Comp. Biochem. Physiol. Vol. 84B, No. 4, pp. 575 588, 1986 0305-0491/86 $3.00+0.00 Printed in Great Britain Pergamon Journals Ltd

ISOZYMES OF GLUCOSEPHOSPHATE ISOMERASE (PGI) IN FISHES OF THE SUBCLASS

ACTINOPTERYGII

ZULEMA COPPES

Departamento de Bioquimica y Biofisica, Facultad de Humanidades y Ciencias, Universidad de la Rephblica, Tristan Narvaja 1674, Montevideo, Uruguay

(Received 9 August 1985)

Abstract--1. A compilation of the species of fishes of the subclass Actinopterygii for the study of the PGI isozyme system is given.

2. PGI appears to be codified by more than one locus in fishes; 65% of the species analysed here have two loci for PGI.

3. PGI duplication in fishes and the relationship of isozymes of PGI with temperature and metabolism are discussed.

INTRODUCTION

Phosphoglucose isomerase (PGI: EC5.3.1.9), a dimeric enzyme with a mol. wt of 132,000 (Darnall and Klotz, 1975), catalyses the interconversion of glucose-6-phosphate and fructose-6-phosphate. PGI is an important enzyme in the regulation of carbo- hydrate metabolism since it determines the amount of D-glucose-6-phosphate that enters the glucolytic way (Meijer and Bloem, 1962). In the metabolic process, this enzyme represents the ramification point between the glycolytic or fermentative pathway and the shunt of pentoses.

PGI was discovered by Lohman (1933), and the first electrophoretic variant was detected in mouse erythrocytes (Carter and Parr, 1967) and man (Detter et al., 1968; Fitch et al., 1968). This enzyme has been studied in several groups of vertebrates: mammals, birds, reptiles and frogs (Carter and Parr, 1967; Zaltitis and Oliver, 1967; Detter et al., 1968; Fitch et al., 1968; Saison, 1968; Carter and Yoshida, 1969; De Lorenzo and Ruddle, 1969; Yoshida and Carter, 1969; Andressen, 1970; Ishimoto, 1970; Welch, 1971; Welch et al., 1971; Blackburn et al., 1972; Carter et al., 1972; Nottebohm and Selander, 1972; Webster et al., 1973; McMorris et al., 1973; Mathers et al., 1974; Tilley et al., 1974; Yang et al., 1974; Ralin and Selander, 1979; Dando, 1980; Fisher et al., 1980) and invertebrates (Selander et al., 1970). In these groups of fishes PGI occurs as a single major form, suggesting a single gene control.

In fishes, PGI appears to be codified by more than one locus. The formation of a heterodimeric enzyme such as PGI, by the association of subunits codified by two gene loci, shows us strong evidence of its homology and consequently of the origin of loci through duplication (Avise and Kitto, 1973). The evolutionary potential of duplicated genes was appre- ciated before the molecular and biochemical tech- niques had documented their existence (Avise and Kitto, 1973). According to the point of view formu- lated by Huxley (1942), Lewis (1951) and Stephens (1951), one locus maintains its previous functions and

the other is free to undergo duplications through chromosomic rearrangements and mutations and to assume new functions, frequently similar to those of the original gene.

There are several examples of homologous en- zymes in fishes: creatine kinase (Eppenberger et al., 1971; Fisher and Whitt, 1978; Fisher et al., 1980; Whitt, 1981), lactate dehydrogenase (Whitt et al., 1973a, b; Markert et al., 1975; Whitt et al., 1975; Fisher et al., 1980; Whitt, 1981; Philipp et al., 1983a,b; Coppes de Achaval, 1984; Panepucci et al., 1984; Whitt, 1984), phosphoglucose isomerase (Avise and Kitto, 1973; Dando, 1974, 1980; Coppes de Achaval, 1980; Fisher et al., 1980; Coppes de Achaval et al., 1982; Philipp et al., 1983a, b; Coppes, 1985), malate dehydrogenase (Clayton et al., 1975; Fisher et al., 1980; Schwantes and Schwantes, 1982). Phos- phoglucose isomerase is one isozyme system that owing to its multigenic nature becomes an interesting model for evolutionary studies, and from this aspect it was investigated (Avise and Kitto, 1973; Dando, 1974, 1980; Coppes, 1985).

Fishes, the most primitive of vertebrates, are excel- lent organisms for studying the formation and evo- lution of isozyme loci (Whitt, 1981). Bony fishes represent the line from which advanced vertebrates (amphibians, reptiles, birds and mammals) evolved. They include the subclass Actinopterygii, with the infraclasses--Chondrostei, Neopterygii and Teleostei (Norman, 1975). Teleosts include approximately 7 superorders, 50 orders, 445 families and a number of species estimated as 21,723, representing 60% of all vertebrates (Nelson, 1984).

