1,592
Views
1
CrossRef citations to date
0
Altmetric
Genomics

Genomes and transcriptomes help unravel the complex life cycle of the blastoclad fungus, Coelomomyces lativittatus, an obligate parasite of mosquitoes and microcrustaceans

ORCID Icon, , , ORCID Icon, , ORCID Icon & ORCID Icon show all
Pages 630-647 | Received 31 Jan 2023, Accepted 19 Jun 2023, Published online: 26 Jul 2023

LITERATURE CITED

  • Abramyan J, Stajich JE. 2012. Species-specific chitin-binding module 18 expansion in the amphibian pathogen Batrachochytrium dendrobatidis. mBio. 3:e00150–12.
  • Amses KR, Rabern Simmons D, Longcore JE, Mondo SJ, Seto K, Jerônimo GH, Bonds AE, Alisha Quandt C, Davis WJ, Chang Y, et al. 2022. Diploid-dominant life cycles characterize the early evolution of Fungi. Proc Natl Acad Sci. 119:e2116841119. doi:10.1073/pnas.2116841119.
  • Armenteros JJA, Tsirigos KD, Sønderby CK, Petersen TN, Winther O, Brunak S, von Heijne G, Nielsen H. 2019. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol. 37:420–23.
  • Benkhali JA, Coppin E, Brun S, Peraza-Reyes L, Martin T, Dixelius C, Lazar N, van Tilbeurgh H, Debuchy R. 2013. A network of HMG-box transcription factors regulates sexual cycle in the fungus Podospora anserina. PLoS Genet. 9:e1003642. doi:10.1371/journal.pgen.1003642.
  • Boutet E, Lieberherr D, Tognolli M, Schneider M, Bansal P, Bridge AJ, Poux S, Bougueleret L, Xenarios I. 2016. UniProtKB/Swiss-Prot, the manually annotated section of the UniProt KnowledgeBase: how to use the entry view. Methods Mol Biol. 1374:23–54.
  • Bray NL, Pimentel H, Melsted P, Pachter L. 2016. Near-optimal probabilistic RNA-seq quantification. Nat Biotechnol. 34:525–27. doi:10.1038/nbt.3519.
  • Brown CT, Titus Brown C, Irber L. 2016. Sourmash: a library for MinHash sketching of DNA. J Open Source Softw. 1:27. doi:10.21105/joss.00027.
  • Buchfink B, Reuter K, Drost H-G. 2021. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat Methods. 18:366–68. doi:10.1038/s41592-021-01101-x.
  • Buchfink B, Xie C, Huson DH. 2015. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 12:59–60. doi:10.1038/nmeth.3176.
  • Bushnell B. 2014. BBMap: short read aligner for DNA and RNA-seq data. https://sourceforge.net/projects/bbmap/.
  • Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. BLAST+: architecture and applications. BMC Bioinform. 10:1–9. doi:10.1186/1471-2105-10-421.
  • Cao Y, Zhu X, Jiao R, Xia Y. 2012. The Magas1 gene is involved in pathogenesis by affecting penetration in Metarhizium acridum. J Microbiol Biotechnol. 22:889–93. doi:10.4014/jmb.1111.11055.
  • Challis R, Richards E, Rajan J, Cochrane G, Blaxter M. 2020. BlobToolKit – interactive quality assessment of genome assemblies. G3 Genes|Genomes|Genetics. 10:1361–74. doi:10.1534/g3.119.400908.
  • Chernomor O, von Haeseler A, Minh BQ. 2016. Terrace aware data structure for phylogenomic inference from supermatrices. Syst Biol. 65:997–1008.
  • Couch JN, Bland CE. 1985. The genus Coelomomyces. Orlando (FL): Academic Press, Inc.
  • Delmont T. 2018. Assessing the completion of eukaryotic bins with anvi’o. http://merenlab.org/delmont-euk-scgs.
  • Desjardins CA, Sanscrainte ND, Goldberg JM, Heiman D, Young S, Zeng Q, Madhani HD, Becnel JJ, Cuomo CA. 2015. Contrasting host–pathogen interactions and genome evolution in two generalist and specialist microsporidian pathogens of mosquitoes. Nat Commun. 6:7121. doi:10.1038/ncomms8121.
  • Diotti R, Esposito M, Shen CH. 2021. Telomeric and sub-telomeric structure and implications in fungal opportunistic pathogens. Microorganisms. 9. p. 1405.
