Department of Biology, University of Louisville, 40292, Louisville, KY, USA.
BIO5 Institute, University of Arizona, 85721, Tucson, AZ, USA.
J Chem Ecol. 2022 Apr;48(4):441-454. doi: 10.1007/s10886-022-01359-1. Epub 2022 Apr 8.
A striking feature of plant ecology is the ability of plants to detect and respond to environmental cues such as herbivore-induced plant volatiles (HIPVs) by priming or directly activating defenses against future herbivores. However, whether seeds also respond to compounds that are common constituents of HIPV blends and initiate future plant resistance is unknown. Considering that seeds depend on other environmental cues to determine basic survival traits such as germination timing, we predicted that seeds exposed to synthetic constituents of HIPV blends would generate well-defended plants. We investigated the effect of seed exposure to common volatiles on growth, reproduction, and resistance characteristics in the model plants Arabidopsis thaliana and Medicago truncatula using herbivores from two feeding guilds. After seed scarification and vernalization, we treated seeds with one of seven different plant-derived volatile compounds for 24 h. Seeds were then germinated and the resulting plants were assayed for growth, herbivore resistance, and expression of inducible defense genes. Of all the synthetic volatiles tested, indole specifically reduced both beet armyworm growth on A. thaliana and pea aphid fecundity on M. truncatula. The induction of defense genes was not affected by seed exposure to indole in either plant species, indicating that activation of direct resistance rather than inducible resistance is the mechanism by which seed priming operates. Moreover, neither plant species showed any negative effect of seed exposure to any synthetic volatile on vegetative and reproductive growth. Rather, M. truncatula plants derived from seeds exposed to (Z)-3-hexanol and (Z)-3-hexenyl acetate grew larger compared to controls. Our results indicate that seeds are sensitive to specific volatiles in ways that enhance resistance profiles with no apparent costs in terms of growth. Seed priming by HIPVs may represent a novel ecological mechanism of plant-to-plant interactions, with broad potential applications in agriculture and seed conservation.
植物生态学的一个显著特征是，植物能够检测和响应环境线索，例如草食性诱导的植物挥发物（HIPVs），通过启动或直接激活针对未来草食动物的防御。然而，种子是否也会对 HIPV 混合物的常见成分做出反应，并引发未来的植物抗性尚不清楚。考虑到种子依赖于其他环境线索来确定基本的生存特征，例如发芽时间，我们预测暴露于 HIPV 混合物合成成分的种子会产生具有良好防御能力的植物。我们使用来自两个取食群的草食动物，研究了种子暴露于 HIPV 混合物常见挥发物对模式植物拟南芥和紫花苜蓿生长、繁殖和抗性特征的影响。在种子表皮刮擦和春化后，我们用七种不同的植物衍生挥发性化合物之一处理种子 24 小时。然后，种子发芽，对所得植物进行生长、草食动物抗性和诱导防御基因表达的测定。在所测试的所有合成挥发物中，吲哚特异性地降低了甜菜夜蛾在拟南芥上的生长和豌豆蚜在紫花苜蓿上的繁殖力。在这两个植物物种中，诱导防御基因的表达都不受种子暴露于吲哚的影响，这表明种子启动的作用机制是直接抗性的激活，而不是诱导抗性的激活。此外，两种植物物种都没有表现出种子暴露于任何合成挥发物对营养生长和生殖生长的任何负面影响。相反，与对照相比，暴露于（Z）-3-己醇和（Z）-3-己烯基乙酸酯的种子衍生的紫花苜蓿植物生长更大。我们的结果表明，种子对特定挥发物敏感，以增强抗性特征，而在生长方面没有明显的成本。HIPVs 的种子启动可能代表植物-植物相互作用的一种新的生态机制，在农业和种子保护中有广泛的潜在应用。
