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A simple molecular identification method of the Thrips tabaci (Thysanoptera: Thripidae) cryptic species complex

Published online by Cambridge University Press:  09 December 2019

Péter Farkas ,
Zsuzsanna György ,
Annamária Tóth ,
Annamária Sojnóczki  and
József Fail Open the ORCID record for József Fail [Opens in a new window]
Péter Farkas
Affiliation:
Department of Entomology, Faculty of Horticultural Science, Szent István University, Budapest, Hungary
Zsuzsanna György
Affiliation:
Department of Genetics and Plant Breeding, Faculty of Horticultural Science, Szent István University, Budapest, Hungary
Annamária Tóth
Affiliation:
Department of Plant Pathology, Faculty of Horticultural Science, Szent István University, Budapest, Hungary
Annamária Sojnóczki
Affiliation:
Department of Entomology, Faculty of Horticultural Science, Szent István University, Budapest, Hungary
József Fail*
Affiliation:
Department of Entomology, Faculty of Horticultural Science, Szent István University, Budapest, Hungary
*
Author for correspondence: József Fail, Email: [email protected]
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Abstract

The onion thrips (Thrips tabaci Lindeman, 1889) is a key pest of a wide range of crops because of its ecological attributes such as polyphagy, high reproduction rate, ability to transmit tospoviruses and resistance to insecticides. Recent studies revealed that T. tabaci is a cryptic species complex and it has three lineages (leek-associated arrhenotokous L1-biotype, leek-associated thelytokous L2-biotype and tobacco-associated arrhenotokous T-biotype), however, the adults remain indistinguishable. T. tabaci individuals were collected from different locations of Hungary to create laboratory colonies from each biotypes. Mitochondrial COI (mtCOI) region was sequenced from morphologically identified individuals. After sequence analysis SNPs were identified and used for CAPS marker development, which were suitable for distinguishing the three T. tabaci lineages. Genetic analysis of the T. tabaci species complex based on mtCOI gene confirmed the three well-known biotypes (L1, L2, T) and a new biotype because the new molecular evidence presented in this study suggests T-biotype of T. tabaci forming two distinct (sub)clades (T1 and T2). This genetic finding indicates that the genetic variability of T. tabaci populations is still not fully mapped. We validated our developed marker on thrips individuals from our thrips colonies. The results demonstrated that the new marker effectively identifies the different T. tabaci biotypes. We believe that our reliable genotyping method will be useful in further studies focusing on T. tabaci biotypes and in pest management by scanning the composition of sympatric T. tabaci populations.

Keywords

CAPS markerCOIcryptic species complexidentificationmitochondrial DNAgenetic analysisThrips tabaci
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 3 , June 2020 , pp. 397 - 405
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Copyright
Copyright © Cambridge University Press 2019

