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Induction of Mitochondrial DNA Heteroplasmy by Intra- and Interspecific Transplantation of Germ Plasm in Drosophila

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Induction of Mitochondrial DNA Heteroplasmy by Intra- and Interspecific Transplantation of Germ Plasm in Drosophila Copyright 0 1989 by the Genetics Society of America Induction of Mitochondrial DNA Heteroplasmy by Intra- and Interspecific Transplantation of Germ Plasm in Drosophila Etsuko T. Matsuura,* SadaoI. Chigusa* and Yuzo Niki? *Department of Biology, Ochanomiru University, 2-1-1 Otsuka, Bunkyo-ku, Tokyo 112, Japanand tDepartment $Biology, Ibaraki University, 2-1-1 Bunkyo, Mito-shi, Ibaraki 310, Japan Manuscript received January 17, 1989 Accepted for publication April 3, 1989 ABSTRACT A new experimental system for inducing mitochondrial DNA heteroplasmy in Drosophila was developed. By transplanting the germ plasm of Drosophila melanogaster and Drosophila mauritiana into the posterior pole of the recipient eggs of D. melanogaster, it was possible to introduce foreign mitochondria into the recipient female germline. Heteroplasmic individuals containing both donor and recipient mtDNA were obtained in intra- and interspecific combinations at similar frequencies. The proportion of donor-derived mtDNA in the heteroplasmic individuals varied considerably from individual to individual irrespectiveof the donor species used. No significant decreasein or elimination of donor mtDNA was observed, andthe heteroplasmic statein female germlines persisted for several generations. The present system should serve very much to promote the study and clarification of the transmission gkneticsof mtDNA in insects. HE geneticsof metazoan mitochondrial DNA germ plasm. The germline ofDrosophila is segregated T (mtDNA) is unique in that apopulation of fromother somatic lines at very earlyembryonic mtDNA molecules is maternallyinherited. Lack of stages through thefunction of germ plasm (ILLMENSEE appropriate genetic markers of mitochondria within and MAHOWALD1974; NIKI 1986). Germ plasm is not an individual makes difficult elucidation of the man- species-specific for inducingfunctional germ cells ner in which mitochondria or mtDNA are transmit- (MAHOWALD,ILLMENSEE and TURNER1976) andcon- ted. Recently,heteroplasmic individuals carrying tains mitochondria in abundance (MAHOWALD 1962). more than one type of mtDNA have been found in Thus, transplanting germ plasm into an egg carrying naturalpopulations. In most cases, heteroplasmy is a different typeof mtDNA shouldgenerate germcells based on size variation, possibly owing to high rates possessing two types of mtDNA inthe cytoplasm pro- of small deletions or additions in mtDNA (SOLIGNAC, vided mitochondria in the donor germ plasm survive MONNEROT and MOUNOLOU1983; MONNEROT, and are successfully transmitted to the next genera- MOUNOLOUand SOLICNAC1984; DENSMORE,WRIGHT tion. Both intra-and interspecifictransplantations and BROWN1985; HARRISON, RAND and WHEELER were carried out in the melanogaster species subgroup, 1985; HAUSWIRTHand CLAYTON 1985; BER- D. melanogaster and D. mauritiana, using D. melano- MINGHAM, LAMB andAVISE 1986; HALEand SINGH gaster as the recipient in each case. Heteroplasmic 1986; WALLIS1987). Heteroplasmy in restriction site individuals were obtained in significant number from variation due to base substitution has been also ob- both intra- andinterspecific transplantations, and do- served (HALE andSINGH 1986). A study ofthe trans- nor mtDNA was retained for several generations. mission of the heteroplasmic state in maternal lineage has beenconducted on the Holstein cows (HAUS- MATERIALS AND METHODS WIRTH and LAIPIS1982), D. mauritiana (SOLIGNAC et Culture and stocks: All Drosophila stocks were cultured al. 1984), and Gryllus jirmus (RAND and HARRISON on standard Drosophila medium at 19’. As the recipient of 1986). SATTAet al. (1988) reported another type of germ-plasm transplantation, bw;e” of D. melanogaster was heteroplasmy in D. simulans, which sharesone used, with the isofemale lines D.of melanogaster (HJ6, Japan) mtDNA type with that found in mauritiana and and D. mauritiana (g20, Mauritius), established from single D. females of wild populations, servingas germ-plasm donors. consider this to stem from “old polymorphism” in an g20 stock was kindlyprovided by Dr. 0. Kitagawa. mtDNAs ancestral population of these twosibling species. This of bw;e”, HJ6 and g20 showed differentHaelII restriction discovery, however, may provide a basis for studying patterns (Figure I), and thus could be easily distinguished. mitochondria transmission in foreign species and spe- Transplantation of germ plasm and establishmentof a Kfounder”female: The germ plasm recipient embryos cies-specific functions of mitochondria. of (bw;e”) was sucked out so that donor germ plasm could be The presentstudy was undertakento induce efficiently incorporated into pole cells. The donor germ mtDNA heteroplasmy in Drosophila by transplanting plasm was transplanted intothe posterior poles of recipient Genetics 122 663-667 (July, 1989) 664 E. T. Matsuura, S. I. Chigusa and Y.Niki this measurement to estimate the proportion of g20 mtDNA. In each gel lane, the relative number of DNA HJ6 C ID1 B 1 molecules in each band could be estimated by dividing the 9 20 A I B 1 amount of DNA in the band, measured as peak area, by its molecular weight. At higher intensity, however, the amount I4 I I ,l,,,,l,,,,l,,,J of DNA in the band detected on negative film and the 0 5 10 15 19 Kb number of DNA molecules did not show a linear relation- ship. The relative number of DNA molecules in each band was thus estimated from the calibration curve constructed. One percent of donor mtDNA was clearlyshown to be present on the gel, as determined from mtDNA extracted Kb from 50 to 100 flies (data not shown). 