Abstract
One of the major impacts of climate change has been the marked rise in global temperature. Recently, we demonstrated that high temperatures (1-week exposure) disrupt prooxidant-antioxidant homeostasis and promote cellular apoptosis in the American oyster. In this study, we evaluated the effects of seasonal sea surface temperature (SST) on tissue morphology, extrapallial fluid (EPF) conditions, heat shock protein-70 (HSP70), dinitrophenyl protein (DNP, an indicator of reactive oxygen species, ROS), 3-nitrotyrosine protein (NTP, an indicator of RNS), catalase (CAT), superoxide dismutase (SOD) protein expressions, and cellular apoptosis in gills and digestive glands of oysters collected on the southern Texas coast during the winter (15 °C), spring (24 °C), summer (30 °C), and fall (27 °C). Histological observations of both tissues showed a notable increase in mucus production and an enlargement of the digestive gland lumen with seasonal temperature rise, whereas biochemical analyses exhibited a significant decrease in EPF pH and protein concentration. Immunohistochemical analyses showed higher expression of HSP70 along with the expression of DNP and NTP in oyster tissues during summer. Intriguingly, CAT and SOD protein expressions exhibited significant upregulation with rising seasonal temperatures (15 to 27 °C), which decreased significantly in summer (30 °C), leaving oysters vulnerable to oxidative and nitrative damage. qRT-PCR analysis revealed a significant increase in HSP70 mRNA levels in oyster tissues during the warmer seasons. In situ TUNNEL assay showed a significant increase in apoptotic cells in seasons with high temperature. These results suggest that elevated SST induces oxidative/nitrative stress through the overproduction of ROS/RNS and disrupts the antioxidant system which promotes cellular apoptosis in oysters.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All relevant data are within the paper, and its supporting information files are available from the corresponding author upon request.
References
Ahsan H (2013) 3-Nitrotyrosine: a biomarker of nitrogen free radical species modified proteins in systemic autoimmunogenic conditions. Human Immunol 74(10):1392–1399. https://doi.org/10.1016/j.humimm.2013.06.009
Allam B, Paillard C (1998) Defense factors in clam extrapallial fluids. Dis Aquat Organis 33(2):123–128. https://doi.org/10.3354/dao033123
Allam B, Paillard C, Auffret M (2000) Alterations in hemolymph and extrapallial fluid parameters in the Manila clam, Ruditapes philippinarum, challenged with the pathogen Vibrio tapetis. J Invert Pathol 76(1):63–69. https://doi.org/10.1006/jipa.2000.4940
Alles A, Alley K, Barrett JC, Buttyan R, Goldgaber D, Lockshi RA et al (2020) Apoptosis: feature a general comment. FASEB J 5:2127–2128. https://doi.org/10.1096/fasebj.5.8.2022310
Amri S, Samar MF, Sellem F, Ouali K (2017) Seasonal antioxidant responses in the sea urchin Paracentrotus lividus (Lamarck 1816) used as a bioindicator of the environmental contamination in the South-East Mediterranean. Mar Poll Bull 122(1–2):392–402. https://doi.org/10.1016/j.marpolbul.2017.06.079
Anestis A, Lazou A, Pörtner HO, Michaelidis B (2007) Behavioral, metabolic, and molecular stress responses of marine bivalve Mytilus galloprovincialis during long-term acclimation at increasing ambient temperature. Am J Physiol Reg Integ Comp Physiol 293(2). https://doi.org/10.1152/ajpregu.00124.2007
Bensaude O, Pinto M, Dubois M-F, Van Trung N, Morange M (1990) Protein denaturation during heat shock and related stress. Stress Proteins 89–99:10487–92. https://doi.org/10.1007/978-3-642-75815-7_8
