Hostname: page-component-76fb5796d-r6qrq Total loading time: 0 Render date: 2024-04-26T11:52:01.069Z Has data issue: false hasContentIssue false
  • English
  • Français

Rapid cold hardening and cold acclimation promote cold tolerance of oriental fruit fly, Bactrocera dorsalis (Hendel) by physiological substances transformation and cryoprotectants accumulation

Published online by Cambridge University Press:  28 July 2023

Zifei Xie ,
Luchen Xu ,
Jie Zhao ,
Na Li ,
Deqiang Qin ,
Chun Xiao ,
Yongyue Lu  and
Zijun Guo Open the ORCID record for Zijun Guo [Opens in a new window]
Zifei Xie
Affiliation:
College of Plant Protection, Yunnan Agricultural University/State Key Laboratory of Yunnan Biological Resources Protection and Utilization, Kunming 650201, China
Luchen Xu
Affiliation:
College of Plant Protection, Yunnan Agricultural University/State Key Laboratory of Yunnan Biological Resources Protection and Utilization, Kunming 650201, China
Jie Zhao
Affiliation:
State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China
Na Li
Affiliation:
College of Plant Protection, Yunnan Agricultural University/State Key Laboratory of Yunnan Biological Resources Protection and Utilization, Kunming 650201, China
Deqiang Qin
Affiliation:
College of Plant Protection, Yunnan Agricultural University/State Key Laboratory of Yunnan Biological Resources Protection and Utilization, Kunming 650201, China
Chun Xiao
Affiliation:
College of Plant Protection, Yunnan Agricultural University/State Key Laboratory of Yunnan Biological Resources Protection and Utilization, Kunming 650201, China
Yongyue Lu
Affiliation:
College of Plant Protection, South China Agricultural University, Guangzhou 510640, China
Zijun Guo*
Affiliation:
College of Plant Protection, Yunnan Agricultural University/State Key Laboratory of Yunnan Biological Resources Protection and Utilization, Kunming 650201, China
*
Corresponding author: Zijun Guo; Email: ynau_gzj@126.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Insect response to cold stress is often associated with adaptive strategies and chemical variation. However, low-temperature domestication to promote the cold tolerance potential of Bactrocera dorsalis and transformation of main internal substances are not clear. Here, we use a series of low-temperature exposure experiments, supercooling point (SCP) measurement, physiological substances and cryoprotectants detection to reveal that pre-cooling with milder low temperatures (5 and 10°C) for several hours (rapid cold hardening) and days (cold acclimation) can dramatically improve the survival rate of adults and pupae under an extremely low temperature (−6.5°C). Besides, the effect of rapid cold hardening for adults could be maintained even 4 h later with 25°C exposures, and SCP was significantly declined after cold acclimation. Furthermore, content of water, fat, protein, glycogen, sorbitol, glycerol and trehalose in bodies were measured. Results showed that water content was reduced and increased content of proteins, glycogen, glycerol and trehalose after two cold domestications. Our findings suggest that rapid cold hardening and cold acclimation could enhance cold tolerance of B. dorsalis by increasing proteins, glycerol, trehalose and decreasing water content. Conclusively, identifying a physiological variation will be useful for predicting the occurrence and migration trend of B. dorsalis populations.

Keywords

Bactrocera dorsalis (Hendel)cold acclimationcold tolerancecryoprotectantrapid cold hardening
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 113 , Issue 4 , August 2023 , pp. 574 - 586
Check for updates
Copyright
Copyright © The Author(s), 2023. 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.)

Footnotes

*

Equal contributors.

