引起雌性东方粘虫成虫趋避行为转变的草地贪夜蛾幼虫虫害诱导玉米挥发物的鉴定

doi:10.1016/j.jia.2024.05.029

Journal of Integrative Agriculture ›› 2025, Vol. 24 ›› Issue (2): 655-667.DOI: 10.1016/j.jia.2024.05.029

引起雌性东方粘虫成虫趋避行为转变的草地贪夜蛾幼虫虫害诱导玉米挥发物的鉴定

收稿日期:2024-02-05 接受日期:2024-04-19 出版日期:2025-02-20 发布日期:2025-01-22

Characterization of core maize volatiles induced by Spodoptera frugiperda that alter the mating-mediated approach–avoidance behaviors of Mythimna separata

Denghai Yang^{1, 2*}, Hengzhe Fan^{1, 2*}, Ruyi Hu^{1, 2}, Yong Huang¹, Chengwang Sheng¹, Haiqun Cao¹, Bin Yang^2#, Xingchuan Jiang^{1, 2#}

¹Anhui Province Key Laboratory of Crop Integrated Pest Management/Key Laboratory of Biology and Sustainable Management of Plant Diseases and Pests of Anhui Higher Education Institutes, College of Plant Protection, Anhui Agricultural University, Hefei 230036, China
²State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China

Received:2024-02-05 Accepted:2024-04-19 Online:2025-02-20 Published:2025-01-22
About author:Denghai Yang, E-mail: ydhc2814@163.com; Hengzhe Fan, E-mail: f04hz14@163.com; #Correspondence Bin Yang, E-mail: yangbin@caas.cn; Xingchuan Jiang, E-mail: jxc678@sina.cn * These authors contributed equally to this study.
Supported by:
This work was supported by the National Key Research and Development Program of China (2021YFD1400700), the Natural Science Foundation of Anhui Province, China (2308085MC89), and the Agricultural Science and Technology Innovation Program of Chinese Academy of Agricultural Sciences (ASTIP).

摘要/Abstract

摘要：

草地贪夜蛾（Spodoptera frugiperda）是一种对玉米具有毁灭性危害的入侵害虫，通过资源竞争等机制显著的影响本地物种和群落。然而，草地贪夜蛾与本地害虫之间的互作关系并不清楚。在本研究中，我们明确了不同交配状态下东方粘虫雌成虫对草地贪夜蛾幼虫为害的玉米植株表现出不同的行为选择：草地贪夜蛾幼虫为害的玉米植株驱避未交配的雌性东方粘虫成虫，但是吸引交配后的雌性东方粘虫成虫。为了进一步解明这种行为差异的嗅觉机制，我们利用气相色谱-质谱联用技术(GC-MS)分析并鉴定到草地贪夜蛾幼虫为害的玉米植株特异性释放了七种挥发物组分，分别是反式-2-己烯醇、芳樟醇、反式-β-法尼烯、顺式-3-乙酸己烯酯、β-石竹烯、反式-α-佛手柑烯和乙酸异戊酯。进一步对不同交配状态的雌性东方粘虫成虫进行了电生理和行为测定，结果表明，反式-β-法尼烯是驱避未交配雌性东方粘虫成虫的核心化合物，反式-2-己烯醛是引诱已交配雌性东方粘虫成虫产卵的核心化合物。该研究结果有助于深入了解外来入侵物种与本地害虫之间的互作机制，为基于害虫嗅觉系统研发害虫行为调控剂提供理论基础。

Abstract:

The fall armyworm (Spodoptera frugiperda) is an invasive species and a destructive pest of maize, which significantly impacts native species and communities via complex mechanisms like competition for resources. However, the interaction between S. frugiperda and local pests remains unclear. In this study, we determined that Oriental armyworm (Mythimna separata) females with different mating status displayed different approach-avoidance behaviors towards maize which was damaged by S. frugiperda larvae. The virgin M. separata females were repelled, while the mated females were attracted by the S. frugiperda-damaged maize. To further understand the olfactory mechanism of this phenomenon, seven volatiles induced by S. frugiperda in maize were characterized by gas chromatography and mass spectrometry (GC-MS), including trans-2-hexenal, linalool, trans-β-farnesene, cis-3-hexenyl acetate, β-caryophyllene, trans-α-bergamotene, and isopentyl acetate. Additionally, electrophysiological and behavioral assays of the seven compounds were performed using both virgin and mated females of M. separata. We determined that virgin and mated females displayed different responses to the HIPV compounds. Trans-β-farnesene was the core compound for repelling virgin females, and trans-2-hexenal was the key attractant for oviposition in mated female M. separata individuals. These findings help our comprehension of the relationships between maize pests and offer new possibilities for controlling them by olfactory-based strategies.

