Evolutionary innovations through gain and loss of genes in the ectomycorrhizal Boletales.
Boletales
CAZymes
brown-rot fungi
comparative genomics
ectomycorrhizal fungi
trait evolution
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
received:
06
09
2021
accepted:
04
11
2021
pubmed:
13
11
2021
medline:
25
3
2022
entrez:
12
11
2021
Statut:
ppublish
Résumé
We aimed to identify genomic traits of transitions to ectomycorrhizal ecology within the Boletales by comparing the genomes of 21 symbiotrophic species with their saprotrophic brown-rot relatives. Gene duplication rate is constant along the backbone of Boletales phylogeny with large loss events in several lineages, while gene family expansion sharply increased in the late Miocene, mostly in the Boletaceae. Ectomycorrhizal Boletales have a reduced set of plant cell-wall-degrading enzymes (PCWDEs) compared with their brown-rot relatives. However, the various lineages retain distinct sets of PCWDEs, suggesting that, over their evolutionary history, symbiotic Boletales have become functionally diverse. A smaller PCWDE repertoire was found in Sclerodermatineae. The gene repertoire of several lignocellulose oxidoreductases (e.g. laccases) is similar in brown-rot and ectomycorrhizal species, suggesting that symbiotic Boletales are capable of mild lignocellulose decomposition. Transposable element (TE) proliferation contributed to the higher evolutionary rate of genes encoding effector-like small secreted proteins, proteases, and lipases. On the other hand, we showed that the loss of secreted CAZymes was not related to TE activity but to DNA decay. This study provides novel insights on our understanding of the mechanisms influencing the evolutionary diversification of symbiotic boletes.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
1383-1400Informations de copyright
© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.
Références
Alexa A, Rahnenfuhrer J. 2020. topGO: enrichment analysis for gene ontology. [WWW document] URL https://www.bioconductor.org/packages//2.10/bioc/html/topGO.html [accessed 15 October 2020].
Alexa A, Rahnenführer J, Lengauer T. 2006. Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22: 1600-1607.
den Bakker HC, Zuccarello GC, Kuyper TW, Noordeloos ME. 2004. Evolution and host specificity in the ectomycorrhizal genus Leccinum. New Phytologist 163: 201-215.
Baldrian P, Kolařík M, Stursová M, Kopecký J, Valášková V, Větrovský T, Zifčáková L, Snajdr J, Rídl J, Vlček Č et al. 2012. Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME Journal 6: 248-258.
Beaudet D, Chen ECH, Mathieu S, Yildirir G, Ndikumana S, Dalpé Y, Séguin S, Farinelli L, Stajich JE, Corradi N. 2018. Ultra-low input transcriptomics reveal the spore functional content and phylogenetic affiliations of poorly studied arbuscular mycorrhizal fungi. DNA Research 25: 217-227.
Bessette A, Roody WC, Bessette AR. 2000. North American Boletes: a color guide to the fleshy pored mushrooms. New York, NY, USA: Syracuse University Press.
Binder M, Hibbett DS. 2006. Molecular systematics and biological diversification of Boletales. Mycologia 98: 971-981.
Binder M, Larsson KH, Matheny PB, Hibbett DS. 2010. Amylocorticiales ord. nov. and Jaapiales ord. nov.: early diverging clades of Agaricomycetidae dominated by corticioid forms. Mycologia 102: 865-880.
Blighe K, Lun A. 2020. PCAtools: everything principal components analysis. R package v.2.2.0. [WWW document] URL https://github.com/kevinblighe/PCAtools [accessed 10 April 2021].
Bougher NL. 1995. Diversity of ectomycorrhizal fungi associated with eucalypts in Australia. In: Brundett M, Dell B, Malajczuk N, Gong MQ, eds. Mycorrhizas for plantation forestry in Asia. Canberra, ACT, Australia: Australian Centre Int Agricultural Research, 8-15.
