Data from: Amino acid change in an orchid desaturase enables mimicry of the pollinator’s sex pheromone

Mimicry illustrates the power of selection to produce phenotypic convergence in biology [ 1 ]. A striking example is the imitation of female insects by plants that are pollinated by sexual deception of males of the same insect species [ 2–4 ]. This involves mimicry of visual, tactile, and chemical signals of females [ 2–7 ], especially their sex pheromones [ 8–11 ]. The Mediterranean orchid Ophrys exaltata employs chemical mimicry of cuticular hydrocarbons, particularly the 7-alkenes, in an insect sex pheromone to attract and elicit mating behavior in its pollinators, males of the cellophane bee Colletes cunicularius [ 11–13 ]. A difference in alkene double-bond positions is responsible for reproductive isolation between O. exaltata and closely related species, such as O. sphegodes [ 13–16 ]. We show that these 7-alkenes are likely determined by the action of the stearoyl-acyl-carrier-protein desaturase (SAD) homolog SAD5. After gene duplication, changes in subcellular localization relative to the ancestral housekeeping desaturase may have allowed proto-SAD5’s reaction products to undergo further biosynthesis to both 7- and 9-alkenes. Such ancestral coproduction of two alkene classes may have led to pollinator-mediated deleterious pleiotropy. Despite possible evolutionary intermediates with reduced activity, amino acid changes at the bottom of the substrate-binding cavity have conferred enzyme specificity for 7-alkene biosynthesis by preventing the binding of longer-chained fatty acid (FA) precursors by the enzyme. This change in desaturase function enabled the orchid to perfect its chemical mimicry of pollinator sex pheromones by escape from deleterious pleiotropy, supporting a role of pleiotropy in determining the possible trajectories of adaptive evolution.

拟态 (Mimicry) 阐释了选择 (selection) 作用在生物学中催生表型趋同 (phenotypic convergence) 的能力[1]。其中一个极具代表性的案例，是通过对同种雄性昆虫实施性欺骗 (sexual deception) 以完成传粉的植物，对雌性昆虫的模仿行为[2-4]。这类模仿涉及对雌性个体的视觉、触觉与化学信号的模拟[2-7]，尤以其性信息素 (sex pheromones) 的模拟最为核心[8-11]。眉兰属 (Ophrys) 的高柱兰 (Ophrys exaltata) 通过对昆虫性信息素中表皮碳氢化合物 (cuticular hydrocarbons) ——尤其是7-烯烃 (7-alkenes) ——的化学拟态，能够吸引其传粉者——雄性纸蜂Colletes cunicularius，并诱发其交配行为[11-13]。烯烃双键位置的差异，是高柱兰与近缘物种（如Ophrys sphegodes）之间形成生殖隔离 (reproductive isolation) 的重要原因[13-16]。本研究表明，这类7-烯烃的合成大概率由硬脂酰-酰基载体蛋白去饱和酶 (stearoyl-acyl-carrier-protein desaturase, SAD) 的同源基因SAD5介导。在经历基因重复 (gene duplication) 事件后，相较于祖先型管家去饱和酶 (ancestral housekeeping desaturase)，SAD5的亚细胞定位 (subcellular localization) 发生了改变，这使得原祖SAD5的反应产物能够进一步通过生物合成途径生成7-烯烃与9-烯烃两类物质。这类祖先型双烯烃类别的共同合成，可能引发了传粉者介导的有害多效性 (deleterious pleiotropy)。尽管存在活性降低的进化中间型，但底物结合腔 (substrate-binding cavity) 底部的氨基酸突变，通过阻止酶与长链脂肪酸 (fatty acid, FA) 前体结合，赋予了SAD5合成7-烯烃的酶特异性。这种去饱和酶功能的改变，使得该兰花得以摆脱有害多效性的束缚，完善了其对传粉者性信息素的化学拟态，这一结果支持了多效性 (pleiotropy) 在决定适应性进化 (adaptive evolution) 潜在轨迹中所发挥的作用。