The present paper is a recompilation of the species of fishes for the study of the PGI isozyme system. The species listed here (Table 1) were classified according to Norman (1975).

PROBABLE NUMBER OF LOCI CODING FOR PHOSPHOGLUCOSE ISOMERASE IN FISHES

In fishes, PGI is encoded by one (Avise and Kitto, 1973; Dando, 1974, 1980; Schmidtke et al., 1975a, b;

575

576 ZULEMA COPPES

Table 1. List of the species of fishes of the subclass Actinopterygii used for the study of the PGI isozymes'

INFRACLASS CHONDROSTEI Order Acipenseriformes

Family Acipenseridac Scaphirhynchus a/bus

Family Polyodontidae Po6"odon spathuhz

INFRACLASS NEOPTERYGI1 Order Semionotiformes

Family Lepisosteidae Lepisosteus ocukm~s tepisosteus osseu~ Lepisosteus platostomus

Order Amiiformes Family Amiidae

Amia cah'ia

INFRACLASS TELEOSTEI

SUPERORDER ELOPOMORPHA Order Anguitliformes

Family Anguillidae Anguilla anguilla Anguilla australis Anguilla rostrata

Family Congridae Conger conger Congrina tiara

Family Muraenidae Muraena rniliaris

SUPERORDER CLUPEOMORPHA Order Clupeiformes

Family Clupeidae grecoorlia lyranllu~ Clupea harengus Oorosoma cepemtianum

Harenguht sardina Sardina pilchardus Sprattus antipodon Sprattus ~prattus

Family Engraulidae Engraulis encrasicolus

SUPERORDER OSTEOGLOSSOMORPHA Order Osteoglossiformes

Family Hiodontidae Hiodon tergisu,~

Family Notopteridae Notopterus kapirat

Family Osteoglossidae Osteoglossum hicirrosum

Family Pantodontidae Panzodon buchh}zi

SUPERORDER PROTACANTHOPTERYGII Order Salmoniformes

Family Argentidae Argentina silus

Family Esocidae Esov americanus

Family Osmeridae Osmerus eperhmus

Family Salmonidae Coregonus /era Coregonus /Ol:arelus Oucorhynchus gorbuschu O. kela O. kLs'utch O. nerka O. tshawytschu Sabno aquohonita S. chlrki S. gairdneri S. irideu~ S. saber S. lrutta

Sah~elinus /ontinalis S. nano'cusch

Family Sternotychidae

(108}

(108)(109)

(l)(to8) (lo8) 0)0o8)

(I) 2 (108)

(2)(3)(92)(93)(94)(95) 1 (5)

(3)(29)(30)(92)195)(108) (2)(4) (2)(4)

(108)

i (i) 1 (1)(2)(6)(9)(31)(88) 2 (Io8)

(1) 008) (2) (5) (2)(8)(77}

(2)

(108)

(2)

(108)

(2)

(108)

(1)(108)

(2)(6)(7)(8)

3 (8) 3 (8) 3 (53)(55)(98) 3 (53)(98) 2 (53)(98) 3 (53)(74)(98) 3 (53)(98) 3 (91) 3 (11)(49)(50)(56)(98) 3 (41)(49)(50)(91)(98)(99) 3 (7)(8) 2 (2)(6)(7)(51)(52)(58) 3 (1)(59)(91) 2 (7)(8)19)(10) 3 (1)(7)(8)(10)(57)(108) 3 (57)

008)

Fish PGI 577

Table 1. (continued)

SUPERORDER OSTARIOPHYSI Order Cypriniformes

Family Anostomidae Leporinus friderici L. silvestri Schizodon nasuttus

Family Catostomidae Carpiodes carpio C. cyprinus C. velifer Catostomus catostomus C. columbianus C. commersoni C. discobulus C. luxatus C. macrocheilus C. occidentalis C. platyrhincus C. plebeius C. fumeiventris C. santaanae Chasmistes brevirostris Cycleptus elongatus Erimyzon oblongus E. sucetta E. tenuis Hypentelium etowanum H. nigricans H. roanokense Ictiobus bubalus L cyprinellus L niger Minytrema melanops noxostoma anisurum M. ariommum M. austrinum M. carinatum M. cervinum M. congestum M. duquesnei M. erythrurum M. hamiltoni M. lachneri M. macrolepidotum M. mascotae M. pappillosum M. peocilurum M. rhothoecum M. robustum M. rupiscartes M. valenciennesi Thorbunia atripinne T. hamiltoni T. rhothoeca Xyrauchen texanus