Cao Y, Zhang Y, Yu Z, Wang P, Tang X, He X, Mi F, Liu C, Yang D, Xu J. 2015. Genome sequence of Phlebopus portentosus strain PP33, a cultivated bolete. Genome Announcements 3: e00326-15.
Castanera R, Pérez G, López-Varas L, Amselem J, LaButti K, Singan V, Lipzen A, Haridas S, Barry K, Grigoriev IV et al. 2017. Comparative genomics of Coniophora olivacea reveals different patterns of genome expansion in Boletales. BMC Genomics 18: e883.
Chang Y, Desirò A, Na H, Sandor L, Lipzen A, Clum A, Barry K, Grigoriev IV, Martin FM, Stajich JE et al. 2019. Phylogenomics of Endogonaceae and evolution of mycorrhizas within Mucoromycota. New Phytologist 222: 511-525.
Chen K, Durand D, Farach-Colton M. 2000. Notung: a program for dating gene duplications and optimizing gene family trees. Journal of Computational Biology 7: 429-447.
Corner EJH. 1972. Boletus in Malaysia. Singapore City, Singapore: Botanic Gardens.
Darling AE, Carey LB, Feng W-C. 2003. The design, implementation, and evaluation of mpiBLAST. In: 4th International Conference on Linux Clusters and ClusterWorld 2003. San Jose, CA, USA.
Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B, Flouri T. 2019. ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Molecular Biology and Evolution 37: 291-294.
Dentinger BTM, Ammirati JF, Both EE, Desjardin DE, Halling RE, Henkel TW, Moreau P-A, Nagasawa E, Soytong K, Taylor AF et al. 2010. Molecular phylogenetics of porcini mushrooms (Boletus section Boletus). Molecular Phylogenetics and Evolution 57: 1276-1292.
van Dongen S. 2000. Graph clustering by flow simulation. PhD thesis, University of Utrecht, Utrecht.
Drehmel D, James T, Vilgalys R. 2008. Molecular phylogeny and biodiversity of the boletes. Fungi 1: 17-23.
Eastwood DC, Floudas D, Binder M, Majcherczyk A, Schneider P, Aerts A, Asiegbu FO, Baker SE, Barry K, Bendiksby M et al. 2011. The plant cell wall-decomposing machinery underlies the functional diversity of forest fungi. Science 333: 762-765.
Eddy SR. 2011. Accelerated profile HMM searches. Plos Computational Biology 7: e1002195.
Floudas D, Bentzer J, Ahrén D, Johansson T, Persson P, Tunlid A. 2020. Uncovering the hidden diversity of litter-decomposition mechanisms in mushroom-forming fungi. The ISME Journal 14: 2046-2059.
Gel B, Díez-Villanueva A, Serra E, Buschbeck M, Peinado MA, Malinverni R. 2016. regioner: an R/Bioconductor package for the association analysis of genomic regions based on permutation tests. Bioinformatics 32: 289-291.
Gel B, Serra E. 2017. karyoploter: an R/Bioconductor package to plot customizable genomes displaying arbitrary data. Bioinformatics 33: 3088-3090.
Grubisha LC, Trappe JM, Molina R, Spatafora JW. 2001. Biology of the ectomycorrhizal genus Rhizopogon. V. Phylogenetic relationships in the Boletales inferred from LSU rDNA sequences. Mycologia 93: 82-89.
Gu Z, Gu L, Eils R, Schlesner M, Brors B. 2014. circlize implements and enhances circular visualization in R. Bioinformatics 30: 2811-2812.
Hage H, Miyauchi S, Virágh M, Drula E, Min B, Chaduli D, Navarro D, Favel A, Norest M, Lesage-Meessen L et al. 2021. Gene family expansions and transcriptome signatures uncover fungal adaptations to wood decay. Environmental Microbiology 23: 5716-5732.
