Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-26T19:56:47.899Z Has data issue: false hasContentIssue false
  • English
  • Français

Transcriptome analysis uncovers different avenues for manipulating cold performance in Chrysomya megacephala (Diptera, Calliphoridae)

Published online by Cambridge University Press:  28 February 2022

Xuewei Qi ,
Yaohui Wang ,
Guijian Zhang ,
Shuai Cao ,
Penghui Xu ,
Xueming Ren ,
Abdelaziz Mansour  and
Changying Niu Open the ORCID record for Changying Niu [Opens in a new window]
Xuewei Qi
Affiliation:
Hubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural University, Wuhan 430070, China
Yaohui Wang
Affiliation:
Hubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural University, Wuhan 430070, China
Guijian Zhang
Affiliation:
Hubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural University, Wuhan 430070, China
Shuai Cao
Affiliation:
Hubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural University, Wuhan 430070, China
Penghui Xu
Affiliation:
Hubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural University, Wuhan 430070, China
Xueming Ren
Affiliation:
Hubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural University, Wuhan 430070, China
Abdelaziz Mansour
Affiliation:
Hubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural University, Wuhan 430070, China Department of Economic Entomology and Pesticides, Faculty of Agriculture, Cairo University, 12613 Giza, Egypt
Changying Niu*
Affiliation:
Hubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural University, Wuhan 430070, China
*
Author for correspondence: Changying Niu, Email: niuchangying88@163.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Temperature strongly impacts the rates of physiological and biochemical processes, which in turn can determine the survival and population size of insects. At low temperatures performance is limited, however, cold tolerance and performance at low temperature can be improved after short- or long-term acclimation in many insect species. To understand mechanisms underlying acclimation, we sequenced and compared the transcriptome of the blowfly Chrysomya megacephala under rapid cold hardening (RCH) and long-term cold acclimation (LCA) conditions. The RCH response was dominated by genes related to immune response, spliceosome, and protein processing in endoplasmic reticulum with up-regulation during recovery from RCH. In contrast, LCA was associated with genes related to carbohydrate metabolism and cytoskeleton branching and stabilizing. Meanwhile, mRNA levels of genes related to glycerophospholipid metabolism, and some heat shock proteins (Hsps) were collectively up-regulated by both RCH and LCA. There were more genes and pathway adjustments associated with LCA than RCH. Overall, the transcriptome data provide basic information of molecular mechanisms underpinning the RCH and LCA response. The partly independent molecular responses to RCH and LCA suggest that several avenues for manipulating cold performance exist and RCH might be more effective as it only triggers fewer genes and affects the general metabolisms less. These observations provide some appropriate methods to improve cold tolerance of C. megacephala, and hold promise for developing an extended use of mass-reared C. megacephala with better cold performance as a pollinator of crops at low temperatures.

Keywords

Chrysomya megacephalacold acclimationrapid cold hardeningtranscriptome
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 3 , June 2022 , pp. 419 - 430
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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

