Insect cross-tolerance to freezing and drought stress: role of metabolic rearrangement

. 2022 Jun 08 ; 289 (1976) : 20220308. [epub] 20220608

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid35673862

The accumulation of trehalose has been suggested as a mechanism underlying insect cross-tolerance to cold/freezing and drought. Here we show that exposing diapausing larvae of the drosophilid fly, Chymomyza costata to dry conditions significantly stimulates their freeze tolerance. It does not, however, improve their tolerance to desiccation, nor does it significantly affect trehalose concentrations. Next, we use metabolomics to compare the complex alterations to intermediary metabolism pathways in response to three environmental factors with different ecological meanings: environmental drought (an environmental stressor causing mortality), decreasing ambient temperatures (an acclimation stimulus for improvement of cold hardiness), and short days (an environmental signal inducing diapause). We show that all three factors trigger qualitatively similar metabolic rearrangement and a similar phenotypic outcome-improved larval freeze tolerance. The similarities in metabolic response include (but are not restricted to) the accumulation of typical compatible solutes and the accumulation of energy-rich molecules (phosphagens). Based on these results, we suggest that transition to metabolic suppression (a state in which chemical energy demand is relatively low but need for stabilization of macromolecules is high) represents a common axis of metabolic pathway reorganization towards accumulation of non-toxic cytoprotective compounds, which in turn stimulates larval freeze tolerance.

Zobrazit více v PubMed

Sinclair B, Ferguson L, Salehipour-shirazi G, MacMillan H. 2013. Cross-tolerance and cross-talk in the cold: relating low temperatures to desiccation and immune stress in insects. Integr. Comp. Biol. 53, 545. (10.1093/icb/ict004) PubMed DOI

Kaunisto S, Ferguson LV, Sinclair BJ. 2016. Can we predict the effects of multiple stressors on insects in a changing climate? Curr. Opin. Insect Sci. 17, 55-61. (10.1016/j.cois.2016.07.001) PubMed DOI

Todgham AE, Stillman JH. 2013. Physiological responses to shifts in multiple environmental stressors: relevance in a changing world. Integr. Comp. Biol. 53, 539-544. (10.1093/icb/ict086) PubMed DOI

Danks H. 2000. Dehydration in dormant insects. J. Insect Physiol. 46, 837-852. (10.1016/S0022-1910(99)00204-8) PubMed DOI

Block W. 1996. Cold or drought—the lesser of two evils for terrestrial arthropods? Eur. J. Entomol. 93, 325-340.

Sinclair BJ. 1999. Insect cold tolerance: How many kinds of frozen? Eur. J. Entomol. 96, 157-164.

Storey KB, Storey JM. 1988. Freeze tolerance in animals. Physiol. Rev. 68, 27-84. (10.1152/physrev.1988.68.1.27) PubMed DOI

Lovelock J. 1954. The protective action of neutral solutes against haemolysis by freezing and thawing. Biochem. J. 56, 265-270. (10.1042/bj0560265) PubMed DOI PMC

Muldrew K, Acker JP, Elliott JA, McGann LE. 2004. The water to ice transition: implications for living cells. In Life in the frozen state (eds Fuller BJ, Lane N, Benson EE), pp. 93-134. Boca Raton, FL: CRC Press.

Mazur P. 1984. Freezing of living cells: mechanisms and implications. Am. J. Physiol. 247, C125-C142. (10.1152/ajpcell.1984.247.3.C125) PubMed DOI

Ring R, Danks H. 1994. Desiccation and cryoprotection: overlapping adaptations. Cryo-letters 15, 181-190.

Sinclair BJ, Chown SL. 2003. Rapid responses to high temperature and desiccation but not to low temperature in the freeze tolerant sub-Antarctic caterpillar Pringleophaga marioni (Lepidoptera, Tineidae). J. Insect Physiol. 49, 45-52. (10.1016/S0022-1910(02)00225-1) PubMed DOI

Levis NA, Yi S-X, Lee RE. 2012. Mild desiccation rapidly increases freeze tolerance of the goldenrod gall fly, Eurosta solidaginis: evidence for drought-induced rapid cold-hardening. J. Exp. Biol. 215, 3768-3773. (10.1242/jeb.076885) PubMed DOI

Hayward SA, Rinehart JP, Sandro LH, Lee RE, Denlinger DL. 2007. Slow dehydration promotes desiccation and freeze tolerance in the Antarctic midge Belgica antarctica. J. Exp. Biol. 210, 836-844. (10.1242/jeb.02714) PubMed DOI

Elnitsky MA, Hayward SA, Rinehart JP, Denlinger DL, Lee RE. 2008. Cryoprotective dehydration and the resistance to inoculative freezing in the Antarctic midge, Belgica antarctica. J. Exp. Biol. 211, 524-530. (10.1242/jeb.011874) PubMed DOI

Hackman W, LAKovAARA S, Saura A, Sorsa M, Vepsalainen K. 1970. On the biology and karyology of Chymomyza costata Zetterstedt, with reference to the taxonomy and distribution of various species of Chymomyza (Dipt., Drosophilidae). Ann. Entomol. Fenn. 36, 1-9.

