Universität zu Köln

Mesny, Fantin ORCID: 0000-0002-3044-1398 (2024). Arabidopsis thaliana root-associated fungi: function, evolution and genomic signatures. PhD thesis, Universität zu Köln.

PDF (Final, accepted PhD thesis of Fantin Mesny) FantinMesny_PhD_thesis_uncompressed.pdf - Accepted Version Bereitstellung unter der CC-Lizenz: Creative Commons Attribution. Download (61MB)

Abstract

While mycorrhizae have been studied for decades, little is known about fungi that do not establish symbiotic structures, but have the ability to colonize roots of asymptomatic plants in nature. The non-mycorrhizal model plant Arabidopsis thaliana hosts in its roots diverse fungal communities, that were previously reported to negatively impact its health in absence of protection from bacterial commensals and innate immune responses. With this thesis, I aimed to better characterize this detrimental mycobiota, focusing on its function, evolution and genomic signatures. While multiple pieces of evidence pointed to the endophytism of A. thaliana mycobiota members, predicted evolutionary histories revealed that most of these fungi derived from pathogenic ancestors. Re-colonization experiments with individual strains highlighted diverse fungal effects on plant performance, spanning along the mutualist-pathogenic continuum. This gradient of effects was correlated to fungal root colonization efficiency, highlighting that fungi with detrimental effects dominate in natural root samples. We showed that pectin-degrading enzymes from family PL1_7 contribute in the aggressiveness of endophytic colonization. While further genomic and transcriptomic analyses corroborated the major role of carbohydrate-active enzymes in root endophytic colonization, intra-species comparative genomics of highly prevalent mycobiota member Plectosphaerella cucumerina revealed a genomic architecture favoring the fast evolution of effector-encoding genes. We notably identified in this species a candidate genomic region predicted to be involved in fungal adaptation to A. thaliana. Taken together, the results compiled in this thesis offer a better understanding of the fine line between endophytism and parasitism in the root mycobiota. They show that fungi robustly colonizing A. thaliana roots in nature rely on carbohydrate-active enzymes to degrade host cell walls, and likely on effectors to overcome innate immune responses.

Item Type:	Thesis (PhD thesis)
Creators:	Creators Email ORCID ORCID Put Code Mesny, Fantin fantin.mesny@me.com orcid.org/0000-0002-3044-1398 UNSPECIFIED
Contributors:	Contribution Name Email Thesis advisor Hacquard, Stéphane hacquard@mpipz.mpg.de
URN:	urn:nbn:de:hbz:38-742898
Date:	2024
Language:	English
Faculty:	Faculty of Mathematics and Natural Sciences
Divisions:	Außeruniversitäre Forschungseinrichtungen > MPI for Plant Breeding Research
Subjects:	Life sciences
Uncontrolled Keywords:	Keywords Language fungi English genomics English plant microbiota English arabidopsis thaliana English carbohydrate-active enzymes English evolution English genetics English endophytes English mycobiota English effectors English plant-microbes interactions English
Date of oral exam:	1 December 2022
Referee:	Name Academic Title Thomma, Bart Professor Stukenbrock, Eva Professor
Related URLs:	Publication
Funders:	Deutsche Forschungsgemeinschaft
References:	1. Gross, M. How plants grow their microbiome. Current Biology 32, R97–R100. doi:10. 1016/J.CUB.2022.01.044 (2022). 2. Trivedi, P., Leach, J. E., Tringe, S. G., Sa, T. & Singh, B. K. Plant–microbiome interac- tions: from community assembly to plant health. Nature Reviews Microbiology 18, 607– 621. doi:10.1038/s41579-020-0412-1 (2020). 3. Getzke, F., Thiergart, T. & Hacquard, S. Contribution of bacterial-fungal balance to plant and animal health. Current Opinion in Microbiology 49, 66–72. doi:10.1016/J.MIB.2019. 10.009 (2019). 4. Vogel, J. Unique aspects of the grass cell wall. Current Opinion in Plant Biology 11, 301– 307. doi:10.1016/j.pbi.2008.03.002 (2008). 5. Bacic, A. Breaking an impasse in pectin biosynthesis. PNAS 103, 5639–5640. doi:10.1073/ pnas.0601297103 (2006). 6. Studer, M. H. et al. Lignin content in natural Populus variants affects sugar release. PNAS 108, 6300–6305. doi:10.1073/pnas.1009252108 (2011). 7. Müller,D.B.,Vogel,C.,Bai,Y.&Vorholt,J.A.Theplantmicrobiota:systems-levelinsights and perspectives. Annual Review of Genetics 50, 211–234. doi:10.1146/ANNUREV-GENET- 120215-034952 (2016). 8. Roman-Reyna, V. et al. The rice leaf microbiome has a conserved community structure controlled by complex host-microbe interactions. bioRxiv, 615278. doi:10.1101/615278 (2019). 9. Teixeira, P. J. P., Colaianni, N. R., Fitzpatrick, C. R. & Dangl, J. L. Beyond pathogens: microbiota interactions with the plant immune system. Current Opinion in Microbiology 49, 7–17. doi:10.1016/J.MIB.2019.08.003 (2019). 10. Hacquard, S., Spaepen, S., Garrido-Oter, R. & Schulze-Lefert, P. Interplay between innate immunity and the plant microbiota. Annual Review of Phytopathology 55, 565–589. doi:10. 1146/ANNUREV-PHYTO-080516-035623 (2017). 11. Xin, X. F. et al. Bacteria establish an aqueous living space in plants crucial for virulence. Nature 539, 524–529. doi:10.1038/nature20166 (2016). 12. Wolinska, K. W. et al. Tryptophan metabolism and bacterial commensals prevent fungal dysbiosis in Arabidopsis roots. PNAS 118, 21115–21118. doi:10.1073/pnas.2111521118 (2021). 13. Lebeis, S. L. et al. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349, 860–864. doi:10.1126/science.aaa8764 (2015). 