  • Duplessis S, Lorrain C, Petre B, Figueroa M, Dodds PN, Aime MC. 2021. Host adaptation and virulence in heteroecious rust fungi. Annu Rev Phytopathol. 59:403–22. doi:10.1146/annurev-phyto-020620-121149.
  • Eddy SR. 2011. Accelerated profile HMM searches. PLoS Comput Biol. 7:e1002195.
  • Ellison AR, DiRenzo GV, McDonald CA, Lips KR, Zamudio KR. 2017. First in vivo Batrachochytrium dendrobatidis transcriptomes reveal mechanisms of host exploitation, host-specific gene expression, and expressed genotype shifts. G3 Genes|Genomes|Genetics. G3(7):269–78.
  • Emms DM, Kelly S. 2019. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20:238. doi:10.1186/s13059-019-1832-y.
  • Eren AM, Murat Eren A, Esen ÖC, Quince C, Vineis JH, Morrison HG, Sogin ML, Delmont TO. 2015. Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ. 3:e1319. doi:10.7717/peerj.1319.
  • Eren AM, Murat Eren A, Kiefl E, Shaiber A, Veseli I, Miller SE, Schechter MS, Fink I, Pan JN, Yousef M, et al. 2021. Community-led, integrated, reproducible multi-omics with anvi’o. Nat Microbiol. 6:3–6. doi:10.1038/s41564-020-00834-3.
  • Federici BA. 1977. Differential pigmentation in the sexual phase of Coelomomyces. Nature. 267:514–15. doi:10.1038/267514a0.
  • Federici BA. 1979. Experimental hybridization of Coelomomyces dodgei and Coelomomyces punctatus. Proc Natl Acad Sci USA. 76:4425–28. doi:10.1073/pnas.76.9.4425.
  • Federici BA. 1983. Species-specific gating of gametangial dehiscence as a temporal reproductive isolating mechanism in Coelomomyces. Proc Natl Acad Sci USA. 80:604–07.
  • Federici BA, Chapman HC. 1977. Coelomomyces dodgei: establishment of an in vivo laboratory culture. J Invertebr Pathol. 30:288–97. doi:10.1016/0022-2011(77)90136-7.
  • Federici BA, Thompson SN. 1979. β-Carotene in the gametophytic phase of Coelomomyces dodgei. Exp Mycol. 3:281–84. doi:10.1016/S0147-5975(79)80053-5.
  • Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, et al. 2014. Pfam: the protein families database. Nucleic Acids Res. 42:D222–30. doi:10.1093/nar/gkt1223.
  • Flynn JM, Hubley R, Goubert C, Rosen J, Clark AG, Feschotte C, Smit AF. 2020. RepeatModeler2 for automated genomic discovery of transposable element families. Proc Natl Acad Sci USA. 117:9451–57.
  • Fu L, Niu B, Zhu Z, Wu S, Li W. 2012. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 28:3150–52. doi:10.1093/bioinformatics/bts565.
  • Gilchrist CLM, Booth TJ, van Wersch B, van Grieken L, Medema MH, Chooi Y-H. 2021. cblaster: a remote search tool for rapid identification and visualization of homologous gene clusters. Bioinform Adv. 1:vbab016. doi:10.1093/bioadv/vbab016.
  • Gilchrist CLM, Chooi Y-H. 2021. Clinker & clustermap.js: automatic generation of gene cluster comparison figures. Bioinformatics. 37:2473–75. doi:10.1093/bioinformatics/btab007.
  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 29:644–52. doi:10.1038/nbt.1883.
  • Grell MN, Mouritzen P, Giese H. 2003. A Blumeria graminis gene family encoding proteins with a C-terminal variable region with homologues in pathogenic fungi. Gene. 311:181–92. doi:10.1016/S0378-1119(03)00610-3.
  • Grigoriev IV, Nikitin R, Haridas S, Kuo A, Ohm R, Otillar R, Riley R, Salamov A, Zhao X, Korzeniewski F, et al. 2014. MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res. 42:D699–704. doi:10.1093/nar/gkt1183.
  • Gueddari NEE, El Gueddari NE, Rauchhaus U, Moerschbacher BM, Deising HB. 2002. Developmentally regulated conversion of surface-exposed chitin to chitosan in cell walls of plant pathogenic fungi. New Phytol. 156:103–12. doi:10.1046/j.1469-8137.2002.00487.x.
  • Gurevich A, Saveliev V, Vyahhi N, Tesler G. 2013. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 29:1072–75. doi:10.1093/bioinformatics/btt086.
  • Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith RK Jr, Hannick LI, Maiti R, Ronning CM, Rusch DB, Town CD, et al. 2003. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 31:5654–66. doi:10.1093/nar/gkg770.
  • Haas BJ, Salzberg SL, Zhu W, Pertea M, Allen JE, Orvis J, White O, Buell CR, Wortman JR. 2008. Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biol. 9:R7. doi:10.1186/gb-2008-9-1-r7.
  • Hardie DG, Ross FA, Hawley SA. 2012. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol. 13:251–62. doi:10.1038/nrm3311.
  • Hiltunen M, Ament-Velásquez SL, Johannesson H. 2021. The assembled and annotated genome of the fairy-ring fungus Marasmius oreades. Genome Biol Evol. 13:evab126. doi:10.1093/gbe/evab126.
  • Huang L, Zhang H, Wu P, Entwistle S, Li X, Yohe T, Yi H, Yang Z, Yin Y. 2018. dbCAN-seq: a database of carbohydrate-active enzyme (CAZyme) sequence and annotation. Nucleic Acids Res. 46:D516–D521. doi:10.1093/nar/gkx894.
  • Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter MC, Rattei T, Mende DR, Sunagawa S, Kuhn M, et al. 2016. eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res. 44:D286–93.
  • Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 11:119. doi:10.1186/1471-2105-11-119.
  • Idnurm A, Walton FJ, Floyd A, Heitman J. 2008. Identification of the sex genes in an early diverged fungus. Nature. 451:193–96. doi:10.1038/nature06453.
  • James TY, Letcher PM, Longcore JE, Mozley-Standridge SE, Porter D, Powell MJ, Griffith GW, Vilgalys R. 2006. A molecular phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). Mycologia. 98:860–71. doi:10.1080/15572536.2006.11832616.
  • James TY, Stajich JE, Hittinger CT, Rokas A. 2020. Toward a fully resolved fungal tree of life. Annu Rev Microbiol. 74:291–313. doi:10.1146/annurev-micro-022020-051835.
  • Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, et al. 2014. InterProScan 5: genome-scale protein function classification. Bioinformatics. 30:1236–40.
  • Käll L, Krogh A, Sonnhammer ELL. 2004. A combined transmembrane topology and signal peptide prediction method. J Mol Biol. 338:1027–36. doi:10.1016/j.jmb.2004.03.016.
  • Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 14:587–89. doi:10.1038/nmeth.4285.
  • Keon J, Rudd JJ, Antoniw J, Skinner W, Hargreaves J, Hammond-Kosack K. 2005. Metabolic and stress adaptation by Mycosphaerella graminicola during sporulation in its host revealed through microarray transcription profiling. Mol Plant Pathol. 6:527–40. doi:10.1111/j.1364-3703.2005.00304.x.
  • Kim D, Paggi JM, Park C, Bennett C, Salzberg SL. 2019. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 37:907–15. doi:10.1038/s41587-019-0201-4.
  • Korf I. 2004. Gene finding in novel genomes. BMC Bioinform. 5:59. doi:10.1186/1471-2105-5-59.
  • Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. doi:10.1186/gb-2009-10-3-r25.
  • Laundon D, Chrismas N, Bird K, Thomas S, Mock T, Cunliffe M. 2022. A cellular and molecular atlas reveals the basis of chytrid development. eLife. 11:e73933. doi:10.7554/eLife.73933.
  • Lee MD. 2019. GToTree: a user-friendly workflow for phylogenomics. Bioinformatics. 35:4162–64. doi:10.1093/bioinformatics/btz188.
  • Lee SC, Ni M, Li W, Shertz C, Heitman J. 2010. The evolution of sex: a perspective from the fungal kingdom. Microbiol Mol Biol Rev. 74:298–340. doi:10.1128/MMBR.00005-10.
  • Léjohn HB, Lovett JS. 1966. Ribonucleic acid and protein synthesis in Rhizophlyctis rosea zoospores. J Bacteriol. 91:709–17. doi:10.1128/jb.91.2.709-717.1966.
  • Leonard G, Galindo LJ, Milner DS, Avelar GM, Gomes-Vieira AL, Gomes SL, Richards TA. 2022. A genome sequence assembly of the phototactic and optogenetic model fungus Blastocladiella emersonii reveals a diversified nucleotide-cyclase repertoire. Genome Biol Evol. 14:evac157. doi:10.1093/gbe/evac157.
