东方粘虫的触角叶嗅小球组织

doi:10.1016/j.jia.2024.04.030

Journal of Integrative Agriculture ›› 2024, Vol. 23 ›› Issue (11): 3812-3829.DOI: 10.1016/j.jia.2024.04.030

东方粘虫的触角叶嗅小球组织

收稿日期:2023-12-04 接受日期:2024-03-20 出版日期:2024-11-20 发布日期:2024-10-10

Glomerular organization in the antennal lobe of the oriental armyworm Mythimna separata

Baiwei Ma^{1, 2, 4}, Qi Chen^{1, 2}, Xi Chu³, Yidong Zuo^{1, 2}, Jiayu Wang⁴, Yi Yang^{1, 2}, Guirong Wang^{4, 5#}, Bingzhong Ren^{1, 2#}

¹Jilin Provincial Key Laboratory of Animal Resource Conservation and Utilization, School of Life Sciences, Northeast Normal University, Changchun 130024, China
²Key Laboratory of Vegetation Ecology, Ministry of Education, Northeast Normal University, Changchun 130024, China
³Chemosensory Lab, Department of Psychology, Norwegian University of Science and Technology, Trondheim 7491, Norway
⁴State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
⁵Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Synthetic Biology Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518120, China

Received:2023-12-04 Accepted:2024-03-20 Online:2024-11-20 Published:2024-10-10
About author:Baiwei Ma, E-mail: mabaiweilmr@163.com; #Correspondence Guirong Wang, Tel: +86-10-62816947, E-mail: wangguirong@caas.cn; Bingzhong Ren, Tel: +86-431-85098200, E-mail: bzren@nenu.edu.cn
Supported by:
This work was supported by the National Natural Science Foundation of China (32130089), and the Norwegian Research Council (324379).

摘要/Abstract

摘要：

在昆虫中，触角叶嗅小球的数量和特异性往往反映了化学感觉基因表达的数量和多样性，这些基因表达与其生态位和特定的嗅觉需求有关。东方粘虫(Mythimna separata)是一种重要且常见的谷物作物害虫。鉴于其关键的行为依赖于嗅觉系统，了解该系统的演化潜力需要对其初级嗅觉中枢的解剖结构进行详细的描绘。本研究通过突触抗体免疫染色和嗅觉感觉神经元泛染，系统地鉴定了东方粘虫所有的触角叶嗅小球，并使用了方便于读者理解的命名方式对雌蛾的69个嗅小球和雄蛾的65个嗅小球进行了系统命名。我们的研究结果揭示了该物种的性别特异性嗅小球，除了MGC外，有10个雌性特异性嗅小球和3个雄性特异性嗅小球，值得注意的是雌性下唇须嗅小球比雄性的大。此外，我们还鉴定了4个触角叶神经束(ALTs)，并通过从蘑菇体冠部位进行逆行标记揭示了所有嗅小球都受到内侧触角叶神经束投射神经元的支配。东方粘虫与生态位重叠的其他蛾类昆虫嗅觉系统结构的比较支持了夜蛾科昆虫的趋同演化。这些研究结果为深入研究东方粘虫的嗅觉处理机制奠定了基础。

Abstract:

In insects, the number and specificity of antennal lobe glomeruli often reflect the number and diversity of expressed chemosensory genes, which are linked to its ecological niche and specific olfactory needs. The oriental armyworm, Mythimna separata, is an important and common lepidopteran pest of cereal crops. Given its reliance on the olfactory system for crucial behaviors, understanding the evolutionary potential of this system requires a thorough characterization of the anatomical structure of the primary olfactory center. Here, we systematically identified all antennal lobe glomeruli of M. separata based on synaptic antibody immunostaining and mass staining of the olfactory sensory neurons. A total of 69 glomeruli were identified in females and 65 in males, and an intuitive nomenclature based on glomerular positions was applied. Our findings uncovered some sex-specific glomeruli in this species. There were ten female-specific glomeruli and three male-specific glomeruli, except for the macroglomerular complex (MGC) units, with a notable observation that the female labial pit organ glomerulus was larger than its male counterpart. Additionally, we identified four antennal-lobe tracts (ALTs) and retrograde labeling from the calyx revealed that all glomeruli were innervated by the medial ALT projection neurons. The comparison of the olfactory system structures between M. separata and sympatric moths supports their evolutionary convergence in noctuid moths. These results collectively lay the foundation for future studies on olfactory processing in M. separata.