14. Tzipilevich, E., Russ, D., Dangl, J. L. & Benfey, P. N. Plant immune system activation is necessary for efficient root colonization by auxin-secreting beneficial bacteria. Cell Host & Microbe 29, 1507–1520.e4. doi:10.1016/J.CHOM.2021.09.005 (2021). 15. Plett, J. M. et al. Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes. PNAS 111, 8299– 8304. doi:10.1073/pnas.1322671111 (2014). 16. Berger, F. & Gutjahr, C. Factors affecting plant responsiveness to arbuscular mycorrhiza. Current Opinion in Plant Biology 59, 101994. doi:10.1016/J.PBI.2020.101994 (2021). 17. Teixeira, P. J. et al. Specific modulation of the root immune system by a community of commensal bacteria. PNAS 118, e2100678118. doi:10.1073/PNAS.2100678118/SUPPL_ FILE/PNAS.2100678118.SD07.XLSX (2021). 18. Deng, S. et al. Genome-wide association study reveals plant loci controlling heritability of the rhizosphere microbiome. The ISME Journal 15, 3181–3194. doi:10.1038/s41396- 021-00993-z (2021). 19. Escudero-Martinez, C. et al. Identifying plant genes shaping microbiota composition in the barley rhizosphere. Nature Communications 13, 1–14. doi:10.1038/s41467-022-31022- y (2022). 20. Neina, D. The role of soil pH in plant nutrition and soil remediation. Applied and Environ- mental Soil Science. doi:10.1155/2019/5794869 (2019). 21. Finkel, O. M. et al. The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response. PLOS Biology 17, e3000534. doi:10.1371/ JOURNAL.PBIO.3000534 (2019). 22. Harbort, C. J. et al. Root-secreted coumarins and the microbiota interact to improve iron nutrition in Arabidopsis. Cell Host & Microbe 28, 825–837.e6. doi:10.1016/J.CHOM. 2020.09.006 (2020). 23. Thiergart, T. et al. Root microbiota assembly and adaptive differentiation among European Arabidopsis populations. Nature Ecology and Evolution 4, 122–131. doi:10.1038/s41559- 019-1063-3 (2020). 24. Carrell, A. A. et al. Habitat-adapted microbial communities mediate Sphagnum peatmoss resilience to warming. New Phytologist 234, 2111–2125. doi:10.1111/NPH.18072 (2022). 25. King, W. L. et al. Soil salinization accelerates microbiome stabilization in iterative selections for plant performance. New Phytologist 234, 2101–2110. doi:10.1111/NPH.17774 (2022). 26. Naylor, D., Degraaf, S., Purdom, E. & Coleman-Derr, D. Drought and host selection influ- ence bacterial community dynamics in the grass root microbiome. The ISME Journal 11, 2691–2704. doi:10.1038/ismej.2017.118 (2017). 27. Xie, J. et al. Drought stress triggers shifts in the root microbial community and alters func- tional categories in the microbial gene pool. Frontiers in Microbiology 12, 3066. doi:10. 3389/FMICB.2021.744897/BIBTEX (2021). 28. Meyer, K. M. et al. Plant neighborhood shapes diversity and reduces interspecific variation of the phyllosphere microbiome. The ISME Journal 16, 1376–1387. doi:10.1038/s41396- 021-01184-6 (2022). 29. Vannier, N., Bittebiere, A. K., Mony, C. & Vandenkoornhuyse, P. Root endophytic fungi im- pact host plant biomass and respond to plant composition at varying spatio-temporal scales. Fungal Ecology 44, 100907. doi:10.1016/j.funeco.2019.100907 (2020). 30. Prado, A., Marolleau, B., Vaissie`re, B. E., Barret, M. & Torres-Cortes, G. Insect pollination: an ecological process involved in the assembly of the seed microbiota. Scientific Reports 10, 1–11. doi:10.1038/s41598-020-60591-5 (2020). 31. Hassani, M. A., Dura ́n, P. & Hacquard, S. Microbial interactions within the plant holobiont. Microbiome 6, 1–17. doi:10.1186/S40168-018-0445-0 (2018). 32. Agler, M. T. et al. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLOS Biology 14, e1002352. doi:10.1371/JOURNAL.PBIO.1002352 (2016). 33. Eitzen, K., Sengupta, P., Kroll, S., Kemen, E. & Doehlemann, G. A fungal member of the Arabidopsis thaliana phyllosphere antagonizes Albugo laibachii via a GH25 lysozyme. eLife 10, 1. doi:10.7554/ELIFE.65306 (2021). 34. Snelders, N. C. et al. Microbiome manipulation by a soil-borne fungal plant pathogen us- ing effector proteins. Nature Plants 6, 1365–1374. doi:10.1038/s41477-020-00799-5 (2020). 35. Pontrelli, S. et al. Metabolic cross-feeding structures the assembly of polysaccharide de- grading communities. Science Advances 8, 3076. doi:10.1126/sciadv.abk3076 (2022). 36. Nagy, L. G. et al. in The Fungal Kingdom 35–56 (ASM Press, Washington, DC, USA, 2017). doi:10.1128/9781555819583.ch2. 37. Martin, F. M., Uroz, S. & Barker, D. G. Ancestral alliances: Plant mutualistic symbioses with fungi and bacteria. Science 356, eaad4501. doi:10.1126/science.aad4501 (2017). 38. Gan, T. et al. Cryptic terrestrial fungus-like fossils of the early Ediacaran period. Nature Communications 2021 12:1 12, 1–12. doi:10.1038/s41467-021-20975-1 (2021). 39. Peay, K. G., Kennedy, P. G. & Talbot, J. M. Dimensions of biodiversity in the Earth my- cobiome. Nature Reviews Microbiology 2016 14:7 14, 434–447. doi:10.1038/nrmicro. 2016.59 (2016). 40. Lindahl, B. D. & Tunlid, A. Ectomycorrhizal fungi – potential organic matter decomposers, yet not saprotrophs. New Phytologist 205, 1443–1447. doi:10.1111/NPH.13201 (2015). 41. Crowther, T. W., Boddy, L. & Hefin Jones, T. Functional and ecological consequences of saprotrophic fungus–grazer interactions. The ISME Journal 6, 1992. doi:10.1038/ISMEJ. 2012.53 (2012). 42. Hage, H. & Rosso, M. N. Evolution of fungal carbohydrate-active enzyme portfolios and adaptation to plant cell-wall polymers. Journal of Fungi 7, 1–16. doi:10.3390/JOF7030185 (2021). 43. Doehlemann,G.,Ökmen,B.,Zhu,W.&Sharon,A.Plantpathogenicfungi.Microbiology Spectrum 5, 5.1.14. doi:10.1128/MICROBIOLSPEC.FUNK-0023-2016 (2017). 