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Sequencing of Tuta absoluta genome to develop SNP genotyping assays for species identification

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Abstract

Tuta absoluta is one of the most devastating pests of fresh market and processing tomatoes. Native to South America, its detection was confined to that continent until 2006 when it was identified in Spain. It has now spread to almost every continent, threatening countries whose economies rely heavily on tomatoes. This insect causes damage to all developmental stages of its host plant, leading to crop losses as high as 80–100%. Although T. absoluta has yet to be found in the USA and China, which makes up a large portion of the tomato production in the world, computer models project a high likelihood of invasion. To halt the continued spread of T. absoluta and limit economic loss associated with tomato supply chain, it is necessary to develop accurate and efficient methods to identify T. absoluta and strengthen surveillance programs. Current identification of T. absoluta relies on examination of morphology and assessment of host plant damage, which are difficult to differentiate from that of native tomato pests. To address this need, we sequenced the genomes of T. absoluta and two closely related Gelechiidae, Keiferia lycopersicella and Phthorimaea operculella, and developed a bioinformatic pipeline to design a panel of 21-SNP markers for species identification. The accuracy of the SNP panel was validated in a multiplex format using the iPLEX chemistry of Agena MassARRAY system. Finally, the new T. absoluta genomic resources we generated can be leveraged to study T. absoluta biology and develop species-specific management strategies.

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Data availability

All genome sequencing data generated from this study have been deposited to BioProject accession number PRJNA512383 in the NCBI BioProject database (https://www.ncbi.nlm.nih.gov/bioproject/). The Whole Genome Shotgun project of T. absoluta has been deposited at DDBJ/ENA/GenBank under the accession SNMR00000000. The version described in this paper is version SNMR01000000.

References

  • Ajamma YU, Mararo E, Omondi D et al (2016) Rapid and high throughput molecular identification of diverse mosquito species by high resolution melting analysis. F1000Research 5:1949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arnó J, Oveja MF, Gabarra R (2018) Selection of flowering plants to enhance the biological control of Tuta absoluta using parasitoids. Biol Control 122:41–50

    Article  Google Scholar 

  • Bahamondes LA, Mallea AL (1969) Biología en Mendoza de Scrobipalpula absoluta (Meyrick) Polvony (Lepidoptera: Gelechiidae), especie nueva para la República Argentina. Revista de la Facultad de Ciencias Agrarias 15:96–104

    Google Scholar 

  • Bawin T, Dujeu D, DeBaker L et al (2015) Could alternative solanaceous hosts act as refuges for the tomato leafminer, Tuta absoluta? Arthropod Plant Interact 9:425–435

    Article  Google Scholar 

  • Bettaibi A, Mezghani-Khemakhem M, Bouktila D et al (2012) Genetic variability of the tomato leaf miner (Tuta absoluta Meyrick; Lepidoptera: Gelechiidae) in Tunisia, inferred from RAPD-PCR. Chilean J Agric Res 72:212–216

    Article  Google Scholar 

  • Biondi A, Narciso R, Guedes C et al (2018) Ecology, worldwide spread, and management of the invasive South American tomato pinworm, Tuta absoluta: past, present, and future. Ann Rev Entomol 63:239–258

    Article  CAS  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • CABI (Centre for Agriculture and Bioscience International) (2016) Tuta absoluta. CABI website https://www.cabi.org/isc/datasheet/49260. Accessed 20 Oct 2018

  • Camargo RA, Herai RH, Santos LN et al (2015) De novo transcriptome assembly and analysis to identify potential gene targets for RNAi-mediated control of the tomato leafminer (Tuta absoluta). BMC Genom 16:635

    Article  CAS  Google Scholar 

  • Camargo RA, Barbosa GO, Possignolo IP et al (2016) RNA interference as a gene silencing tool to control Tuta absoluta in tomato (Solanum lycopersicum). Peer J 4:e2673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campos MR, Biondi A, Adiga A (2017) From the Western Palaearctic region to beyond: Tuta absoluta ten years after invading Europe. J Pest Sci 90:787–796

    Article  Google Scholar 

  • Cifuentes D, Chynoweth R, Bielza P (2011) Genetic study of Mediterranean and South American populations of tomato leafminer Tuta absoluta (Povolny, 1994) (Lepidoptera: Gelechiidae) using ribosomal and mitochondrial markers. Pest Manag Sci 67:1155–1162

    CAS  PubMed  Google Scholar 

  • Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5:e11147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Desneux N, Wajberg E, Wyckhuys K et al (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83:197–215

    Article  Google Scholar 

  • Desneux N, Luna M, Guillemaud T et al (2011) The invasive South America tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. J Pest Sci 84:403–408

