Genomic landscape of a relict fir-associated fungus reveals rapid convergent adaptation towards endophytism
1.Tigano A, Colella JP, MacManes MD. Comparative and population genomics approaches reveal the basis of adaptation to deserts in a small rodent. Mol Ecol. 2020;29:1300–14.CAS
PubMed
PubMed Central
Google Scholar
2.Gladieux P, Ropars J, Badouin H, Branca A, Aguileta G, de Vienne DM, et al. Fungal evolutionary genomics provides insight into the mechanisms of adaptive divergence in eukaryotes. Mol Ecol. 2014;23:753–73.PubMed
Google Scholar
3.Martin F, Aerts A, Ahrén D, Brun A, Danchin EG, Duchaussoy F, et al. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature. 2008;452:88–92.CAS
PubMed
Google Scholar
4.Weiß M, Waller F, Zuccaro A, Selosse MA. Sebacinales-one thousand and one interactions with land plants. New Phytol. 2016;211:20–40.PubMed
Google Scholar
5.Knapp DG, Németh JB, Barry K, Hainaut M, Henrissat B, Johnson J, et al. Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi. Sci Rep. 2018;8:6321.PubMed
PubMed Central
Google Scholar
6.Martino E, Morin E, Grelet GA, Kuo A, Kohler A, Daghino S, et al. Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists. New Phytol. 2018;217:1213–29.CAS
PubMed
Google Scholar
7.Arnold AE. Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev. 2007;21:51–66.
Google Scholar
8.Carroll G. Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology. 1988;69:2–9.
Google Scholar
9.Miller JD, Sumarah MW, Adams GW. Effect of a rugulosin-producing endophyte in Picea glauca on Choristoneura fumiferana. J Chem Ecol. 2008;34:362–8.CAS
PubMed
Google Scholar
10.White JF Jr, Torres MS. Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol Plant. 2010;138:440–6.CAS
PubMed
PubMed Central
Google Scholar
11.May G, Nelson P. Defensive mutualisms: do microbial interactions within hosts drive the evolution of defensive traits? Funct Ecol. 2014;28:356–63.
Google Scholar
12.Carroll G. The foraging ascomycete, in: Abstracts of the 16th International Botanical Congress. St Louis, Missouri, USA, 1999.13.Müller MM, Valjakka R, Suokko A, Hantula J. Diversity of endophytic fungi of single Norway spruce needles and their role as pioneer decomposers. Mol Ecol. 2001;10:1801–10.PubMed
Google Scholar
14.Thomas DC, Vandegrift R, Ludden A, Carroll GC, Roy BA. Spatial ecology of the fungal genus Xylaria in a tropical cloud forest. Biotropica. 2016;48:381–93.
Google Scholar
15.Naranjo-Ortiz MA, Gabaldón T. Fungal evolution: major ecological adaptations and evolutionary transitions. Biol Rev Camb Philos Soc. 2019;94:1443–76.PubMed
PubMed Central
Google Scholar
16.Oono R, Lutzoni F, Arnold AE, Kaye L, U’Ren JM, May G, et al. Genetic variation in horizontally transmitted fungal endophytes of pine needles reveals population structure in cryptic species. Am J Bot. 2014;101:1362–74.PubMed
Google Scholar
17.Shao S, Jin Z. In Species Diversity and Extinction (ed. Tepper, GH) Ch. 15. Nova Science Publishers. 2010.18.Yuan ZL, Rao LB, Chen YC, Zhang CL, Wu YG. From pattern to process: species and functional diversity in fungal endophytes of Abies beshanzuensis. Fungal Biol. 2011;115:197–213.PubMed
Google Scholar
19.Yuan ZL, Verkley GJM. Pezicula neosporulosa sp. nov. (Helotiales, Ascomycota), an endophytic fungus associated with Abies spp. in China and Europe. Mycoscience. 2014;56:205–13.
