Genome evolution in fungal plant pathogens: looking beyond the two-speed genome model

Aguileta, 2009, Rapidly evolving genes in pathogens: Methods for detecting positive selection and examples among fungi, bacteria, viruses and protists, Infectection, Genetics, and Evolution, 9, 656, 10.1016/j.meegid.2009.03.010 Akagi, 2009, Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus, Eukaryot. Cell, 8, 1732, 10.1128/EC.00135-09 Batada, 2007, Evolution of chromosome organization driven by selection for reduced gene expression noise, Nat. Genet., 39, 945, 10.1038/ng2071 Bennetzen, 2014, The contributions of transposable elements to the structure, function, and evolution of plant genomes, Annu. Rev. Plant Biol., 65, 505, 10.1146/annurev-arplant-050213-035811 Brown, 2010, Rapid expansion and functional divergence of subtelomeric gene families in yeasts, Curr. Biol., 20, 895, 10.1016/j.cub.2010.04.027 Carr, 2012, Evolutionary genomics of transposable elements in Saccharomyces cerevisiae, PloS One, 7, 10.1371/journal.pone.0050978 Chujo, 2019, Complex epigenetic regulation of alkaloid biosynthesis and host interaction by heterochromatin protein I in a fungal endophyte-plant symbiosis, Fungal Genet. Biol., 125, 71, 10.1016/j.fgb.2019.02.001 Chujo, 2014, Histone H3K9 and H3K27 methylation regulates fungal alkaloid biosynthesis in a fungal endophyte-plant symbiosis, Mol. Microbiol., 92, 413, 10.1111/mmi.12567 Chuong, 2016, Regulatory evolution of innate immunity through co-option of endogenous retroviruses, Science, 351, 1083, 10.1126/science.aad5497 Collemare, 2019, Nonproteinaceous effectors: The terra incognita of plant-fungal interactions, New Phytol., 223, 590, 10.1111/nph.15785 Collemare, 2019, Chromatin-dependent regulation of secondary metabolite biosynthesis in fungi: is the picture complete?, FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev., 43, 591 Connolly, 2013, The Fusarium graminearum histone H3 K27 methyltransferase KMT6 regulates development and expression of secondary metabolite gene clusters, PLoS Genet., 9, 10.1371/journal.pgen.1003916 Cook, 2020, Chromatin features define adaptive genomic regions in a fungal plant pathogen, bioRxiv, 2020 Cook, 2015, Understanding plant immunity as a surveillance system to detect invasion, Annu. Rev. Phytopathol., 53, 541, 10.1146/annurev-phyto-080614-120114 Croll, 2012, The accessory genome as a cradle for adaptive evolution in pathogens, PLoS Pathog., 8, 10.1371/journal.ppat.1002608 Crombach, 2007, Chromosome rearrangements and the evolution of genome structuring and adaptability, Mol. Biol. Evol., 24, 1130, 10.1093/molbev/msm033 Cuypers, 2012, Virtual genomes in flux: An interplay of neutrality and adaptability explains genome expansion and streamlining, Genome Biology and Evolution, 4, 212, 10.1093/gbe/evr141 de Jonge, 2013, Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen, Genome Res., 23, 1271, 10.1101/gr.152660.112 de Jonge, 2012, Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing, Proc. Natl. Acad. Sci. U.S.A., 109, 5110, 10.1073/pnas.1119623109 Depotter, 2019, Dynamic virulence-related regions of the plant pathogenic fungus Verticillium dahliae display enhanced sequence conservation, Mol. Ecol., 28, 3482, 10.1111/mec.15168 Devos, 2002, Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis, Genome Res., 12, 1075, 10.1101/gr.132102 Dixon, 2012, Topological domains in mammalian genomes identified by analysis of