    Article  Google Scholar 

  • Dhami MK, Kumarasinghe L (2014) A HRM real-time PCR assay for rapid and specific identification of the emerging pest Spotted-Wing Drosophila (Drosophila suzukii). PLoS ONE 9:e98934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhami MK, Dsouza M, Waite DW et al (2016) Real-time PCR assay for the identification of the brown marmorated stink bug (Halyomorpha halys). Front Mol Biosci 3:5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dobin A, Davis CA, Schlesinger F et al (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15–21

    Article  CAS  PubMed  Google Scholar 

  • Đurić Z, Delić D, Hrnčić S et al (2014) Distribution and molecular identification of Tuta absoluta (Meyrick, 1917) (Lepidoptera, Gelechiidae) populations in Bosnia and Herzegovina and Montenegro. Pol J Entomol 83:121–129

    Article  Google Scholar 

  • EPPO Global Database (2019) Tecia solanivora (TECASO). https://gd.eppo.int/taxon/TECASO/distribution. Accessed 15 Feb 2019

  • FAOSTAT (Food Agric. Org. U. N.) (2017) FAOSTAT statistics database. Rome, Italy. http://www.fao.org/faostat. Accessed 20 Oct 2018

  • Gabriel S, Ziaugra L, Tabbaa D (2009) SNP genotyping using the Sequenom MassARRAY iPLEX platform. Curr Protoc Hum Genet 2:1–18

    Google Scholar 

  • Gaskill DAR (2013) Tuta absoluta and the tomato commodity survey. Florida CAPS annual workshop and meeting presentation. https://www.freshfromflorida.com/Divisions-Offices/Plant-Industry/Bureaus-and-Services/CAPS/CAPS-Presentations-and-Outreach. Accessed 15 Feb 2019

  • Guillemaud T, Blin A, Le Goff I et al (2015) The tomato borer, Tuta absoluta, invading the Mediterranean Basin, originates from a single introduction from Central Chile. Sci Rep 5:8371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han P, Zhang YN, Lu ZZ et al (2018) Are we ready for the invasion of Tuta absoluta? Unanswered key questions for elaborating an integrated pest management package. Entomol Gen 38:113–125

    Article  Google Scholar 

  • Han P, Bayram Y, Shaltiel-Harpez L et al (2019) Tuta absoluta continues to disperse in Asia: damage, ongoing management and future challenges. J Pest Sci. https://doi.org/10.1007/s10340-018-1062-1

    Article  Google Scholar 

  • Katoh K, Standley D (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Bio Evol 30:772–780

    Article  CAS  Google Scholar 

  • Kopylova E, Noé L, Touzet H (2012) SortMeRNA: fast and accurate filtering of ribosomal RNAs in meta-transcriptomic data. Bioinformatics 28:3211–3217

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Brambila J (2012) A new species of the genus Sinoe (Lepidoptera: Gelechiidae: Litini) from Florida. Fla Entomol 95:873–876

    Article  Google Scholar 

  • Lee Y, Marsden CD, Norris LC et al (2013) Spatiotemporal dynamics of gene flow and hybrid fitness between the M and S forms of the malaria mosquito, Anopheles gambiae. Proc Natl Acad Sci USA 110:19854–19859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee Y, Marsden CD, Nieman CC et al (2014) A new multiplex SNP genotyping assay for detecting hybridization and introgression between the M and S molecular forms of Anopheles gambiae. Mol Ecol Resour 14:297–305

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, Weakley AM, Nieman CC et al (2015) A multi-detection assay for malaria transmitting mosquitoes. J Vis Exp 96:e52385

    Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Linck H, Kruger E, Reineke A (2017) A multiplex TaqMan aPCR assay for sensitive and rapid detection of phytoplasmas infecting Rubus species. PLoS ONE 12:e0177808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo R, Liu B, Xie Y et al (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1:18

    Article  PubMed  PubMed Central  Google Scholar 

  • Mansour R, Brevault T, Chailleux A et al (2018) Occurrence, biology, natural enemies and management of Tuta absoluta in Africa. Entomol Gen 38:83–112

    Article  Google Scholar 

  • Marçais G, Kingsford C (2011) A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27:764–770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michalak PS (2011) New pest guidelines for tomato leaf miner (Tuta absoluta). http://www.aphis.usda.gov/import_export/plants/manuals/emergency/index.shtml. Accessed 20 Oct 2018

  • Mohamed ESI, Mahmoud MEE, Elhaj MAM (2015) Host plants record for tomato leaf miner Tuta absoluta (Meyrick) in Sudan. Bull OEPP/EPPO 45:108–111

    Article  Google Scholar 

  • Mutamiswa R, Machekano H, Nyamukondiwa C (2017) First report of tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), in Botswana. Agric Food Secur 6:49

    Article  Google Scholar 

  • Negi S, Sharma PL, Sharma KC (2018) Effect of host plants on developmental and population parameters of invasive leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Phytoparasitica 46:213–221

