Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-14T10:49:28.528Z Has data issue: false hasContentIssue false
  • English
  • Français

Novel host immune evasion strategy of the endoparasitoid Drino inconspicuoides

Published online by Cambridge University Press:  07 February 2019

K. Yamashita ,
K. Zhang ,
R.T. Ichiki ,
S. Nakamura Open the ORCID record for S. Nakamura [Opens in a new window]  and
S. Furukawa Open the ORCID record for S. Furukawa [Opens in a new window]
K. Yamashita
Affiliation:
Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan
K. Zhang
Affiliation:
Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan
R.T. Ichiki
Affiliation:
National Agriculture and Food Research Organization (NARO), Tsukuba, Ibaraki, Japan
S. Nakamura
Affiliation:
Japan International Research Center for Agricultural Sciences (JIRCAS), Tsukuba, Ibaraki, Japan
S. Furukawa*
Affiliation:
Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan
*
*Author for correspondence Phone: +81-29-853-4706 Fax: +81-29-853-4706 E-mail: furukawa.seiichi.ew@u.tsukuba.ac.jp
Get access Rights & Permissions [Opens in a new window]

Abstract

The tachinid fly Drino inconspicuoides (Diptera: Tachinidae) is an ovolarviparous endoparasitoid whose larvae develop in the host haemocoel and avoids the host immune system. In this study, we investigated the immune evasion mechanisms of this species during infestation in the host Mythimna separata (Lepidoptera: Noctuidae). We discovered a unique ‘cloak’ that surrounded D. inconspicuoides larvae that penetrated into the host and determined through genomic polymerase chain reaction analysis that this structure originated from the host rather than the tachinid. The ‘cloak’ contained both haemocytes and fat body cells from the host, with the haemocytes assembling around the larvae first and the fat body cells then covering the haemocyte layer, following which the two mixed. Living D. inconspicuoides larvae that were wrapped in the ‘cloak’ were not melanized whereas encapsulated dead larvae were melanized, suggesting that this structure contributes to the avoidance of host immune reactions.

