Abstract
Fishes endemic to the Qinghai–Tibetan Plateau are comparatively well adapted to aquatic environments with low oxygen partial pressures (hypoxia). Here, we cloned the complete cDNA of hemoglobin (Hb) α and β from the Tibetan schizothoracine fish Schizopygopsis pylzovi, and then investigated changes in Hb mRNA and protein levels in spleen, liver and kidney in response to hypoxia. We applied severe hypoxia (4 h at PO2 = 0.6 kPa) and moderate hypoxia (72 h at PO2 = 6.0 kPa) to adult S. pylzovi. Changes of Hb expression under hypoxia, together with the investigations of spleen somatic index, kidney somatic index and Hb concentration in circulation, suggest that the kidney may not only serve as the erythropoietic organ, but also act as the major blood reservoir in S. pylzovi. From this perspective, the transcriptional activity of Hb in S. pylzovi, as reflected in the kidney, was turned down quickly after the onset of severe hypoxia, while under moderate hypoxia the transcriptional activity of Hb showed upregulation for a short time, but then the transcriptional machinery was turned down slowly on prolonged exposure. Notably, the changes in Hb protein levels in spleen, liver and kidney in response to severe and moderate hypoxia were not in line with the changes in mRNA levels, which are related with the blood reservoir in the kidney. Tibetan schizothoracine fish, at least S. pylzovi, show a particular response of the transcription regulation of Hb to moderate hypoxia, which is different from that of other fish species.
Similar content being viewed by others
References
Affonso EG, Polez VL, Correa CF, Mazon AF, Araujo MR, Moraes G, Rantin FT (2002) Blood parameters and metabolites in the teleost fish Colossoma macropomum exposed to sulfide or hypoxia. Comp Biochem Physiol C Toxicol Pharmacol 133:375–382
Capossela KM, Brill RW, Fabrizio MC, Bushnell PG (2012) Metabolic and cardiorespiratory responses of summer flounder Paralichthys dentatus to hypoxia at two temperatures. J Fish Biol 81:1043–1058
Catton WT (1951) Blood cell formation in certain teleost fish. Blood 6:39–60
Chao Y, Zhao LY, Li CZ, Xie BS, Shen ZX, Wang GJ, Wang ZG, Li C, Bai BQ, Zhang H, Qi DL (2012) cDNA cloning and expression analysis of MSTN gene from Schizopygopsis pylzovi. Zool Res 33:473–480
Chen YF, Cao WY (2000) Schizothoracinae. In: Yue PQ (ed) Fauna Sinica, Osteichthyes, Cypriniformes III. Science Press, Beijing, pp 273–390
Cossins AR, Crawford DL (2005) Fish as models for environmental genomics. Nat Rev Genet 6:324–333
Cossins AR, Williams DR, Foulkes NS, Berenbrink M, Kipar A (2009) Diverse cell-specific expression of myoglobin isoforms in brain, kidney, gill and liver of the hypoxia-tolerant carp and zebrafish. J Exp Biol 212:627–638
Fraser J et al (2006) Hypoxia-inducible myoglobin expression in nonmuscle tissues. Proc Natl Acad Sci USA 103:2977–2981
Hardison R (1998) Hemoglobins from bacteria to man: evolution of different patterns of gene expression. J Exp Biol 201:1099–1117
Homechaudhuri S, Jah A (2001) A technique to evaluate the erythropoietic efficiency in fish. Asian Fish Sci 14:453–455
Houston AH, Murad A (1992) Erythrodynamics in goldfish, Carassius auratus L.: temperature effects. Physiol Zool 65:55–76
Houston AH, Roberts WC, Kennington JA (1996) Hematological response in fish: pronephric and splenic involvements in the goldfish, Carassius auratus L. Fish Physiol Biochem 15:481–489
Kondera E (2011) Haematopoiesis in the head kidney of common carp (Cyprinus carpio L.): a morphological study. Fish Physiol Biochem 37:355–362
Lai JC, Kakuta I, Mok HO, Rummer JL, Randall D (2006) Effects of moderate and substantial hypoxia on erythropoietin levels in rainbow trout kidney and spleen. J Exp Biol 209:2734–2738
Liu Y, Zhang S, Jiang G, Yang D, Lian J, Yang Y (2004) The development of the lymphoid organs of flounder, Paralichthys olivaceus, from hatching to 13 months. Fish Shellfish Immunol 16:621–632
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)). Method Methods 25:402–408
Mandic M, Todgham AE, Richards JG (2009) Mechanisms and evolution of hypoxia tolerance in fish. Proc Biol Sci 276:735–744
Murad A, Everill S, Houston A (1993) Division of goldfish erythrocytes in circulation. Can J Zool 71:2190–2198
Nikinmaa M (2001) Haemoglobin function in vertebrates: evolutionary changes in cellular regulation in hypoxia. Respir Physiol 128:317–329
Nikinmaa M (2002) Oxygen-dependent cellular functions—why fishes and their aquatic environment are a prime choice of study. Comp Biochem Physiol A Mol Integr Physiol 133:1–16
Nikinmaa M, Rees BB (2005) Oxygen-dependent gene expression in fishes. Am J Physiol Regul Integr Comp Physiol 288:R1079–R1090
Nilsson GE (2007) Gill remodeling in fish—a new fashion or an ancient secret? J Exp Biol 210:2403–2409
