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  • .Aquaculture 197 2001 205228www.elsevier.nlrlocateraqua-online

    Genetic improvement of aquaculture finfish speciesby chromosome manipulation techniques in Japan

    Katsutoshi Arai)

    Laboratory of Breeding Science, Diision of Marine Biosciences, Graduate School of Fisheries Sciences,Hokkaido Uniersity, Hakodate, 041-8611, Japan

    Received 1 October 2000; accepted 31 December 2000

    Abstract

    The purpose of this review is to introduce recent advances in research, development andapplication of chromosome manipulation techniques in Japan. Triploids have been induced andutilized to improve growth. In most cases, triploids are produced as all-female populations byusing spermatozoa of artificially sex-reversed males, so as to assure their complete sterility. Incontrast, triploid males show better gonadal development and sometimes generate functionalspermatozoa, which give rise to inviable aneuploids in most species. Although induced tetraploidscan be useful for mass production of triploids by mating with normal diploids, tetraploid lineshave only been produced in rainbow trout by a few institutes belonging to prefectural govern-ments. In most cases, the techniques to inhibit the first cleavage often result in very low survival

    .and mosaicism. In the loach Cobitidae , polyploid lines such as hexaploids have been developedby using natural tetraploid individuals as an intermediate step. Cloned fish can be produced by thesecond cycle of gynogenesis in the eggs of completely homozygous diploids, which wereproduced by inhibiting first cleavage after induction of gynogenetic and androgenetic develop-ment. The second cycle of androgenesis, using spermatozoa of completely homozygous males, canalso generate clonal lines. The most serious technical problem of cloning is the extremely lowsurvival of homozygous gynogenetic and androgenetic diploids, probably due to the expression ofdeleterious recessive genes and side effect of treatments. However, cloned populations have beenrealized in commercially important ayu Plecoglossus altielis, amago salmon Oncorhynchus

    .masou ishikawae, coho salmon O. kisutch, hirame Japanese flounder Paralichthys oliaceus,fancy carp Cyprinus carpio, and red sea bream Pagrus major. In hirame, a practical method formass production of clones was proposed and better performance has been reported in a heterozy-

    ) Tel.: q81-138-40-5535; fax: q81-138-40-5537. .E-mail address: araikt@fish.hokudai.ac.jp K. Arai .

    0044-8486r01r$ - see front matter q2001 Elsevier Science B.V. All rights reserved. .PII: S0044-8486 01 00588-9

  • ( )K. ArairAquaculture 197 2001 205228206

    gous clone, produced by hybridization between two different homozygous clonal lines. Repeated .meiotic polar body gynogenesis may be more practical than cloning from homozygous gynogens

    as a method to generate isogenic lines. In meiotic gynogenesis, the proximal region of chromo-somes should be homozygous, whereas the distal region should be heterozygous due to high ratesof genecentromere recombination. Consequently, similar genotypes are predicted in the secondand later generations of gynogenetic progeny. Their isogenic nature has been confirmed byminisatellite, microsatellite, and other DNA analyses. Gynogenesis, androgenesis and cloning canbe used for elucidation of genetic sex determination. The involvement of environmental factorshas been indicated from the sex ratios of chromosomally manipulated populations of severalspecies. Finally, the regulation of chromosomally manipulated fish by the guidelines and theintegration of such techniques with molecular genetics for further gene mapping and transgenicsare discussed. q 2001 Elsevier Science B.V. All rights reserved.

    Keywords: Polyploid; Gynogenesis; Androgenesis; Clone; Sex determination

    1. Introduction

    There has been an explosive growth in both research and application of chromosomemanipulation techniques to various finfish species in the last 2 decades Hussain, 1996;

    .Arai, 1997a,b; Pandian and Koteeswaran, 1998 . In Japan, pioneering works concerningploidy manipulation and induction of unisexual development began in the late 1970s andearly 1980s in some universities and national institutes. The results were presented inannual meetings of the Japanese Society of Fisheries Science and were soon recognizedas a breakthrough for the rapid improvement of genetic traits of fish and shellfishspecies, in which conventional selection has been considered difficult due to their longlife cycle. Due to such backgrounds, research projects collectively referred to asAPromotion of Regional BiotechnologyB had been allotted to each prefectural govern-ment under the initiative of the Fisheries Agency of the Japanese Government since1984, so as to develop systematic techniques of chromosome manipulations for a fishspecies, which is especially important for the fisheries industry of each prefecture .Fisheries Agency, 1997 . Since 1991, such projects have been taken over by more

    .advanced ones in order to apply techniques directly to aquaculture Seki, 1999 . Fromthese projects as well as other activities, sterile triploids, all-female populations andclonal lines have been produced for several finfish species over the last 1.5 decades in

    .all areas of Japan Arai, 1997a,b; Seki, 1999 . Besides such practical research, pilotstudies on the production of higher polyploidies using natural tetraploidy as a stepping

    stone, as well as of clones using unreduced eggs, have been conducted Arai et al., 1993,.1995, 1999; Matsubara et al., 1995; Zhang and Arai, 1996; Arai and Mukaino, 1997 .

