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Journal of Integrative Agriculture  2023, Vol. 22 Issue (3): 825-843    DOI: 10.1016/j.jia.2022.08.027
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Chromosome-level genome assembly of Cylas formicarius provides insights into its adaptation and invasion mechanisms

HUA Jin-feng1, 2#, ZHANG Lei1, HAN Yong-hua1, GOU Xiao-wan1, CHEN Tian-yuan2, HUANG Yong-mei2, LI Yan-qing2, MA Dai-fu1, 3#, LI Zong-yun1#

1 Institute of Integrative Plant Biology/Jiangsu Key Laboratory of Phylogenomics and Comparative Genomics/School of Life Sciences, Jiangsu Normal University, Xuzhou 221116, P.R.China

2 Sweet Potato Laboratory, Institute of Maize Research, Guangxi Academy of Agricultural Sciences, Nanning 530007, P.R.China

3 Xuzhou Academy of Agricultural Sciences/Institute of Sweet Potato Research, Chinese Academy of Agricultural Sciences, Xuzhou 221131, P.R.China

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摘要  

甘薯小象甲是甘薯上危害最为严重的世界性害虫,对生态环境和社会经济遭受巨大损失。为提高甘薯小象甲综合防治的效果和深入理解其遗传进化机制,我们对甘薯小象甲功能基因组学进行了的深入研究。利用 Illumina  PacBio技术,对单对交配15代的甘薯小象甲进行测序。获得了甘薯小象甲成虫染色体水平的基因组,基因组大小为338.84MbContig N50  Scaffold N50 分别为 14.97 Mb34.23 Mb。预测重复序列为 157.51 Mb 11907 个编码蛋白质基因。共有 337.06 Mb长度的基因组序列被定位到 11 条染色体上,其中能够确定顺序和方向的序列长度为 333.79 Mb,占定位到染色体上总序列长度的 99.03 %。比较基因组学分析表明,甘薯小象甲和中欧山松大小蠹亲缘关系较近,约 1.38 亿年前从中欧山松大小蠹的祖先分化而来。许多重要的基因家族在甘薯小象甲基因组中得到了扩张,包括农药解毒、耐冷应激和化学感觉系统相关基因家族。为了进一步解析气味结合蛋白在甘薯小象甲嗅觉识别过程中的作用,竞争性结合分析结果表明,CforOBP4-6对性信息素其他配体具有很强的结合亲和力。高质量的甘薯小象甲基因组图谱为揭示其分子生态学基础、群体遗传和适应性进化机制及绿色有效防控的新方法和新技术提供了坚实的基础。



Abstract  

Cylas formicarius is one of the most important pests of sweet potato worldwide, causing considerable ecological and economic damage.  This study improved the effect of comprehensive management and understanding of genetic mechanisms by examining the functional genomics of Cformicarius.  Using Illumina and PacBio sequencing, this study obtained a chromosome-level genome assembly of adult weevils from lines inbred for 15 generations.  The high-quality assembly obtained was 338.84 Mb, with contig and scaffold N50 values of 14.97 and 34.23 Mb, respectively.  In total, 157.51 Mb of repeat sequences and 11 907 protein-coding genes were predicted.  A total of 337.06 Mb of genomic sequences was located on the 11 chromosomes, accounting for 99.03% of the total length of the associated chromosome.  Comparative genomic analysis showed that Cformicarius was sister to Dendroctonus ponderosae, and Cformicarius diverged from Dponderosae approximately 138.89 million years ago (Mya).  Many important gene families expanded in the Cformicarius genome were involved in the detoxification of pesticides, tolerance to cold stress and chemosensory system.  To further study the role of odorant-binding proteins (OBPs) in olfactory recognition of Cformicarius, the binding assay results indicated that CforOBP4–6 had strong binding affinities for sex pheromones and other ligands.  The high-quality Cformicarius genome provides a valuable resource to reveal the molecular ecological basis, genetic mechanism, and evolutionary process of major agricultural pests; it also offers new ideas and new technologies for ecologically sustainable pest control.