chromatin interactions, Nature, 485, 376, 10.1038/nature11082 Dong, 2015, The two-speed genomes of filamentous pathogens: Waltz with plants, Curr. Opin. Genet. Dev., 35, 57, 10.1016/j.gde.2015.09.001 Duchaud, 2003, The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens, Nat. Biotechnol., 21, 1307, 10.1038/nbt886 Dutheil, 2016, A tale of genome compartmentalization: The evolution of virulence clusters in smut fungi, Genome Biology and Evolution, 8, 681, 10.1093/gbe/evw026 Fablet, 2011, Evolvability, epigenetics and transposable elements, Biomol. Concepts, 2, 333, 10.1515/BMC.2011.035 Faino, 2016, Transposons passively and actively contribute to evolution of the two-speed genome of a fungal pathogen, Genome Res., 26, 1091, 10.1101/gr.204974.116 Feurtey, 2019, 864561 Fleetwood, 2011, Abundant degenerate miniature inverted-repeat transposable elements in genomes of epichloid fungal endophytes of grasses, Genome Biology and Evolution, 3, 1253, 10.1093/gbe/evr098 Fokkens, 2018, 465070 Fouché, 2020, Stress-driven transposable element de-repression dynamics and virulence evolution in a fungal pathogen, Mol. Biol. Evol., 37, 221, 10.1093/molbev/msz216 Frantzeskakis, 2018, Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen, BMC Genom., 19, 381, 10.1186/s12864-018-4750-6 Frantzeskakis, 2019, The need for speed: Compartmentalized genome evolution in filamentous phytopathogens, Mol. Plant Pathol., 20, 3, 10.1111/mpp.12738 Fudal, 2009, Repeat-induced point mutation (RIP) as an alternative mechanism of evolution toward virulence in Leptosphaeria maculans, Mol. Plant Microbe Interact., 22, 932, 10.1094/MPMI-22-8-0932 Galagan, 2004, RIP: The evolutionary cost of genome defense, Trends Genet., 20, 417, 10.1016/j.tig.2004.07.007 Galazka, 2016, 203115 Gokcumen, 2011, Refinement of primate copy number variationhotspots identifies candidate genomic regions evolving under positive selection, Genome Biol., 12, R52, 10.1186/gb-2011-12-5-r52 Goodwin, 2011, Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis, PLoS Genet., 7, e1002070, 10.1371/journal.pgen.1002070 Grewal, 2007, Heterochromatin revisited, Nat. Rev. Genet., 8, 35, 10.1038/nrg2008 Haas, 2009, Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans, Nature, 461, 393, 10.1038/nature08358 Hartmann, 2017, A fungal wheat pathogen evolved host specialization by extensive chromosomal rearrangements, ISME J., 11, 1189, 10.1038/ismej.2016.196 Hastings, 2009, Mechanisms of change in gene copy number, Nat. Rev. Genet., 10, 551, 10.1038/nrg2593 Heermann, 2008, Comparative analysis of the Photorhabdus luminescens and the Yersinia enterocolitica genomes: Uncovering candidate genes involved in insect pathogenicity, BMC Genom., 9, 40, 10.1186/1471-2164-9-40 Hocher, 2020, Subtelomeres as specialized chromatin domains, Bioessays, 42, 10.1002/bies.201900205 Hollister, 2009, Epigenetic silencing of transposable elements: A trade-off between reduced transposition and deleterious effects on neighboring gene expression, Genome Res., 19, 1419, 10.1101/gr.091678.109 Hurst, 2004, The evolutionary dynamics of eukaryotic gene order, Nat. Rev. Genet., 5, 299, 10.1038/nrg1319 Janevska, 2018, Elucidation of the two H3K36me3 histone methyltransferases Set 2 and Ash 1 in Fusarium fujikuroi unravels their different chromosomal targets and a major impact of Ash1 on genome stability, Genetics, 208, 153, 10.1534/genetics.117.1119 Juárez-Reyes, 2019, Chromatin