Key words: chemical ecology , mating behavior , attractants , repellents , HIPVs , plant volatiles

Denghai Yang, Hengzhe Fan, Ruyi Hu, Yong Huang, Chengwang Sheng, Haiqun Cao, Bin Yang, Xingchuan Jiang. 引起雌性东方粘虫成虫趋避行为转变的草地贪夜蛾幼虫虫害诱导玉米挥发物的鉴定[J]. Journal of Integrative Agriculture, 2025, 24(2): 655-667.

Denghai Yang, Hengzhe Fan, Ruyi Hu, Yong Huang, Chengwang Sheng, Haiqun Cao, Bin Yang, Xingchuan Jiang. Characterization of core maize volatiles induced by Spodoptera frugiperda that alter the mating-mediated approach–avoidance behaviors of Mythimna separata[J]. Journal of Integrative Agriculture, 2025, 24(2): 655-667.

参考文献

Aartsma Y, Bianchi F J J A, van der Werf W, Poelman E H, Dicke M. 2017. Herbivore-induced plant volatiles and tritrophic interactions across spatial scales. New Phytologist, 216, 1054–1063.

Bernasconi M L, Turlings T C J, Ambrosetti L, Bassetti P, Dorn S. 1998. Herbivore‐induced emissions of maize volatiles repel the corn leaf aphid, Rhopalosiphum maidis. Entomologia Experimentalis et Applicata, 87, 133–142.

Boettner G H, Elkinton J S, Boettner C J. 2000. Effects of a biological control introduction on three nontarget native species of saturniid moths. Conservation Biology, 14, 1798–1806.

Bruce T J A, Pickett J A. 2011. Perception of plant volatile blends by herbivorous insects-finding the right mix. Phytochemistry, 72, 1605–1611.

Bukovinszky T, Gols R, Posthumus M A, Vet L E M, Van Lenteren J C. 2005. Variation in plant volatiles and attraction of the parasitoid Diadegma semiclausum (Hellen). Journal of Chemical Ecology, 31, 461–480.

Carde R T, Minks A K. 1995. Control of moth pests by mating disruption: Successes and constraints. Annual Review of Entomology, 40, 559–585.

Clavijo Mccormick A, Gershenzon J, Unsicker S B. 2014. Little peaks with big effects: Establishing the role of minor plant volatiles in plant–insect interactions. Plant, Cell & Environment, 37, 1836–1844.

Copping L G, Duke S O. 2007. Natural products that have been used commercially as crop protection agents. Pest Management Science, 63, 524–554.

De Lange E S, Laplanche D, Guo H, Xu W, Vlimant M, Erb M, Ton J, Turlings T C J. 2020. Spodoptera frugiperda caterpillars suppress herbivore-induced volatile emissions in maize. Journal of Chemical Ecology, 46, 344–360.

De Moraes C M, Mescher M C, Tumlinson J H. 2001. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature, 410, 577–580.

Degen T, Dillmann C, Marion-Poll F, Turlings T C J. 2004. High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiology, 135, 1928–1938.

Dicke M, Van Loon J J, Soler R. 2009. Chemical complexity of volatiles from plants induced by multiple attack. Nature Chemical Biology, 5, 317–324.

Duan Y, Gong Z J, Wu R H, Miao J, Jiang Y L, Li T, Wu X B, Wu Y Q. 2017. Transcriptome analysis of molecular mechanisms responsible for light-stress response in Mythimna separata (Walker). Scientific Reports, 7, 45188.

Dudareva N, Pichersky E, Gershenzon J. 2004. Biochemistry of plant volatiles. Plant Physiology, 135, 1893–1902.

