Gene family expansions and transcriptome signatures uncover fungal adaptations to wood decay

. 2021 Oct ; 23 (10) : 5716-5732. [epub] 20210215

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.

Perzistentní odkaz   https://www.medvik.cz/link/pmid33538380

Because they comprise some of the most efficient wood-decayers, Polyporales fungi impact carbon cycling in forest environment. Despite continuous discoveries on the enzymatic machinery involved in wood decomposition, the vision on their evolutionary adaptation to wood decay and genome diversity remains incomplete. We combined the genome sequence information from 50 Polyporales species, including 26 newly sequenced genomes and sought for genomic and functional adaptations to wood decay through the analysis of genome composition and transcriptome responses to different carbon sources. The genomes of Polyporales from different phylogenetic clades showed poor conservation in macrosynteny, indicative of genome rearrangements. We observed different gene family expansion/contraction histories for plant cell wall degrading enzymes in core polyporoids and phlebioids and captured expansions for genes involved in signalling and regulation in the lineages of white rotters. Furthermore, we identified conserved cupredoxins, thaumatin-like proteins and lytic polysaccharide monooxygenases with a yet uncharacterized appended module as new candidate players in wood decomposition. Given the current need for enzymatic toolkits dedicated to the transformation of renewable carbon sources, the observed genomic diversity among Polyporales strengthens the relevance of mining Polyporales biodiversity to understand the molecular mechanisms of wood decay.

Zobrazit více v PubMed

Aksoy, S. , and Haralick, R.M. (2001) Feature normalization and likelihood‐based similarity measures for image retrieval. Pattern Recogn Lett 22: 563–582.

Altschul, S.F. , Gish, W. , Miller, W. , Myers, E.W. , and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403–410. PubMed

Arantes, V. , Jellison, J. , and Goodell, B. (2012) Peculiarities of brown‐rot fungi and biochemical Fenton reaction with regard to their potential as a model for bioprocessing biomass. Appl Microbiol Biotechnol 94: 323–338. PubMed

Arnesano, F. , Banci, L. , Bertini, I. , and Thompsett, A.R. (2002) Solution structure of CopC: a cupredoxin‐like protein involved in copper homeostasis. Structure 10: 1337–1347. PubMed

Ayuso‐Fernández, I. , Ruiz‐Dueñas, F.J. , and Martínez, A.T. (2018) Evolutionary convergence in lignin‐degrading enzymes. Proc Natl Acad Sci 115: 6428–6433. PubMed PMC

Bennati‐Granier, C. , Garajova, S. , Champion, C. , Grisel, S. , Haon, M. , Zhou, S. , PubMed PMC

Berrin, J.‐G. , Navarro, D. , Couturier, M. , Olivé, C. , Grisel, S. , Haon, M. , PubMed PMC

Berrin, J.‐G. , Rosso, M.‐N. , and Abou, H.M. (2017) Fungal secretomics to probe the biological functions of lytic polysaccharide monooxygenases. Carbohydr Res 448: 155–160. PubMed

Blanchette, R.A. (1984) Screening wood decayed by white rot fungi for preferential lignin degradation. Appl Environ Microbiol 48: 647–653. PubMed PMC

Blanchette, R.A. , Krueger, E.W. , Haight, J.E. , Akhtar, M. , and Akin, D.E. (1997) Cell wall alterations in loblolly pine wood decayed by the white‐rot fungus,

Boberg, J.B. , Finlay, R.D. , Stenlid, J. , Ekblad, A. , and Lindahl, B.D. (2014) Nitrogen and carbon reallocation in fungal mycelia during decomposition of boreal forest litter (RA Wilson, Ed.). PLoS ONE 9: e92897. PubMed PMC

Capella‐Gutiérrez, S. , Silla‐Martínez, J.M. , and Gabaldón, T. (2009) trimAl: a tool for automated alignment trimming in large‐scale phylogenetic analyses. Bioinformatics (Oxford, England) 25: 1972–1973. PubMed PMC

Chalak, A. , Villares, A. , Moreau, C. , Haon, M. , Grisel, S. , d'Orlando, A. , PubMed PMC

Chen, K. , Durand, D. , and Farach‐Colton, M. (2000) NOTUNG: a program for dating gene duplications and optimizing gene family trees. J Comput Biol 7: 429–447. PubMed