architecture and virulence-related gene expression in eukaryotic microbial pathogens, Curr. Genet., 65, 435, 10.1007/s00294-018-0903-z Kawakatsu, 2016, Epigenomic diversity in a global collection of Arabidopsis thaliana accessions, Cell, 166, 492, 10.1016/j.cell.2016.06.044 Kema, 2018, Stress and sexual reproduction affect the dynamics of the wheat pathogen effector AvrStb6 and strobilurin resistance, Nat. Genet., 23, 678 Kidwell, 2001, Perspective: Transposable elements, parasitic DNA, and genome evolution, Evolution, 55, 1, 10.1111/j.0014-3820.2001.tb01268.x Kombrink, 2017, Verticillium dahliae LysM effectors differentially contribute to virulence on plant hosts, Mol. Plant Pathol., 18, 596, 10.1111/mpp.12520 Laun, 2006, The leukocyte receptor complex in chicken is characterized by massive expansion and diversification of immunoglobulin-like loci, PLoS Genet., 2, e73, 10.1371/journal.pgen.0020073 Leister, 2004, Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene, Trends Genet., 20, 116, 10.1016/j.tig.2004.01.007 Liu, 2020 Lo Presti, 2015, Fungal effectors and plant susceptibility, Annu. Rev. Plant Biol., 66, 513, 10.1146/annurev-arplant-043014-114623 Lynch, 2007 Ma, 2010, Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium, Nature, 464, 367, 10.1038/nature08850 Makova, 2015, The effects of chromatin organization on variation in mutation rates in the genome, Nat. Rev. Genet., 16, 213, 10.1038/nrg3890 Mascher, 2017, A chromosome conformation capture ordered sequence of the barley genome, Nature, 544, 427, 10.1038/nature22043 Möller, 2019, Destabilization of chromosome structure by histone H3 lysine 27 methylation, PLoS Genet., 15, 10.1371/journal.pgen.1008093 Müller, 2019, A chromosome-scale genome assembly reveals a highly dynamic effector repertoire of wheat powdery mildew, New Phytol., 221, 2176, 10.1111/nph.15529 Muszewska, 2019, Transposable elements contribute to fungal genes and impact fungal lifestyle, Sci. Rep., 9, 4307, 10.1038/s41598-019-40965-0 Nottensteiner, 2018, A barley powdery mildew fungus non-autonomous retrotransposon encodes a peptide that supports penetration success on barley, J. Exp. Bot., 69, 3745, 10.1093/jxb/ery174 Oliver, 2009, Transposable elements: Powerful facilitators of evolution, Bioessays, 31, 703, 10.1002/bies.200800219 Omrane, 2017, Plasticity of the MFS1 promoter leads to multidrug resistance in the wheat pathogen Zymoseptoria tritici, mSphere, 2, 10.1128/mSphere.00393-17 Papkou, 2019, The genomic basis of Red Queen dynamics during rapid reciprocal host-pathogen coevolution, Proc. Natl. Acad. Sci. Unit. States Am., 116, 923, 10.1073/pnas.1810402116 Peter, 2018, Genome evolution across 1,011 Saccharomyces cerevisiae isolates, Nature, 556, 339, 10.1038/s41586-018-0030-5 Peter, 2016, Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum, Nat. Commun., 7, 12662, 10.1038/ncomms12662 Pfannenstiel, 2019, On top of biosynthetic gene clusters: How epigenetic machinery influences secondary metabolism in fungi, Biotechnol. Adv., 37, 107345, 10.1016/j.biotechadv.2019.02.001 Plissonneau, 2018, Pangenome analyses of the wheat pathogen Zymoseptoria tritici reveal the structural basis of a highly plastic eukaryotic genome, BMC Biol., 16, 5, 10.1186/s12915-017-0457-4 Plissonneau, 2016, The evolution of orphan regions in genomes of a fungal pathogen of wheat, mBio, 7, e01231, 10.1128/mBio.01231-16 Raffaele, 2010, Genome evolution following host jumps in