Koštál V, Zahradníčková H, Šimek P. 2011. Hyperprolinemic larvae of the drosophilid fly, Chymomyza costata, survive cryopreservation in liquid nitrogen. Proc. Natl Acad. Sci. USA 108, 13 041-13 046. (10.1073/pnas.1107060108) PubMed DOI PMC

Rozsypal J, Moos M, Šimek P, Koštál V. 2018. Thermal analysis of ice and glass transitions in insects that do and do not survive freezing. J. Exp. Biol. 221, 170464. (10.1242/jeb.170464) PubMed DOI

Des Marteaux LE, Hůla P, Koštál V. 2019. Transcriptional analysis of insect extreme freeze tolerance. Proc. R. Soc. B 286, 20192019. (10.1098/rspb.2019.2019) PubMed DOI PMC

Grimaldi D. 1986. The Chymomyza aldrichii species-group (Diptera: Drosophilidae); relationships, new neotropical species, and the evolution of some sexual traits. J. N. Y. Entomol. Soc. 94, 342-371.

Markow TA, O'Grady PM. 2006. Phylogenetic relationships of Drosophilidae. In Drosophila: A guide to species identification and use (eds Markow TA, O'Grady PM), pp. 3-64. London, UK: Academic Press.

Band H, Band R. 1982. Multiple overwintering mechanisms in Chymomyza amoena larvae (Diptera: Drosophilidae) and laboratory induction of freeze tolerance. Experientia 38, 1448-1449. (10.1007/BF01955762) DOI

Rinehart JP, Hayward SA, Elnitsky MA, Sandro LH, Lee RE, Denlinger DL. 2006. Continuous up-regulation of heat shock proteins in larvae, but not adults, of a polar insect. Proc. Natl Acad. Sci. USA 103, 14 223-14 227. (10.1073/pnas.0606840103) PubMed DOI PMC

Hand SC, Menze MA, Toner M, Boswell L, Moore D. 2011. LEA proteins during water stress: not just for plants anymore. Annu. Rev. Physiol. 73, 115-134. (10.1146/annurev-physiol-012110-142203) PubMed DOI

Holmstrup M, Hedlund K, Boriss H. 2002. Drought acclimation and lipid composition in Folsomia candida: implications for cold shock, heat shock and acute desiccation stress. J. Insect Physiol. 48, 961-970. (10.1016/S0022-1910(02)00175-0) PubMed DOI

Lopez-Martinez G, Elnitsky MA, Benoit JB, Lee RE Jr, Denlinger DL. 2008. High resistance to oxidative damage in the Antarctic midge Belgica antarctica, and developmentally linked expression of genes encoding superoxide dismutase, catalase and heat shock proteins. Insect Biochem. Mol. Biol. 38, 796-804. (10.1016/j.ibmb.2008.05.006) PubMed DOI

Philip BN, Yi S-X, Elnitsky MA, Lee RE. 2008. Aquaporins play a role in desiccation and freeze tolerance in larvae of the goldenrod gall fly, Eurosta solidaginis. J. Exp. Biol. 211, 1114-1119. (10.1242/jeb.016758) PubMed DOI

Ring R, Danks H. 1998. The role of trehalose in cold-hardiness and desiccation. CryoLetters 19, 275-282.

Benoit JB, Lopez-Martinez G, Michaud MR, Elnitsky MA, Lee RE Jr, Denlinger DL. 2007. Mechanisms to reduce dehydration stress in larvae of the Antarctic midge, Belgica antarctica. J. Insect Physiol. 53, 656-667. (10.1016/j.jinsphys.2007.04.006) PubMed DOI

Tapia H, Koshland DE. 2014. Trehalose is a versatile and long-lived chaperone for desiccation tolerance. Curr. Biol. 24, 2758-2766. (10.1016/j.cub.2014.10.005) PubMed DOI

Crowe JH, Hoekstra FA, Crowe LM. 1992. Anhydrobiosis. Annu. Rev. Physiol. 54, 579-599. (10.1146/annurev.ph.54.030192.003051) PubMed DOI

Storey KB, Storey JM. 2013. Molecular biology of freezing tolerance. Compr. Physiol. 3, 1283-1308. (10.1002/cphy.c130007) PubMed DOI

Toxopeus J, Sinclair BJ. 2018. Mechanisms underlying insect freeze tolerance. Biol. Rev. 93, 1891-1914. (10.1111/brv.12425) PubMed DOI

Thompson SN. 2003. Trehalose—the insect ‘blood'sugar. Adv. Insect Physiol. 31, 205-285. (10.1016/S0065-2806(03)31004-5) DOI

Yancey PH. 2005. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol. 208, 2819-2830. (10.1242/jeb.01730) PubMed DOI

Crowe JH. 2007. Trehalose as a ‘chemical chaperone’. In Molecular aspects of the stress response: chaperones, membranes and networks (eds Csermely P, Vígh L), pp. 143-158. Berlin, Germany: Springer.