Keywords

tachinid flyDrino inconspicuoidesMythimna separatacloakcell lineage
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 109 , Issue 5 , October 2019 , pp. 643 - 648
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Baranov, N. (1934) Messages about gezucktete oriental larvaevoriden (Insecta: Diptera). Entomologische Nachrichten 8, 41–49.Google Scholar
Chen, C.H., Sun, L. & Mochly-Rosen, D. (2010) Mitochondrial aldehyde dehydrogenase and cardiac diseases. Cardiovascular Research 88, 51–57.Google Scholar
Dindo, M.L. (2011) Tachinid parasitoids: are they to be considered as koinobionts? BioControl 56, 249–255.Google Scholar
Dowden, P.B. (1934) Zenillia libatrix Panzer, a tachinid parasite of the gypsy moth and the brown-tail moth. Journal of Agricultural Research 48, 97–114.Google Scholar
Dubovskii, I.M., Grizanova, E.V., Chertkova, E.A., Slepneva, I.A., Komarov, D.A., Vorontsova, Ya.L. & Glupov, VV. (2010) Generation of reactive oxygen species and activity of antioxidants in hemolymph of the moth larvae Galleria mellonella (L.) (Lepidoptera: Piralidae) at development of the process of encapsulation. Journal of Evolutionary Biochemistry and Physiology 46, 35–43.Google Scholar
Dudzic, J.P., Kondo, S., Ueda, R., Bergman, C.M. & Lemaitre, B. (2015) Drosophila innate immunity: regional and functional specialization of prophenoloxidases. BMC Biology 13, 81.Google Scholar
Gardenghi, G. & Mellini, E. (1995) Note sul canale alimentare delle larve del parassitoide Exorista larvarum (L.) (Dipt. Tachinidae). Bollettino dell'Istituto di Entomologia “Guido Grandi” University of Bologna 49, 197–209.Google Scholar
Hayakawa, Y. (1986) Inhibition of lipid transport in insects by a factor secreted by the parasite, Blepharipa sericariae. FEBS Letters 195, 122–124.Google Scholar
Hirose, Y. (2005) Discovery of insect parasitism and subsequent development of parasitoid research in Japan. Biological Control 32, 49–56.Google Scholar
Ichiki, R. & Shima, H. (2003) Immature life of Compsilura concinnata (Meigen) (Diptera: Tachinidae). Annals of the Entomological Society of America 96, 161–167.Google Scholar
Ishihara, T., Maruyama, Y. & Furukawa, S. (2017) Gene expression and molecular characterization of a novel C-type lectin, encapsulation promoting lectin (EPL), in the rice armyworm, Mythimna Separata. Insect Biochemistry and Molecular Biology 89, 51–57.Google Scholar
Ji, Y-J., Zhang, D-X. & He, L-J. (2003) Evolutionary conservation and versatility of a new set of primers for amplifying the ribosomal internal transcribed spacer regions in insects and other invertebrates. Molecular Ecology Notes 3, 581–585.Google Scholar
Kalyebi, A. & Nakamura, S. (2006) The biology of the parasitoid fly Drino inconspicuoides (Diptera: Tachinidae) in the host Mythimna separata (Lepidoptera: Noctuidae). Applied Entomology and Zoology 41, 365–370.Google Scholar
Kathirithamby, J., Ross, L.D. & Johnston, J.S. (2003) Masquerading as self? Endoparasitic Strepsiptera (Insecta) enclose themselves in host-derived epidermal bag. Proceedings of the National Academy of Sciences of the United States of America 100, 7655–7659.Google Scholar
Lackie, A.M. (1988) Immune mechanisms in insects. Parasitology Today 4, 98–105.Google Scholar
Lavine, M.D. & Strand, M.R. (2002) Insect hemocytes and their role in cellular immune responses. Insect Biochemistry and Molecular Biology 32, 1237–1242.Google Scholar
Michalková, V., Valigurová, A., Dindo, M.L. & Vanhara, J. (2009) Larval morphology and anatomy of the parasitoid Exorista larvarum (Diptera: Tachinidae), with an emphasis on cephalopharyngeal skeleton and digestive tract. Journal of Parasitology 95, 544–554.Google Scholar
Moreau, S.J.M. & Asgari, S. (2015) Venom proteins from parasitoid wasps and their biological functions. Toxins (Basel) 7, 2385–2412.Google Scholar
Namba, O., Nakamatsu, Y., Tateishi, K., Miura, K. & Tanaka, T. (2009) Cuticular encystment of Autographa nigrisigna eggs by epidermal cell migration. Journal of Insect Physiology 55, 629–636.Google Scholar
Nappi, A.J., Vass, E., Frey, F. & Carton, Y. (1995) Superoxide anion generation in Drosophila during melanotic encapsulation of parasites. European Journal of Cell Biology 68, 450–456.Google Scholar
Pech, L.L. & Strand, M.R. (2000) Plasmatocytes from the moth Pseudoplusia includens induce apoptosis of granular cells. Journal of Insect Physiology 46, 1565–1573.Google Scholar
Ribeiro, C. & Brehélin, M. (2006) Insect haemocytes: what type of cell is that? Journal of Insect Physiology 52, 417–429.Google Scholar
Salt, G. (1968) The resistance of insect parasitoids to the defence reactions of their hosts. Biological Reviews 43, 200–232.Google Scholar
Satyavathi, V.V., Minz, A. & Nagaraju, J. (2014) Nodulation: an unexplored cellular defense mechanism in insects. Cellular Signalling 26, 1753–1763.Google Scholar
Shima, H. (1999) Host-parasite catalog of Japanese Tachinidae (Diptera). Makunagi/Acta Dipterologica 1, 1–108.Google Scholar
Stireman, J.O. & Singer, M.S. (2003) Determinants of parasitoid-host associations: insights from a natural tachinid-lepidopteran community. Ecology 84, 296–310.Google Scholar
Stireman, J.O., O'Hara, J.E. & Wood, D.M. (2006) Tachinidae: evolution, behavior, and ecology. Annual Review of Entomology 51, 525–555.Google Scholar
Yamaguchi, K., Matsumoto, H., Ochiai, M., Tsuzuki, S. & Hayakawa, Y. (2012) Enhanced expression of stress-responsive cytokine-like gene retards insect larval growth. Insect Biochemistry and Molecular Biology 42, 183–192.Google Scholar