Family Characidae Astyanaz mexicanus Cheirodon axelrodi

Family Cobitidae Acanthopthalmus choirorhyncus .4. semicunctus Botia macrocantha B. modesta

Family Cyprinidae Abramis brama Barbus barbus B. tetrazona Brachydanio albolineatus B. rerio Carassius auratus

Cyprinus carpio

Campostoma anomalum C. oligolepis C. ornatum Ctenopharygodon idella Gila orcutti Hesperoleucus symmetrivus Hypohthalmichthys nobUis

3 (19)(20) 4 (19)(20) 3 (19)(20)

4 (32)(60) 4 (17)(32)(60) 4 (32)(60) 4 (17)(32)(60)(108) 4 (32) 4 (17)(32)(60)(109) 3 (17)(32)(90)(109) 4 (32) 4 (32) 4 (32) 3 (32) 3 (32)(35)(60) 4 (79) 3 (79)(80) 4 (17)(32) 4 (17)(32)(60) 3 (17)(32)(50) 3 (I 5)(32)(60)(64)(108) 3 (l 7)(32)(60) 3 (12)(32)(106) 3 (l 2)(I 7)(32)(60)(107) 4 (12)(106) 4 (17)(32)(60) 4 (32)(60) 4 (32)(60) 4 (60) 3 (12) 3 (12) 3 (12) 3 (12)(60) 3 (12)(32)(60) 3 (12)(32) 3 (12)(17)(32)(60) 3 (12)(17)(32) 2 (16) 4 (12)(41) 3 (12)(32)(60) 3 (12) 3 (12) 3 (12) 3 (16)(32) 3 (12) 3 (12) 3 (12) 3 (107) 3 (107) 3 (107) 4 (17)(32)

(1)(33) (34)

(18) (18) (18) (18)

(7)(8) (7) (7)(8) (97) (97)

3 (1) 4 (7) 2 (13) 3 (36)(76)(108)

(40) (40) (40) (38)(39) (79) (37) (39)

578 ZULEMA COPPES

Table 1. (continued)

Lavinia exilicauda Notropis

Subgenre Luxilus Nolropis venustus Scardinius erythrothalnius Notimigonus crysoh, ucas

Order Gonorynchiformes Family Chaniidae

Chanos chanos Order Siluriformes

Family Ariidae Arius fi'lis

Family Callichthyidae Corydoras aeneus C. julii C. myersi C. sp.

Family Ictaluridae Ictalurus rnelas I. natalis 1. punctatus

Family Loricariidae 14~Tostomus sp.

Family Pimelodidae Pimelodus maculatus

SUPERORDER SCOPELOMORPHA Order Myctophiformes

Family Myctophidae Argyropeleeus offerri

Family Synodontidae Synodon ./oetens

S. intermedius

SUPERORDER PARACANTHOPTERYGll Order Batrachoidiformes

Family Batrachoidae Opsanus beta Poriehthys porosissimus

Order Gadiformes Family Carapidae

Carapus bermudensis Family Gadidae

Gadus morhua Lola h~ta Microgadus tomcod Theragra ehah'ogramma Uruphyeis chuss

Family Macrouridae Coelorhynehus coelorhynchus

Family Merluciidae Merlucius australia'

Family Ophidiidae Rissola marginata Genvpterus blacodes

Family Zoarcidae Zoarces viviparus macrozoarces artterieanus

Order Lophiiformes Family Antennariidae

Antennarius sp. Family Lophiidae

Lophius piscatorius Family Ogocephalidae

Dibranchus atlanticus

SUPERORDER ACANTHOPTERYGII Order Atheriniformes

Family Atherinidae Allanetta harringtonensis A therina presbyter Menidia audens M. beo'llina M. extensa M. menidia M. peninsulae

Family Belonidae Bellone belhme 7),losure.~ crocodilus

(37)

(13) (1) (2) (108)

(42)

(1)

3 (43) (43) (43) (108)

(I)(108) (108) (4)(108)

5 (19)(20)

4 (19)(20)

(108)

2 (108) I ( I )

(108)

(1) (108)

(108)

(2) (108) (1) (87) (108)

(108)

I (5) 2 (1)(72)

(1) I (5)(73)

( 1 )(44) (108)

(2)

(2)

(108)

(108) (2) (86) (84)(86) (86) (84)(86) (84)(86)

(2) (108)

Family Cyprinidontidae Cyprinodon variegatus Fundulus heteroclitus F. notatum

Family Exocoetidae Hyporhamphus unifasciatus

Family Poecilidae Gambusia affinis Gambusia geiserie Gambusia heterochir Poecilia formosa Genus Xiphophorus X. couchianus X. helleri X. maculatus

