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Molecular Origins and Mechanisms of Fish Antifreeze Evolution

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Antifreeze Proteins Volume 1

Abstract

Independent evolution of distinctive types of antifreeze glycoprotein (AFGP) and peptides (AFP) in various polar and subpolar bony fish lineages bespeaks the breath of evolutionary ingenuity in converging on a similar life-preserving solution under extreme selective pressures from lethal, icy freezing marine conditions. Fish AF(G)Ps represent clear examples of a single adaptive genotype conferring a crucial fitness phenotype in a clear causal manner, which are exceptionally rare in evolutionary biology. Studies of the antifreeze function have richly enhanced our understanding of this new form of biochemical and physiological adaptation to extreme cold in marine vertebrate ectotherm. Additionally, the diverse AF(G)P genotypes are genetic novelties, and studies of their evolution have richly informed the field of molecular evolution on the array of innovative processes by which new genes arose, from classical evolution through gene duplication, to creating protein-coding gene from entirely noncoding DNA. This chapter reviews the origins and molecular mechanisms of fish AF(G)P genes that have been deduced in the past three decades and outstanding uncertainties, narrated as a historical account, with relevant environmental, organismal, physiological, and evolutionary considerations.

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References

  • Albers CN, Bjørn-Mortensen M, Hansen PE, Ramløv H, Sørensen T (2007) Purification and structural analysis of a type III antifreeze protein from the european eelpout Zoarces viviparus. Cryo Lett 28:51–60

    CAS  Google Scholar 

  • Anderson ME (1994) Systematics and osteology of the Zoarcidae (Teleostei: Perciformes). In: Icthyological bulletin, vol 60. J.L.B. Smith Institute of Ichthyology, Grahamstown, pp 1–120. http://vital.seals.ac.za:8080/vital/access/manager/Repository/vital:15033

    Google Scholar 

  • Andriashev AP (ed) (1970) Cryopelagic fishes in the Arctic and Antarctic and their significance in polar ecosystems. Academic Press, London

    Google Scholar 

  • Baardsnes J, Davies PL (2001) Sialic acid synthase: the origin of fish type III antifreeze protein? Trends Biochem Sci 26:468–469

    Article  CAS  PubMed  Google Scholar 

  • Barry RG (1989) The present climate of the Arctic Ocean and possible past and future states. In: Herman Y (ed) The Arctic seas: climatology, oceanography, geology, and biology. Van Nostrand Reinhold, New York

    Google Scholar 

  • Barsukov VV (1986) Anarhichadidae. In: Whitehead PJP, Bauchot M-L, Hureau J-C, Nielsen J, Tortonese E (eds) Fishes of the North-eastern Atlantic and the Mediterranean. UNESCO, Paris, pp 1113–1116

    Google Scholar 

  • Betenbaugh MJ, Yin B, Blake E, Kristoffersen L, Narang S, Viswanathan K (2014) N-Acetylneuraminic acid synthase (NANS). In: Taniguchi N, Honke K, Fukuda M, Narimatsu H, Yamaguchi Y, Angata T (eds) Handbook of glycosyltransferases and related genes. Springer, Tokyo

    Google Scholar 

  • Bredow M, Walker VK (2017) Ice-binding proteins in plants. Front Plant Sci 8:2153

    Article  PubMed  PubMed Central  Google Scholar 

  • Carr SM, Marshall HD (2008) Intraspecific phylogeographic genomics from multiple complete mtDNA genomes in Atlantic cod (Gadus morhua): origins of the “Codmother,” transatlantic vicariance and midglacial population expansion. Genetics 180:381–389

    Article  PubMed  PubMed Central  Google Scholar 

  • Carrete Vega G, Wiens JJ (2013) Why are there so few fish in the sea? Proc R Soc B 279:2323–2329

    Article  Google Scholar 

  • Celik Y, Graham LA, Mok Y-F, Bar M, Davies PL, Braslavsky I (2010) Superheating of ice crystals in antifreeze protein solutions. Proc Natl Acad Sci 107:5423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaw RC, Saski CA, Hayashi CY (2017) Complete gene sequence of spider attachment silk protein (PySp1) reveals novel linker regions and extreme repeat homogenization. Insect Biochem Mol Biol 81:80–90