References

Ahn, JJ, Choi, K, Huang, S, Al Baki, MA, Ahmed, S and Kim, Y (2018) Calcium/calmodulin-dependent protein kinase II of the oriental fruit fly, Bactrocera dorsalis, and its association with rapid cold hardiness. Journal of Asia-Pacific Entomology 21, 1275–1282.CrossRefGoogle Scholar
Bale, J (1996) Insect cold hardiness: a matter of life and death. European Journal of Entomology 93, 369–382.Google Scholar
Benelli, G, Daane, KM, Canale, A, Niu, C, Messing, RH and Vargas, RI (2014) Sexual communication and related behaviours in Tephritidae: current knowledge and potential applications for Integrated Pest Management. Journal of Pest Science 87, 385–405.CrossRefGoogle Scholar
Bürgi, LP and Mills, NJ (2010) Cold tolerance of the overwintering larval instars of light brown apple moth Epiphyas postvittana. Journal of Insect Physiology 56, 1645–1650.CrossRefGoogle ScholarPubMed
Chen, H, Liang, GM, Zou, LY, Guo, F, Wu, KM and Guo, YY (2010) Research progresses in the cold hardiness of insects. Plant Protection Science 36, 18–24.Google Scholar
Clarke, AR, Armstrong, KF, Carmichael, AE, Milne, JR, Raghu, S, Roderick, GK and Yeates, DK (2005) Invasive phytophagous pests arising through a recent tropical evolutionary radiation: the Bactrocera dorsalis complex of fruit flies. Annual Review of Entomology 50, 293–319.CrossRefGoogle ScholarPubMed
Dong, YX, Pei, JH, Shao, YY, Zong, SX and Hou, ZH (2021) Cold tolerance and cold tolerant substances of larva and adult of Dendroctonus valens LeConte. Journal of Environmental Entomology 43, 978–985.Google Scholar
Duman, JG, Bennett, V, Sformo, T, Hochstrasser, R and Barnes, BM (2004) Antifreeze proteins in Alaskan insects and spiders. Journal of Insect Physiology 50, 259–266.CrossRefGoogle ScholarPubMed
Durak, R, Depciuch, J, Kapusta, I, Kisała, J and Durak, T (2021) Changes in chemical composition and accumulation of cryoprotectants as the adaptation of anholocyclic aphid Cinara tujafilina to overwintering. International Journal of Molecular Sciences 22, 511.CrossRefGoogle ScholarPubMed
Fahim, RM, Wang, YC, Cai, ZH, Bai, S, Yao, ZC, Anwar, AU, Zhang, ZY, Zheng, WW and Zhang, HY (2020) Gut microbiota promotes host resistance to low-temperature stress by stimulating its arginine and proline metabolism pathway in adult Bactrocera dorsalis. PLoS Pathogens 16, e1008441.Google Scholar
Feng, YQ, Zhang, L, Li, WB, Yang, X and Zong, SX (2017) Cold hardiness of overwintering larvae of Sphenoptera sp. (Coleoptera: Buprestidae) in Western China. Journal of Economic Entomology 111, 247–251.CrossRefGoogle Scholar
Fuller, BJ (2004) Cryoprotectants: the essential antifreezes to protect life in the frozen state. Cryo-Letters 25, 375.Google ScholarPubMed
Guo, ZJ, Lu, YY, Yang, F, Zeng, L, Liang, GW and Xu, YJ (2017) Transmission modes of a pesticide-degrading symbiont of the oriental fruit fly Bactrocera dorsalis (Hendel). Applied Microbiology and Biotechnology 101, 8543–8556.CrossRefGoogle ScholarPubMed
Han, RD, Sun, XG, Xu, YY and Zhang, WG (2005) The biochemical mechanism of cold-hardiness in overwintering larva of Dend rolimus spectabilis Butler (Lepidoptera: Lasiocampidae). Acta Ecologica Sinica 25, 1352–1356.Google Scholar
Heydari, M and Izadi, H (2014) Effects of seasonal acclimation on cold tolerance and biochemical status of the carob moth, Ectomyelois ceratoniae Zeller, last instar larvae. Bulletin of Entomological Research 104, 592–600.CrossRefGoogle ScholarPubMed
Hou, BH and Zhang, RJ (2005) Potential distributions of the fruit fly Bactrocera dorsalis (Diptera: Tephritidae) in China as predicted by CLIMEX. Acta Ecologica Sinica 25, 1569–1574.Google Scholar
Huang, NN (2014) Study on Tolerance of Melon fly, Bactrocera cucuribitae Coquillett to Low Temperature and Its Physiological and Biochemical Mechanisms. Wuhan, China: Huazhong Agriculture University.Google Scholar
Kang, L, Chen, B, Wei, JN and Liu, TX (2009) Roles of thermal adaptation and chemical ecology in Liriomyza distribution and control. Annual Review of Entomology 54, 127–145.CrossRefGoogle ScholarPubMed