Keywords:  Cylas formicarius        PacBio sequencing        High-through chromosome conformation capture        chromosome-level genome        chemosensory genes        fluorescence competitive binding  
Received: 13 February 2022   Accepted: 31 May 2022
Fund: 

This research was supported by the Natural Science Foundation of Guangxi Autonomous Region, China (2022GXNSFAA035558), the Technology Development Foundation of Guangxi Academy of Agricultural Sciences (2021ZX09), the China Agriculture Research System of MOF and MARA (CARS-10-B3 and CARS-10-C19), the Guangxi Innovation Team Construction Project (nycytxgxcxtd-11-03), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

 

About author:  #Correspondence LI Zong-yun, Tel: +86-516-83500083, E-mail: zongyunli@jsnu.edu.cn; MA Dai-fu, Tel: +86-516-82189200, E-mail: daifuma@163.com; HUA Jin-feng, Tel: +86-771-3243101, E-mail: heda321@163.com

Cite this article: 

HUA Jin-feng, ZHANG Lei, HAN Yong-hua, GOU Xiao-wan, CHEN Tian-yuan, HUANG Yong-mei, LI Yan-qing, MA Dai-fu, LI Zong-yun. 2023. Chromosome-level genome assembly of Cylas formicarius provides insights into its adaptation and invasion mechanisms. Journal of Integrative Agriculture, 22(3): 825-843.

Austin D F, Jansson R K, Wolfe G W. 1991. Convolvulaceae and Cylas: A proposed hypothesis on the origins of this plant/insect relationship. Journal of Tropical Medicine, 68, 162-170.Bin S Y, Qu M Q, Pu X H, Wu Z Z, Lin J T. 2017. Antennal transcriptome and expression analyses of olfactory genes in the sweetpotato weevil Cylas formicarius. Scientific Reports, 7, 11073.

Bao W, Kojima K K, Kohany O. 2015. Repbase update, a database of repetitive elements in eukaryotic genomes. Mobile DNA, 6, 11.

Bin S Y, Qu M Q, Pu X H, Wu Z Z, Lin J T. 2017. Antennal transcriptome and expression analyses of olfactory genes in the sweetpotato weevil Cylas formicarius. Scientific Reports, 7, 11073.

Birney E, Clamp M, Durbin R. 2004. GeneWise and genomewise. Genome Research, 14, 988-995.

Blomquist G J, Tittiger C, Maclean M, Keeling C I. 2021. Cytochromes P450: Terpene detoxification and pheromone production in bark beetles. Current Opinion in Insect Science, 43, 97–102.

Bouchard P, Bousquet Y, Davies A E, Alonso-Zarazaga M A, Lawrence J F, Lyal C H, Newton A F, Reid C A, Schmitt M, Slipinski S A, Smith A B. 2011. Family-group names in Coleoptera (Insecta). Zookeys, 88, 1-972.

Bovell-Benjamin A C. 2007. Sweet potato: A review of its past, present, and future role in human nutrition. Advances in Food and Nutrition Research, 52, 1-59.

Burton J N, Adey A, Patwardhan R P, Qiu R, Kitzman J O, Shendure J. 2013. Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nature Biotechnology, 31, 1119-1125.

Capinera J L, Jansson R K, Raman K V. 1999. Sweet potato pest management. A global perspective. Florida Entomologist, 82, 125.

Choi J H, Kijimoto T, Snell-Rood E, Tae H, Yang Y, Moczek A P, Andrews J. 2010. Gene discovery in the horned beetle Onthophagus taurus. BMC Genomics, 11, 703.

Coffelt J A, Vick K W, Sower L L, McClellan W T. 1978. Sex pheromone of the sweetpotato weevil,Cylas formicarius elegantulus: Laboratory bioassay and evidence for a multiple component system. Journal of Environmental Entomology, 7, 756-758.

Consortium C E S. 1998. Genome sequence of the nematode C. elegans: A platform for investigating biology. Science, 282, 2012-2018.

Cunningham C B, Ji L, Wiberg R A, Shelton J, McKinney E C, Parker D J, Meagher R B, Benowitz K M, Roy-Zokan E M, Ritchie M G, Brown S J, Schmitz R J, Moore A J. 2015. The genome and methylome of a beetle with complex social behavior, Nicrophorus vespilloides (Coleoptera: Silphidae). Genome Biology and Evolution, 7, 3383-3396.

De Bie T, Cristianini N, Demuth J P, Hahn M W. 2006. I: A computational tool for the study of gene family evolution. Bioinformatics, 22, 1269-1271.

Dermauw W, Ilias A, Riga M, Tsagkarakou A, Vontas J. 2012. The cys-loop ligand-gated ion channel gene family of Tetranychus urticae: Implications for acaricide toxicology and a novel mutation associated with abamectin resistance. Insect Biochemistry and Molecular Biology, 42, 455-465.

Fleischer J, Pregitzer P, Breer H, Krieger J. 2018. Access to the odor world: Olfactory receptors and their role for signal transduction in insects. Cellular and Molecular Life Sciences, 75, 485-508.