Han L-H, Feng B, Wu G, Halling RE, Buyck B, Yorou NS, Ebika STN, Yang Z-L. 2018. African origin and global distribution patterns: evidence inferred from phylogenetic and biogeographical analyses of ectomycorrhizal fungal genus Strobilomyces. Journal of Biogeography 45: 201-212.
Heinemann P. 1951. Champignons récoltés au Congo belge par Madame M. Goossens-Fontana I. Boletineae. Bulletin du Jardin Botanique de l'État a Bruxelles 21: 223-346.
Henkel TW, Terborgh J, Vilgalys RJ. 2002. Ectomycorrhizal fungi and their leguminous hosts in the Pakaraima Mountains of Guyana. Mycological Research 106: 515-531.
Hess J, Skrede I, Chaib De Mares M, Hainaut M, Henrissat B, Pringle A. 2018. Rapid divergence of genome architectures following the origin of an ectomycorrhizal symbiosis in the genus Amanita. Molecular Biology and Evolution 35: 2786-2804.
Hibbett DS, Matheny PB. 2009. The relative ages of ectomycorrhizal mushrooms and their plant hosts estimated using Bayesian relaxed molecular clock analyses. BMC Biology 7: e13.
Hosen MI, Feng B, Wu G, Zhu XT, Li Y-C, Yang ZL. 2013. Borofutus, a new genus of Boletaceae from tropical Asia: phylogeny, morphology and taxonomy. Fungal Diversity 58: 215-226.
Ji K-P, Cao Y, Zhang C-X, He M-X, Liu J, Wang W-B, Wang Y. 2011. Cultivation of Phlebopus portentosus in southern China. Mycological Progress 10: 293-300.
Johnson B. 2018. Taxonomically restricted genes are fundamental to biology and evolution. Frontiers in Genetics 9: e407.
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: 1236-1240.
Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772-780.
Kirk PM, Cannon PF, Minter D, Stalpers JA. 2008. Dictionary of the fungi, 10th edn. Wallingford, UK: CAB International.
Kohler A, Kuo A, Nagy LG, Morin E, Barry KW, Buscot F, Canbäck B, Choi C, Cichocki N, Clum A et al. 2015. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nature Genetics 47: e410.
Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. 2019. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35: 4453-4455.
Krah F-S, Bässler C, Heibl C, Soghigian J, Schaefer H, Hibbett DS. 2018. Evolutionary dynamics of host specialization in wood-decay fungi. BMC Evolutionary Biology 18: e119.
Kumla J, Hobbie EA, Suwannarach N, Lumyong S. 2016. The ectomycorrhizal status of a tropical black bolete, Phlebopus portentosus, assessed using mycorrhizal synthesis and isotopic analysis. Mycorrhiza 26: 333-343.
Lebreton A, Zeng Q, Miyauchi S, Kohler A, Dai Y-C, Martin FM. 2021. Evolution of the mode of nutrition in symbiotic and saprotrophic fungi in forest ecosystems. Annual Review of Ecology, Evolution and Systematics 52: 385-404.
LePage BA, Currah RS, Stockey RA, Rothwell GW. 1997. Fossil ectomycorrhizae from the middle Eocene. American Journal of Botany 84: 410-412.
Lofgren LA, Nguyen NH, Vilgalys R, Ruytinx J, Liao H-L, Branco S, Kuo A, LaButti K, Lipzen A, Andreopoulos W et al. 2021. Comparative genomics reveals dynamic genome evolution in host specialist ectomycorrhizal fungi. New Phytologist 230: 774-792.
Looney B, Miyauchi S, Morin E, Drula E, Courty PE, Kohler A, Kuo A, LaButti K, Pangilinan J, Lipzen A et al. 2021. Evolutionary transition to the ectomycorrhizal habit in the genomes of a hyper-diverse lineage of mushroom-forming fungi. New Phytologist, in press.