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References

Altschul, SF, Gish, W, Miller, W, Myers, EW and Lipman, DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410. https://doi.org/10.1006/jmbi.1990.9999.CrossRefGoogle ScholarPubMed
Asokan, R, Krishna Kumar, N, Kumar, V and Ranganath, H (2007) Molecular differences in the mitochondrial cytochrome oxidase I (mtCOI) gene and development of a species-specific marker for onion thrips, Thrips tabaci Lindeman, and melon thrips, T. palmi karny (Thysanoptera: Thripidae), vectors of tospoviruses (Bunyaviridae). Bulletin of Entomological Research 97, 461–470. https://doi.org/10.1017/S0007485307005147.CrossRefGoogle Scholar
Bandelt, H, Forster, P and Röhl, A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16(1), 37–48. https://doi:10.1093/oxfordjournals.molbev.a026036.CrossRefGoogle ScholarPubMed
Brunner, PC, Fleming, C and Frey, JE (2002) A molecular identification key for economically important thrips species (Thysanoptera:Thripidae) using direct sequencing and a PCR-RFLP-based approach. Agricultural and Foresst Entomology 4, 127–136. https://doi.org/10.1046/j.1461-9563.2002.00132.x.CrossRefGoogle Scholar
Brunner, PC, Chatzivassiliou, EK, Katis, NI and Frey, JE (2004) Host-associated genetic differentiation in Thrips tabaci (Insecta; Thysanoptera), as determined from mtDNA sequence data. Heredity 93, 364–370. https://dx.doi.org/10.1038/sj.hdy.6800512.CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) JModeltest2: more models, new heuristics and high-performance computing. Nature Methods 9(8), 772. https://doi: 10.1038/nmeth.2109.CrossRefGoogle Scholar
De Barro, PJ and Driver, F (1997) Use of RAPD PCR to distinguish the B biotype from other biotypes of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Australian Journal of Entomology 36(2), 149–152. https://doi: 10.1111/j.1440-6055.1997.tb01447.x.CrossRefGoogle Scholar
Diaz-Montano, J, Fuchs, M, Nault, BA, Fail, J and Shelton, AM (2011) Onion thrips (Thysanoptera: Thripidae): a global pest of increasing concern in onion. Journal of Economic Entomology 104, 1–13. https://doi.org/10.1603/EC10269.CrossRefGoogle ScholarPubMed
Farris, RE, Ruiz-Arce, R, Ciomperlik, M, Vasquez, JD and DeLeón, R (2010) Development of a ribosomal DNA ITS2 marker for the identification of the thrips, Scirtothrips dorsalis. Journal of Insect Science 10, 1–15. https://dx.doi.org/10.1673/031.010.2601CrossRefGoogle ScholarPubMed
Fekrat, L, Manzari, S and Shishehbor, P (2014) Morphometric and molecular variation in Thrips tabaci Lindeman (ThysanopterahyThripidae) populations on onion and tobacco in Iran. Journal of Agricultural Science and Technology 16, 1505–1516. https://doi: 10.1111/j.1558-5646.1985.tb00420.x.Google Scholar
Felsenstein, J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791. https://doi: 10.1111/j.1558-5646.1985.tb00420.x.CrossRefGoogle ScholarPubMed
Frey, JE and Frey, B (2004) Origin of intra-individual variation in PCR amplified mitochondrial cytochrome oxidase I of Thrips tabaci (Thysanoptera: Thripidae): mitochondrial heteroplasmy or nuclear integration. Hereditas 140, 92–98. https://doi: 10.1111/j.1601-5223.2004.01748.x.CrossRefGoogle ScholarPubMed
Gawande, SJ, Anandhan, S, Ingle, AA and Jacobson, A (2017) Heteroplasmy due to coexistence of mtCOI haplotypes from different lineages of the Thrips tabaci cryptic species group. Bulletin of Entomological Research 107(4), 534–542. https://10.1017/S0007485317000025.CrossRefGoogle ScholarPubMed
Hasegawa, M, Kishino, H and Yano, T (1985) Dating the human-ape split by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160–174.CrossRefGoogle Scholar
Jacobson, AL, Booth, W, Vargo, EL and Kennedy, GG (2013) Thrips tabaci population genetic structure and polyploidy in relation to competency as a vector of Tomato Spotted Wilt Virus. PLoS ONE 8(1), e54484. https://doi.org/10.1371/journal.pone.0054484.CrossRefGoogle ScholarPubMed
