Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii

Dimitrios Floudas; Benjamin W. Held; Robert Riley; Laszlo G. Nagy; Gage Koehler; Anthony S. Ransdell; Hina Younus; Julianna Chow; Jennifer Chiniquy; Anna Lipzen; Andrew Tritt; Hui Sun; Sajeet Haridas; Kurt LaButti; Robin A. Ohm; Ursula Kües; Robert A. Blanchette; Igor V. Grigoriev; Robert E. Minto; David S. Hibbett

doi:10.1016/j.fgb.2015.02.002

Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii

Dimitrios Floudas, Benjamin W. Held, Robert Riley, Laszlo G. Nagy, Gage Koehler, Anthony S. Ransdell, Hina Younus, Julianna Chow, Jennifer Chiniquy, Anna Lipzen, Andrew Tritt, Hui Sun, Sajeet Haridas, Kurt LaButti, Robin A. Ohm, Ursula Kües, Robert A. Blanchette, Igor V. Grigoriev, Robert E. Minto, David S. Hibbett

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117 Scopus citations

Abstract

Wood decay mechanisms in Agaricomycotina have been traditionally separated in two categories termed white and brown rot. Recently the accuracy of such a dichotomy has been questioned. Here, we present the genome sequences of the white-rot fungus Cylindrobasidium torrendii and the brown-rot fungus Fistulina hepatica both members of Agaricales, combining comparative genomics and wood decay experiments. C. torrendii is closely related to the white-rot root pathogen Armillaria mellea, while F. hepatica is related to Schizophyllum commune, which has been reported to cause white rot. Our results suggest that C. torrendii and S. commune are intermediate between white-rot and brown-rot fungi, but at the same time they show characteristics of decay that resembles soft rot. Both species cause weak wood decay and degrade all wood components but leave the middle lamella intact. Their gene content related to lignin degradation is reduced, similar to brown-rot fungi, but both have maintained a rich array of genes related to carbohydrate degradation, similar to white-rot fungi. These characteristics appear to have evolved from white-rot ancestors with stronger ligninolytic ability. F. hepatica shows characteristics of brown rot both in terms of wood decay genes found in its genome and the decay that it causes. However, genes related to cellulose degradation are still present, which is a plesiomorphic characteristic shared with its white-rot ancestors. Four wood degradation-related genes, homologs of which are frequently lost in brown-rot fungi, show signs of pseudogenization in the genome of F. hepatica. These results suggest that transition toward a brown-rot lifestyle could be an ongoing process in F. hepatica. Our results reinforce the idea that wood decay mechanisms are more diverse than initially thought and that the dichotomous separation of wood decay mechanisms in Agaricomycotina into white rot and brown rot should be revisited.

Original language	English (US)
Pages (from-to)	78-92
Number of pages	15
Journal	Fungal Genetics and Biology
Volume	76
DOIs	https://doi.org/10.1016/j.fgb.2015.02.002
State	Published - Mar 1 2015

Bibliographical note

Funding Information:
This work was supported by the PolyPEET project, Taxonomy and Evolution of the Polyporales (Basidiomycota, Fungi) under the NSF award DEB-0933081 (DSH) and the Open Tree of Life project under the NSF award DEB-1208719 (DSH). It was also partially supported by the National Institutes of Health ( 7R15 GM069493 REM ), National Science Foundation ( MCB 0919938 REM ), and the Center for Membrane Biosciences, IUPUI . The work conducted by the U.S. Department of Energy Joint Genome Institute is supported by the Office of Science of the U.S. Department of Energy under contract DE-AC02-05CH11231 . We thank Francis Martin for kindly providing permission to use data of the unpublished genomes of G. luxurians, H. sublateritium, and P. crispa. The alignments of sequence data for the organismal phylogeny have been deposited at TreeBASE ( http://purl.org/phylo/treebase/phylows/study/TB2:S16800 ). All data related to the species phylogeny or the wood decay gene families phylogenies have also been deposited at Dryad (doi:10.5061/dryad.71tg4). Assemblies and annotations of the reported genomes of F. hepatica ATCC 64428 and C. torrendii FP15055 ss-10 are available from the JGI fungal portal MycoCosm ( http://jgi.doe.gov/fungi ) and from DDBJ/EMBL/GenBank under the following accessions: JYFI00000000, JYFH00000000.

Publisher Copyright:
© 2015 Elsevier Inc.

