DNA polymorphism in recombining and non-recombining mating-type-specific loci of the smut fungus Microbotryum

Abstract

The population-genetic processes leading to the genetic degeneration of non-recombining regions have mainly been studied in animal and plant sex chromosomes. Here, we report population genetic analysis of the processes in the non-recombining mating-type-specific regions of the smut fungus Microbotryum violaceum. M. violaceum has A1 and A2 mating types, determined by mating-type-specific 'sex chromosomes' that contain 1-2 Mb long non-recombining regions. If genetic degeneration were occurring, then one would expect reduced DNA polymorphism in the non-recombining regions of this fungus. The analysis of DNA diversity among 19 M. violaceum strains, collected across Europe from Silene latifolia flowers, revealed that (i) DNA polymorphism is relatively low in all 20 studied loci (π∼0.15%), (ii) it is not significantly different between the two mating-type-specific chromosomes nor between the non-recombining and recombining regions, (iii) there is substantial population structure in M. violaceum populations, which resembles that of its host species, S. latifolia, and (iv) there is significant linkage disequilibrium, suggesting that widespread selfing in this species results in a reduction of the effective recombination rate across the genome. We hypothesise that selfing-related reduction of recombination across the M. violaceum genome negates the difference in the level of DNA polymorphism between the recombining and non-recombining regions, and may possibly lead to similar levels of genetic degeneration in the mating-type-specific regions of the non-recombining 'sex chromosomes' and elsewhere in the genome.

Figure 1

Neighbour-joining phylogenies of M. violaceum constructed from concatenated A1- and A2-linked genes. The branch lengths are proportional to the maximum-composite likelihood distance from MEGA4 (Tamura et al., 2007).

Figure 2

The results of Bayesian clustering analysis of recombining genes using Structure2 (Pritchard et al., 2000). The horizontal axis shows the number of clusters (K). (a) The posterior probability of the data, given the number of clusters, averaged across 10 runs with s.d. between runs. (b) The second order rate of change of the likelihood function (ΔK) with respect to K (Evanno et al., 2005).

Figure 3

Cluster membership for K=2 (a), 4 (b) and 7 (c) based on the recombining regions in the data set, identified by Structure (Pritchard et al., 2000).

Figure 4

Per-nucleotide DNA polymorphism (π) in recombining (Rec) and non-recombining (A1 and A2) regions of the M. violaceum genome for the entire sample (three leftmost data points) and for three sub-populations (groups 1–3, as defined in Figure 3b). Group 4 consists only of two Iberian individuals and is not shown. The error bars represent s.d. of the DNA diversity estimates.

Figure 5

LD between polymorphisms in the studied genes. Significant pairwise LD values (χ²-test: P<0.05%) are shown as black boxes. As polymorphisms in the non-recombining regions are linked, only one randomly chosen polymorphic site is shown for the A1- and A2-linked loci to save space. For the recombining (pa- and aut-) loci, all polymorphisms are shown.