Chen, J. , Heikkinen, J. , Hobbie, E.A. , Rinne‐Garmston, K.T. , Penttilä, R. , and Mäkipää, R. (2019) Strategies of carbon and nitrogen acquisition by saprotrophic and ectomycorrhizal fungi in Finnish boreal Picea abies‐dominated forests. Fungal Biol 123: 456–464. PubMed

Chin, C.‐S. , Alexander, D.H. , Marks, P. , Klammer, A.A. , Drake, J. , Heiner, C. , PubMed

Couturier, M. , Ladevèze, S. , Sulzenbacher, G. , Ciano, L. , Fanuel, M. , Moreau, C. , PubMed

Deroy, A. , Saiag, F. , Kebbi‐Benkeder, Z. , Touahri, N. , Hecker, A. , Morel‐Rouhier, M. , PubMed PMC

Eastwood, D.C. , Floudas, D. , Binder, M. , Majcherczyk, A. , Schneider, P. , Aerts, A. , PubMed

Feldman, D. , Yarden, O. , and Hadar, Y. (2020) Seeking the roles for fungal small‐secreted proteins in affecting saprophytic lifestyles. Front Microbiol 11: 455. PubMed PMC

Fernandez‐Fueyo, E. , Ruiz‐Dueñas, F.J. , Ferreira, P. , Floudas, D. , Hibbett, D.S. , Canessa, P. , PubMed PMC

Floudas, D. , Binder, M. , Riley, R. , Barry, K. , Blanchette, R.A. , Henrissat, B. , PubMed

Garcia‐Santamarina, S. , Probst, C. , Festa, R.A. , Ding, C. , Smith, A.D. , Conklin, S.E. , PubMed PMC

Gnerre, S. , MacCallum, I. , Przybylski, D. , Ribeiro, F.J. , Burton, J.N. , Walker, B.J. , PubMed PMC

Grigoriev, I.V. , Nikitin, R. , Haridas, S. , Kuo, A. , Ohm, R. , Otillar, R. , PubMed PMC

Gu, Z. , Gu, L. , Eils, R. , Schlesner, M. , and Brors, B. (2014) Circlize implements and enhances circular visualization in R. Bioinformatics 30: 2811–2812. PubMed

Gutiérrez, A. , del Río, J.C. , Martínez‐Íñigo, M.J. , Martínez, M.J. , and Martínez, Á.T. (2002) Production of new unsaturated lipids during wood decay by ligninolytic basidiomycetes. Appl Environ Microbiol 68: 1344–1350. PubMed PMC

Hori, C. , Gaskell, J. , Igarashi, K. , Kersten, P. , Mozuch, M. , Samejima, M. , and Cullen, D. (2014) Temporal alterations in the secretome of the selective ligninolytic PubMed PMC

Justo, A. , Miettinen, O. , Floudas, D. , Ortiz‐Santana, B. , Sjökvist, E. , Lindner, D. , PubMed

Kadimaliev, D.A. , Nadezhina, O.S. , Atykyan, N.A. , Revin, V.V. , and Samuilov, V.D. (2006) Interrelation between the composition of lipids and their peroxidation products and the secretion of ligninolytic enzymes during growth of PubMed

Kim, K.‐T. , Jeon, J. , Choi, J. , Cheong, K. , Song, H. , Choi, G. , PubMed PMC

Kirk, P. , Cannon, P. , Minter, D. , and Stalpers, J. (2009) Dictionary of the fungi. Mycol Res 113: 908–910.

Knobloch, E. , and Kotlaba, F. (1994)

Korripally, P. , Hunt, C.G. , Houtman, C.J. , Jones, D.C. , Kitin, P.J. , Cullen, D. , and Hammel, K.E. (2015) Regulation of gene expression during the onset of ligninolytic oxidation by PubMed PMC

Kuroyama, H. , Tsutsui, N. , Hashimoto, Y. , and Tsumuraya, Y. (2001) Purification and characterization of a beta‐glucuronidase from PubMed

Kuuskeri, J. , Häkkinen, M. , Laine, P. , Smolander, O.‐P. , Tamene, F. , Miettinen, S. , PubMed PMC

Labourel, A. , Frandsen, K.E.H. , Zhang, F. , Brouilly, N. , Grisel, S. , Haon, M. , PubMed