Betteridge DJ (2000) What is oxidative stress? Metabolism 49(2):3–8. https://doi.org/10.1016/S0026-0495(00)80077-3
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Brierley AS, Kingsford MJ (2009) Impacts of climate change on marine organisms and ecosystems. Crrr Biol R602-R614. https://doi.org/10.1016/j.cub.2009.05.046
Cameron LP, Reymond CE, Müller-Lundin F, Westfield I, Grabowski JH, Westphal H, Ries JB (2019) Effects of temperature and ocean acidification on the extrapallial fluid pH, calcification rate, and condition factor of the king scallop Pecten maximus. J Shellfish Res 38(3):763. https://doi.org/10.2983/035.038.0327
Canesi L, Pertica M, Hill C, Bay W (1991) Seasonal variations in the antioxidant defence systems and lipid peroxidation of the digestive gland of mussels. Methods l(l):187–190
Chainy GBN, Paital B, Dandapat J (2016) An overview of seasonal changes in oxidative stress and antioxidant defence parameters in some invertebrate and vertebrate species. Scientifica 2016:6126570. https://doi.org/10.1155/2016/6126570
Chapman G, Newell GE (1956) The rôle of the body fluid in the movement of soft-bodied invertebrates – II. The extenstion of the siphons of Mya arenaria L. and Scrobicularia plana (da Costa). Proc R Soc Biol Sci 145(921):564–580. https://doi.org/10.1098/rspb.1956.0065
Chaudière J, Ferrari-Iliou R (1999) Intracellular antioxidants: from chemical to biochemical mechanisms. Food Chem Toxicol 37(9–10):949–962. https://doi.org/10.1016/S0278-6915(99)00090-3
Chen M, Yang H, Delaporte M, Zhao S (2007) Immune condition of Chlamys farreri in response to acute temperature challenge. Aquaculture 271:479–487. https://doi.org/10.1016/j.aquaculture.2007.04.051
Clark MS, Peck LS, Thyrring J (2021) Resilience in Greenland intertidal Mytilus: the hidden stress defense. Sci Total Environ 767:144366. https://doi.org/10.1016/j.scitotenv.2020.144366
Dalle-Donne I, Rossi R, Giustarini D, Milzani A, Colombo R (2003) Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta 329(1–2):23–38. https://doi.org/10.1016/S0009-8981(03)00003-2
Di Meo S, Reed TT, Venditti P, Victor VM (2016) Role of ROS and RNS sources in physiological and pathological conditions. Oxid Med Cell Long 1–44. https://doi.org/10.1155/2016/1245049
Durán EG, Cuaya MP, Gutiérrez MV, León JA (2018) Effects of temperature and pH on the oxidative stress of benthic marine invertebrates. Biol Bull 610–616. https://doi.org/10.1134/S1062359018660019
Dutta SM, Banerjee S, Raha S (2018) Ecotoxicology and environmental safety biomonitoring role of some cellular markers during heat stress-induced changes in highly representative fresh water mollusc, Bellamya bengalensis: implication in climate change and biological adaptation. Comp Biochem Physiol 157A:482–490. https://doi.org/10.1016/j.ecoenv.2018.04.001
Dzwonkowski B, Coogan J, Fournier S, Lockridge G, Park K, Lee T (2020) Compounding impact of severe weather events fuels marine heatwave in the coastal ocean. Nat Commun 11:4623. https://doi.org/10.1038/s41467-020-18339-2
Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35(4):495–516. https://doi.org/10.1080/01926230701320337
Fabioux C, Huvet A, Le Souchu P, Le Pennec M, Pouvreau S (2005) Temperature and photoperiod drive Crassostrea gigas reproductive internal clock. Aquaculture 250(1–2):458–470. https://doi.org/10.1016/j.aquaculture.2005.02.038
Gosling E (2015) Marine bivalve molluscs. Wiley, Marine Bivalve Molluscs. https://doi.org/10.1002/9781119045212