    The significance of meiotic gynogenesis has also been revalued as a more practical .method to fix desirable genotypes than cloning Arai, 1997a,b .

    In the present review, the current status of technologies and applications of chromo-some manipulations developed in Japan are outlined, and mention was made of theguidelines for use in manipulated fish, and the possible development of the technologyby integration with molecular techniques.

  • ( )K. ArairAquaculture 197 2001 205228 207

    2. Application of polyploid techniques for aquaculture

    2.1. Induction techniques and performances of triploid fish

    The most popular method of chromosome manipulation is the production of fish with .extra set s of chromosomes, i.e., polyploidy. In finfish, triploids can be easily induced

    .by blocking the second polar body release with high temperature heat , low temperature .cold , or high hydrostatic pressure shocks, just after fertilization with normal spermato-

    .zoa Fig. 1 . Chemical treatments using cytochalasin B and other kinds of agents are notpopular in triploidization of finfish. For practical induction, optimum treatment condi-

    .tions such as magnitude temperature or pressure level , duration, and timing, must bedetermined by trial and error approaches so as to yield 100% triploidy without seriouslydecreasing survival rates. Effective protocols have been developed for a large number of

    species in the last 2 decades as seen in several reviews Ueno, 1989; Hussain, 1996;.Arai, 1997a,b; Pandian and Koteeswaran, 1998 .

    In Japan, application-oriented studies of triploids are now in progress in about 26finfish and seven shellfish species by research organizations, such as AFisheries Experi-

    .mental StationB belonging to prefectural governments Fisheries Agency, 1997 . Espe-cially in rainbow trout, Oncorhynchus mykiss, biological characteristics and aquacultureperformances of induced triploids have been intensively studied for commercial applica-

    . tions in Hokkaido Okada, 1985 , Shiga Kobayashi, 1992, 1997; Kobayashi and. .Fushiki, 1997; Kobayashi et al., 1993, 1995, 1998a , Gifu Usuda, 1988 and other

    active prefectures. Similar approaches have been made in ayu, Plecoglossus altielis, in . .Fukuoka Inada, 1997 , Gifu Mori, 1990; Kuwada et al., 1992a,b , Wakayama

    .Tsujimura et al., 1991 and other active prefectures. According to these works, thepre-maturation growth of induced triploids is similar to that of diploids in separaterearing conditions, but is a little inferior to that of diploids in communal rearingconditions due to strong inter-individual competitions. However, during the period offinal maturation, there is a consensus that triploids show better growth, survival andmeat quality than diploids. Such advantages of induced triploids can be well explainedby the sterility expressed in females, which may reduce energy costs of reproduction. Incontrast, triploid males exhibit more gonadal development than females and showsecondary sex characters. Thus, males are semi-fertile and exhibit no improved growth.To assure better growth in induced triploids, all-female triploids have been produced in

    .rainbow trout by fertilization with sex-reversed physiological males neomales . Aneffective protocol of androgen treatment to masculinize genetic females has been

    .developed in rainbow trout Okada et al., 1979 . Similar procedures to produce andutilize all-female triploids for aquaculture were also developed in other salmonids.

    . .Current status of seed production individual number and aquaculture metric ton ofall-female triploid salmonids produced is shown in Table 1. In ayu, sex-reversedphysiological XX males and XX intersexes with both ovary and functional testis have

    .been experimentally produced by androgen treatments Tsujimura et al., 1991 . Thecommercial production of all-female triploid ayu is operated by Kanagawa Prefecture .Fisheries Agency, 1997; Hara, 1999 .

  • ( )K. ArairAquaculture 197 2001 205228208

    .Fig. 1. A schematic diagram of inducing polyploidy triploidy and tetraploidy and different types of gynogens.1PB: first polar body; 2PB: second polar body.

    In contrast to the

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