23.1 9.4 6.6 RESULTS 4.4 Construction of “founder” females by germ-plasm 2.3 2.0 transplantation: The germ plasm of freshly laid eggs of donor flies was transplanted into 300 to 400 bw;e” recipienteggs, and the results are summarized in 0.6 Table 1. The adult flies developedconstituted less than 10% the total eggs injected. Among them, ten R .:. Iriisa, females from the transplantation of HJ6 (D.melano- gaster) germ plasm and 1 1 from that of g20 (D. maur- FIGURE I.-Linearized Hue111 restriction maps of mtDNA of werefertile. These “founder” females were bw;e’l, HJ6 and g20 strains and their restriction patterns. Capital itiana) letters show relative fragment size in decreasing order. Proportions individually crossed to bw;e” males, and the emerged of donor mtDNA were calculated using the “B” fragments of bw;e” progeny (Go)in all cases showed thebw;e” phenotype. and H.16 or the “A” fragments of 6w;e” and g20. At the left-most Thus, no donor nuclei were contaminated at the time lane of the gel, lambda phage DNA digested with Hind111 is shown of injection. Out of 21 fertile females, 18 (nine for 21s the size marker. HJ6 and nine for g20) produced sufficient numbers embryos through the same site from which recipient cyto- of progeny (Go) for mtDNA analysis. plasm had previously been sucked out. The embryos were Heteroplasmic nature of GO flies: To examine immersed in FL 100 oil and observed with an inverted phase contrast optic, IMT2 (Olympus, Tokyo) to avoidco- whether donor mitochondria were incorporated into transplantation of donor nuclei. Their development pro- the germline cells of recipients and transmitted into ceeded to adulthood as already described (NIKI 1986). The theirprogeny, we firstanalyzed mtDNAextracted adult female flies thus obtained (designated as “founder” from about 50 to 100 Go flies from each of the 18 females) were individually crossed to bw;e” males, and the “founder” females. Based on their HaeIII restriction phenotype of their progeny was examined to confirm co- transplantation of donor nuclei. patterns,both donor and recipient mtDNA were Establishment of heteroplasmic lines: To assess the cy- shown to be present in mtDNA samples from more toplasmic state of the germline cellsof each “founder” than half the “founder” females, six out of nine for female, mtDNA was extracted from 50 to 100 flies of the donor HJ6 and five out of nine for donor g20 (data progeny (GO)from the cross of a “founder” female to bw;e” not shown). As for the cytoplasmic nature of the GO males and Hue111 restriction patterns of mtDNA were ex- amined. When there were two types of mtDNA in mtDNA flies fromthe “founder” females,two possibilities samplesfrom the Go progeny, isofemalelines could be should be considered. First, a “founder” female may established from individual Go females. Mitochondrial types have its donor- and recipient-derived mitochondria ofindividual GO femaleswere then determined from segregated into different germcells. The coexistence mtDNA extracted from 50 to 100 GI flies. The parental of these two types of mtDNA in the progeny would female (GO)was considered heteroplasmic if both recipient- and donor-derived mtDNA were present. The isofemale thus be due to the factthat two types of mtDNA lines weremaintained at 19” by brother-sister matings, using derive fromdifferent individual flies. As asecond more than 50 flies. possibility, the germ cells of a “founder” female may Analysis of mtDNA: mtDNA was usually extracted from be heteroplasmic and both donor- and recipient-de- the purified mitochondria of 50 to 100 flies as already rivedmitochondria coexist in eachgerm cell. The described (SATTAet ul. 1988), using the homogenizing buffer of TAMURAand AOTSUKA(1 988). mtDNA digested latter situation should be regarded as heteroplasmy. with Hue111 restriction enzyme was separated on 0.8% aga- To determine thecytoplasmic nature ofGo individ- rose gel. After being stained with ethidium bromide, the gel uals,isofemale lines were established from the Go was photographed under UV light. Each lane on negative progeny as described above. We randomly chose 16 film of the gels was scanned with a densitometer. To esti- and 27 isofemale lines for donors HJ6 and g20, re- mate the proportion of HJ6 mtDNA, intensities of the “B” fragments of bw;e” and HJ6 of each lane were measured. spectively, and analyzed mtDNA extracted from their The “B” fragment of g20 comigrated with that of bw;e”, progeny (GI). Examples of the Hue111 restriction pat- and thus the “A” fragments of bw;e” and g20 were used for terns of some isofemale lines are shown in Figure 2.
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