The dynamics of cyanide defences in the life cycle of an aposematic butterfly: Biosynthesis versus sequestration
The dynamics of cyanide defences in the life cycle of an aposematic butterfly: Biosynthesis versus sequestration
复制标题
DOI：
10.1016/j.ibmb.2019.103259
复制
发表时间：
2020-01-01
影响因子：
3.8
通讯作者：
Bak, Soren
中科院分区：
文献类型：
--
作者：
de Castro, Erika C. Pinheiro;Demirtas, Rojan;Bak, Soren
Heliconius蝴蝶在西番莲属植物中高度专业化，产卵和幼虫仅在它们身上进食。有趣的是，Heliconius蝴蝶和西番莲属植物都含有生氰葡糖苷（CNglcs）。当以特定的西番莲属物种为食时，Heliconius melpomene幼虫能够隔离简单的环戊烯基CNglcs，这是该植物属中最常见的CNglcs。然而，据报道，西番莲属物种中存在芳香族、脂肪族和修饰的CNglc，但从未对它们进行过螺旋藻幼虫的封存测试。与其他生氰鳞翅目昆虫一样，H.美泊烯还生物合成脂族CNglc linamarin和lotaustralin，并且它们的毒性不完全依赖于螯合。虽然编码CNglc生物合成酶的基因尚未在蝴蝶中进行生物化学表征，但细胞色素P450 CYP 405 A4、CYP 405 A5、CYP 405 A6和CYP 332 A1已被假设参与H.美波美在这项研究中，我们确定了参与这些化合物生物合成的推定P450的CNglc组成和表达在蝎尾蝶的不同发育阶段如何变化。我们还确定了哪种CNglcs H.黑果番荔枝幼虫可以与西番莲隔离。通过对不同西番莲饵料下的幼虫血淋巴化学成分的分析，我们发现西番莲幼虫血淋巴中的化学成分与西番莲幼虫的血淋巴中的化学成分有关。melpomene能够螯合来自P. platyloba的prunasin，一种芳香的CNglc。它们还能够螯合涂在植物叶片上的苦杏仁苷、gynocardin、[C-13/C-14]linamarin和[C-13/C-14]lotaustralin。在幼虫血淋巴中未检测到来自蓝绿萤的CNglc tetraphyllin B-硫酸盐，表明这种修饰的CNglc不能被Heliconius螯合。虽然蛹和处女成虫含有幼虫隔离产生的二氢gynocardin，这种化合物在成年期代谢，而不是用作婚姻礼物或转移到后代。因此，我们推测，dihydrogynocardin被分解代谢，以回收氮和葡萄糖，和/或在求偶过程中产生健身信号。成熟成虫具有比任何其他发育阶段更高浓度的CNglc，这是由于亚麻苦苷和lotaustralin的从头生物合成增加。因此，所有CYP 405 A在成虫中表达，而幼虫主要表达CYP 405 A4。我们的研究结果阐明了CNglcs对Heliconius生物学及其与西番莲的共同进化的重要性。
Heliconius butterflies are highly specialized in Passiflora plants, laying eggs and feeding as larvae only on them. Interestingly, both Heliconius butterflies and Passiflora plants contain cyanogenic glucosides (CNglcs). While feeding on specific Passiflora species, Heliconius melpomene larvae are able to sequester simple cyclopentenyl CNglcs, the most common CNglcs in this plant genus. Yet, aromatic, aliphatic, and modified CNglcs have been reported in Passiflora species and they were never tested for sequestration by heliconiine larvae. As other cyanogenic lepidopterans, H. melpomene also biosynthesize the aliphatic CNglcs linamarin and lotaustralin, and their toxicity does not rely exclusively on sequestration. Although the genes encoding the enzymes in the CNglc biosynthesis have not yet been biochemically characterized in butterflies, the cytochromes P450 CYP405A4, CYP405A5, CYP405A6 and CYP332A1 have been hypothesized to be involved in this pathway in H. melpomene. In this study, we determine how the CNglc composition and expression of the putative P450s involved in the biosynthesis of these compounds vary at different developmental stages of Heliconius butterflies. We also establish which kind of CNglcs H. melpomene larvae can sequester from Passiflora. By analysing the chemical composition of the haemolymph from larvae fed with different Passiflora diets, we show that H. melpomene is able to sequestered prunasin, an aromatic CNglcs, from P. platyloba. They are also able to sequester amygdalin, gynocardin, [C-13/C-14]linamarin and [C-13/C-14]lotaustralin painted on the plant leaves. The CNglc tetraphyllin B-sulphate from P. caerulea is not detected in the larval haemolymph, suggesting that such modified CNglcs cannot be sequestered by Heliconius. Although pupae and virgin adults contain dihydrogynocardin resulting from larval sequestration, this compound was metabolized during adulthood, and not used as nuptial gift or transferred to the offspring. Thus, we speculate that dihydrogynocardin is catabolized to recycle nitrogen and glucose, and/or to produce fitness signals during courtship. Mature adults have a higher concentration of CNglcs than any other developmental stages due to increased de novo biosynthesis of linamarin and lotaustralin. Accordingly, all CYP405As are expressed in adults, whereas larvae mostly express CYP405A4. Our results shed light on the importance of CNglcs for Heliconius biology and their coevolution with Passiflora.