绿盲蝽感觉神经元膜蛋白1a（SNMP1a）在性信息素识别中的功能研究

doi:10.1016/j.jia.2024.03.043

Journal of Integrative Agriculture ›› 2024, Vol. 23 ›› Issue (12): 4120-4135.DOI: 10.1016/j.jia.2024.03.043

所属专题：昆虫分子生物与功能基因Insect molecular biology

绿盲蝽感觉神经元膜蛋白1a（SNMP1a）在性信息素识别中的功能研究

收稿日期:2023-12-15 接受日期:2024-01-17 出版日期:2024-12-20 发布日期:2024-11-15

Functional characterization of sensory neuron membrane protein 1a involved in sex pheromone detection of Apolygus lucorum (Hemiptera: Miridae)

Yan Li^{1, 2}, Xingkui An¹, Shuang Shan^{1, 3}, Xiaoqian Pang^{1, 4}, Xiaohe Liu¹, Yang Sun², Adel Khashaveh^1#, Yongjun Zhang^1#

¹State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
²Anhui Provincial Key Laboratory of Molecular Enzymology and Mechanism of Major Diseases, College of Life Sciences, Anhui Normal University, Wuhu 241000, China
³State Key Laboratory of Resource Insects, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100193, China
⁴School of Resource and Environment, Henan Institute of Science and Technology, Xinxiang 453003, China

Received:2023-12-15 Accepted:2024-01-17 Online:2024-12-20 Published:2024-11-15
About author:Yan Li, E-mail: 1950198243@qq.com, #Correspondence Adel Khashaveh, E-mail: akhashaveh@caas.cn; Yongjun Zhang, Tel: +86-10-62815929, E-mail: yjzhang@ippcaas.cn
Supported by:
This work was supported by the National Natural Science Foundation of China (32150410366, 31972338, and 32372639), the earmarked fund for China Agriculture Research System (CARS-02-26), the National Key Research and Development Program of China (2021YFD1400700), and the Special Grant of China Postdoctoral Science Foundation (2022T150712).

摘要/Abstract

摘要：

绿盲蝽Apollygus lucorum（半翅目：盲蝽科）是一种杂食性害虫，危害多种寄主植物。由于它的快速繁殖，目前绿盲蝽的防治仍具有挑战性，因此了解其性信息素的传播是必需的。性信息素的识别由多种化学感觉相关蛋白介导，对求偶和交配行为至关重要。其中，感觉神经元膜蛋白（SNMP），一种CD36相关蛋白，被认为在检测性信息素方面发挥着至关重要的作用。在本研究中，通过对绿盲蝽转录组和基因组数据分析以及系统发育进化进行研究，共鉴定出四个具有完整开放阅读框的假定SNMP基因（AlucSNMP1a, AlucSNMP1b, AlucSNMP2a, 和AlucSNMP2b）。表达谱分析显示，AlucSNMP转录本在多种组织中普遍存在，只有AlucSNMP1a在雄性触角中偏向性表达，这表明其在雄性化学感受中可能发挥作用。利用非洲爪蟾卵母细胞表达系统结合双电极电压钳记录进行功能分析表明，与单独表达性信息受体（PRs）和共受体（Orco）相比，AlucSNMP1a与特异性信息素受体和共受体的共表达显著增强了对性信息素的电生理反应。此外，研究结果表明，AlucSNMP1a的存在不仅影响了对性信息素的反应，还影响了诱导信号的动力学反应（激活和失活）。相反，AlucSNMP1b与AlucPR/Orco复合物的共表达对两种性信息素化合物诱导的电流反应没有影响。对20个物种的SNMP1基因的选择压力的研究表明，这些基因具有很强的正向选择压力，这意味着在各种昆虫中具有潜在的功能保守性。这些发现强调了AlucSNMP1a在性信息素反应中的关键作用。

Abstract:

The mirid bug Apolygus lucorum (Hemiptera: Miridae) is a polyphagous pest that affects a wide range of host plants. Its control remains challenging mainly due to its rapid reproduction, necessitating an understanding of sex pheromone communication. The recognition of sex pheromones is vital for courtship and mating behaviors, and is mediated by various chemosensory-associated proteins. Among these, sensory neuron membrane protein (SNMP), a CD36-related protein, is suggested to play crucial roles in detecting sex pheromones. In this study, we employed transcriptomic and genomic data from A. lucorum and phylogenetic approaches, and identified four putative SNMP genes (AlucSNMP1a, AlucSNMP1b, AlucSNMP2a, and AlucSNMP2b) with full open reading frames. Expression analysis revealed the ubiquitous presence of AlucSNMP transcripts in multiple tissues, with only AlucSNMP1a exhibiting male-biased expression in the antennae, suggesting its potential role in male chemosensation. Functional analysis using the Xenopus oocyte expression system, coupled with two-electrode voltage clamp recording, demonstrated that the co-expression of AlucSNMP1a with specific pheromone receptors (PRs) and the Odorant receptor co-receptor (Orco) significantly enhanced electrophysiological responses to sex pheromones compared to the co-expression of PRs and Orco alone. Moreover, the results indicated that the presence of AlucSNMP1a not only affected the responsiveness to sex pheromones but also influenced the kinetics (activation and inactivation) of the induced signals. In contrast, the co-expression of AlucSNMP1b with AlucPR/Orco complexes had no impact on the inward currents induced by two pheromone compounds. An examination of the selective pressures on SNMP1 genes across 20 species indicated strong purifying selection, implying potential functional conservation in various insects. These findings highlight the crucial role of AlucSNMP1a in the response to sex pheromones.

Key words: mirid bug , pheromone perception , sensory neuron membrane proteins , expression profile , receptor interaction , evolution

Yan Li, Xingkui An, Shuang Shan, Xiaoqian Pang, Xiaohe Liu, Yang Sun, Adel Khashaveh, Yongjun Zhang. 绿盲蝽感觉神经元膜蛋白1a（SNMP1a）在性信息素识别中的功能研究[J]. Journal of Integrative Agriculture, 2024, 23(12): 4120-4135.

Yan Li, Xingkui An, Shuang Shan, Xiaoqian Pang, Xiaohe Liu, Yang Sun, Adel Khashaveh, Yongjun Zhang. Functional characterization of sensory neuron membrane protein 1a involved in sex pheromone detection of Apolygus lucorum (Hemiptera: Miridae)[J]. Journal of Integrative Agriculture, 2024, 23(12): 4120-4135.

参考文献

An X K, Khashaveh A, Liu D F, Xiao Y, Wang Q, Wang S N, Geng T, Gu S H, Zhang Y J. 2020. Functional characterization of one sex pheromone receptor (AlucOR4) in Apolygus lucorum (Meyer-Dür). Journal of Insect Physiology, 120, 103986.

An X K, Sun L, Liu H W, Liu D F, Ding Y X, Li L M, Zhang Y J, Guo Y Y. 2016. Identification and expression analysis of an olfactory receptor gene family in green plant bug Apolygus lucorum (Meyer-Dür). Scientific Reports, 6, 37870.

Andersson M N, Corcoran J A, Zhang D D, Hillbur Y, Newcomb R D, Löfstedt C. 2016. A sex pheromone receptor in the hessian fly Mayetiola destructor (Diptera, Cecidomyiidae). Frontiers in Cellular Neuroscience, 10, 212.

Ando T, Yamamoto M. 2020. Semiochemicals containing lepidopteran sex pheromones: Wonderland for a natural product chemist. Journal of Pesticide Science, 45, 191–205.

Benton R, Vannice K S, Vosshall L B. 2007. An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature, 450, 289–293.

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.

Capella-Gutierrez S, Silla-Martinez J M, Gabaldon T. 2009. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics, 25, 1972–1973.

Cassau S, Krieger J. 2021. The role of SNMPs in insect olfaction. Cell and Tissue Research, 383, 21–33.