Hansen J, Sato M, Hearty P, Ruedy R, Kelley M, Masson-Delmotte V et al (2016) Ice melt, sea level rise and superstorms: evidence from paleoclimate data, climate modeling, and modern observations that 2°C global warming could be dangerous. Atmos Chem Phys 16(6):3761–3812. https://doi.org/10.5194/acp-16-3761-2016
Hollingsworth MJ (1968) Environmental temperature and life span in poikilotherms, Nature. Nature Publishing Group, 218, p. 869. Available at: https://doi.org/10.1038/218869a0
Hu M, Li L, Sui Y, Li J, Wang Y, Lu W, Dupont S (2015) Effect of pH and temperature on antioxidant responses of the thick shell mussel Mytilus coruscus. Fish Shellfish Immunol 46(2):573–583. https://doi.org/10.1016/j.fsi.2015.07.025
IPCC (2019) Annex I: glossary [Weyer, NM (ed.)]. In: IPCC special report on the ocean and cryosphere in a changing climate [HO Portner, DC Roberts, V Masson-Delmotte, P Zhai, M Tignor, E Poloczanska, K Mintenbeck, A Alegria, M Nicolai, A Okem, J Petzold, B Rama, NM Weyer (eds.)]. (in press). https://www.ipcc.ch/site/assets/uploads/sites/3/2019/11/12_SROCC_AnnexI-Glossary_FINAL.pdf
Javid B, MacAry PA, Lehner PJ (2014) Structure and function: heat shock proteins and adaptive immunity. J Immunol 179(4):2035–2040. https://doi.org/10.4049/jimmunol.179.4.2035
Jin Z, El-Deiry WS (2005) Overview of cell death signaling pathways. Cancer Biol Therapy 4(2):147–171. https://doi.org/10.4161/cbt.4.2.1508
Johnstone J, Nash S, Hernandez E, Rahman MS (2019) Effects of elevated temperature on gonadal functions, cellular apoptosis, and oxidative stress in Atlantic sea urchin Arbacia punculata. Mar Environ Res 149:40–49. https://doi.org/10.1016/j.marenvres.2019.05.017
Jones MC, Dye SR, Fernandes JA, Frölicher TL, Pinnegar JK, Warren R, Cheung WWL (2013) Predicting the impact of climate change on threatened species in UK waters. PLoS ONE 8(1):e54216. https://doi.org/10.1371/journal.pone.0054216
Kesel J, Sedlak V (2014) Global climate change and security threats. Europ Sci J 20:31
Kodama K, Rahman MS, Horiguchi T, Thomas P (2012) Upregulation of hypoxia-inducible factor (HIF)-1α and HIF-2α mRNA levels in dragonet Callionymus valenciennei exposed to environmental hypoxia in Tokyo Bay. Mar Poll Bull 64:1339–1347. https://doi.org/10.1016/j.marpolbul.2012.05.002
Lau YT, Sussman L, Pales Espinosa E, Katalay S, Allam B (2017) Characterization of hemocytes from different body fluids of the eastern oyster Crassostrea virginica. Fish Shellfish Immunol 71:372–379. https://doi.org/10.1016/j.fsi.2017.10.025
Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Ann Rev Physiol 68(1):253–278. https://doi.org/10.1146/annurev.physiol.68.040104.110001
Li Y, Qin JG, Abbott CA, Li X, Benkendorff K (2007) Synergistic impacts of heat shock and spawning on the physiology and immune health of Crassostrea gigas: an explanation for summer mortality in Pacific oysters. Amer J Physiol Regul Integ Comp Physiol 293(6):R2353-2362. https://doi.org/10.1152/ajpregu.00463.2007
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆Ct method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Manabe S, Ploshay J, Lau N-C (2011) Seasonal variation of surface temperature changes during the last several decades. J Climate 24(15):3817–3821. https://doi.org/10.1175/JCLI-D-11-00129.1
Mangum CP, Shick JM (1972) The pH of body fluids of marine invertebrates. Comp Biochem Physiol 42A(3):693–697. https://doi.org/10.1016/0300-9629(72)90447-1
Maria-Jose, V. (2020) 2019 was the second warmest year on record, Earth Observatory. NASA Earth Observatory. https://earthobservatory.nasa.gov/images/146154/2019-was-the-second-warmest-year-on-record.
Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62(6):670–684. https://doi.org/10.1007/s00018-004-4464-6
Morris PJ, Swindles GT, Valdes PJ, Ivanovic RF, Gregoire LJ, Smith MW et al (2018) Global peatland initiation driven by regionally asynchronous warming. Proc Natl Acad Sci 115(19):201717838. https://doi.org/10.1073/pnas.1717838115
Nash S, Johnstone J, Rahman MS (2019) Elevated temperature attenuates ovarian functions and induces apoptosis and oxidative stress in the American oyster, Crassostrea virginica: potential mechanisms and signaling pathways. Cell Stress Chaper 24(5):957–967. https://doi.org/10.1007/s12192-019-01023-w
Nash S, Rahman MS (2019) Short-term heat stress impairs testicular functions in the American oyster, Crassostrea virginica: molecular mechanisms and induction of oxidative stress and apoptosis in spermatogenic cells. Mol Reprod Develop 86(10):1444–1458. https://doi.org/10.1002/mrd.23268
Norbury CJ, Hickson ID (2001) Cellular response to DNA damage. Ann Rev Pharmacol Toxicol 41(1):367–401. https://doi.org/10.1146/annurev.pharmtox.41.1.367
Padmini E, Tharani J (2014) Heat-shock protein 70 modulates apoptosis signal-regulating kinase 1 in stressed hepatocytes of Mugil cephalus. Fish Physiol Biochem 40(5):1573–1585. https://doi.org/10.1007/s10695-014-9949-0
Parrinello N, Rindone D, Canicattl C (1979) Naturally occurring hemolysis in the coelomic fluid of Holothuria polii delle chiaie (Echinodermata). Develop Comp Immunol 3(2):45–54. https://doi.org/10.1016/S0145-305X(79)80005-1
Perrigault M, Dahl SF, Espinosa EP, Gambino L, Allam B (2011) Effects of temperature on hard clam (Mercenaria mercennaria) immunity and QPX (quahog parasite unknown) disease development: II Defense parameters. J Invert Pathol 106:322–332. https://doi.org/10.1016/j.jip.2010.11.004
Piano A, Asirelli C, Caselli F, Fabbri E (2002) Hsp70 expression in thermally stressed Ostrea edulis, a commercially important oyster in Europe. Cell Stress Chaper 7(3):250–257. https://doi.org/10.1379/1466-1268(2002)007%3c0250:HEITSO%3e2.0.CO;2
Rahman MS, Rahman MS (2021) Effects of elevated temperature on prooxidant-antioxidant homeostasis and redox status in the American oyster: signaling pathways of cellular apoptosis during heat stress. Environ Res 196:110428. https://doi.org/10.1016/j.envers.2020.110428
Rahman MA, Henderson S, Mioller-Ezzy P, Li XX, Qin JG (2019) Immune response to temperature stress in three bivalve species: Pacific oyster Crassostrea gigas, Mediterranean mussel Mytilus galloprovincialis and mud cockle Katelysia rhytiphora. Fish Shellfish Immunol 86(868–874):10. https://doi.org/10.1016/j.fsi.2018.12.017
Rahman MS, Kline RJ, Vázquez OA, Khan IA, Thomas P (2020) Molecular characterization and expression of arginine vasotocin V1a2 receptor in Atlantic croaker brain: potential mechanisms of its downregulation by PCB77. J Biochem Mol Toxicol 34:e22500. https://doi.org/10.1002/jbt.22500
Rastrick SPS, Whiteley NM (2013) Influence of natural thermal gradients on whole animal rates of protein synthesis in marine gammarid amphipods. PLoS ONE 8(3):e60050. https://doi.org/10.1371/journal.pone.0060050
Robertson JD (1939) The inorganic composition of the body fluids of three marine invertebrates. J Exper Biol 16(4):387–397
Ryter SW, Kim HP, Hoetzel A, Park JW, Nakahira K, Wang X, Choi AMK (2007) Mechanisms of cell death in oxidative stress. Antioxid Redox Signal 9(1):49–89. https://doi.org/10.1089/ars.2007.9.49
Sastry AN, Blake NJ (1971) Regulation of gonad development in the bay scallop, Aequipecten irradians Lamarck. Biol Bull 140:274–283
