Life Sciences, University of Manchester, Manchester, United Kingdom.
PLoS One. 2012;7(8):e42022. doi: 10.1371/journal.pone.0042022. Epub 2012 Aug 14.
Chromosomal rearrangements occur readily in nature and are a major reshaping force during genome evolution. Such large scale modifications are usually deleterious causing several fitness defects, but sometimes can confer an advantage and become adaptive. For example the DAL metabolic cluster in yeast was assembled in recent evolutionary times in the Hemiascomycetes lineage, through a set of rearrangements that brought together the genes involved in the allantoin degradation pathway. In eukaryotes, the existence of physical clustering of genes with related functions supports the notion that neighbouring ORFs tend to be co-expressed and that the order of genes along the chromosomes may have biological significance, rather than being random as previously believed. In this study, we investigate the phenotypic effect that inversions have on the DAL gene cluster, expressed during nitrogen starvation. In all Saccharomyces "sensu stricto" species the order of the DAL cluster is conserved, while in the "sensu lato" species Naumovia castellii, which grows significantly worse than S. cerevisiae on allantoin, the cluster includes two nested inversions encompassing three DAL genes. We constructed several inverted and non-inverted S. cerevisiae strains possessing different inversions including those to mimic the configuration of the N. castellii DAL cluster. We showed that the inversion of DAL2 lower its own expression and reduces yeast fitness during nitrogen starvation. This rearrangement also altered the expression of the neighbouring genes DAL1 and DAL4. Moreover, we showed that the expression of the DAL4 anti-sense transcript (SUT614) does not change upon inversions of DAL2 and therefore is unlikely to be involved in its regulation. These results show that the order of the DAL cluster has an impact on the phenotype and gene expression, suggesting that these rearrangements may have been adaptive in the "sensu stricto" group in relation to the low availability of nitrogen in the environment.
染色体重排在自然界中很容易发生，是基因组进化过程中的主要重塑力量。这种大规模的修饰通常是有害的，导致多种适应性缺陷，但有时也能带来优势并变得具有适应性。例如，酵母中的 DAL 代谢簇是在最近的进化时期，通过一系列重排，将参与尿囊素降解途径的基因聚集在一起而在半子囊菌目谱系中组装的。在真核生物中，具有相关功能的基因的物理聚类的存在支持了这样一种观点，即邻近的 ORF 往往是共表达的，并且染色体上基因的顺序可能具有生物学意义，而不是像以前认为的那样是随机的。在这项研究中，我们研究了倒位对 DAL 基因簇在氮饥饿期间表达的表型效应。在所有酿酒酵母“狭义”物种中，DAL 簇的顺序是保守的，而在“广义”物种 Naumovia castellii 中，它在尿囊素上的生长明显比 S. cerevisiae 差，该簇包含两个嵌套的倒位，包含三个 DAL 基因。我们构建了几个倒置和非倒置的 S. cerevisiae 菌株，具有不同的倒置，包括模拟 N. castellii DAL 簇配置的倒置。我们表明，DAL2 的倒置降低了自身的表达，并降低了氮饥饿期间酵母的适应性。这种重排还改变了邻近基因 DAL1 和 DAL4 的表达。此外，我们表明，DAL4 反义转录物（SUT614）的表达不会因 DAL2 的倒置而改变，因此不太可能参与其调节。这些结果表明，DAL 簇的顺序对表型和基因表达有影响，表明这些重排可能与环境中氮的低可用性有关，在“狭义”组中是适应性的。