Jacobson, AL, Nault, BA, Vargo, EL and Kennedy, GG (2016) Restricted gene flow among lineages of Thrips tabaci supports genetic divergence among cryptic species groups. PLoS ONE 11(9), e0163882. https://doi:10.1371/journal.pone.0163882CrossRefGoogle Scholar
Jenser, G and Szénási, Á (2004) Review of the biology and vector capability of Thrips tabaci Lindeman (Thysanoptera: Thripidae). Acta Phytopathologica et Entomologica Hungarica 39, 137–155.CrossRefGoogle Scholar
Jenser, G, Szénási, A, Törjek, O, Gyulai, G, Kiss, E, Heszky, L and Fail, J (2001) Molecular polymorphism between population of Thrips tabaci Lindeman (Thysanoptera: Thripidae) propagating on tobacco and onion. Acta Phytopathologica et Entomologica Hungarica 36, 365–368.Google Scholar
Klein, M and Gafni, R (1996) Morphological and molecular variations in thrips populations collected on onion plants in Israel. Folia Entomologica Hungarica 57, 57–59.Google Scholar
Kobayashi, K and Hasegawa, E (2012) Discrimination of reproductive forms of Thrips tabaci (Thysanoptera: Thripidae) by PCR with sequence specific primers. Journal of Economic Entomology 105(2), 555–559. https://doi.org/10.1603/EC11320CrossRefGoogle ScholarPubMed
Kobayashi, K, Yoshimura, J and Hasegawa, E (2013) Coexistence of sexual individuals and genetically isolated asexual counterparts in a thrips. Scientific Report 3, 3286. https://doi.org/10.1038/srep03286.CrossRefGoogle Scholar
Kraus, M, Schreiter, G and Moritz, G (1999) Molecular genetic studies of thrips species. In Vierbergen G and Tunc I (eds), Proceedings of the 6th International Symposium on Thysanoptera, 27 April–1 May 1998, Akdeniz University, Antalya, Turkey 1999. 77–80. Orkun Ozan Medya, Hizmetleri A.S. Antalya, Turkey.Google Scholar
Lewis, T (1973) Thrips-Their Biology, Ecology and Economic Importance. London: New York Academic Press.Google Scholar
Li, X-W, Wang, P, Fail, J and Shelton, AM (2015) Detection of gene flow from sexual to asexual lineages in Thrips tabaci (Thysanoptera: Thripidae). PLoS ONE 10(9), e0138353. https://doi.org/10.1371/journal.pone.0138353.CrossRefGoogle Scholar
Librado, P and Rozas, J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics (Oxford, England) 25, 1451–1452. https://doi.org/10.1093/bioinformatics/btp187.CrossRefGoogle ScholarPubMed
Mehle, S and Trdan, S (2012) Traditional and modern methods for the identification of thrips (Thysanoptera) species. Journal of Pest Science 85(2), 179–190. https://10.1007/s10340-012-0423-4.CrossRefGoogle Scholar
Moritz, G (1997) Structure, growth and development. In Lewis, T (ed.), Thrips as Crop Pests. New York, NY: CAB International, pp. 15–64.Google Scholar
Moritz, G, Morris, D and Mound, LA (2001) ThripsID – Pest Thrips of the World. An Interactive Identification and Information System. CD-ROM published by ACIAR, Australia. CSIRO Publishing, Melbourne, Australia.Google Scholar
Moritz, G, Paulsen, M, Delker, C, Picl, S and Kumm, S (2002) Identification of thrips using ITS-RFLP analysis. In Marullo, R and Mound, LA (eds), Thrips and Tospoviruses: Proceedings of the 7th International Symposium on Thysanoptera. Canberra: Australian National Insect Collection CSIRO, pp. 365–367.Google Scholar
Mound, LA and Kibby, G (1998) Thysanoptera. An Identification Guide, 2nd Edn. Wallingford, UK: CAB International.Google Scholar
Nault, BA, Shelton, AM, Gangloff-Kaufamm, JL, Clark, ME, Werren, JL, Cabrera-LA Rosa, JC and Kennedy, GG (2006) Reproductive modes in onion thrips (Thysanoptera: Thripidae) populations from New York onion fields. Environmental Entomology 35, 1264–1271. https://doi.org/10.1093/ee/35.5.1264.CrossRefGoogle Scholar
