四种化学信号可以在保持植物生长发育平衡的同时非损伤性的诱导增强甜橙对亚洲柑橘木虱的抗性

doi:10.1016/j.jia.2024.11.034

摘要/Abstract

摘要：

亚洲柑橘木虱（Asian citrus psyllid，ACP）是柑橘作物的重要害虫，主要以柑橘韧皮部汁液为食，可传播柑橘黄龙病，对柑橘产业构成了严重威胁。具有植物间通讯功能的挥发性信号能够在最小程度影响植物生长的前提下，有效增强受体植物对植食性昆虫的抗性。(E)-4,8-二甲基-1,3,7-壬三烯（DMNT）、(E,E)-4,8,12-三甲基-1,3,7,11-三烯（TMTT）、(E)-β-石竹烯和二甲基二硫醚（DMDS）是番石榴与甜橙间交流的信号分子，然而对它们能否在不影响植物生长的情况下增强柑橘对ACP成虫的抗取食能力尚不明确。因此，本研究评价了化学信号DMNT、TMTT、(E)-β-石竹烯和DMDS的非损伤诱导对甜橙抗ACP取食能力，防御性植物化学物质、防御酶、功能性营养物质、光系统II的光能利用和分配、光合色素、生长和叶片气孔的影响。研究结果表明，化学信号DMNT、TMTT、(E)-β-石竹烯和DMDS的非损伤诱导可增强柑橘对ACP的取食抗性，进一步测定发现诱导后的甜橙中防御酶多酚氧化酶（PPO）的活性增强，总酚、单宁和萜类防御性植物化学物质的含量增加。其中，DMNT和DMDS在诱导抗性方面的作用比TMTT和(E)-β-石竹烯更为显著。不同暴露诱导期柑橘叶绿素荧光参数和光合色素的变化特征显示，这些化学信号能够维持柑橘光合系统的稳定性，调节其捕获、传输和分配光能的能力，显著增强柑橘的非光化学猝灭能力（Y(NPQ)）。此外，这些化学信号的非损伤诱导可以优化柑橘叶片功能营养物质的水平，主要表现为可溶性糖、脯氨酸或可溶性蛋白的上调，气孔面积和气孔开度的减小，维持叶片含水量和LMA的稳定，在增强柑橘抗ACP取食能力的同时保持其健康生长。这些结果充分证明，化学信号DMNT、TMTT、(E)-β-石竹烯和DMDS的非损伤诱导不仅可以增强柑橘对ACP的抗性，而且能够保持植物抗性与生长之间的平衡，避免对柑橘生长造成毁灭性危害，展现出与其他有害生物治理策略相结合的潜力，为实现作物的集体保护提供了新的视角。本研究为化学信号分子诱导剂的开发和农业系统中ACP的防治提供了理论支持和实践指导。

Abstract:

Asian citrus psyllid (ACP) is a significant pest of citrus crops that can transmit citrus Huanglongbing (HLB) by feeding on the phloem sap of citrus plants, which poses a significant threat to citrus production. Volatile signal chemicals with plant communication functions can effectively enhance the resistance of recipient plants to herbivorous insects with minimal impacts on plant growth. While (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), (E,E)-4,8,12-trimethyl-1,3,7,11-tridecene (TMTT), (E)-β-caryophyllene, and dimethyl disulfide (DMDS), are known as signaling molecules in guava-sweet orange communication, whether these four chemical signals can enhance the resistance of Citrus sinensis to feeding by ACP adults with no apparent costs in terms of plant growth remains unclear. Therefore, this study measured the effect of non-damaging induction by DMNT, TMTT, (E)-β-caryophyllene, and DMDS on the ability of C. sinensis to resist feeding by ACP, as well as their impacts on the defensive phytochemicals, defensive enzymes, functional nutrients, Photosystem II’s utilization and allocation of light energy, photosynthetic pigments, growth conditions, and leaf stomatal aperture in C. sinensis. The results indicate that non-damaging induction by these four chemicals can enhance the activity of the defensive enzyme polyphenol oxidase (PPO) and increase the contents of total phenols, tannins, and terpenoid defensive phytochemicals within C. sinensis, thereby enhancing the resistance of C. sinensis to ACP feeding. Specifically, DMNT and DMDS exhibit more significant effects in inducing resistance compared to TMTT and (E)-β-caryophyllene. The characteristics of chlorophyll fluorescence parameters and changes in photosynthetic pigments in C. sinensis during different post-exposure induction periods revealed these chemicals can maintain the stability of the photosynthetic system in C. sinensis and regulate its capacity to capture, transmit, and distribute light energy, which significantly enhances the non-photochemical quenching ability of C. sinensis. In addition, detailed measurements of the water content, leaf mass per unit area (LMA), functional nutrients (soluble protein, soluble sugar, and amino acids), and stomatal parameters in C. sinensis leaves further indicated that the non-destructive induction by these chemicals can optimize the levels of functional nutrients in C. sinensis, primarily manifesting as the upregulation of soluble sugars, proline, or soluble proteins, and reduction of stomatal area and aperture, which maintains a stable leaf water content and LMA, thereby enhancing resistance to ACP while sustaining the healthy growth of C. sinensis. These results fully substantiate that the non-damaging induction by the signal chemicals DMNT, TMTT, (E)-β-caryophyllene, and DMDS can enhance the resistance of C. sinensis to ACP feeding while maintaining the balance between pest resistance and growth. This balance prevents any catastrophic effects on the growth of C. sinensis, so these agents can potentially be integrated with other pest management strategies for the collective protection of crops. This study provides theoretical support and assistance for the development of signal chemical inducers for the prevention and management of ACP in agricultural systems.

Key words: volatile signals , defense priming , Asian citrus psyllid resistance , Citrus sinensis , defensive metabolites , physiology and biochemistry

Wei Wang, Chuxiao Lin, Yirong Zhang, Shiyan Liu, Jiali Liu, Xinnian Zeng. 四种化学信号可以在保持植物生长发育平衡的同时非损伤性的诱导增强甜橙对亚洲柑橘木虱的抗性[J]. Journal of Integrative Agriculture, 2025, 24(7): 2732-2748.

Wei Wang, Chuxiao Lin, Yirong Zhang, Shiyan Liu, Jiali Liu, Xinnian Zeng. Four signal chemicals can non-destructively induce enhanced resistance to Asian citrus psyllids in Citrus sinensis while maintaining balanced plant growth and development[J]. Journal of Integrative Agriculture, 2025, 24(7): 2732-2748.

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