44. Van Vu, B., Itoh, K., Nguyen, Q. B., Tosa, Y. & Nakayashiki, H. Cellulases belonging to glycoside hydrolase families 6 and 7 contribute to the virulence of Magnaporthe oryzae. Molecular Plant-Microbe Interactions 25, 1135–1141. doi:10.1094/MPMI-02-12-0043-R (2012). 45. Redkar, A. et al. Conserved secreted effectors contribute to endophytic growth and multihost plant compatibility in a vascular wilt fungus. The Plant Cell 34, 3214–3232. doi:10.1093/ PLCELL/KOAC174 (2022). 46. Zhang, L. et al. Fungal endopolygalacturonases are recognized as microbe-associated molec- ular patterns by the Arabidopsis receptor-like protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1. Plant Physiology 164, 352–364. doi:10.1104/PP.113. 230698 (2014). 47. Lo Presti, L. et al. Fungal effectors and plant susceptibility. Annual Reviews in Plant Pathol- ogy 66, 513–545. doi:10.1146/ANNUREV-ARPLANT-043014-114623 (2015). 48. Tanaka, S. et al. A secreted Ustilago maydis effector promotes virulence by targeting antho- cyanin biosynthesis in maize. eLife 3. doi:10.7554/ELIFE.01355.001 (2014). 49. De Jonge, R. et al. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329, 953–955. doi:10.1126/SCIENCE.1190859 (2010). 50. Shen, Q., Liu, Y. & Naqvi, N. I. Fungal effectors at the crossroads of phytohormone sig- naling. Current Opinion in Microbiology 46, 1–6. doi:10.1016/J.MIB.2018.01.006 (2018). 51. Djamei, A. et al. Metabolic priming by a secreted fungal effector. Nature 478, 395–398. doi:10.1038/nature10454 (2011). 52. Van Den Burg, H. A., Harrison, S. J., Joosten, M. H., Vervoort, J. & De Wit, P. J. Cladospo- rium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accu- mulating during infection. Molecular Plant-Microbe Interactions 19, 1420–1430. doi:10. 1094/MPMI-19-1420 (2007). 53. Van Esse, H. P. et al. The Cladosporium fulvum virulence protein Avr2 inhibits host pro- teases required for basal defense. The Plant Cell 20, 1948–1963. doi:10.1105/TPC.108. 059394 (2008). 54. Ökmen, B. et al. Detoxification of α-tomatine by Cladosporium fulvum is required for full virulence on tomato. New Phytologist 198, 1203–1214. doi:10.1111/NPH.12208 (2013). 55. Dutton, M. V. & Evans, C. S. Oxalate production by fungi: its role in pathogenicity and ecology in the soil environment. Canadian Journal of Microbiology 42, 881–895. doi:10. 1139/M96-114 (2011). 56. Manning, V. A., Hardison, L. K. & Ciuffetti, L. M. Ptr ToxA interacts with a chloroplast- localized protein. Molecular Plant-Microbe Interactions 20, 168–177. doi:10.1094/MPMI- 20-2-0168 (2007). 57. Faris, J. D. et al. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. PNAS 107, 13544–13549. doi:10.1073/pnas. 1004090107 (2010). 58. Vela ́squez, A. C., Castroverde, C. D. M. & He, S. Y. Plant–pathogen warfare under changing climate conditions. Current Biology 28, R619–R634. doi:10.1016/J.CUB.2018.03.054 (2018). 59. Brundrett, M. Diversity and classification of mycorrhizal associations. Biological Reviews 79, 473–495. doi:10.1017/S1464793103006316 (2004). 60. Kakouridis, A. et al. Routes to roots: direct evidence of water transport by arbuscular my- corrhizal fungi to host plants. New Phytologist 236, 210–221. doi:10.1111/NPH.18281 (2022). 61. Salvioli di Fossalunga, A. & Novero, M. To trade in the field: the molecular determinants of arbuscular mycorrhiza nutrient exchange. Chemical and Biological Technologies in Agri- culture 6, 1–12. doi:10.1186/S40538-019-0150-7 (2019). 62. Karandashov, V. & Bucher, M. Symbiotic phosphate transport in arbuscular mycorrhizas. Trends in Plant Science 10, 22–29. doi:10.1016/j.tplants.2004.12.003 (2005). 63. Bucher, M. Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytologist 173, 11–26. doi:10.1111/J.1469-8137.2006.01935.X (2007). 64. Malar C, M. et al. The genome of Geosiphon pyriformis reveals ancestral traits linked to the emergence of the arbuscular mycorrhizal symbiosis. Current Biology 31, 1570–1577.e4. doi:10.1016/J.CUB.2021.01.058 (2021). 65. Keymer, A. & Gutjahr, C. Cross-kingdom lipid transfer in arbuscular mycorrhiza symbiosis and beyond. Current Opinion in Plant Biology 44, 137–144. doi:10.1016/J.PBI.2018. 04.005 (2018). 66. Kiers, E. T. et al. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333, 880–882. doi:10.1126/science.1208473 (2011). 67. Martin, F., Kohler, A., Murat, C., Veneault-Fourrey, C. & Hibbett, D. S. Unearthing the roots of ectomycorrhizal symbioses. Nature Reviews Microbiology 14, 760–773. doi:10.1038/ nrmicro.2016.149 (2016). 68. Liu, Y., Li, X. & Kou, Y. Ectomycorrhizal fungi: Participation in nutrient turnover and com- munity assembly pattern in forest ecosystems. Forests 11, 453. doi:10.3390/F11040453 (2020). 69. Miyauchi, S. et al. Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits. Nature Communications 11, 1–17. doi:10.1038/ s41467-020-18795-w (2020). 70. Hardoim, P. R. et al. The hidden world within plants: Ecological and evolutionary considera- tions for defining functioning of microbial endophytes. Microbiology and Molecular Biology Reviews 79, 293–320. doi:10.1128/MMBR.00050-14 (2015). 71. Schulz, B. & Boyle, C. The endophytic continuum. Mycological research 109, 661–686. doi:10.1017/S095375620500273X (2005). 72. Collinge, D. B., Jensen, B. & Jørgensen, H. J. Fungal endophytes in plants and their rela- tionship to Plant Disease. Current Opinion in Microbiology 69, 102177. doi:10.1016/J. MIB.2022.102177 (2022). 73. Glynou, K. et al. The local environment determines the assembly of root endophytic fungi at a continental scale. Environmental Microbiology 18, 2418–2434. doi:10.1111/1462- 2920.13112 (2016). 