Early R, González-Moreno P, Murphy S T, Day R. 2018. Forecasting the global extent of invasion of the cereal pest Spodoptera frugiperda, the fall armyworm. NeoBiota, 40, 25–50.

Edwards L J, Siddall J B, Dunham L L, Uden P, Kislow C J. 1973. Trans-β-farnesene, alarm pheromone of the green peach aphid, Myzus persicae (Sulzer). Nature, 241, 126–127.

Fatouros N E, Dicke M, Mumm R, Meiners T, Hilker M. 2008. Foraging behavior of egg parasitoids exploiting chemical information. Behavioral Ecology, 19, 677–689.

Goergen G, Kumar P L, Sankung S B, Togola A, Tamò M. 2016. First report of outbreaks of the fall armyworm Spodoptera frugiperda (JE Smith)(Lepidoptera, Noctuidae), a new alien invasive pest in West and Central Africa. PLoS ONE, 11, e0165632.

Gouinguené S P, Turlings T C J. 2002. The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiology, 129, 1296–1307.

Gregg P C, Del Socorro A P, Landolt P J. 2018. Advances in attract-and-kill for agricultural pests: Beyond pheromones. Annual Review of Entomology, 63, 453–470.

Guo J F, Qi J F, He K L, Wu J Q, Bai S X, Zhang T T, Zhao J R, Wang Z Y. 2019. The Asian corn borer Ostrinia furnacalis feeding increases the direct and indirect defence of mid-whorl stage commercial maize in the field. Plant Biotechnology Journal, 17, 88–102.

Halitschke R, Stenberg J A, Kessler D, Kessler A, Baldwin I T. 2008. Shared signals-‘alarm calls’ from plants increase apparency to herbivores and their enemies in nature. Ecology Letters, 11, 24–34.

Hare J D. 2011. Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annual Review of Entomology, 56, 161–180.

He J, Fandino R A, Halitschke R, Luck K, Köllner T G, Murdock M H, Ray R, Gase K, Knaden M, Baldwin I T. 2019. An unbiased approach elucidates variation in (S)-(+)-linalool, a context-specific mediator of a tri-trophic interaction in wild tobacco. Proceedings of the National Academy of Sciences of the United States of America, 116, 14651–14660.

He P, Li Z Q, Zhang Y F, Chen L, Wang J, Xu L, Zhang Y N, He M. 2017. Identification of odorant-binding and chemosensory protein genes and the ligand affinity of two of the encoded proteins suggest a complex olfactory perception system in Periplaneta americana. Insect Molecular Biology, 26, 687–701.

Heath R R, Manukian A. 1994. An automated system for use in collecting volatile chemicals released from plants. Journal of Chemical Ecology, 20, 593–608.

Holopainen J K. 2004. Multiple functions of inducible plant volatiles. Trends in Plant Science, 9, 529–533.

Hu X Y, Su S L, Liu Q S, Jiao Y Y, Peng Y F, Li Y H, Turlings T C J. 2020. Caterpillar-induced rice volatiles provide enemy-free space for the offspring of the brown planthopper. Elife, 9, e55421.

Huang C H, Yan F M, Byers J A, Wang R J, Xu C R. 2009. Volatiles induced by the larvae of the Asian corn borer (Ostrinia furnacalis) in maize plants affect behavior of conspecific larvae and female adults. Insect Science, 16, 311–320.

Jenkins M A. 2003. Impact of the balsam woolly adelgid (Adelges piceae Ratz.) on an Abies fraseri (Pursh) Poir. dominated stand near the summit of Mount LeConte, Tennessee. Castanea, 68, 109–118.

Jensen A B, Palmer K A, Boomsma J J, Pedersen B V. 2005. Varying degrees of Apis mellifera ligustica introgression in protected populations of the black honeybee, Apis mellifera mellifera, in northwest Europe. Molecular Ecology, 14, 93–106.

Jia H R, Guo J L, Wu Q L, Hu C X, Li X K, Zhou X Y, Wu K M. 2021. Migration of invasive Spodoptera frugiperda (Lepidoptera: Noctuidae) across the Bohai Sea in northern China. Journal of Integrative Agriculture, 20, 685–693.