    Article  CAS  PubMed  Google Scholar 

  • Chen L, DeVries AL, Cheng C-HC (1997a) Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. Proc Natl Acad Sci USA 94:3811–3816

    Google Scholar 

  • Chen L, DeVries AL, Cheng C-HC (1997b) Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod. Proc Natl Acad Sci USA 94:3817–3822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng C-HC (1998) Origin and mechanism of evolution of antifreeze glycoproteins in polar fishes. In: Di Prisco G, Pisano E, Clarke A (eds) Evolution of the Antarctic Ichthyofauna. Springer, Berlin, pp 311–328

    Google Scholar 

  • Cheng C-HC, Chen L (1999) Evolution of an antifreeze glycoprotein. Nature 40:443–444

    Article  CAS  Google Scholar 

  • Cheng C-HC, DeVries AL (1989) Structures of antifreeze peptides from the antarctic eel pout, Austrolycichthys brachycephalus. Biochim Biophys Acta 997:55–64

    Article  CAS  PubMed  Google Scholar 

  • Cheng C-HC, Cziko PA, Evans CW (2006) Nonhepatic origin of notothenioid antifreeze reveals pancreatic synthesis as common mechanism in polar fish freezing avoidance. Proc Natl Acad Sci USA 103:10491–10496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cohen DM, Inada T, Iwamoto T, Scialabba N, Whitehead PJP (1990) FAO species catalogue: vol. 10 gadiform fishes of the world (order gadiformes), an annotated and illustrated catalogue of Cods. Hakes, grenadiers and other gadiform fishes known to date. FAO

    Google Scholar 

  • Conant GC, Wolfe KH (2008) Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 9:938–950

    Article  CAS  PubMed  Google Scholar 

  • Coulson MW, Marshall HD, Pepin PC, Carr SM (2006) Mitochondrial genomics of gadine fishes: implications for taxonomy and biogeographic origins from whole-genome data sets. Genome Biol 49:1115–1130

    Article  CAS  Google Scholar 

  • Cziko PA, DeVries AL, Evans CW, Cheng C-HC (2014) Antifreeze protein-induced superheating of ice inside Antarctic notothenioid fishes inhibits melting during summer warming. Proc Natl Acad Sci 111:14583–14588

    Google Scholar 

  • Davies PL, Graham LA (2018) Protein evolution revisited. Syst Biol Reprod Med 64:403–416

    Article  CAS  PubMed  Google Scholar 

  • de Jong WW, Lubsen NH, Kraft HJ (1994) Molecular evolution of the eye lens. Prog Retin Eye Res 13:391–442

    Article  Google Scholar 

  • Deng C, Cheng C-HC, Ye H, He X, Chen L (2010) Evolution of an antifreeze protein by neofunctionalization under escape from adaptive conflict. Proc Natl Acad Sci 107:21593–21598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denstad J-P, Aunaas T, Borseth JF, Aaset AV, Zachariassen KE (1987) Thermal hysteresis antifreeze agents in fishes from Spitsbergen waters. Polar Res 5:171–174

    Article  Google Scholar 

  • Desjardins M, Graham LA, Davies PL, Fletcher GL (2012) Antifreeze protein gene amplification facilitated niche exploitation and speciation in wolffish. FEBS J 279:2215–2230

    Article  CAS  PubMed  Google Scholar 

  • DeVries AL (1968) Freezing resistance in some Antractic fishes (PhD thesis). PhD thesis, Stanford University

    Google Scholar 

  • DeVries AL (1971) Glycoproteins as biological antifreeze agents in Antarctic fishes. Science 172:1152–1155

    Article  CAS  PubMed  Google Scholar 

  • DeVries AL (1974) Survival at freezing temperatures. In: Malins DC, Sargent JR (eds) Biochemical and biophysical perspectives in marine biology. Academic Press, London, pp 289–330

    Google Scholar 

  • DeVries AL, Lin Y (1977) The role of glycoprotein antifreezes in the survival of Antarctic fishes. In: Llano GA (ed) Adaptations within Antarctic ecosystems. Gulf, Houston, pp 439–458

