Community-wide convergent evolution in insect adaptation to toxic cardenolides by substitutions in the Na,K-ATPase

被引:207
作者
Dobler, Susanne [1 ]
Dalla, Safaa [1 ]
Wagschal, Vera [1 ]
Agrawal, Anurag A. [2 ]
机构
[1] Univ Hamburg, Dept Biol, D-20146 Hamburg, Germany
[2] Cornell Univ, Dept Ecol & Evolutionary Biol, Ithaca, NY 14853 USA
基金
美国国家科学基金会;
关键词
insect-plant interactions; specialist herbivores; target site insensitivity; toxin resistance; cardiac glycosides; OUABAIN-BINDING-SITE; RESISTANT SODIUM-CHANNELS; HIGH-AFFINITY BINDING; AMINO-ACID-RESIDUES; ALPHA-SUBUNIT; DIRECTED MUTAGENESIS; GASTRIC H; K-ATPASE; ECHOLOCATING BATS; DANAUS-PLEXIPPUS; MOLECULAR-BASIS;
D O I
10.1073/pnas.1202111109
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The extent of convergent molecular evolution is largely unknown, yet is critical to understanding the genetics of adaptation. Target site insensitivity to cardenolides is a prime candidate for studying molecular convergence because herbivores in six orders of insects have specialized on these plant poisons, which gain their toxicity by blocking an essential transmembrane carrier, the sodium pump (Na,K-ATPase). We investigated gene sequences of the Na,K-ATPase alpha-subunit in 18 insects feeding on cardenolide-containing plants (spanning 15 genera and four orders) to screen for amino acid substitutions that might lower sensitivity to cardenolides. The replacement N122H that was previously shown to confer resistance in the monarch butterfly (Danaus plexippus) and Chrysochus leaf beetles was found in four additional species, Oncopeltus fasciatus and Lygaeus kalmii (Heteroptera, Lygaeidae), Labidomera clivicollis (Coleoptera, Chrysomelidae), and Liriomyza asclepiadis (Diptera, Agromyzidae). Thus, across 300 Myr of insect divergence, specialization on cardenolide-containing plants resulted in molecular convergence for an adaptation likely involved in coevolution. Our screen revealed a number of other substitutions connected to cardenolide binding in mammals. We confirmed that some of the particular substitutions provide resistance to cardenolides by introducing five distinct constructs of the Drosophila melanogaster gene into susceptible eucaryotic cells under an ouabain selection regime. These functional assays demonstrate that combined substitutions of Q(111) and N-122 are synergistic, with greater than twofold higher resistance than either substitution alone and >12-fold resistance over the wild type. Thus, even across deep phylogenetic branches, evolutionary degrees of freedom seem to be limited by physiological constraints, such that the same molecular substitutions confer adaptation.
引用
收藏
页码:13040 / 13045
页数:6
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