the Irish potato famine pathogen lineage, Science, 330, 1540, 10.1126/science.1193070 Raffaele, 2012, Genome evolution in filamentous plant pathogens: why bigger can be better, Nat. Rev. Microbiol., 10, 417, 10.1038/nrmicro2790 Rebollo, 2011, Retrotransposon-induced heterochromatin spreading in the mouse revealed by insertional polymorphisms, PLoS Genet., 7, 10.1371/journal.pgen.1002301 Roach, 2005, The evolution of vertebrate Toll-like receptors, Proc. Natl. Acad. Sci. U.S.A., 102, 9577, 10.1073/pnas.0502272102 Rouxel, 2011, Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations, Nat. Commun., 2, 202, 10.1038/ncomms1189 Rovenich, 2014, Filamentous pathogen effector functions: of pathogens, hosts and microbiomes, Curr. Opin. Plant Biol., 20C, 96, 10.1016/j.pbi.2014.05.001 Sabelleck, 2018, Novel jack-in-the-box effector of the barley powdery mildew pathogen?, J. Exp. Bot., 69, 3511, 10.1093/jxb/ery192 Sánchez-Vallet, 2018, The genome biology of effector gene evolution in filamentous plant pathogens, Annu. Rev. Phytopathol., 56, 21, 10.1146/annurev-phyto-080516-035303 Sasaki, 2014, Heterochromatin controls γH2A localization in Neurospora crassa, Eukaryot. Cell, 13, 990, 10.1128/EC.00117-14 Schirawski, 2010, Pathogenicity determinants in smut fungi revealed by genome comparison, Science, 330, 1546, 10.1126/science.1195330 Schotanus, 2015, Histone modifications rather than the novel regional centromeres of Zymoseptoria tritici distinguish core and accessory chromosomes, Epigenet. Chromatin, 8, 41, 10.1186/s13072-015-0033-5 Schrader, 2014, Transposable element islands facilitate adaptation to novel environments in an invasive species, Nat. Commun., 5, 10.1038/ncomms6495 Schrader, 2019, The impact of transposable elements in adaptive evolution, Mol. Ecol., 28, 1537, 10.1111/mec.14794 Schuster-Böckler, 2012, Chromatin organization is a major influence on regional mutation rates in human cancer cells, Nature, 488, 504, 10.1038/nature11273 Schwessinger, 2020, Distinct life histories impact dikaryotic genome evolution in the rust fungus Puccinia striiformis causing stripe rust in wheat, Genome Biology and Evolution, 12, 597, 10.1093/gbe/evaa071 Schwessinger, 2018, A near-complete haplotype-phased genome of the dikaryotic wheat stripe rust fungus Puccinia striiformis f. sp. tritici reveals high interhaplotype diversity, mBio, 9, 10.1128/mBio.02275-17 Seidl, 2016, Chromatin biology impacts adaptive evolution of filamentous plant pathogens, PLoS Pathog., 12, 10.1371/journal.ppat.1005920 Seidl, 2014, Sex or no sex: Evolutionary adaptation occurs regardless, Bioessays, 36, 335, 10.1002/bies.201300155 Seidl, 2017, Transposable elements direct the coevolution between plants and microbes, Trends Genet., 33, 842, 10.1016/j.tig.2017.07.003 Sentmanat, 2012, Ectopic assembly of heterochromatin in Drosophila melanogaster triggered by transposable elements, Proc. Natl. Acad. Sci. Unit. States Am., 109, 14104, 10.1073/pnas.1207036109 Slotkin, 2007, Transposable elements and the epigenetic regulation of the genome, Nat. Rev. Genet., 8, 272, 10.1038/nrg2072 Snelders, 2018, Plant pathogen effector proteins as manipulators of host microbiomes?, Mol. Plant Pathol., 19, 257, 10.1111/mpp.12628 Soyer, 2014, Epigenetic control of effector gene expression in the plant pathogenic fungus Leptosphaeria maculans, PLoS Genet., 10, 10.1371/journal.pgen.1004227 Soyer, 2019, 544627 Stam, 2018, A new reference genome