    Google Scholar 

  • DeVries AL, Steffensen JF (2005) The Arctic and Antarctic polar marine environments. In: Farrell AP, Steffensen JF (eds) Fish physiology. Academic Press, San Diego, pp 1–24

    Google Scholar 

  • DeVries AL, Komatsu SK, Feeney RE (1970) Chemical and physical properties of freezing point depressing glycoproteins from Antarctic fishes. J Biol Chem 245:2901–2908

    Article  CAS  PubMed  Google Scholar 

  • DeVries AL, Vandenheede J, Feeney RE (1971) Primary structure of freezing point-depressing glycoproteins. J Biol Chem 246:305–308

    Article  CAS  PubMed  Google Scholar 

  • Doucet D, Walker VK, Qin W (2009) The bugs that came in from the cold: molecular adaptations to low temperatures in insects. Cell Mol Life Sci 66:1404–1418

    Article  CAS  PubMed  Google Scholar 

  • Duman JG, DeVries AL (1975) The role of macromolecular antifreezes in cold water fishes. Comp Biochem Physiol 52A:193–199

    Article  Google Scholar 

  • Dunton K (1992) Arctic biogeography: the paradox of the marine benthic fauna and flora. Trends Ecol Evol 7:183–189

    Article  CAS  PubMed  Google Scholar 

  • Eastman JT (2005) The nature of the diversity of Antarctic fishes. Polar Biol 28:93–107

    Article  Google Scholar 

  • Eastman JT (2017) Bathymetric distributions of notothenioid fishes. Polar Biol 40:2077–2095

    Article  Google Scholar 

  • Eastman JT, McCune AR (2000) Fishes on the Antarctic continental shelf: evolution of a marine species flock? J Fish Biol 57:84–102

    Google Scholar 

  • Enevoldsen LT, Heiner I, DeVries AL, Steffensen JF (2003) Does fish from the Disko Bay area of Greenland possess antifreeze proteins during the summer? Polar Biol 26:365–370

    Article  Google Scholar 

  • Evans CW, Hellman L, Middleditch M, Wojnar JM, Brimble MA, Devries AL (2012) Synthesis and recycling of antifreeze glycoproteins in polar fishes. Antarct Sci 24:259–268

    Article  Google Scholar 

  • Ewart KV, Fletcher GL (1990) Isolation and characterization of antifreeze proteins from smelt (Osmerus mordax) and Atlantic herring (Culpea harengus harengus). Can J Zool 68:1652–1658

    Article  CAS  Google Scholar 

  • Ewart KV, Fletcher GL (1993) Herring antifreeze protein: primary structure and evidence for a C-type lectin evolutionary origin. Mol Mar Biol Biotechnol 2:20–27

    CAS  PubMed  Google Scholar 

  • Ewart KV, Rubinsky B, Fletcher GL (1992) Structural and functional similarity between fish antifreeze proteins and calcium-dependent lectins. Biochim Biophy Res Commun 185:335–340

    Article  CAS  Google Scholar 

  • Ewart KV, Li Z, Yang DSC, Fletcher GL, Hew CL (1998) The ice-binding site of Atlantic herring antifreeze protein corresponds to the carbohydrate-binding site of C-type lectins. Biochemist 37:4080–4085

    Article  CAS  Google Scholar 

  • Ewart KV, Lin Q, Hew CL (1999) Structure, function and evolution of antifreeze proteins. Cell Mol Life Sci 55:271–283

    Article  CAS  PubMed  Google Scholar 

  • Fletcher GL, Hew CL, Li X, Haya K, Kao MH (1985) Year-round presence of high levels of plasma antifreeze peptides in a temperate fish, ocean pout (Macrozoarces americanus). Can J Zool 63:488–493

    Article  CAS  Google Scholar 

  • Fletcher G, Kao M, Haya K (2011) Seasonal and phenotypic variations in plasma protein antifreeze levels in a population of marine fish, sea raven (Hemitripterus americanus). Can J Fish Aquat Sci 41:819–824

    Article  Google Scholar 

  • Gauthier SY, Scotter AJ, Lin F-H, Baardsnes J, Fletcher GL, Davies PL (2008) A re-evaluation of the role of type IV antifreeze protein. Cryobiology 57:292–296

