Rapid transcriptome sequencing of an invasive pest, the brown marmorated stink bug Halyomorpha halys

BMC Genomics

Julie C Dunning Hotopp³  Leslie Pick⁵  Luke J Tallon⁴  Naomi Sengamalay⁴  Melissa Flowers⁴  Sandra Ott⁴  Amol Shetty⁴  Joshua Orvis⁴  Marcus C Chibucos³  Sean Daugherty⁴  Todd Creasy²  Nikhil Kumar⁴  Yong Lu⁵  Panagiotis Ioannidis¹ 

[1]Current address: Department of Genetic Medicine and Development, University of Geneva Medical School, Geneva 1211, Switzerland

[2]Current address: Gaithersburg, MD, USA

[3]Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, USA

[4]Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, USA

[5]Departments of Entomology and Cell Biology & Molecular Genetics, University of Maryland College Park, College Park, MD, USA

关键词: Lysozyme;    Mannanase;    Horizontal gene transfer;    Lateral gene transfer;    Invasive species;    Hemiptera;    Transcriptome;    Halyomorpha halys;    Brown marmorated stink bug;   

Others  :  1141128
DOI  :  10.1186/1471-2164-15-738

 received in 2014-05-16, accepted in 2014-08-21,  发布年份 2014

【 摘 要 】

Background

Halyomorpha halys (Stål) (Insecta:Hemiptera;Pentatomidae), commonly known as the Brown Marmorated Stink Bug (BMSB), is an invasive pest of the mid-Atlantic region of the United States, causing economically important damage to a wide range of crops. Native to Asia, BMSB was first observed in Allentown, PA, USA, in 1996, and this pest is now well-established throughout the US mid-Atlantic region and beyond. In addition to the serious threat BMSB poses to agriculture, BMSB has become a nuisance to homeowners, invading home gardens and congregating in large numbers in human-made structures, including homes, to overwinter. Despite its significance as an agricultural pest with limited control options, only 100 bp of BMSB sequence data was available in public databases when this project began.

Results

Transcriptome sequencing was undertaken to provide a molecular resource to the research community to inform the development of pest control strategies and to provide molecular data for population genetics studies of BMSB. Using normalized, strand-specific libraries, we sequenced pools of all BMSB life stages on the Illumina HiSeq. Trinity was used to assemble 200,000 putative transcripts in >100,000 components. A novel bioinformatic method that analyzed the strand-specificity of the data reduced this to 53,071 putative transcripts from 18,573 components. By integrating multiple other data types, we narrowed this further to 13,211 representative transcripts.

Conclusions

Bacterial endosymbiont genes were identified in this dataset, some of which have a copy number consistent with being lateral gene transfers between endosymbiont genomes and Hemiptera, including ankyrin-repeat related proteins, lysozyme, and mannanase. Such genes and endosymbionts may provide novel targets for BMSB-specific biocontrol. This study demonstrates the utility of strand-specific sequencing in generating shotgun transcriptomes and that rapid sequencing shotgun transcriptomes is possible without the need for extensive inbreeding to generate homozygous lines. Such sequencing can provide a rapid response to pest invasions similar to that already described for disease epidemiology.