Google Scholar
20.Sieber T. Endophytic fungi in forest trees: are they mutualists? Fungal Biol Rev. 2007;21:75–89.
Google Scholar
21.Levis NA, Martin RA, O’Donnell KA, Pfennig DW. Intraspecific adaptive radiation: competition, ecological opportunity, and phenotypic diversification within species. Evolution. 2017;71:2496–509.PubMed
Google Scholar
22.Grigoriev IV, Nikitin R, Haridas S, Kuo A, Ohm R, Otillar R, et al. MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res. 2014;42:D699–D704.CAS
PubMed
Google Scholar
23.Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42:D490–D495.CAS
PubMed
Google Scholar
24.Zhang H, Yohe T, Huang L, Entwistle S, Wu P, Yang Z, et al. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2018;46:W95–W101.CAS
PubMed
PubMed Central
Google Scholar
25.Blin K, Wolf T, Chevrette MG, Lu XW, Schwalen CJ, Kautsar SA, et al. antiSMASH 4.0-improvements in chemistry prediction and gene cluster boundary identification. Nucleic Acids Res. 2017;45:W36–W41.CAS
PubMed
PubMed Central
Google Scholar
26.Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 2015;16:157.PubMed
PubMed Central
Google Scholar
27.Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7.CAS
PubMed
PubMed Central
Google Scholar
28.Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540–52.CAS
PubMed
Google Scholar
29.Enright AJ, Dongen SV, Ouzounis CA. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. 2002;30:1575–84.CAS
PubMed
PubMed Central
Google Scholar
30.Han MV, Thomas GW, Lugo-Martinez J, Hahn MW. Estimating gene gain and loss rates in the presence of error in genome assembly and annotation using CAFE 3. Mol Biol Evol. 2013;30:1987–97.CAS
PubMed
Google Scholar
31.Walkowiak S, Rowland O, Rodrigue N, Subramaniam R. Whole genome sequencing and comparative genomics of closely related Fusarium Head Blight fungi: Fusarium graminearum, F. meridionale and F. asiaticum. BMC Genomics. 2016;17:1014.PubMed
PubMed Central
Google Scholar
32.Li H, Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics. 2010;26:589–95.PubMed
PubMed Central
Google Scholar
33.Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078–9.PubMed
PubMed Central
Google Scholar
34.Van der Auwera GA, Carneiro MO, Hartl C, Poplin R, Del Angel G, Levy-Moonshine A, et al. From FastQ data to high confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr Protoc Bioinformatics. 2013;43:11.10.1–11.10.33.
Google Scholar
35.Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123:585–95.CAS
PubMed
PubMed Central
Google Scholar
36.Fu YX, Li WH. Statistical tests of neutrality of mutations. Genetics. 1993;133:693–709.CAS
PubMed
PubMed Central
Google Scholar
37.Hutter S, Vilella AJ, Rozas J. Genome-wide DNA polymorphism analyses using VariScan. BMC Bioinform. 2006;7:409.
Google Scholar
38.Richards JK, Stukenbrock EH, Carpenter J, Liu Z, Cowger C, Faris JD, et al. Local adaptation drives the diversification of effectors in the fungal wheat pathogen Parastagonospora nodorum in the United States. PLoS Genet. 2019;15:e1008223.CAS
PubMed
PubMed Central
Google Scholar
39.Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23:254–67.CAS
PubMed
Google Scholar
40.Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31:3210–2.PubMed
Google Scholar
41.Looney B, Miyauchi S, Morin E, Drula E, Courty PE, Kohler A, et al. Evolutionary priming and transition to the ectomycorrhizal habit in an iconic lineage of mushroom-forming fungi: is preadaptation a requirement? bioRxiv. 2021. https://doi.org/10.1101/2021.02.23.432530.42.Wey T, Schlegel M, Stroheker S, Gross A. MAT-gene structure and mating behavior of Hymenoscyphus fraxineus and Hymenoscyphus albidus. Fungal Genet Biol. 2016;87:54–63.CAS
PubMed
Google Scholar
43.Zijlstra JD, Van’t Hof P, Baar J, Verkley GJM, Summerbell RC, Paradi I, et al. Diversity of symbiotic root endophytes of the Helotiales in ericaceous plants and the grass, Deschampsia flexuosa. Stud Mycol. 2005;53:147–62.