    Article  CAS  PubMed  Google Scholar 

  • Gong Z, Fletcher GL, Hew CL (1992) Tissue distribution of fish antifreeze protein mRNAs. Can J Zool 70:810–814

    Article  CAS  Google Scholar 

  • Gradinger RR, Bluhm BA (2004) In-situ observations on the distribution and behavior of amphipods and Arctic cod (Boreogadus saida) under the sea ice of the high Arctic Canada Basin. Polar Biol 27:595–603

    Article  Google Scholar 

  • Graham LA, Davies PL (2005) Glycine-rich antifreeze proteins from snow fleas. Science 310:461–461

    Google Scholar 

  • Graham LA, Lougheed SC, Ewart KV, Davies PL (2008) Lateral transfer of a lectin-like antifreeze protein gene in fishes. PLoS One 3(7):e2616

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Graham LA, Li J, Davidson WS, Davies PL (2012) Smelt was the likely beneficiary of an antifreeze gene laterally transferred between fishes. BMC Evol Biol 12:190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graham LA, Hobbs RS, Fletcher GL, Davies PL (2013) Helical antifreeze proteins have independently evolved in fishes on four occasions. PLoS One 8(12):e81285

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Griffith M, Lumb C, Wiseman SB, Wisniewski M, Johnson RW, Marangoni AG (2005) Antifreeze proteins modify the freezing process in planta. Plant Physiol 138:330–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hahn MW (2009) Distinguishing among evolutionary models for the maintenance of gene duplicates. J Hered 100:605–617

    Article  CAS  PubMed  Google Scholar 

  • Herberg S, Gert KR, Schleiffer A, Pauli A (2018) The Ly6/uPAR protein bouncer is necessary and sufficient for species-specific fertilization. Science 361:1029–1033

    Google Scholar 

  • Hew CL, Slaughter D, Fletcher GL, Joshi S (1981) Antifreeze glycoproteins in the plasma of Newfoundland Atlantic cod (Gadus morhua). Can J Zool 59:2186–2192

    Article  CAS  Google Scholar 

  • Hew CL, Slaughter D, Joshi S, Fletcher GL, Ananthanarayanan VS (1984) Antifreeze polypeptides from the Newfoundland Ocean pout, Macrozoarces americanus: presence of multiple and compositionally diverse components. J Comp Physiol B155:81–88

    Article  Google Scholar 

  • Hew CL, Wang N-C, Joshi S, Fletcher GL, Scott GK, Hayes PH, Buettner B, Davies PL (1988) Multiple genes provide the basis for antifreeze protein diversity and dosage in the ocean pout, Macrozoarces americanus. J Biol Chem 263:12049–12055

    Article  CAS  PubMed  Google Scholar 

  • Hon WC, Griffith M, Mlynarz A, Kwok YC, Yang DS (1995) Antifreeze proteins in winter rye are similar to pathogenesis-related proteins. Plant Physiol 109:879–889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howe GJ (1991) Biogeography of gadoid fishes. J Biogeogr 18:595–622

    Article  Google Scholar 

  • Hsiao K-C, Cheng C, Fernandes IE, Detrich HW, DeVries AL (1990) An antifreeze glycopeptide gene from the Antarctic cod Notothenia coriiceps neglecta encodes a polyprotein of high peptide copy number. Proc Natl Acad Sci 87:9265–9269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang HH, Liao HK, Chen YJ, Hwang TS, Lin YH, Lin CH (2005) Structural characterization of sialic acid synthase by electrospray mass spectrometry - a tetrameric enzyme composed of dimeric dimers. J Am Soc Mass Spectrom 16:324–332

    Article  CAS  PubMed  Google Scholar 

  • Hunt BM, Hoefling K, Cheng C-HC (2003) Annual warming episodes in seawater temperatures in McMurdo Sound in relationship to endogenous ice in notothenioid fish. Antarct Sci 15:333–338

    Article  Google Scholar 

  • Jacob F (1977) Evolution and tinkering. Science 196:1161–1166

    Article  CAS  PubMed  Google Scholar 

  • Jensen LE, Thiel S, Petersen TE, Jensenius JC (1997) A rainbow trout lectin with multimeric structure. Comp Biochem Physiol B Biochem Mol Biol 116:385–390

