Impact of rearing temperature on encapsulation and the accumulation of transcripts putatively involved in capsule formation in a parasitized lepidopteran host

Seehausen, M. L.; Naumann, Paul-Henri; Béliveau, C.; Martel, V.; Cusson, M.

doi:10.1016/j.jinsphys.2018.04.013

Article (Scientific journals)

Impact of rearing temperature on encapsulation and the accumulation of transcripts putatively involved in capsule formation in a parasitized lepidopteran host

Seehausen, M. L.; Naumann, Paul-Henri; Béliveau, C. et al.

2018 • In Journal of Insect Physiology, 107, p. 244-249

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/265873

DOI
10.1016/j.jinsphys.2018.04.013

PubMed
29704478

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

1-s2.0-S0022191018300775-main.pdf

Publisher postprint (541.5 kB)

Request a copy

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Choristoneura fumiferana; Encapsulation; Endoparasitoid; Melanisation; Temperature; Tranosema rostrale; Hexapoda; Hymenoptera; Ichneumonidae; Lepidoptera; Tortricidae; Animals; Down-Regulation; Gene Expression Regulation; Host-Parasite Interactions; Hot Temperature; Insect Proteins; Larva; Moths; Up-Regulation

Abstract :

[en] Encapsulation and melanisation are innate immune reactions of insects against foreign intruders such as parasitoids. In an earlier study, we observed that immature life stages of the endoparasitoid Tranosema rostrale (Hymenoptera: Ichneumonidae) parasitizing Choristoneura fumiferana (Lepidoptera: Tortricidae) larvae experienced higher mortality due to encapsulation and melanisation when reared at high (30 °C) than at lower (10 °C, 20 °C) temperatures. Downregulation of T. rostrale polydnavirus genes in parasitized hosts and upregulation of two genes involved in the spruce budworm's melanisation process were identified as likely contributors to parasitoid mortality at high temperature. However, levels of transcripts of genes involved in the spruce budworm's cellular encapsulation process were not measured inasmuch as candidate genes, in the spruce budworm, had not yet been identified. In addition, our assessment of temperature-dependent encapsulation and melanisation of foreign objects in spruce budworm larvae was only partial. To fill these knowledge gaps, we injected Sephadex™ beads into unparasitized spruce budworm larvae and assessed their encapsulation/melanisation after the insects had been held at three different temperatures (10, 20, and 30 °C), and we identified spruce budworm genes putatively involved in the encapsulation process and quantified their transcripts at the same three temperatures, using a qPCR approach. As expected, both encapsulation and melanisation of Sephadex™ beads increased as a function of temperature. At the molecular level, three of the five genes examined (Integrin β1, Hopscotch, Stat92E) clearly displayed temperature-dependent upregulation. The results of this study further support the hypothesis that a temperature-dependent increase in the encapsulation response of C. fumiferana against T. rostrale is due to the combined effects of reduced expression of polydnavirus genes and enhanced expression of host immune genes. © 2018 Elsevier Ltd

Disciplines :

Anatomy (cytology, histology, embryology...) & physiology

Author, co-author :

Seehausen, M. L.; University of Toronto, Faculty of Forestry, 33 Willcocks Street, Toronto, Ontario M5S 3B3, Canada

Naumann, Paul-Henri ; Université de Liège - ULiège

Béliveau, C.; Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, 1055 du P.E.P.S., Quebec City, G1V 4C7, Canada

Martel, V.; Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, 1055 du P.E.P.S., Quebec City, G1V 4C7, Canada

Cusson, M.; Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, 1055 du P.E.P.S., Quebec City, G1V 4C7, Canada

Language :

English

Title :

Impact of rearing temperature on encapsulation and the accumulation of transcripts putatively involved in capsule formation in a parasitized lepidopteran host

Publication date :

2018

Journal title :

Journal of Insect Physiology

ISSN :

0022-1910

Publisher :

Elsevier, United Kingdom

Volume :

107

Pages :

244-249

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

Research and Development; FedDev Ontario; Atlantic Canada Opportunities Agency; Canadian Forest Service