Jiao Y Y, Hu X Y, Peng Y F, Wu K M, Romeis J, Li Y H. 2018. Bt rice plants may protect neighbouring non-Bt rice plants against the striped stem borer, Chilo suppressalis. Proceedings of the Royal Society (B: Biological Sciences), 285, 20181283.

Kenis M, Auger-Rozenberg M A, Roques A, Timms L, Péré C, Cock M J W, Settele J, Augustin S, Lopez-Vaamonde C. 2009. Ecological effects of invasive alien insects. Biological Invasions, 11, 21–45.

Kessler A, Baldwin I T. 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science, 291, 2141–2144.

Kessler A, Baldwin I T. 2002. Plant responses to insect herbivory: The emerging molecular analysis. Annual Review of Plant Biology, 53, 299–328.

Kong W N, Wang Y, Guo Y F, Chai X H, Li J, Ma R Y. 2020. Behavioral effects of different attractants on adult male and female oriental fruit moths, Grapholita molesta. Pest Management Science, 76, 3225–3235.

Li H J, Ren L, Xie M X, Gao Y, He M Y, Hassan B, Lu Y Y, Cheng D F. 2020. Egg-surface bacteria are indirectly associated with oviposition aversion in bactrocera dorsalis. Current Biology, 30, 4432–4440. e4434.

Liu Q S, Hu X Y, Su S L, Ning Y S, Peng Y F, Ye G Y, Lou Y G, Turlings T C J, Li Y H. 2021. Cooperative herbivory between two important pests of rice. Nature Communications, 12, 6772.

Lou Y G, Hua X Y, Turlings T C J, Cheng J A, Chen X X, Ye G Y. 2006. Differences in induced volatile emissions among rice varieties result in differential attraction and parasitism of Nilaparvata lugens eggs by the parasitoid Anagrus nilaparvatae in the field. Journal of Chemical Ecology, 32, 2375–2387.

Martins C B, Zarbin P H. 2013. Volatile organic compounds of conspecific-damaged Eucalyptus benthamii influence responses of mated females of Thaumastocoris peregrinus. Journal of Chemical Ecology, 39, 602–611.

Montezano D G, Sosa-Gómez D, Specht A, Roque-Specht V F, Sousa-Silva J C, Paula-Moraes S D, Peterson J A, Hunt T. 2018. Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. African Entomology, 26, 286–300.

Nagoshi R N, Meagher R L. 2008. Review of fall armyworm (Lepidoptera: Noctuidae) genetic complexity and migration. Florida Entomologist, 91, 546–554.

Nissinen A, Ibrahim M, Kainulainen P, Tiilikkala K, Holopainen J K. 2005. Influence of carrot psyllid (Trioza apicalis) feeding or exogenous limonene or methyl jasmonate treatment on composition of carrot (Daucus carota) leaf essential oil and headspace volatiles. Journal of Agricultural and Food Chemistry, 53, 8631–8638.

Reitz S R, Trumble J T. 2002. Competitive displacement among insects and arachnids. Annual Review of Entomology, 47, 435–465.

Robert C A M, Erb M, Duployer M, Zwahlen C, Doyen G R, Turlings T C J. 2012. Herbivore-induced plant volatiles mediate host selection by a root herbivore. New Phytologist, 194, 1061–1069.

Scutareanu P, Bruin J, Posthumus M A, Drukker B. 2003. Constitutive and herbivore-induced volatiles in pear, alder and hawthorn trees. Chemoecology, 13, 63–74.

Shiojiri K, Takabayashi J, Yano S, Takafuji A. 2002. Oviposition preferences of herbivores are affected by tritrophic interaction webs. Ecology Letters, 5, 186–192.

Signoretti A G, Peñaflor M F, Bento J M. 2012. Fall Armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), female moths respond to herbivore-induced corn volatiles. Neotropical Entomology, 41, 22–26.

Snyder W E, Evans E W. 2006. Ecological effects of invasive arthropod generalist predators. Annual Review of Ecology, Evolution, and Systematics, 37, 95–122.