Order Beryciformes Family Holoncentridae

Holocentrus ascensionis Order Gasteroiformes

Family Sygnathidae Corythoichthys braehycephalus Syngnathus fuscus

Order Perciformes Family Acanthuridae

Acanthurus chirurgus Family Arripidae

Arripis trutta Family Carangidae

Caranx crysops C. georgianus Seriola grandis Trachurus declives T. novaezelandidae

Family Centrolophidae Seriolella brama

Family Cheilodactylidae Cheilodactylus macropterus C. douglasi

Family Cichlidae Cichlasoma cyanoguttatum Haplochromus flaviijosephi Sarotherodon niloticus S. aureus Tilapia zillii Tristamella sacra 72 simonis

Family Centrarchidae Acanthatchus pomotis Ambloplites rupestris Archopfites interruptus Centrarchus macropterus Elassoma evergladei E. okefenokee Enneacanthus gloriosus E. obesus Lepomis auritus L. cyanellus

L. gibbosus L. gulosus L. humilus L. macrochirus L. marginatus L. megalotis L. microlophus L. punclalus Micropterus dolomieui M. salmoides Pomoxis annularis P. nigromaculatus

Family Cottidae Hemitripterus americanus

Family Gempylidae Rexea solandri Thrysites atun

Family Gerreidae Eucinostomus lefroyi

Family Kyphosidae Girella tricuspidata

Fish PGI

Table 1. (continued)

(1) (I)(46)(47)(48)(100)(108) (108)

008)

(1) (l) (1) (l) 011) (75) (45)(75)(76) (45)(75)(76)

(108)

(1o8) i (1)

(108)

1 (5)

(108) (5)(67)

2 (5) i (5)(67) 1 (5) 2 (25)

1 (5)

2 (5)(67) (5)

(I) (61) (61) (61) (61) (61) (61)

(62)(104) (62)(69)(108) (62) (62)(104) (62) (62) (104) (62)(104) (62) (21 )(22)(62)(63 )(64)( 65)(81 )( 101 ) (102)(103)(105)(106)(108) (62) (22)(62)(69)(103)(104)(108) (1)(62) (1)(62)(69)(103)(104)(108) (62) (62)(103)(108) (62)(69)(101)(102)(104)(105)(108) (62)(104) (23)(69)(108) (1)(23)(62)(66)(69)(78)(81)(104)(108) (69)(108) (62)(104)

(1)

1 (5) 1 (5)

(108)

(5)

579

580 ZULEMA COPPES

Table 1. (continued)

Family M ugilidae Mugil eephalus

Family Percichthidae morone americana M. cho'sops M. mississipiensis M. saxatilis

Family Percidae Etheostoma jontieola E. mieropereu E. proeliare Perehta eaprodes

Family Percophididae Hemeroeoetes sp.

Family Pomadasydae Haemulon seiurus Orthopristis ehrysoptera

Family Pomatomidae Pomalomus saltatrix

Family Pseudochidae Pseudophyeis bacchus

Family Scaridae Sparisoma ruhripinnae

Family Sciaenidae Aplodinotus gruniens Qvnoseion striatus (~voseions nolhus Maerodon ancylodon Mieropogon undulatus Mieropogonias [i~rnieri

Family Scombridae Seomber scombrus S. austra[asieus

Family Serranidae ('entropristri.v striata Dieentrarchus labrax Epinephelu.~ adseem'ionis

Family Sparidae Cho'sophrys auratus Lagodon rhomhoides Stenotomus chrysops

Family Sphyraenidae Sphyruena argentea S. barracuda S. ensis S. idiaste,~ S. lucasana

Family Stromateidae Prepilus triaeanthus

Family Trichiuridae Trichiurus lepturus

Order Pleuronectiformes Family Bothidae

Ancylopsetta quadraeellata Pho,norhombus novogieus

Family Cyonoglossidae Symphurus plugissa

Family Pleuronectidae Limanda limanda Plaliehthys flesus Pleuronectes phttessa Pseudopleuronectes americanus Reinhardtius hippoglossoides

Family Soleidae Achirus lineatus Solea solea

Order Scorpaeniformes Family Scorpaenidae

Sehastes alutus S. caurinus S. elongatus

Family Triglidae Prionotus trihulus P. sp. Trigla kumei

Order Tetraodontiformes Family Balistidae

Nm'odon scaber Family Ostraciidae

Ostraeion diaphanum

( i )

(68) (69)( 1 o8) (108) (68)

(70) (7O) (7O) (I)

(5)

008) (1)

1 (1)

(67)

(108)

008) 3 (28)

(I) 3 (28)

(I) 3 (28)

(1)(2)(24)(82) (1)(5)(25)

(1) (2) (IO8)

(5)(25)(89) (1o8) (i)

(96) 008) (96) (96) (96)

(1)

(i)(1o8)

