基于比较基因组学苹果蠹蛾入侵生物学特性分析

doi:10.16409/j.cnki.2095-039x.2024.11.007

摘要/Abstract

摘要： 苹果蠹蛾是全球性的入侵果树害虫，目前已扩散到我国9个省市195个区县，严重威胁苹果、梨和其他果树产业安全。近年来，比较基因组学的兴起为研究入侵昆虫的基因组进化和适应机制提供了新的视角和方法。本文选取了包括苹果蠹蛾在内的7种全球性重要入侵昆虫和7种亲缘关系相近的非入侵性昆虫，鉴定获得2324个单拷贝直系同源基因，其中110个基因在入侵昆虫中进化速率显著高于非入侵昆虫，336个基因在入侵昆虫中均存在正选择位点，这些基因参与机体热量生成及代谢速率调节等生理活动。对入侵和非入侵昆虫进行直系同源基因和Treefam基因家族的扩增和收缩分析，结果显示分别有3个直系同源基因和18个Treefam基因家族在入侵性昆虫之间显著扩增，这些扩增的基因主要参与生物体的物质和能量代谢、环境适应等。此外，入侵性昆虫在基因组上P450基因家族数量显著高于非入侵性昆虫。本研究运用比较基因组学分析方法，揭示了苹果蠹蛾等入侵性昆虫中在基因组进化上的一些共性分子特征，为入侵害虫的入侵机制研究和科学防控提供重要的理论支撑。

关键词: 苹果蠹蛾, 入侵昆虫, 比较基因组学, 入侵机制, 分子进化

Abstract: The codling moth (Cydia pomonella), a globally invasive pest affecting fruit trees, has now spread to 195 districts and counties across nine provinces and municipalities in China, which poses a significant threat to the apple, pear, and other fruit tree industries. In recent years, the advent of comparative genomics has offered novel perspectives and methodologies for investigating the genomic evolution and adaptive mechanisms of invasive species. In this study, we selected seven globally key invasive insect species, including the codling moth (Cydia pomonella), and seven closely related non-invasive insect species. We identified 2,324 single-copy orthologous genes, among which 110 genes exhibited significantly higher evolutionary rates in invasive species compared to non-invasive species. Additionally, 336 genes in invasive species displayed signs of positive selection, and these genes are involved in physiological processes such as thermogenesis and metabolic rate regulation. Our analysis of the expansion and contraction of orthologous genes and Treefam gene families between invasive and non-invasive species revealed that three orthologous gene families and 18 Treefam gene families were significantly expanded in invasive species. These expanded gene families are primarily associated with material and energy metabolism, as well as environmental adaptation. Furthermore, the number of P450 gene families in the genomes of invasive species was more than that in non-invasive species. This study utilizes comparative genomics analysis methods to elucidate common molecular characteristics in the genomic evolution of invasive insect species like the codling moth. These findings provide important theoretical support for understanding the invasion mechanisms and establishing control strategies of invasive pests.

Key words: Cydia pomonella, invasive insects, comparative genomics, invasion mechanisms, molecular evolution

中图分类号:

S476

陶少敏, 何诗甜, 范月圆, 尹传林, 俞晓平. 基于比较基因组学苹果蠹蛾入侵生物学特性分析[J]. 中国生物防治学报, 2025, 41(3): 721-732.

TAO Shaomin, HE Shitian, FAN Yueyuan, YIN Chuanlin, YU Xiaoping. A Comparative Genomics Analysis of the Biological Invasion Characteristics of Cydia pomonella[J]. Chinese Journal of Biological Control, 2025, 41(3): 721-732.