【 授权许可】

   
2014 Ioannidis et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 9.

【 参考文献 】

• [1]Hoebeke ER, Carter ME: Halyomorpha halys (Stål) (Heteroptera:Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc Entomol Soc Wash 2003, 105:225-237.
• [2]Brown Marmorated Stink Bug occurrence in US and Canada stateshttp://www.stopbmsb.org/where-is-bmsb/state-by-state/ webcite
• [3]Fogain R, Graff S: First records of the invasive pest, Halyomorpha halys (Hemiptera: Pentatomidae) in Ontario and Quebec. J Entomol Soc Ontario 2011, 142:45.
• [4]Rabitsch W: Alien true bugs of Europe (Insecta:Hemiptera:Heteroptera). Zootaxa 2008, 1827:1-44.
• [5]Wermelinger B, Wyniger D, Forster B: First records of an invasive bug in Europe: Halyomorpha halys Stål (Heteroptera:Pentatomidae), a new pest on woody ornamentals and fruit trees? Mitteilungen der Schweizerischen Entomologischen Gesellschaft 2008, 81:1-8.
• [6]Wyniger D, Kment P: Key for the separation of Halyomorpha halys (Stål) from similar-appearing pentatomids (Insecta: Heteroptera: Pentatomidae) occurring in Central Europe, with new Swiss records. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 2010, 83:261-270.
• [7]Panizzi AR, McPherson JE, James DG, Javahery M, McPherson BA: Stink bugs (Pentatomidae). In Heteroptera of Economic Importance. Edited by Panizi CW Sa AR. New York, NY, USA: CRC; 2000:828.
• [8]Zhu G, Bu W, Gao Y, Liu G: Potential geographic distribution of brown marmorated stink bug invasion (Halyomorpha halys). PLoS One 2012, 7:e31246.
• [9]Nielson AL, Shearer PW, Hamilton GC: Toxicity of insecticides to Halyomorpha halys (Hemiptera: Pentatomidae) using glass-vial bioassays. J Econ Entomol 2008, 101:1439-1442.
• [10]General information on the Brown Marmorated Stink Bughttp://www.epa.gov/pesticides/controlling/stinkbugs/#epa webcite
• [11]Nielson AL, Hamilton GC: Seasonal occurence and impact of Halyomorpha halys (Hemiptera: Pentatomidae) in tree fruit. J Econ Entomol 2009, 102:1133-1140.
• [12]Leskey TC, Hamilton GC, Nielsen AL, Polk DF, Rodriguez-Saona C, Bergh JC, Herbert DA, Kuhar TP, Pfeiffer D, Dively GP, Hooks CRR, Raupp MJ, Shrewsbury PM, Krawczyk G, Shearer PW, Whalen J, Koplinka-Loehr C, Myers E, Inkley D, Hoelmer KA, Lee D, Wright SE: Pest Status of the Brown Marmorated Stink Bug, Halyomorpha halys in the USA. Outlooks Pest Manag 2012, 23:218-226.
• [13]Harris A: Halyomorpha halys (Hemiptera: Pentatomidae) and Protaetia brevitarsis (Coleoptera: Scarabaeidae: Cetoniinae) intercepted in Dunedin. Weta 2010, 40:42-44.
• [14]Jones JR, Lambin PL: New county and state records for Tennessee of an exotic pest, Halyomorpha halys (Hemiptera: Pentatomidae), with potential economic and ecological implications. Fla Entomol 2009, 92:177-179.
• [15]Rasko DA, Webster DR, Sahl JW, Bashir A, Boisen N, Scheutz F, Paxinos EE, Sebra R, Chin CS, Iliopoulos D, Klammer A, Peluso P, Lee L, Kislyuk AO, Bullard J, Kasarskis A, Wang S, Eid J, Rank D, Redman JC, Steyert SR, Frimodt-Møller J, Struve C, Petersen AM, Krogfelt KA, Nataro JP, Schadt EE, Waldor MK: Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N Engl J Med 2011, 365:709-717.
• [16]Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A: Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29:644-652.
• [17]Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, Macmanes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, Leduc RD, Friedman N, Regev A: De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 2013, 8:1494-1512.
• [18]The International Aphid Genomics Consortium: Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol 2010, 8:e1000313.
• [19]Zhu L, Zhang Y, Guo W, Xu XJ, Wang Q: De novo assembly and characterization of Sophora japonica transcriptome using RNA-seq. Biomed Res Int 2014, 2014:750961.
• [20]Wei L, Li S, Liu S, He A, Wang D, Wang J, Tang Y, Wu X: Transcriptome analysis of Houttuynia cordata Thunb. by Illumina paired-end RNA sequencing and SSR marker discovery. PLoS One 2014, 9:e84105.
• [21]Zhu JY, Zhao N, Yang B: Global transcriptome profiling of the pine shoot beetle, Tomicus yunnanensis (Coleoptera: Scolytinae). PLoS One 2012, 7:e32291.