Key words: antennal lobe , glomerulus , olfactory sensory neuron , projection neuron , antennal-lobe tract , Mythimna separata

Baiwei Ma, Qi Chen, Xi Chu, Yidong Zuo, Jiayu Wang, Yi Yang, Guirong Wang, Bingzhong Ren. 东方粘虫的触角叶嗅小球组织[J]. Journal of Integrative Agriculture, 2024, 23(11): 3812-3829.

Baiwei Ma, Qi Chen, Xi Chu, Yidong Zuo, Jiayu Wang, Yi Yang, Guirong Wang, Bingzhong Ren. Glomerular organization in the antennal lobe of the oriental armyworm Mythimna separata[J]. Journal of Integrative Agriculture, 2024, 23(11): 3812-3829.

参考文献

Anton S, Homberg U. 1999. Antennal lobe structure. In: Hansson B S, ed., Insect Olfaction. Springer, Heidelberg. pp. 97–124.

Ashfaq M, Ahmad A, Cheema G M. 1999. Further studies on pest-host interaction in IPM of Mythimna separata (Walk.). South Pacific Study, 19, 23–29.

Axel R. 2005. Scents and sensibility: A molecular logic of olfactory perception (Nobel lecture). Angewandte Chemie (International Edition), 44, 6110–6127.

Beerwinkle K, Shaver T, Lingren P, Raulston J. 1996. Free-choice olfactometer bioassay system for evaluating the attractiveness of plant volatiles to adult Helicoverpa zea. The Southwestern Entomologist, 21, 395–405.

Berg B G, Galizia C G, Brandt R, Mustaparta H. 2002. Digital atlases of the antennal lobe in two species of tobacco budworm moths, the oriental Helicoverpa assulta (male) and the American Heliothis virescens (male and female). Journal of Comparative Neurology, 446, 123–134.

Cao S, Sun D, Liu Y, Yang Q, Wang G. 2023. Mutagenesis of odorant coreceptor Orco reveals the distinct role of olfaction between sexes in Spodoptera frugiperda. Journal of Integrative Agriculture, 22, 2162–2172.

Carle T, Watanabe H, Yamawaki Y, Yokohari F. 2016. Organization of the antennal lobes in the praying mantis (Tenodera aridifolia). Journal of Comparative Neurology, 525, 1685–1706.

Chen Q H, Zhu F, Tian Z, Zhang W M, Guo R, Liu W, Pan L, Du Y. 2018. Minor components play an important role in interspecific recognition of insects: A basis to pheromone based electronic monitoring tools for rice pests. Insects, 9, 192.

Chu X, Heinze S, Ian E, Berg B G. 2020a. A novel major output target for pheromone-sensitive projection neurons in male moths. Frontiers in Cellular Neuroscience, 14, 147.

Chu X, Kc P, Ian E, Kvello P, Liu Y, Wang G R, Berg B G. 2020b. Neuronal architecture of the second-order CO2 pathway in the brain of a noctuid moth. Scientific Reports, 10, 19838.

Cork A, Boo K S, Dunkelblum E, Hall D R, Jee-Rajunga K, Kehat M, Kong Jie E, Park K C, Tepgidagarn P, Xun L. 1992. Female sex pheromone of oriental tobacco budworm, Helicoverpa assulta (Guenee) (Lepidoptera: Noctuidae): Identification and field testing. Journal of Chemical Ecology, 18, 403–418.

Couto A, Alenius M, Dickson B J. 2005. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Current Biology, 15, 1535–1547.

Dong J, Jiang N, Zhao X, Tang R. 2020. Antennal lobe atlas of an emerging corn pest, Athetis dissimilis. Frontiers in Neuroanatomy, 14, 23.

Drake V A, Gatehouse A G. 1995. Insect Migration: Tracking Resources Through Space and Time. Cambridge University, Cambridge.

Dreyer D, Vitt H, Dippel S, Goetz B, el Jundi B, Kollmann M, Huetteroth W, Schachtner J. 2010. 3D standard brain of the red flour beetle Tribolium castaneum: A tool to study metamorphic development and adult plasticity. Frontiers in Systems Neuroscience, 4, 3.

Du L, Zhao X, Liang X, Gao X, Liu Y, Wang G. 2018. Identification of candidate chemosensory genes in Mythimna separata by transcriptomic analysis. BMC Genomics, 19, 518.