Fu X, Li J, Tian Y, Quan W, Zhang S, Liu Q, Liang F, Zhu X, Zhang L, Wang D, Hu J. 2017. Long-read sequence assembly of the firefly Pyrocoelia pectoralis genome. Gigascience, 6, 1-7.

Gelbart W M. 1992. The return of the fly. Science, 257, 1421-1422.

Gunter N L, Oberprieler R G, Cameron S L. 2016. Molecular phylogenetics of Australian weevils (Coleoptera: Curculionoidea): Exploring relationships in a hyperdiverse lineage through comparison of independent analyses. Austral Entomology, 55, 217-233.

Haas B J, Salzberg S L, Zhu W, Pertea M, Allen J E, Orvis J, White O, Buell C R, Wortman J R. 2008. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biology, 9, R7.

Heath R R, Coffelt J A, Sonnet P E, Proshold F I, Dueben B, Tumlinson J H. 1986. Identification of sex pheromone produced by female sweetpotato weevil, Cylas formicarius elegantulus (Summers). Journal of Chemical Ecology, 12, 1489-1503.

Hlerema I, Laurie S, Eiasu B. 2017. Preliminary observations on use of Beauveria bassiana for the control of the sweet potato weevil (Cylas sp.) in South Africa. Open Agriculture, 2, 595-599.

Hua J, Zhang S, Cui J, Wang D, Wang C, Luo J. Lv L. 2012. Identification and binding characterization of three odorant binding proteins and one chemosensory protein from Apolygus lucorum (Meyer-Dur). Journal of Chemical Ecology, 38,1163-1170.

Hua J, Zhang S, Cui J, Wang D, Wang C, Luo J, Ma Y. 2013. Functional characterizations of one odorant binding protein and three chemosensory proteins from Apolygus lucorum (meyer-dur) (hemiptera: miridae) legs. Journal of Insect Physiology, 59, 690-696.

Hua J, Pan C, Huang Y, Li Y, Li H, Wu C, Chen T, Ma D, Li Z. 2021a. Functional characteristic analysis of three odorant-binding proteins from the sweet potato weevil (Cylas formicarius) in the perception of sex pheromones and host plant volatiles. Pest Management Science, 77, 300-312.

Hua J, Fu Y, Zhou Q, Huang Y, Li H, Chen T, Ma D, Li Z. 2021b. Three chemosensory proteins from the sweet potato weevil, Cylas formicarius, are involved in the perception of host plant volatiles. Pest Management Science, 77, 4497-4509.

Huang L H, Wang C Z, Kang L. 2009. Cloning and expression of five heat shock protein genes in relation to cold hardening and development in the leafminer, Liriomyza sativa. Journal of Insect Physiology, 55, 279-285.

Jin J, Li Y, Zhou Z, Zhang H, Wan F. 2020. Heat shock factor is involved in regulating the transcriptional expression of two potential Hsps (AhHsp70 and AhsHsp21) and its role in heat shock response of Agasicles hygrophila. Frontiers in Physiology, 11, 562204.

Keeling C I, Yuen M M, Liao N Y, Docking T R, Chan S K, Taylor G A, Palmquist D L, Jackman S D, Nguyen A, Li M, Henderson H, Janes J K, Zhao Y, Pandoh P, Moore R, Sperling F A, Huber D P, Birol I, Jones S J, Bohlmann J. 2013. Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest. Genome Biology, 14, R27.

Keilwagen J, Wenk M, Erickson J L, Schattat M H, Grau J, Hartung F. 2016. Using intron position conservation for homology-based gene prediction. Nucleic Acids Research, 44, e89.

Keith D E. 2010. Genome sequence of the pea aphid Acyrthosiphon pisum. Plos Biology, 8, e1000313.

Koren S, Walenz B P, Berlin K, Miller J R, Bergman N H, Phillippy A M. 2017. Canu: Scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Research, 27, 722-736.

Kusy D, Motyka M, Bocek M, Vogler A P, Bocak L. 2018. Genome sequences identify three families of Coleoptera as morphologically derived click beetles (Elateridae). Scientific Reports, 8, 17084.

Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754-1760.

Ma J, Wang R, Li X, Gao B, Chen S. 2016. Transcriptome and gene expression analysis of Cylas formicarius (Coleoptera: Brentidae) during different development stages. Journal of Insect Science, 16, 1-11.

McKenna D D, Scully E D, Pauchet Y, Hoover K, Kirsch R, Geib S M, Mitchell R F, Waterhouse R M, Ahn S J, Arsala D, Benoit J B, Blackmon H, Bledsoe T, Bowsher J H, Busch A, Calla B, Chao H, Childers A K, Childers C, Clarke D J, et al. 2016. Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle-plant interface. Genome Biology, 17, 227.

