Codon optimization underpins generalist parasitism in fungi.
The range of hosts that parasites can infect is a key determinant of the emergence and spread of disease. Yet, the impact of host range variation on the evolution of parasite genomes remains unknown. Here, we show that codon optimization underlies genome adaptation in broad host range parasites. We found that the longer proteins encoded by broad host range fungi likely increase natural selection on codon optimization in these species. Accordingly, codon optimization correlates with host range across the fungal kingdom. At the species level, biased patterns of synonymous substitutions underpin increased codon optimization in a generalist but not a specialist fungal pathogen. Virulence genes were consistently enriched in highly codon-optimized genes of generalist but not specialist species. We conclude that codon optimization is related to the capacity of parasites to colonize multiple hosts. Our results link genome evolution and translational regulation to the long-term persistence of generalist parasitism.
LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.
Thomas
T
Badet
LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.
Remi
R
Peyraud
LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.
Malick
M
Mbengue
LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.
Olivier
O
Navaud
Centre for Crop and Disease Management, Department of Environment and Agriculture, Curtin University, Perth, Australia.
Mark
M
Derbyshire
Centre for Crop and Disease Management, Department of Environment and Agriculture, Curtin University, Perth, Australia.
Richard P
RP
Oliver
LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.
Adelin
0000-0003-3156-272X
A
Barbacci
LIPM, Université de Toulouse, INRA, CNRS, Castanet-Tolosan, France.
Sylvain
0000-0002-2442-9632
S
Raffaele
D001203:Ascomycota / Q000145:classification / Q000235:genetics* / Q000472:pathogenicity; D001487:Basidiomycota / Q000145:classification / Q000235:genetics* / Q000472:pathogenicity; D005075:Biological Evolution; D003062:Codon; D005656:Fungal Proteins / Q000235:genetics; D005815:Genetic Code; D016681:Genome, Fungal; D058507:Host Specificity; D003904:Mitosporic Fungi / Q000145:classification / Q000235:genetics* / Q000472:pathogenicity; D010802:Phylogeny; D010944:Plants / Q000382:microbiology*; D012641:Selection, Genetic; D014774:Virulence
D003062:Codon; D005656:Fungal Proteins
codon usage; evolutionary biology; fungal parasites; genome evolution; genomics; host range