Alonso, MA, Souza, CM, Linhares, AX and Thyssen, PJ (2015) Egg developmental time and survival of Chrysomya megacephala and Chrysomya putoria (Diptera: Calliphoridae) under different temperatures. Journal of Medical Entomology 52, 551–556.CrossRefGoogle ScholarPubMed
Armstrong, GA, Rodríguez, EC and Meldrum, RR (2012) Cold hardening modulates K+ homeostasis in the brain of Drosophila melanogaster during chill coma. Journal of Insect Physiology 58, 1511–1516.CrossRefGoogle ScholarPubMed
Barbosa, LS, Couri, MS, Coelho, VM and Avelino-Capistrano, F (2016) The classic episode of biological invasion: Cochliomyia macellaria (Fabricius, 1775) versus Chrysomya megacephala (Fabricius, 1794) (Diptera: Calliphoridae) – evaluation of the biotic potential. Anais Da Academia Brasileira de Ciências 88, 1401–1406.CrossRefGoogle ScholarPubMed
Bhatnagar, BS, Bogner, RH and Pikal, MJ (2007) Protein stability during freezing: separation of stresses and mechanisms of protein stabilization. Pharmaceutical Development and Technology 12, 505–523.CrossRefGoogle ScholarPubMed
Boersma, N, Boardman, L, Gilbert, M and Terblanche, JS (2019) Cold treatment enhances low-temperature flight performance in false codling moth, Thaumatotibia leucotreta (Lepidoptera: Tortricidae). Agricultural and Forest Entomology 21, 243–251.CrossRefGoogle Scholar
Brodie, BS, Smith, MA, Lawrence, J and Gries, G (2015) Effects of floral scent, color and pollen on foraging decisions and oocyte development of common green bottle flies. PLoS ONE 10, e0145055.CrossRefGoogle ScholarPubMed
Coello Alvarado, LE, MacMillan, HA and Sinclair, BJ (2015) Chill-tolerant Gryllus crickets maintain ion balance at low temperatures. Journal of Insect Physiology 77, 15–25.CrossRefGoogle ScholarPubMed
Colinet, H, Lee, SF and Hoffmann, A (2010) Knocking down expression of Hsp22 and Hsp23 by RNA interference affects recovery from chill coma in Drosophila melanogaster. Journal of Experimental Biology 213, 4146–4150.CrossRefGoogle ScholarPubMed
Cui, M, Hu, P, Wang, T, Tao, J and Zong, S (2017) Differential transcriptome analysis reveals genes related to cold tolerance in seabuckthorn carpenter moth, Eogystia hippophaecolus. PLoS ONE 12, e0187105.CrossRefGoogle ScholarPubMed
Des Marteaux, LE, McKinnon, AH, Udaka, H, Toxopeus, J and Sinclair, BJ (2017) Effects of cold-acclimation on gene expression in fall field cricket (Gryllus pennsylvanicus) ionoregulatory tissues. BMC Genomics 18, 357.CrossRefGoogle ScholarPubMed
Dutertre, M, Sanchez, G, Barbier, J, Corcos, L and Auboeuf, D (2011) The emerging role of pre-messenger RNA splicing in stress responses: sending alternative messages and silent messengers. RNA Biology 8, 740–747.CrossRefGoogle ScholarPubMed
Ellis, CR, Feltham, H, Park, K, Hanley, N and Goulson, D (2017) Seasonal complementary in pollinators of soft-fruit crops. Basic and Applied Ecology 19, 45–55.CrossRefGoogle Scholar
Enriquez, T, Renault, D, Charrier, M and Colinet, H (2018) Cold acclimation favors metabolic stability in Drosophila suzukii. Frontiers in Physiology 9, 1506.CrossRefGoogle ScholarPubMed
Fujikake, N, Nagai, Y, Popiel, HA, Kano, H, Yamaguchi, M and Toda, T (2005) Alternative splicing regulates the transcriptional activity of Drosophila heat shock transcription factor in response to heat/cold stress. FEBS Letters 579, 3842–3848.CrossRefGoogle ScholarPubMed
Fujiwara, Y and Denlinger, DL (2007) p38 MAPK is a likely component of the signal transduction pathway triggering rapid cold hardening in the flesh fly Sarcophaga crassipalpis. Journal of Experimental Biology 210, 3295–3300.CrossRefGoogle ScholarPubMed
Gerken, AR, Eller, OC, Hahn, DA and Morgan, TJ (2015) Constraints, independence, and evolution of thermal plasticity: probing genetic architecture of long- and short-term thermal acclimation. Proceedings of the National Academy of Sciences 112, 4399–4404.CrossRefGoogle ScholarPubMed
Gerken, AR, Eller-Smith, OC and Morgan, TJ (2018) Speed of exposure to rapid cold hardening and genotype drive the level of acclimation response in Drosophila melanogaster. Journal of Thermal Biology 76, 21–28.CrossRefGoogle ScholarPubMed
Grabherr, MG, Haas, BJ, Yassour, M, Levin, JZ, Thompson, DA, Amit, I, Adiconis, X, Fan, L, Raychowdhury, R, Zeng, Q, Chen, Z, Mauceli, E, Hacohen, N, Gnirke, A, Rhind, N, di Palma, F, Birren, BW, Nusbaum, C, Lindblad-Toh, K, Friedman, N and Regev, A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29, 644–652. doi: 10.1038/nbt.1883.CrossRefGoogle ScholarPubMed