    Article  CAS  PubMed  Google Scholar 

  • Jin Y, DeVries AL (2006) Antifreeze glycoprotein levels in Antarctic notothenioid fishes inhabiting different thermal environments and the effect of warm acclimation. Comp Biochem Physiol 76B:560–600

    Google Scholar 

  • Kadler KE, Baldock C, Bella J, Boot-Handford RP (2007) Collagens at a glance. J Cell Sci 120:1955

    Article  CAS  PubMed  Google Scholar 

  • Kaessmann H (2010) Origins, evolution, and phenotypic impact of new genes. Genome Res 20:1313–1326

    Google Scholar 

  • Kennett JP (1977) Cenozoic evolution of Antarctic glaciation, the circum-Antarctic Ocean, and their impact on global paleoceanography. J Geophys Res 82:3843–3860

    Article  CAS  Google Scholar 

  • Knight CA, Devries AL (1989) Melting inhibition and superheating of ice by an antifreeze Glycopeptide. Science 245:505–507

    Google Scholar 

  • Kurlansky M (1997) Cod: a biography of the fish that changed the world. Penguin Books, New York

    Google Scholar 

  • La Mesa M, Eastman JT, Vacchi M (2004) The role of notothenioid fish in the food web of the Ross Sea shelf waters: a review. Polar Biol 27:321–338

    Article  Google Scholar 

  • Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, Funke R, Gage D, Harris K, Heaford A, Howland J, Kann L, Lehoczky J, LeVine R, McEwan P, McKernan K, Meldrim J, Mesirov JP, Miranda C, Morris W, Naylor J, Raymond C, Rosetti M, Santos R, Sheridan A, Sougnez C, Stange-Thomann Y, Stojanovic N, Subramanian A, Wyman D, Rogers J, Sulston J, Ainscough R, Beck S, Bentley D, Burton J, Clee C, Carter N, Coulson A, Deadman R, Deloukas P, Dunham A, Dunham I, Durbin R, French L, Grafham D, Gregory S, Hubbard T, Humphray S, Hunt A, Jones M, Lloyd C, McMurray A, Matthews L, Mercer S, Milne S, Mullikin JC, Mungall A, Plumb R, Ross M, Shownkeen R, Sims S, Waterston RH, Wilson RK, Hillier LW, McPherson JD, Marra MA, Mardis ER, Fulton LA, Chinwalla AT, Pepin KH, Gish WR, Chissoe SL, Wendl MC, Delehaunty KD, Miner TL, Delehaunty A, Kramer JB, Cook LL, Fulton RS, Johnson DL, Minx PJ, Clifton SW, Hawkins T, Branscomb E, Predki P, Richardson P, Wenning S, Slezak T, Doggett N, Cheng JF, Olsen A, Lucas S, Elkin C, Uberbacher E, Frazier M, Gibbs RA, Muzny DM, Scherer SE, Bouck JB, Sodergren EJ, Worley KC, Rives CM, Gorrell JH, Metzker ML, Naylor SL, Kucherlapati RS, Nelson DL, Weinstock GM, Sakaki Y, Fujiyama A, Hattori M, Yada T, Toyoda A, Itoh T, Kawagoe C, Watanabe H, Totoki Y, Taylor T, Weissenbach J, Heilig R, Saurin W, Artiguenave F, Brottier P, Bruls T, Pelletier E, Robert C, Wincker P, Smith DR, Doucette-Stamm L, Rubenfield M, Weinstock K, Lee HM, Dubois J, Rosenthal A, Platzer M, Nyakatura G, Taudien S, Rump A, Yang H, Yu J, Wang J, Huang G, Gu J, Hood L, Rowen L, Madan A, Qin S, Davis RW, Federspiel NA, Abola AP, Proctor MJ, Myers RM, Schmutz J, Dickson M, Grimwood J, Cox DR, Olson MV, Kaul R, Raymond C, Shimizu N, Kawasaki K, Minoshima S, Evans GA, Athanasiou M, Schultz R, Roe BA, Chen F, Pan H, Ramser J, Lehrach H, Reinhardt R, WR MC, de la Bastide M, Dedhia N, Blöcker H, Hornischer K, Nordsiek G, Agarwala R, Aravind L, Bailey JA, Bateman A, Batzoglou S, Birney E, Bork P, Brown DG, Burge CB, Cerutti L, Chen HC, Church D, Clamp M, Copley RR, Doerks T, Eddy SR, Eichler EE, Furey TS, Galagan J, Gilbert JG, Harmon C, Hayashizaki Y, Haussler D, Hermjakob H, Hokamp K, Jang W, Johnson LS, Jones TA, Kasif S, Kaspryzk A, Kennedy S, Kent WJ, Kitts P, Koonin EV, Korf I, Kulp D, Lancet D, Lowe TM, McLysaght A, Mikkelsen T, Moran JV, Mulder N, Pollara VJ, Ponting CP, Schuler G, Schultz J, Slater G, Smit AF, Stupka E, Szustakowki J, Thierry-Mieg D, Thierry-Mieg J, Wagner L, Wallis J, Wheeler R, Williams A, Wolf YI, Wolfe KH, Yang SP, Yeh RF, Collins F, Guyer MS, Peterson J, Felsenfeld A, Wetterstrand KA, Patrinos A, Morgan MJ, de Jong P, Catanese JJ, Osoegawa K, Shizuya H, Choi S, Chen YJ, Szustakowki J, International Human Genome Sequencing Consortium (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921