Kelty, JD and Lee, JRE (1999) Induction of rapid cold hardening by cooling at ecologically relevant rates in Drosophila melanogaster. Journal of Insect Physiology 45, 719–726.CrossRefGoogle ScholarPubMed
Kim, Y and Kim, N (1997) Cold hardiness in Spodoptera exigua (Lepidoptera: Nocuidae). Environmental Entomology 26, 1117–1123.CrossRefGoogle Scholar
Kostal, V, Zahradnickova, H, Simek, P and Zeleny, J (2007) Multiple component system of sugars and polyols in the overwintering spruce bark beetle, Ips typographus. Journal of Insect Physiology 53, 580–586.CrossRefGoogle ScholarPubMed
Koveos, DS (2001) Rapid cold hardening in the olive fruit fly Bactrocera oleae under laboratory and field conditions. Entomologia Experimentalis et Applicata 101, 257–263.CrossRefGoogle Scholar
Kristiansen, E, Ramløv, H, Hagen, L, Pedersen, SA, Andersen, RA and Zachariassen, KE (2005) Isolation and characterization of hemolymph antifreeze proteins from larvae of the longhorn beetle Rhagium inquisitor (L.). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 142, 90–97.CrossRefGoogle ScholarPubMed
Larsen, KJ and Lee, RE (1994) Cold tolerance including rapid cold-hardening and inoculative freezing of fall migrant monarch butterflirs in Ohio. Journal of Insect Physiology 40, 859–864.CrossRefGoogle Scholar
Lee, REJ, Chen, CP and Denlinger, DL (1987) A rapid cold-hardening process in insects. Science (American Association for the Advancement of Science) 238, 1415–1417.CrossRefGoogle ScholarPubMed
Lehmann, P, Lyytinen, A, Sinisalo, T and Lindström, L (2012) Population dependent effects of photoperiod on diapause related physiological traits in an invasive beetle (Leptinotarsa decemlineata). Journal of Insect Physiology 58, 1146–1158.CrossRefGoogle Scholar
Li, NG (2012) Relationships between cold hardiness, and ice nucleating activity, glycerol and protein contents in the hemolymph of caterpillars, Aporia crataegi L. Cryo-Letters 33, 135.Google ScholarPubMed
Li, XP, Song, LW, Zhang, HH, Chen, YQ, Zuo, TT, Wang, J and Sun, W (2012) Responses of Arma chinensis cold tolerance to rapid cold hardening and underlying physiological mechanisms. Chinese Journal of Applied Ecology 23, 791–797.Google ScholarPubMed
Mohammadzadeh, M, Borzoui, E and Izadi, H (2017) Physiological and biochemical differences in diapausing and nondiapausing larvae of Eurytoma plotnikovi (Hymenoptera: Eurytomidae). Environmental Entomology 46, 1424–1431.CrossRefGoogle ScholarPubMed
Nieminen, P, Käkelä, R, Paakkonen, T, Halonen, T and Mustonen, A (2013) Fatty acid modifications during autumnal cold-hardening in an obligatory ectoparasite, the deer ked (Lipoptena cervi). Journal of Insect Physiology 59, 631–637.CrossRefGoogle Scholar
Park, Y, Kim, Y, Park, G, Lee, J and Lee, K (2017) Supercooling capacity along with up-regulation of glycerol content in an overwintering butterfly, Parnassius bremeri. Journal of Asia-Pacific Entomology 20, 949–954.CrossRefGoogle Scholar
Powell, SJ and Bale, JS (2004) Cold shock injury and ecological costs of rapid cold hardening in the grain aphid Sitobion avenae (Hemiptera: Aphididae). Journal of Insect Physiology 50, 277–284.CrossRefGoogle ScholarPubMed
Rajamohan, A and Sinclair, BJ (2008) Short term hardening effects on survival of acute and chronic cold exposure by Drosophila melanogaster larvae. Journal of Insect Physiology 54, 708–718.CrossRefGoogle ScholarPubMed
Ren, L (2006) Adaptive Response of Bactrocera dorsalis (Hendel) to Several Environmental Stresses. South China Agricultural University.Google Scholar
Sadeghi, R, Izadi, H and Mahdian, K (2012) Energy allocation changes in overwintering adults of the common pistachio Psylla, Agonoscena pistaciae Burckhardt & Lauterer (Hemiptera: Psyllidae). Neotropical Entomology 41, 493–498.CrossRefGoogle ScholarPubMed
Saeidi, M and Moharramipour, S (2017) Physiology of cold hardiness, seasonal fluctuations, and cryoprotectant contents in overwintering adults of Hypera postica (Coleoptera: Curculionidae). Environmental Entomology 46, 960–966.CrossRefGoogle ScholarPubMed
