Identification and tissue distribution of odorant binding protein genes in Harmonia axyridis (Coleoptera: Coccinellidae)

doi:10.1016/S2095-3119(20)63297-X

摘要/Abstract

摘要：

昆虫嗅觉系统在其寻找寄主、交配和产卵等行为中发挥重要作用。气味结合蛋白（OBPs）参与化学信息素的识别，OBPs识别结合气味分子并将其运送至嗅觉神经元上的气味受体。异色瓢虫（鞘翅目：瓢甲科）作为重要的生防天敌被广泛用于防治多种农林业害虫。本研究中，从异色瓢虫成虫触角和整虫转录组中共鉴定到19个OBP基因，所有OBP基因均具有全长开放阅读框，其编码蛋白中11个属于‘Classic’OBPs，7 个属于‘Minus-C’OBPs ，1 个属于‘Plus-C’OBP。它们编码125-241个氨基酸，相对分子量为13.74KDa-27.75 KDa，等电点范围为4.15-8.80。利用系统发育分析研究了异色瓢虫气味结合蛋白与其他鞘翅目昆虫气味结合蛋白的关系。荧光定量PCR结果表明HaxyOBP2，3，5，8，10，12，13，14和15在雌雄成虫触角中高表达；其中HaxyOBP2，3，5，12和15在触角中的表达量显著高于其他组织，HaxyOBP13和HaxyOBP14在触角和头部的表达量相当，而其他基因在胸、腹、足和翅等非嗅觉组织中高表达。本研究结果为进一步探究异色瓢虫嗅觉系统提供了有价值信息，并将增强异色瓢虫作为生防天敌的应用效果。

Abstract:

The olfactory system of insects is crucial in modulating behaviors such as host seeking, mating, and oviposition. Odorant-binding proteins (OBPs) are involved in semiochemical recognition. OBPs recognize and bind odorants and transport them to odorant receptors located in olfactory neurons. Harmonia axyridis (Coleoptera: Coccinellidae) is a widely used predacious biological control agent for many agricultural and forestry pests. This study identified 19 OBPs in H.?axyridis based on the antennal and whole-body transcriptomes of adults and obtained all the full-length open reading frames, including 11 ‘Classic’ OBPs, 7 ‘Minus-C’ OBPs and 1 ‘Plus-C’ OBP. They encoded 125 to 241 amino acid proteins with molecular weights ranging from 13.75 to 27.75 kDa and isoelectric points ranging from 4.15 to 8.80. Phylogenetic analyses were used to study the relationships between H.?axyridis OBPs and OBPs from other species of Coleoptera. Quantitative real-time PCR (qPCR) analysis showed that HaxyOBP2, 3, 5, 8, 10, 12, 13, 14, and 15 were highly expressed in antennae of both adult females and males. Moreover, HaxyOBP2, 3, 5, 12, and 15 were more abundantly expressed in antennae than other body parts, while HaxyOBP13 and HaxyOBP14 were expressed predominantly, and at similar levels, in the head and antennae. The other OBP genes were highly expressed in non-olfactory tissues including the thorax, abdomen, legs, and wings. These results provide valuable information for further study of H.?axyridis olfaction, which may ultimately enhance its use as a biocontrol agent.

Key words: odorant-binding proteins , Harmonia axyridis , expression profile , phylogenetic tree

. [J]. Journal of Integrative Agriculture, 2021, 20(8): 2204-2213.

QU Cheng, WANG Ran, CHE Wu-nan, LI Feng-qi, ZHAO Hai-peng, WEI Yi-yun, LUO Chen, XUE Ming. Identification and tissue distribution of odorant binding protein genes in Harmonia axyridis (Coleoptera: Coccinellidae)[J]. Journal of Integrative Agriculture, 2021, 20(8): 2204-2213.

