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Journal of Integrative Agriculture  2023, Vol. 22 Issue (6): 1782-1796    DOI: 10.1016/j.jia.2023.02.020
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Diurnal emission of herbivore-induced (Z)-3-hexenyl acetate and allo-ocimene activates sweet potato defense responses to sweet potato weevils

XIAO Yang-yang1, 2*, QIAN Jia-jia1, 2*, HOU Xing-liang1, 3, ZENG Lan-ting1, 3, LIU Xu1, 3, MEI Guo-guo1, 2, LIAO Yin-yin1, 3#

1 Guangdong Provincial Key Laboratory of Digital Botanical Garden and Popular Science/Key Laboratory of South China Agricultural Plant Molecular Analysis and Genetic Improvement, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, P.R.China

2 College of Life Sciences, University of Chinese Academy of Sciences, Beijing 100049, P.R.China

3 Center of Economic Botany, Core Botanical Gardens, Chinese Academy of Sciences, Guangzhou 510650, P.R.China

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甘薯小象虫(Cylas formicarius Fab.)(Coleoptera: Brentidae))是一种以甘薯(Ipomoea batatasL.Lam.Solanales: Convolvulaceae))为食的害虫,每年造成巨大的经济损失。然而,目前还没有找到安全有效的方法来保护甘薯免受甘薯小象甲的侵害。昆虫侵害诱导的植物挥发物(HIPVs)能激活多种防御的生物活性,但它们在甘薯中的形成和防御机制仍未清晰。为了明确甘薯中合成的防御性HIPVs,我们监测了虫侵害过程中甘薯挥发物的释放动态。通过稳定同位素示踪以及转录和代谢水平的分析,揭示了候选HIPVs的生物合成途径和调控因子。最后,对候选HIPVs的抗虫活性和防御机制进行了评估。本研究表明,(Z)-3-己烯基乙酯(z3HAC)和别罗勒烯由甘薯小象甲诱导合成,具有明显的昼夜节律。本文还首次报道了Ipomoea batatas ocimene synthaseIbOS)是别罗勒烯合成路径的基因。昆虫侵害造成的损伤促进了底物 (Z)-3-己烯醇的积累,并上调了IbOS的表达,从而分别导致z3HAC和别罗勒烯含量的增加。z3HAC和别罗勒烯气体分子能激活临近植株对甘薯小象甲的防御能力。本研究提供了关于甘薯防御性挥发物的形成、调控和信号转导机制的信息,对于建立有效的甘薯小象甲防治措施具有重要意义。


The sweet potato weevil (Cylas formicarius (Fab.) (Coleoptera: Brentidae)) is a pest that feeds on sweet potato (Ipomoea batatas (L.) Lam. (Solanales: Convolvulaceae)), causing substantial economic losses annually.  However, no safe and effective methods have been found to protect sweet potato from this pest.  Herbivore-induced plant volatiles (HIPVs) promote various defensive bioactivities, but their formation and the defense mechanisms in sweet potato have not been investigated.  To identify the defensive HIPVs in sweet potato, the release dynamics of volatiles was monitored.  The biosynthetic pathways and regulatory factors of the candidate HIPVs were revealed via stable isotope tracing and analyses at the transcriptional and metabolic levels.  Finally, the anti-insect activities and the defense mechanisms of the gaseous candidates were evaluated.  The production of (Z)-3-hexenyl acetate (z3HAC) and allo-ocimene was induced by sweet potato weevil feeding, with a distinct circadian rhythm.  Ipomoea batatas ocimene synthase (IbOS) is first reported here as a key gene in allo-ocimene synthesis.  Insect-induced wounding promoted the production of the substrate, (Z)-3-hexenol, and upregulated the expression of IbOS, which resulted in higher contents of z3HAC and allo-ocimene, respectively.  Gaseous z3HAC and allo-ocimene primed nearby plants to defend themselves against sweet potato weevils.  These results provide important data regarding the formation, regulation, and signal transduction mechanisms of defensive volatiles in sweet potato, with potential implications for improving sweet potato weevil management strategies.

Keywords:  sweetpotato        (Z)-3-hexenyl acetate        allo-ocimene        defense        signaling  
Received: 07 July 2022   Online: 17 February 2023   Accepted: 22 November 2022
Fund: This work was supported by the National Natural Science Foundation of China–Guangdong Natural Science Foundation Joint Project (U1701234).
About author:  XIAO Yang-yang, Tel: +86-20-37021938, E-mail: xiaoyangyang17; #Correspondence LIAO Yin-yin, Tel: +86-20-37021938, E-mail: * These authors contributed equally to this study.

Cite this article: 

XIAO Yang-yang, QIAN Jia-jia, HOU Xing-liang, ZENG Lan-ting, LIU Xu, MEI Guo-guo, LIAO Yin-yin. 2023.

Diurnal emission of herbivore-induced (Z)-3-hexenyl acetate and allo-ocimene activates sweet potato defense responses to sweet potato weevils . Journal of Integrative Agriculture, 22(6): 1782-1796.

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