74. Kia, S. H. et al. Influence of phylogenetic conservatism and trait convergence on the interac- tions between fungal root endophytes and plants. ISME Journal 11, 777–790. doi:10.1038/ ismej.2016.140 (2017). 75. Glynou, K., Nam, B., Thines, M. & Macia ́-Vicente, J. G. Facultative root-colonizing fungi dominate endophytic assemblages in roots of nonmycorrhizal Microthlaspi species. New Phytologist 217, 1190–1202. doi:10.1111/nph.14873 (2018). 76. Fesel, P. H. & Zuccaro, A. Dissecting endophytic lifestyle along the parasitism/mutualism continuum in Arabidopsis. Current Opinion in Microbiology 32, 103–112. doi:10.1016/j. mib.2016.05.008 (2016). 77. Lahrmann, U. et al. Mutualistic root endophytism is not associated with the reduction of saprotrophic traits and requires a noncompromised plant innate immunity. New Phytologist 207, 841–857. doi:10.1111/nph.13411 (2015). 78. Hiruma, K. et al. Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status-dependent. Cell 165, 464–474. doi:10.1016/j.cell.2016.02.028 (2016). 79. Hacquard, S. et al. Survival trade-offs in plant roots during colonization by closely re- lated beneficial and pathogenic fungi. Nature Communications 7, 1–13. doi:10 . 1038 / ncomms11362 (2016). 80. Hettiarachchige, I. K. et al. Global changes in asexual Epichloe ̈ transcriptomes during the early stages, from seed to seedling, of symbiotum establishment. Microorganisms 9, 991. doi:10.3390/MICROORGANISMS9050991 (2021). 81. Almario, J. et al. Root-associated fungal microbiota of nonmycorrhizal Arabis alpina and its contribution to plant phosphorus nutrition. PNAS 114, E9403–E9412. doi:10.1073/pnas. 1710455114 (2017). 82. Knapp, D. G. et al. Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi. Scientific Reports 8, 6321. doi:10. 1038/s41598-018-24686-4 (2018). 83. Zhang, H. et al. A 2-kb mycovirus converts a pathogenic fungus into a beneficial endophyte for Brassica protection and yield enhancement. Molecular Plant 13, 1420–1433. doi:10. 1016/J.MOLP.2020.08.016 (2020). 84. Hiruma, K. et al. A fungal secondary metabolism gene cluster enables mutualist-pathogen transition in root endophyte Colletotrichum tofieldiae. bioRxiv. doi:10.1101/2022.07.07. 499222 (2022). 85. Poveda, J., D ́ıaz-Gonza ́lez, S., D ́ıaz-Urbano, M., Velasco, P. & Sacrista ́n, S. Fungal endo- phytes of Brassicaceae: Molecular interactions and crop benefits. Frontiers in Plant Science, 2605. doi:10.3389/FPLS.2022.932288 (2022). 86. Macia ́-Vicente,J.G.etal.Nutrientavailabilitydoesnotaffectcommunityassemblyin root-associated fungi but determines fungal effects on plant growth. mSystems 7 (ed Schadt, C. W.) e00304–22. doi:10.1128/MSYSTEMS.00304-22 (2022). 87. Dura ́n, P. et al. Microbial interkingdom interactions in roots promote Arabidopsis survival. Cell 175, 973–983.e14. doi:10.1016/j.cell.2018.10.020 (2018). 88. Mahdi, L. K. et al. The fungal root endophyte Serendipita vermifera displays inter-kingdom synergistic beneficial effects with the microbiota in Arabidopsis thaliana and barley. The ISME Journal 16, 876–889. doi:10.1038/s41396-021-01138-y (2021). 89. Li, J., Cornelissen, B. & Rep, M. Host-specificity factors in plant pathogenic fungi. Fungal Genetics and Biology 144, 103447. doi:10.1016/J.FGB.2020.103447 (2020). 90. Ayukawa, Y. et al. A pair of effectors encoded on a conditionally dispensable chromosome of Fusarium oxysporum suppress host-specific immunity. Communications Biology 4, 1–12. doi:10.1038/s42003-021-02245-4 (2021). 91. Mesny, F. et al. Genetic determinants of endophytism in the Arabidopsis root mycobiome. Nature Communications 12, 1–15. doi:10.1038/s41467-021-27479-y (2021). 92. Hou, S. et al. A microbiota–root–shoot circuit favours Arabidopsis growth over defence under suboptimal light. Nature Plants 7, 1078–1092. doi:10.1038/s41477-021-00956-4 (2021). 93. Van der Heijden, M. G., de Bruin, S., Luckerhoff, L., van Logtestijn, R. S. & Schlaeppi, K. A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment. The ISME Journal 10, 389–399. doi:10.1038/ismej.2015.120 (2015). 94. Carrion, V. J. et al. Pathogen-induced activation of disease-suppressive functions in the en- dophytic root microbiome. Science 366, 606–612. doi:10.1126/SCIENCE.AAW9285 (2019). 95. Wagg, C., Schlaeppi, K., Banerjee, S., Kuramae, E. E. & van der Heijden, M. G. A. Fungal- bacterial diversity and microbiome complexity predict ecosystem functioning. Nature Com- munications 10, 1–10. doi:10.1038/s41467-019-12798-y (2019). 96. Brundrett, M. C. & Tedersoo, L. Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytologist 220, 1108–1115. doi:10.1111/nph.14976 (2018). 97. Delavaux, C. S. et al. Mycorrhizal fungi influence global plant biogeography. Nature Ecol- ogy and Evolution 3, 424–429. doi:10.1038/s41559-019-0823-4 (2019). 98. Soudzilovskaia, N. A. et al. Global mycorrhizal plant distribution linked to terrestrial carbon stocks. Nature Communications 10, 1–10. doi:10.1038/s41467-019-13019-2 (2019). 99. Steidinger, B. S. et al. Climatic controls of decomposition drive the global biogeography of forest-tree symbioses. Nature 569, 404–408. doi:10.1038/s41586-019-1128-0 (2019). 100. Lugtenberg, B. J., Caradus, J. R. & Johnson, L. J. Fungal endophytes for sustainable crop production. FEMS Microbiology Ecology 92, fiw194. doi:10.1093/FEMSEC/FIW194 (2016). 101. U’Ren, J. M. et al. Host availability drives distributions of fungal endophytes in the imper- illed boreal realm. Nature Ecology and Evolution 3, 1430–1437. doi:10.1038/s41559- 019-0975-2 (2019). 102. Macia-Vicente, J. G., Piepenbring, M. & Koukol, O. Brassicaceous roots as an unexpected diversity hot-spot of helotialean endophytes. IMA Fungus 11, 1–23. doi:10.1186/s43008- 020-00036-w (2020). 