Insights on the evolution of mycoparasitism from the genome of Clonostachys rosea

Magnus Karlsson; Mikael Brandström Durling; Jaeyoung Choi; Chatchai Kosawang; Gerald Lackner; Georgios D Tzelepis; Kristiina Nygren; Mukesh K Dubey; Nathalie Kamou; Anthony Levasseur; Antonio Zapparata; Jinhui Wang; Daniel Buchvaldt Amby; Birgit Jensen; Sabrina Sarrocco; Emmanuel Panteris; Anastasia L Lagopodi; Stefanie Pöggeler; Giovanni Vannacci; David B. Collinge; Dirk Hoffmeister; Bernard Henrissat; Yong-Hwan Lee; Dan Funck Jensen

doi:10.1093/gbe/evu292

Insights on the evolution of mycoparasitism from the genome of Clonostachys rosea

Magnus Karlsson, Mikael Brandström Durling, Jaeyoung Choi, Chatchai Kosawang, Gerald Lackner, Georgios D Tzelepis, Kristiina Nygren, Mukesh K Dubey, Nathalie Kamou, Anthony Levasseur, Antonio Zapparata, Jinhui Wang, Daniel Buchvaldt Amby, Birgit Jensen, Sabrina Sarrocco, Emmanuel Panteris, Anastasia L Lagopodi, Stefanie Pöggeler, Giovanni Vannacci, David B. CollingeDirk Hoffmeister, Bernard Henrissat, Yong-Hwan Lee, Dan Funck Jensen

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Abstract

Clonostachys rosea is a mycoparasitic fungus that can control several important plant diseases. Here, we report on the genome sequencing of C. rosea and a comparative genome analysis, in order to resolve the phylogenetic placement of C. rosea and to study the evolution of mycoparasitism as a fungal lifestyle. The genome of C. rosea is estimated to 58.3 Mb, and contains 14,268 predicted genes. A phylogenomic analysis shows that C. rosea clusters as sister taxon to plant pathogenic Fusarium species, with mycoparasitic/saprotrophic Trichoderma species in an ancestral position. A comparative analysis of gene family evolution reveals several distinct differences between the included mycoparasites. Clonostachys rosea contains significantly more ATP-binding cassette (ABC) transporters, polyketide synthases, cytochrome P450 monooxygenases, pectin lyases, glucose-methanol-choline oxidoreductases, and lytic polysaccharide monooxygenases compared with other fungi in the Hypocreales. Interestingly, the increase of ABC transporter gene number in C. rosea is associated with phylogenetic subgroups B (multidrug resistance proteins) and G (pleiotropic drug resistance transporters), whereas an increase in subgroup C (multidrug resistance-associated proteins) is evident in Trichoderma virens. In contrast with mycoparasitic Trichoderma species, C. rosea contains very few chitinases. Expression of six group B and group G ABC transporter genes was induced in C. rosea during exposure to the Fusarium mycotoxin zearalenone, the fungicide Boscalid or metabolites from the biocontrol bacterium Pseudomonas chlororaphis. The data suggest that tolerance toward secondary metabolites is a prominent feature in the biology of C. rosea.

Original language	English
Journal	Genome Biology and Evolution
Volume	7
Issue number	2
Pages (from-to)	465-480
Number of pages	16
ISSN	1759-6653
DOIs	https://doi.org/10.1093/gbe/evu292
Publication status	Published - 22 Jan 2015

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Karlsson, M., Durling, M. B., Choi, J., Kosawang, C., Lackner, G., Tzelepis, G. D., Nygren, K., Dubey, M. K., Kamou, N., Levasseur, A., Zapparata, A., Wang, J., Amby, D. B., Jensen, B., Sarrocco, S., Panteris, E., Lagopodi, A. L., Pöggeler, S., Vannacci, G., ... Jensen, D. F. (2015). Insights on the evolution of mycoparasitism from the genome of Clonostachys rosea. Genome Biology and Evolution, 7(2), 465-480. https://doi.org/10.1093/gbe/evu292

