The evolution of cardenolide-resistant forms of Na plus ,K plus -ATPase in Danainae butterflies
The evolution of cardenolide-resistant forms of Na plus ,K plus -ATPase in Danainae butterflies
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DOI：
10.1111/j.1365-294x.2011.05379.x
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发表时间：
2012-01-01
影响因子：
4.9
通讯作者：
Andolfatto, Peter
中科院分区：
文献类型：
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作者：
Aardema, Matthew L.;Zhen, Ying;Andolfatto, Peter
Cardenolide是一类植物次生化合物，能抑制敏感动物体内Na+，K+-ATPase的正常功能。尽管如此，许多昆虫物种还是能够为了自己的防御而隔离卡宾内酯。这些蝴蝶包括达奈亚科(科：若蝶科)的蝴蝶，如帝王蝶(Danaus Plexippus)。以往的研究表明，帝王蜂在Na+，K+-ATPase(ATPA)的a亚基中存在天冬酰胺(N)到组氨酸(H)的取代(N122H)，从而降低了这种酶对Cardenolide的敏感性。最近，有人提出，在ATPA第111位，君主还可能含有亮氨酸(L)/谷氨酰胺(Q)多态。这种较晚的氨基酸也可能导致腰果内酯不敏感。然而，我们发现，对最初报道的ATPA DNA序列的错误注释导致了几个错误的结论。利用帝王及其近亲的群体遗传学和系统发育分析，我们发现在所有丹纳亚科动物辐射之前发生了一次古老的Q111L替换，随后在同一位置发生了第二次Valine(V)的替换，这是在Danaus属多样化之前出现的。相比之下，N122H似乎是最近专门针对君主的替代品。令人惊讶的是，对更广泛的昆虫系统发育的研究发现，氨基酸替换(Q111L？L111V+N122H)也存在于摄食含Cardenolide的寄主植物的合欢甲虫(叶甲科：叶甲亚科)中。这两个远亲谱系中氨基酸替换的平行模式与这些替换在降低Cardenolide敏感性方面的适应作用是一致的，并表明它们的时间顺序可能受到上位相互作用的限制。
Cardenolides are a class of plant secondary compounds that inhibit the proper functioning of the Na+, K+-ATPase enzyme in susceptible animals. Nonetheless, many insect species are able to sequester cardenolides for their own defence. These include butterflies in the subfamily Danainae (Family: Nymphalidae) such as the monarch (Danaus plexippus). Previous studies demonstrated that monarchs harbour an asparagine (N) to histidine (H) substitution (N122H) in the a subunit of Na+, K+-ATPase (ATPa) that reduces this enzymes sensitivity to cardenolides. More recently, it has been suggested that at ATPa position 111, monarchs may also harbour a leucine (L)/glutamine (Q) polymorphism. This later amino acid could also contribute to cardenolide insensitivity. However, here we find that incorrect annotation of the initially reported DNA sequence for ATPa has led to several erroneous conclusions. Using a population genetic and phylogenetic analysis of monarchs and their close relatives, we show that an ancient Q111L substitution occurred prior to the radiation of all Danainae, followed by a second substitution at the same site to valine (V), which arose before the diversification of the Danaus genus. In contrast, N122H appears to be a recent substitution specific to monarchs. Surprisingly, examination of a broader insect phylogeny reveals that the same progression of amino acid substitutions (Q111L ? L111V + N122H) has also occurred in Chyrsochus beetles (Family: Chrysomelidae, Subfamily: Eumolpinae) that feed on cardenolide-containing host plants. The parallel pattern of amino acid substitution in these two distantly related lineages is consistent with an adaptive role for these substitutions in reducing cardenolide sensitivity and suggests that their temporal order may be limited by epistatic interactions.