参考文献

Andersson M N, Grosse-Wilde E, Keeling C I, Bengtsson J M, Yuen M M S, Li M, Hillbur Y, Bohlmann J, Hansson B S, Schlyter F. 2013. Antennal transcriptome analysis of the chemosensory gene families in the tree killing bark beetles, Ips typographus and Dendroctonus ponderosae (Coleoptera: Curculionidae: Scolytinae). BMC Genomics, 14, 198.
Asahina K, Pavlenkovich V, Vosshall L B. 2008. The survival advantage of olfaction in a competitive environment. Current Biology, 18, 1153–1155.
Brito N F, Moreira M F, Melo A C A. 2016. A look inside odorant-binding proteins in insect chemoreception. Journal of Insect Physiology, 95, 51–65.
Cao Y S, Liu J B, Guo J X, Wu H, Zhang G R. 2018. Identification and analysis of odorant-binding protein genes from the wolf spider Pardosa pseudoannulata (Araneae: Lycosidae) based on its transcriptome. Chemoecology, 28, 123–130.
Del Campo M L, Palmer S, Caillaud M. 2011. Characterization of a new odorant binding protein gene in gustatory organs of Manduca sexta Larvae (Lepidoptera: Sphingidae). Annals of the Entomological Society of America, 104, 319–325.
Cui Y, Kang C, Wu Z Z, Lin J T. 2019. Identification and expression analyses of olfactory gene families in the rice grasshopper, Oxya chinensis, from antennal transcriptomes. Frontiers in Physiology, 10, 1223.
Dani F R, Michelucci E, Francese S, Mastrobuoni G, Cappellozza S, La Marca G, Niccolini A, Felicioli A, Moneti G, Pelosi P. 2011. Odorant-binding proteins and chemosensory proteins in pheromone detection and release in the silkmoth Bombyx mori. Chemical Senses, 36, 335–344.
Dippel S, Oberhofer G, Kahnt J, Gerischer L, Opitz L, Schachtner J, Stanke M, Schuetz S, Wimmer E A, Angeli S. 2014. Tissue-specific transcriptomics, chromosomal localization, and phylogeny of chemosensory and odorant binding proteins from the red flour beetle Tribolium castaneum reveal subgroup specificities for olfaction or more general functions. BMC Genomics, 15, 1141.
Gong Z J, Miao J, Duan Y, Jiang Y L, Li T, Wu Y Q. 2014. Identification and expression profile analysis of putative odorant-binding proteins in Sitodiplosis mosellana (Gehin) (Diptera: Cecidomyiidae). Biochemical and Biophysical Research Communications, 444, 164–170.
Gu X C, Zhang Y N, Kang K, Dong S L, Zhang L W. 2015. Antennal transcriptome analysis of odorant reception genes in the red turpentine beetle (RTB), Dendroctonus valens. PLoS ONE, 10, e0125159.
Hickner P V, Rivaldi C L, Johnson C M, Siddappaji M, Raster G J, Syed Z. 2016. The making of a pest: Insights from the evolution of chemosensory receptor families in a pestiferous and invasive fly, Drosophila suzukii. BMC Genomics, 17, 648.
Ishida Y, Tsuchiya W, Fujii T, Fujimoto Z, Miyazawa M, Ishibashi J, Matsuyama S, Ishikawa Y, Yamazaki T. 2014. Niemann-Pick type C2 protein mediating chemical communication in the worker ant. Proceedings of the National Academy of Sciences of the United States of America, 111, 3847–3852.
Ju Q, Li X, Jiang X J, Qu M J, Guo X Q, Han Z J, Li F. 2014. Transcriptome and tissue-specific expression analysis of OBP and CSP genes in the dark black chafer. Archives of Insect Biochemistry and Physiology, 87, 177–200.
Koch R L. 2003. The multicolored Asian lady beetle, Harmonia axyridis: A review of its biology, uses in biological control, and non-target impacts. Journal of Insect Science, 3, 32.
