium fulvum in Wild Tomato. Mol Plant Microbe Interact 2018; 31:145–162 [View Article]
    [Google Scholar]
  111. Lazar N, Mesarich CH, Petit-Houdenot Y, Talbi N, de la Sierra-Gallay IL et al. A new family of structurally conserved fungal effectors displays epistatic interactions with plant resistance proteins. Plant Biology 2020 [View Article]
    [Google Scholar]
  112. Houterman PM, Speijer D, Dekker HL, DE Koster CG, Cornelissen BJC et al. The mixed xylem sap proteome of Fusarium oxysporum-infected tomato plants. Mol Plant Pathol 2007; 8:215–221 [View Article] [PubMed]
    [Google Scholar]
  113. Rep M, van der Does HC, Meijer M, van Wijk R, Houterman PM et al. A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato. Mol Microbiol 2004; 53:1373–1383 [View Article] [PubMed]
    [Google Scholar]
  114. Yang H, Yu H, Ma L-J. Accessory chromosomes in Fusarium oxysporum. Phytopathology 2020; 110:1488–1496
    [Google Scholar]
  115. Balesdent M-H, Fudal I, Ollivier B, Bally P, Grandaubert J et al. The dispensable chromosome of Leptosphaeria maculans shelters an effector gene conferring avirulence towards Brassica rapa. New Phytol 2013; 198:887–898 [View Article] [PubMed]
    [Google Scholar]
  116. Temporini ED, VanEtten HD. Distribution of the pea pathogenicity (PEP) genes in the fungus Nectria haematococca mating population VI. Curr Genet 2002; 41:107–114 [View Article] [PubMed]
    [Google Scholar]
  117. Stewart EL, Croll D, Lendenmann MH, Sanchez-Vallet A, Hartmann FE et al. Quantitative trait locus mapping reveals complex genetic architecture of quantitative virulence in the wheat pathogen Zymoseptoria tritici. Mol Plant Pathol 2018; 19:201–216 [View Article] [PubMed]
    [Google Scholar]
  118. Peng Z, Oliveira-Garcia E, Lin G, Hu Y, Dalby M et al. Effector gene reshuffling involves dispensable mini-chromosomes in the wheat blast fungus. PLoS Genet 2019; 15:e1008272 [View Article] [PubMed]
    [Google Scholar]
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