Phylogenomic analyses of Alternaria section Alternaria: A high-resolution, genome-wide study of lineage sorting and gene tree discordance

LITERATURE CITED

• Andrew M, Peever TL, Pryor BM. 2009. An expanded multilocus phylogeny does not resolve morphological species within the small-spored Alternaria species complex. Mycologia 101:95–109.
   PubMed Web of Science ®Google Scholar
• Armitage AD, Barbara DJ, Harrison RJ, Lane CR, Sreenivasaprasad S, Woodhall JW, Clarkson JP. 2015. Discrete lineages within Alternaria alternata species group: identification using new highly variable loci and support from morphological characters. Fungal Biology 119:994–1006.
   PubMed Web of Science ®Google Scholar
• Armitage AD, Cockerton HM, Sreenivasaprasad S, Woodhall J, Lane CR, Harrison RJ, Clarkson JP. 2020. Genomics evolutionary history and diagnostics of the Alternaria alternata species group including apple and Asian pear pathotypes. Frontiers in Microbiology 10:3124.
   PubMed Web of Science ®Google Scholar
• Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology 19:455–477.
   PubMed Web of Science ®Google Scholar
• Bihon W, Cloete M, Gerrano AS, Oelofse D, Adebola P. 2016. Draft genome sequence of Alternaria alternata isolated from onion leaves in South Africa. Genome Announcements 4:301022–16.
   Google Scholar
• Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120.
   PubMed Web of Science ®Google Scholar
• da Cruz Cabral L, Rodriguero M, Stenglein S, Fog Nielsen K, Patriarca A. 2017. Characterization of small-spored Alternaria from Argentinean crops through a polyphasic approach. International Journal of Food Microbiology 257:206–215.
   PubMed Web of Science ®Google Scholar
• Dang HX, Pryor B, Peever T, Lawrence CB. 2015. The Alternaria genomes database: a comprehensive resource for a fungal genus comprised of saprophytes, plant pathogens, and allergenic species. BMC Genomics 16:239.
   PubMed Web of Science ®Google Scholar
• Dettman JR, Jacobson DJ, Taylor JW. 2003. A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote neurospora. Evolution 57:2703–2720.
   PubMed Web of Science ®Google Scholar
• Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32:1792–1797.
   PubMed Web of Science ®Google Scholar
• Emms DM, Kelly S. 2019. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biology 20:238.
   PubMed Web of Science ®Google Scholar
• Gebru ST, Gangiredla J, Tournas VH, Tartera C, Mammel MK. 2020. Draft genome sequences of Alternaria strains isolated from grapes and apples. Microbiology Resource Announcements 9:e01491–19.
   Google Scholar
• Hong SG, Cramer RA, Lawrence CB, Pryor BM. 2005. Alt a 1 allergen homologs from Alternaria and related taxa: analysis of phylogenetic content and secondary structure. Fungal Genetics and Biology 42:119–129.
   PubMed Web of Science ®Google Scholar
• Hu J, Chen C, Peever T, Dang H, Lawrence C, Mitchell T. 2012. Genomic characterization of the conditionally dispensable chromosome in Alternaria arborescens provides evidence for horizontal gene transfer. BMC Genomics 13:171.
   PubMed Web of Science ®Google Scholar
• Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL. 2004. Versatile and open software for comparing large genomes. Genome Biology 5:R12.
   PubMed Web of Science ®Google Scholar
• Lawrence DP, Gannibal PB, Peever TL, Pryor BM. 2013. The sections of Alternaria: formalizing species-group concepts. Mycologia 105:530–546.
   PubMed Web of Science ®Google Scholar
• Lawrence DP, Rotondo F, Gannibal PB. 2016. Biodiversity and taxonomy of the pleomorphic genus Alternaria. Mycological Progress 15:3.
   Web of Science ®Google Scholar
• Meena M, Gupta SK, Swapnil P, Zehra A, Dubey MK, Upadhyay RS. 2017. Alternaria toxins: potential virulence factors and genes related to pathogenesis. Frontiers in Microbiology 8:1451.
   PubMed Web of Science ®Google Scholar
• Mehta RS, Rosenberg NA. 2019. The probability of reciprocal monophyly of gene lineages in three and four species. Theoretical Population Biology 129:133–147.
   PubMed Web of Science ®Google Scholar
• Meng JW, Zhu W, He MH, Wu EJ, Duan GH, Xie YK, Jin YJ, Yang LN, Shang LP, Zhan J. 2015. Population genetic analysis reveals cryptic sex in the phytopathogenic fungus Alternaria alternata. Scientific Reports 5:18250.
   PubMed Web of Science ®Google Scholar
• Mikheenko A, Prjibelski A, Saveliev V, Antipov D, Gurevich A. 2018. Versatile genome assembly evaluation with QUAST-LG. Bioinformatics 34:i142–i150.
   PubMed Web of Science ®Google Scholar
• Möller EM, Bahnweg G, Sandermann H, Geiger HH. 1992. A simple and efficient protocol for isolation of high molecular weight DNA from filamentous fungi, fruit bodies, and infected plant tissues. Nucleic Acids Research 20:6115–6116.
   PubMed Web of Science ®Google Scholar
• Möller M, Stukenbrock EH. 2017. Evolution and genome architecture in fungal plant pathogens. Nature Reviews Microbiology 15:756–771.
   PubMed Web of Science ®Google Scholar
• Nees von Esenbeck C. 1817. Das System der Pilze und Schwämme. Wurzburg, Germany: Stahel. 474 p.