    Article  CAS  PubMed  Google Scholar 

  • Lin Y, Duman JG, DeVries AL (1972) Studies on the structure and activity of low molecular weight glycoproteins from an antarctic fish. Biochem Biophys Res Commun 46:87–92

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Li Z, Lin Q, Kosinski J, Seetharaman J, Bujnicki JM, Sivaraman J, Hew C-L (2007) Structure and evolutionary origin of Ca2+-dependent herring type II antifreeze protein. PLoS One 2:e548

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Livermore R, Nankivell A, Eagles G, Morris P (2005) Paleogene opening of Drake passage. Earth Planet Sci Lett 236:459–470

    Article  CAS  Google Scholar 

  • Lopes-Ferreira M, Magalhães GS, Fernandez JH, de Junqueira-de-Azevedo ILM, Le Ho P, Lima C, Valente RH, Moura-da-Silva AM (2011) Structural and biological characterization of Nattectin, a new C-type lectin from the venomous fish Thalassophryne nattereri. Biochimie 93:971–980

    Article  CAS  PubMed  Google Scholar 

  • Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155

    Google Scholar 

  • Lynch M, Katju V (2004) The altered evolutionary trajectories of gene duplicates. Trends Genet 20:544–549

    Article  CAS  PubMed  Google Scholar 

  • Maslin MA, Li XS, Loutre MF, Berger A (1998) The contribution of orbital forcing to the progressive intensification of northern hemisphere glaciation. Quat Sci Rev 17:411–426

    Article  Google Scholar 

  • Matschiner M, Hanel R, Salzburger W (2011) On the origin and trigger of the Notothenioid adaptive radiation. PLoS One 6:e18911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McLysaght A, Guerzoni D (2015) New genes from non-coding sequence: the role of de novo protein-coding genes in eukaryotic evolutionary innovation. Philos Trans R Soc B 370:20140332

    Article  CAS  Google Scholar 

  • McLysaght A, Hurst LD (2016) Open questions in the study of de novo genes: what, how and why. Nat Rev Genet 17:579–579

    Article  CAS  Google Scholar 

  • Nicodemus-Johnson J, Silic S, Ghigliotti L, Pisano E, Cheng C-HC (2011) Assembly of the antifreeze glycoprotein/trypsinogen-like protease genomic locus in the Antarctic fish Dissostichus mawsoni (Norman). Genomics. https://doi.org/10.1016/j.ygeno.2011.06.002

  • Nishimiya Y, Kondo H, Yasui M, Sugimoto H, Noro N, Sato R, Suzuki M, Miura A, Tsuda S (2006) Crystallization and preliminary X-ray crystallographic analysis of Ca2+-independent and Ca2+-dependent species of the type II antifreeze protein. Acta Crystallogr Sect F Struct Biol Cryst Commun 62:538–541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishimiya Y, Kondo H, Takamichi M, Sugimoto H, Suzuki M, Miura A, Tsuda S (2008) Crystal structure and mutational analysis of Ca2+-independent type II antifreeze protein from Longsnout poacher, Brachyopsis rostratus. J Mol Biol 382:734–746

