Evolution of pyrrolizidine alkaloid biosynthesis in Apocynaceae: revisiting the defence de-escalation hypothesis

Plants produce specialized metabolites for their defence. However, specialist herbivores (食草动物) adapt to these compounds and use them for their own benefit. Plants attacked predominantly by specialists may be under selection to reduce or eliminate production of co-opted chemicals: the defence de-escalation hypothesis. We studied the evolution of pyrrolizidine alkaloids (PAs; 吡咯啶生物碱) in Apocynaceae (夹竹桃科), larval host (幼虫宿主) plants for PA-adapted butterflies (Danainae, milkweed and clearwing butterflies), to test if the evolutionary pattern is consistent with de-escalation. We used the first PA biosynthesis specific enzyme (homospermidine synthase, HSS 类精脒合酶) as tool for reconstructing PA evolution. We found hss orthologues in diverse Apocynaceae species, not all of them known to produce PAs. The phylogenetic analysis showed a monophyletic origin of the putative hss sequences early in the evolution of one Apocynaceae lineage (the APSA clade). We found an hss pseudogene in Asclepias syriaca, a species known to produce cardiac glycosides (强心苷) but no PAs, and four losses of an HSS amino acid motif. APSA clade species are significantly more likely to be Danainae larval host plants than expected if all Apocynaceae species were equally likely to be exploited. Our findings are consistent with PA de-escalation as an adaptive response to specialist attack.

植物会合成一些特异的代谢物以用于防御反应。然而，一些食草动物已经适应了这些化合物，并且能够妥善利用这些植物化合物作用于自身。植物受到这些食草动物的侵噬可能处于选择作用下，进而减少或消除这些化合物的合成，这个过程也叫做防御降级理论（the defence de-escalation hypothesis）。作者研究了夹竹桃科中的吡咯啶生物碱PA的演化，夹竹桃植物是某些适应PA蝴蝶的幼虫宿主植物，通过这个研究测试夹竹桃植物PA的演化模式是否与de-escalation一致。作者利用PA生物合成特异性酶类精脒合酶HSS重建PA演化。作者发现在大多数的夹竹桃科物种中均存在hss基因的同源基因，但并不是所有的这些物种均能够产生PA的。进化分析显示hss基因是单系起源，在夹竹桃科APSA类群早期演化过程中产生。作者在Asclepias syriaca中鉴定到了一个hss假基因，该物种能够合成强心苷但并不能合成PA，并且发现一个HSS氨基酸基序的四次丢失事件。APSA类物种相比于其它的夹竹桃科物种更有可能作为斑蝶的幼虫寄主植物。本文的发现表明吡咯啶生物碱的de-escalation作为夹竹桃APSA类植物响应食草动物啃食的适应性反应。

通讯：Tatyana Livshultz (http://drexel.edu/coas/faculty-research/faculty-directory/Livshultz/)

个人简介：1995年，美国芝加哥大学，学士；2003年，康奈尔大学，博士。

doi: 10.1111/nph.15061