Selection-Driven Evolution of Sex-Biased Genes Is Consistent with Sexual Selection in Arabidopsis thaliana

Selection-Driven Evolution of Sex-Biased Genes Is Consistent with Sexual Selection in Arabidopsis thaliana
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DOI:
10.1093/molbev/mst226
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发表时间:
2014-03-01
影响因子:
10.7
通讯作者:
Schmid, Karl J.
Schmid, Karl J.
中科院分区:
生物学1区
文献类型:
--
作者:
Gossmann, Toni I.;Schmid, Marc W.;Schmid, Karl J.

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性别偏倚基因是指在一种性别中具有优先或特定表达的基因,在动物中往往表现出加速的进化速度。为了解释观察到的快速进化模式,人们提出了各种各样的假设——这些假设并不相互排斥。一种可能的解释是积极选择,但这只在少数动物物种中出现,而且主要是雄性特有的基因。在这里,我们提出了一项大规模的研究,调查了主要自交受精植物拟南芥性别偏向基因的进化模式。与大多数动物物种不同,拟南芥不具有性染色体,其花同时发育雄性和雌性性器官,其特点是异交率低。利用细胞特异性基因表达数据,我们确定了在雄性和雌性配子(精子、卵子和中心细胞)以及协同体、花粉和花粉管中表达丰富的基因,这些基因在生殖中也起着重要作用。与全基因组平均水平相比,配子和协同体中特异性表达的基因显示出更高的蛋白质进化率,没有证据表明存在正选择。相比之下,花粉和花粉管特异性基因不仅具有较低的蛋白质进化速率,而且具有较高的适应性氨基酸取代比例。我们表明,这是花粉和花粉管特异性表达基因的纯化和正选择水平增加的结果。适应性替代比例的增加不能用花粉和花粉管表达的基因在片段重复中丰富、平均年龄较大或有效群体规模较大的事实来解释。我们的观察结果与前合子性选择是一致的,这是授粉和花粉管生长过程中相互作用的结果,如花粉管竞争。
Sex-biased genes are genes with a preferential or specific expression in one sex and tend to show an accelerated rate of evolution in animals. Various hypotheses-which are not mutually exclusive-have been put forth to explain observed patterns of rapid evolution. One possible explanation is positive selection, but this has been shown only in few animal species and mostly for male-specific genes. Here, we present a large-scale study that investigates evolutionary patterns of sex-biased genes in the predominantly self-fertilizing plant Arabidopsis thaliana. Unlike most animal species, A. thaliana does not possess sex chromosomes, its flowers develop both male and female sexual organs, and it is characterized by low outcrossing rates. Using cell-specific gene expression data, we identified genes whose expression is enriched in comparison with all other tissues in the male and female gametes (sperm, egg, and central cell), as well as in synergids, pollen, and pollen tubes, which also play an important role in reproduction. Genes specifically expressed in gametes and synergids show higher rates of protein evolution compared with the genome-wide average and no evidence for positive selection. In contrast, pollen-and pollen tube-specific genes not only have lower rates of protein evolution but also exhibit a higher proportion of adaptive amino acid substitutions. We show that this is the result of increased levels of purifying and positive selection among genes with pollen- and pollen tube-specific expression. The increased proportion of adaptive substitutions cannot be explained by the fact that pollen- and pollen tube-expressed genes are enriched in segmental duplications, are on average older, or have a larger effective population size. Our observations are consistent with prezygotic sexual selection as a result of interactions during pollination and pollen tube growth such as pollen tube competition.