    Article  CAS  PubMed  Google Scholar 

  • O’Grady SM, Schrag JD, Raymond JA, DeVries AL (1982) Comparison of antifreeze glycopeptides from Arctic and Antarctic fishes. J Exp Zool 224:177–185

    Article  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer, Berlin

    Book  Google Scholar 

  • Osuga DT, Feeney RE (1978) Antifreeze glycoproteins from Arctic fish. J Biol Chem 253:5338–5343

    Article  CAS  PubMed  Google Scholar 

  • Patil JG, Khoo HW (1996) Nuclear internalization of foreign DNA by zebrafish spermatozoa and its enhancement by electroporation. J Exp Zool 274:121–129

    Article  CAS  PubMed  Google Scholar 

  • Petzel DH, Reisman HM, DeVries AL (1980) Seasonal variation of antifreeze peptide in the winter flounder, Pseudopleuronectes americanus. J Exp Zool 211:63–69

    Article  CAS  Google Scholar 

  • Piatigorsky J (1998) Multifunctional lens crystallins and corneal enzymes. More than meets the eye. Ann N Y Acad Sci 842:7–15

    Article  CAS  PubMed  Google Scholar 

  • Præbel K, Ramløv H (2005) Antifreeze activity in the gastrointestinal fluids of Arctogadus glacialis (Peters 1874) is dependent upon food type. J Exp Biol 208:2609–2613

    Article  PubMed  Google Scholar 

  • Prosser CL (1973) Water: osmotic balance; hormonal regulation. In: Prosser CL (ed) Comparative animal physiology. Saunders, Philadelphia, pp 1–78

    Google Scholar 

  • Raymond JA (1992) Glycerol is a colligative antifreeze in some northern fishes. J Exp Zool 262:347–352

    Article  CAS  Google Scholar 

  • Raymond JA (1993) Glycerol and water balance in a near-isosmotic teleost, winter-acclimatized rainbow smelt. Can J Zool 71:1849–1854

    Article  CAS  Google Scholar 

  • Raymond JA, DeVries AL (1972) Freezing behavior of fish blood glycoproteins with antifreeze properties. Cryobiology 9:541–547

    Article  CAS  PubMed  Google Scholar 

  • Raymond JA, DeVries AL (1977) Adsorption-inhibition as a mechanism of freezing resistance in polar fishes. Proc Natl Acad Sci USA 74:2589–2593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond JA, Lin Y, DeVries AL (1975) Glycoprotein and protein antifreezes in two Alaskan fishes. J Exp Zool 193:125–130

    Article  CAS  PubMed  Google Scholar 

  • Reisman HM, Kao MH, Fletcher GL (1984) Antifreeze glycoprotein in a southern population of Atlantic tomcod, Microgadus tomcod. Comp Biochem Physiol 78A:445–447

    Article  CAS  Google Scholar 

  • Robins CR, Ray GC (1986) A field guide to Atlantic coast fishes of North America. Houghton Mifflin Company, Boston

    Google Scholar 

  • Russell S, Young KM, Smith M, Hayes MA, Lumsden JS (2008) Cloning, binding properties, and tissue localization of rainbow trout (Oncorhynchus mykiss) ladderlectin. Fish Shellfish Immunol 24:669–683

    Article  CAS  PubMed  Google Scholar 

  • Schlötterer C (2015) Genes from scratch–the evolutionary fate of de novo genes. Trends Genet 31:215–219

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Scholander PF, van Dam L, Kanwisher JW, Hammel HT, Gordon MS (1957) Supercooling and osmoregulation in arctic fish. J Cell Comp Physiol 49:5–24

    Article  CAS  Google Scholar 

  • Schrag JD, Cheng C-HC, Panico M, Morris HR, DeVries AL (1987) Primary and secondary structure of antifreeze peptides from arctic and antarctic zoarcid fishes. Biochim Biophys Acta 915:357–370

