甘薯小象甲侵害诱导的(Z)-3-己烯基乙酯和别罗勒烯的昼夜节律性释放激活甘薯对甘薯小象甲的防御反应

doi:10.1016/j.jia.2023.02.020

Journal of Integrative Agriculture ›› 2023, Vol. 22 ›› Issue (6): 1782-1796.DOI: 10.1016/j.jia.2023.02.020

甘薯小象甲侵害诱导的(Z)-3-己烯基乙酯和别罗勒烯的昼夜节律性释放激活甘薯对甘薯小象甲的防御反应

收稿日期:2022-07-07 修回日期:2023-02-17 接受日期:2022-11-22 出版日期:2023-06-20 发布日期:2022-11-22

Diurnal emission of herbivore-induced (Z)-3-hexenyl acetate and allo-ocimene activates sweet potato defense responses to sweet potato weevils

XIAO Yang-yang^{1, 2*}, QIAN Jia-jia^{1, 2*}, HOU Xing-liang^{1, 3}, ZENG Lan-ting^{1, 3}, LIU Xu^{1, 3}, MEI Guo-guo^{1, 2}, LIAO Yin-yin^{1, 3#}

¹Guangdong 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
³Center of Economic Botany, Core Botanical Gardens, Chinese Academy of Sciences, Guangzhou 510650, P.R.China

Received:2022-07-07 Revised:2023-02-17 Accepted:2022-11-22 Online:2023-06-20 Published:2022-11-22
About author:XIAO Yang-yang, Tel: +86-20-37021938, E-mail: xiaoyangyang17 @scbg.ac.cn; #Correspondence LIAO Yin-yin, Tel: +86-20-37021938, E-mail: honey_yyliao@scbg.ac.cn * These authors contributed equally to this study.
Supported by:
This work was supported by the National Natural Science Foundation of China–Guangdong Natural Science Foundation Joint Project (U1701234).

摘要/Abstract

摘要：

甘薯小象虫（Cylas formicarius （Fab.）（Coleoptera: Brentidae））是一种以甘薯（Ipomoea batatas（L.）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 synthase（IbOS）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。

Abstract:

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.

Key words: sweetpotato , (Z)-3-hexenyl acetate , allo-ocimene , defense , signaling

XIAO Yang-yang, QIAN Jia-jia, HOU Xing-liang, ZENG Lan-ting, LIU Xu, MEI Guo-guo, LIAO Yin-yin. 甘薯小象甲侵害诱导的(Z)-3-己烯基乙酯和别罗勒烯的昼夜节律性释放激活甘薯对甘薯小象甲的防御反应[J]. Journal of Integrative Agriculture, 2023, 22(6): 1782-1796.

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

Diurnal emission of herbivore-induced (Z)-3-hexenyl acetate and allo-ocimene activates sweet potato defense responses to sweet potato weevils [J]. Journal of Integrative Agriculture, 2023, 22(6): 1782-1796.

参考文献

Braun A R, Van De Fliert E. 1999. Evaluation of the impact of sweetpotato weevil (Cylas formicarius) and of the effectiveness of Cylas sex pheromone traps at the farm level in Indonesia. International Journal of Pest Management, 45, 101–110.

Cascone P, Iodice L, Maffei M E, Bossi S, Arimura G I, Guerrieri E. 2015. Tobacco overexpressing β-ocimene induces direct and indirect responses against aphids in receiver tomato plants. Journal of Plant Physiology, 173, 28–32.

Chen F, Tholl D, D’Auria J C, Farooq A, Pichersky E, Gershenzon J. 2003. Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. The Plant Cell, 15, 481–494.

Chen H, Yue Y, Yu R, Fan Y. 2019. A Hedychium coronarium short chain alcohol dehydrogenase is a player in allo-ocimene biosynthesis. Plant Molecular Biology, 101, 297–313.

D’Auria J C, Pichersky E, Schaub A, Hansel A, Gershenzon J. 2007. Characterization of a BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. The Plant Journal, 49, 194–207.

Dudareva N, Negre F, Nagegowda D A, Orlova I. 2006. Plant volatiles: Recent advances and future perspectives. Critical Reviews in Plant Sciences, 25, 417–440.