   Google Scholar
• Nguyen HDT, Lewis CT, Lévesque CA, Gräfenhan T. 2016. Draft genome sequence of Alternaria alternata ATCC 34957. Genome Announcements 4:e01554–15.
   PubMedGoogle Scholar
• Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32:268–274.
   PubMed Web of Science ®Google Scholar
• Nishikawa J, Nakashima C. 2019. Morphological and molecular characterization of the strawberry black leaf spot pathogen referred to as the strawberry pathotype of Alternaria alternata. Mycoscience 60:1–9.
   Web of Science ®Google Scholar
• Pamilo P, Nei M. 1988. Relationships between gene trees and species trees. Molecular Biology and Evolution 5:568–583.
   PubMed Web of Science ®Google Scholar
• Park SY, Jeon J, Kim JA, Jeon MJ, Jeong MH, Kim Y, Lee Y, Chung H, Lee YH, Kim S. 2020. Draft genome sequence of Alternaria alternata JS-1623, a fungal endophyte of Abies koreana. Mycobiology, doi:https://doi.org/10.1080/12298093.2020.1756134
   Google Scholar
• Peever TL, Su G, Carpenter-Boggs L, Timmer LW. 2004. Molecular systematics of citrus-associated Alternaria species. Mycologia 96:119–134.
   PubMed Web of Science ®Google Scholar
• Pryor B, Gilberston R. 2000. Molecular phylogenetic relationships amongst Alternaria species and related fungi based upon analysis of nuclear ITS and mt SSU rDNA sequences. Mycological Research 104:1312–1312.
   Web of Science ®Google Scholar
• Rotondo F, Collina M, Brunelli A, Pryor BM. 2012. Comparison of Alternaria spp. Collected in Italy from apple with A. mali and other AM-toxin producing strains. Phytopathology 102:1130–1142.
   Google Scholar
• Simão FA, Waterhouse RM, Ioannidis P, Kriventseva E V., Zdobnov EM. 2015. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31: 3210–3212.
   Google Scholar
• Simmons E. 1999a. Alternaria themes and variations (236–243). Host-specific toxin producers. Mycotaxon 70:325–369.
   Google Scholar
• Simmons E. 1999b. Alternaria themes and variations (226–235). Classification of citrus pathogens. Mycotaxon 70:263–323.
   Google Scholar
• Simmons E. 2007. Alternaria: an identification manual. CBS Biodiversity Series 6. Utrecht, The Netherlands: CBS Fungal Biodiversity Centre. 780 p.
   Google Scholar
• Simmons EG. 1967. Typification of Alternaria, Stemphylium, and Ulocladium. Mycologia 59:67–92.
   PubMed Web of Science ®Google Scholar
• Stewart JE, Timmer LW, Lawrence CB, Pryor BM, Peever TL. 2014. Discord between morphological and phylogenetic species boundaries: incomplete lineage sorting and recombination results in fuzzy species boundaries in an asexual fungal pathogen. BMC Evolutionary Biology 14:38.
   PubMed Web of Science ®Google Scholar
• Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC. 2000. Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology 31:21–32.
   PubMed Web of Science ®Google Scholar
• Tittlemier SA, Blagden R, Chan J, Gaba D, Mckendry T, Pleskach K, Roscoe M. 2019. Fusarium and Alternaria mycotoxins present in Canadian wheat and durum harvest samples. Canadian Journal of Plant Pathology 41:403–414.
   Web of Science ®Google Scholar
• Tralamazza SM, Piacentini KC, Iwase CHT, Rocha Lde O. 2018. Toxigenic Alternaria species: impact in cereals worldwide. Current Opinion in Food Science 23:57–63.
   Google Scholar
• Ushijima K, Yamamoto M. 2019. A sequence resource of autosomes and additional chromosomes in the peach pathotype of Alternaria alternata. Molecular Plant-Microbe Interactions 32:1273–1276.
   PubMed Web of Science ®Google Scholar
• Wang M, Fu H, Shen XX, Ruan R, Rokas A, Li H. 2019. Genomic features and evolution of the conditionally dispensable chromosome in the tangerine pathotype of Alternaria alternata. Molecular Plant Pathology 20:1425–1438.
   PubMed Web of Science ®Google Scholar
• Wang M, Sun X, Yu D, Xu J, Chung K, Li H. 2016. Genomic and transcriptomic analyses of the tangerine pathotype of Alternaria alternata in response to oxidative stress. Scientific Reports 6:32437.
   PubMed Web of Science ®Google Scholar
• Woudenberg JHC, Groenewald JZ, Binder M, Crous PW. 2013. Alternaria redefined. Studies in Mycology 75:171–212.
   PubMed Web of Science ®Google Scholar
• Woudenberg JHC, Seidl MF, Groenewald JZ, de Vries M, Stielow JB, Thomma BPHJ, Crous PW. 2015. Alternaria section Alternaria: species, formae speciales or pathotypes? Studies in Mycology 82:1–21.
   Google Scholar
• Zeiner CA, Purvine SO, Zink EM, Paša-Tolić L, Chaput DL, Haridas S, Wu S, LaButti K, Grigoriev IV, Henrissat B, Santelli CM, Hansel CM. 2016. Comparative analysis of secretome profiles of manganese(II)-oxidizing ascomycete fungi. PLoS ONE 1:e0157844.
   Google Scholar
• Zhang C, Rabiee M, Sayyari E, Mirarab S. 2018. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics 19(Suppl 6):153.
   PubMed Web of Science ®Google Scholar
• Zheng HH, Zhao J, Wang TY, Wu XH. 2015. Characterization of Alternaria species associated with potato foliar diseases in China. Plant Pathology 64:425–433.
   Web of Science ®Google Scholar