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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. In this paper, 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.more » 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. Finally, 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.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [5]; ORCiD logo [5];  [3];  [3];  [3];  [3];  [3];  [3];  [3];  [6];  [7];  [2];  [3];  [5];  [8]
+ Show Author Affiliations
  1. Clark Univ., Worcester, MA (United States); MEMEG, Lund (Sweden)
  2. Univ. of Minnesota, Minneapolis, MN (United States)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Clark Univ., Worcester, MA (United States); Biological Research Centre of the Hungarian Academy of Sciences, Szeged (Hungary)
  5. Indiana Univ.-Purdue Univ., Indianapolis, IN (United States)
  6. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of Utrecht (Netherlands)
  7. Univ. of Goettingen (Germany)
  8. Clark Univ., Worcester, MA (United States)
Publication Date:
Research Org.:
US Department of Energy (DOE) Joint Genome Inst., Walnut Creek, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1344454
Alternate Identifier(s):
OSTI ID: 1233941
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Fungal Genetics and Biology
Additional Journal Information:
Journal Volume: 76; Journal ID: ISSN 1087-1845
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Wood decay; White rot; Brown rot; Reconciliation; Pseudogenes; Genome sequencing

Citation Formats

Floudas, Dimitrios, Held, Benjamin W., Riley, Robert, Nagy, Laszlo G., Koehler, Gage, Ransdell, Anthony S., Younus, Hina, Chow, Julianna, Chiniquy, Jennifer, Lipzen, Anna, Tritt, Andrew, Sun, Hui, Haridas, Sajeet, LaButti, Kurt, Ohm, Robin A., Kües, Ursula, Blanchette, Robert A., Grigoriev, Igor V., Minto, Robert E., and Hibbett, David S. Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii. United States: N. p., 2015. Web. doi:10.1016/j.fgb.2015.02.002.
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Floudas, Dimitrios, Held, Benjamin W., Riley, Robert, Nagy, Laszlo G., Koehler, Gage, Ransdell, Anthony S., Younus, Hina, Chow, Julianna, Chiniquy, Jennifer, Lipzen, Anna, Tritt, Andrew, Sun, Hui, Haridas, Sajeet, LaButti, Kurt, Ohm, Robin A., Kües, Ursula, Blanchette, Robert A., Grigoriev, Igor V., Minto, Robert E., & Hibbett, David S. Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii. United States. https://doi.org/10.1016/j.fgb.2015.02.002
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Floudas, Dimitrios, Held, Benjamin W., Riley, Robert, Nagy, Laszlo G., Koehler, Gage, Ransdell, Anthony S., Younus, Hina, Chow, Julianna, Chiniquy, Jennifer, Lipzen, Anna, Tritt, Andrew, Sun, Hui, Haridas, Sajeet, LaButti, Kurt, Ohm, Robin A., Kües, Ursula, Blanchette, Robert A., Grigoriev, Igor V., Minto, Robert E., and Hibbett, David S. Thu . "Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii". United States. https://doi.org/10.1016/j.fgb.2015.02.002. https://www.osti.gov/servlets/purl/1344454.
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@article{osti_1344454,
title = {Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii},
author = {Floudas, Dimitrios and Held, Benjamin W. and Riley, Robert and Nagy, Laszlo G. and Koehler, Gage and Ransdell, Anthony S. and Younus, Hina and Chow, Julianna and Chiniquy, Jennifer and Lipzen, Anna and Tritt, Andrew and Sun, Hui and Haridas, Sajeet and LaButti, Kurt and Ohm, Robin A. and Kües, Ursula and Blanchette, Robert A. and Grigoriev, Igor V. and Minto, Robert E. and Hibbett, David S.},
abstractNote = {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. In this paper, 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. Finally, 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.},
doi = {10.1016/j.fgb.2015.02.002},
url = {https://www.osti.gov/biblio/1344454}, journal = {Fungal Genetics and Biology},
issn = {1087-1845},
number = ,
volume = 76,
place = {United States},
year = {2015},
month = {2}
}
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Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1016/j.fgb.2015.02.002
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Cited by: 30 works
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Figures / Tables:

Figure 1 Figure 1: Species phylogeny of 13 Agaricales species and $P. crispa$ (Amylocorticiales) as outgroup. Both ML and Bayesian analyses of 21167 amino acid characters from 26 single copy genes resulted in identical topologies and received maximum bootstrap and posterior probability support at all nodes. The ML tree is shown here.more » WR, white rot; BR, brown rot; LD, litter decomposer; (WR), reported as white rot, but wood decay strategy is uncertain.« less
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    The fungus that came in from the cold: dry rot’s pre-adapted ability to invade buildings
    journal, January 2018

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