(l) (2)

i (1)

(2) (2) (2)(27)(71)(I I I) (109) (83)

(I) (2)

(26) (26) (26)

(lO8) (1) (5)(67)

i (5)

(108)

Fish PGI

Table I. (continued)

581

Family Tetraodontidae Diodon hystri (108) Lagocephalus lagocephalus (2) Sphoeroides parvus (1)

Order Zeiformes Family Zeidae

Cyttus austral& 1 (5) Zeus japonicus 1 (5)

I. Avise and Kitto (1973); 2. Dando (1974); 3. Comparini et al. (1977); 4. Mo et al. (1975); 5. Gauldie and Smith (1978); 6. Schmidtke and Engel (1974); 7. Schmidtke et al. (1975a); 8. Schmidtke et al. (1975b); 9. Engel et al. (1975); 10. Engel et al. (1977); II. Reinitz (1977); 12. Buth (1979a); 13. Buth (1979b); 14. Ferris and Whitt (1977a); 15. Shaklee et al. (1974); 16. Buth (1977); 17. Ferris and Whitt (1979); 18. Ferris and Whitt (1977b); 19. Coppes de Achaval (1980); 20. Coppes de Achaval et al. (1982); 21. Champion and Whitt (1976a); 22. Champion and Whitt (1976b); 23. Philipp et al. (1979); 24. Smith and Jamieson (1978); 25. Smith and Crossland (1977); 26. Johnson et al. (1973); 27. Purdom et al. (1976); 28. Coppes (1985); 29. Koehn and Williams (1978); 30. Williams et aL (1973); 31. Grant (1981); 32. Ferris et al. (1979); 33. Avise and Selander (1972); 34. Kuhl et al. (1976); 35. Ferris et al. (1982); 36. Schmidtke and Engel (1975); 37. Avise et al. (1975); 38. Utter and Folmar (1978); 39. Magee and Philipp (1982); 40. Buth and Burr (1978); 41. Buth (1982); 42. Winans (1979); 43. Dunham et al. (1980); 44. Yngaard (1972); 45. Siciliano and Wright (1976); 46. Palumbi et al. (1980); 47. Powers and Place (1978); 48. Mitton and Koehn (1975); 49. Utter et al. (1976); 50. Allendorf and Phelps (1980); 51. Cross and Ward (1980); 52. Wilkins (1972a); 53. May (1975); 54. Allendorf (1975); 55. Seeb and Whishard (1977); 56. Campton (1980); 57. May et al. (1980); 58. Wilkins (1972b); 59. Allendorf et al. (1977); 60. Ferris and Whitt (1980); 61. Kornfield et al. (1979); 62. Avise et al. (1977); 63. Shaklee et al. (1977); 64. Champion et al. (1975); 65. Whitt et al. (1976); 66. Philipp et al. (1981); 67. Gauldie and Johnston (1980); 68. Sidell and Otto (1978); 69. Philipp et al. (1983a); 70. Buth et al. (1980); 71. Ward and Beardmore (1977); 72. Smith et al. (1979); 73. Smith (1979); 74. Grant et al. (1980); 75. Morizot and Siciliano (1982a); 76. Morizot and Siciliano (1982b); 77. Smith and Robertson (1981); 78. Philipp et al. (1983b); 79. Crabtree and Buth (1981); 80. Buth and Crabtree (1982); 81. Whitt et aL (1977); 82. Smith and Jamieson (1980); 83. Fairbain (1981); 84. Johnson (1974); 85. Vuorinen (1984); 86. Johnson (1975); 87. Grant and Utter (1980); 88. Anderson et al. (1981); 89. Smith et al. (1978); 90. Smith et al. (1983); 91. Wishard et al. (1984); 92. Williams and Koehn (1984); 93. Comparini et aL (1975); 94. Rodino and Comparini (1978); 95. Comparini and Rodino (1980); 96. Graves and Somero (1982); 97. Pontier and Hart (1981); 98. Utter et al. (1980); 99. Busack et al. (1980); 100. Place and Powers (1978); 101. Pasdar et al. (1984a); 102. Pasdar et al. (1984b); 103. Parker et al. (1985a); 104. Parker et al. (1985b); 105. Pasdar et al. (1984c); 106. Buth (1980); 107. Buth (1979c); 108. Fisher et al. (1980); 109. Carlsson et aL (1982); 110. Morizot and Siciliano (1983); 111. Galleguillos and Ward (1982)

*The number of loci was noted down in the species that possess other than two loci. All the others possess two loci for PGI.