Marqués-Gálvez JE, Miyauchi S, Paolocci F, Navarro-Ródenas A, Arenas F, Pérez-Gilabert M, Morin E, Auer L, Barry KW, Kuo A et al. 2021. Desert truffle genomes reveal their reproductive modes and new insights into plant-fungal interaction and ectendomycorrhizal lifestyle. New Phytologist 229: 2917-2932.
Martin F, Kohler A, Murat C, Veneault-Fourrey C, Hibbett DS. 2016. Unearthing the roots of ectomycorrhizal symbioses. Nature Reviews Microbiology 14: 760-773.
Miyauchi S, Kiss E, Kuo A, Drula E, Kohler A, Sánchez-García M, Morin E, Andreopoulos B, Barry KW, Bonito G et al. 2020. Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits. Nature Communications 11: e5125.
Muñoz JA. 2005. Fungi Europaei 2: Boletus s.l.: Strobilomycetaceae. Alassio, Italy: Edizioni Candusso.
Murat C, Payen T, Noel B, Kuo A, Morin E, Chen J, Kohler A, Krizsán K, Balestrini R, Da Silva C et al. 2018. Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle. Nature Ecology & Evolution 2: 1956-1965.
Nagy LG, Ohm RA, Kovács GM, Floudas D, Riley R, Gácser A, Sipiczki M, Davis JM, Doty SL, de Hoog GS et al. 2014. Latent homology and convergent regulatory evolution underlies the repeated emergence of yeasts. Nature Communications 5: e4471.
Nagy LG, Riley R, Tritt A, Adam C, Daum C, Floudas D, Sun H, Yadav JS, Pangilinan J, Larsson K-H et al. 2016. Comparative genomics of early-diverging mushroom-forming fungi provides insights into the origins of lignocellulose decay capabilities. Molecular Biology and Evolution 33: 959-970.
Newman EI, Reddell P. 1987. The distribution of mycorrhizas among families of vascular plants. New Phytologist 106: 745-751.
Nicolás C, Martin-Bertelsen T, Floudas D, Bentzer J, Smits M, Johansson T, Troein C, Persson P, Tunlid A. 2019. The soil organic matter decomposition mechanisms in ectomycorrhizal fungi are tuned for liberating soil organic nitrogen. The ISME Journal 13: 977-988.
Nuhn ME, Binder M, Taylor AFS, Halling RE, Hibbett DS. 2013. Phylogenetic overview of the Boletineae. Fungal Biology 117: 479-511.
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P et al. 2019. vegan: community ecology package. R package v.2.5-6. [WWW document] URL https://CRAN.R-project.org/package=vegan [accessed 25 April 2019].
Ortega-Martínez P, Águeda B, Fernández-Toirán LM, Martínez-Peña F. 2011. Tree age influences on the development of edible ectomycorrhizal fungi sporocarps in Pinus sylvestris stands. Mycorrhiza 21: 65-70.
Peay KG, Kennedy PG, Talbot JM. 2016. Dimensions of biodiversity in the earth mycobiome. Nature Reviews Microbiology 14: 434-447.
Pellegrin C, Morin E, Martin FM, Veneault-Fourrey C. 2015. Comparative analysis of secretomes from ectomycorrhizal fungi with an emphasis on small-secreted proteins. Frontiers in Microbiology 6: e1278.
Pham N-D, Suzuki A, Pham N-D, Yamada A, Shimizu K, Noda K, Dang L-A, Suzuki A. 2012. A sheathing mycorrhiza between the tropical bolete Phlebopus spongiosus and Citrus maxima. Mycoscience 53: 347-353.
Rapior S, Fruchier A, Bessière J-M. 1997. Volatile aroma constituents of agarics and boletes. In: Pandalai SG, ed. Recent research developments in phytochemistry. Trivandrum, India: Research Signpost, 567-584.
Ruiz-Dueñas FJ, Barrasa JM, Sánchez-García M, Camarero S, Miyauchi S, Serrano A, Linde D, Babiker R, Drula E, Ayuso-Fernández I et al. 2020. Genomic analysis enlightens Agaricales lifestyle evolution and increasing peroxidase diversity. Molecular Biology and Evolution 38: 1428-1446.