Karlsson, M, Durling, MB, Choi, J, Kosawang, C, Lackner, G, Tzelepis, GD, Nygren, K, Dubey, MK, Kamou, N, Levasseur, A, Zapparata, A, Wang, J, Amby, DB , Jensen, B, Sarrocco, S, Panteris, E, Lagopodi, AL, Pöggeler, S, Vannacci, G, Collinge, DB, Hoffmeister, D, Henrissat, B, Lee, Y-H & Jensen, DF 2015, 'Insights on the evolution of mycoparasitism from the genome of Clonostachys rosea', Genome Biology and Evolution, vol. 7, no. 2, pp. 465-480. https://doi.org/10.1093/gbe/evu292

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title = "Insights on the evolution of mycoparasitism from the genome of Clonostachys rosea",

abstract = "Clonostachys rosea is a mycoparasitic fungus that can control several important plant diseases. Here, we report on the genome sequencing of C. rosea and a comparative genome analysis, in order to resolve the phylogenetic placement of C. rosea and to study the evolution of mycoparasitism as a fungal lifestyle. The genome of C. rosea is estimated to 58.3 Mb, and contains 14,268 predicted genes. A phylogenomic analysis shows that C. rosea clusters as sister taxon to plant pathogenic Fusarium species, with mycoparasitic/saprotrophic Trichoderma species in an ancestral position. A comparative analysis of gene family evolution reveals several distinct differences between the included mycoparasites. Clonostachys rosea contains significantly more ATP-binding cassette (ABC) transporters, polyketide synthases, cytochrome P450 monooxygenases, pectin lyases, glucose-methanol-choline oxidoreductases, and lytic polysaccharide monooxygenases compared with other fungi in the Hypocreales. Interestingly, the increase of ABC transporter gene number in C. rosea is associated with phylogenetic subgroups B (multidrug resistance proteins) and G (pleiotropic drug resistance transporters), whereas an increase in subgroup C (multidrug resistance-associated proteins) is evident in Trichoderma virens. In contrast with mycoparasitic Trichoderma species, C. rosea contains very few chitinases. Expression of six group B and group G ABC transporter genes was induced in C. rosea during exposure to the Fusarium mycotoxin zearalenone, the fungicide Boscalid or metabolites from the biocontrol bacterium Pseudomonas chlororaphis. The data suggest that tolerance toward secondary metabolites is a prominent feature in the biology of C. rosea.",

author = "Magnus Karlsson and Durling, {Mikael Brandstr{\"o}m} and Jaeyoung Choi and Chatchai Kosawang and Gerald Lackner and Tzelepis, {Georgios D} and Kristiina Nygren and Dubey, {Mukesh K} and Nathalie Kamou and Anthony Levasseur and Antonio Zapparata and Jinhui Wang and Amby, {Daniel Buchvaldt} and Birgit Jensen and Sabrina Sarrocco and Emmanuel Panteris and Lagopodi, {Anastasia L} and Stefanie P{\"o}ggeler and Giovanni Vannacci and Collinge, {David B.} and Dirk Hoffmeister and Bernard Henrissat and Yong-Hwan Lee and Jensen, {Dan Funck}",

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T1 - Insights on the evolution of mycoparasitism from the genome of Clonostachys rosea

AU - Karlsson, Magnus

AU - Durling, Mikael Brandström

AU - Choi, Jaeyoung

AU - Kosawang, Chatchai

AU - Lackner, Gerald

AU - Tzelepis, Georgios D

AU - Nygren, Kristiina

AU - Dubey, Mukesh K

AU - Kamou, Nathalie

AU - Levasseur, Anthony

AU - Zapparata, Antonio

AU - Wang, Jinhui

AU - Amby, Daniel Buchvaldt

AU - Jensen, Birgit

AU - Sarrocco, Sabrina

AU - Panteris, Emmanuel

AU - Lagopodi, Anastasia L

AU - Pöggeler, Stefanie

AU - Vannacci, Giovanni

AU - Collinge, David B.