Fisher et al., 1980), two (Avise and Kitto, 1973; Johnson et al., 1973; Dando, 1974, 1980; Mo et al., 1975; Schmidtke et al., 1975a, b; Champion and Whitt, 1976a, b; Allendorf et al., 1977; Comparini et al., 1977; Engel et al., 1977; Smith and Crossland, 1977; Gauldie and Smith, 1978; Place and Powers, 1978; Smith and Jamieson, 1978; Smith, 1979; Buth, 1979a, b,c; Cross and Ward, 1980; Dunham et al., 1980; Fisher et al., 1980; Philipp et al., 1983a,b; Pasdar et al., 1984a, b,c; Parker et al., 1985a,b), three (Avise and Kitto, 1973; Shaklee et al., 1974; Schmidtke et al., 1975a,b; Kuhl et al., 1976; Allendorf et al., 1977; Engel et al., 1977; Dunham et al., 1980; Coppes de Achaval et al., 1982; Coppes, 1985), four (Schmidtke et al., 1975b; Coppes de Achaval, 1980; Coppes de Achaval et al., 1982) and five (Coppes de Achaval et al., 1982) gene loci.

The PGI codified by two gene loci genetically independent in the majority of fishes studied, shows a modification and divergence in the structure and function which follows gene duplication. The two enzymes which catalyse the same reaction show marked differences in electrophoretic mobility, heat inactivation, and reaction with inhibitors (Avise and Kitto, 1973).

As we can see in Table 1, the majority of the species of fishes studied show the existence of two gene loci which codify PGI, with a differential expression in tissues. According to Schmidtke et al. (1975b), only some species of Salmonidae and Cyprinidae, show more than two PGI loci, reflecting the tetraploid

origin of these species. Thus, Ohno (1970) thinks that polyploidization has been an important factor in the primitive formation of chordates (nearly 500 million years ago) and it has caused the great diversity of isozymes found in present day vertebrates. The elec- trophoretic analysis of proteins of recent polyploids (50 to 100 million years), suggests that these are codified by a number of loci greater than their related diploid species (Allendorf et al., 1975; Engel et al., 1975; Ferris and Whitt, 1977a,b,c). To consider polyploidy as an evolutionary factor in vertebrates, it is necessary to admit diploidization. A recent polyploid begins its evolution containing four homologous chromosomes. If a tetraploid state could contribute to the creation of new gene loci, the diploid state might eventually be reestablished by the functional diversification of the four original hom- ologous. The preferential formation of two bivalent contrasts to the quadrivalents in meiosis is a pre- requisite for diploidization (Ohno, 1970). Thus in the diploid species studied by Coppes de Achaval (1980), Coppes de Achaval et al. (1982), Coppes (1985) and belonging to the orders Cypriniformes and Siluri- formes, three, four and five genetic loci were found for PGI, suggesting a tetraploid origin with later diploidization. However, in the species studied by these authors, there is no indication of polyploidy. In this case, it is difficult to admit that the number of loci which determine PGI would be owed to any hypo- thetical and ancient polyploidy. As PGI is frequently polymorphic the occurrence of duplications of this

582 ZULEMA COPPES

type increases. However, several proteins studied from subtropical regions (Hb, MDH and LDH), as well as those from temperate regions (LDH, s-MDH and CK) did not show codification by a number of loci greater than those expected for diploid species.

PG| DUPLICATIONS IN FISHES: POSSIBLE ORIGIN

To determine the occurrence of PGI loci in fishes with the fundamental purpose of understanding the evolutionary history of gene duplication and its ori- gin, data in literature were collected from 283 species belonging to 21 orders, subclass Actinopterygii. The whole discussion is based on the phylogeny of Osteichthyes, of Romer (1966) and the classification by Norman (1975). Arise and Kitto (1973) study- ing 53 species belonging to 15 orders gave an evolutionary history for PGI loci in fishes.

In the order Perciformes (Acanthopterygii), the majority of fishes, 73 of the 84 species belonging to 28 families have two loci for PGI. Analysing the Superorder Protacanthopterygii, from which prob- ably all higher teleosts arose (Avise and Kitto, 1973), in the order Salmoniformes, 14 species of 18 have three loci for PGI. According to Avise and Kitto (1973) the possibility of secondary loss of a duplicate locus in higher teleosts cannot be excluded, so they conclude that the original gene duplication occurred sometime before the branching of the Prota- canthopterygii and is now manifest in nearly all higher teleosts, so the majority of higher teleosts show two loci for PGI. However, analysing the Superorder Ostariophysi (more advanced teleosts than the Protacanthopterygii), we see that of a total of 87 species, 31 show three loci for PGI and 20, four. Thus, 51 species of 87 present more than two loci for PGI (representing 58%).

