Codon optimization underpins generalist parasitism in fungi
- LIPM, Université de Toulouse, INRA, CNRS, France
- Curtin University, Australia
Figures
Figure 1
Contrasted length distribution in proteomes is expected to increase selection on codon optimization in generalist fungi.
(A) Distribution of length (number of codons) in the ribosomal, intracellular and predicted secreted proteomes of 13 specialist fungal parasites and 15 generalist fungal parasites. (B) Relationship …
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Figure 1—source data 1
Equations forming the mathematical model of protein biosynthesis related to protein length and codon optimization parameters; list of parameters and variables used for modeling of growth rate based on proteome properties; and values of parameters used for modeling of growth rate based on proteome properties.
- https://doi.org/10.7554/eLife.22472.003
Figure 2
Codon optimization correlates with host range in fungal parasites.
Genome-scale codon optimization correlates with host range in 36 parasites across the kingdom Fungi. Species considered as specialists (less than four host genera) are shown in green, species …
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Figure 2—source data 1
Codon optimization is dependent on breadth of host range but not genome assembly parameters.
Results of an analysis of variance (ANOVA) considering the number of contigs in genome assemblies (no. contigs, as a descriptor of the quality of assemblies), host range and their interaction as factors; values of host range, number of contigs and codon optimization (S) for each genome.
- https://doi.org/10.7554/eLife.22472.005
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Figure 2—source data 2
List of core ortholog genes and their codon adaptation indices.
- https://doi.org/10.7554/eLife.22472.006
Figure 3
Codon optimization and host range co-evolved multiple times across fungal phylogeny.
(A) Phylogeny, genome-scale codon optimization and host range in 36 parasites across the kingdom Fungi. Nine non-pathogenic species belonging to the major branches of Fungi are shown for comparison. …
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Figure 3—source data 1
Overview of host range features for the 45 fungal species analyzed in this work.
- https://doi.org/10.7554/eLife.22472.009
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Figure 3—source data 2
Phylogenetic tree of the 45 fungal species analyzed in this work.
- https://doi.org/10.7554/eLife.22472.010
Figure 4 with 2 supplements
Biased synonymous substitution patterns underpin codon optimization in local populations of a generalist but not a specialist fungal parasite.
(A) Genome-wide frequencies of variant codons in local populations of the host generalist Sclerotinia sclerotiorum and the host specialist Zymoseptoria tritici, according to the number of genomic …
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Figure 4—source data 1
Codon statistics for S. sclerotiorum and Z. tritici genomes.
- https://doi.org/10.7554/eLife.22472.012
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Figure 4—source data 2
Frequency of codon substitutions in S. sclerotiorum and Z. tritici populations (as % of all codons).
Ref. indicates codons in the reference genome (isolate 1980 for S. sclerotiorum and isolate IPO323 for Z. tritici) tog ether with their total number, Var. indicates variant codons.
- https://doi.org/10.7554/eLife.22472.013
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Figure 4—source code 1
Python scripts for in silico evolution of codon usage.
- https://doi.org/10.7554/eLife.22472.014
Figure 4—figure supplement 1
Experimental determination of S. sclerotiorum tRNA accumulation supports a good correlation between genomic copy numbers and tRNA accumulation.
The accumulation of tRNA transcripts was determined by sequencing small RNAs of S. sclerotiorum grown in vitro and in planta. (A) Normalized read depth correlated exponentially with tRNA copy number …
Figure 4—figure supplement 2
Analysis of Single Nucleotide Polymorphisms (SNPs) in a natural population of the generalist plant pathogen Sclerotinia sclerotiorum.
(A) IGS-based phylogeny of the S. sclerotiorum isolates re-sequenced in this work. (B) Frequency of SNPs according to codon position and SNP type. (C) SNPs in coding regions do not show significant …
Figure 5
Codon optimization strongly associates with host colonization in generalist fungal parasites.
(A) Genes induced during host infection are enriched among high tRNA adaptation index genes in generalist but not specialist parasite genomes. Error bars show standard error of the mean. (B) Genes …
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Figure 5—source data 1
Summary of gene expression data used for the analysis of tAI in host-induced genes.
- https://doi.org/10.7554/eLife.22472.018
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Figure 5—source data 2
Distribution of host-induced genes according to tAI (as % of all host-induced genes).
- https://doi.org/10.7554/eLife.22472.019
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Figure 5—source data 3
Distribution of secreted protein genes according to tAI (as % of all host-induced genes).
- https://doi.org/10.7554/eLife.22472.020
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Figure 5—source data 4
Codon optimization values in secreted and non-secreted proteins for each of the 45 fungal genomes analyzed in this work.
Cat. Category; NP, non parasitic; Gen, generalist; Spe, specialist; No. Sec. Prot., Number of secreted proteins.