    Article  Google Scholar 

  • Nieman CC, Yamasaki Y, Collier TC et al (2015) A DNA extraction protocol for improved DNA yield from individual mosquitoes. F1000Research 4:1314

    Article  PubMed  PubMed Central  Google Scholar 

  • Pereyra P, Sanchez N (2006) Effect of two solanaceous host plants on development and population parameters of the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotrop Entomol 35:671–676

    Article  PubMed  Google Scholar 

  • Povolny D (1975) On three neotropical species of Gnorimoschemini (Lepidoptera, Gelechiidae) mining Solanaceae. Acta Univ Agric 23:379–393

    Google Scholar 

  • Povolny D (1994) Gnorimoschemini of southern South America VI: identification keys, checklist of Neotropical taxa and general considerations (Insecta, Lepidoptera, Gelechiidae). Steenstrupia 20:1–42

    Google Scholar 

  • Simao FA, Waterhouse RM, Ioannidis P et al (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–3212

    Article  CAS  PubMed  Google Scholar 

  • Sint D, Sporleder M, Wallinger C et al (2016) A two-dimensional pooling approach towards efficient detection of parasitoid and pathogen DNA at low infestation rates. Methods Ecol Evol 7:1548–1557

    Article  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teeter KC, Thibodeau LM, Gompert Z et al (2010) The variable genomic architecture of isolation between hybridizing species of house mice. Evolution 64:472–485

    Article  CAS  PubMed  Google Scholar 

  • Tonnang HEZ, Mohamed SF, Khamis F (2015) Identification and risk assessment for worldwide invasion and spread of Tuta absoluta with a focus on sub-Saharan Africa: implications for phytosanitary measures and management. PLoS ONE 10:e0135283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • USDA (United States Department of Agriculture) (2011) New pest response guidelines: tomato leafminer (Tuta absoluta). USDA Animal and Plant Health and Inspection Service website. https://www.aphis.usda.gov/import_export/plants/manuals/emergency/downloads/Tuta-absoluta.pdf. Accessed 20 Oct 2018

  • Vurture GW, Sedlazeck FJ, Nattestad M et al (2017) GenomeScope: fast reference-free genome profiling from short reads. Bioinformatics 33:2202–2220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamasaki YK, Nieman CC, Chang AN (2016) Improved tools for genomic DNA library construction of small insects. F1000Research 5:211

    Google Scholar 

  • Zhang Z, Schwartz S, Wagner L et al (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214

    Article  CAS  PubMed  Google Scholar 

  • Zhang T, Wang YJ, Guo W (2016) DNA barcoding, species–species PCR and real-time PCR techniques for the identification of six Tribolium pests of stored products. Sci Rep 6:28494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank Dr. Yannery Gómez Bonilla (Investigator, Entomologia, INTA, Costa Rica) for the samples from Costa Rica, Dr. Phil Stansly (Professor, University of Florida, USA) for the K. lycopersicella samples, and David Haviland (Entomology and IPM Farm Advisor, University of California Cooperative Extension, Bakersfield, CA, USA) for the P. operculella samples.

Funding

This project was supported by the Specialty Crop Block Program at the USA Department of Agriculture (USDA) through Grant 14-SCBGP-CA-006 to KG, FGZ, and JCC and USDA NIFA CA-D-ENM-2150-H awarded to JCC. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the USDA. JA and NA are funded by CERCA Programme (Generalitat de Catalunya).

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Authors and Affiliations

  1. Department of Entomology and Nematology, University of California, Davis, Davis, USA

    Christine A. Tabuloc, Kyle M. Lewald, William R. Conner, Ernest K. Lee, Frank G. Zalom & Joanna C. Chiu

  2. Department of Pathology, Microbiology and Immunology, School of Veterinary Medicine, University of California, Davis, Davis, USA

    Yoosook Lee

  3. Contained Research Facility, University of California, Davis, Davis, USA

    Alexander B. Cain & Kristine E. Godfrey

  4. IRTA (Institute of Agrifood Research and Technology), Cabrils, Barcelona, Spain

    Judit Arnó & Nuria Agustí

  5. Department of Crop Protection, Universidade Federal de Santa Maria (UFSM), Santa Maria, Rio Grande do Sul, Brazil

    Clerison R. Perini & Jerson C. Guedes

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  1. Christine A. Tabuloc
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  2. Kyle M. Lewald
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Correspondence to Joanna C. Chiu.

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Tabuloc, C.A., Lewald, K.M., Conner, W.R. et al. Sequencing of Tuta absoluta genome to develop SNP genotyping assays for species identification. J Pest Sci 92, 1397–1407 (2019). https://doi.org/10.1007/s10340-019-01116-6

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