Studies on plant-mediated interactions between root parasitic nematodes and aboveground herbivores are rapidly increasing. However, outcomes for the interacting organisms vary, and the mechanisms involved remain ambiguous. We hypothesized that the impact of root infection by the root-knot nematode Meloidogyne incognita on the performance of the aboveground caterpillar Spodoptera exigua is modulated by the nematode’s infection cycle. We challenged root-knot nematode-infected tomato plants with caterpillars when the nematode’s infection cycle was at the invasion, galling, and reproduction stages. We found that M. incognita root infection enhanced S. exigua performance during the galling stage, while it did not affect the caterpillar’s performance at the invasion and reproduction stages. Molecular and chemical analyses performed at the different stages of the nematode infection cycle revealed that M. incognita root infection systemically affected the jasmonic acid-, salicylic acid-, and abscisic acid-related responses, as well as the changes in the leaf metabolome triggered during S. exigua feeding. The M. incognita-induced leaf responses varied over the nematode’s root infection cycle. These findings suggest that specific leaf responses triggered systemically by the nematode at its different life-cycle stages underlie the differential impact of M. incognita on plant resistance against the caterpillar S. exigua.

中文翻译：

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南方根结线虫根部感染调节叶片抗草食动物防御和植物对甜菜夜蛾的抗性

关于根寄生线虫和地上食草动物之间植物介导的相互作用的研究正在迅速增加。然而，相互作用的生物体的结果各不相同，并且所涉及的机制仍然不明确。我们假设根结线虫根部感染对地上毛虫甜菜夜蛾性能的影响是由线虫的感染周期调节的。当线虫的感染周期处于入侵、磨伤和繁殖阶段时，我们用毛毛虫对根结线虫感染的番茄植株进行攻击。我们发现，南方根结线虫根部感染增强了甜菜夜蛾在虫蛀阶段的表现，而它并不影响毛虫在入侵和繁殖阶段的表现。在线虫感染周期的不同阶段进行的分子和化学分析表明，南方根结线虫根部感染系统性地影响茉莉酸、水杨酸和脱落酸相关反应，以及感染过程中引发的叶片代谢组的变化。甜菜夜蛾进食。南方根结线虫诱导的叶子反应随着线虫根部感染周期的变化而变化。这些发现表明，线虫在其不同生命周期阶段系统地触发的特定叶片反应是南方根结线虫对植物对甜菜夜蛾毛虫抗性产生不同影响的基础。