Sánchez-García M, Ryberg M, Kalsoom Khan F, Varga T, Nagy LG, Hibbett DS. 2020. Fruiting body form, not nutritional mode, is the major driver of diversification in mushroom-forming fungi. Proceedings of the National Academy of Sciences, USA 117: 32528-32534.
Sanmee R, Lumyong S, Lumyong P, Dell B. 2010. In vitro cultivation and fruit body formation of the black bolete, Phlebopus portentosus, a popular edible ectomycorrhizal fungus in Thailand. Mycoscience 51: 15-22.
Sato H, Toju H. 2019. Timing of evolutionary innovation: scenarios of evolutionary diversification in a species-rich fungal clade, Boletales. New Phytologist 222: 1924-1935.
Sato H, Yumoto T, Murakami N. 2007. Cryptic species and host specificity in the ectomycorrhizal genus Strobilomyces (Strobilomycetaceae). American Journal of Botany 94: 1630-1641.
Stamatakis A. 2014. RAxML v.8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313.
Tedersoo L, Smith ME. 2013. Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biology Reviews 27: 83-99.
Varga T, Krizsán K, Földi C, Dima B, Sánchez-García M, Sánchez-Ramírez S, Szöllősi GJ, Szarkándi JG, Papp V, Albert L et al. 2019. Megaphylogeny resolves global patterns of mushroom evolution. Nature Ecology & Evolution 3: 668-678.
Wilson AW, Binder M, Hibbett DS. 2012. Diversity and evolution of ectomycorrhizal host associations in the Sclerodermatineae (Boletales, Basidiomycota). New Phytologist 194: 1079-1095.
Wolfe BE, Tulloss RE, Pringle A. 2012. The irreversible loss of a decomposition pathway marks the single origin of an ectomycorrhizal symbiosis. PLoS ONE 7: e39597.
Wright ES. 2015. decipher: harnessing local sequence context to improve protein multiple sequence alignment. BMC Bioinformatics 16: e322.
Wu G, Feng B, Xu J, Zhu X-T, Li Y-C, Zeng N-K, Hosen MI, Yang Z-L. 2014. Molecular phylogenetic analyses redefine seven major clades and reveal 22 new generic clades in the fungal family Boletaceae. Fungal Diversity 69: 93-115.
Wu G, Li Y-C, Zhu X-T, Zhao K, Han L-H, Cui Y-Y, Li F, Xu J-P, Yang Z-L. 2016. One hundred noteworthy boletes from China. Fungal Diversity 81: 25-188.
Yang Z. 2007. Paml 4: a program package for phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24: 1586-1591.
Zang M. 2006. Flora fungorum sinicorum. Vol. 22, Boletaceae (I). Beijing, China: Science Press.
Zhang F, Anasontzis GE, Labourel A, Champion C, Haon M, Kemppainen M, Commun C, Deveau A, Pardo A, Veneault-Fourrey C et al. 2018. The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development. New Phytologist 220: 1309-1321.
Zhang F, Labourel A, Haon M, Kemppainen M, Silva Machado ED, Brouilly N, Veneault-Fourrey C, Kohler A, Rosso M-N, Pardo A et al. 2021. The ectomycorrhizal basidiomycete Laccaria bicolor releases a GH28 polygalacturonase that plays a key role in symbiosis establishment. bioRxiv. doi: 10.1101/2021.09.24.461608.
Zhao R-L, Li G-J, Sánchez-Ramírez S, Stata M, Yang Z-L, Wu G, Dai Y-C, He S-H, Cui B-K, Zhou J-L. 2017. A six-gene phylogenetic overview of Basidiomycota and allied phyla with estimated divergence times of higher taxa and a phyloproteomics perspective. Fungal Diversity 88: 43-74.