- https://doi.org/10.7554/eLife.22472.021
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Figure 5—source data 5
Distribution of tRNA adaptation indices per Gene Ontology in generalist and specialist genomes.
- https://doi.org/10.7554/eLife.22472.022
Tables
Table 1
List of fungal species analyzed in this work, their host range and genome-scale codon optimization values. Genome-scale codon optimization was calculated using tRNA adaptation indiced (S), codon …
Species | Host range | Class* | S | SCAI | SscnRCA |
|---|---|---|---|---|---|
Cryptococcus neoformans | 800 | Gen. | 0.843 | 0.870 | 0.860 |
Rhizoctonia solani | 690 | Gen. | 0.432 | 0.624 | 0.583 |
Botrytis cinerea | 556 | Gen. | 0.597 | 0.675 | 0.653 |
sclerotinia sclerotiorum | 332 | Gen. | 0.524 | 0.583 | 0.553 |
Beauveria bassiana | 269 | Gen. | 0.616 | 0.619 | 0.747 |
Metarhizium acridum | 228 | Gen. | 0.647 | 0.595 | 0.712 |
Aspergillus fumigatus | 175 | Gen. | 0.609 | 0.643 | 0.684 |
Batrachochytrium dendrobatidis | 153 | Gen. | 0.545 | 0.521 | 0.602 |
Verticilium dahliae | 78 | Gen. | 0.537 | 0.426 | 0.627 |
Fusarium graminearum | 72 | Gen. | 0.788 | 0.818 | 0.819 |
Colletotrichum graminicola | 59 | Gen. | 0.572 | 0.444 | 0.644 |
Rhizopus oryzae | 28 | Gen. | 0.625 | 0.563 | 0.691 |
Penicillium digitatum | 17 | Gen. | 0.545 | 0.602 | 0.630 |
Alternaria brassicicola | 16 | Gen. | 0.400 | 0.592 | 0.628 |
Pyrenophora tritici-repentis | 11 | Gen. | 0.419 | 0.569 | 0.570 |
Pseudogymnoascus destructans | 8 | 0.484 | 0.513 | 0.505 | |
Encephalitozoon intestinalis | 7 | 0.313 | 0.558 | 0.528 | |
Melampsora larici-populina | 7 | 0.194 | 0.142 | 0.055 | |
Stagonospora nodorum | 7 | 0.155 | 0.431 | 0.462 | |
Colletotrichum higginsianum | 6 | 0.393 | 0.295 | 0.480 | |
Sporisorium reilianum | 5 | 0.476 | 0.200 | 0.429 | |
Taphrina deformans | 4 | 0.403 | 0.679 | 0.671 | |
Magnaporthe oryzae | 4 | 0.437 | 0.424 | 0.575 | |
Puccinia graminis | 2 | Spe. | −0.032 | 0.344 | 0.249 |
Wolfiporia cocos | 2 | Spe. | 0.217 | 0.266 | 0.316 |
Moniliophthora roreri | 2 | Spe. | 0.406 | 0.530 | 0.551 |
Passalora fulva | 2 | Spe. | −0.011 | 0.513 | 0.514 |
Rozella allomycis | 1 | Spe. | 0.236 | 0.096 | 0.259 |
Nosema ceranae | 1 | Spe. | 0.021 | −0.155 | −0.085 |
Puccinia triticina | 1 | Spe. | 0.204 | 0.501 | 0.472 |
Dothistroma septosporum | 1 | Spe. | 0.211 | 0.447 | 0.354 |
Pseudocercospora fijiensis | 1 | Spe. | 0.227 | 0.495 | 0.490 |
Zymoseptoria tritici | 1 | Spe. | −0.019 | 0.355 | 0.248 |
Blumeria graminis | 1 | Spe. | 0.116 | −0.187 | 0.164 |
Erysiphe necator | 1 | Spe. | 0.174 | −0.092 | 0.117 |
Ophiocordyceps unilateralis | 1 | Spe. | 0.166 | 0.268 | 0.458 |
Gonapodya prolifera | 0 | np | 0.115 | 0.311 | 0.363 |
Rhodotorula toruloides | 0 | np | 0.344 | 0.385 | 0.470 |
Serpula lacrymans | 0 | np | −0.001 | 0.379 | 0.395 |
Laccaria bicolor | 0 | np | −0.026 | 0.237 | 0.155 |
Agaricus bisporus | 0 | np | 0.361 | 0.432 | 0.400 |
Tuber melanosporum | 0 | np | 0.230 | 0.319 | 0.349 |
Oidiodendron maius | 0 | np | 0.147 | 0.442 | 0.388 |
Myceliophthora thermophila | 0 | np | 0.246 | 0.123 | 0.323 |
Chaetomium globosum | 0 | np | 0.148 | 0.204 | 0.342 |
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*The class column indicates whether species were considered as generalist (Gen.), specialist (Spe.) or non-parasitic (np).