Cassau S, Krieger J. 2023. Evidence for a role of SNMP2 and antennal support cells in sensillum lymph clearance processes of moth pheromone-responsive sensilla. Insect Biochemistry and Molecular Biology, 164, 104046.

Cassau S, Sander D, Karcher T, Laue M, Hause G, Breer H, Krieger J. 2022. The sensilla-specific expression and subcellular localization of SNMP1 and SNMP2 reveal novel insights into their roles in the antenna of the desert locust Schistocerca gregaria. Insects, 13, 579.

Chang H T, Liu Y, Yang T, Pelosi P, Dong S L, Wang G R. 2015. Pheromone binding proteins enhance the sensitivity of olfactory receptors to sex pheromones in Chilo suppressalis. Scientific Reports, 5, 13093.

Chen C G, Chen H, Zhang Y, Thomas H R, Frank M H, He Y H, Xia R. 2020. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 13, 1194–1202.

Edgar R C. 2004. MUSCLE: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5, 113.

Fernandez M P, Kravitz E A. 2013. Aggression and courtship in Drosophila: Pheromonal communication and sex recognition. Journal of Comparative Physiology (A: Neuroethology Sensory Neural and Behavioral Physiology), 199, 1065–1076.

Fleischer J, Krieger J. 2021. Molecular mechanisms of pheromone detection. In: Blomquist G J, Vogt R G, eds., Insect Pheromone Biochemistry and Molecular Biology. 2nd ed. Academic Press, London. pp. 355–413.

Forstner M, Gohl T, Gondesen I, Raming K, Breer H, Krieger J. 2008. Differential expression of SNMP-1 and SNMP-2 proteins in pheromone-sensitive hairs of moths. Chemical Senses, 33, 291–299.

Galizia C G. 2021. Insect olfaction. In: Fritzsch B ed., The Senses: A Comprehensive Reference. 2nd ed. Elsevier, Oxford. pp. 423–452.

Gasteiger E, Hoogland C, Gattiker A, Duvaud S E, Wilkins M R, Appel R D, Bairoch A. 2005. Protein identification and analysis tools on the ExPASy server. In: Walker J M, ed., The Proteomics Protocols Handbook. Humana Press, New Jersey. pp. 571–607.

Gomez-Diaz C, Bargeton B, Abuin L, Bukar N, Reina J H, Bartoi T, Graf M, Ong H, Ulbrich M H, Masson J F, Benton R. 2016. A CD36 ectodomain mediates insect pheromone detection via a putative tunnelling mechanism. Nature Communications, 7, 11866.

Große-Wilde E, Gohl T, Bouché E, Breer H, Krieger J. 2007. Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromonal compounds. European Journal of Neuroscience, 25, 2364–2373.

Guo H, Mo B T, Li G C, Li Z L, Huang L Q, Sun Y L, Dong J F, Smith D P, Wang C Z. 2022. Sex pheromone communication in an insect parasitoid, Campoletis chlorideae Uchida. Proceedings of the National Academy of Sciences of the United States of America, 119, e2215442119.

Ha T S, Smith D P. 2022. Recent insights into insect olfactory receptors and odorant-binding proteins. Insects, 13, 926.

Hou Z Q, Liu J J, Li H P, Ma L, Luo X, Xu P, Chen K P, Qu S X. 2022. Characteristic and expression of the SNMP gene family in the storage mite, Tyrophagus putrescentiae (Astigmata: Acaridae). International Journal of Acarology, 48, 295–299.

Hu B, Jin J P, Guo A Y, Zhang H, Luo J C, Gao G. 2015. GSDS 2.0: An upgraded gene feature visualization server. Bioinformatics, 31, 1296–1297.

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.

Ji P, Liu J T, Gu S H, Zhu X Q, Zhang Y J, Guo Y Y. 2013. Expression and binding specificity analysis of odorant binding protein AlucOBP7 from Apolygus lucorum (Hemiptera: Miridae). Acta Entomologica Sinica, 56, 575–583.