Koch R L, Hutchison W D, Venette R C, Heimpel G E. 2003. Susceptibility of immature monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae: Danainae), to predation by Harmonia axyridis (Coleoptera: Coccinellidae). Biological Control, 28, 265–270.
Leal W S. 2013. Odorant reception in insects: Roles of receptors, binding proteins, and degrading enzymes. Annual Review of Entomology, 58, 373–391.
Li X M, Zhu X Y, Wang Z Q, Wang Y, He P, Chen G, Sun L, Deng D G, Zhang Y N. 2015. Candidate chemosensory genes identified in Colaphellus bowringi by antennal transcriptome analysis. BMC Genomics, 16, 1028.
Matsuo T, Sugaya S, Yasukawa J, Aigaki T, and Fuyama Y. 2007. Odorant-binding proteins OBP57d and OBP57e affect taste perception and host-plant preference in Drosophila sechellia. PLoS Biology, 5, 985–996.
Mitaka H, Matsuo T, Miura N, Ishikawa Y. 2011. Identification of odorant-binding protein genes from antennal expressed sequence tags of the onion fly, Delia antiqua. Molecular Biology Reports, 38, 1787–1792.
Pelletier J, Leal W S. 2009. Genome analysis and expression patterns of odorant-binding proteins from the southern house mosquito Culex pipiens quinquefasciatus. PLoS ONE, 4, e6237.
Pelosi P, Iovinella I, Felicioli A, Dani F R. 2014. Soluble proteins of chemical communication: An overview across arthropods. Frontiers in Physiology, 5, 320.
Pelosi P, Zhou J J, Ban L P, Calvello M. 2006. Soluble proteins in insect chemical communication. Cellular and Molecular Life Sciences, 63, 1658–1676.
Qu C, Wang R, Che W N, Zhu X, Li F Q, Luo C. 2018. Selection and evaluation of reference genes for expression analysis using quantitative real-time PCR in the Asian ladybird Harmonia axyridis (Coleoptera: Coccinellidae). PLoS ONE, 13, e0192521.
Schmittgen T D, Livak K J. 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3, 1101–1108.
Schultze A, Schymura D, Forstner M, Krieger J. 2012. Expression pattern of a ‘Plus-C’ class odorant binding protein in the antenna of the malaria vector Anopheles gambiae. Insect Molecular Biology, 21, 187–195.
Shanbhag S, Park S K, Pikielny C, Steinbrecht R. 2001. Gustatory organs of Drosophila melanogaster: Fine structure and expression of the putative odorant-binding protein PBPRP2. Cell & Tissue Research, 304, 423–437.
Song Y Q, Sun H Z, Du J. 2018. Identification and tissue distribution of chemosensory protein and odorant binding protein genes in Tropidothorax elegans Distant (Hemiptera: Lygaeidae). Scientific Reports, 8, 7803.
Spinelli S, Lagarde A, Iovinella I, Legrand P, Tegoni M, Pelosi P, Cambillau C. 2012. Crystal structure of Apis mellifera OBP14, a C-minus odorant-binding protein, and its complexes with odorant molecules. Insect Biochemistry and Molecular Biology, 42, 41–50.
Sun Y L, Huang L Q, Pelosi P, Wang C Z. 2012. Expression in antennae and reproductive organs suggests a dual role of an odorant-binding protein in two sibling Helicoverpa Species. PLoS ONE, 7, e30040.
Tang Q F, Shen C, Zhang Y, Yang Z P, Han R R, Wang J. 2019. Antennal transcriptome analysis of the maize weevil Sitophilus zeamais: Identification and tissue expression profiling of candidate odorant-binding protein genes. Archives of Insect Biochemistry and Physiology, 101, e21542.
Trouve C, Ledee S, Ferran A, Brun J. 1997. Biological control of the damson-hop aphid, Phorodon humuli (Hom.: Aphididae), using the lady beetle Harmonia axyridis (Col.: Coccinellidae). Entomophaga, 42, 57–62.