103. Oita, S. et al. Climate and seasonality drive the richness and composition of tropical fungal endophytes at a landscape scale. Communications Biology 4, 1–11. doi:10.1038/s42003- 021-01826-7 (2021). 104. Jumpponen, A., Herrera, J., Porras-Alfaro, A. & Rudgers, J. in Biogeography of Mycorrhizal Symbiosis 195–222 (Springer International Publishing, Cham, 2017). doi:10.1007/978-3- 319-56363-3_10. 105. Bokati, D., Herrera, J. & Poudel, R. Soil influences colonization of root-associated fungal endophyte communities of maize, wheat, and their progenitors. Journal of Mycology 2016, 1–9. doi:10.1155/2016/8062073 (2016). 106. Card, S. D. et al. Beneficial endophytic microorganisms of Brassica – A review. Biological Control 90, 102–112. doi:10.1016/J.BIOCONTROL.2015.06.001 (2015). 107. Junker, C., Draeger, S. & Schulz, B. A fine line - endophytes or pathogens in Arabidopsis thaliana. Fungal Ecology 5, 657–662. doi:10.1016/j.funeco.2012.05.002 (2012). 108. Kohler, A. et al. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nature Genetics 47, 410–415. doi:10.1038/ng.3223 (2015). 109. Spatafora, J. W., Sung, G.-H., J.-M., S., Hywel-Jones, N. L. & White, J. F. Phylogenetic ev- idence for an animal pathogen origin of ergot and the grass endophytes. Molecular Ecology 16, 1701–1711. doi:10.1111/J.1365-294X.2007.03225.X (2007). 110. Xu, X. H. et al. The rice endophyte Harpophora oryzae genome reveals evolution from a pathogen to a mutualistic endophyte. Scientific Reports 4, 1–9. doi:10.1038/srep05783 (2014). 111. Weiß, M., Waller, F., Zuccaro, A. & Selosse, M.-A. Sebacinales – one thousand and one interactions with land plants. New Phytologist 211, 20–40. doi:10.1111/nph.13977 (2016). 112. Veˇtrovsky ́, T. et al. GlobalFungi, a global database of fungal occurrences from high-throughput- sequencing metabarcoding studies. Scientific Data 7, 1–14. doi:10.1038/s41597-020- 0567-7 (2020). 113. Nguyen, N. H. et al. FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology 20, 241–248. doi:10.1016/j.funeco.2015. 06.006 (2016). 114. Selosse, M.-A., Schneider-Maunoury, L. & Martos, F. Time to re-think fungal ecology? Fungal ecological niches are often prejudged. New Phytologist 217, 968–972. doi:10.1111/ NPH.14983 (2018). 115. Zuccaro, A. et al. Endophytic life strategies decoded by genome and transcriptome analy- ses of the mutualistic root symbiont Piriformospora indica. PLoS Pathogens 7, e1002290. doi:10.1371/journal.ppat.1002290 (2011). 116. David, A. S. et al. Draft genome sequence of Microdochium bolleyi, a dark septate fungal endophyte of beach grass. Genome Announcements 4. doi:10.1128/GENOMEA.00270-16 (2016). 117. Walker, A. K. et al. Full genome of Phialocephala scopiformis DAOMC 229536, a fun- gal endophyte of spruce producing the potent anti-insectan compound rugulosin. Genome Announcements 4. doi:10.1128/GENOMEA.01768-15 (2016). 118. Wu, W. et al. Characterization of four endophytic fungi as potential consolidated biopro- cessing hosts for conversion of lignocellulose into advanced biofuels. Applied Microbiology and Biotechnology, 2603–2618. doi:10.1007/s00253-017-8091-1 (2017). 119. Emms, D. M. & Kelly, S. OrthoFinder: Phylogenetic orthology inference for comparative genomics. Genome Biology 20, 1–14. doi:10.1186/s13059-019-1832-y (2019). 120. Csűös, M. Count: Evolutionary analysis of phylogenetic profiles with parsimony and likeli- hood. Bioinformatics 26, 1910–1912. doi:10.1093/BIOINFORMATICS/BTQ315 (2010). 121. Shah, F. et al. Ectomycorrhizal fungi decompose soil organic matter using oxidative mecha- nisms adapted from saprotrophic ancestors. New Phytologist 209, 1705–1719. doi:10.1111/ nph.13722 (2016). 122. Pellegrin, C., Morin, E., Martin, F. M. & Veneault-Fourrey, C. Comparative analysis of se- cretomes from ectomycorrhizal fungi with an emphasis on small-secreted proteins. Frontiers in Microbiology 6, 1278. doi:10.3389/fmicb.2015.01278 (2015). 123. Szklarczyk, D. et al. STRING v11: Protein-protein association networks with increased cov- erage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Research 47, D607–D613. doi:10.1093/nar/gky1131 (2019). 124. Si Tung Ho, L. & Ane ́, C. A linear-time algorithm for gaussian and non-gaussian trait evo- lution models. Systematic Biology 63, 397–408. doi:10.1093/sysbio/syu005 (2014). 125. Klopfenstein, D. V. et al. GOATOOLS: A Python library for Gene Ontology analyses. Sci- entific Reports 8, 1–17. doi:10.1038/s41598-018-28948-z (2018). 126. Kim, D., Paggi, J. M., Park, C., Bennett, C. & Salzberg, S. L. Graph-based genome align- ment and genotyping with HISAT2 and HISAT-genotype. Nature Biotechnology 37, 907– 915. doi:10.1038/s41587-019-0201-4 (2019). 127. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15, 550. doi:10.1186/s13059-014-0550-8 (2014). 128. Cantarel, B. I. et al. The Carbohydrate-Active EnZymes database (CAZy): An expert re- source for glycogenomics. Nucleic Acids Research 37, 233–238. doi:10.1093/nar/gkn663 (2009). 129. Curran, D. M., Gilleard, J. S. & Wasmuth, J. D. MIPhy: Identify and quantify rapidly evolv- ing members of large gene fam. PeerJ 2018, e4873. doi:10.7717/peerj.4873 (2018). 130. Atanasova, L. et al. Evolution and functional characterization of pectate lyase PEL12, a member of a highly expanded Clonostachys rosea polysaccharide lyase 1 family. BMC Mi- crobiology 18, 1–19. doi:10.1186/s12866-018-1310-9 (2018). 131. Keim, J., Mishra, B., Sharma, R., Ploch, S. & Thines, M. Root-associated fungi of Arabidop- sis thaliana and Microthlaspi perfoliatum. Fungal Diversity 66, 99–111. doi:10.1007/ s13225-014-0289-2 (2014). 