• [22]Wang XW, Luan JB, Li JM, Bao YY, Zhang CX, Liu SS: De novo characterization of a whitefly transcriptome and analysis of its gene expression during development. BMC Genomics 2010, 11:400. BioMed Central Full Text
• [23]Li H, Jiang W, Zhang Z, Xing Y, Li F: Transcriptome analysis and screening for potential target genes for RNAi-mediated pest control of the beet armyworm. PLoS One 2013, 8:e65931.
• [24]Kuhar TP, Doughty H, Kamminga K, Lillison L: Bioassay Evaluation of Insecticides Using a Bean Dip Bioassay for Control of Brown Marmorated Stink Bug, 2011. Arthropod Manag Tests 2012, 37:L1.
• [25]Bergmann EJ, Raupp MJ: Efficacy of common ready to use insecticides against Halyomorpha halys (Hemiptera: Pentatomidae). Fla Entomol 2014. in press
• [26]Riley DR, Sieber KB, Robinson KM, White JR, Ganesan A, Nourbakhsh S, Dunning Hotopp JC: Bacteria-human somatic cell lateral gene transfer is enriched in cancer samples. PLoS Comput Biol 2013, 9:e1003107.
• [27]Kobayashi H, Kawasaki K, Takeishi K, Noda H: Symbiont of the stink bug Plautia stali synthesizes rough-type lipopolysaccharide. Microbiol Res 2011, 167:48-54.
• [28]Taylor CM, Coffey PL, Delay BD, Dively GP: The Importance of Gut Symbionts in the Development of the Brown Marmorated Stink Bug, Halyomorpha halys (Stal). PLoS One 2014, 9:e90312.
• [29]Schmitz-Esser S, Tischler P, Arnold R, Montanaro J, Wagner M, Rattei T, Horn M: The genome of the amoeba symbiont "Candidatus Amoebophilus asiaticus" reveals common mechanisms for host cell interaction among amoeba-associated bacteria. J Bacteriol 2010, 192:1045-1057.
• [30]Sabree ZL, Kambhampati S, Moran NA: Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. Proc Natl Acad Sci U S A 2009, 106:19521-19526.
• [31]Wu D, Daugherty SC, Van Aken SE, Pai GH, Watkins KL, Khouri H, Tallon LJ, Zaborsky JM, Dunbar HE, Tran PL, Moran NA, Eisen JA: Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol 2006, 4:e188.
• [32]Penz T, Schmitz-Esser S, Kelly SE, Cass BN, Muller A, Woyke T, Malfatti SA, Hunter MS, Horn M: Comparative genomics suggests an independent origin of cytoplasmic incompatibility in Cardinium hertigii. PLoS Genet 2012, 8:e1003012.
• [33]Baldo L: Dunning Hotopp JC, Jolley KA, Bordenstein SR, Biber SA, Choudhury RR, Hayashi C, Maiden MC, Tettelin H, Werren JH: Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microbiol 2006, 72:7098-7110.
• [34]Werren JH, Richards S, Desjardins CA, Niehuis O, Gadau J, Colbourne JK, Beukeboom LW, Desplan C, Elsik CG, Grimmelikhuijzen CJ, Kitts P, Lynch JA, Murphy T, Oliveira DC, Smith CD, van de Zande L, Worley KC, Zdobnov EM, Aerts M, Albert S, Anaya VH, Anzola JM, Barchuk AR, Behura SK, Bera AN, Berenbaum MR, Bertossa RC, Bitondi MM, Bordenstein SR, Bork P, et al.: Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 2010, 327:343-348.
• [35]Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
• [36]Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680.
• [37]Stamatakis A, Ludwig T, Meier H: RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 2005, 21:456-463.
• [38]Nikoh N, McCutcheon JP, Kudo T, Miyagishima SY, Moran NA, Nakabachi A: Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its host. PLoS Genet 2010, 6:e1000827.
• [39]Nikoh N, Nakabachi A: Aphids acquired symbiotic genes via lateral gene transfer. BMC Biol 2009, 7:12. BioMed Central Full Text
• [40]Katoh K, Kuma K, Toh H, Miyata T: MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 2005, 33:511-518.
• [41]Cryan JR, Urban JM: Higher-level phylogeny of the insect order Hemiptera: is Auchenorrhyncha really paraphyletic? Syst Entomol 2012, 37:7-21.
• [42]Tulin S, Aguiar D, Istrail S, Smith J: A quantitative reference transcriptome for Nematostella vectensis early embryonic development: a pipeline for de novo assembly in emerging model systems. Evodevo 2013, 4:16. BioMed Central Full Text
• [43]Gutierrez-Gonzalez JJ, Tu ZJ, Garvin DF: Analysis and annotation of the hexaploid oat seed transcriptome. BMC Genomics 2013, 14:471. BioMed Central Full Text