Vieira F G, Rozas J. 2011. Comparative genomics of the odorant-binding and chemosensory protein gene families across the arthropoda: Origin and evolutionary history of the chemosensory system. Genome Biology and Evolution, 3, 476–490.
Vogt R G, Riddiford LM. 1981. Pheromone binding and inactivation by moth antennae. Nature, 293, 161–163.
Wang G Y, Zhu M F, Jiang Y D, Zhou W W, Liu S, Heong K L, Cheng J, Zhu Z R. 2017a. Identification of candidate odorant-binding protein and chemosensory protein genes in Cyrtorhinus lividipennis (Hemiptera: Miridae), a key predator of the rice planthoppers in Asia. Environmental Entomology, 46, 654–662.
Wang R, Li F, Zhang W, Zhang X M, Qu C, Tetreau G, Sun L J, Luo C, Zhou J J. 2017b. Identification and expression profile analysis of odorant binding protein and chemosensory protein genes in Bemisia tabaci MED by head transcriptome. PLoS ONE, 12, e0171739.
Wang S, Tan X L, Michaud J P, Shi Z K, Zhang F. 2015. Sexual selection drives the evolution of limb regeneration in Harmonia axyridis (Coleoptera: Coccinellidae). Bulletin of Entomological Research, 105, 245–252.
Wen X J, Wang Q, Gao P, Wen J B. 2018. Identification and comparison of chemosensory genes in the antennal transcriptomes of Eucryptorrhynchus scrobiculatus and
E. brandti fed on Ailanthus altissima. Frontiers in Physiology, 9, 1652.
Xu W, Cornel A J, Leal W S. 2010. Odorant-binding proteins of the malaria mosquito Anopheles funestus sensu stricto. PLoS ONE, 5, e15403.
Yan W, Liu L, Qin W Q, Luo Y Q, Ma X Z, Haider N, Inayeh M. 2016. Identification and tissue expression profiling of odorant binding protein genes in the red palm weevil, Rhynchophorus ferrugineus. SpringerPlus, 5, 1542.
Yuan X, Jiang Y D, Wang G Y, Yu H, Zhou W W, Liu S, Yang M F, Cheng J, Gurr G M, Way M O, Zhu Z R. 2016. Odorant-binding proteins and chemosensory proteins from an invasive pest Lissorhoptrus oryzophilus (Coleoptera: Curculionidae). Environmental Entomology, 45, 1276–1286.
Zhang Y N, Kang K, Xu L, Zhu X Y, Qian J L, Zhang Z J, He P, Li X M. 2017a. Deep sequencing of antennal transcriptome from Callosobruchus chinensis to characterize odorant binding protein and chemosensory protein genes. Journal of Stored Products Research, 74, 13–21.
Zhang Y N, Zhu X Y, Ma J F, Dong Z P, Xu J W, Kang K, Zhang L W. 2017b. Molecular identification and expression patterns of odorant binding protein and chemosensory protein genes in Athetis lepigone (Lepidoptera: Noctuidae). PeerJ, 5, e3157.
Zheng Y, Wang S N, Peng Y, Lu Z Y, Shan S, Yang Y Q, Li R J, Zhang Y J, Guo Y Y. 2018. Functional characterization of a Niemann-Pick type C2 protein in the parasitoid wasp Microplitis mediator. Insect Science, 25, 765–777.
Zhou J J, Huang W S, Zhang G A, Pickett J A, Field L M. 2004. “Plus-C” odorant-binding protein genes in two Drosophila species and the malaria mosquito Anopheles gambiae. Gene, 327, 117–129.
Zhou J J, Vieira F G, He X L, Smadja C, Liu R, Rozas J, Field L M. 2010. Genome annotation and comparative analyses of the odorant-binding proteins and chemosensory proteins in the pea aphid Acyrthosiphon pisum. Insect Molecular Biology, 19, 113–122.
Zhu J, Guo M B, Ban L P, Song L M, Liu Y, Pelosi P, Wang G R. 2018. Niemann-Pick C2 proteins: A new function for an old family. Frontiers in Physiology, 9, 52.