Keywords

Brown rot
Genome sequencing
Pseudogenes
Reconciliation
White rot
Wood decay

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10.1016/j.fgb.2015.02.002

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Floudas, D., Held, B. W., Riley, R., Nagy, L. G., Koehler, G., Ransdell, A. S., Younus, H., Chow, J., Chiniquy, J., Lipzen, A., Tritt, A., Sun, H., Haridas, S., LaButti, K., Ohm, R. A., Kües, U., Blanchette, R. A., Grigoriev, I. V., Minto, R. E., & Hibbett, D. S. (2015). Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii. Fungal Genetics and Biology, 76, 78-92. https://doi.org/10.1016/j.fgb.2015.02.002

Floudas, D, Held, BW, Riley, R, Nagy, LG, Koehler, G, Ransdell, AS, Younus, H, Chow, J, Chiniquy, J, Lipzen, A, Tritt, A, Sun, H, Haridas, S, LaButti, K, Ohm, RA, Kües, U, Blanchette, RA, Grigoriev, IV, Minto, RE & Hibbett, DS 2015, 'Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii', Fungal Genetics and Biology, vol. 76, pp. 78-92. https://doi.org/10.1016/j.fgb.2015.02.002

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title = "Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii",

abstract = "Wood decay mechanisms in Agaricomycotina have been traditionally separated in two categories termed white and brown rot. Recently the accuracy of such a dichotomy has been questioned. Here, we present the genome sequences of the white-rot fungus Cylindrobasidium torrendii and the brown-rot fungus Fistulina hepatica both members of Agaricales, combining comparative genomics and wood decay experiments. C. torrendii is closely related to the white-rot root pathogen Armillaria mellea, while F. hepatica is related to Schizophyllum commune, which has been reported to cause white rot. Our results suggest that C. torrendii and S. commune are intermediate between white-rot and brown-rot fungi, but at the same time they show characteristics of decay that resembles soft rot. Both species cause weak wood decay and degrade all wood components but leave the middle lamella intact. Their gene content related to lignin degradation is reduced, similar to brown-rot fungi, but both have maintained a rich array of genes related to carbohydrate degradation, similar to white-rot fungi. These characteristics appear to have evolved from white-rot ancestors with stronger ligninolytic ability. F. hepatica shows characteristics of brown rot both in terms of wood decay genes found in its genome and the decay that it causes. However, genes related to cellulose degradation are still present, which is a plesiomorphic characteristic shared with its white-rot ancestors. Four wood degradation-related genes, homologs of which are frequently lost in brown-rot fungi, show signs of pseudogenization in the genome of F. hepatica. These results suggest that transition toward a brown-rot lifestyle could be an ongoing process in F. hepatica. Our results reinforce the idea that wood decay mechanisms are more diverse than initially thought and that the dichotomous separation of wood decay mechanisms in Agaricomycotina into white rot and brown rot should be revisited.",

keywords = "Brown rot, Genome sequencing, Pseudogenes, Reconciliation, White rot, Wood decay",

author = "Dimitrios Floudas and Held, {Benjamin W.} and Robert Riley and Nagy, {Laszlo G.} and Gage Koehler and Ransdell, {Anthony S.} and Hina Younus and Julianna Chow and Jennifer Chiniquy and Anna Lipzen and Andrew Tritt and Hui Sun and Sajeet Haridas and Kurt LaButti and Ohm, {Robin A.} and Ursula K{\"u}es and Blanchette, {Robert A.} and Grigoriev, {Igor V.} and Minto, {Robert E.} and Hibbett, {David S.}",

note = "Funding Information: This work was supported by the PolyPEET project, Taxonomy and Evolution of the Polyporales (Basidiomycota, Fungi) under the NSF award DEB-0933081 (DSH) and the Open Tree of Life project under the NSF award DEB-1208719 (DSH). It was also partially supported by the National Institutes of Health ( 7R15 GM069493 REM ), National Science Foundation ( MCB 0919938 REM ), and the Center for Membrane Biosciences, IUPUI . The work conducted by the U.S. Department of Energy Joint Genome Institute is supported by the Office of Science of the U.S. Department of Energy under contract DE-AC02-05CH11231 . We thank Francis Martin for kindly providing permission to use data of the unpublished genomes of G. luxurians, H. sublateritium, and P. crispa. The alignments of sequence data for the organismal phylogeny have been deposited at TreeBASE ( http://purl.org/phylo/treebase/phylows/study/TB2:S16800 ). All data related to the species phylogeny or the wood decay gene families phylogenies have also been deposited at Dryad (doi:10.5061/dryad.71tg4). Assemblies and annotations of the reported genomes of F. hepatica ATCC 64428 and C. torrendii FP15055 ss-10 are available from the JGI fungal portal MycoCosm ( http://jgi.doe.gov/fungi ) and from DDBJ/EMBL/GenBank under the following accessions: JYFI00000000, JYFH00000000. Publisher Copyright: {\textcopyright} 2015 Elsevier Inc.",

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doi = "10.1016/j.fgb.2015.02.002",

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T1 - Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii

AU - Floudas, Dimitrios

AU - Held, Benjamin W.

AU - Riley, Robert

AU - Nagy, Laszlo G.

AU - Koehler, Gage

AU - Ransdell, Anthony S.

AU - Younus, Hina

AU - Chow, Julianna

AU - Chiniquy, Jennifer

AU - Lipzen, Anna

AU - Tritt, Andrew

AU - Sun, Hui

AU - Haridas, Sajeet

AU - LaButti, Kurt

AU - Ohm, Robin A.

AU - Kües, Ursula

AU - Blanchette, Robert A.

AU - Grigoriev, Igor V.