  • Li H. 2018. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 34:3094–100. doi:10.1093/bioinformatics/bty191.
  • Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 25:1754–60. doi:10.1093/bioinformatics/btp324.
  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R; 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map format and SAMtools. Bioinformatics. 25:2078–79. doi:10.1093/bioinformatics/btp352.
  • Li Y, Steenwyk JL, Chang Y, Wang Y, James TY, Stajich JE, Spatafora JW, Groenewald M, Dunn CW, Hittinger CT, et al. 2021. A genome-scale phylogeny of the kingdom Fungi. Curr Biol. 31:1653–1665.e5. doi:10.1016/j.cub.2021.01.074.
  • Liu P, Stajich JE. 2015. Characterization of the Carbohydrate binding module 18 gene family in the amphibian pathogen Batrachochytrium dendrobatidis. Fungal Genet Biol. 77:31–39. doi:10.1016/j.fgb.2015.03.003.
  • Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. 2014. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42:D490–5. doi:10.1093/nar/gkt1178.
  • 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.
  • Lovett JS. 1968. Reactivation of ribonucleic acid and protein synthesis during germination of Blastocladiella zoospores and the role of the ribosomal nuclear cap. J Bacteriol. 96:962–69. doi:10.1128/jb.96.4.962-969.1968.
  • Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25:955–64. doi:10.1093/nar/25.5.955.
  • Majoros WH, Pertea M, Salzberg SL. 2004. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics. 20:2878–79. doi:10.1093/bioinformatics/bth315.
  • Menzel P, Ng KL, Krogh A. 2016. Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat Commun. 7:11257. doi:10.1038/ncomms11257.
  • Mesquita I, Moreira D, Sampaio-Marques B, Laforge M, Cordeiro-da-Silva A, Ludovico P, Estaquier J, Silvestre R. 2016. AMPK in pathogens. In: Cordero M, Viollet B, editors. AMP-activated protein Kinase. Cham (Switzerland): Springer; p. 287–323.
  • Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R. 2020. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 37:1530–34. doi:10.1093/molbev/msaa015.
  • Morgan M, Falcon S, Gentleman R. 2022. GSEABase: gene set enrichment data structures and methods. http://bioconductor.org/packages/GSEABase/.
  • Palmer JM, Stajich J. 2020. Funannotate v1.8.1: eukaryotic genome annotation. http://doi.org/10.5281/zenodo.4054262.
  • Pantano L. 2022. DEGreport: report of DEG analysis. http://lpantano.github.io/DEGreport/.
  • Porter TM, Martin W, James TY, Longcore JE, Gleason FH, Adler PH, Letcher PM, Vilgalys R. 2011. Molecular phylogeny of the Blastocladiomycota (Fungi) based on nuclear ribosomal DNA. Fungal Biol. 115:381–92. doi:10.1016/j.funbio.2011.02.004.
  • Powell MJ. 2017. Blastocladiomycota. In: Archibald J, Simpson A, Slamovits C, editors. Handbook of the protists. Cham, Boston: Springer; p. 1497–521.
  • Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. 2020. Using SPAdes de novo assembler. Curr Protoc Bioinformatics. 70:e102. doi:10.1002/cpbi.102.
  • Rawlings ND, Barrett AJ, Bateman A. 2014. Using the MEROPS database for proteolytic enzymes and their inhibitors and substrates. Curr Protoc Bioinformatics. 48:1.25.1–33. doi:10.1002/0471250953.bi0125s48.
  • R Core Team. 2020. R: a language and environment for statistical computing. Vienna (Austria). https://www.R-project.org/.
  • Schmoyer IR, Lovett JS. 1969. Regulation of protein synthesis in zoospores of Blastocladiella. J Bacteriol. 100:854–64. doi:10.1128/jb.100.2.854-864.1969.
  • Seemann T. 2018. barrnap: bAsic rapid ribosomal RNA predictor. https://github.com/tseemann/barrnap.
  • Shen D, Nyawira KT, Xia A. 2020. New discoveries and applications of mosquito fungal pathogens. Curr Opin Insect Sci. 40:111–16. doi:10.1016/j.cois.2020.05.003.
  • Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. 2015. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 31:3210–12. doi:10.1093/bioinformatics/btv351.
  • Smit AFA, Hubley R, Green P. 2013–2015. RepeatMasker. http://www.repeatmasker.org.