Fishilevich E, Vosshall L B. 2005. Genetic and functional subdivision of the Drosophila antennal lobe. Current Biology, 15, 1548–1553.

Galizia C G, Mcilwrath S L, Menzel R. 1999. A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell and Tissue Research, 295, 383–394.

Galizia C G, Rössler W. 2010. Parallel olfactory systems in insects: Anatomy and function. Annual Review of Entomology, 55, 399–420.

Gao Q, Yuan B, Chess A. 2000. Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nature Neuroscience, 3, 780–785.

Grabe V, Strutz A, Baschwitz A, Hansson B S, Sachse S. 2014. Digital in vivo 3D atlas of the antennal lobe of Drosophila melanogaster. Journal of Comparative Neurology, 523, 530–544.

Greiner B, Gadenne C, Anton S. 2004. Three-dimensional antennal lobe atlas of the male moth, Agrotis ipsilon: A tool to study structure–function correlation. Journal of Comparative Neurology, 475, 202–210.

Hansson B, Anton S, Christensen T. 1994. Structure and function of antennal lobe neurons in the male turnip moth, Agrotis segetum (Lepidoptera: Noctuidae). Journal of Comparative Physiology, 175, 547–562.

Hansson B S, Anton S. 2000. Function and morphology of the antennal lobe: New developments. Annual Review of Entomology, 45, 203–231.

Hansson B S, Christensen T A, Hildebrand J G. 1991. Functionally distinct subdivisions of the macroglomerular complex in the antennal lobe of the male sphinx moth Manduca sexta. Journal of Comparative Neurology (A: Sensory, Neural, and Behavioral Physiology), 312, 264–278.

Hartlieb E, Anderson P. 1999. Olfactory-released behaviours. In: Hansson B S, ed., Insect olfaction. Springer, Heidelberg. pp. 315–349.

Heath R R, Landolt P J, Dueben B, Lenczewski B. 1992. Identification of floral compounds of night-blooming jessamine attractive to cabbage looper moths. Environmental Entomology, 21, 854–859.

Heinze S, Reppert S M. 2012. Anatomical basis of sun compass navigation I: The general layout of the monarch butterfly brain. Journal of Comparative Neurology, 520, 1599–1628.

Hildebrand J G, Shepherd G M. 1997. Mechanisms of olfactory discrimination: Converging evidence for common principles across phyla. Annual Review of Neuroscience, 20, 595–631.

Homberg U, Christensen T A, Hildebrand J. 1989. Structure and function of the deutocerebrum in insects. Annual Review of Entomology, 34, 477–501.

Homberg U, Montague R, Hildebrand J. 1988. Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell and Tissue Research, 254, 255–281.

Hu J, Sun F. 2020. The morphology of the antennal lobe of Ambrostoma quadriimpressum (Coleoptera: Chrysomelidae). Journal of Forestry Research, 31, 526–533.

Hu J, Wang Z, Sun F. 2011. Anatomical organization of antennal-lobe glomeruli in males and females of the scarab beetle Holotrichia diomphalia (Coleoptera: Melolonthidae). Arthropod Structure & Development, 40, 420–428.

Huang T, Zhang R, Yang L, Cao S, Francis F, Wang B, Wang G. 2022. Identification and functional characterization of ApisOr23 in pea aphid Acyrthosiphon pisum. Journal of Integrative Agriculture, 21, 1414–1423.

Ian E, Berg A, Lillevoll S C, Berg B G. 2016a. Antennal-lobe tracts in the noctuid moth, Heliothis virescens: New anatomical findings. Cell and Tissue Research, 366, 23–35.

Ian E, Chu X, Berg B G. 2022. Brain investigation on sexual dimorphism in a gynandromorph moth. Insects, 13, 284.

Ian E, Zhao X C, Lande A, Berg B G. 2016b. Individual neurons confined to distinct antennal-lobe tracts in the Heliothine moth: Morphological characteristics and global projection patterns. Frontiers in Neuroanatomy, 10, 101.

Ignell R, Anton S, Hansson B S. 2001. The antennal lobe of orthoptera–anatomy and evolution. Brain Behavior and Evolution, 57, 1–17.

Immonen E V, Dacke M, Heinze S, el Jundi B. 2017. Anatomical organization of the brain of a diurnal and a nocturnal dung beetle. Journal of Comparative Neurology, 525, 1879–1908.