参考文献

[1] Barnes M. Codling moth occurrence, host race formation, and damage//van der Geest L P S, Evenhuis H H, eds. Tortricid Pests: Their Biology, Natural Enemies and Control [M]. Amsterdam: Elsevier Science, 1991.
[2] 张学祖. 苹果蠹蛾(Carpocapsa pomonella L.)在我国的新发现[J]. 昆虫学报, 1957, 7(4): 467-472.
[3] Wan F, Yin C, Tang R, et al. A chromosome-level genome assembly of Cydia pomonella provides insights into chemical ecology and insecticide resistance[J]. Nature Communications, 2019, 10(1): 4237.
[4] Early R, Bradley B A, Dukes J S, et al. Global threats from invasive alien species in the twenty-first century and national response capacities[J]. Nature Communications, 2016, 7(1): 12485.
[5] Hufbauer R A, Torchin M E. Integrating ecological and evolutionary theory of biological invasions[J]. Biological Invasions, 2007, 9(1): 79-96.
[6] Blossey B, Notzold R. Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis[J]. Journal of Ecology, 1995, 83(5): 887-896.
[7] Papanicolaou A, Schetelig M F, Arensburger P, et al. The whole genome sequence of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species[J]. Genome Biology, 2016, 17: 1-31.
[8] Chen W, Hasegawa D K, Kaur N, et al. The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance[J]. BMC Biology, 2016, 14: 1-15.
[9] Pearce S L, Clarke D F, East P D, et al. Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species[J]. BMC Biology, 2017, 15: 1-30.
[10] Cheng T, Wu J, Wu Y, et al. Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest[J]. Nature Ecology & Evolution, 2017, 1(11): 1747-56.
[11] Chen Q, Zhao H, Wen M, et al. Genome of the webworm Hyphantria cunea unveils genetic adaptations supporting its rapid invasion and spread[J]. Bmc Genomics, 2020, 21: 1-22.
[12] Liu Z, Xing L, Huang W, et al. Chromosome-level genome assembly and population genomic analyses provide insights into adaptive evolution of the red turpentine beetle, Dendroctonus valens[J]. BMC Biology, 2022, 20(1): 190.
[13] Soudi S, Crepeau M, Collier T C, et al. Genomic signatures of local adaptation in recent invasive Aedes aegypti populations in California[J]. BMC Genomics, 2023, 24(1): 311.
[14] Men Q L, Chen M H, Zhang Y L, et al. Genetic structure and diversity of a newly invasive species, the codling moth, Cydia pomonella (L.)(Lepidoptera: Tortricidae) in China[J]. Biological invasions, 2013, 15: 447-58.
[15] Zhou Z. A review on control of tobacco caterpillar, Spodoptera litura[J]. Chinese Bulletin of Entomology, 2009, 46(3): 354-61.
[16] Valencia-Montoya W A, Elfekih S, North H L, et al. Adaptive introgression across semipermeable species boundaries between local Helicoverpa zea and invasive Helicoverpa armigera moths[J]. Molecular Biology and Evolution, 2020, 37(9): 2568-83.
[17] Gershman A, Romer T G, Fan Y, et al. De novo genome assembly of the tobacco hornworm moth (Manduca sexta)[J]. G3, 2021, 11(1): jkaa047.
[18] 罗晨, 张芝利. 烟粉虱Bemisia tabaci (Gennadius)研究概述[J]. 北京农业科学, 2000(S1): 4-13.
[19] Giunti G, Benelli G, Campolo O, et al. Biology, ecology and invasiveness of the Mediterranean fruit fly, Ceratitis capitata: A review[J]. Entomologia Generalis, 2023, 43(6): 1221-39.
[20] Walsh D B, Bolda M P, Goodhue R E, et al. Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential[J]. Journal of Integrated Pest Management, 2011, 2(1): G1-G7.
[21] Sayers E W, Beck J, Bolton E E, et al. Database resources of the national center for biotechnology information[J]. Nucleic Acids Research, 2021, 49(D1): D10.
[22] Emms D M, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy[J]. Genome Biology, 2015, 16: 1-14.
