Blocked Recombination along the Mating-Type Chromosomes of Neurospora Tetrasperma Involves Both Structural Heterozygosity and Autosomal Genes

By Jacobson, David J. | Genetics, October 2005 | Go to article overview

Blocked Recombination along the Mating-Type Chromosomes of Neurospora Tetrasperma Involves Both Structural Heterozygosity and Autosomal Genes


Jacobson, David J., Genetics


ABSTRACT

The Neurospora tetrasperma mating-type chromosomes have been shown to be structurally heterozygous by reciprocal introgression of these chromosomes between N. tetrasperma and N. crassa. This structural heterozygosity correlates with both a previously described recombination block and cytologically visible unpaired chromosomes at pachytene. Genes on the autosomes are also implicated in blocking recombination.

THE filamentous fungus Neurospora teirasperma is selffertile with a vegetative thallus (mycelium) that is heterokaryotic for mating type (pseudohomothallic). Sexual development in N. ieirasperma has been genetically and developmentally reprogrammed so that two haploid nuclei of opposite mating type (mat A and mat a) are delivered into each of the four ascospores (DODGE 1927; RAJU and PERKINS 1994). To accomplish this nuclear packaging, crossing over is suppressed in the mating-type bivalent (but not in the autosomes), ensuring that mat A and mat a will segregate at the first division of meiosis. Recombination is blocked for >120 MU, which is ^90% of this chromosome (linkage group I) and ~12% of the total genome (GALLEGOS et al. 2000). The two homologs of the mating-type bivalent are seen to remain unpaired at pachytene over most of its length. Chiasmata near the ends hold the homologs together and ensure proper disjunction at anaphase I. Spindles at the second division are precisely repositioned pairwise to ensure that two nuclei of opposite mating type are enclosed in each ascospore, rendering it self-fertile. Pseudohomothallism, as exemplified in N. ieirasperma, leads to sustained but not absolute inbreeding, with profound consequences for population structure and evolution (POWELL et al. 2001).

Because recombination is blocked on the mating-type chromosomes of N. tetrasperma, the regions linked to mat A and mat a have undergone substantial sequence divergence (MERINO et al. 1996). Sequences in the region of suppressed crossing over exhibit heteroallelism (heterozygosity), even when sibling nuclei from the same wild-type isolate are compared. In contrast, the autosomes recombine freely and sibling nuclei of opposite mating type from each wild-type isolate exhibit nearly complete homoallelism (homozygosity) along the autosomes. N. tetrasperma mating-type chromosomes resemble the sex chromosomes in animals in failing to recombine over most of their length. The structure, function, and evolution of fungal mating-type loci and chromosomes is an area of current interest (e.g., FRASER et al. 2004; HOOD et al. 2004). Three questions arise from these observations:

1. Why has the crossover block come to be extended over most of the chromosome? A recombination block in the short region between mat and centromere would suffice to provide the mechanism for pseudohomothallism by maintaining first-division segregation of mating type and the subsequent packaging of opposite mating-type nuclei into individual ascospores.

2. What are the consequences of an extended recombination block for a haploid organism in the context of free recombination in the autosomes? The mating-type chromosome should be subject to Muller's ratchet, resulting in accumulation of alleles of reduced fitness as expected for a nonrecombining chromosome in an otherwise recombining genome (MULLER 1964).

3. What is the cellular basis of blocked recombination?

This study is concerned with the third question.

A likely explanation for the cellular basis of the recombination block would be structural heterozygosity between the mat a and mat A mating-type chromosomes of N. tetrasperma, involving rearrangements such as inversions. However, blocked recombination might be under some other genetically controlled mechanism based on particular gene(s), the mating-type chromosome, and/or the autosomes. To test these alternatives, the mating-type chromosomes were introgressed reciprocally between N. ieiraspermaand N. …

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