Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis.
Ustilago maydis is a ubiquitous pathogen of maize and a well-established model organism for the study of plant-microbe interactions. This basidiomycete fungus does not use aggressive virulence strategies to kill its host. U. maydis belongs to the group of biotrophic parasites (the smuts) that depend on living tissue for proliferation and development. Here we report the genome sequence for a member of this economically important group of biotrophic fungi. The 20.5-million-base U. maydis genome assembly contains 6,902 predicted protein-encoding genes and lacks pathogenicity signatures found in the genomes of aggressive pathogenic fungi, for example a battery of cell-wall-degrading enzymes. However, we detected unexpected genomic features responsible for the pathogenicity of this organism. Specifically, we found 12 clusters of genes encoding small secreted proteins with unknown function. A significant fraction of these genes exists in small gene families. Expression analysis showed that most of the genes contained in these clusters are regulated together and induced in infected tissue. Deletion of individual clusters altered the virulence of U. maydis in five cases, ranging from a complete lack of symptoms to hypervirulence. Despite years of research into the mechanism of pathogenicity in U. maydis, no 'true' virulence factors had been previously identified. Thus, the discovery of the secreted protein gene clusters and the functional demonstration of their decisive role in the infection process illuminate previously unknown mechanisms of pathogenicity operating in biotrophic fungi. Genomic analysis is, similarly, likely to open up new avenues for the discovery of virulence determinants in other pathogens.
Kämper
Jörg
J
Department of Organismic Interactions, Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch Strasse, D-35043 Marburg, Germany. kahmann@mpi-marburg.mpg.de
Kahmann
Regine
R
Bölker
Michael
M
Ma
Li-Jun
LJ
Brefort
Thomas
T
Saville
Barry J
BJ
Banuett
Flora
F
Kronstad
James W
JW
Gold
Scott E
SE
Müller
Olaf
O
Perlin
Michael H
MH
Wösten
Han A B
HA
de Vries
Ronald
R
Ruiz-Herrera
José
J
Reynaga-Peña
Cristina G
CG
Snetselaar
Karen
K
McCann
Michael
M
Pérez-Martín
José
J
Feldbrügge
Michael
M
Basse
Christoph W
CW
Steinberg
Gero
G
Ibeas
Jose I
JI
Holloman
William
W
Guzman
Plinio
P
Farman
Mark
M
Stajich
Jason E
JE
Sentandreu
Rafael
R
González-Prieto
Juan M
JM
Kennell
John C
JC
Molina
Lazaro
L
Schirawski
Jan
J
Mendoza-Mendoza
Artemio
A
Greilinger
Doris
D
Münch
Karin
K
Rössel
Nicole
N
Scherer
Mario
M
Vranes
Miroslav
M
Ladendorf
Oliver
O
Vincon
Volker
V
Fuchs
Uta
U
Sandrock
Björn
B
Meng
Shaowu
S
Ho
Eric C H
EC
Cahill
Matt J
MJ
Boyce
Kylie J
KJ
Klose
Jana
J
Klosterman
Steven J
SJ
Deelstra
Heine J
HJ
Ortiz-Castellanos
Lucila
L
Li
Weixi
W
Sanchez-Alonso
Patricia
P
Schreier
Peter H
PH
Häuser-Hahn
Isolde
I
Vaupel
Martin
M
Koopmann
Edda
E
Friedrich
Gabi
G
Voss
Hartmut
H
Schlüter
Thomas
T
Margolis
Jonathan
J
Platt
Darren
D
Swimmer
Candace
C
Gnirke
Andreas
A
Chen
Feng
F
Vysotskaia
Valentina
V
Mannhaupt
Gertrud
G
Güldener
Ulrich
U
Münsterkötter
Martin
M
Haase
Dirk
D
Oesterheld
Matthias
M
Mewes
Hans-Werner
HW
Mauceli
Evan W
EW
DeCaprio
David
D
Wade
Claire M
CM
Butler
Jonathan
J
Young
Sarah
S
Jaffe
David B
DB
Calvo
Sarah
S
Nusbaum
Chad
C
Galagan
James
J
Birren
Bruce W
BW
D005656:Fungal Proteins / Q000235:genetics / Q000378:metabolism; D020869:Gene Expression Profiling; D015966:Gene Expression Regulation, Fungal; D005800:Genes, Fungal / Q000235:genetics; D016681:Genome, Fungal / Q000235:genetics*; D023281:Genomics; D005810:Multigene Family / Q000235:genetics; D014588:Ustilago / Q000235:genetics* / Q000254:growth & development / Q000472:pathogenicity*; D014774:Virulence / Q000235:genetics; D003313:Zea mays / Q000382:microbiology*
D005656:Fungal Proteins