Engelberth J, Alborn H T, Schmelz E A, Tumlinson J H. 2004. Airborne signals prime plants against insect herbivore attack. Proceedings of the National Academy of Sciences of the United States of America, 101, 1781–1785.

Fenske M P, Hazelton K D H, Hempton A K, Shim J S, Yamamoto B M, Riffell J A, Imaizumi T. 2015. Circadian clock gene LATE ELONGATED HYPOCOTYL directly regulates the timing of floral scent emission in Petunia. Proceedings of the National Academy of Sciences of the United States of America, 112, 9775–9780.

Frost C J, Mescher M C, Dervinis C, Davis J M, Carlson J E, De Moraes C M. 2008. Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytologist, 180, 722–734.

Fürstenberg-Hägg J, Zagrobelny M, Bak S. 2013. Plant defense against insect herbivores. International Journal of Molecular Sciences, 14, 10242–10297.

Hu L F, Ye M, Erb M. 2019. Integration of two herbivore-induced plant volatiles results in synergistic effects on plant defence and resistance. Plant, Cell & Environment, 42, 959–971.

Jian G T, Jia Y X, Li L, Zhou X C, Liao Y Y, Dai G Y, Zhou Y, Tang J C, Zeng L T. 2021. Elucidation of the regular emission mechanism of volatile β-ocimene with anti-insect function from tea plants (Camellia sinensis) exposed to herbivore attack. Journal of Agricultural and Food Chemistry, 69, 11204–11215.

Jing T T, Du W K, Gao T, Wu Y, Zhang N, Zhao M Y, Jin J Y, Wang J M, Schwab W, Wan X C, Song C K. 2021a. Herbivore-induced DMNT catalyzed by CYP82D47 plays an important role in the induction of JA-dependent herbivore resistance of neighboring tea plants. Plant, Cell & Environment, 44, 1178–1191.

Jing T T, Qian X N, Du W K, Gao T, Li D F, Guo D Y, He F, Yu G M, Li S P, Schwab W, Wan X, C, Sun X L, Song C K. 2021b. Herbivore-induced volatiles influence moth preference by increasing the β-ocimene emission of neighbouring tea plants. Plant, Cell & Environment, 44, 3667–3680.

Joo Y, Schuman M C, Goldberg J K, Kim S G, Yon F, Brütting C, Baldwin I T. 2018. Herbivore-induced volatile blends with both “fast” and “slow” components provide robust indirect defence in nature. Functional Ecology, 32, 136–149.

Joo Y, Schuman M C, Goldberg J K, Wissgott A, Kim S G, Baldwin I T. 2019. Herbivory elicits changes in green leaf volatile production via jasmonate signaling and the circadian clock. Plant, Cell & Environment, 42, 972–982.

Kishimoto K, Matsui K, Ozawa R, Takabayashi J. 2006. Analysis of defensive responses activated by volatile allo-ocimene treatment in Arabidopsis thaliana. Phytochemistry, 67, 1520–1529.

Laurie S, Faber M, Adebola P, Belete A. 2015. Biofortification of sweet potato for food and nutrition security in South Africa. Food Research International, 76, 962–970.

Liao Y Y, Tan H B, Jian G T, Zhou X C, Huo L Q, Jia Y X, Zeng L T, Yang Z Y. 2021. Herbivore-induced (Z)-3-hexen-1-ol is an airborne signal that promotes direct and indirect defenses in tea (Camellia sinensis) under light. Journal of Agricultural and Food Chemistry, 69, 12608–12620.

Liao Y Y, Zeng L T, Rao S F, Gu D C, Liu X, Wang Y R, Zhu H B, Hou X L, Yang Z Y. 2020. Induced biosynthesis of chlorogenic acid in sweetpotato leaves confers the resistance against sweetpotato weevil attack. Journal of Advanced Research, 24, 513–522.

Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods, 25, 402–408.

Lu S, Xu R, Jia J W, Pang J, Matsuda S P, Chen X Y. 2002. Cloning and functional characterization of a β-pinene synthase from Artemisia annua that shows a circadian pattern of expression. Plant Physiology, 130, 477–486.