Salvemini D, Doyle TM, Cuzzocrea S (2006) Superoxide, peroxynitrite, and oxidative and nitrative stress in inflamation. Biochem Soc Trans 34(5):965–970. https://doi.org/10.1042/BST0340965
Sardi AE, Sandrini-Neto L, da Cunha LP, Camus L (2020) Seasonal variation of oxidative biomarkers in gills and digestive glands of the clam Anomalocardia flexuosa and the mangrove oyster Crassostrea rhizophorae. Mar Poll Bull 156:1111193. https://doi.org/10.1016/j.marpolbul.2020.111193
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Meth. 9:671–675. org/https://doi.org/10.1038/nmeth.2089
Schmitt P, Rosa RD, Duperthuy M, de Lorgeril J, Bachere E, Destoumieux-Garzon D (2012) The antimicrobial defense of the Pacific oyster, Crassostrea gigas How diversity may compensate for scarcity in the regulation of resident pathogenic microflora. Front Microbiol 3:160
Seney EE, Rowland MJ, Lowery RA, Griffis RB, Mcclure MM (2013) Climate change marine environments, and the U.S. endangered species act. Conser Biol 27(6):1138–1146. https://doi.org/10.1111/cobi.12167
Sengupta S, Bhattacharjee A (2018) Dynamics of protein tyrosine nitration and denitration a review. J Proteom Genom 1(1):1–13. https://doi.org/10.15744/2576-7690.1.105
Shenai-Tirodkar PS, Gauns MU, Mujawar MWA, Ansari ZA (2017) Antioxidant responses in gills and digestive gland of oyster Crassostrea madrasensis (Preston) under lead exposure. Ecotoxicol Environ Safety 142:87–94. https://doi.org/10.1016/j.ecoenv.2017.03.056
Sies H (1993) Strategies of antioxidant defense. Europ J Biochem 215(2):213–219. https://doi.org/10.1111/j.1432-1033.1993.tb18025.x
Sleight VA, Thome MAS, Peck LS, Arivalagan J, Berland S, Marie A, Clark MS (2016) Characterization of the mantle transcription and biomineralisation genes in the bluent-gaper clam, Mya truncata. Mar Genomics 27:47–55. https://doi.org/10.1016/j.margen.2016.01.003
Sleight VA, Peck LS, Dyrynda EA, Smith VJ, Clark MS (2018) Cellular stress responses to chronic heat shock and shell damage in temperate Mya truncata. Cell Stress Chaper 23(5):1003–1017. https://doi.org/10.1007/s12192-018-0910-5
Slimen I, Najar T, Ghram A, Dabbebi H, Ben Mrad M, Abdrabbah M (2014) Reactive oxygen species heat stress and oxidative-induced mitochondrial damage. a review. Inter J Hyperth 30(7):513–523. https://doi.org/10.3109/02656736.2014.971446
Sokolova IM (2013) Energy-limited tolerance to stress as aconceptual framwork to integrate the effects of multiple stressors. Intgr Comp Biol 53(4):597–608. https://doi.org/10.1093/icb/ict028
Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA (2012) Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar Environ Res 79:1–15. https://doi.org/10.1016/j.marenvres.2012.04.003
Thomas P, Rahman M (2010) Region-wide impairment of Atlantic croaker testicular development and sperm production in the northern Gulf of Mexico hypoxic dead zone. Mar Environ Res 69:S59-62. https://doi.org/10.1016/j.marenvres.2009.10.017
Trueman B (1966) The fluid dynamics of the bivalve molluscs. Mya and Margaritifera J Exper Biol 45(2):369–382
Ueda N, Boettcher A (2009) Differences in heat shock protein 70 expression during larval and early spat development in the Eastern oyster, Crassostrea virginica (Gmelin, 1791). Cell Stress Chaper 14(4):439–443. https://doi.org/10.1007/s12192-008-0096-3
Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Rozen SG (2012) Primer3 new capabilities and interfaces. Nucleic Acids Res 40:e115. https://doi.org/10.2983/035.028.0414
Varghese F, Bukhari AB, Malhotra R, De A (2014) IHC profiler: an open source plugin for the quantitative evaluation and automated scoring of immunohistochemistry images of human tissue samples. PLoS ONE 9(5):e96801. https://doi.org/10.1371/journal.pone.0096801