Jacob V, Scolari F, Delatte H, Gasperi G, Jacquin-Joly E, Malacrida A R, Duyck P F. 2017. Current source density mapping of antennal sensory selectivity reveals conserved olfactory systems between tephritids and Drosophila. Scientific Reports, 7, 15304.

Jiang N J, Tang R, Guo H, Ning C, Li J C, Wu H, Huang L Q, Wang C Z. 2020. Olfactory coding of intra- and interspecific pheromonal messages by the male Mythimna separata in North China. Insect Biochemistry and Molecular Biology, 125, 103439.

Jiang N J, Tang R, Wu H, Xu M, Ning C, Huang L Q, Wang C Z. 2019. Dissecting sex pheromone communication of Mythimna separata (Walker) in North China from receptor molecules and antennal lobes to behavior. Insect Biochemistry and Molecular Biology, 111, 103176.

Jiang X, Luo L, Zhang L, Sappington T W, Hu Y. 2011. Regulation of migration in Mythimna separata (Walker) in China: A review integrating environmental, physiological, hormonal, genetic, and molecular factors. Environmental Entomology, 40, 516–533.

Joerges J, Küttner A, Galizia C G, Menzel R. 1997. Representations of odours and odour mixtures visualized in the honeybee brain. Nature, 387, 285–288.

Kanzaki R, Arbas E A, Strausfeld N J, Hildebrand J G. 1989. Physiology and morphology of projection neurons in the antennal lobe of the male moth Manduca sexta. Journal of Comparative Physiology (A: Sensory, Neural, and Behavioral Physiology), 165, 427–453.

Kazawa T, Namiki S, Fukushima R, Terada M, Soo K, Kanzaki R. 2009. Constancy and variability of glomerular organization in the antennal lobe of the silkmoth. Cell and Tissue Research, 336, 119–136.

Kehat M, Dunkelblum E. 1990. Behavioral responses of male Heliothis armigera (Lepidoptera: Noctuidae) moths in a flight tunnel to combinations of components identified from female sex pheromone glands. Journal of Insect Behavior, 3, 75–83.

Kehat M, Gothilf S, Dunkelblum E, Greenberg S. 1980. Field evaluation of female sex pheromone components of the cotton bollworm. Heliothis armigera. Entomologia Experimentalis et Applicata, 27, 188–193.

Kent K, Harrow I, Quartararo P, Hildebrand J. 1986. An accessory olfactory pathway in Lepidoptera: The labial pit organ and its central projections in Manduca sexta and certain other sphinx moths and silk moths. Cell and Tissue Research, 245, 237–245.

Kymre J H, Berge C N, Chu X, Ian E, Berg B G. 2021a. Antennal-lobe neurons in the moth Helicoverpa armigera: Morphological features of projection neurons, local interneurons, and centrifugal neurons. Journal of Comparative Neurology, 529, 1516–1540.

Kymre J H, Chu X, Ian E, Berg B G. 2022. Organization of the parallel antennal-lobe tracts in the moth. Journal of Comparative Physiology (A: Sensory, Neural, and Behavioral Physiology), 208, 707–721.

Kymre J H, Liu X, Ian E, Berge C N, Wang G, Berg B G, Zhao X, Chu X. 2021b. Distinct protocerebral neuropils associated with attractive and aversive female-produced odorants in the male moth brain. eLife, 10, e65683.

Laissue P, Reiter C, Hiesinger P, Halter S, Fischbach K, Stocker R. 1999. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. Journal of Comparative Neurology, 405, 543–552.

Lee J K, Altner H. 1986. Primary sensory projections of the labial palp-pit organ of Pieris rapae L. (Lepidoptera: Pieridae). International Journal of Insect Morphology and Embryology, 15, 439–448.

Lee S G, Celestino C F, Stagg J, Kleineidam C, Vickers N J. 2019. Moth pheromone-selective projection neurons with cell bodies in the antennal lobe lateral cluster exhibit diverse morphological and neurophysiological characteristics. Journal of Comparative Neurology, 527, 1443–1460.

Li G B, Wang H X, Hu W X. 1964. Route of the seasonal migration of the oriental armyworm moth in eastern China as indicated by a three year result of releasing and recapturing of marked moths. Acta Phytophylacica Sinica, 3, 101–109. (in Chinese)

Liu J, He K, Luo Z X, Cai X M, Bian L, Li Z Q, Chen Z M. 2021. Anatomical comparison of antennal lobes in two sibling Ectropis moths: Emphasis on the macroglomerular complex. Frontiers in Physiology, 12, 685012.