Meents A K, Chen S P, Reichelt M, Lu H H, Bartram S, Yeh K W, Mithöfer A. 2019. Volatile DMNT systemically induces jasmonate-independent direct anti-herbivore defense in leaves of sweet potato (Ipomoea batatas) plants. Scientific Reports, 9, 1–13.

Piesik D, Łyszczarz A, Tabaka P, Lamparski R, Bocianowski J, Delaney K J. 2010. Volatile induction of three cereals: Influence of mechanical injury and insect herbivory on injured plants and neighbouring uninjured plants. Annals of Applied Biology, 157, 425–434.

Pokhilko A, Bou-Torrent J, Pulido P, Rodríguez-Concepción M, Ebenhöh O. 2015. Mathematical modelling of the diurnal regulation of the MEP pathway in Arabidopsis. New Phytologist, 206, 1075–1085.

Roos J, Bejai S, Mozūraitis R, Dixelius C. 2015. Susceptibility to Verticillium longisporum is linked to monoterpene production by TPS 23/27 in Arabidopsis. The Plant Journal, 81, 572–585.

Skaliter O, Kitsberg Y, Sharon E, Shklarman E, Shor E, Masci T, Yue Y L, Arien Y, Tabach Y, Shafir S, Vainstein A. 2021. Spatial patterning of scent in Petunia corolla is discriminated by bees and involves the ABCG1 transporter. The Plant Journal, 106, 1746–1758.

Takemoto H, Takabayashi J. 2015. Parasitic wasps Aphidius ervi are more attracted to a blend of host-induced plant volatiles than to the independent compounds. Journal of Chemical Ecology, 41, 801–807.

Turlings T C, Erb M. 2018. Tritrophic interactions mediated by herbivore-induced plant volatiles: Mechanisms, ecological relevance, and application potential. Annual Review of Entomology, 63, 433–452.

Wang Y, Kays S J. 2002. Sweetpotato volatile chemistry in relation to sweetpotato weevil (Cylas formicarius) behavior. Journal of the American Society for Horticultural Science, 127, 656–662.

Whitmee S, Haines A, Beyrer C, Boltz F, Capon A G, de Souza Dias B F, Ezeh A, Frumkin H, Gong P, Head P, Horton R, Mace G M, Marten R, Myers S S, Nishtar S, Osofsky S A, Pattanayak S K, Pongsiri M J, Romanelli C, Soucat A, et al. 2015. Safeguarding human health in the Anthropocene epoch: Report of The Rockefeller Foundation– Lancet Commission on planetary health. The lancet, 386, 1973–2028.

Xu Q S, Cheng L, Mei Y, Huang L L, Zhu J Y, Mi X Z, Yu Y B, Wei C L. 2019. Alternative splicing of key genes in LOX pathway involves biosynthesis of volatile fatty acid derivatives in tea plant (Camellia sinensis). Journal of Agricultural and Food Chemistry, 67, 13021–13032.

Yon F, Joo Y, Llorca L C, Rothe E, Baldwin I T, Kim S G. 2016. Silencing Nicotiana attenuata LHY and ZTL alters circadian rhythms in flowers. New Phytologist, 209, 1058–1066.

Zebelo S A, Matsui K, Ozawa R, Maffei M E. 2012. Plasma membrane potential depolarization and cytosolic calcium flux are early events involved in tomato (Solanum lycopersicon) plant-to-plant communication. Plant Science, 196, 93–100.

Zeng L T, Watanabe N, Yang Z T. 2019. Understanding the biosyntheses and stress response mechanisms of aroma compounds in tea (Camellia sinensis) to safely and effectively improve tea aroma. Critical Reviews in Food Science and Nutrition, 59, 2321–2334.

Zhang S F, Wei J N, Guo X J, Liu T X, Kang L. 2010. Functional synchronization of biological rhythms in a tritrophic system. PLoS ONE, 5, e11064.

甘薯小象甲侵害诱导的(Z)-3-己烯基乙酯和别罗勒烯的昼夜节律性释放激活甘薯对甘薯小象甲的防御反应

Diurnal emission of herbivore-induced (Z)-3-hexenyl acetate and allo-ocimene activates sweet potato defense responses to sweet potato weevils

PDF

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 0

编辑推荐

Metrics