Google Scholar
44.Almario J, Jeena G, Wunder J, Langen G, Zuccaro A, Zuccaro A, et al. Root-associated fungal microbiota of nonmycorrhizal Arabis alpina and its contribution to plant phosphorus nutrition. Proc Natl Acad Sci USA. 2017;114:E9403–E9412.CAS
PubMed
PubMed Central
Google Scholar
45.Gazis R, Kuo A, Riley R, LaButti K, Lipzen A, Lin J, et al. The genome of Xylona heveae provides a window into fungal endophytism. Fungal Biol. 2016;120:26–42.CAS
PubMed
Google Scholar
46.Perotto S, Daghino S, Martino E. Ericoid mycorrhizal fungi and their genomes: another side to the mycorrhizal symbiosis? New Phytol. 2018;220:1141–7.PubMed
Google Scholar
47.Wrzosek M, Ruszkiewicz-Michalska M, Sikora K, Damszel M, Sierota Z. The plasticity of fungal interactions. Mycol Prog. 2017;16:101–8.
Google Scholar
48.Parrent JL, James TY, Vasaitis R, Taylor AF. Friend or foe? Evolutionary history of glycoside hydrolase family 32 genes encoding for sucrolytic activity in fungi and its implications for plant-fungal symbioses. BMC Evol Biol. 2009;9:148.PubMed
PubMed Central
Google Scholar
49.Zhang F, Anasontzis GE, Labourel A, Champion C, Haon M, Kemppainen M, et al. The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development. New Phytol. 2018;220:1309–21.CAS
PubMed
Google Scholar
50.Mesny F, Miyauchi S, Thiergart T, Pickel B, Atanasova L, Karlsson M, et al. Genetic determinants of endophytism in the Arabidopsis root mycobiome. Nat Commun. 2021;12:7227.CAS
PubMed
Google Scholar
51.Schulz B, Sucker J, Aust HJ. Biologically active secondary metabolites of endophytic Pezicula species. Mycol Res. 1995;99:1007–15.CAS
Google Scholar
52.Tanney JB, McMullin DR, Miller JD. Toxigenic Foliar Endophytes from the Acadian Forest. In: Pirttilä A, Frank A (eds) Endophytes of Forest Trees. Forestry Sciences, vol 86. Springer, Cham. 2018;343–81.53.Yue Q, Li Y, Chen L, Zhang X, Liu X, An Z, et al. Genomics-driven discovery of a novel self-resistance mechanism in the echinocandin-producing fungus Pezicula radicicola. Environ Microbiol. 2018;20:3154–67.CAS
PubMed
Google Scholar
54.Rogers RL, Grizzard SL, Titus-McQuillan JE, Bockrath K, Patel S, Wares JP, et al. Gene family amplification facilitates adaptation in freshwater unionid bivalve Megalonaias nervosa. Mol Ecol. 2021;30:1155–73.CAS
PubMed
Google Scholar
55.Mäkinen M, Kuuskeri J, Laine P, Smolander OP, Kovalchuk A, Zeng Z, et al. Genome description of Phlebia radiata 79 with comparative genomics analysis on lignocellulose decomposition machinery of phlebioid fungi. BMC Genomics. 2019;20:430.PubMed
PubMed Central
Google Scholar
56.Yang Y, Liu X, Cai J, Chen Y, Li B, Guo Z, et al. Genomic characteristics and comparative genomics analysis of the endophytic fungus Sarocladium brachiariae. BMC Genomics. 2019;20:782.PubMed
PubMed Central
Google Scholar
57.Franco MEE, Wisecaver JH, Arnold AE, Ju YM, Slot JC, Ahrendt S, et al. Secondary metabolism drives ecological breadth in the Xylariaceae. bioRxiv. 2021. https://doi.org/10.1101/2021.06.01.446356.58.Matsuda Y, Yamakawa M, Inaba T, Obase K, Ito S. Intraspecific variation in mycelial growth of Cenococcum geophilum isolates in response to salinity gradients. Mycoscience. 2017;58:369–77.
