Massive Changes in Genome Architecture Accompany the Transition to Self-Fertility in the Filamentous Fungus Neurospora Tetrasperma

By Ellison, Christopher E.; Stajich, Jason E. et al. | Genetics, September 2011 | Go to article overview

Massive Changes in Genome Architecture Accompany the Transition to Self-Fertility in the Filamentous Fungus Neurospora Tetrasperma


Ellison, Christopher E., Stajich, Jason E., Jacobson, David J., Natvig, Donald O., Lapidus, Alla, Foster, Brian, Aerts, Andrea, Riley, Robert, Lindquist, Erika A., Grigoriev, Igor V., Taylor, John W., Genetics


ABSTRACT A large region of suppressed recombination surrounds the sex-determining locus of the self-fertile fungus Neurospora tetrasperma. This region encompasses nearly one-fifth of the N. tetrasperma genome and suppression of recombination is necessary for self-fertility. The similarity of the N. tetrasperma mating chromosome to plant and animal sex chromosomes and its recent origin (,5 MYA), combined with a long history of genetic and cytological research, make this fungus an ideal model for studying the evolutionary consequences of suppressed recombination. Here we compare genome sequences from two N. tetrasperma strains of opposite mating type to determine whether structural rearrangements are associated with the nonrecombining region and to examine the effect of suppressed recombination for the evolution of the genes within it. We find a series of three inversions encompassing the majority of the region of suppressed recombination and provide evidence for two different types of rearrangement mechanisms: the recently proposed mechanism of inversion via staggered single-strand breaks as well as ectopic recombination between transposable elements. In addition, we show that the N. tetrasperma mat a mating-type region appears to be accumulating deleterious substitutions at a faster rate than the other mating type (mat A) and thus may be in the early stages of degeneration.

THE elimination of recombination can have a dramatic effect on the evolutionary trajectory of a genomic region. Without recombination, selection acts on linked genetic complexes rather than independent genetic elements. Theory predicts the accumulation of deleterious mutations and selfish genetic elements in the absence of recombinational purging and a reduced ability to fix adaptive mutations (Charlesworth and Charlesworth 2000; Charlesworth et al. 2005).

The genetic consequences of suppressed recombination have been best studied in the sex chromosomes of outcrossing eukaryotes, e.g., plants, insects, and mammals, because the initial step in the formation of sex chromosomes is posited to be a cessation of recombination across a genomic region that includes the sex-determining locus (Charlesworth et al. 2005). The suppression of recombination across such a region will be selected for if it creates linkage between the sex-determining locus and other genes that are sexually antagonistic in that their functions are beneficial to only one of the sexes. The nonrecombining region can be formed from the spread of recombinational suppressors or structural changes to the chromosome that prevent synapsis. In either case, studies in mammals, birds, and plants have shown evidence that present-day nonrecombining regions are composed of multiple discrete blockage events that occurred at different time points in the evolutionary history of the taxon in question [termed "evolutionary strata" by Lahn and Page 1999 (Charlesworth et al. 2005)].

Because large, nonrecombining, sex-linked regions appear to have evolved independently across a diverse array of taxonomic groups, comparing the evolution of such regions across disparate taxa will make it possible to understand the evolutionary events associated with their formation as well as the genomic consequences of suppressed recombination.

In several species of fungi, the properties of the chromosomal region surrounding the mating-type locus have been studied extensively because of their similarities to the sex chromosomes of other organisms (Fraser and Heitman 2004, 2005). The mating-type locus of Cryptococcus neoformans occurs within an 100-kb region where recombination is suppressed due to multiple chromosomal rearrangements (Lengeler et al. 2002; Fraser et al. 2007). The evolutionary history of this region includes the accumulation of transposable elements as well as gene conversion, gene loss, and pseudogenization (Fraser et al. 2004; Metin et al. 2010). The mating-type region of Ustilago hordei resides within a 500-kb region that is characterized by suppressed recombination and chromosomal rearrangements (Lee et al. …

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Massive Changes in Genome Architecture Accompany the Transition to Self-Fertility in the Filamentous Fungus Neurospora Tetrasperma
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