Sources of Fungal Genetic Variation and Associating It with Phenotypic Diversity

Abstract

The first eukaryotic genome to be sequenced was fungal, and there continue to be more sequenced genomes in the kingdom Fungi than in any other eukaryotic kingdom. Comparison of these genomes reveals many sources of genetic variation, from single nucleotide polymorphisms to horizontal gene transfer and on to changes in the arrangement and number of chromosomes, not to mention endofungal bacteria and viruses. Population genomics shows that all sources generate variation all the time and implicate natural selection as the force maintaining genome stability. Variation in wild populations is a rich resource for associating genetic variation with phenotypic variation, whether through quantitative trait locus mapping, genome-wide association studies, or reverse ecology. Subjects of studies associating genetic and phenotypic variation include model fungi, e.g., Saccharomyces and Neurospora, but pioneering studies have also been made with fungi pathogenic to plants, e.g., Pyricularia (= Magnaporthe), Zymoseptoria, and Fusarium, and to humans, e.g., Coccidioides, Cryptococcus, and Candida.

FIGURE 1

Gene family Bayesian phylogeny for proteinase genes with S8 domains showing (top) some phylogenetic lineages with no expansion and (below) others with a large expansion due to nine gene duplications (asterisks). Key to taxon abbreviations preceding gene identifiers: Aspergillus oryzae (aory), Aspergillus fumigatus (afum), Aspergillus nidulans (anid), Uncinocarpus reesii (uree), Coccidioides immitis (cimm), C. posadasii (cpos), Sclerotinia sclerotiorum (sscl), Botrytis cinerea (bcin), Stagonospora nodorom (snod), Magnaporthe grisea (mgri), Trichoderma reesii (tree), Laccaria bicolor (lbic), and Coprinopsis cinerea (ccin). Adapted from reference .

FIGURE 2

Diagrams showing aneuploidy and loss of heterozygosity (LOH) in haploid and diploid genomes. Each individual has seven distinct chromosomes colored to show heterozygosity.

FIGURE 3

Contour-clamped homogeneous electric field gel karyotype of Fusarium oxysporum chromosomes showing conditionally dispensable chromosomes (CDCs) and their transmission between strains. (A) Donor strain Fol007 (left) harbors CDCs 1 and 2 (arrows), and recipient strain Fo-47 (right) lacks them. Strains 1A-3C (middle lanes) are derived from simple coincubation of Fol007 and Fo-47. These strains have the Fo-47 karyotype and have gained CDCs 1 or 2 (arrows), or both, from Fol007. (B) Southern hybridization of the contour-clamped homogeneous electric field gel to a probe with DNA from CDC 1 (SIX6), confirming the presence of CDC 1 in donor strain Fol007 and progeny strains 1A-3C, which possess the karyotype of the recipient strain Fo-47. Adapted from reference .

FIGURE 4

Population structure. (A) Bayesian phylogenetic analysis of SNPs from transcriptomes of 50 Neurospora crassa individuals from around the Gulf of Mexico showing that individuals thought to form one population actually are found in seven populations. Adapted from reference . (B) Bayesian phylogenetic analysis of SNPs from transcriptomes of 112 N. crassa individuals from the same geographic area as the Louisiana population in A showing no population subdivision. Note the many individuals with the same genotype as the laboratory strain, FGSC 2489, indicative of mistakes made in transferring isolates. Adapted from reference .

FIGURE 5

Hybridization and introgression in weakly diverged populations. Hybridization and introgression can be detected in genome scans of closely related populations when the genes are introduced from a more diverged population. (Top) Genome scan by Fst (a measure of relative genetic divergence) showing that nearly all genes have low divergence (yellow dots and one red dot), but one gene shows exceptionally large divergence (blue dot). (Bottom) Population tree with one gene tree highlighted in yellow showing that well-diverged genes entering from older, more diverged populations (blue dots and arrows) will be detected by comparison with the low divergence in the rest of the genome. However, genes exchanged between the populations will be missed (red dots and arrows) due to their low divergence being indistinguishable from the rest of the genome.

FIGURE 6

Hybridization and introgression in strongly diverged populations or species. Hybridization and introgression can be detected in genome scans of distantly related populations or species when the gene flow is between the two well-diverged groups. (Top) Genome scan by Fst (a measure of relative genetic divergence) showing that nearly all genes have high divergence (yellow dots and one red dot), but one gene shows exceptionally low divergence (blue dot). (Bottom) Population tree with one gene tree highlighted in yellow showing that genes exchanged between the populations will be detected (blue dots and arrows) due to their lack of divergence compared to the high divergence of the rest of the genome. However, genes entering from populations from other well-diverged lineages (red dots and arrows) will show divergence similar to the rest of the genome and be missed.

FIGURE 7

Regions of extreme divergence between populations of N. crassa. Rows are aligned genomes of Louisiana (LA), Caribbean (Carib), and other populations (out) seen in Fig. 4. Columns are nucleotide positions in four colors for the four bases. Highlighted is the region of high divergence between the Louisiana population and the Caribbean and other populations. The genome variation in this region is consistent with a history in the Louisiana population of hybridization and introgression. Low variation among Louisiana individuals in this region is consistent with a recent selective sweep. Variation in the length of introgressed regions in the Louisiana population may indicate that the sweep is still in progress. Among the six genes in the region of divergence is PAC10-like, which codes for a prefoldin that chaperones cold-sensitive proteins. Adapted from reference .

FIGURE 8

Evidence of recent hybridization. Genome scans for introgressed DNA in the 20 largest contigs of eight Neurospora discreta individuals from the Alaska-European lineage. Numbers of SNPs introgressed from the New Mexico-Washington (NM-WA) lineage are shown on the y axis. Alaskan strain AKFA12 stands out as having 12% of its genome introgressed from the NM-WA lineage, as expected from a few matings between a hybrid individual and members of the Alaskan population. Adapted from reference .