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DNA barcoding of pear psyllids (Hemiptera: Psylloidea: Psyllidae), a tale of continued misidentifications

Published online by Cambridge University Press:  10 February 2020

G. Cho Open the ORCID record for G. Cho [Opens in a new window] ,
I. Malenovský Open the ORCID record for I. Malenovský [Opens in a new window] ,
D. Burckhardt Open the ORCID record for D. Burckhardt [Opens in a new window] ,
H. Inoue  and
S. Lee
G. Cho
Affiliation:
Department of Agricultural Biotechnology, Insect Biosystematics Laboratory, Research Institute of Agriculture and Life Science, Seoul National University, Seoul151-921, Korea
I. Malenovský
Affiliation:
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37Brno, Czech Republic
D. Burckhardt
Affiliation:
Naturhistorisches Museum, Augustinergasse 2, 4001Basel, Switzerland
H. Inoue
Affiliation:
Institute of Fruit Tree and Tea Science, National Agriculture and Food Research Organization (NARO), Akitsu, Higashihiroshima, Hiroshima739-2494, Japan
S. Lee*
Affiliation:
Department of Agricultural Biotechnology, Insect Biosystematics Laboratory, Research Institute of Agriculture and Life Science, Seoul National University, Seoul151-921, Korea
*
Author for correspondence: S. Lee, Email: seung@snu.ac.kr
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Abstract

Pear psyllids (Hemiptera: Psylloidea: Psyllidae: Cacopsylla spp.) belong to the most serious pests of pear (Pyrus spp.). They damage pear trees by excessive removal of phloem sap, by soiling the fruits with honeydew which, in turn, provides a substrate for sooty mould, and by transmission of Candidatus Phytoplasma spp., the causal agents of the pear decline disease. The morphological similarity, the presence of seasonal dimorphism that affects adult colour, size and wing morphology and uncritical use of species names, led to much confusion in the taxonomy of pear psyllids. As a result, pear psyllids have been frequently misidentified. Many of the entries attributed to Cacopsylla pyricola and other species in the GenBank are misidentifications which led to additional, unnecessary confusion. Here we analysed DNA barcodes of 11 pear psyllid species from eastern Asia, Europe and Iran using four mitochondrial gene fragments (COI 658 bp, COI 403 bp, COI-tRNAleu-COII 580 bp and 16S rDNA 452 bp). The efficiency of identification was notably high and considerable barcoding gaps were observed in all markers. Our results confirm the synonymies of the seasonal forms of Cacopsylla jukyungi ( = C. cinereosignata, winter form) and C. maculatili ( = C. qiuzili, summer form) previously suggested based on morphology. Some previous misidentifications (C. chinensis from China, Japan and Korea = misidentification of C. jukyungi; C. pyricola and C. pyrisuga from East Asia = misidentification of C. jukyungi and C. burckhardti, respectively; C. pyricola from Iran = misidentification of C. bidens, C. pyri and Cacopsylla sp.) are also corrected. There is no evidence for the presence of European pear psyllid species in East Asia.

Keywords

Cacopsyllajumping plant licemolecular diagnosticspest identificationphytoplasma vectors
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 4 , August 2020 , pp. 521 - 534
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Amouroux, P, Crochard, D, Germain, JF, Correa, M, Ampuero, J, Groussier, G, Kreiter, P, Malausa, T and Zaviezo, T (2017) Genetic diversity of armored scales (Hemiptera: Diaspididae) and soft scales (Hemiptera: Coccidae) in Chile. Scientific Reports 7, 2014.CrossRefGoogle Scholar
Boehme, P, Amendt, J, Disney, RHL and Zehner, R (2010) Molecular identification of carrion-breeding scuttle flies (Diptera: Phoridae) using COI barcodes. International Journal of Legal Medicine 124, 577–581.CrossRefGoogle ScholarPubMed