Jin X, Ha T S, Smith D P. 2008. SNMP is a signaling component required for pheromone sensitivity in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 105, 10996–11001.

Josephs E B, Lee Y W, Stinchcombe J R, Wright S I. 2015. Association mapping reveals the role of purifying selection in the maintenance of genomic variation in gene expression. Proceedings of the National Academy of Sciences of the United States of America, 112, 15390–15395.

Kannan K, Galizia C, Nouvian M. 2022. Olfactory strategies in the defensive behaviour of insects. Insects, 13, 470.

Karlson P, Luscher M. 1959. Pheromones: A new term for a class of biologically active substances. Nature, 183, 55–56.

Katoh K, Standley D M. 2013. MAFFT Multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.

Knight A L, Stelinski L L, Hebert V, Gut L, Light D, Brunner J. 2012. Evaluation of novel semiochemical dispensers simultaneously releasing pear ester and sex pheromone for mating disruption of codling moth (Lepidoptera: Tortricidae). Journal of Applied Entomology, 136, 79–86.

Leal W S. 2013. Odorant reception in insects: Roles of receptors, binding proteins, and degrading enzymes. Annual Review of Entomology, 58, 373–391.

Letunic I, Bork P. 2021. Interactive tree of life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucleic Acids Research, 49, W293-W296.

Li Z B, Zhang Y Y, An X K, Wang Q, Khashaveh A, Gu S H, Liu S, Zhang Y J. 2020. Identification of leg chemosensory genes and sensilla in the Apolygus lucorum. Frontiers in Physiology, 11, 276.

Li Z Z, Ni J D, Huang J, Montell C. 2014. Requirement for Drosophila SNMP1 for rapid activation and termination of pheromone-induced activity. PLoS Genetics, 10, e1004600.

Liu N Y, Zhang T, Ye Z F, Li F, Dong S L. 2015. Identification and characterization of candidate chemosensory gene families from Spodoptera exigua developmental transcriptomes. International Journal of Biological Sciences, 11, 1036.

Liu S, Chang H T, Liu W, Cui W C, Liu Y, Wang Y L, Ren B Z, Wang G R. 2020. Essential role for SNMP1 in detection of sex pheromones in Helicoverpa armigera. Insect Biochemistry and Molecular Biology, 127, 103485.

Liu Y, Liu H W, Wang H C, Huang T Y, Liu B, Yang B, Yin L J, Li B, Zhang Y, Zhang S, Jiang F, Zhang X X, Ren Y W, Wang B, Wang S, Lu Y H, Wu K M, Fan W, Wang G R. 2021. Apolygus lucorum genome provides insights into omnivorousness and mesophyll feeding. Molecular Ecology Resources, 21, 287–300.

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

Lu Y H, Wu K M, Jiang Y Y, Guo Y Y, Desneux N. 2012. Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature, 487, 362–365.

Lu Y H, Wyckhuys K A G, Wu K M. 2024. Pest status, bio-ecology, and area-wide management of mirids in East Asia. Annual Review of Entomology, 69, 393–413.

Minh B Q, Schmidt H A, Chernomor O, Schrempf D, Woodhams M D, Von Haeseler A, Lanfear R. 2020. IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution, 37, 1530–1534.

Mnguni S, Peter Heshula L U N. 2023. A review of chemically based communication in Miridae, with a focus on two sympatric species of Eccritotarsus. Journal of Entomological Science, 58, 277–293.

Nichols Z, Vogt R G. 2008. The SNMP/CD36 gene family in Diptera, Hymenoptera and Coleoptera: Drosophila melanogaster, D. pseudoobscura, Anopheles gambiae, Aedes aegypti, Apis mellifera, and Tribolium castaneum. Insect Biochemistry and Molecular Biology, 38, 398–415.

Omasits U, Ahrens C H, Müller S, Wollscheid B. 2014. Protter: Interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics, 30, 884–886.