Meyer J M, Markov G V, Baskaran P, Herrmann M, Sommer R J, Rodelsperger C. 2016. Draft genome of the scarab beetle Oryctes borbonicus on La Reunion Island. Genome Biology and Evolution, 8, 2093-2105.

Mitchell R F, Schneider T M, Schwartz A M, Andersson M N, McKenna D D. 2020. The diversity and evolution of odorant receptors in beetles (Coleoptera). Insect Molecular Biology, 29, 77-91.

Munkhbayar O, Liu N, Li M, Qiu X. 2021. First report of voltage-gated sodium channel M918V and molecular diagnostics of nicotinic acetylcholine receptor R81T in the cotton aphid. Journal of Applied Entomology, 145, 261-269.

Nagano T, Lubling Y, Yaffe E, Wingett S W, Dean W, Tanay A, Fraser P. 2015. Single-cell Hi-C for genome-wide detection of chromatin interactions that occur simultaneously in a single cell. Nature Protocols, 10, 1986-2003.

Parra G, Bradnam K, Korf I. 2007. CEGMA: A pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics, 23, 1061-1067.

Pittendrigh B R, Clark J M, Johnston J S, Lee S H, Romero-Severson J, Dasch G A. 2006. Sequencing of a new target genome: The Pediculus humanus humanus (Phthiraptera: Pediculidae) genome project. Journal of Medical Entomology, 43, 1103-1111.

Rao S S, Huntley M H, Durand N C, Stamenova E K, Bochkov I D, Robinson J T, Sanborn A L, Machol I, Omer A D, Lander E S, Aiden E L. 2014. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell, 159, 1665-1680.

Rosenfeld J A, Reeves D, Brugler M R, Narechania A, Simon S, Durrett R, Foox J, Shianna K, Schatz M C, Gandara J, Afshinnekoo E, Lam E T, Hastie A R, Chan S, Cao H, Saghbini M, Kentsis A, Planet P J, Kholodovych V, Tessler M, et al. 2016. Genome assembly and geospatial phylogenomics of the bed bug Cimex lectularius. Nature Communications, 7, 10164.

Ruan J, Li H. 2020. Fast and accurate long-read assembly with wtdbg2. Nature Methods, 17, 155-158.

Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall L B, Touhara K. 2008. Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature, 452, 1002-1006.

Schon K, Skuhrovec J. 2016. A new species of the genus Corimalia Gozis, 1885 (Coleoptera: Brentidae: Nanophyinae) from the Caucasus. Zootaxa, 4169, 571-578.

Schoville S D, Chen Y H, Andersson M N, Benoit J B, Bhandari A, Bowsher J H, Brevik K, Cappelle K, Chen M M, Childers A K, Childers C, Christiaens O, Clements J, Didion E M, Elpidina E N, Engsontia P, Friedrich M, Garcia-Robles I, Gibbs R A, Goswami C, et al. 2018. A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Scientific Reports, 8, 1931.

Sequencing Consortium T H G. 2006. Erratum: Insights into social insects from the genome of the honeybee Apis mellifera. Nature, 444, 512-512.

Servant N, Varoquaux N, Lajoie B R, Viara E, Chen C J, Vert J P, Heard E, Dekker J, Barillot E. 2015. HiC-Pro: An optimized and flexible pipeline for Hi-C data processing. Genome Biology, 16, 259.

She R, Chu J S, Wang K, Pei J, Chen N. 2009. GenBlastA: Enabling BLAST to identify homologous gene sequences. Genome Research, 19, 143-149.

Simao F A, Waterhouse R M, Ioannidis P, Kriventseva E V, Zdobnov E M. 2015. BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics, 31, 3210-3212.

Sutherland J A. 1986a. Damage by Cylas formicarius Fab. to sweet potato vines and tubers, and the effect of infestations on total yield in Papua New Guinea. Tropical Pest Management, 32, 316-323.

Sutherland J A. 1986b. A review of the biology and control of the sweetpotato weevil Cylas formicarius (Fab). Tropical Pest Management, 32, 304-315.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731-2739.

Tang F, Tu H, Shang Q, Gao X, Liang P. 2020. Molecular cloning and characterization of five glutathione s-transferase genes and promoters from Micromelalopha troglodyta (Graeser) (Lepidoptera: Notodontidae) and their response to tannic acid stress. Insects, 11, 1-16.