Patel S et al (2009) Ontogeny of lymphoid organs and development of IgM-bearing cells in Atlantic halibut (Hippoglossus hippoglossus L.). Fish Shellfish Immunol 26:385–395
Person Le Ruyet J, Boeuf G, Zambonino Infante J, Helgason S, Le Roux A (1998) Short-term physiological changes in turbot and seabream juveniles exposed to exogenous ammonia. Comp Biochem Physiol A Mol Integr Physiol 119:511–518
Qi D, Chao Y, Guo S, Zhao L, Li T, Wei F, Zhao X (2012) Convergent, parallel and correlated evolution of trophic morphologies in the subfamily schizothoracinae from the Qinghai–Tibetan plateau. PLoS One 7:e34070
Roesner A, Hankeln T, Burmester T (2006) Hypoxia induces a complex response of globin expression in zebrafish (Danio rerio). J Exp Biol 209:2129–2137
Roesner A, Mitz SA, Hankeln T, Burmester T (2008) Globins and hypoxia adaptation in the goldfish, Carassius auratus. FEBS J 275:3633–3643
Rombout JH, Huttenhuis HB, Picchietti S, Scapigliati G (2005) Phylogeny and ontogeny of fish leucocytes. Fish Shellfish Immunol 19:441–455
Shang EH, Wu RS (2004) Aquatic hypoxia is a teratogen and affects fish embryonic development. Environ Sci Technol 38:4763–4767
Smith RW, Houlihan DF, Nilsson GE, Brechin JG (1996) Tissue-specific changes in protein synthesis rates in vivo during anoxia in crucian carp. Am J Physiol 271:R897–R904
Soldatov AA (1996) The effect of hypoxia on red blood cells of flounder: a morphologic and autoradiographic study. J Fish Biol 48:321–328
Sollid J, Nilsson GE (2006) Plasticity of respiratory structures—adaptive remodeling of fish gills induced by ambient oxygen and temperature. Respir Physiol Neurobiol 154:241–251
Sollid J, De Angelis P, Gundersen K, Nilsson GE (2003) Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J Exp Biol 206:3667–3673
Sollid J, Weber RE, Nilsson GE (2005) Temperature alters the respiratory surface area of crucian carp Carassius carassius and goldfish Carassius auratus. J Exp Biol 208:1109–1116
Storz JF, Scott GR, Cheviron ZA (2010) Phenotypic plasticity and genetic adaptation to high-altitude hypoxia in vertebrates. J Exp Biol 213:4125–4136
Suzuki M, Kajita A, Hanaoka C (1973) Improved method for preparation of crystalline oxyhemoglobin free from catalase and methemoglobin. J Biochem 41:401–408
Timmerman CM, Chapman LJ (2004) Behavioral and physiological compensation for chronic hypoxia in the sailfin molly (Poecilia latipinna). Physiol Biochem Zool 77:601–610
Ton C, Stamatiou D, Liew CC (2003) Gene expression profile of zebrafish exposed to hypoxia during development. Physiol Genom 13:97–106
Tzaneva V, Bailey S, Perry SF (2011) The interactive effects of hypoxemia, hyperoxia, and temperature on the gill morphology of goldfish (Carassius auratus). Am J Physiol Regul Integr Comp Physiol 300:R1344–R1351
Valenzuela A, Silva V, Tarifeno E, Klempau A (2005) Effect of acute hypoxia in Trout (Oncorhynchus mykiss) on immature erythrocyte release and production of oxidative radicals. Fish Physiol Biochem 31:65–72
Wawrowski A, Gerlach F, Hankeln T, Burmester T (2011) Changes of globin expression in the Japanese medaka (Oryzias latipes) in response to acute and chronic hypoxia. J Comp Physiol B 181:199–208
Witeska M (2013) Erythrocytes in teleost fishes: a review. Zool Ecol 23:275–281
Wu YF, Wu CZ (1992) The fishes of the Qinghai–Xizang plateau. Science and Technology Press, Chengdu
Wu RSS, Zhou BS, Randall DJ, Woo NYS, Lam PKS (2003) Aquatic hypoxia is an endocrine disruptor and impairs fish reproduction. Environ Sci Techonol 37:1137–1141
Yang S et al (2015) Morphogenesis of blood cell lineages in Ya-fish (Schizothorax prenanti) Chinese. J Zool 50:231–242
Yuan S, Zhu A, Jiang L, Chai X (2011) Observations on the developments of blood cells in Nibea japonica. J Fish China 35:1374–1380
Zhao ZX et al (2014) Duplication and differentiation of common carp (Cyprinus carpio) myoglobin genes revealed by BAC analysis. Gene 548:210–216
Acknowledgments
This work was supported by Grants from the National Natural Science Foundation of China [31460094]; and the Natural Science Foundation of Qinghai Science & Technology Department in China [2015-ZJ-901]. We would like to thank the native English speaking scientists of Elixigen Company (Huntington Beach, California) for editing our manuscript.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Communicated by H.V. Carey.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Xia, M., Chao, Y., Jia, J. et al. Changes of hemoglobin expression in response to hypoxia in a Tibetan schizothoracine fish, Schizopygopsis pylzovi . J Comp Physiol B 186, 1033–1043 (2016). https://doi.org/10.1007/s00360-016-1013-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-016-1013-1