Burckhardt, D (1994) Psylloid pests of temperate and subtropical crop and ornamental plants (Hemiptera, Psylloidea): a review. Entomology (Trends in Agricultural Sciences) 2, 173–186.Google Scholar
Burckhardt, D and Hodkinson, ID (1986) A revision of the West Palaearctic pear psyllids (Hemiptera: Psyllidae). Bulletin of Entomological Research 76, 119–132.CrossRefGoogle Scholar
Burckhardt, D and Lauterer, P (1993) The jumping plant-lice of Iran (Homoptera, Psylloidea). Revue Suisse de Zoologie 100, 829–898.CrossRefGoogle Scholar
Chen, P, Liu, Q, Qiao, X, Wang, J and Zhang, T (2018) Identification and phylogenetic analysis of pear psyllids (Hemiptera: Psyllidae) in Chinese pear orchards. Journal of Economic Entomology 20, 1–6.Google Scholar
Cho, G and Lee, S (2015) Identification of invasive Cacopsylla chinensis (Hemiptera: Psyllidae) lineage based on two mitochondrial sequences, pp. 64 in Korean society of applied entomology (2015) Proceeding of Korean Society of Applied Entomology: diversity and pest management. Korean Society of Applied Entomology, Suwon, Korea.Google Scholar
Cho, G, Burckhardt, D, Inoue, H, Luo, X and Lee, S (2017) Systematics of the east Palaearctic pear psyllids (Hemiptera: Psylloidea) with particular focus on the Japanese and Korean fauna. Zootaxa 4362, 75–98.CrossRefGoogle ScholarPubMed
Collins, RA, Boykin, LM, Cruickshank, RH and Armstrong, K (2012) Barcoding's next top model: an evaluation of nucleotide substitution models for specimen identification. Methods in Ecology and Evolution 3, 457–465.CrossRefGoogle Scholar
FAO (2016) Food and Agricultural Organization of the United Nation FAO. Rome, Italy: FAO. Available at http://faostat3.fao.org/download/Q/QC/EGoogle Scholar
Folmer, O, Black, M, Hoeh, W, Lutz, R and Vrijenhoek, R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Gwiazdowski, RA, Foottit, RG, Maw, HEL and Hebert, PDN (2015) The Hemiptera (Insecta) of Canada: constructing a reference library of DNA barcodes. PLoS ONE 10, e0125635.CrossRefGoogle ScholarPubMed
Hebert, PDN and Ratnasingham, S (2007) BOLD: the barcode of life data system (www.barcodinglife.org). Molecular Ecology Notes 7, 355–364.Google Scholar
Hebert, PDN, Ratnasingham, S and deWaard, JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society B: Biological Sciences 270, S96–S99.CrossRefGoogle ScholarPubMed
Hodkinson, ID (1984) The biology and ecology of the gall-forming Psylloidea (Homoptera). In Ananthakrishnan, TN (ed.), Biology of Gall Insects. London, Great Britain: Edward Arnord, pp. 59–77.Google Scholar
Inoue, H (2010) The generic affiliation of Japanese species of the subfamily Psyllinae (Hemiptera: Psyllidae) with a revised checklist. Journal of Natural History 44, 333–360.CrossRefGoogle Scholar
Inoue, H, Kuchiki, F, Ide, Y and Mishima, S (2012) First report of the occurrence of Cacopsylla chinensis (Yang & Li) (Hemiptera: Psyllidae) on cultivated Japanese pear in Japan. Japanese Journal of Applied Entomology and Zoology 56, 111–113.CrossRefGoogle Scholar
Kang, AR, Baek, JY, Lee, SH, Cho, YS, Kim, WS, Han, YS and Kim, IS (2012) Geographic homogeneity and high gene flow of the pear psylla, Cacopsylla pyricola (Hemiptera: Psyllidae), detected by mitochondrial COI gene and nuclear ribosomal internal transcribed spacer 2. Animal Cells and Systems 16, 145–153.CrossRefGoogle Scholar
Kanturski, M, Lee, Y, Choi, J and Lee, S (2018) DNA barcoding and a precise morphological comparison revealed a cryptic species in the Nippolachnus piri complex (Hemiptera: Aphididae: Lachninae). Scientific Reports 8, 8998.CrossRefGoogle Scholar
Katoh, K and Toh, H (2008) Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFT-based framework. BMC Bioinformatics 9, 212.CrossRefGoogle ScholarPubMed
Katoh, K, Misawa, K, Kuma, K and Miyata, T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.CrossRefGoogle ScholarPubMed