  • Sreesankar E, Senthilkumar R, Bharathi V, Mishra RK, Mishra K. 2012. Functional diversification of yeast telomere associated protein, Rif1, in higher eukaryotes. BMC Genom. 13:255. doi:10.1186/1471-2164-13-255.
  • Stajich J, Palmer J. 2019. stajichlab/AAFTF: v0.2.3. doi:10.5281/zenodo.3437300.
  • Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B. 2006. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 34:W435–9. doi:10.1093/nar/gkl200.
  • Steenwyk JL, Buida TJ 3rd, Li Y, Shen X-X, Rokas A. 2020. ClipKIT: a multiple sequence alignment trimming software for accurate phylogenomic inference. PLoS Biol. 18:e3001007. doi:10.1371/journal.pbio.3001007.
  • Supek F, Bošnjak M, Škunca N, Šmuc T. 2011. REVIGO summarizes and visualizes long lists of gene ontology terms. PloS One. 6:e21800. doi:10.1371/journal.pone.0021800.
  • Ter-Hovhannisyan V, Lomsadze A, Chernoff YO, Borodovsky M. 2008. Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res. 18:1979–90. doi:10.1101/gr.081612.108.
  • Testa AC, Hane JK, Ellwood SR, Oliver RP. 2015. CodingQuarry: highly accurate hidden Markov model gene prediction in fungal genomes using RNA-seq transcripts. BMC Genom. 16:170. doi:10.1186/s12864-015-1344-4.
  • Travland LB. 1979. Initiation of infection of mosquito larvae (Culiseta inornata) by Coelomomyces psorophorae. J Invertebr Pathol. 33:95–105. doi:10.1016/0022-2011(79)90136-8.
  • van den Burg HA, Harrison SJ, Joosten MHAJ, Vervoort J, de Wit PJGM. 2006. Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol Plant-Microbe Interact. 19:1420–30. doi:10.1128/EC.00312-09.
  • van de Vossenberg BTLH, Warris S, Nguyen HDT, van Gent-Pelzer MPE, Joly DL, van de Geest HC, Bonants PJM, Smith DS, André Lévesque C, van der Lee TAJ. 2019. Comparative genomics of chytrid fungi reveal insights into the obligate biotrophic and pathogenic lifestyle of Synchytrium endobioticum. Sci Rep. 9:1–14. doi:10.1038/s41598-019-45128-9.
  • Vieira ALG, Gomes SL. 2010. Global gene expression analysis during sporulation of the aquatic fungus Blastocladiella emersonii. Eukaryot Cell. 9:415–23.
  • Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wortman J, Young SK, et al. 2014. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 9:e112963. doi:10.1371/journal.pone.0112963.
  • Wallen RM, Perlin MH. 2018. An overview of the function and maintenance of sexual reproduction in dikaryotic fungi. Front Microbiol. 9:503. doi:10.3389/fmicb.2018.00503.
  • Whisler HC, Karanja DMS, Shemanchuk JA, Zebold SL, Romney SV, Nielsen LT. 2009. The life history and in vivo culture of Coelomomyces utahensis (Blastocladiomycetes). J Invertebr Pathol. 100:40–43. doi:10.1016/j.jip.2008.09.009.
  • Whisler HC, Zebold SL, Shemanchuk JA. 1975. Life history of Coelomomyces psorophorae. Proc Natl Acad Sci USA. 72:693–96. doi:10.1073/pnas.72.2.693.
  • Wickham H. 2009. ggplot2: elegant graphics for data analysis. New York: Springer-Verlag.
  • Wickham H, Averick M, Bryan J, Chang W, McGowan LD, François R, Grolemund G, Hayes A, Henry L, Hester J, et al. 2019. Welcome to the tidyverse. J Open Source Softw. 4:1686. doi:10.21105/joss.01686.
  • Wyatt NA, Richards JK, Brueggeman RS, Friesen TL. 2020. A comparative genomic analysis of the barley pathogen Pyrenophora teres f. teres identifies subtelomeric regions as drivers of virulence. Mol Plant-Microbe Interact. 33:173–88. doi:10.1094/MPMI-05-19-0128-R.
  • Zebold SL, Whisler HC, Shemanchuk JA, Travland LB. 1979. Host specificity and penetration in the mosquito pathogen Coelomomyces psorophorae. Can J Bot. 57:2766–70.
  • Zhao Y, Park R-D, Muzzarelli RAA. 2010. Chitin deacetylases: properties and applications. Mar Drugs. 8:24–46. doi:10.3390/md8010024.