Løfaldli. 2010. Integration of the antennal lobe glomeruli and three projection neurons in the standard brain atlas of the moth Heliothis virescens. Frontiers in Systems Neuroscience, 4, 5.

Masante-Roca I, Gadenne C, Anton S. 2005. Three-dimensional antennal lobe atlas of male and female moths, Lobesia botrana (Lepidoptera: Tortricidae) and glomerular representation of plant volatiles in females. Journal of Experimental Biology, 208, 1147–1159.

Montgomery S H, Ott S R. 2014. Brain composition in Godyris zavaleta, a diurnal butterfly, reflects an increased reliance on olfactory information. Journal of Comparative Neurology, 523, 869–891.

Montell. 2008. TRP channels: It's not the heat, it's the humidity. Current Biology, 18, R123–R126.

Namiki S, Kanzaki R. 2011. Heterogeneity in dendritic morphology of moth antennal lobe projection neurons. Journal of Comparative Neurology, 519, 3367–3386.

Nesbitt B, Beevor P, Hall D, Lester R. 1980. (Z)-9-Hexadecenal: A minor component of the female sex pheromone of Heliothis armigera (Hübner) (Lepidoptera, Noctuidae). Entomologia Experimentalis et Applicata, 27, 306–308.

Roselino A C, Hrncir M, Landim C da C, Giurfa M, Sandoz J C. 2015. Sexual dimorphism and phenotypic plasticity in the antennal lobe of a stingless bee, Melipona scutellaris. Journal of Comparative Neurology, 523, 1461–1473.

Rospars J P. 1983. Invariance and sex-specific variations of the glomerular organization in the antennal lobes of a moth, Mamestra brassicae, and a butterfly, Pieris brassicae. Journal of Comparative Neurology, 220, 80–96.

Seki Y, Dweck H K M, Rybak J, Wicher D, Sachse S, Hansson B S. 2017. Olfactory coding from the periphery to higher brain centers in the Drosophila brain. BMC Biology, 15, 56.

Shankar S, McMeniman C J. 2020. An updated antennal lobe atlas for the yellow fever mosquito Aedes aegypti. PLoS Neglected Tropical Diseases, 14, e0008729.

Shaver T, Lingren P, Raulston J, Marshall H. 1998. Plant chemicals as attractants for Helicoverpa zea (Lepidoptera: Noctuidae) and other insect species. Southwestern Entomologist, 21, 37–46.

Singh S, Joseph J. 2019. Evolutionarily conserved anatomical and physiological properties of olfactory pathway through fourth-order neurons in a species of grasshopper (Hieroglyphus banian). Journal of Comparative Physiology (A: Sensory, Neural, and Behavioral Physiology), 205, 813–838.

Skiri H T, Rø H, Berg B G, Mustaparta H. 2005. Consistent organization of glomeruli in the antennal lobes of related species of heliothine moths. Journal of Comparative Neurology, 491, 367–380.

Solari P, Corda V, Sollai G, Kreissl S, Galizia C G, Crnjar R. 2016. Morphological characterization of the antennal lobes in the Mediterranean fruit fly Ceratitis capitata. Journal of Comparative Physiology (A: Sensory, Neural, and Behavioral Physiology), 202, 131–146.

Streinzer M, Kelber C, Pfabigan S, Kleineidam C J, Spaethe J. 2013. Sexual dimorphism in the olfactory system of a solitary and a eusocial bee species. Journal of Comparative Neurology, 521, 2742–2755.

Szyszka P, Galizia C G. 2015. Olfaction in insects. In: Doty R L, ed., Handbook of Olfaction and Gustation. John Wiley & Sons, Hoboken. pp. 531–546.

Tanaka N K, Suzuki E, Dye L, Ejima A, Stopfer M. 2012. Dye fills reveal additional olfactory tracts in the protocerebrum of wild-type Drosophila. Journal of Comparative Neurology, 520, 4131–4140.

Tang R, Jiang N J, Ning C, Li G C, Huang L Q, Wang C Z. 2020. The olfactory reception of acetic acid and ionotropic receptors in the Oriental armyworm, Mythimna separata Walker. Insect Biochemistry and Molecular Biology, 118, 103312.