Sørensen, JG, Kristensen, TN and Loeschcke, V (2003) The evolutionary and ecological role of heat shock proteins. Ecology Letters 6, 1025–1037.CrossRefGoogle Scholar
Teets, NM and Denlinger, DL (2013) Physiological mechanisms of seasonal and rapid cold-hardening in insects. Physiological Entomology 38, 105–116.CrossRefGoogle Scholar
Walters, KF, Bale, JS and McDonald, JR (1997) Rapid cold hardening in the western flower thrips Frankliniella occidentalis. Journal of Insect Physiology 43, 759–766.Google ScholarPubMed
Wang, X and Kang, L (2003) Rapid cold hardening in young hoppers of the migratory locust Locusta migratoria L. (Orthoptera: Acridiidae). Cryo-Letters 24, 331.Google ScholarPubMed
Wang, JH, Zeng, L and Han, ZJ (2014) An assessment of cold hardiness and biochemical adaptations for cold tolerance among different geographic populations of the Bactrocera dorsalis (Diptera: Tephritidae) in China. Journal of Insect Science (Tucson, Ariz.) 14, 292.Google ScholarPubMed
Wang, J, Gao, GQ, Zhang, RR, Dai, LL and Chen, H (2017) Metabolism and cold tolerance of Chinese white pine beetle Dendroctonus armandi (Coleoptera: Curculionidae: Scolytinae) during the overwintering period. Agricultural and Forest Entomology 19, 10–22.CrossRefGoogle Scholar
Wang, DY, Ru, YT, Wang, Y, Ma, YY, Na, S, Sun, LZ, Jiang, YR and Qin, L (2018) Gene expression patterns and activities of trehalases in Antheraea pernyi (Lepidoptera: Saturniidae) pupae during diapause and diapause termination. Acta Entomologica Sinica 61, 784–794.Google Scholar
Williams, CM, Nicolai, A, Ferguson, LV, Bernards, MA, Hellmann, JJ and Sinclair, BJ (2014) Cold hardiness and deacclimation of overwintering Papilio zelicaon pupae. Comparative biochemistry and physiology. Part A, Molecular & Integrative Physiology 178, 51–58.CrossRefGoogle ScholarPubMed
Worland, MR and Block, W (2003) Desiccation stress at sub-zero temperatures in polar terrestrial arthropods. Journal of Insect Physiology 49, 193–203.CrossRefGoogle ScholarPubMed
Worland, MR, Leinaas, HP and Chown, SL (2006) Supercooling point frequency distributions in Collembola are affected by moulting. Functional Ecology 20, 323–329.CrossRefGoogle Scholar
Xu, LR, He, KL and Wang, ZY (2012) Studies on variation in cold hardiness in relation to the in vivo water, lipid and sugar content of Conogethes punctiferalis (Guenée) larvae living on three different host plant species. Chinese Journal of Applied Entomology 49, 197–204.Google Scholar
Yang, GP, Wen, JH, Han, YQ and Hou, ML (2018) Rapid cold hardening confers a transient increase in low temperature survival in diapausing Chilo suppressalis larvae. Insects 9, 53.CrossRefGoogle ScholarPubMed
Yang, HB, Hu, ZJ, Dong, JF and Li, DX (2019) Changes in the cold hardiness of overwintering larvae of Histia rhodope (Lepidoptera: Zygaenidae). Acta Entomologica Sinica 62, 979–986.Google Scholar
Yin, YC and Wang, QY (2014) Beware of Bactrocera dorsalis, a new pest in northern orchards. Hebei Agriculture 11, 48–49.Google Scholar
Yu, ZJ, Lu, YL, Yang, XL, Chen, J, Wang, H, Wang, D and Liu, JZ (2014) Cold hardiness and biochemical response to low temperature of the unfed bush tick Haemaphysalis longicornis (Acari: Ixodidae). Parasites & Vectors 7, 346–346.CrossRefGoogle ScholarPubMed
Zhang, YA and Zhao, XQ (1994) A study on Bactrocera dorsalis in Sichuan. Southwest China Journal of Agricultural Sciences 7, 71–75.Google Scholar
Zhao, J, Chen, ZZ, Qu, JJ, Zhang, F, Yin, XC and Xu, YY (2010) Responses of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) adults to cold acclimation and the related changes of activities of several enzymes in their bodies. Acta Entomologica Sinica 53, 147–153.Google Scholar
Zhu, YF, Shang, MQ, Teng, ZW, Tan, XM, Guo, Y, Jin, MJ, Wan, FH and Zhou, HX (2020) Analysis of invasion, distribution and spreading trend of Bactrocera dorsalis. Shandong Agricultural Sciences 52, 141–149.Google Scholar