Katoh, K, Kuma, K, Toh, H and Miyata, T (2005) MAFFT Version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33, 511–518.CrossRefGoogle ScholarPubMed
Katoh, H, Inoue, H, Kuchiki, F, Ide, Y, Uechi, N and Iwanami, T (2013) Identification of a distinct lineage of Cacopsylla chinensis (Hemiptera: Psyllidae) in Japan on the basis of two mitochondrial DNA sequences. Journal of Economic Entomology 106, 536–542.CrossRefGoogle ScholarPubMed
Katoh, H, Inoue, H, Uechi, N, Fujikawa, T, Miyata, S and Iwanami, T (2014) Analysis of the genetic population structure of Cacopsylla chinensis (Hemiptera: Psyllidae) with mitochondrial DNA markers in Saga and Yamaguchi prefectures, Japan. Japan Agricultural Research Quarterly: JARQ 48, 413–417.CrossRefGoogle Scholar
Kim, DS, Cho, MR, Jeon, HY, Yiem, MS and Lee, JH (2000) Population trends and temperature-dependent development of pear psylla, Cacopsylla pyricola (Foerster) (Homoptera: Psyllidae). Korean Journal of Applied Entomology 39, 73–82.Google Scholar
Kim, DS, Yang, CY and Jeon, HY (2007) An empirical model for the prediction of the onset of upward-movement of overwintered Cacopsylla pyricola (Homoptera: Psyllidae) in pear orchards. Korean Journal of Agricultural and Forest Meteorology 9, 228–233.CrossRefGoogle Scholar
Kim, H, Hoelmer, KA, Lee, W, Kwon, YD and Lee, S (2010) Molecular and morphological identification of the soybean aphid and other Aphis species on the primary host Rhamnus davurica in Asia. Annals of the Entomological Society of America 103, 532–543.CrossRefGoogle Scholar
Kwon, YJ (1983) Psylloidea of Korea (Homoptera: Sternorrhyncha). Seoul, Korea: Insecta Koreana.Google Scholar
Kwon, JH, Suh, SJ and Kwon, YJ (2016) A preliminary check list of jumping plant-lice from Korea (Homoptera: Psylloidea). Entomological Research Bulletin 32, 131–137.Google Scholar
Lee, HC, Yang, MM, Li, F and Yeh, WB (2007) Genetic variation of Cacopsylla chinensis (Hemiptera: Psyllidae) in Taiwan based on mitochondrial 16S rDNA sequence. Formosan Entomologist 27, 157–168.Google Scholar
Lee, HC, Yang, MM and Yeh, WB (2008) Identification of two invasive Cacopsylla chinensis (Hemiptera: Psyllidae) lineages based on two mitochondrial sequences and restriction fragment length polymorphism of cytochrome oxidase I amplicon. Journal of Economic Entomology 101, 1152–1157.CrossRefGoogle ScholarPubMed
Leite, LAR (2012) Mitochondrial pseudogenes in insect DNA barcoding: differing points of view on the same issue. Biota Neotropica 12, 301–308.CrossRefGoogle Scholar
Lunt, DH, Zhang, DX, Szymura, JM and Hewitt, OM (1996) The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic studies. Insect Molecular Biology 5, 153–165.CrossRefGoogle ScholarPubMed
Luo, X, Li, F, Ma, Y and Cai, W (2012) A revision of Chinese pear psyllids (Hemiptera: Psylloidea) associated with Pyrus ussuriensis. Zootaxa 3489, 58–80.CrossRefGoogle Scholar
Martoni, F, Bulman, S, Pitman, A, Taylor, G and Armstrong, K (2018) DNA barcoding highlights cryptic diversity in the New Zealand Psylloidea (Hemiptera: Sternorrhyncha). Diversity 10, 50.CrossRefGoogle Scholar
Ossiannilsson, F (1992) The Psylloidea (Homoptera) of Fennoscandia and Denmark. Fauna Entomologica Scandinavica. Leiden, Netherlands: E.J. Brill.Google Scholar
Paik, WH (1963) Agricultural and Forest Pestology. Seoul, Korea: Hyangmunsa.Google Scholar
Park, HC (1996) Taxonomy of Korean psyllids (Homoptera: Psylloidea) 1. A revised checklist. Korean Journal of Entomology 26, 267–278.Google Scholar
Park, DS, Suh, SJ, Oh, HW and Hebert, PD (2010) Recovery of the mitochondrial COI barcode region in diverse Hexapoda through tRNA-based primers. BMC Genomics 11, 423.CrossRefGoogle ScholarPubMed
Park, JW, Park, YU, An, JJ, Park, SE, Choi, JJ, Koo, HN and Kim, GH (2013) Insecticidal activity of 27 insecticides to pear psylla, Cacopsylla pyricola (Foerster) (Hemiptera: Psyllidae) in Jincheon. The Korean Journal of Pesticide Science 17, 72–75.CrossRefGoogle Scholar