Lam, K.‐K. , LaButti, K. , Khalak, A. , and Tse, D. (2015) FinisherSC: a repeat‐aware tool for upgrading de novo assembly using long reads. Bioinformatics 31: 3207–3209. PubMed

Lenfant, N. , Hainaut, M. , Terrapon, N. , Drula, E. , Lombard, V. , and Henrissat, B. (2017) A bioinformatics analysis of 3400 lytic polysaccharide oxidases from family AA9. Carbohydr Res 448: 166–174. PubMed

Lombard, V. , Golaconda Ramulu, H. , Drula, E. , Coutinho, P.M. , and Henrissat, B. (2014) The carbohydrate‐active enzymes database (CAZy) in 2013. Nucleic Acids Res 42: D490–D495. PubMed PMC

Love, M.I. , Huber, W. , and Anders, S. (2014) Moderated estimation of fold change and dispersion for RNA‐seq data with DESeq2. Genome Biol 15: 550. PubMed PMC

Lundell, T.K. , Mäkelä, M.R. , de Vries, R.P. , and Hildén, K.S. (2014) Chapter eleven ‐ genomics, lifestyles and future prospects of wood‐decay and litter‐decomposing Basidiomycota. In Advances in Botanical Research: Fungi, Vol. 70, Martin, F.M. (ed). London: Academic Press, pp. 329–370.

Martin, R. , Gazis, R. , Skaltsas, D. , Chaverri, P. , and Hibbett, D. (2015) Unexpected diversity of basidiomycetous endophytes in sapwood and leaves of Hevea. Mycologia 107: 284–297. PubMed

Martínez, A.T. , Ruiz‐Dueñas, F.J. , Camarero, S. , Serrano, A. , Linde, D. , Lund, H. , PubMed

Martínez, A.T. , Speranza, M. , Ruiz‐Dueñas, F.J. , Ferreira, P. , Camarero, S. , Guillén, F. , PubMed

Martins, I. , Hartmann, D.O. , Alves, P.C. , Martins, C. , Garcia, H. , Leclercq, C.C. , PubMed PMC

Maeder H. (2018) FALCON: experimental PacBio diploid assembler. [WWW document] URL https://github.com/PacificBiosciences/FALCON.

Maeder H. (2019)

Mattila, H.K. , Mäkinen, M. , and Lundell, T. (2020) Hypoxia is regulating enzymatic wood decomposition and intracellular carbohydrate metabolism in filamentous white rot fungus. Biotechnol Biofuels 13: 26. PubMed PMC

Maxim H. (2018) RVAideMemoire: testing and plotting procedures for biostatistics. R Package Version 0.9–69.

Mesny F. (2020) Detecting the effect of biological categories on genomes composition [WWW document]. URL https://github.com/fantin-mesny/Effect-Of-Biological-Categories-On-Genomes-Composition

Miettinen, O. , Riley, R. , Barry, K. , Cullen, D. , de Vries, R.P. , Hainaut, M. , PubMed PMC

Miyauchi, S. , Hage, H. , Drula, E. , Lesage‐Meessen, L. , Berrin, J.‐G. , Navarro, D. , PubMed PMC

Miyauchi, S. , Navarro, D. , Grisel, S. , Chevret, D. , Berrin, J.‐G. , and Rosso, M.‐N. (2017) The integrative omics of white‐rot fungus PubMed PMC

Miyauchi, S. , Rancon, A. , Drula, E. , Hage, H. , Chaduli, D. , Favel, A. , PubMed PMC

Morin, E. , Miyauchi, S. , San Clemente, H. , Chen, E.C.H. , Pelin, A. , de la Providencia, I. , PubMed

Moudy, M. , and Stites, W. (2017) Investigation of methionine sulfoxide formation as a regulator of proteolysis. Biophys J 112: 202a.

Nagy, L.G. , Ohm, R.A. , Kovács, G.M. , Floudas, D. , Riley, R. , Gácser, A. , PubMed

Nagy, L.G. , Riley, R. , Bergmann, P.J. , Krizsán, K. , Martin, F.M. , Grigoriev, I.V. , PubMed

Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin P, O'Hara RB, et al. (2012) Vegan: Community Ecology Package. R package version 2.0‐2.

