Abstract
The stone leek leafminer Liriomyza chinensis (Kato, 1949) (Diptera: Agromyzidae) is a serious insect pest that invades the Japanese bunching onion (JSAEZ (ed.) 2006). A novel population of L. chinensis, here termed biotype B, has been repeatedly detected in many prefectures in Japan since 2016, which showed larval mine forms different from those of the native L. chinensis populations (biotype A). Though a previous study examined a portion of the mitochondrial cytochrome c oxidase I (mtCOI) sequences of these biotypes and revealed that there is DNA polymorphism between biotypes A and B, their nuclear DNA has not been examined; therefore, hybrid individuals have not been detected. To identify the biotypes of L. chinensis collected around Japan with precision, a novel nuclear DNA marker was established. Moreover, to reveal their phylogenetic relationships, phylogenetic analyses were conducted by comparing the biotype mtCOI and D2 region sequences of the 28S rDNA, which represent useful indexes of phylogenetic differentiation. Based on these analyses, the monophyly of L. chinensis was strongly supported (100% bootstrap support). The nuclear and mitochondrial DNA markers facilitated gathering maternal mitochondrial information and distinguishing hybrid individuals. This approach may help elucidate reproductive interference, which may cause the replacement of biotype A with biotype B.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Campbell BC, Steffen-Campbell JD, Werren JH (1993) Phylogeny of the Nasonia species complex (Hymenoptera: Pteromalidae) inferred from an internal transcribed spacer (ITS2) and 28S rDNA sequences. Insect Mol Biol 2:225–237. https://doi.org/10.1111/j.1365-2583.1994.tb00142.x
Carapelli A, Soltani A, Leo C, Vitale M, Amri M, Mediouni-Ben JJ (2018) Cryptic diversity hidden within the leafminer genus Liriomyza (Diptera: Agromyzidae). Genes 9:554. https://doi.org/10.3390/genes9110554
Chen XJ, Lang F, Xu Z, Jun-hua HE, Ma Y (2003) The occurrence of leafminers and their parasitoids on vegetables and weeds in Hangzhou area, Southeast China. Biocontrol 48:515–527. https://doi.org/10.1023/A:1025726813462
Chen JY, Chang YW, Zheng SZ, Lu MX, Du YZ (2018) Comparative analysis of the Liriomyza chinensis mitochondrial genome with other Agromyzids reveals conserved genome features. Sci Rep 8:1–10. https://doi.org/10.1038/s41598-018-27213-7
Choi IH, Kim CH, Kim JH, Kim GH (2003) Injury aspects of the stone leek leafminer, Liriomyza chinensis Kato (Diptera: Agromyzidae) on welsh onion. Korean J Appl Entomol 42:335–434 (in Korean with English abstract)
Crowder DW, Sitvarin MI, Carrière Y (2010) Plasticity in mating behaviour drives asymmetric reproductive interference in whiteflies. Anim Behav 79:579–587. https://doi.org/10.1016/j.anbehav.2009.11.025
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol and Biotech 3:294–299
Fujito S, Urairi C, Yamashita KI, Wako T, Kawai A, Takeda M (2021) Japanese bunching onion line with a high resistance to the stone leek leafminer, Liriomyza chinensis from the ‘Beicong’population: evaluating the inheritance of resistance. Euphytica 217:1–8. https://doi.org/10.1007/s10681-020-02764-x
Gillespie JJ, Munro JB, Heraty JM, Yoder MJ, Owen AK, Carmichael AE (2005) A secondary structural model of the 28S rRNA expansion segments D2 and D3 for chalcidoid wasps (Hymenoptera: Chalcidoidea). Mol Biol Evol 22:1593–1608. https://doi.org/10.1093/molbev/msi152
Gröning J, Hochkirch A (2008) Reproductive interference between animal species. Q Rev Biol 83:257–282. https://doi.org/10.1086/590510
JSAEZ (2006) Major insect and other pests of economic plants in Japan, Revised. Japan Plant Protection Association, Tokyo, p 387 (in Japanese)
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Martinez M (1982) Contribution a l’etude des Agromyzidae de France (Dipt.). Liriomyza nietzkei Spencer et Liriomyza chinensis (Kato), deux especes d’importance economique presentes en France. Bulletin-Societe Entomologique De France 87:302–308 (in French)
Martynov VV, Nikulina TV, Gubin AI (2016) Range expansion of invasive stone leek leafminer Liriomyza chinensis (Kato, 1949) (Diptera: Agromyzidae) in Eastern Europe. Euroasian Entomol J 15:420–421
Nakamura S, Masuda T, Mochizuki A, Konishi K, Tokumaru S, Ueno K, Yamaguchi T (2013) Primer design for identifying economically important Liriomyza species (Diptera: Agromyzidae) by multiplex PCR. Mol Ecol Resour 13:96–102. https://doi.org/10.1111/1755-0998.12025
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
Okada T, Sasakawa M (2003) The stone leek leafminer. In: Umeya K, Okada T (eds) Agricultural insect pests in Japan. Zenkoku Noson Kyoiku Kyokai, Tokyo, pp 295–296 (in Japanese)
Papp L, Cerny M (2017) Agromyzidae (Diptera) of Hungary, vol 3. Pars Ltd, Nagykovácsi