Velez C, Figueira E, Soares AMVM, Freitas R (2017) Effects of seawater temperature increase on economically relevant native and introduced clam species. Mar Environ Res 123:62–70. https://doi.org/10.1016/j.marenvres.2016.11.010
Verlecar XN, Jena KB, Chainy GBN (2007) Biochemical markers of oxidative stress in Perna viridis exposed to mercury and temperature. Chemico-Biol Interact 167(3):219–226. https://doi.org/10.1016/j.cbi.2007.01.018
Wang J, Ren RM, Yao CL (2018) Oxidative stress responses of Mytilus galloprovincialis to acute cold and heat during air exposure. J Molluscan Stud 84(3):285–292. https://doi.org/10.1093/mollus/eyy027
Wyllie AH (1997) Apoptosis: an overview. British Med Bull 53(3):451–465
Yang C-Y, Sierp MT, Abbott CA, Li Y, Qin JG (2016) Responses to thermal and salinity stress in wild and farmed Pacific oysters Crassostrea gigas. Comp Biochem Physiol A Mol Integr Physiol 201:22–29. https://doi.org/10.1016/j.cbpa.2016.06.024
Yang C, Gao Q, Liu C, Wang L, Zhou Z, Gong C et al (2017) The transcriptional response of the Pacific oyster Crassostrea gigas against acute heat stress. Fish Shellfish Immunol 68:132–143. https://doi.org/10.1016/j.fsi.2017.07.016
Zhang H, Wang H, Chen H, Wang M, Zhou Z, Qiu L, Wang L, Song L (2019) The transcriptional response of the Pacific oyster Crassostrea gigas under simultaneous bacterial and heat stresses. Dev Comp Immunol 94:1–10. https://doi.org/10.1016/j.dci.2019.01.006
Acknowledgements
We greatly appreciate for the cordial help of Maruf Billah, Brittney Lacy, and Md Faizur Rahman, School of Earth, Environmental, and Marine Sciences (SEEMS), University of Texas Rio Grande Valley (UTRGV), with the oyster collections and dissections. We also give thanks to the Texas Park & Wildlife Department for allowing us in collecting oysters, and Dr. Aubrey Converse, University of Texas Marine Science Institute, for her valuable comments and suggestions on the manuscript. We would also like to thank and appreciate Dr. Manuela Truebano, Senior Editor, Cell Stress and Chaperones, and anonymous reviewers, for providing constructive comments and valuable suggestions on our manuscript.
Funding
This study was funded in part by the University of Texas Rio Grande Valley (UTRGV) Presidential Graduate Research Assistantship to Md Sadequr Rahman and the start-up fund and UTRGV College of Science SEED grant (grant no. 210000371) to Dr. Md Saydur Rahman.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
The UTRGV Institutional Animal Care and Use Committee does not require any animal care and/or handling protocol for terrestrial and aquatic invertebrates. All oysters, however, were handled and/or cared according to the Guide for Care and Use Animals for research in the US National Research Council Committee (https://grants.nih.gov/grants/olaw/guide-for-the-care-and-use-of-laboratory-animals.pdf).
Consent to partcipitate
Md Sadequr Rahman: field sampling, data collecting, statistical analyzing, writing original draft of manuscript. Md Saydur Rahman: field sampling; data collecting and analyzing; writing, reviewing, and editing manuscript; supervision.
Consent for publication
The authors have read and approved to submit the final version of manuscript.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rahman, M.S., Rahman, M.S. Elevated seasonal temperature disrupts prooxidant-antioxidant homeostasis and promotes cellular apoptosis in the American oyster, Crassostrea virginica, in the Gulf of Mexico: a field study. Cell Stress and Chaperones 26, 917–936 (2021). https://doi.org/10.1007/s12192-021-01232-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12192-021-01232-2