Most diploid teleosts have two gene loci encoding PGI isozymes (Arise and Kitto, 1973: Johnson et al., 1973; Dando, 1974; Mo et al., 1975; Schmidtke et al., 1975a, b; Champion and Whitt, 1976a,b; Allendorf et al. , 1977; Comparini et al., 1977; Engel et al., 1977; Smith and Crossland, 1977; Gauldie and Smith, 1978; Place and Powers, 1978; Smith and Jamieson, 1978; Smith, 1979; Buth, 1979a,b; Dunham et al., 1980; Fisher et al., 1980; Philipp et al., 1983a,b) (Table I). Thus, the duplicate gene for PGI is of widespread occurrence in fish. In the Superorder Ostariophysi, Cypriniformes diploid fishes were found to have their PGI encoded by two loci (Arise and Selander, 1972; Avise and Kitto, 1973; Dando, 1974; Schmidtke et al., 1975a,b; Kuhl et al., 1976; Buth, 1977; Ferris and Whitt, 1977a,b; Buth, 1979a,b; Ferris and Whitt, 1979), whereas in the case of tetraploid fish, the PGI is encoded by three (Arise and Kitto, 1973; Shaklee et al., 1974; Engel et al., 1975; Schmidtke et al., 1975a, b) or four loci (Schmidtke et al., 1975b). However the data presented by Coppes de Achaval et al. (1982) showed a number of loci higher than that reported for other Cypriniformes diploid species: thus, the authors believe that the PGI loci correspond to the ones described for the tetraploid fish of this order. Among diploid species of the order Siluri- formes PGI is also encoded by two gene loci (Arise and Kitto, 1973; Mo et al., 1975; Dunham et al.,

1980; Fisher et al., 1980). Dunham et al. (1980) showed a duplication at the PGI-2 locus in a South American catfish (family Callichthydae), a pre- sumptive tctraploid species. Here again the number of loci obtained in a diploid species by Coppes de Achawd et al. (1982) correspond to that for a letra- ploid species. In the genus l l y p o s t o m u s , Coppes de Achaval el al. (1982) found a species, which accord- ing to Miehelle et al. (1977) possess a haploid chro- mosome number (n = 34 and 37), with PGI encoded by five loci.

The time postulated by Arise and Kitlo (1973~ oi PGI gene duplication was early in the teleost line since the most primitive group in which they lbund two PGI loci was the Anguilliformes. But Fisher et al, (1980) and Dando (1980) have observed that the most primitive group in which they found two PGI loci was the Cyclostomata. The observations taken by Arise and Kitto (1973) were due to the single locus lbund in the Semionotiformes, the most primitive fishes the5' studied. The two PGI loci clearly expressed in lhe agnathans (lampreys) strongly suggest that the time of PGI gene duplication was much earlier lhan tile time postulated by Arise and Kitto. This idea is strengthened by the observation of Fisher ~'; ul. (1980) that two PGI loci were found in Cross- opterygii and Dipnoi (Subclass Sarcopterygii).

According to these observations and for us to localise the group of fishes we are studying here, a scheme was made (Fig. 1),

Since Zuckerkandl and Pauling (1965) have shown that the analysis of phylogeny at molecular level is valuable in resolving questions about systematics o1" advanced groups, these have become more frequent. These studies are, of course, limited to extant species, and the complexity of the problem varies with the particular group studied. Fishes are advantageous because of the numcrous taxa today they are repre- sented and the existence of one or more species morphologically similar to their ancestors.

Several authors (Fisher and Whitt, 1978: Fisher et al., 1980: Whitt, 1981, 1983: Schwantes and Schwantes, 1982a,b); lhink that the morphological conservation of certain extant species reflects a partial conservation of the pattern of the ancestral gene function, which in its turn reflects a conservation of one portion of the structure of the genome. A study of one multilocus isozyme system in several remain- der groups of fishes may lead to suggestions about the patterns of gene regulation at different evolutionary levels (Markert et al., 1975; Whitt et al., 1975: Whitt, 1983).

The evolutionary importance of gene duplication has been repeatedly emphasized (Lewis, 1951: Ingrain, 1961; Zuckerkandl and Pauling, 1965: Ohno et al., 1967: Watts and Watts, 1968a,b: Ohno, 1970, 1974: Arise and Kitto, 1973; Wilson, 1975; Sparraw and Naumann, 1976: Wilson et al., 1977: WhiH, 1983).

According to Fisher and Whitt (1978), the evo- lutionary alterations that occurred after the establish- ment of the simplest way o1" life, were originated by modifications of pre-existing specifically functional genes. The evolutionary transformation of a neutral gene with a new function would involve a loss of the ancient function: at least the transformation would

Fish PGI 583

Act inopteryg t i

¢ Poroconthopterygi ( I, 2) ~con)thopterygi i ( 2 )

Ostoriophysi (2,3,4,5)

~ ~ e r y g i i (3 41

If

I! - Osteoglossomorpha (2) Teleosteii / / Clupeomorpho (I)

Neopterygii ( I ?, 2 )

Chondros~ei (2)

Fig. 1. Probable number of loci for PGI (in brackets) that are present in fishes Actinopterygii.

be measured by the formation of additional copies of the ancestral gene.