AU - Minto, Robert E.

AU - Hibbett, David S.

N1 - Funding Information: This work was supported by the PolyPEET project, Taxonomy and Evolution of the Polyporales (Basidiomycota, Fungi) under the NSF award DEB-0933081 (DSH) and the Open Tree of Life project under the NSF award DEB-1208719 (DSH). It was also partially supported by the National Institutes of Health ( 7R15 GM069493 REM ), National Science Foundation ( MCB 0919938 REM ), and the Center for Membrane Biosciences, IUPUI . The work conducted by the U.S. Department of Energy Joint Genome Institute is supported by the Office of Science of the U.S. Department of Energy under contract DE-AC02-05CH11231 . We thank Francis Martin for kindly providing permission to use data of the unpublished genomes of G. luxurians, H. sublateritium, and P. crispa. The alignments of sequence data for the organismal phylogeny have been deposited at TreeBASE ( http://purl.org/phylo/treebase/phylows/study/TB2:S16800 ). All data related to the species phylogeny or the wood decay gene families phylogenies have also been deposited at Dryad (doi:10.5061/dryad.71tg4). Assemblies and annotations of the reported genomes of F. hepatica ATCC 64428 and C. torrendii FP15055 ss-10 are available from the JGI fungal portal MycoCosm ( http://jgi.doe.gov/fungi ) and from DDBJ/EMBL/GenBank under the following accessions: JYFI00000000, JYFH00000000. Publisher Copyright: © 2015 Elsevier Inc.

PY - 2015/3/1

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N2 - Wood decay mechanisms in Agaricomycotina have been traditionally separated in two categories termed white and brown rot. Recently the accuracy of such a dichotomy has been questioned. Here, we present the genome sequences of the white-rot fungus Cylindrobasidium torrendii and the brown-rot fungus Fistulina hepatica both members of Agaricales, combining comparative genomics and wood decay experiments. C. torrendii is closely related to the white-rot root pathogen Armillaria mellea, while F. hepatica is related to Schizophyllum commune, which has been reported to cause white rot. Our results suggest that C. torrendii and S. commune are intermediate between white-rot and brown-rot fungi, but at the same time they show characteristics of decay that resembles soft rot. Both species cause weak wood decay and degrade all wood components but leave the middle lamella intact. Their gene content related to lignin degradation is reduced, similar to brown-rot fungi, but both have maintained a rich array of genes related to carbohydrate degradation, similar to white-rot fungi. These characteristics appear to have evolved from white-rot ancestors with stronger ligninolytic ability. F. hepatica shows characteristics of brown rot both in terms of wood decay genes found in its genome and the decay that it causes. However, genes related to cellulose degradation are still present, which is a plesiomorphic characteristic shared with its white-rot ancestors. Four wood degradation-related genes, homologs of which are frequently lost in brown-rot fungi, show signs of pseudogenization in the genome of F. hepatica. These results suggest that transition toward a brown-rot lifestyle could be an ongoing process in F. hepatica. Our results reinforce the idea that wood decay mechanisms are more diverse than initially thought and that the dichotomous separation of wood decay mechanisms in Agaricomycotina into white rot and brown rot should be revisited.

AB - Wood decay mechanisms in Agaricomycotina have been traditionally separated in two categories termed white and brown rot. Recently the accuracy of such a dichotomy has been questioned. Here, we present the genome sequences of the white-rot fungus Cylindrobasidium torrendii and the brown-rot fungus Fistulina hepatica both members of Agaricales, combining comparative genomics and wood decay experiments. C. torrendii is closely related to the white-rot root pathogen Armillaria mellea, while F. hepatica is related to Schizophyllum commune, which has been reported to cause white rot. Our results suggest that C. torrendii and S. commune are intermediate between white-rot and brown-rot fungi, but at the same time they show characteristics of decay that resembles soft rot. Both species cause weak wood decay and degrade all wood components but leave the middle lamella intact. Their gene content related to lignin degradation is reduced, similar to brown-rot fungi, but both have maintained a rich array of genes related to carbohydrate degradation, similar to white-rot fungi. These characteristics appear to have evolved from white-rot ancestors with stronger ligninolytic ability. F. hepatica shows characteristics of brown rot both in terms of wood decay genes found in its genome and the decay that it causes. However, genes related to cellulose degradation are still present, which is a plesiomorphic characteristic shared with its white-rot ancestors. Four wood degradation-related genes, homologs of which are frequently lost in brown-rot fungi, show signs of pseudogenization in the genome of F. hepatica. These results suggest that transition toward a brown-rot lifestyle could be an ongoing process in F. hepatica. Our results reinforce the idea that wood decay mechanisms are more diverse than initially thought and that the dichotomous separation of wood decay mechanisms in Agaricomycotina into white rot and brown rot should be revisited.

KW - Brown rot

KW - Genome sequencing

KW - Pseudogenes

KW - Reconciliation

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KW - Wood decay

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ER -

Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii

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Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii

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Bibliographical note

Keywords

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HItachi S3500N Variable Pressure SEM

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