Timasheff SN. 2002. Protein-solvent preferential interactions, protein hydration, and the modulation of biochemical reactions by solvent components. Proc. Natl Acad. Sci. USA 99, 9721-9726. (10.1073/pnas.122225399) PubMed DOI PMC

Olgenblum GI, Sapir L, Harries D. 2020. Properties of aqueous trehalose mixtures: glass transition and hydrogen bonding. J. Chem. Theory Comput. 16, 1249-1262. (10.1021/acs.jctc.9b01071) PubMed DOI PMC

Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN. 1982. Living with water stress: evolution of osmolyte systems. Science 217, 1214-1222. (10.1126/science.7112124) PubMed DOI

Hochachka PW, Somero GN. 2002. Biochemical adaptation: mechanism and process in physiological evolution. Oxford, UK: Oxford University Press.

Pullin AS. 1996. Physiological relationships between insect diapause and cold tolerance: coevolution or coincidence. Eur. J. Entomol. 93, 121-130.

Kučera L, et al. 2022. A mixture of innate cryoprotectants is key for freeze tolerance and cryopreservation of a drosophilid fly larva. J. Exp. Biol. 225, jeb243934. (10.1242/jeb.243934) PubMed DOI

Riihimaa, Kimura. 1988.

Kostal V, Noguchi H, Shimada K, Hayakawa Y. 1998. Developmental changes in dopamine levels in larvae of the fly Chymomyza costata: comparison between wild-type and mutant-nondiapause strains. J. Insect Physiol. 44, 605-614. (10.1016/S0022-1910(98)00043-2) PubMed DOI

Lakovaara S. 1969. Malt as a culture medium for Drosophila species. Drosophila Inf. Serv. 44, 128.

De Mercado E, Hernandez M, Sanz E, Rodriguez A, Gomez E, Vazquez J, Martinez E, Roca J. 2009. Evaluation of l-glutamine for cryopreservation of boar spermatozoa. Anim. Reprod. Sci. 115, 149-157. (10.1016/j.anireprosci.2008.11.014) PubMed DOI

Koštál V, Štětina T, Poupardin R, Korbelová J, Bruce AW. 2017. Conceptual framework of the eco-physiological phases of insect diapause development justified by transcriptomic profiling. Proc. Natl Acad. Sci. USA 114, 8532-8537. (10.1073/pnas.1707281114) PubMed DOI PMC

Moos M, Korbelová J, Štětina T, Opekar S, Šimek P, Grgac R, Koštál V. 2022. Cryoprotective metabolites are sourced from both external diet and internal macromolecular reserves during metabolic reprogramming for freeze tolerance in drosophilid fly, Chymomyza costata. Metabolites 12, 163. (10.3390/metabo12020163) PubMed DOI PMC

ter Braak CJ, Šmilauer P. 2012. Canoco reference manual and user's guide: software for ordination (version 5.0) . Ithaca, NY: Microcomputer Power.

Benoit JB, Lopez-Martinez G, Elnitsky MA, Lee RE Jr, Denlinger DL. 2009. Dehydration-induced cross tolerance of Belgica antarctica larvae to cold and heat is facilitated by trehalose accumulation. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 152, 518-523. (10.1016/j.cbpa.2008.12.009) PubMed DOI

Koštál V, Korbelová J, Poupardin R, Moos M, Šimek P. 2016. Arginine and proline applied as food additives stimulate high freeze tolerance in larvae of Drosophila melanogaster. J. Exp. Biol. 219, 2358-2367. (10.1242/jeb.142158) PubMed DOI

Koštál V, Šimek P, Zahradníčková H, Cimlová J, Štětina T. 2012. Conversion of the chill susceptible fruit fly larva (Drosophila melanogaster) to a freeze tolerant organism. Proc. Natl Acad. Sci. USA 109, 3270-3274. (10.1073/pnas.1119986109) PubMed DOI PMC

Li Y, Zhang L, Chen H, Koštál V, Simek P, Moos M, Denlinger DL. 2015. Shifts in metabolomic profiles of the parasitoid Nasonia vitripennis associated with elevated cold tolerance induced by the parasitoid's diapause, host diapause and host diet augmented with proline. Insect Biochem. Mol. Biol. 63, 34-46. (10.1016/j.ibmb.2015.05.012) PubMed DOI

