Table_2_The Active Jasmonate JA-Ile Regulates a Specific Subset of Plant Jasmonate-Mediated Resistance to Herbivores in Nature.CSV

The jasmonate hormones are essential regulators of plant defense against herbivores and include several dozen derivatives of the oxylipin jasmonic acid (JA). Among these, the conjugate jasmonoyl isoleucine (JA-Ile) has been shown to interact directly with the jasmonate co-receptor complex to regulate responses to jasmonate signaling. However, functional studies indicate that some aspects of jasmonate-mediated defense are not regulated by JA-Ile. Thus, it is not clear whether JA-Ile is best characterized as the master jasmonate regulator of defense, or if it regulates more specific aspects. We investigated possible functions of JA-Ile in anti-herbivore resistance of the wild tobacco Nicotiana attenuata, a model system for plant-herbivore interactions. We first analyzed the soluble and volatile secondary metabolomes of irJAR4xirJAR6, asLOX3, and WT plants, as well as an RNAi line targeting the jasmonate co-receptor CORONATINE INSENSITIVE 1 (irCOI1), following a standardized herbivory treatment. irJAR4xirJAR6 were the most similar to WT plants, having a ca. 60% overlap in differentially regulated metabolites with either asLOX3 or irCOI1. In contrast, while at least 25 volatiles differed between irCOI1 or asLOX3 and WT plants, there were few or no differences in herbivore-induced volatile emission between irJAR4xirJAR6 and WT plants, in glasshouse- or field-collected samples. We then measured the susceptibility of jasmonate-deficient vs. JA-Ile-deficient plants in nature, in comparison to wild-type (WT) controls, and found that JA-Ile-deficient plants (irJAR4xirJAR6) are much better defended even than a mildly jasmonate-deficient line (asLOX3). The differences among lines could be attributed to differences in damage from specific herbivores, which appeared to prefer either one or the other jasmonate-deficient phenotype. We further investigated the elicitation of one herbivore-induced volatile known to be jasmonate-regulated and to mediate resistance to herbivores: (E)-α-bergamotene. We found that JA was a more potent elicitor of (E)-α-bergamotene emission than was JA-Ile, and when treated with JA, irJAR4xirJAR6 plants emitted 20- to 40-fold as much (E)-α-bergamotene than WT. We conclude that JA-Ile regulates specific aspects of herbivore resistance in N. attenuata. This specificity may allow plants flexibility in their responses to herbivores and in managing trade-offs between resistance, vs. growth and reproduction, over the course of ontogeny.

茉莉素类激素是植物抵御草食动物的关键调控因子，其包含数十种氧脂类茉莉酸（JA）衍生物。其中，结合态分子茉莉酰异亮氨酸（JA-Ile）已被证实可直接与茉莉素共受体复合物结合，从而调控茉莉素信号通路相关应答。但功能研究表明，茉莉素介导的防御反应中，部分过程并不受JA-Ile调控。因此，目前尚不明确JA-Ile是否可被定义为调控防御反应的核心茉莉素调控因子，抑或仅参与调控特定的生理过程。
本研究以植物-草食动物互作的模式系统——野生烟草渐狭叶烟草（Nicotiana attenuata）为研究对象，探究了JA-Ile在其抗草食动物抗性中的潜在功能。我们首先对经过标准化草食动物处理后的irJAR4xirJAR6、asLOX3、野生型（WT）植株，以及靶向茉莉素共受体冠菌素不敏感1（CORONATINE INSENSITIVE 1）的RNA干扰株系（irCOI1）的可溶性与挥发性次生代谢组进行了分析。结果显示，irJAR4xirJAR6与WT植株的相似性最高，其差异调控代谢物与asLOX3或irCOI1的重叠比例约为60%。与之形成对比的是，尽管irCOI1或asLOX3与WT植株间至少存在25种挥发性物质的差异，但无论是温室还是田间采集的样本中，irJAR4xirJAR6与WT植株在草食动物诱导的挥发性物质释放方面几乎无显著差异。
随后，我们在自然环境中对比了茉莉素缺陷型与JA-Ile缺陷型植株相较于野生型对照的感虫性，结果发现JA-Ile缺陷型植株（irJAR4xirJAR6）的防御能力甚至强于轻度茉莉素缺陷型株系asLOX3。不同株系间的防御差异可归因于特定草食动物造成的损伤程度差异——这些草食动物似乎更偏好某一种茉莉素缺陷型表型。我们进一步探究了一种已知受茉莉素调控并介导抗虫性的草食动物诱导挥发性物质：(E)-α-香柠檬烯。研究发现，相较于JA-Ile，JA对(E)-α-香柠檬烯释放的诱导活性更强；且经JA处理后，irJAR4xirJAR6植株释放的(E)-α-香柠檬烯量是WT植株的20至40倍。
综上，我们认为JA-Ile仅在渐狭叶烟草的抗草食动物抗性中调控特定的生理过程。这种特异性可能使植物在应对草食动物时具备应答灵活性，并能在个体发育过程中平衡抗性与生长、繁殖之间的权衡关系。