[23] Katoh K, Misawa K, Kuma K I, et al. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform[J]. Nucleic Acids Research, 2002, 30(14): 3059-66.
[24] Capella-Gutiérrez S, Silla-Martínez J M, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses[J]. Bioinformatics, 2009, 25(15): 1972-1975.
[25] Darriba D, Posada D, Kozlov A M, et al. ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models[J]. Molecular Biology and Evolution, 2020, 37(1): 291-295.
[26] Kozlov A M, Darriba D, Flouri T, et al. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference[J]. Bioinformatics, 2019, 35(21): 4453-4458.
[27] Yang Z. PAML 4: phylogenetic analysis by maximum likelihood[J]. Molecular Biology and Evolution, 2007, 24(8): 1586-1591.
[28] Han M V, Thomas G W, Lugo-Martinez J, et al. Estimating gene gain and loss rates in the presence of error in genome assembly and annotation using CAFE 3[J]. Molecular Biology and Evolution, 2013, 30(8): 1987-1997.
[29] Potter S C, Luciani A, Eddy S R, et al. HMMER web server: 2018 update[J]. Nucleic Acids Research, 2018, 46(W1): W200-W4.
[30] Castillo-Davis C I, Hartl D L. GeneMerge—post-genomic analysis, data mining, and hypothesis testing[J]. Bioinformatics, 2003, 19(7): 891-893.
[31] El-Gebali S, Mistry J, Bateman A, et al. The Pfam protein families database in 2019[J]. Nucleic Acids Research, 2019, 47(D1): D427-D32.
[32] Mavrevski R, Traykov M, Trenchev I, et al. Approaches to modeling of biological experimental data with GraphPad Prism software[J]. WSEAS Trans Syst Control, 2018, 13(1): 242-249.
[33] Li X, Zhou Y, Wu K. Biological characteristics and energy metabolism of migrating insects[J]. Metabolites, 2023, 13(3): 439.
[34] Zhao Z, Hui C, Peng S, et al. The world's 100 worst invasive alien insect species differ in their characteristics from related non-invasive species[J].Journal of Applied Ecology, 2023, 60(9): 1929-1938.
[35] Lubawy J, Chowański S, Adamski Z, et al. Mitochondria as a target and central hub of energy division during cold stress in insects[J]. Frontiers in Zoology, 2022, 19(1): 1.
[36] Bertrand C, Valet P, Castan-Laurell I. Apelin and energy metabolism[J]. Frontiers in Physiology, 2015, 6: 137232.
[37] Hardie D G. Energy sensing by the AMP-activated protein kinase and its effects on muscle metabolism[J]. Proceedings of the Nutrition Society, 2011, 70(1): 92-9.
[38] Ma E H, Poffenberger M C, Wong A H, et al. The role of AMPK in T cell metabolism and function[J]. Current Opinion in Immunology, 2017, 46: 45-52.
[39] González-Sarrías A, Espín J C, Tomás-Barberán F A, et al. Gene expression, cell cycle arrest and MAPK signalling regulation in Caco-2 cells exposed to ellagic acid and its metabolites, urolithins[J]. Molecular Nutrition & Food Research, 2009, 53(6): 686-98.
[40] 张霞, 孙琳琳, 钟殿胜. LKB1-AMPK-mTOR信号传导通路在肿瘤中的研究进展[J]. 中国肺癌杂志, 2011, 14(8): 685-693.
[41] Saxton R A, Sabatini D M. mTOR signaling in growth, metabolism, and disease[J]. Cell, 2017, 168(6): 960-976.
[42] López M. Hypothalamic AMPK and energy balance[J]. European Journal of Clinical Investigation, 2018, 48(9): e12996.
[43] Huang Z, Tian Z, Zhao Y, et al. MAPK signaling pathway is essential for female reproductive regulation in the cabbage beetle, Colaphellus bowringi[J]. Cells, 2022, 11(10): 1602.
[44] Xu Y, Wei W, Lin G, et al. The Ras/MAPK pathway is required for regenerative growth of wing discs in the black cutworm Agrotis ypsilon[J]. Insect Biochemistry and Molecular Biology, 2021, 131: 103552.
[45] Yuan J, Dong X, Yap J, et al. The MAPK and AMPK signalings: interplay and implication in targeted cancer therapy[J]. Journal of Hematology & Oncology, 2020, 13(1): 113.