Zhang L, et al. 2016. L-proline: a highly effective cryoprotectant for mouse oocyte vitrification. Sci. Rep. 6, 1-8. (10.1038/s41598-016-0001-8) PubMed DOI PMC

Dou M, Li Y, Sun Z, Li L, Rao W. 2019. L-proline feeding for augmented freeze tolerance of Camponotus japonicus Mayr. Sci. Bull. 64, 1795-1804. (10.1016/j.scib.2019.09.028) PubMed DOI

Tuncer PB, Sarıözkan S, Bucak MN, Ulutaş PA, Akalın PP, Büyükleblebici S, Canturk F. 2011. Effect of glutamine and sugars after bull spermatozoa cryopreservation. Theriogenology 75, 1459-1465. (10.1016/j.theriogenology.2010.12.006) PubMed DOI

Toxopeus J, Koštál V, Sinclair BJ. 2019. Evidence for non-colligative function of small cryoprotectants in a freeze-tolerant insect. Proc. R. Soc. B 286, 20190050. (10.1098/rspb.2019.0050) PubMed DOI PMC

Gertrudes A, Craveiro R, Eltayari Z, Reis RL, Paiva A, Duarte ARC. 2017. How do animals survive extreme temperature amplitudes? The role of natural deep eutectic solvents. ACS Sustain. Chem. Eng. 5, 9542-9553. (10.1021/acssuschemeng.7b01707) DOI

Xin Z, Browse J. 2000. Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ. 23, 893-902. (10.1046/j.1365-3040.2000.00611.x) DOI

Arakawa T, Timasheff S. 1985. The stabilization of proteins by osmolytes. Biophys. J. 47, 411-414. (10.1016/S0006-3495(85)83932-1) PubMed DOI PMC

Rasmussen PH, Jørgensen B, Nielsen J. 1997. Aqueous solutions of proline and NaCl studied by differential scanning calorimetry at subzero temperatures. Thermochim. Acta 303, 23-30. (10.1016/S0040-6031(97)00241-4) DOI

Crowe JH, Carpenter JF, Crowe LM. 1998. The role of vitrification in anhydrobiosis. Annu. Rev. Physiol. 60, 73-103. (10.1146/annurev.physiol.60.1.73) PubMed DOI

McLain SE, Soper AK, Terry AE, Watts A. 2007. Structure and hydration of L-proline in aqueous solutions. J. Phys. Chem. B 111, 4568-4580. (10.1021/jp068340f) PubMed DOI

Troitzsch R, Vass H, Hossack W, Martyna G, Crain J. 2008. Molecular mechanisms of cryoprotection in aqueous proline: light scattering and molecular dynamics simulations. J. Phys. Chem. B 112, 4290-4297. (10.1021/jp076713m) PubMed DOI

de Molina PM, Alvarez F, Frick B, Wildes A, Arbe A, Colmenero J. 2017. Investigation of the dynamics of aqueous proline solutions using neutron scattering and molecular dynamics simulations. Phys. Chem. Chem. Phys. 19, 27 739-27 754. (10.1039/C7CP05474B) PubMed DOI

Choi YH, van Spronsen J, Dai Y, Verberne M, Hollmann F, Arends IW, Witkamp G-J, Verpoorte R. 2011. Are natural deep eutectic solvents the missing link in understanding cellular metabolism and physiology? Plant Physiol. 156, 1701-1705. (10.1104/pp.111.178426) PubMed DOI PMC

Amidi F, Pazhohan A, Nashtaei MS, Khodarahmian M, Nekoonam S. 2016. The role of antioxidants in sperm freezing: a review. Cell Tissue Bank. 17, 745-756. (10.1007/s10561-016-9566-5) PubMed DOI

Wilsterman K, Ballinger MA, Williams CM. 2021. A unifying, eco-physiological framework for animal dormancy. Funct. Ecol. 35, 11-31. (10.1111/1365-2435.13718) DOI

Yancey PH, Siebenaller JF. 2015. Co-evolution of proteins and solutions: protein adaptation versus cytoprotective micromolecules and their roles in marine organisms. J. Exp. Biol. 218, 1880-1896. (10.1242/jeb.114355) PubMed DOI

Hula P, Moos M, Marteaux LD, Šimek P, Koštál V. 2022. Insect cross-tolerance to freezing and drought stress: role of metabolic rearrangement. FigShare. (10.6084/m9.figshare.c.6006457) PubMed DOI PMC

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Insect cross-tolerance to freezing and drought stress: role of metabolic rearrangement

. 2022 Jun 08 ; 289 (1976) : 20220308. [epub] 20220608

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...