Gruner, SV, Slone, DH, Capinera, JL and Turco, MP (2017) Development of the oriental latrine fly, Chrysomya megacephala (Diptera: Calliphoridae), at five constant temperatures. Journal of Medical Entomology 54, 290–298.Google Scholar
Huang, H, Xue, J, Zhuo, J, Cheng, R, Xu, H and Zhang, C (2017) Comparative analysis of the transcriptional responses to low and high temperatures in three rice planthopper species. Molecular Ecology 26, 2726–2737.CrossRefGoogle ScholarPubMed
Izadi, H, Mohammadzadeh, M and Mehrabian, M (2019) Cold tolerance of the Tribolium castaneum (Coleoptera: Tenebrionidae), under different thermal regimes: impact of cold acclimation. Journal of Economic Entomology 112, 1983–1988.CrossRefGoogle ScholarPubMed
Jensen, K, Sorensen, JG and Holmstrup, M (2019) Interactive effects of temperature and time on cold tolerance and spring predation in overwintering soil predatory mites (Gaeolaelaps aculeifer Canestrini). Biological Control 132, 169–176.CrossRefGoogle Scholar
Kim, M, Robich, RM, Rinehart, JP and Denlinger, DL (2006) Upregulation of two actin genes and redistribution of actin during diapause and cold stress in the northern house mosquito, Culex pipiens. Journal of Insect Physiology 52, 1226–1233.CrossRefGoogle ScholarPubMed
Kristensen, TN, Hoffmann, AA, Overgaard, J, Sorensen, JG, Hallas, R and Loeschcke, V (2007) Costs and benefits of cold acclimation in field-released Drosophila. Proceedings of the National Academy of Sciences 105, 216–221.CrossRefGoogle ScholarPubMed
Lee, RE Jr., Chen, CP and Denlinger, DL (1987) A rapid cold-hardening process in insects. Science (New York, N.Y.) 238, 1415–1417.CrossRefGoogle ScholarPubMed
Li, B and Dewey, CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323.CrossRefGoogle ScholarPubMed
Li, FQ, Fu, NN, Qu, C, Wang, R, Xu, YH and Luo, C (2017) Understanding the mechanisms of dormancy in an invasive alien Sycamore lace bug, Corythucha ciliata through transcript and metabolite profiling. Scientific Reports 7, 2631. doi: 10.1038/s41598-017-02876-wGoogle Scholar
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods (San Diego, Calif.) 25, 402–408.CrossRefGoogle Scholar
Luo, C (2018) Pollination efficiency of major pollinators for Jatropha curcas. Southwest China Journal of Agricultural Sciences 31, 849–855 (in Chinese).Google Scholar
MacMillan, HA, Ferguson, LV, Nicolai, A, Donini, A, Staples, JF and Sinclair, BJ (2014) Parallel ionoregulatory adjustments underlie phenotypic plasticity and evolution of Drosophila cold tolerance. Journal of Experimental Biology 218, 423–432.Google ScholarPubMed
MacMillan, HA, Knee, JM, Dennis, AB, Udaka, H, Marshall, KE, Merritt, TJ and Sinclair, BJ (2016) Cold acclimation wholly reorganizes the Drosophila melanogaster transcriptome and metabolome. Scientific Reports 6, 28999.CrossRefGoogle ScholarPubMed
Munawar, MS, Raja, S, Sarwar, G and Niaz, S (2011) Comparative performance of honeybees and blowflies in onion seed production. Journal of Agricultural research (Pakistan) 49, 49–56.Google Scholar
Nylin, S (2013) Induction of diapause and seasonal morphs in butterflies and other insects: knowns, unknowns and the challenge of integration. Physiological Entomology 38, 96–104.CrossRefGoogle Scholar
Overgaard, J and MacMillan, HA (2017) The integrative physiology of insect chill tolerance. Annual Review of Physiology 79, 187–208.CrossRefGoogle ScholarPubMed
Park, Y and Kim, Y (2014) A specific glycerol kinase induces rapid cold hardening of the diamondback moth, Plutella xylostella. Journal of Insect Physiology 67, 56–63.CrossRefGoogle ScholarPubMed
Ramírez, F and Davenport, TL (2016) Mango (Mangifera indica L.) pollination: a review. Scientia Horticulturae 203, 158–168.CrossRefGoogle Scholar
Rinehart, JP, Li, A, Yocum, GD, Robich, RM, Hayward, SAL and Denlinger, DL (2007) Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proceedings of the National Academy of Sciences 104, 11130–11137.CrossRefGoogle ScholarPubMed
Schou, MF, Kristensen, TN, Pedersen, A, Karlsson, BG, Loeschcke, V and Malmendal, A (2016) Metabolic and functional characterization of effects of developmental temperature in Drosophila melanogaster. American Journal of Physiology-Regulatory. Integrative and Comparative Physiology 312, R211–R222.CrossRefGoogle ScholarPubMed
Shearer, PW, West, JD, Walton, VM, Brown, PH, Svetec, N and Chiu, JC (2016) Seasonal cues induce phenotypic plasticity of Drosophila suzukii to enhance winter survival. BMC Ecology 16, 11.CrossRefGoogle ScholarPubMed