Park, MW, Kwon, HR, Yu, YM and Youn, YN (2016) Feeding behaviors of Cacopsylla pyricola (Hemiptera: Psyllidae) using electrical penetration graphs (EPGs). Korean Journal of Agricultural Science 43, 194–204.CrossRefGoogle Scholar
Percy, DM (2003) Radiation, diversity, and host–plant interactions among island and continental legume-feeding psyllids. Evolution 57, 2540–2556.CrossRefGoogle ScholarPubMed
Percy, DM, Crampton-Platt, A, Sveinsson, S, Lemmon, AR, Lemmon, EM, Ouvrard, D and Burckhardt, D (2018) Resolving the psyllid tree of life: phylogenomic analyses of the superfamily Psylloidea (Hemiptera). Systematic Entomology 43, 762–776.CrossRefGoogle Scholar
Seemüller, E, Schneider, B and Jarausch, B (2011) Pear decline Phytoplasma. In Hadidi, A, Barba, M, Candresse, T and Jelkmann, W (eds), Virus and Virus-like Diseases of Pome and Stone Fruits. MN, USA: APS press, pp. 77–84.CrossRefGoogle Scholar
Shin, S, Jung, S, Lee, H and Lee, S (2013) Molecular identification of dipteran pests (Diptera: Sciaroidea) from shiitake mushroom. Molecular Ecology Resources 13, 200–209.CrossRefGoogle ScholarPubMed
Simon, C, Frati, F, Beckenbach, A, Cresip, B, Liu, H and Flook, P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–701.CrossRefGoogle Scholar
Simon, C, Buckley, TR, Frati, F, Stewart, JB and Beckenbach, AT (2006) Incorporating molecular evolution into phylogenetic analysis, and a new compilation of conserved polymerase chain reaction primers for animal mitochondrial DNA. Annual Review of Ecology, Evolution, and Systematics 37, 545–549.CrossRefGoogle Scholar
Song, H, Buhay, JE, Whiting, MF and Crandall, KA (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences 105, 13468–13491.CrossRefGoogle ScholarPubMed
Song, C, Lin, XL, Wang, Q and Wang, XH (2018) DNA Barcodes successfully delimit morphospecies in a superdiverse insect genus. Zoologica Scripta 47, 311–324.CrossRefGoogle Scholar
Soroker, V, Alchanatis, V, Harari, A, Talebaev, S, Anshelevich, L, Reneh, S and Levsky, S (2013) Phenetic plasticity in the pear psyllid, Cacopsylla bidens (Šulc) (Hemiptera, Psylloidea, Psyllidae) in Israel. Israel Journal of Entomology 43, 21–31.Google Scholar
Srivathsan, A and Meier, R (2012) On the inappropriate use of Kimura-2-parameter (K2P) divergences in the DNA-barcoding literature. Cladistics 28, 190–194.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Valle, D, Burckhardt, D, Mujica, V, Zopolo, R and Morelli, E (2017) The occurrence of the pear psyllid, Cacopsylla bidens (Šulc, 1907) (Insecta: Hemiptera: Psyllidae), in Uruguay. Check List (Luis Felipe Toledo) 13, 2088.CrossRefGoogle Scholar
Weintraub, PG and Jones, P (eds) (2010) Phytoplasmas: Genomes, Plant Hosts, and Vectors. Wallingford, UK: CABI.Google Scholar
Wu, Y, Trepanowski, NF, Molongoski, JJ, Reagel, PF, Lingafelter, SW, Nadel, H, Myers, SW and Ray, AM (2016) Identification of wood-boring beetles (Cerambycidae and Buprestidae) intercepted in trade-associated solid wood packaging material using DNA barcoding and morphology. Scientific Reports 7, 40316.CrossRefGoogle Scholar
Yang, MM, Huang, JH and Li, F (2004) A new record of Cacopsylla species (Hemiptera: Psyllidae) from pear orchards in Taiwan. Formosan Entomologist 24, 213–220.Google Scholar
Yeh, WB, Yang, CT and Kang, SC (1997) Identification of two sibling species, Ephemera formosana and E. sauteri (Ephemeroptera: Ephemeridae), based on mitochondrial DNA sequence analysis. Chinese Journal of Entomology 17, 257–268.Google Scholar
Zendedel, A, Burckhardt, D, Fekrat, L, Manzari, S and Namaghi, HS (2016) An annotated checklist of the jumping plant-lice (Hemiptera: Psylloidea) of Iran. Journal of the Entomological Research Society 18, 37–55.Google Scholar