AU - Hoffmeister, Dirk

AU - Henrissat, Bernard

AU - Lee, Yong-Hwan

AU - Jensen, Dan Funck

N1 - © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

PY - 2015/1/22

Y1 - 2015/1/22

N2 - Clonostachys rosea is a mycoparasitic fungus that can control several important plant diseases. Here, we report on the genome sequencing of C. rosea and a comparative genome analysis, in order to resolve the phylogenetic placement of C. rosea and to study the evolution of mycoparasitism as a fungal lifestyle. The genome of C. rosea is estimated to 58.3 Mb, and contains 14,268 predicted genes. A phylogenomic analysis shows that C. rosea clusters as sister taxon to plant pathogenic Fusarium species, with mycoparasitic/saprotrophic Trichoderma species in an ancestral position. A comparative analysis of gene family evolution reveals several distinct differences between the included mycoparasites. Clonostachys rosea contains significantly more ATP-binding cassette (ABC) transporters, polyketide synthases, cytochrome P450 monooxygenases, pectin lyases, glucose-methanol-choline oxidoreductases, and lytic polysaccharide monooxygenases compared with other fungi in the Hypocreales. Interestingly, the increase of ABC transporter gene number in C. rosea is associated with phylogenetic subgroups B (multidrug resistance proteins) and G (pleiotropic drug resistance transporters), whereas an increase in subgroup C (multidrug resistance-associated proteins) is evident in Trichoderma virens. In contrast with mycoparasitic Trichoderma species, C. rosea contains very few chitinases. Expression of six group B and group G ABC transporter genes was induced in C. rosea during exposure to the Fusarium mycotoxin zearalenone, the fungicide Boscalid or metabolites from the biocontrol bacterium Pseudomonas chlororaphis. The data suggest that tolerance toward secondary metabolites is a prominent feature in the biology of C. rosea.

AB - Clonostachys rosea is a mycoparasitic fungus that can control several important plant diseases. Here, we report on the genome sequencing of C. rosea and a comparative genome analysis, in order to resolve the phylogenetic placement of C. rosea and to study the evolution of mycoparasitism as a fungal lifestyle. The genome of C. rosea is estimated to 58.3 Mb, and contains 14,268 predicted genes. A phylogenomic analysis shows that C. rosea clusters as sister taxon to plant pathogenic Fusarium species, with mycoparasitic/saprotrophic Trichoderma species in an ancestral position. A comparative analysis of gene family evolution reveals several distinct differences between the included mycoparasites. Clonostachys rosea contains significantly more ATP-binding cassette (ABC) transporters, polyketide synthases, cytochrome P450 monooxygenases, pectin lyases, glucose-methanol-choline oxidoreductases, and lytic polysaccharide monooxygenases compared with other fungi in the Hypocreales. Interestingly, the increase of ABC transporter gene number in C. rosea is associated with phylogenetic subgroups B (multidrug resistance proteins) and G (pleiotropic drug resistance transporters), whereas an increase in subgroup C (multidrug resistance-associated proteins) is evident in Trichoderma virens. In contrast with mycoparasitic Trichoderma species, C. rosea contains very few chitinases. Expression of six group B and group G ABC transporter genes was induced in C. rosea during exposure to the Fusarium mycotoxin zearalenone, the fungicide Boscalid or metabolites from the biocontrol bacterium Pseudomonas chlororaphis. The data suggest that tolerance toward secondary metabolites is a prominent feature in the biology of C. rosea.

U2 - 10.1093/gbe/evu292

DO - 10.1093/gbe/evu292

M3 - Journal article

C2 - 25575496

SN - 1759-6653

VL - 7

SP - 465

EP - 480

JO - Genome Biology and Evolution

JF - Genome Biology and Evolution

IS - 2

ER -

Insights on the evolution of mycoparasitism from the genome of Clonostachys rosea

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