132. Vannier, N., Agler, M. & Hacquard, S. Microbiota-mediated disease resistance in plants. PLOS Pathogens 15, e1007740. doi:10.1371/journal.ppat.1007740 (2019). 133. Lofgren, L. A. et al. Genome-based estimates of fungal rDNA copy number variation across phylogenetic scales and ecological lifestyles. Molecular Ecology 28, 721–730. doi:10 . 1111/MEC.14995 (2019). 134. Karasov, T. L. et al. Arabidopsis thaliana and Pseudomonas pathogens exhibit stable associ- ations over evolutionary timescales. Cell Host and Microbe 24, 168–179.e4. doi:10.1016/ j.chom.2018.06.011 (2018). 135. Karasov, T. L. et al. The relationship between microbial population size and disease in the Arabidopsis thaliana phyllosphere. bioRxiv. doi:10.1101/828814 (2020). 136. Benen, J. A., Kester, H. C., Paˇrenicova ́, L. & Visser, J. Characterization of Aspergillus niger pectate lyase A. Biochemistry 39, 15563–15569. doi:10.1021/bi000693w (2000). 137. Bauer, S., Vasu, P., Persson, S., Mort, A. J. & Somerville, C. R. Development and application of a suite of polysaccharide-degrading enzymes for analyzing plant cell walls. PNAS 103, 11417–11422. doi:10.1073/pnas.0604632103 (2006). 138. Bacete, L. et al. Arabidopsis response reGUlator 6 (ARR6) modulates plant cell-wall com- position and disease resistance. Molecular Plant-Microbe Interactions 33, 767–780. doi:10. 1094/MPMI-12-19-0341-R (2020). 139. Molina, A. et al. Arabidopsis cell wall composition determines disease resistance specificity and fitness. PNAS 118, e2010243118. doi:10.1073/pnas.2010243118 (2021). 140. Sun, Z.-B. et al. Biology and applications of Clonostachys rosea. Journal of Applied Micro- biology 129, 486–495. doi:10.1111/JAM.14625 (2020). 141. Broberg, M. et al. Comparative genomics highlights the importance of drug efflux trans- porters during evolution of mycoparasitism in Clonostachys subgenus Bionectria (Fungi, Ascomycota, Hypocreales). Evolutionary Applications 14, 476–497. doi:10.1111/EVA. 13134 (2021). 142. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461. doi:10.1093/bioinformatics/btq461 (2010). 143. Chin, C. S. et al. Phased diploid genome assembly with single-molecule real-time sequenc- ing. Nature Methods 13, 1050–1054. doi:10.1038/nmeth.4035 (2016). 144. Grabherr, M. G. et al. Trinity: Reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nature biotechnology 29, 644. doi:10.1038/NBT.1883 (2011). 145. Grigoriev, I. V. et al. MycoCosm portal: Gearing up for 1000 fungal genomes. Nucleic Acids Research 42, D699–D704. doi:10.1093/nar/gkt1183 (2014). 146. Nilsson, R. H. et al. The UNITE database for molecular identification of fungi: Handling dark taxa and parallel taxonomic classifications. Nucleic Acids Research 47, D259–D264. doi:10.1093/nar/gky1022 (2019). 147. Solovyev, V., Kosarev, P., Seledsov, I. & Vorobyev, D. Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome biology 7, 1–12. doi:10.1186/gb-2006-7- s1-s10 (2006). 148. Cohen, O., Ashkenazy, H., Belinky, F., Huchon, D. & Pupko, T. GLOOME: gain loss map- ping engine. Bioinformatics 26, 2914–2915. doi:10.1093/bioinformatics/btq549 (2010). 149. Pedregosa, F. et al. Scikit-learn: machine learning in Python. The Journal of Machine Learn- ing Research 12, 2825–2830 (2011). 150. Seppey, M., Manni, M. & Zdobnov, E. M. in Methods in Molecular Biology 227–245 (Hu- mana Press Inc., 2019). doi:10.1007/978-1-4939-9173-0_14. 151. Morin, E. et al. Comparative genomics of Rhizophagus irregularis, R. cerebriforme, R. di- aphanus and Gigaspora rosea highlights specific genetic features in Glomeromycotina. New Phytologist 222, 1584–1598. doi:10.1111/nph.15687 (2019). 152. Rawlings, N. D., Barrett, A. J. & Finn, R. Twenty years of the MEROPS database of pro- teolytic enzymes, their substrates and inhibitors. Nucleic Acids Research 44, D343–D350. doi:10.1093/nar/gkv1118 (2016). 153. Fischer, M. & Pleiss, J. The Lipase Engineering Database: a navigation and analysis tool for protein families. Nucleic Acids Research 31, 319–321. doi:10.1093/nar/gkg015 (2003). 154. Cock, P. J. A. et al. Biopython: Freely available Python tools for computational molecular bi- ology and bioinformatics. Bioinformatics 25, 1422–1423. doi:10.1093/bioinformatics/ btp163 (2009). 155. Deorowicz, S., Debudaj-Grabysz, A. & Gudys, A. FAMSA: Fast and accurate multiple sequence alignment of huge protein families. Scientific Reports 6, 1–13. doi:10.1038/ srep33964 (2016). 156. Eddy, S. R. Accelerated profile HMM searches. PLoS Computational Biology 7. doi:10. 1371/journal.pcbi.1002195 (2011). 157. Shannon, P. et al. Cytoscape: A software Environment for integrated models of biomolecular interaction networks. Genome Research 13, 2498–2504. doi:10.1101/gr.1239303 (2003). 158. Morris, J. H. et al. ClusterMaker: A multi-algorithm clustering plugin for Cytoscape. BMC Bioinformatics 12, 436. doi:10.1186/1471-2105-12-436 (2011). 159. Gruber, B. D., Giehl, R. F., Friedel, S. & von Wire ́n, N. Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiology 163, 161–179. doi:10.1104/pp.113. 218453 (2013). 160. Hedges, L. V. Distribution theory for Glass’s estimator of effect size and related estimators. Journal of Educational Statistics 6, 107–128. doi:10.3102/10769986006002107 (1981). 161. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120. doi:10.1093/bioinformatics/btu170 (2014). 162. Liao, Y., Smyth, G. K. & Shi, W. featureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930. doi:10.1093/ bioinformatics/btt656 (2014). 