    Article  CAS  PubMed  Google Scholar 

  • Scott GK, Hew CL, Davies PL (1985) Antifreeze proteins genes are tandemly linked and clustered in the genome of the genome of the winter flounder. Proc Natl Acad Sci USA 82:2613–2617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shier WT, DeVries AL (1975) Carbohydrate of antifreeze glycoproteins from an Antarctic fish. FEBS Lett 54:135–138

    Google Scholar 

  • Shier WT, Lin Y, DeVries AL (1972) Structure and mode of action of glycoproteins from Antarctic fishes. Biochim Biophys Acta 263:406–413

    Article  CAS  PubMed  Google Scholar 

  • Slaughter D, Fletcher GL, Ananthanarayanan VS, Hew CH (1981) Antifreeze proteins from the sea raven, Hemitripterus americanus. J Biol Chem 256:2022–2026

    Article  CAS  PubMed  Google Scholar 

  • Smith K, Spadafora C (2005) Sperm-mediated gene transfer: applications and implications. BioEssays 27:551–562

    Article  CAS  PubMed  Google Scholar 

  • Sorhannus U (2012) Evolution of type II antifreeze protein genes in teleost fish: a complex scenario involving lateral gene transfers and episodic directional selection. Evol Bioinform 8:535–544

    Article  CAS  Google Scholar 

  • Sutherland TD, Young JH, Weisman S, Hayashi CY, Merritt DJ (2009) Insect silk: one name, many materials. Annu Rev Entomol 55:171–188

    Article  CAS  Google Scholar 

  • Tautz D (2014) The discovery of de novo gene evolution. Perspect Biol Med 57:149–161

    Article  PubMed  Google Scholar 

  • Tautz D, Domazet-Lošo T (2011) The evolutionary origin of orphan genes. Nat Rev Genet 12:692–702

    Article  CAS  PubMed  Google Scholar 

  • Venugopal T, Anathy V, Kirankumar S, Pandian TJ (2004) Growth enhancement and food conversion efficiency of transgenic fish Labeo rohita. J Exp Zool A Comp Exp Biol 301A:477–490

    Article  CAS  Google Scholar 

  • Wang X, DeVries AL, Cheng C-HC (1995a) Antifreeze peptide heterogeneity in an Antarctic eel pout includes an unusually large major variant comprised of two 7 kDa type III AFPs linked in tandem. Biochim Biophys Acta 1247:163–172

    Article  PubMed  Google Scholar 

  • Wang X, DeVries AL, Cheng C-HC (1995b) Genomic basis for antifreeze peptide heterogeneity and abundance in an Antarctic eel pout: gene structures and organization. Mol Mar Biol Biotechnol 4:135–147

    CAS  PubMed  Google Scholar 

  • Yamashita Y, Miura R, Takemoto Y, Tsuda S, Kawahara H, Obata H (2003) Type II antifreeze protein from a mid-latitude freshwater fish, Japanese smelt (Hypomesus nipponensis). Biosci Biotechnol Biochem 67:461–466

    Article  CAS  PubMed  Google Scholar 

  • Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–693

    Article  CAS  PubMed  Google Scholar 

  • Zelensky AN, Gready JE (2005) The C-type lectin-like domain superfamily. FEBS J 272:6179–6217

    Article  CAS  PubMed  Google Scholar 

  • Zhuang X, Yang C, Fevolden S-E, Cheng CC (2012) Protein genes in repetitive sequence-antifreeze glycoproteins in Atlantic cod genome. BMC Genomics 13:293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhuang X, Murphy KR, Ghigliotti L, Pisano E, Cheng CC, (2018) Reconstruction of the repetitive antifreeze genomic loci in the cold-water gadids Boreogadus saida and Microgadus tomcod. Mar Genomics 39:73–84

    Google Scholar 

  • Zhuang X, Yang C, Murphy KR, Cheng CHC (2019) Molecular mechanism and history of non-sense to sense evolution of antifreeze glycoprotein gene in northern gadids. Proc Natl Acad Sci 116:4400–4405

    Google Scholar 

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Correspondence to C.-H. Christina Cheng .

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Cheng, CH.C., Zhuang, X. (2020). Molecular Origins and Mechanisms of Fish Antifreeze Evolution. In: Ramløv, H., Friis, D. (eds) Antifreeze Proteins Volume 1. Springer, Cham. https://doi.org/10.1007/978-3-030-41929-5_9

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