Within‐plant variation in chemical defence of Erysimum cheiranthoides does not explain Plutella xylostella feeding preference

Plants invest a substantial fraction of their resources into defence
against herbivores, with the highest levels of defence often allocated
only to the most valuable tissues. Plants in the genus Erysimum
(Brassicaceae) have evolved the ability to produce novel cardenolides, in
addition to ancestrally conserved glucosinolates. While these plants
co‐express both defences, differences in tissue‐specific expression might
represent an effective cost‐saving strategy. Larvae of the
glucosinolate‐resistant diamondback moth Plutella xylostella occasionally
feed on Erysimum cheiranthoides but tend to avoid younger leaves. Here, we
predict that caterpillar feeding preference is shaped by variations in
cardenolide levels. Thus, we quantified within‐plant variations in defence
and nutritional traits of vegetative or early reproductive plants and
performed feeding assays to evaluate the relative importance of
cardenolides. In accordance with optimal defence theory (ODT), the
youngest leaves contained the most nutrients and had highest levels of
cardenolides, glucosinolates and trichomes, with more extreme within‐plant
differences found in reproductive plants. Caterpillars consistently
avoided the well‐defended youngest leaves, both on whole plants and
detached leaf discs. Surprisingly, neither experimental addition (external
application) nor removal (CRISPR‐Cas9 knockout) of cardenolides
significantly affected caterpillar feeding preference. Physical and
chemical defences, including cardenolides, co‐vary within E.
cheiranthoides to maximize defence of youngest leaves. While P. xylostella
clearly responds to some of these traits, the prominent cardenolide
defence appears to lack potency against this specialist herbivore.
Nonetheless, the careful regulation and re‐mobilization of cardenolides to
younger leaves during plant development suggests an important role in
plant functioning.

植物会将大量资源投入到抵御植食性动物的防御过程中，且通常仅将最高水平的防御策略分配给最具价值的组织。隶属于十字花科（Brassicaceae）糖芥属（Erysimum）的植物，除了保留祖先遗留的硫代葡萄糖苷（glucosinolates）之外，还演化出了合成新型强心甾内酯（cardenolides）的能力。尽管这类植物会共表达这两种防御机制，但组织特异性的表达差异或许是一种高效的资源节约策略。对硫代葡萄糖苷具有抗性的小菜蛾（Plutella xylostella）幼虫偶尔会取食桂竹香糖芥（Erysimum cheiranthoides），但通常会避开幼嫩叶片。本研究推测，幼虫的取食偏好受到强心甾内酯含量差异的调控。为此，我们对营养生长期及早期生殖生长期的植株，开展了防御相关性状与营养性状的植株内差异定量分析，并通过取食实验评估了强心甾内酯的相对重要性。根据最优防御理论（optimal defence theory, ODT），最幼嫩的叶片不仅营养物质含量最高，同时强心甾内酯、硫代葡萄糖苷与表皮毛（trichomes）的含量也最高，且生殖生长期植株的植株内性状差异更为显著。无论是完整植株还是离体叶盘实验中，幼虫均会持续避开防御能力较强的幼嫩叶片。令人意外的是，无论是通过外源施加（实验性添加）还是CRISPR-Cas9基因敲除（实验性移除）来调控强心甾内酯的含量，均未显著影响幼虫的取食偏好。在桂竹香糖芥中，包括强心甾内酯在内的物理与化学防御性状之间存在协同变化，以最大化对幼嫩叶片的防御效果。尽管小菜蛾显然会对部分防御性状产生响应，但占主导地位的强心甾内酯防御机制似乎对这种专食性植食动物并无显著效力。尽管如此，在植物生长发育过程中，对强心甾内酯的精准调控与重新转运至幼嫩叶片的过程，仍提示其在植物生理功能中发挥着重要作用。