163. Zhu, A., Ibrahim, J. G. & Love, M. I. Heavy-tailed prior distributions for sequence count data: removing the noise and preserving large differences. Bioinformatics 35, 2084–2092. doi:10.1093/bioinformatics/bty895 (2019). 164. Mo ̈ller,M.&Stukenbrock,E.H.Evolutionandgenomearchitectureinfungalplantpathogens. Nature Reviews Microbiology 15, 756–771. doi:10.1038/nrmicro.2017.76 (2017). 165. Temporini, E. D. & VanEtten, H. D. Distribution of the pea pathogenicity (PEP) genes in the fungus Nectria haematococca mating population VI. Current Genetics 41, 107–114. doi:10.1007/S00294-002-0279-X (2002). 166. Ma, L. J. et al. Comparative genomics reveals mobile pathogenicity chromosomes in Fusar- ium. Nature 464, 367–373. doi:10.1038/nature08850 (2010). 167. Feurtey, A. et al. Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria. BMC Genomics 21, 1–15. doi:10.1186/S12864-020- 06871-W/FIGURES/5 (2020). 168. Seidl, M. F. & Thomma, B. P. Transposable elements direct the coevolution between plants and microbes. Trends in Genetics 33, 842–851. doi:10.1016/j.tig.2017.07.003 (2017). 169. Faino, L. et al. Transposons passively and actively contribute to evolution of the two-speed genome of a fungal pathogen. Genome Research 26, 1091–1100. doi:10.1101/GR.204974. 116 (2016). 170. Torres, D. E., Oggenfuss, U., Croll, D. & Seidl, M. F. Genome evolution in fungal plant pathogens: looking beyond the two-speed genome model. Fungal Biology Reviews 34, 136– 143. doi:10.1016/J.FBR.2020.07.001 (2020). 171. Dong, S., Raffaele, S. & Kamoun, S. The two-speed genomes of filamentous pathogens: waltz with plants. Current Opinion in Genetics & Development 35, 57–65. doi:10.1016/J. GDE.2015.09.001 (2015). 172. Snelders, N. C., Rovenich, H. & Thomma, B. P. H. J. Microbiota manipulation through the secretion of effector proteins is fundamental to the wealth of lifestyles in the fungal kingdom. FEMS Microbiology Reviews 2022, 1–16. doi:10.1093/FEMSRE/FUAC022 (2022). 173. Stukenbrock, E. H. & McDonald, B. A. Population genetics of fungal and oomycete effectors involved in gene-for-gene interactions. Molecular Plant-Microbe Interactions 22, 371–380. doi:10.1094/MPMI-22-4-0371 (2009). 174. Redkar, A., Sabale, M., Zuccaro, A. & Di Pietro, A. Determinants of endophytic and pathogenic lifestyle in root colonizing fungi. Current Opinion in Plant Biology 67, 102226. doi:10. 1016/J.PBI.2022.102226 (2022). 175. Mun ̃oz-Barrios, A. et al. Differential expression of fungal genes determines the lifestyle of Plectosphaerella strains during Arabidopsis thaliana colonization. Molecular Plant-Microbe Interactions 33, 1299–1314. doi:10.1094/MPMI-03-20-0057-R (2020). 176. Schirrmann, M. K. et al. Genomewide signatures of selection in Epichloe ̈ reveal candidate genes for host specialization. Molecular Ecology 27, 3070–3086. doi:10.1111/MEC.14585 (2018). 177. Schirrmann, M. K. & Leuchtmann, A. The role of host-specificity in the reproductive iso- lation of Epichloe ̈ endophytes revealed by reciprocal infections. Fungal Ecology 15, 29–38. doi:10.1016/J.FUNECO.2015.02.004 (2015). 178. Wippel, K. et al. Host preference and invasiveness of commensal bacteria in the Lotus and Arabidopsis root microbiota. Nature Microbiology 2021 6:9 6, 1150–1162. doi:10.1038/ s41564-021-00941-9 (2021). 179. Deshpande, V. et al. Fungal identification using a Bayesian classifier and the Warcup training set of internal transcribed spacer sequences. Mycologia 108, 1–5. doi:10.3852/14-293 (2017). 180. Giraldo, A. & Crous, P. Inside Plectosphaerellaceae. Studies in mycology 92, 227–286 (2019). 181. Tedersoo, L. et al. The Global Soil Mycobiome consortium dataset for boosting fungal di- versity research. Fungal Diversity 111, 573–588. doi:10.1007/s13225-021-00493-7 (2021). 182. Cantalapiedra, C. P., Hernandez-Plaza, A., Letunic, I., Bork, P. & Huerta-Cepas, J. eggNOG- mapper v2: Functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Molecular Biology and Evolution 38, 5825–5829. doi:10.1093/MOLBEV/ MSAB293 (2021). 183. Odenbach, D. et al. The transcription factor Con7p is a central regulator of infection-related morphogenesis in the rice blast fungus Magnaporthe grisea. Molecular Microbiology 64, 293–307. doi:10.1111/J.1365-2958.2007.05643.X (2007). 184. Ruiz-Rolda ́n,C.,Pareja-Jaime,Y.,Gonza ́lez-Reyes,J.A.&Roncero,M.I.G.Thetran- scription factor Con7-1 is a master regulator of morphogenesis and virulence in Fusarium oxysporum. Molecular Plant-Microbe Interactions 28, 55–68. doi:10.1094/MPMI-07-14- 0205-R (2014). 185. Gao, D. J. et al. First report of Chinese cabbage wilt caused by Plectosphaerella cucumerina in inner Mongolia of China. Plant Disease. doi:10.1094/PDIS-10-21-2210-PDN (2022). 186. Li, P. L., Chai, A. L., Shi, Y. X., Xie, X. W. & Li, B. J. First report of root rot caused by Plectosphaerella cucumerina on cabbage in China. Mycobiology 45, 110–113. doi:10. 5941/MYCO.2017.45.2.110 (2018). 187. Garibaldi, A., Gilardi, G., Ortu, G. & Gullino, M. L. First report of Plectosphaerella cuc- umerina on greenhouse cultured wild rocket (Diplotaxis tenuifolia) in Italy. Plant Disease 96, 1825. doi:10.1094/PDIS-06-12-0583-PDN (2012). 188. Rivedal, H. M., Tabima, J. F., Stone, A. G. & Johnson, K. B. Identity and pathogenicity of fungi associated with root, crown, and vascular symptoms related to winter squash yield decline. Plant Disease 106, 1660–1668. doi:10.1094/PDIS-09-20-2090-RE (2022). 189. Rivedal, H. M., Stone, A. G., Severns, P. M. & Johnson, K. B. Characterization of the fungal community associated with root, crown, and vascular symptoms in an undiagnosed yield decline of winter squash. Phytobiomes Journal 4, 178–192. doi:10.1094/PBIOMES-11- 18-0056-R (2020). 