Cis-by-Trans regulatory divergence causes the asymmetric lethal effects of an ancestral hybrid incompatibility gene.
Cis-by-Trans regulatory divergence causes the asymmetric lethal effects of an ancestral hybrid incompatibility gene.
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DOI：
10.1371/journal.pgen.1002597
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发表时间：
2012
期刊：
影响因子：
4.5
通讯作者：
Barbash DA
中科院分区：
文献类型：
--
作者：
Maheshwari S;Barbash DA
Dobzhansky和Muller（D-M）模型通过两个或多个位点上的谱系特异性衍生等位基因之间的相互作用来解释杂种不亲和性（HI）的进化。与HI是由功能分歧引起的预期一致，许多导致物种间不相容性的蛋白质编码基因显示出适应性进化的特征，包括Lhr，其编码的异染色质蛋白的氨基酸序列在果蝇和果蝇之间广泛分歧。模拟自然选择。D.黑腹果蝇D. simulans F1杂种子系通过去除D. simulans Lhr，而不是D. Lhr的致死效应，表明该致死效应是适应性进化的结果。simulans血统有人提出，适应性蛋白分歧LHR反映了拮抗协同进化与物种特异性异染色质序列和LHR蛋白定位的缺陷导致杂交致死。在这里，我们提出了令人惊讶的结果，这是不一致的编码序列为基础的模型。使用在天然条件下表达的Lhr转基因，我们没有发现LHR定位在D. melanogaster和D. simulans，我们也没有发现证据表明它在种间杂种中定位错误。相反，我们证明了Lhr直系同源物在杂交背景中的差异表达，D. simulans Lhr是D.黑腹菌我们进一步表明，这种不对称的表达是由顺式由反式调节分歧的LHR。因此，Lhr直向同源物的非等效杂交致死效应可以通过两种直向同源物共享的分子功能的不对称表达来解释，因此推测是从Lhr的祖先等位基因遗传的。我们提出了一个模型，即杂交致死性发生的进化祖先和衍生等位基因之间的相互作用。当两个不同的物种交配时，杂交后代通常是不育的或致命的。这种杂种不相容性导致物种之间的生殖隔离，是维持物种作为独立单位的重要机制。一种名为致命杂交拯救（Lhr）的基因是果蝇物种之间杂交致死的部分原因。像许多其他杂交不亲和基因一样，杂交物种中的Lhr蛋白质序列通过自然选择彼此分化。这一发现和其他发现导致了Lhr的功能在两个物种之间发生了变化的假设，这就是Lhr成为杂交致死基因的原因。使用一系列遗传、分子和细胞学检测，我们报告了与这些假设相反的证据，即杂交致死活性是两个物种共有的功能，并从它们的共同祖先遗传而来。这个结果是特别令人惊讶的，因为来自两个物种的Lhr基因对杂种活力具有不同的影响。我们发现，这些差异性的影响是由LHR在杂交中的表达水平的差异，而不是由其蛋白质编码序列的变化引起的。我们的研究结果表明，虽然自然选择在进化杂交不相容性方面可能很重要，但在这种情况下它是如何做到这一点的仍然是个谜。
The Dobzhansky and Muller (D-M) model explains the evolution of hybrid incompatibility (HI) through the interaction between lineage-specific derived alleles at two or more loci. In agreement with the expectation that HI results from functional divergence, many protein-coding genes that contribute to incompatibilities between species show signatures of adaptive evolution, including Lhr, which encodes a heterochromatin protein whose amino acid sequence has diverged extensively between Drosophila melanogaster and D. simulans by natural selection. The lethality of D. melanogaster/D. simulans F1 hybrid sons is rescued by removing D. simulans Lhr, but not D. melanogaster Lhr, suggesting that the lethal effect results from adaptive evolution in the D. simulans lineage. It has been proposed that adaptive protein divergence in Lhr reflects antagonistic coevolution with species-specific heterochromatin sequences and that defects in LHR protein localization cause hybrid lethality. Here we present surprising results that are inconsistent with this coding-sequence-based model. Using Lhr transgenes expressed under native conditions, we find no evidence that LHR localization differs between D. melanogaster and D. simulans, nor do we find evidence that it mislocalizes in their interspecific hybrids. Rather, we demonstrate that Lhr orthologs are differentially expressed in the hybrid background, with the levels of D. simulans Lhr double that of D. melanogaster Lhr. We further show that this asymmetric expression is caused by cis-by-trans regulatory divergence of Lhr. Therefore, the non-equivalent hybrid lethal effects of Lhr orthologs can be explained by asymmetric expression of a molecular function that is shared by both orthologs and thus was presumably inherited from the ancestral allele of Lhr. We present a model whereby hybrid lethality occurs by the interaction between evolutionarily ancestral and derived alleles. When two different species mate, the hybrid progeny are often sterile or lethal. Such hybrid incompatibilities cause reproductive isolation between species and are an important mechanism for maintaining species as separate units. A gene called Lethal hybrid rescue (Lhr) is part of the cause of hybrid lethality between Drosophila species. Like many other hybrid incompatibility genes, Lhr protein sequences in the hybridizing species have diverged from one another by natural selection. This and other findings led to the hypotheses that the function of Lhr has changed between the two species, and this is what makes Lhr a hybrid lethality gene. Using a series of genetic, molecular, and cytological assays, we report evidence contrary to these hypotheses, that hybrid lethal activity is instead a function shared by both species and inherited from their common ancestor. This result is particularly surprising because the Lhr genes from the two species have different effects on hybrid viability. We discovered that these differential effects are caused by differences in expression levels of Lhr in hybrids rather than by changes in its protein-coding sequence. Our results demonstrate that, while natural selection may be important in evolving hybrid incompatibilities, how it does so in this case remains mysterious.
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影响因子：
9.8
作者：
Chou JY;Hung YS;Lin KH;Lee HY;Leu JY
通讯作者：
Leu JY
影响因子：
64.8
作者：
HUTTER, P;ASHBURNER, M
通讯作者：
ASHBURNER, M
DOI：
10.1073/pnas.0804761105
发表时间：
2008-08-12
影响因子：
11.1
作者：
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通讯作者：
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影响因子：
9.8
作者：
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通讯作者：
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影响因子：
3.3
作者：
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通讯作者：
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