Rugman-Jones, PF, Hoddle, MS, Mound, LA and Stouthamer, R (2006) Molecular identification key for pest species of Scirtothrips (thysanoptera: Thripidae). Journal of Economic Entomology 99(5), 1813–1819. https://doi.org/10.1093/jee/99.5.1813.CrossRefGoogle Scholar
Rychlik, W (2007) OLIGO 7 primer analysis software. In Yuryev, A (eds), PCR Primer Design. Methods in Molecular Biology™, vol. 402. Humana Press, pp. 35–59. https://doi.org/10.1007.CrossRefGoogle Scholar
Sabahi, S, Fekrat, L and Zakiaghl, M (2017) A simple and rapid molecular method for simultaneous identification of four economically important thrips species. Journal of Agricultural Science and Technology 19(6), 1279–1290.Google Scholar
Shelton, AM, Plate, J and Chen, M (2008) Advances in control of onion thrips (Thysanoptera: Thripidae) in cabbage. Journal of Economic Entomology 101(2), 438–443. https://doi.org/10.1093/jee/101.2.438.CrossRefGoogle Scholar
Sogo, K, Miura, K, Aizawa, M, Watanabe, T and Stouthamer, R (2015) Genetic structure in relation to reproduction mode in Thrips tabaci (Insecta: Thysanoptera). Applied Entomology Zoology 50, 73–77. doi: 10.1007/s13355-014-0306-7. https://doi:10.1007/s13355-014-0306-7.CrossRefGoogle Scholar
Sojnóczki, A, Pájtli, É, Reiter, D, Farkas, P and Fail, J (2015) Comparative study of Thrips tabaci (Lindeman) cytochrome-c-oxidase gene subunit I (COI) sequences data. Die Bodenkultur 66(3–4), 41–45.Google Scholar
Takeuchi, R and Toda, S (2011) Discrimination of two reproductive forms of Thrips tabaci by PCR-RFLP, and distribution of arrhenotokous T. tabaci in Tottori prefecture. Japanese Journal of Applied Entomology and Zoology 55, 254–257. https://doi.org/10.1303/jjaez.2011.254.CrossRefGoogle Scholar
Tamura, K and Nei, M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023.Google ScholarPubMed
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729. https://doi.org/10.1093/molbev/mst197.CrossRefGoogle ScholarPubMed
Toda, S and Komazaki, S (2002) Identification of thrips species (Thysanoptera:Thripidae) on Japanese fruit trees by polymerase chain reaction and restriction fragment length polymorphism of the ribosomal ITS2 region. Bulletin of Entomological Research 92, 359–363. https://doi.org/10.1079/BER2002177.CrossRefGoogle ScholarPubMed
Toda, S and Murai, T (2007) Phylogenetic analysis based on mitochondrial COI gene sequences in Thrips tabaci Lindeman (Thysanoptera: Thripidae) in relation to reproductive forms and geographic distribution. Applied Entomology and Zoology 42, 309–316. https://doi.org/10.1303/aez.2007.309.CrossRefGoogle Scholar
Trdan, S, Žnidar, D, Vali, N, Rozman, L and Vidridh, M (2006) Intercropping against onion thrips, Thrips tabaci Lindeman (Thysanoptera: Thripidae) in onion production: on the suitability of orchard grass, lacy phacelia, and buckwheat as alternatives for white clover. Journal of Plant Diseases and Protection 113(1), 24–30. https://www.jstor.org/stable/44754883.Google Scholar
Trdan, S, Valič, N and Žnidarčič, D (2007) Field efficacy of deltamethrin in reducing damage caused by Thrips tabaci Lindeman (Thysanoptera: Thripidae) on early white cabbage. Journal of Pest Science 80, 217. https://doi.org/10.1007/s10340-007-0174-9.CrossRefGoogle Scholar
Westmore, GC, Poke, FS, Allen, GR and Wilson, CR (2013) Genetic and host-associated differentiation within Thrips tabaci Lindeman (Thysanoptera: Thripidae) and its links to Tomato spotted wilt virus-vector competence. Heredity 111(3), 210–215. https://doi.org/10.1038/hdy.2013.39.CrossRefGoogle ScholarPubMed
Zawirska, I (1976) Untersuchungen über zwei biologische Typen von Thrips tabaci Lind. (Thysanoptera, Thripidae) in der VR Polen. Archives of Phytopathology & Plant Protection 12, 411–422. https://doi.org/10.1080/03235407609431780.CrossRefGoogle Scholar
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