Google Scholar
59.Taylor JW, Branco S, Gao C, Hann-Soden C, Montoya L, Sylvain I, et al. Sources of fungal genetic variation and associating it with phenotypic diversity. Microbiol Spectr. 2017;5:1–21.CAS
Google Scholar
60.Chen ECH, Morin E, Beaudet D, Noel J, Yildirir G, Ndikumana S, et al. High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis. New Phytol. 2018;220:1161–71.CAS
PubMed
Google Scholar
61.McCutcheon TL, Carroll GC, Schwab S. Genotypic diversity in populations of a fungal endophyte from Douglas Fir. Mycologia. 1993;85:180–6.
Google Scholar
62.Perotto S, Girlanda M, Martino E. Ericoid mycorrhizal fungi: some new perspectives on old acquaintances. Plant Soil. 2002;244:41–53.CAS
Google Scholar
63.Müller MM, Valjakka R, Hantula J. Genetic diversity of Lophodermium piceae in South Finland. For Pathol. 2007;37:329–37.
Google Scholar
64.Morgenstern K, Polster J-U, Krabel D. Genetic variation between and within two populations of Rhabdocline pseudotsugae in Germany. Can J Res. 2016;46:716–24.CAS
Google Scholar
65.Atwell S, Corwin JA, Soltis NE, Subedy A, Denby KJ, Kliebenstein DJ. Whole genome resequencing of Botrytis cinerea isolates identifies high levels of standing diversity. Front Microbiol. 2015;6:996.PubMed
PubMed Central
Google Scholar
66.Gasca-Pineda J, Velez P, Hosoya T. Phylogeography of post-Pleistocene population expansion in Dasyscyphella longistipitata (Leotiomycetes, Helotiales), an endemic fungal symbiont of Fagus crenata in Japan. MycoKeys. 2020;65:1–24.PubMed
PubMed Central
Google Scholar
67.Groenewald M, Linde CC, Groenewald JZ, Crous PW. Indirect evidence for sexual reproduction in Cercospora beticola populations from sugar beet. Plant Pathol. 2008;57:25–32.CAS
Google Scholar
68.Nordborg M, Charlesworth B, Charlesworth D. Increased levels of polymorphism surrounding selectively maintained sites in highly selfing species. Proc R Soc B. 1996;263:1033–9.
Google Scholar
69.Koenig D, Hagmann J, Li R, Bemm F, Slotte T, Neuffer B, et al. Long-term balancing selection drives evolution of immunity genes in Capsella. Elife. 2019;8:e43606.PubMed
PubMed Central
Google Scholar
70.Carbone I, Jakobek JL, Ramirez-Prado JH, Horn BW. Recombination, balancing selection and adaptive evolution in the aflatoxin gene cluster of Aspergillus parasiticus. Mol Ecol. 2007;16:4401–17.CAS
PubMed
Google Scholar
71.Drott MT, Debenport T, Higgins SA, Buckley DH, Milgroom MG. Fitness cost of aflatoxin production in Aspergillus flavus when competing with soil microbes could maintain balancing selection. mBio. 2019;10:e02782–18.CAS
PubMed
PubMed Central
Google Scholar
72.Chen F, Goodwin PH, Khan A, Hsiang T. Population structure and mating-type genes of Colletotrichum graminicola from Agrostis palustris. Can J Microbiol. 2002;48:427–36.CAS
PubMed
Google Scholar More