Pan H S, Liu B, Lu Y H, Wyckhuys K A G. 2015. Seasonal alterations in host range and fidelity in the polyphagous mirid bug, Apolygus lucorum (Heteroptera: Miridae). PLoS ONE, 10, e0117153.

Pan H S, Lu Y H, Wyckhuys K A G, Wu K M. 2013. Preference of a polyphagous mirid bug, Apolygus lucorum (Meyer-Dür) for flowering host plants. PLoS ONE, 8, e68980.

Pan Y, Zhang X X, Wang Z, Qi L Z, Zhang X S, Zhang J H, Xi J H. 2022. Identification and analysis of chemosensory genes encoding odorant-binding proteins, chemosensory proteins and sensory neuron membrane proteins in the antennae of Lissorhoptrus oryzophilus. Bulletin of Entomological Research, 112, 287–297.

Pregitzer P, Greschista M, Breer H, Krieger J. 2014. The sensory neurone membrane protein SNMP1 contributes to the sensitivity of a pheromone detection system. Insect Molecular Biology, 23, 733–742.

Pregitzer P, Jiang X, Große-Wilde E, Breer H, Krieger J, Fleischer J. 2017. In search for pheromone receptors: Certain members of the odorant receptor family in the desert locust Schistocerca gregaria (Orthoptera: Acrididae) are co-expressed with SNMP1. International Journal of Biological Sciences, 13, 911–922.

Pregitzer P, Jiang X, Lemke R S, Krieger J, Fleischer J, Breer H. 2019. A subset of odorant receptors from the desert locust Schistocerca gregaria is co-expressed with the sensory neuron membrane protein 1. Insects, 10, 350.

Rogers M E, Sun M, Lerner M R, Vogt R G. 1997. Snmp-1, a novel membrane protein of olfactory neurons of the silk moth antheraea polyphemus with homology to the CD36 family of membrane proteins. Journal of Biological Chemistry, 272, 14792–14799.

Ronderos D S, Lin C C, Potter C J, Smith D P. 2014. Farnesol-detecting olfactory neurons in Drosophila. The Journal of Neuroscience, 34, 3959–3968.

Shan S, Wang S N, Song X, Khashaveh A, Lu Z Y, Dhiloo K H, Li R J, Gao X W, Zhang Y J. 2020. Molecular characterization and expression of sensory neuron membrane proteins in the parasitoid Microplitis mediator (Hymenoptera: Braconidae). Insect Science, 27, 425–439.

Shiota Y, Sakurai T, Ando N, Haupt S S, Mitsuno H, Daimon T, Kanzaki R. 2021. Pheromone binding protein is involved in temporal olfactory resolution in the silkmoth. iScience, 24, 103334.

Slater G S C, Birney E. 2005. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics, 6, 31.

Sparks J T. 2004. The intricate molecular landscape of insect chemosensation: The sensory neuron membrane protein gene family. Ph D thesis, University of South Carolina, United States, South Carolina. p. 102.

Stelinski L L, Gut L J, Miller J R. 2013. An attempt to increase efficacy of moth mating disruption by co-releasing pheromones with kairomones and to understand possible underlying mechanisms of this technique. Environmental Entomology, 42, 158–166.

Sun M J, Liu Y, Walker W B, Liu C C, Lin K J, Gu S H, Zhang Y J, Zhou J J, Wang G R. 2013. Identification and characterization of pheromone receptors and interplay between receptors and pheromone binding proteins in the diamondback moth, Plutella xyllostella. PLoS ONE, 8, e62098.

Tamura K, Stecher G, Kumar S. 2021. MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38, 3022–3027.

Teng D, Liu D, Khashaveh A, Sun P, Geng T, Zhang D, Zhang Y. 2022. Biosynthesis of artemisinic acid in engineered Saccharomyces cerevisiae and its attractiveness to the mirid bug Apolygus lucorum. Journal of Integrative Agriculture, 21, 2984–2994.

Tsirigos K D, Peters C, Shu N, Käll L, Elofsson A. 2015. The TOPCONS web server for consensus prediction of membrane protein topology and signal peptides. Nucleic Acids Research, 43, W401–W407.