190. Alam, M. W., Malik, A., Rehman, A., Sarwar, M. & Mehboob, S. First report of potato wilt caused by Plectosphaerella cucumerina in Pakistan. Journal of Plant Pathology 103, 687– 687. doi:10.1007/S42161-021-00771-Y (2021). 191. Xu, J., Xu, X. D., Cao, Y. Y. & Zhang, W. M. First report of greenhouse tomato wilt caused by Plectosphaerella cucumerina in China. Plant Disease 98, 158. doi:10.1094/PDIS-05- 13-0566-PDN (2013). 192. Carlucci, A., Raimondo, M. L., Santos, J. & Phillips, A. J. Plectosphaerella species associ- ated with root and collar rots of horticultural crops in southern Italy. Persoonia: Molecular Phylogeny and Evolution of Fungi 28, 34–48. doi:10.3767/003158512X638251 (2012). 193. Zhao, Y. Q., Shi, K., Yu, X. Y. & Zhang, L. J. First Report of Alfalfa root rot caused by Plectosphaerella cucumerina in inner Mongolia autonomous region of China. Plant Disease 105, 87. doi:10.1094/PDIS-03-21-0515-PDN (2021). 194. Yang, L., Lu, X. H., Li, S. D. & Wu, B. M. First report of common bean (Phaseolus vulgaris) root rot caused by Plectosphaerella cucumerina in China. Plant Disease 102, 1849. doi:10. 1094/PDIS-10-17-1659-PDN (2018). 195. Zhang, Y. et al. The genome of opportunistic fungal pathogen Fusarium oxysporum carries a unique set of lineage-specific chromosomes. Communications Biology 3, 1–12. doi:10. 1038/s42003-020-0770-2 (2020). 196. Petre, B., Lorrain, C., Stukenbrock, E. H. & Duplessis, S. Host-specialized transcriptome of plant-associated organisms. Current Opinion in Plant Biology 56, 81–88. doi:10.1016/J. PBI.2020.04.007 (2020). 197. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335–336. doi:10.1038/nmeth.f.303 (2010). 198. Edgar, R. C. UNOISE2: improved error-correction for Illumina 16S and ITS amplicon se- quencing. bioRxiv, 081257. doi:10.1101/081257 (2016). 199. Bengtsson-Palme, J. et al. Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods in Ecology and Evolution 4, 914–919. doi:10.1111/2041-210X. 12073 (2013). 200. Virtanen, P. et al. SciPy 1.0: fundamental algorithms for scientific computing in Python. Nature Methods 17, 261–272. doi:10.1038/s41592-019-0686-2 (2020). 201. Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, 10–12. doi:10.14806/EJ.17.1.200 (2011). 202. Huerta-Cepas, J. et al. eggNOG 5.0: A hierarchical, functionally and phylogenetically anno- tated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Research 47, D309–D314. doi:10.1093/NAR/GKY1085 (2019). 203. Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nature Methods 12, 59–60. doi:10.1038/nmeth.3176 (2014). 204. Zhang, H. et al. dbCAN2: A meta server for automated carbohydrate-active enzyme anno- tation. Nucleic Acids Research 46, W95–W101. doi:10.1093/NAR/GKY418 (2018). 205. Sperschneider, J. & Dodds, P. N. EffectorP 3.0: Prediction of apoplastic and cytoplasmic ef- fectors in fungi and oomycetes. Molecular Plant-Microbe Interactions 35, 146–156. doi:10. 1094/MPMI-08-21-0201-R (2022). 206. Riehl, K., Riccio, C., Miska, E. A. & Hemberg, M. TransposonUltimate: Software for trans- poson classification, annotation and detection. Nucleic Acids Research 50, e64–e64. doi:10. 1093/NAR/GKAC136 (2022). 207. Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: Im- provements in performance and usability. Molecular Biology and Evolution 30, 772–780. doi:10.1093/MOLBEV/MST010 (2013). 208. Capella-Gutie ́rrez,S.,Silla-Mart ́ınez,J.M.&Gabaldo ́n,T.trimAl:Atoolforautomated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973. doi:10.1093/BIOINFORMATICS/BTP348 (2009). 209. Minh, B. Q. et al. IQ-TREE 2: New models and efficient methods for phylogenetic infer- ence in the genomic era. Molecular Biology and Evolution 37, 1530–1534. doi:10.1093/ MOLBEV/MSAA015 (2020). 210. Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K., Von Haeseler, A. & Jermiin, L. S. Mod- elFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods 2017 14:6 14, 587–589. doi:10.1038/nmeth.4285 (2017). 211. Kozlov, A. M., Darriba, D., Flouri, T., Morel, B. & Stamatakis, A. RAxML-NG: A fast, scal- able and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35, 4453–4455. doi:10.1093/BIOINFORMATICS/BTZ305 (2019). 212. Borowiec, M. L. AMAS: A fast tool for alignment manipulation and computing of summary statistics. PeerJ 4, e1660. doi:10.7717/PEERJ.1660/SUPP-2 (2016). 213. Emms, D. M., Kelly & Affiliations. STAG: Species tree inference from all genes. bioRxiv, 267914. doi:10.1101/267914 (2018). 214. Zhang, C., Sayyari, E. & Mirarab, S. in RECOMB international workshop on comparative genomics 53–75 (2017). doi:10.1007/978-3-319-67979-2_4. 215. Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094– 3100. doi:10.1093/BIOINFORMATICS/BTY191 (2018). 216. Goel, M., Sun, H., Jiao, W. B. & Schneeberger, K. SyRI: Finding genomic rearrangements and local sequence differences from whole-genome assemblies. Genome Biology 20, 1–13. doi:10.1186/S13059-019-1911-0 (2019). 217. Goel, M. & Schneeberger, K. plotsr: Visualizing structural similarities and rearrangements between multiple genomes. Bioinformatics 38, 2922–2926. doi:10.1093/BIOINFORMATICS/ BTAC196 (2022). 218. Selosse, M. A., Dubois, M. P. & Alvarez, N. Do Sebacinales commonly associate with plant roots as endophytes? Mycological research 113, 1062–1069. doi:10.1016/J.MYCRES. 2009.07.004 (2009). 219. Selosse, M. A. et al. The waiting room hypothesis revisited by orchids: Were orchid myc- orrhizal fungi recruited among root endophytes? Annals of Botany 129, 259–270. doi:10. 1093/AOB/MCAB134 (2022).
Refereed:	Yes
URI:	http://kups.ub.uni-koeln.de/id/eprint/74289