• [44]Acuna R, Padilla BE, Florez-Ramos CP, Rubio JD, Herrera JC, Benavides P, Lee SJ, Yeats TH, Egan AN, Doyle JJ, Rose JK: Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proc Natl Acad Sci U S A 2012, 109:4197-4202.
• [45]Brown Marmorated Stink Bug as a pest of corn and soybeanshttp://ento.psu.edu/extension/factsheets/brown-marmorated-stink-bug-as-a-pest-of-corn-and-soybeans webcite
• [46]Zhang D, de Souza RF, Anantharaman V, Iyer LM, Aravind L: Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol Direct 2012, 7:18. BioMed Central Full Text
• [47]Korochkina S, Barreau C, Pradel G, Jeffery E, Li J, Natarajan R, Shabanowitz J, Hunt D, Frevert U, Vernick KD: A mosquito-specific protein family includes candidate receptors for malaria sporozoite invasion of salivary glands. Cell Microbiol 2006, 8:163-175.
• [48]Woolfit M, Iturbe-Ormaetxe I, McGraw EA, O'Neill SL: An ancient horizontal gene transfer between mosquito and the endosymbiotic bacterium Wolbachia pipientis. Mol Biol Evol 2009, 26:367-374.
• [49]Klasson L, Kambris Z, Cook PE, Walker T, Sinkins SP: Horizontal gene transfer between Wolbachia and the mosquito Aedes aegypti. BMC Genomics 2009, 10:33. BioMed Central Full Text
• [50]Futahashi R, Tanaka K, Tanahashi M, Nikoh N, Kikuchi Y, Lee BL, Fukatsu T: Gene expression in gut symbiotic organ of stinkbug affected by extracellular bacterial symbiont. PLoS One 2013, 8:e64557.
• [51]Rannikko K, Ortutay C, Vihinen M: Immunity genes and their orthologs: a multi-species database. Int Immunol 2007, 19:1361-1370.
• [52]Gerardo NM, Altincicek B, Anselme C, Atamian H, Barribeau SM, de Vos M, Duncan EJ, Evans JD, Gabaldon T, Ghanim M, Heddi A, Kaloshian I, Latorre A, Moya A, Nakabachi A, Parker BJ, Pérez-Brocal V, Pignatelli M, Rahbé Y, Ramsey JS, Spragg CJ, Tamames J, Tamarit D, Tamborindeguy C, Vincent-Monegat C, Vilcinskas A: Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol 2010, 11:R21. BioMed Central Full Text
• [53]Altincicek B, Gross J, Vilcinskas A: Wounding-mediated gene expression and accelerated viviparous reproduction of the pea aphid Acyrthosiphon pisum. Insect Mol Biol 2008, 17:711-716.
• [54]Langmead B, Salzberg SL: Fast gapped-read alignment with Bowtie 2. Nat Methods 2012, 9:357-359.
• [55]Picardhttp://picard.sourceforge.net webcite
• [56]Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R: The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078-2079.
• [57]Galens K, Orvis J, Daugherty S, Creasy HH, Angiuoli S, White O, Wortman J, Mahurkar A, Giglio MG: The IGS Standard Operating Procedure for Automated Prokaryotic Annotation. Stand Genomic Sci 2011, 4:244-251.
• [58]Suzek BE, Huang H, McGarvey P, Mazumder R, Wu CH: UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics 2007, 23:1282-1288.
• [59]Rice P, Longden I, Bleasby A: EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 2000, 16:276-277.
• [60]Haft DH, Selengut JD, White O: The TIGRFAMs database of protein families. Nucleic Acids Res 2003, 31:371-373.
• [61]Haft DH, Selengut JD, Richter RA, Harkins D, Basu MK, Beck E: TIGRFAMs and Genome Properties in 2013. Nucleic Acids Res 2013, 41:D387-D395.
• [62]Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M: Pfam: the protein families database. Nucleic Acids Res 2014, 42:D222-D230.
• [63]Eddy SR: Accelerated Profile HMM Searches. PLoS Comput Biol 2011, 7:e1002195.
• [64]Consortium UP: Activities at the Universal Protein Resource (UniProt). Nucleic Acids Res 2014, 42:D191-D198.
• [65]Trapnell C, Pachter L, Salzberg SL: TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111.
• [66]Dunning Hotopp JC, Grifantini R, Kumar N, Tzeng YL, Fouts D, Frigimelica E, Draghi M, Giuliani MM, Rappuoli R, Stephens DS, Grandi G, Tettelin H: Comparative genomics of Neisseria meningitidis: core genome, islands of horizontal transfer and pathogen-specific genes. Microbiology 2006, 152:3733-3749.
• [67]Dunning Hotopp JC, Clark ME, Oliveira DC, Foster JM, Fischer P, Torres MC, Giebel JD, Kumar N, Ishmael N, Wang S, Ingram J, Nene RV, Shepard J, Tomkins J, Richards S, Spiro DJ, Ghedin E, Slatko BE, Tettelin H, Werren JH: Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 2007, 317:1753-1756.