Shintani, Y and Ishikawa, Y (2007) Relationship between rapid cold hardening and cold acclimation in the eggs of the yellow-spotted longicorn beetle, Psacothea hilaris. Journal of Insect Physiology 53, 1055–1062.CrossRefGoogle ScholarPubMed
Sontigun, N, Sukontason, KL, Klong-Klaew, T, Sanit, S, Samerjai, C, Somboon, P, Thanapornpoonpong, SN, Amendt, J and Sukontason, K (2018) Bionomics of the oriental latrine fly Chrysomya megacephala (Fabricius) (Diptera: Calliphoridae): temporal fluctuation and reproductive potential. Parasites & Vectors 11, 415. doi: 10.1186/s13071-018-2986-2CrossRefGoogle ScholarPubMed
Sørensen, JG, Schou, MF, Kristensen, TN and Loeschcke, V (2016) Thermal fluctuations affect the transcriptome through mechanisms independent of average temperature. Scientific Reports 6, 30975. doi: 10.1038/srep30975.CrossRefGoogle ScholarPubMed
Stetina, T, Poupardin, R, Moos, M, Simek, P, Smilauer, P and Kostal, V (2019) Larvae of Drosophila melanogaster exhibit transcriptional activation of immune response pathways and antimicrobial peptides during recovery from supercooling stress. Insect Biochemistry and Molecular Biology 105, 60–68.CrossRefGoogle ScholarPubMed
Storey, KB, Baust, JG and Storey, JM (1981) Intermediary metabolism during low-temperature acclimation in the overwintering gall fly larva, Eurosta solidaginis. Journal of Comparative Physiology 144, 183–190.CrossRefGoogle Scholar
Sturn, A, Quackenbush, J and Trajanoski, Z (2002) Genesis: cluster analysis of microarray data. Bioinformatics (Oxford, England) 18, 207–208.CrossRefGoogle ScholarPubMed
Teets, NM and Denlinger, DL (2013) Physiological mechanisms of seasonal and rapid cold-hardening in insects. Physiological Entomology 38, 105–116.CrossRefGoogle Scholar
Teets, NM and Denlinger, DL (2016) Quantitative phosphoproteomics reveals signaling mechanisms associated with rapid cold hardening in a chill-tolerant fly. Journal of Proteome Research 15, 2855–2862.CrossRefGoogle Scholar
Teets, NM, Peyton, JT, Ragland, GJ, Colinet, H, Renault, D, Hahn, DA and Denlinger, DL (2012) Combined transcriptomic and metabolomic approach uncovers molecular mechanisms of cold tolerance in a temperate flesh fly. Physiological Genomics 44, 764–777.CrossRefGoogle Scholar
Teets, NM, Yi, SX, Lee, RE Jr. and Denlinger, DL (2013) Calcium signaling mediates cold sensing in insect tissues. Proceedings of the National Academy of Sciences 110, 9154–9159.CrossRefGoogle ScholarPubMed
Wang, J, Zhao, F and Lei, C (2005) Effect of Chrysomya megacephala (Fabricius.) pollination on yield of Brassica campestris. Chinese Journal of oil Crop Sciences 27, 31–34 (in Chinese).Google Scholar
Wang, J, Ma, YX, Cui, DL, Wang, RX, Lu, YY and Qin, J (2011) An observation on pollinating insects and their flower-visiting behavior on Fatsia japonica. Chinese Journal of Applied Entomology 48, 764–768 (in Chinese).Google Scholar
Wang, H, Li, K, Zhu, J, Fang, Q and Ye, G (2012) Cloning and expression pattern of heat shock protein genes from the endoparasitoid wasp, Pteromalus puparum in response to environmental stresses. Archives of Insect Biochemistry and Physiology 79, 247–263.CrossRefGoogle ScholarPubMed
Wang, X, Xiong, M, Wang, J, Lei, C and Zhu, F (2015 a) Reference gene stability of a synanthropic fly, Chrysomya megacephala. Parasites & Vectors 8, 565.CrossRefGoogle ScholarPubMed
Wang, X, Xiong, M, Lei, C and Zhu, F (2015 b) The developmental transcriptome of the synanthropic fly Chrysomya megacephala and insights into olfactory proteins. BMC Genomics 16, 20.CrossRefGoogle ScholarPubMed
Xu, J and James, RR (2012) Temperature stress affects the expression of immune response genes in the alfalfa leafcutting bee, Megachile rotundata. Insect Molecular Biology 21, 269–280.CrossRefGoogle ScholarPubMed
Yanagi, T, Miura, H, Isobe, S, Okuda, N and Yoshida, Y (2017) Effect of insect pollinator on inbreeding versus outbreeding in open pollinated strawberry seeds. Scientia Horticulturae 215, 112–116.CrossRefGoogle Scholar
Yang, S, Zhang, X, Wang, J, Wang, S, Pan, Y, Zhang, J and Xi, J (2018) Identification and analysis of up-regulated proteins in Lissorhoptrus oryzophilus adults for rapid cold hardening. Gene 642, 9–15.CrossRefGoogle ScholarPubMed
Zhang, M, Yu, H, Yang, YY, Song, C, Hu, XJ and Zhang, GR (2013) Analysis of the transcriptome of blowfly Chrysomya megacephala (Fabricius) larvae in responses to different edible oils. PLoS ONE 8, e63168.CrossRefGoogle ScholarPubMed
Supplementary material: File

Qi et al. supplementary material

Qi et al. supplementary material

Download Qi et al. supplementary material(File)
File 4.5 MB