Tarailo-Graovac M, Chen N. 2009. Using RepeatMasker to identify repetitive elements in genomic sequences. Current Protocols in Bioinformatics, 4, 4-10.

Terrapon N, Li C, Robertson H M, Ji L, Meng X, Booth W, Chen Z, Childers C P, Glastad K M, Gokhale K, Gowin J, Gronenberg W, Hermansen R A, Hu H, Hunt B G, Huylmans A K, Khalil S M, Mitchell R D, Munoz-Torres M C, Mustard J A, et al. 2014. Molecular traces of alternative social organization in a termite genome. Nature Communications, 5, 3636.

TGSC (Tribolium Genome Sequencing Consortium). 2008. The genome of the model beetle and pest Tribolium castaneum. Nature, 452, 949-955.

Treangen T J, Salzberg S L. 2012. Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nature Reviews Genetics, 13, 36-46.

Vega F E, Brown S M, Chen H, Shen E, Nair M B, Ceja-Navarro J A, Brodie E L, Infante F, Dowd P F, Pain A. 2015. Draft genome of the most devastating insect pest of coffee worldwide: the coffee berry borer, Hypothenemus hampei. Scientific Reports, 5, 12525.

Wang X, Fang X, Yang P, Jiang X, Jiang F, Zhao D, Li B, Cui F, Wei J, Ma C, Wang Y, He J, Luo Y, Wang Z, Guo X, Guo W, Wang X, Zhang Y, Yang M, Hao S, et al. 2014. The locust genome provides insight into swarm formation and long-distance flight. Nature Communications, 5, 2957.

Wolfe G W. 1991. The origin and dispersal of the pest species of Cylas with a key to the pest species groups of the world. Sweet Potato Pest Manag on a Global Perspective, 13-43.

Wt K, Hongbo Z, Amoanimaa-Dede H, Meiwei G, Yeboah A. 2019. The major sweet potato weevils; management and control: A review. Entomology, Ornithology & Herpetology: Current Research, 8, 1-9.

Wu Y M, Li J, Chen X S. 2018. Draft genomes of two blister beetles Hycleus cichorii and Hycleus phaleratus. Gigascience, 7, 1-7.

Wu N, Zhang S, Li X, Cao Y, Liu X, Wang Q, Liu Q, Liu H, Hu X, Zhou X J, James A A, Zhang Z, Huang Y, Zhan S. 2019. Fall webworm genomes yield insights into rapid adaptation of invasive species. Nature Ecology & Evolution, 3, 105-115.

Wurm Y, Wang J, Riba-Grognuz O, Corona M, Nygaard S, Hunt B G, Ingram K K, Falquet L, Nipitwattanaphon M, Gotzek D, Dijkstra M B, Oettler J, Comtesse F, Shih C J, Wu W J, Yang C C, Thomas J, Beaudoing E, Pradervand S, Flegel V, et al. 2011. The genome of the fire ant Solenopsis invicta. Proceedings of the National Academy of Sciences of the United States of America, 108, 5679-5684.

Xia Q, Zhou Z, Lu C, Cheng D, Dai F, Li B, Zhao P, Zha X, Cheng T, Chai C, Pan G, Xu J, Liu C, Lin Y, Qian J, Hou Y, Wu Z, Li G, Pan M, Li C, et al. 2004. A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science, 306, 1937-1940.

Xie W, He C, Fei Z, Zhang Y. 2020. Chromosome-level genome assembly of the greenhouse whitefly (Trialeurodes vaporariorum Westwood). Molecular Ecology Resources, 20, 995-1006.

Xu P, Atkinson R, Jones D N, Smith D P. 2005. Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron, 45, 193-200.

Yang H, Li Y. 2019. Complete mitochondrial genome of Cylas formicarius (Coleoptera: Brentidae) from China. Mitochondrial DNA Part B-Resources, 4, 1241-1242.

Yang J, Wan W, Xie M, Mao J, Dong Z, Lu S, He J, Xie F, Liu G, Dai X, Chang Z, Zhao R, Zhang R, Wang S, Zhang Y, Zhang W, Wang W, Li X. 2020. Chromosome-level reference genome assembly and gene editing of the dead-leaf butterfly Kallima inachus. Molecular Ecology Resources, 20, 1080-1092.

Zhang L, Li S, Luo J, Du P, Wu L, Li Y, Zhu X, Wang L, Zhang S, Cui J. 2020. Chromosome-level genome assembly of the predator Propylea japonica to understand its tolerance to insecticides and high temperatures. Molecular Ecology Resources, 20, 292-307.

 

 

 

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