Ministry of Agriculture and Rural Affairs Key Laboratory of Sustainable Crop Production in the Middle Reaches of the Yangtze River (Co-construction by Ministry and Province), Hubei Engineering Technology Center for Pest Forewarning and Management, College of Agriculture, Yangtze University, Jingzhou, 434025, China.
Plant J. 2022 Nov;112(3):694-708. doi: 10.1111/tpj.15973. Epub 2022 Sep 21.
Rapid callose accumulation has been shown to mediate defense in certain plant-virus interactions. Exposure to the green leaf volatile (Z)-3-hexenol (Z-3-HOL) can prime tomato (Solanum lycopersicum) for an enhanced defense against subsequent infection by whitefly-transmitted Tomato yellow leaf curl virus (TYLCV). However, the molecular mechanisms affecting Z-3-HOL-induced resistance are poorly understood. Here, we explored the mechanisms underlying Z-3-HOL-induced resistance against whitefly-transmitted TYLCV infection and the role of callose accumulation during this process. Tomato plants pre-treated with Z-3-HOL displayed callose priming upon whitefly infestation. The callose inhibitor 2-deoxy-d-glucose abolished Z-3-HOL-induced resistance, confirming the importance of callose in this induced resistance. We also found that Z-3-HOL pre-treatment enhanced salicylic acid levels and activated sugar signaling in tomato upon whitefly infestation, which increased the expression of the cell wall invertase gene Lin6 to trigger augmented callose deposition against TYLCV infection resulting from whitefly transmission. Using virus-induced gene silencing, we demonstrated the Lin6 expression is relevant for sugar accumulation mediated callose priming in restricting whitefly-transmitted TYLCV infection in plants that have been pre-treated with Z-3-HOL. Moreover, Lin6 induced the expression of the callose synthase gene Cals12, which is also required for Z-3-HOL-induced resistance of tomato against whitefly-transmitted TYLCV infection. These findings highlight the importance of sugar signaling in the priming of callose as a defense mechanism in Z-3-HOL-induced resistance of tomato against whitefly-transmitted TYLCV infection. The results will also increase our understanding of defense priming can be useful for the biological control of viral diseases.
已证实快速胼胝质积累可介导某些植物-病毒互作中的防御反应。暴露于绿叶挥发物(Z)-3-己烯醇（Z-3-HOL）可使番茄（Solanum lycopersicum）对随后由粉虱传播的番茄黄曲叶病毒（TYLCV）感染产生增强的防御反应。然而，影响 Z-3-HOL 诱导抗性的分子机制尚不清楚。在此，我们探讨了 Z-3-HOL 诱导抗性抵御粉虱传播的 TYLCV 感染的机制以及在此过程中胼胝质积累的作用。用 Z-3-HOL 预处理的番茄植株在粉虱侵袭时显示出胼胝质的初级积累。用葡聚糖抑制剂 2-脱氧-D-葡萄糖处理会消除 Z-3-HOL 诱导的抗性，证实了胼胝质在此诱导抗性中的重要性。我们还发现，Z-3-HOL 预处理可增强番茄在粉虱侵袭时的水杨酸水平和糖信号转导，从而增加细胞壁转化酶基因 Lin6 的表达，触发 TYLCV 感染导致的胼胝质沉积增加，从而限制了由粉虱传播的 TYLCV 感染。通过病毒诱导的基因沉默，我们证明了 Lin6 的表达与糖积累介导的胼胝质初级积累相关，这有助于用 Z-3-HOL 预处理的植物限制由粉虱传播的 TYLCV 感染。此外，Lin6 诱导了胼胝质合成酶基因 Cals12 的表达，这也是番茄对 Z-3-HOL 诱导的、由粉虱传播的 TYLCV 感染抗性所必需的。这些发现强调了糖信号在 Z-3-HOL 诱导的番茄抵抗粉虱传播的 TYLCV 感染的防御反应中胼胝质初级积累的重要性。这些结果还将增加我们对防御初级反应的理解，这对病毒病的生物防治可能有用。
