Yao Yang, Lin Huan-Tai, Chen Yao-Hui, Chen Li-Lan, Zhang Hui-Li, Fu Hua-Ying, Gao San-Ji, Wang Ran, Feng Hong-Lin, Wang Jin-da
National Engineering Research Center of Sugarcane, Fujian Agriculture and Forestry University, Fuzhou, China.
Institute of Plant Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China.
Plant Cell Environ. 2025 Jan;48(1):406-420. doi: 10.1111/pce.15121. Epub 2024 Sep 12.
Plants have developed various resistance mechanisms against herbivorous insects through prolonged coevolution. Plant defence responses can be triggered by specific compounds present in insect saliva. Apyrase, a known enzyme that catalyzes the hydrolysis of adenosine triphosphate (ATP) and adenosine diphosphate (ADP) into adenosine monophosphate (AMP) and inorganic phosphorus, has recently been identified in some herbivorous insects. However, whether insect salivary apyrase induces or inhibits plant responses remains poorly understood. In this study, we identified an apyrase-like protein in the salivary proteome of the fall armyworm, Spodoptera frugiperda, named Sfapyrase. Sfapyrase was primarily expressed in the salivary gland and secreted into plants during insect feeding. Transient expression of Sfapyrase in tobacco and maize enhanced plant resistance and resulted in decreased insect feeding. Knockdown of Sfapyrase through RNA interference led to increased growth and feeding of S. frugiperda. Furthermore, we showed that Sfapyrase activates the jasmonic acid signalling pathway and promotes the synthesis of secondary metabolites, especially benzoxazinoids, thereby enhancing resistance to S. frugiperda. In summary, our findings demonstrated that Sfapyrase acts as a salivary elicitor, inducing maize jasmonic acid defence responses and the production of insect-resistant benzoxazinoids. This study provides valuable insights into plant-insect interactions and offers potential targets for developing innovative insect pest management strategies.
通过长期的共同进化，植物已经形成了多种抵御食草昆虫的抗性机制。植物的防御反应可由昆虫唾液中存在的特定化合物触发。腺苷三磷酸双磷酸酶是一种已知的酶，可催化三磷酸腺苷（ATP）和二磷酸腺苷（ADP）水解为单磷酸腺苷（AMP）和无机磷，最近在一些食草昆虫中被发现。然而，昆虫唾液中的腺苷三磷酸双磷酸酶是诱导还是抑制植物反应仍知之甚少。在本研究中，我们在草地贪夜蛾（Spodoptera frugiperda）的唾液蛋白质组中鉴定出一种腺苷三磷酸双磷酸酶样蛋白，命名为Sfapyrase。Sfapyrase主要在唾液腺中表达，并在昆虫取食期间分泌到植物中。Sfapyrase在烟草和玉米中的瞬时表达增强了植物抗性，并导致昆虫取食减少。通过RNA干扰敲低Sfapyrase导致草地贪夜蛾的生长和取食增加。此外，我们发现Sfapyrase激活茉莉酸信号通路并促进次生代谢产物尤其是苯并恶嗪类的合成，从而增强对草地贪夜蛾的抗性。总之，我们的研究结果表明Sfapyrase作为一种唾液激发子，诱导玉米茉莉酸防御反应并产生抗虫苯并恶嗪类。本研究为植物 - 昆虫相互作用提供了有价值的见解，并为开发创新的害虫管理策略提供了潜在靶点。