Available on ORBi :

since 08 December 2021

Statistics

Number of views

47 (1 by ULiège)

Number of downloads

1 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Blumberg, D., Seasonal variations in the encapsulation of eggs of the encyrtid parasitoid Metaphycus stanleyi by the pyriform scale, Protopulvinaria pyriformis. Entomol. Exp. Appl. 58 (1991), 231–237.
Cao, X., He, Y., Hu, Y., Wang, Y., Chen, Y.R., Bryant, B., Clem, R.J., Schwartz, L.M., Blissard, G., Jiang, H., The immune signaling pathways of Manduca sexta. Insect Biochem. Mol. Biol. 62 (2015), 64–74.
Chen, J.Y., Niu, L.M., Li, L., Han, D.Y., Fu, Y.G., Influence of constant temperature on development and reproduction of Encarsia guadeloupae Viggiani (Hymenoptera: Aphelinidae), a parasitoid of the spiraling whitefly Aleurodicus dispersus Russell (Hemiptera: Aleyrodidae). Neotrop. Entomol. 44 (2015), 160–165.
Cherqui, A., Duvic, B., Brehelin, M., Purification and characterization of prophenoloxidase from the haemolymph of Locusta migratoria. Arch. Insect Biochem. Physiol. 32 (1996), 225–235.
Chevignon, G., Cambier, S., Da Silva, C., Poulain, J., Drezen, J.M., Huguet, E., Moreau, S.J., Transcriptomic response of Manduca sexta immune tissues to parasitization by the bracovirus associated wasp Cotesia congregata. Insect Biochem. Mol. Biol. 62 (2015), 86–99.
Cusson, M., Lucarotti, C., Stoltz, D., Krell, P., Doucet, D., A polydnavirus from the spruce budworm parasitoid, Tranosema rostrale (Ichneumonidae). J. Invertebr. Pathol. 72 (1998), 50–56.
Dorémus, T., Jouan, V., Urbach, S., Cousserans, F., Wincker, P., Ravallec, M., Wajnberg, E., Volkoff, A.-N., Hyposoter didymator uses a combination of passive and active strategies to escape from the Spodoptera frugiperda cellular immune response. J. Insect Physiol. 59 (2013), 500–508.
Doucet, D., Cusson, M., Role of calyx fluid in alterations of immunity in Choristoneura fumiferana larvae parasitized by Tranosema rostrale. Comp. Biochem. Physiol. A Physiol. 114 (1996), 311–317.
Doucet, D., Cusson, M., Alteration of developmental rate and growth of Choristoneura fumiferana parasitized by Tranosema rostrale: role of the calyx fluid. Entomol. Exp. Appl. 81 (1996), 21–30.
Dubovskiy, I.M., Kryukova, N.A., Glupov, V.V., Ratcliffe, N.A., Encapsulation and nodulation in insects. Invertebr. Surv. J. 13 (2016), 229–246.
Fellowes, M., Kraaijeveld, A., Godfray, H., Cross-resistance following artificial selection for increased defense against parasitoids in Drosophila melanogaster. Evolution 53 (1999), 966–972.
Hara, T., Miyoshi, T., Tsukamoto, T., Comparative studies on larval and pupal phenoloxidase of the housefly, Musca domestica L. Comp. Biochem. Physiol. B: Biochem. 106 (1993), 287–292.
Hayakawa, Y., Yasuhara, Y., Growth-blocking peptide or polydnavirus effects on the last instar larvae of some insect species. Insect Biochem. Mol. Biol. 23 (1993), 225–231.
Karban, R., Caterpillar basking behavior and nonlethal parasitism by tachinid flies. J. Insect Behav. 11 (1998), 713–723.
Lavine, M.D., Strand, M.R., Insect hemocytes and their role in immunity. Insect Biochem. Mol. Biol. 32 (2002), 1295–1309.
Levin, D.M., Breuer, L.N., Zhuang, S., Anderson, S.A., Nardi, J.B., Kanost, M.R., A hemocyte-specific integrin required for hemocytic encapsulation in the tobacco hornworm, Manduca sexta. Insect Biochem. Mol. Biol. 35 (2005), 369–380.