There are several examples of gene duplication which lead to homologous proteins: haemoglobin (Goodman et al., 1975), cytochrome c (Goldberg, 1977), lactate dehydrogenase (Markert et aL, 1975), phosphoglucose isomerase (Avise and Kitto, 1973; Dando, 1974; Coppes de Achaval et al., 1982), carbonic anhydrase (Tashian et al., 1983), immuno- globulins (Dayhoff, 1972). PGI as well as other enzymes (s-MDH, CK, LDH) is a good isozymic system which serves as a model for studying the evolution of isozymic loci (Fisher et al., 1980; Whitt, 1983), and was formed by relatively ancient gene duplication and maintained for hundreds of million years (Whitt, 1983).

The number of isozymic loci present in a given species is easily estimated by electrophoresis since those loci diverged and therefore, their isozymes are different owing to the unnumbered amino acid substi- tutions. The confirmation of number of loci present is obtained by (1) presence of genetic variants, (2) observations of the number and relative intensities of isozymes and (3) physical and antigenic properties of isozymes (Fisher et al., 1980; Whitt, 1981).

ISOZYMES OF PGI, TEMPERATURE AND METABOLISM

Body temperature of poikilothermic animals changes with ambient temperature but it is not necessarily the same as that of the environment (Hochachka and Somero, 1973, 1984; Jankowsky, 1973). The gradient of temperature between the body and the environment is not only a function of the production and loss of heat. There are also, a number of environmental factors which surround the organ- ism, such as solar radiation, humidity and drought (Jankowsky, 1973).

We could consider organisms as a total of inter- related chemical reactions, catalysed by enzymes.

These are macromolecules widely influenced by fac- tors such as pH, temperature, salinity and inhibitors.

One of the pioneer works about adaptation of enzymes to temperature was done by Hochachka and Somero (1968). These authors show that the affinity of LDH with substrate varies with temperature and reaches its maximum value (minimum Km) at the temperature to which the organism is adapted. Moon (1975), Schwantes et aL (1976), De Luca (1980), Schwantes and Schwantes (1982a, b), De Luca et al. (1983), suggest that alterations in ambient tem- perature act as positive or negative modulators, inducing increasing or decreasing of enzyme activity of certain isozymes during acclimation. So, ecto- therms would alter the isozymic complement, prefer- entially yielding a quantity of isozymes with great catalytic efficiency at each temperature. Thus, there would be cold and warm adapted isozymes. The existence of multiple forms of an enzyme, would permit the organism to have catalytic material available to face changes in the environment which influence the inner environment of ectotherms.

Isozymes of PGI, resist in a different way, alter- ations in temperature (Arise and Kitto, 1973; Shaklee et al., 1977; Coppes de Achaval, 1980; Coppes de Achaval et al., 1982; Coppes, 1985). Thus, meanwhile PGI-B2 is more resistent to heat inactivation, PGI-A2 is more thermolabile.

The isozymic alterations detected during the pro- cess of acclimation, led some authors to propose that these could be important components in thermo- acclimation of ectotherms in general, and thus would represent "qualitative strategies of biochemical adap- tation" (Somero and Hochachka, 1971; Hochachka and Somero, 1973, 1984). On the other hand, the existence of divergence in PGI loci at the different tissues would permit a difference in the regulation of metabolism. According to Pearse (1972), PGI is an important enzyme in the regulation of metabolism of carbohydrates since it determines the quantity o1 D-glucose-6-phosphate in glycolysis. The reaction

C.BP 8 4 4 ~ K

584 ZULEMA COPPES

catalysed by PGI is reversible, yielding G-6-P or F-6-P, depending on the direct ion of the reaction. If the reaction is diverted to the fo rmat ion of G-6-P it can be t r ans formed to G-1-P and yield glycogen in the liver, or can be diverted to the pentose shunt . Based on specific activity, we suggest tha t PGI-A: would catalyse more efficiently the reaction to the fo rmat ion of glycogen. Similarly, the p redominance of less anodic zone in skeletal muscle, would suggest tha t the p roduc t of Pgi-B locus would be adapted to the glycolytic direction.

The present work shows that gene dupl icat ion for PGI in fishes commonly found in the l i terature, can be seen in diploid species. The presence of iso- zymes, as demons t ra ted for o ther ectotherms, and o ther proteins, seems to be a strategy of biochemical adap ta t ion to different envi ronments .

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