Todd J, Haynes K, Baker T. 1992. Antennal neurones specific for redundant pheromone components in normal and mutant Trichoplusia ni males. Physiological Entomology, 17, 183–192.

Varela N, Couton L, Gemeno C, Avilla J, Rospars J P, Anton S. 2009. Three-dimensional antennal lobe atlas of the oriental fruit moth, Cydia molesta (Busck) (Lepidoptera: Tortricidae): Comparison of male and female glomerular organization. Cell and Tissue Research, 337, 513–526.

Vickers N, Christensen T, Hildebrand J. 1998. Combinatorial odor discrimination in the brain: Attractive and antagonist odor blends are represented in distinct combinations of uniquely identifiable glomeruli. Journal of Comparative Neurology, 400, 35–56.

Wang C, Wang B, Wang G. 2021. Functional characterization of sex pheromone neurons and receptors in the armyworm, Mythimna separata (Walker). Frontiers in Neuroanatomy, 15, 673420.

Wang H L, Zhao C H, Wang C Z. 2005. Comparative study of sex pheromone composition and biosynthesis in Helicoverpa armigera, H. assulta and their hybrid. Insect Biochemistry and Molecular Biology, 35, 575–583.

Winnington A P, Napper R M, Mercer A R. 1996. Structural plasticity of identified glomeruli in the antennal lobes of the adult worker honey bee. Journal of Comparative Neurology, 365, 479–490.

Wu H, Hou C, Huang L, Yan F, Wang C. 2013. Peripheral coding of sex pheromone blends with reverse ratios in two Helicoverpa species. PLoS ONE, 8, e70078.

Xu H, Turlings T C J. 2018. Plant volatiles as mate-finding cues for insects. Trends in Plant Science, 23, 100–111.

Xu M, Dong J F, Wu H, Zhao X C, Huang L Q, Wang C Z. 2017. The inheritance of the pheromone sensory system in two Helicoverpa species: Dominance of H. armigera and possible introgression from H. assulta. Frontiers in Cellular Neuroscience, 10, 302.

Xu M, Guo H, Hou C, Wu H, Huang L Q, Wang C Z. 2016. Olfactory perception and behavioral effects of sex pheromone gland components in Helicoverpa armigera and Helicoverpa assulta. Scientific Reports, 6, 22998.

Yan X, Wang Z, Xie J, Deng C, Sun X, Hao C. 2019. Glomerular organization of the antennal lobes of the diamondback moth, Plutella xylostella L. Frontiers in Neuroanatomy, 13, 4.

Zhao X C, Chen Q Y, Guo P, Xie G Y, Tang Q B, Guo X R, Berg B G. 2016a. Glomerular identification in the antennal lobe of the male moth Helicoverpa armigera. Journal of Comparative Neurology, 524, 2993–3013.

Zhao X C, Kvello P, Løfaldli B B, Lillevoll S C, Mustaparta H, Berg B G. 2014. Representation of pheromones, interspecific signals, and plant odors in higher olfactory centers; mapping physiologically identified antennal-lobe projection neurons in the male heliothine moth. Frontiers in Systems Neuroscience, 8, 186.

Zhao X C, Ma B W, Berg B G, Xie G Y, Tang Q B, Guo X R. 2016b. A global-wide search for sexual dimorphism of glomeruli in the antennal lobe of female and male Helicoverpa armigera. Scientific Reports, 6, 35204.

Zhao X C, Tang Q B, Berg B G, Liu Y, Wang Y R, Yan F M, Wang G R. 2013. Fine structure and primary sensory projections of sensilla located in the labial-palp pit organ of Helicoverpa armigera (Insecta). Cell and Tissue Research, 353, 399–408.

Zhang Y, Liu H, Cao S, Li B, Liu Y, Wang G. 2024. Identification of transient receptor potential channel genes and functional characterization of TRPA1 in Spodoptera frugiperda. Journal of Integrative Agriculture, 23, 1994–2005.

Zhang Y, Yang B, Yu J, Pang B, Wang G. 2022. Expression profiles and functional prediction of ionotropic receptors in Asian corn borer, Ostrinia furnacalis (Lepidoptera: Crambidae). Journal of Integrative Agriculture, 21, 474–485.

东方粘虫的触角叶嗅小球组织

Glomerular organization in the antennal lobe of the oriental armyworm Mythimna separata

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