Paredes-Esquivel C, Donnelly MJ, Harbach RE, Townson H (2009) A molecular phylogeny of mosquitoes in the Anopheles barbirostris subgroup reveals cryptic species: implications for identification of disease vectors. Mol Phylogenet Evol 50:141–151
Scheffer JS, Winkler SI, Wiegmann MB (2007) Phylogenetic relationships within the leaf-mining flies (Diptera: Agromyzidae) inferred from sequence data from multiple genes. Mol Ecol Resour 13:96–102. https://doi.org/10.1111/1755-0998.12025
Sun DB, Li J, Liu YQ, Crowder DW, Liu SS (2014) Effects of reproductive interference on the competitive displacement between two invasive whiteflies. Bull Entomol Res 104:334–346. https://doi.org/10.1017/S0007485314000108
Takagi M, Wari D, Ogawara T, Uesugi R (2021) Simplified rapid differentiation of Liriomyza chinensis Kato (Diptera; Agromyzidae) genotypes A and B using PCR-RFLP. J Appl Entomol 145:726–730. https://doi.org/10.1111/jen.12876
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis, version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Tokumaru S (2016) Effects of temperature and photoperiod on development and reproductive potential of Liriomyza chinensis (Diptera: Agromyzidae). Jpn J Appl Entomol Zool 60:189–196. https://doi.org/10.1303/jjaez.2016.189(inJapanesewithEnglishabstract)
Tokumaru S, Uesugi R, Urairi C, Toyoshima S, Aoki Y, Iwasaki A (2021) Detection of two biotypes of Liriomyza chinensis (Kato) (Diptera: Agromyzidae) in Japan. J Econ Entomol 114:1406–1410. https://doi.org/10.1093/jee/toab037
Tran DH, Takagi M (2005) Susceptibility of the stone leek leafminer Liriomyza chinensis (Diptera: Agromyzidae) to insecticides. J Facul Agric Kyushu Univ 50:383–390
Ueno T, Tran DH (2015) Neochrysocharis okazakii (Hymenoptera: Eulophidae) as a major parasitoid wasp of stone leek leaf miner Liriomyza chinensis (Diptera: Agromyzidae) in central Vietnam. Psyche J Entomol 2015:1–6. https://doi.org/10.1155/2015/179560
Urairi C, Kawai A, Takeda M (2020) A method for mass-rearing Liriomyza chinensis (Diptera: Agromyzidae). Appl Entomol Zool 55:423–428. https://doi.org/10.1007/s13355-020-00697-4
Wang HL, Lei T, Xia WQ, Cameron SL, Liu YQ, Zhang Z, Gowda MN, De Barro P, Navas-Castillo J, Omongo CA, Delatte H, Lee KY, Patel RK, Ng J, Wu SL, Fiallo-Olive E, Liu SS, Colvin J, Wang XW (2019) Insight into the microbial world of Bemisia tabaci cryptic species complex and its relationships with its host. Sci Rep 9:1–15. https://doi.org/10.1038/s41598-019-42793-8
Williams HC, Ormerod SJ, Bruford MW (2006) Molecular systematics and phylogeography of the cryptic species complex Baetis rhodani (Ephemeroptera, Baetidae). Mol Phylogenet Evol 40:370–382. https://doi.org/10.1016/j.ympev.2006.03.004
Xu J, De Barro PJ, Liu SS (2010) Reproductive incompatibility among genetic groups of Bemisia tabaci supports the proposition that the whitefly is a cryptic species complex. Bull Entomol Res 100:359–366. https://doi.org/10.1017/S0007485310000015
Acknowledgements
We thank Prof. Dr. N. Hinomoto, Dr. S. Tokumaru, Mr. A. Iwasaki and Dr. S. Toyoshima for the useful discussions. We also thank Ms. M. Kikuchi, Ms. K. Shirotsuka, Mr. J. Yase, Mr. Y. Nakanishi, Ms. Y. Aoki, Mr. M. Doi, Ms. R. Ogino, Mr. Y. Takahashi, Mr. H. Fukuda, Dr. A. Nagasaka, Mr. M. Kaneko, Ms. T. Fujita, Mr. T. Tsukamoto, Mr. S. Yamaguchi, Mr. T. Mizuno, Mr. H. Yokoyama, Dr. K. Shimizu, Mr. R. Iwase, Ms. I. Fujita, and Ms. C. Asano for the collecting of flies. We also thank Editage (www.editage.com) for English language editing.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
13355_2022_790_MOESM2_ESM.docx
Supplementary file2 Fig. S1 Two types of damage caused on Japanese bunching onion by Liriomyza chinensis larvae a discontinuous mine forms generated by several biotype A larvae, which rarely cause severe economic damage; b continuous mine forms generated by dozens of biotype B larvae, which cause the entire leaf to turn white. Fig. S2 Alignment of mtCOI of Liriomyza chinensis haplotype A, B1, and B2 Restriction site of PvuI indicated; ‘MG252777’ indicates the sequence of a Chinese population of L. chinensis collected in Laiwu, Shangdong (Chen et al. 2018). mtCOI is a region of the mitochondrial DNA (The mitochondrial gene, cytochrome oxidase I). Fig. S3 Bunching onion leaves oviposited by Liriomyza chinensis biotypes A and B Arrows indicate positions of eggs. a Biotype A females oviposit inside the unifacial leaf of Japanese bunching onions; thus, eggs are observed by opening the leaf lengthwise with an insect pin; b biotype B females oviposit immediately under the epidermis and lengthwise intensively. (DOCX 3562 KB)
Rights and permissions
About this article
Cite this article
Urairi, C., Uesugi, R. & Fujito, S. Development of a novel nuclear DNA marker to identify biotypes A and B of the stone leek leafminer, Liriomyza chinensis (Diptera: Agromyzidae). Appl Entomol Zool 57, 313–322 (2022). https://doi.org/10.1007/s13355-022-00790-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13355-022-00790-w