Soler R, Harvey J A, Rouchet R, Schaper S V, Bezemer T M. 2010. Impacts of belowground herbivory on oviposition decisions in two congeneric butterfly species. Entomologia Experimentalis et Applicata, 136, 191–198.

Song Y F, Yang X M, Zhang H W, Zhang D D, He W, Wyckhuys K A G, Wu K M. 2021. Interference competition and predation between invasive and native herbivores in maize. Journal of Pest Science, 94, 1053–1063.

Sun X L, Wang G C, Gao Y, Zhang X Z, Xin Z J, Chen Z M. 2014. Volatiles emitted from tea plants infested by Ectropis obliqua larvae are attractive to conspecific moths. Journal of Chemical Ecology, 40, 1080–1089.

Sun X X, Hu C X, Jia H R, Wu Q L, Shen X J, Zhao S Y, Jiang Y Y, Wu K M. 2021. Case study on the first immigration of fall armyworm, Spodoptera frugiperda invading into China. Journal of Integrative Agriculture, 20, 664–672.

Takabayashi J, Dicke M. 1996. Plant-carnivore mutualism through herbivore-induced carnivore attractants. Trends in Plant Science, 1, 109–113.

Tamiru A, Bruce T J A, Woodcock C M, Caulfield J C, Midega C A O, Ogol C K P O, Mayon P, Birkett M A, Pickett J A, Khan Z R. 2011. Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. Ecology Letters, 14, 1075–1083.

Todd E L, Poole R W. 1980. Keys and illustrations for the armyworm moths of the noctuid genus Spodoptera Guenée from the Western Hemisphere. Annals of the Entomological Society of America, 73, 722–738.

Turlings T C J, Bernasconi M, Bertossa R, Bigler F, Caloz G, Dorn S. 1998. The induction of volatile emissions in maize by three herbivore species with different feeding habits: Possible consequences for their natural enemies. Biological Control, 11, 122–129.

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

Vet L E M, Dicke M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology, 37, 141–172.

Wang X Y, Liu Q S, Meissle M, Peng Y F, Wu K M, Romeis J, Li Y H. 2018. Bt rice could provide ecological resistance against nontarget planthoppers. Plant Biotechnology Journal, 16, 1748–1755.

Witzgall P, Kirsch P, Cork A. 2010. Sex pheromones and their impact on pest management. Journal of Chemical Ecology, 36, 80–100.

Wu H, Li R T, Dong J F, Jiang N J, Huang L Q, Wang C Z. 2019. An odorant receptor and glomerulus responding to farnesene in Helicoverpa assulta (Lepidoptera: Noctuidae). Insect Biochemistry and Molecular Biology, 115, 103106.

Yan H, Zeng J, Zhong G. 2015. The push–pull strategy for citrus psyllid control. Pest Management Science, 71, 893–896.

Yan Z G, Wang C Z. 2006. Similar attractiveness of maize volatiles induced by Helicoverpa armigera and Pseudaletia separata to the generalist parasitoid Campoletis chlorideae. Entomologia Experimentalis et Applicata, 118, 87–96.

Yao C C, Du L X, Liu Q S, Hu X Y, Ye W F, Turlings T C J, Li Y H. 2023. Stemborer-induced rice plant volatiles boost direct and indirect resistance in neighboring plants. New Phytologist, 237, 2375–2387.

Yu H, Zhang Y J, Wyckhuys K A, Wu K M, Gao X W, Guo Y Y. 2010. Electrophysiological and behavioral responses of Microplitis mediator (Hymenoptera: Braconidae) to caterpillar-induced volatiles from cotton. Environmental Entomology, 39, 600–609.

Zhao J, Hoffmann A, Jiang Y P, Xiao L B, Tan Y G, Zhou C Y, Bai L X. 2022. Competitive interactions of a new invader (Spodoptera frugiperda) and indigenous species (Ostrinia furnacalis) on maize in China. Journal of Pest Science, 95, 159–168.

引起雌性东方粘虫成虫趋避行为转变的草地贪夜蛾幼虫虫害诱导玉米挥发物的鉴定

Characterization of core maize volatiles induced by Spodoptera frugiperda that alter the mating-mediated approach–avoidance behaviors of Mythimna separata

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