shows the one-speed genome structure of the barley pathogen Ramularia collo-cygni, Genome Biology and Evolution, 10, 3243, 10.1093/gbe/evy240 Strotz, 2018, Getting somewhere with the Red Queen: Chasing a biologically modern definition of the hypothesis, Biol. Lett., 14, 20170734, 10.1098/rsbl.2017.0734 Stuart, 2016, Population scale mapping of transposable element diversity reveals links to gene regulation and epigenomic variation, eLife, 5, 10.7554/eLife.20777 Sun, 2016, Preferential protection of genetic fidelity within open chromatin by the mismatch repair machinery, J. Biol. Chem., 291, 17692, 10.1074/jbc.M116.719971 Thon, 2006, The role of transposable element clusters in genome evolution and loss of synteny in the rice blast fungus Magnaporthe oryzae, Genome Biol., 7, R16, 10.1186/gb-2006-7-2-r16 van Dam, 2017, A mobile pathogenicity chromosome in Fusarium oxysporum for infection of multiple cucurbit species, Sci. Rep., 7, 9042, 10.1038/s41598-017-07995-y van de Vossenberg, 2019, The Synchytrium endobioticum AvrSen1 triggers a hypersensitive response in Sen 1 potatoes while natural variants evade detection, Mol. Plant Microbe Interact., 32, 1536, 10.1094/MPMI-05-19-0138-R van de Vossenberg, 2019, Comparative genomics of chytrid fungi reveal insights into the obligate biotrophic and pathogenic lifestyle of Synchytrium endobioticum, Sci. Rep., 9, 8672, 10.1038/s41598-019-45128-9 van Wersch, 2019, Stronger when together: Clustering of plant NLR disease resistance genes, Trends Plant Sci., 24, 688, 10.1016/j.tplants.2019.05.005 Wang, 2014, Chromosome boundary elements and regulation of heterochromatin spreading, Cell. Mol. Life Sci., 71, 4841, 10.1007/s00018-014-1725-x Wang, 2015, Rapid epigenetic adaptation to uncontrolled heterochromatin spreading, eLife, 4, 10.7554/eLife.06179 Wang, 2017, Characterization of the two-speed subgenomes of Fusarium graminearum reveals the fast-speed subgenome specialized for adaption and infection, Front. Plant Sci., 8, 140 Waterfield, 2002, Genomic islands in Photorhabdus, Trends Microbiol., 10, 541, 10.1016/S0966-842X(02)02463-0 Wicker, 2007, A unified classification system for eukaryotic transposable elements, Nat. Rev. Genet., 8, 973, 10.1038/nrg2165 Winter, 2018, Repeat elements organise 3D genome structure and mediate transcription in the filamentous fungus Epichloë festucae, PLoS Genet., 14, 10.1371/journal.pgen.1007467 Wyka, 2020, Whole genome comparisons of ergot fungi reveals the divergence and evolution of species within the genus Claviceps are the result of varying mechanisms driving genome evolution and host range expansion, bioRxiv, 2020, 39230 Xia, 2018, Genomic insights into host adaptation between the wheat stripe rust pathogen (Puccinia striiformis f. sp. tritici) and the barley stripe rust pathogen (Puccinia striiformis f. sp. hordei), BMC Genom., 19, 664, 10.1186/s12864-018-5041-y Yasuhara, 2005, Evolution of heterochromatic genes of Drosophila, Proc. Natl. Acad. Sci. Unit. States Am., 102, 10958, 10.1073/pnas.0503424102 Yeaman, 2013, Genomic rearrangements and the evolution of clusters of locally adaptive loci, Proc. Natl. Acad. Sci. Unit. States Am., 110, E1743, 10.1073/pnas.1219381110 Yue, 2017, Contrasting evolutionary genome dynamics between domesticated and wild yeasts, Nat. Genet., 49, 913, 10.1038/ng.3847 Zhong, 2017, A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene, New Phytol., 214, 619, 10.1111/nph.14434