Lockey, T.D., Ourth, D.D., Isolation and characterization of hemolymph phenoloxidase from Heliothis virescens larvae. Comp. Biochem. Physiol. B: Comp. Biochem. 102 (1992), 891–896.
Lovallo, N., Cox-Foster, D.L., Alteration in FAD–glucose dehydrogenase activity and hemocyte behavior contribute to initial disruption of Manduca sexta immune response to Cotesia congregata parasitoids. J. Insect Physiol. 45 (1999), 1037–1048.
McMorran, A., A synthetic diet for the spruce budworm, Choristoneura fumiferana (Clem.)(Lepidoptera: Tortricidae). Can. Entomol. 97 (1965), 58–62.
Nappi, A.J., Christensen, B.M., Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochem. Mol. Biol. 35 (2005), 443–459.
Ouedraogo, R.M., Goettel, M.S., Brodeur, J., Behavioral thermoregulation in the migratory locust: a therapy to overcome fungal infection. Oecologia 138 (2004), 312–319.
Ouedraogo, R.M., Cusson, M., Goettel, M.S., Brodeur, J., Inhibition of fungal growth in thermoregulating locusts, Locusta migratoria, infected by the fungus Metarhizium anisopliae var acridum. J. Invertebr. Pathol. 82 (2003), 103–109.
Ribeiro, C., Brehélin, M., Insect haemocytes: what type of cell is that?. J. Insect Physiol. 52 (2006), 417–429.
Rutledge, R.G., A Java program for LRE-based real-time qPCR that enables large-scale absolute quantification. PLoS One, 6, 2011, e17636.
SAS Institute Inc., SAS Studio 3.4: User's Guide. 2015, SAS Institute Inc., Cary.
Seehausen, M.L., Régnière, J., Martel, V., Smith, S.M., Developmental and reproductive responses of the spruce budworm (Lepidoptera: Tortricidae) parasitoid Tranosema rostrale (Hymenoptera: Ichneumonidae) to temperature. J. Insect Physiol. 98 (2017), 38–46.
Seehausen, M.L., Cusson, M., Régnière, J., Bory, M., Stewart, D., Djoumad, A., Smith, S.M., Martel, V., High temperature induces downregulation of polydnavirus gene transcription in lepidopteran host and enhances accumulation of host immunity gene transcripts. J. Insect Physiol. 98 (2017), 126–133.
Sorrentino, R.P., Melk, J.P., Govind, S., Genetic analysis of contributions of dorsal group and JAK-Stat92E pathway genes to larval hemocyte concentration and the egg encapsulation response in Drosophila. Genetics 166 (2004), 1343–1356.
Spanoudis, C.G., Andreadis, S.S., Temperature-dependent survival, development, and adult longevity of the koinobiont endoparasitoid Venturia canescens (Hymenoptera: Ichneumonidae) parasitizing Plodia interpunctella (Lepidoptera: Pyralidae). J. Pest Sci. 85 (2012), 75–80.
Strand, M.R., Hayakawa, Y., Clark, K.D., Plasmatocyte spreading peptide (PSP1) and growth blocking peptide (GBP) are multifunctional homologs. J. Insect Physiol. 46 (2000), 817–824.
Theopold, U., Krause, E., Schmidt, O., Cloning of a VLP-protein coding gene from a parasitoid wasp Venturia canescens. Arch. Insect Biochem. Physiol. 26 (1994), 137–145.
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., Speleman, F., Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3 (2002), 1–12.
Zufelato, M.S., Lourenço, A.P., Simões, Z.L., Jorge, J.A., Bitondi, M.M., Phenoloxidase activity in Apis mellifera honey bee pupae, and ecdysteroiddependent expression of the prophenoloxidase mRNA. Insect Biochem. Mol. Biol. 34 (2004), 1257–1268.