Evidence of the accumulation of allele-specific non-synonymous substitutions in the young region of recombination suppression within the mating-type chromosomes of Neurospora tetrasperma

Currently, little is known about the origin and early evolution of sex chromosomes. This largely due to the fact that ancient non-recombining sex chromosomes are highly degenerated, and thus provide little information about the early genomic events in their evolution. The Neurospora tetrasperma mating-type (mat) chromosomes contain a young (<6 Mya) and large region (>6.6Mb) of suppressed recombination, thereby providing a model system to study early stages of sex chromosome evolution. Here, we examined alleles of 207 genes located on the N. tetrasperma mat a and mat A chromosomes to test for signs of genomic alterations at the protein level in the young region of recombination suppression. We report that the N. tetrasperma mat a and mat A chromosomes have each independently accumulated allele-specific non-synonymous codon substitutions in a time-dependent, and gene-specific manner in the recombinationally suppressed region. In addition, examination of the ratio (ω) of non-synonymous substitutions (dN) to synonymous substitutions (dS) using maximum likelihood analyses, indicates that such changes are associated with relaxed purifying selection, a finding consistent with genomic degeneration. We also reveal that sex specific biases in mutation rates or selection pressures are not necessary for genomic alterations in sex chromosomes, and that recombination suppression in itself is sufficient to explain these results. The present findings greatly extend our current understanding of genomic events associated within the young region of recombination suppression in these fungal sex regulating chromosomes.

目前，学界对性染色体的起源与早期演化仍知之甚少。究其主要原因，古老的非重组性染色体已发生高度退化，因此几乎无法为其演化过程中的早期基因组事件提供有效研究信息。四孢脉孢菌（Neurospora tetrasperma）的交配型（mating-type, mat）染色体包含一个年轻（距今不足6百万年）且长度超过6.6Mb的重组抑制区域，由此为探究性染色体演化的早期阶段提供了理想的模式系统。本研究针对四孢脉孢菌mat a与mat A染色体上的207个基因的等位基因展开分析，以检测该重组抑制年轻区域内蛋白质水平的基因组变异迹象。研究结果显示，四孢脉孢菌的mat a与mat A染色体各自独立地在重组抑制区域内，以时间依赖性及基因特异性的方式积累了等位基因特异性的非同义密码子替换。此外，通过最大似然分析法计算非同义替换（non-synonymous substitution, dN）与同义替换（synonymous substitution, dS）的比值（ω），结果表明这类变异与松弛纯化选择存在关联，这一发现与基因组退化的特征相符。本研究还揭示，性染色体出现基因组变异并不需要突变率或选择压力存在性别偏倚，仅重组抑制本身即可合理解释上述实验结果。本研究结果极大地拓展了学界对这类真菌性调控染色体中重组抑制年轻区域相关基因组事件的认知。