Paradis, E. , Claude, J. , and Strimmer, K. (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290. PubMed

Payen, T. , Murat, C. , and Martin, F. (2016) Reconstructing the evolutionary history of gypsy retrotransposons in the Périgord black truffle ( PubMed

Pellegrin, C. , Morin, E. , Martin, F.M. , and Veneault‐Fourrey, C. (2015) Comparative analysis of secretomes from ectomycorrhizal fungi with an emphasis on small‐secreted proteins. Front Microbiol 6: 1278. PubMed PMC

Presley, G.N. , and Schilling, J.S. (2017) Distinct growth and secretome strategies for two taxonomically divergent brown rot fungi. Appl Environ Microbiol 83: e02987–e02916. PubMed PMC

Price, A.L. , Jones, N.C. , and Pevzner, P.A. (2005) De novo identification of repeat families in large genomes. Bioinformatics 21: i351–i358. PubMed

Puttick, M.N. (2019) MCMCtreeR: functions to prepare MCMCtree analyses and visualize posterior ages on trees. Bioinformatics 35: 5321–5322. PubMed

Qhanya, L.B. , Matowane, G. , Chen, W. , Sun, Y. , Letsimo, E.M. , Parvez, M. , PubMed PMC

Rayner, A.D.M. , Boddy, L. , and Dowson, C.G. (1987) Temporary parasitism of

Riley, R. , Salamov, A.A. , Brown, D.W. , Nagy, L.G. , Floudas, D. , Held, B.W. , PubMed PMC

Rivera‐Hoyos, C.M. , Morales‐Álvarez, E.D. , Poutou‐Piñales, R.A. , Pedroza‐Rodríguez, A.M. , RodrÍguez‐Vázquez, R. , and Delgado‐Boada, J.M. (2013) Fungal laccases. Fungal Biol Rev 27: 67–82.

Ruiz‐Dueñas, F.J. , Lundell, T. , Floudas, D. , Nagy, L.G. , Barrasa, J.M. , Hibbett, D.S. , and Martínez, A.T. (2013) Lignin‐degrading peroxidases in Polyporales: an evolutionary survey based on 10 sequenced genomes. Mycologia 105: 1428–1444. PubMed

Ruiz‐Dueñas, F.J. , Barrasa, J.M. , Sánchez‐García, M. , Camarero, S. , Miyauchi, S. , Serrano, A. , PubMed PMC

Schilling, J.S. , Kaffenberger, J.T. , Held, B.W. , Ortiz, R. , and Blanchette, R.A. (2020) Using wood rot phenotypes to illuminate the “gray” among decomposer fungi. Front Microbiol 11: 1288. PubMed PMC

Sokolski, S. , Bernier‐Cardou, M. , Piché, Y. , and Bérubé, J.A. (2007) Black spruce (

Song, J. , and Cui, B.‐K. (2017) Phylogeny, divergence time and historical biogeography of PubMed PMC

Suzuki, H. , MacDonald, J. , Syed, K. , Salamov, A. , Hori, C. , Aerts, A. , PubMed PMC

Syed, K. , Shale, K. , Pagadala, N.S. , and Tuszynski, J. (2014) Systematic identification and evolutionary analysis of catalytically versatile cytochrome p450 monooxygenase families enriched in model basidiomycete fungi. PLOS ONE 9: e86683. PubMed PMC

Varga, T. , Krizsán, K. , Földi, C. , Dima, B. , Sánchez‐García, M. , Sánchez‐Ramírez, S. , PubMed PMC

Wattam, A.R. , Abraham, D. , Dalay, O. , Disz, T.L. , Driscoll, T. , Gabbard, J.L. , PubMed PMC

Wright, E.S. (2015) DECIPHER: harnessing local sequence context to improve protein multiple sequence alignment. BMC Bioinformatics 16: 322. PubMed PMC

Wu, B. , Gaskell, J. , Held, B.W. , Toapanta, C. , Vuong, T. , Ahrendt, S. , PubMed PMC

Zhang, J. , Silverstein, K.A.T. , Castaño, J.D. , Figueroa, M. , and Schilling, J.S. (2019) Gene regulation shifts shed light on fungal adaption in plant biomass decomposers. mBio 10: e02176–e02119. PubMed PMC

Zhou, S. , Raouche, S. , Grisel, S. , Navarro, D. , Sigoillot, J.‐C. , and Herpoël‐Gimbert, I. (2015) Solid‐state fermentation in multi‐well plates to assess pretreatment efficiency of rot fungi on lignocellulose biomass. J Microbial Biotechnol 8: 940–949. PubMed PMC

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...