Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen.
Some of the most damaging tree pathogens can attack woody stems, causing lesions (cankers) that may be lethal. To identify the genomic determinants of wood colonization leading to canker formation, we sequenced the genomes of the poplar canker pathogen, Mycosphaerella populorum, and the closely related poplar leaf pathogen, M. populicola. A secondary metabolite cluster unique to M. populorum is fully activated following induction by poplar wood and leaves. In addition, genes encoding hemicellulose-degrading enzymes, peptidases, and metabolite transporters were more abundant and were up-regulated in M. populorum growing on poplar wood-chip medium compared with M. populicola. The secondary gene cluster and several of the carbohydrate degradation genes have the signature of horizontal transfer from ascomycete fungi associated with wood decay and from prokaryotes. Acquisition and maintenance of the gene battery necessary for growth in woody tissues and gene dosage resulting in gene expression reconfiguration appear to be responsible for the adaptation of M. populorum to infect, colonize, and cause mortality on poplar woody stems.
Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4;
Braham
B
Dhillon
Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4; feaunico@mail.ubc.ca Richard.Hamelin@RNCan-NRCan.gc.ca.
Nicolas
N
Feau
US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
Andrea L
AL
Aerts
Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4;
Stéphanie
S
Beauseigle
Centre d'Étude de la Forêt, Université Laval, Québec, QC, Canada G1V 0A6;
Louis
L
Bernier
US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
Alex
A
Copeland
Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Québec, QC, Canada G1V 4C7;
Adam
A
Foster
Department of Botany, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4;
Navdeep
N
Gill
UMR 7257 Centre National de la Recherche Scientifique, Aix-Marseille University, 13288 Marseille, France; Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia;
Bernard
B
Henrissat
Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4;
Padmini
P
Herath
US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
Kurt M
KM
LaButti
Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes (URMITE), UM63, CNRS 7278, IRD 198, INSERM U1095, IHU Méditerranée Infection, Aix-Marseille University, 13005 Marseille, France;
Anthony
A
Levasseur
US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
Erika A
EA
Lindquist
Fungal Physiology, Centraalbureau voor Schimmelcultures-Royal Netherlands Academy of Arts and Sciences Fungal Biodiversity Centre (CBS-KNAW), 3584 CT, Utrecht, The Netherlands; Fungal Molecular Physiology, Utrecht University, 3584 CT, Utrecht, The Netherlands;
Eline
E
Majoor
US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
Robin A
RA
Ohm
US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
Jasmyn L
JL
Pangilinan
Forest Products Biotechnology and Bioenergy, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4; and.
Amadeus
A
Pribowo
Forest Products Biotechnology and Bioenergy, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4; and.
John N
JN
Saddler
Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4;
Monique L
ML
Sakalidis
Fungal Physiology, Centraalbureau voor Schimmelcultures-Royal Netherlands Academy of Arts and Sciences Fungal Biodiversity Centre (CBS-KNAW), 3584 CT, Utrecht, The Netherlands; Fungal Molecular Physiology, Utrecht University, 3584 CT, Utrecht, The Netherlands;
Ronald P
RP
de Vries
US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;
Igor V
IV
Grigoriev
US Department of Agriculture-Agricultural Research Service Crop Production and Pest Control Research Unit, Purdue University, West Lafayette, IN 47907-2054.
Stephen B
SB
Goodwin
Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Québec, QC, Canada G1V 4C7;
Philippe
P
Tanguay
Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4; Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Québec, QC, Canada G1V 4C7; feaunico@mail.ubc.ca Richard.Hamelin@RNCan-NRCan.gc.ca.
Richard C
RC
Hamelin
D000222:Adaptation, Physiological / Q000235:genetics*; D001203:Ascomycota / Q000235:genetics* / Q000254:growth & development* / Q000472:pathogenicity; D001483:Base Sequence; D015169:Colony Count, Microbial; D018628:Gene Dosage; D015966:Gene Expression Regulation, Fungal; D022761:Gene Transfer, Horizontal; D049810:Genetic Speciation; D016681:Genome, Fungal / Q000235:genetics; D054884:Host-Pathogen Interactions / Q000235:genetics; D026121:Indole Alkaloids / Q000378:metabolism; D008969:Molecular Sequence Data; D009584:Nitrogen / Q000378:metabolism; D010802:Phylogeny; D032107:Populus / Q000382:microbiology; D059748:Proteolysis; D026801:Synteny / Q000235:genetics; D013997:Time Factors; D014197:Trees / Q000382:microbiology*; D014934:Wood / Q000382:microbiology*
D026121:Indole Alkaloids; C019290:chaetoglobosins; D009584:Nitrogen
Septoria canker; fungal genomics; poplar pathogen; tree disease