Tunstall N E, Warr C G. 2012. Chemical communication in insects: The peripheral odour coding system of Drosophila Melanogaster. In: López-Larrea C, ed., Sensing in Nature. Springer, New York. pp. 59–77.

Vogt R G, Miller N E, Litvack R, Fandino R A, Sparks J, Staples J, Friedman R, Dickens J C. 2009. The insect SNMP gene family. Insect Biochemistry and Molecular Biology, 39, 448–456.

Vogt R G, Sparks J T, Fandino R A, Ashourian K T. 2021. Reflections on antennal proteins: The evolution of pheromone binding proteins; diversity of pheromone degrading enzymes; and the distribution and behavioral roles of SNMPs. In: Blomquist G J, Vogt R G, eds., Insect Pheromone Biochemistry and Molecular Biology. 2nd ed. Academic Press, London. pp. 675–707.

Wang H L, Ding B J, Dai J Q, Nazarenus T J, Borges R, Mafra-Neto A, Cahoon E B, Hofvander P, Stymne S, Löfstedt C. 2022. Insect pest management with sex pheromone precursors from engineered oilseed plants. Nature Sustainability, 5, 981–990.

Waterhouse A M, Procter J B, Martin D M A, Clamp M, Barton G J. 2009. Jalview Version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics, 25, 1189–1191.

Wheelwright M, Whittle C R, Riabinina O. 2021. Olfactory systems across mosquito species. Cell and Tissue Research, 383, 75–90.

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

Xu W, Zhang H J, Liao Y L, Papanicolaou A. 2021. Characterization of sensory neuron membrane proteins (SNMPs) in cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae). Insect Science, 28, 769–779.

Yang C Y, Kim S J, Kim J H, Kang T J, Ahn S J. 2015. Sex pheromones and reproductive isolation in five mirid species. PLoS ONE, 10, e0127051.

Yang H Y, Ning S Y, Sun X, Chen C, Liu L X, Feng J N. 2020. Identification and characterization of two sensory neuron membrane proteins from onion maggot (Diptera: Anthomyiidae). Journal of Economic Entomology, 113, 418–426.

Yang Z H. 2007. PAML 4: Phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24, 1586–1591.

Yuvaraj J K, Jordan M D, Zhang D D, Andersson M N, Löfstedt C, Newcomb R D, Corcoran J A. 2021. Sex pheromone receptors of the light brown apple moth, Epiphyas postvittana, support a second major pheromone receptor clade within the Lepidoptera. Insect Biochemistry and Molecular Biology, 141, 103708.

Zhang H J, Xu W, Chen Q M, Sun L N, Anderson A, Xia Q Y, Papanicolaou A. 2020. A phylogenomics approach to characterizing sensory neuron membrane proteins (SNMPs) in Lepidoptera. Insect Biochemistry and Molecular Biology, 118, 103313.

Zhang S, Yan S W, Zhang Z X, Cao S, Li B, Liu Y, Wang G R. 2021. Identification and functional characterization of sex pheromone receptors in mirid bugs (Heteroptera: Miridae). Insect Biochemistry and Molecular Biology, 136, 103621.

Zhang T, Mei X D, Zhang X F, Lu Y H, Ning J, Wu K M. 2020. Identification and field evaluation of the sex pheromone of Apolygus lucorum (Hemiptera: Miridae) in China. Pest Management Science, 76, 1847–1855.

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.

Zhao Y J, Li G C, Zhu J Y, Liu N Y. 2020. Genome-based analysis reveals a novel SNMP group of the Coleoptera and chemosensory receptors in Rhaphuma horsfieldi. Genomics, 112, 2713–2728.

绿盲蝽感觉神经元膜蛋白1a（SNMP1a）在性信息素识别中的功能研究

Functional characterization of sensory neuron membrane protein 1a involved in sex pheromone detection of Apolygus lucorum (Hemiptera: Miridae)

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