THE GENETIC FACTORS ALTERED IN HOMOZYGOUS. Manuscript received October 25, 1985 Revised copy accepted July 26, 1986
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1 Copyright by the Genetics Society of America THE GENETIC FACTORS ALTERED IN HOMOZYGOUS ABO STOCKS OF DROSOPHILA MELANOGASTER WILLIAM SULLIVAN' and SERGIO PIMPINELLI' Department of Genetics, University of Washington, Seattle, Washington Manuscript received October 25, 1985 Revised copy accepted July 26, 1986 ABSTRACT Females homozygous for the maternal-effect mutation abo (2-44.0) produce a large fraction of eggs which arrest during embryogenesis. Increasing doses of defined heterochromatic regions inherited by offspring of abo mothers from their fathers function zygotically to bring about a partial rescue of the aboinduced embryonic lethality. Another property of the abo mutation is that the severity of the maternal effect decreases when an abo stock is maintained in homozygous condition for a number of generations. Here, we show that the factors which change in homozygous abo stocks to result in the decrease in maternally induced embryonic lethality, act zygotically, dominantly and additively. More importantly, we show that the X and second chromosomes, but not the Y and third chromosomes, derived from homozygous abo stocks are, when inherited from males, more effective in promoting zygotic rescue of the aboinduced lethality than are the equivalent chromosomes derived from an abo stock maintained in heterozygous condition. The chromosomal locations of the factors altered in the homozygous stock, as well as their behavior, strongly suggest that the same heterochromatic elements that are responsible for rescuing embryos from the abo-induced maternal effect are altered in homozygous abo flies in such a way that the maternal effect itself is less severe. HE heterochromatic element, ABO, is defined by its interaction with the T euchromatic maternal-effect mutation abnormal-oocyte, abo (SANDLER 1970). Females homozygous for abo produce a large fraction of eggs which do not hatch. An increasing fraction of this abo-induced embryonic lethality is rescued by increasing doses of a specific heterochromatic factor, AB0 (PIMPI- NELLI et al. 1985). To date, AB0 heterochromatin has been mapped to small regions in the X centric heterochromatin, the Y, and also the centromeric heterochromatin of the right arm of the second chromosome (PARRY and SANDLER 1974; SANDLER 1977; YEDVOBNICK, KRIDER and LEVINE 1980; PIM- PINELLI et al. 1985). The heterochromatic rescue is most strikingly demonstrated by the altered sex ratio produced when homozygous abo females carrying two normal X chro- ' Present address: Department of Biochemistry and Biophysics, University of California, San Francisco. California * Present address: Dipartimento di Genetica e Biologia Molecolare, Citta Universitaria 00185, Roma, Italy. Genetics 114: November, 1986.
2 886 W. SULLIVAN AND S. PIMPINELLI mosomes are crossed to do+ males carrying YSX.YL,ln( I)EN,y B/O. Because the X and Y chromosomes in such males share a single centromere, they segregate together. Thus, the resulting progeny are XXY females and XO malesthe former having three doses of AB0 on its sex chromosomes and the latter only one. As a consequence, females survive the do-induced defect five- to tenfold better than do the males, skewing the sex ratio accordingly. Typically, the d o allele is maintained in heterozygous condition to reduce the chance of selecting for modifiers of the maternal effect. KRIDER and LEV- INE (1975) discovered that, if an abo stock is maintained in homozygous condition for a number of generations, homozygous abo females no longer produce the diagnostic skewed sex ratio in crosses to YSX.YL,In(l)EN, y B/O males. Concomitant with this normalization of the sex ratio, KRIDER and LEVINE also discovered that the rdna copy number becomes unstable. They interpreted this result, by analogy to the behavior of rdna under selection, to mean that AB0 heterochromatin was a repeated unit that could change copy number under appropriate conditions (KRIDER and LEVINE 1975). Here, we further characterize the genetic elements that are responsible for suppression of the abo maternally induced lethality in homozygous d o stocks. In particular, we analyze the effects of these factors produced in homozygous stocks but derived from males. This enables us to separate zygotic from maternal effects and, therefore, to map and to more directly relate the properties of these factors to those of the zygotically defined do-heterochromatic rescuing element. MATERIALS AND METHODS Progeny counts: The crosses were performed in shell vials on standard cornmealmolasses-agar medium at 25". Each vial consisted of either one male and two females or the reciprocal, depending on the sex of the genotype being examined. The parents were transferred to fresh vials on the fifth day of the cross and were discarded after five more days. All of the progeny that emerged before the 17th day after the parents had been placed in the bottle were scored. Adult survival values were determined by egg-to-adult counts. With mass matings, large quantities of eggs were collected for 4-5 hr; these were counted and transferred to fresh media in half-pint bottles. All flies emerging before day 17 were scored. Recovery and survival value calculations: In Tables 2 and 3, the survival of each sex is computed from the egg-to-adult counts using the following equation: E,C,/C,E,, where E, is the number of experimental adults of the sex being examined, C, is the number of control adults of the sex being examined, E, is the total number of experimental eggs and C, is the total number of control eggs. For the original description of this calculation, see SANDLER (1970). In Table 2, the homozygous stock does not have a control; therefore, the control from the heterozygous stock was used. In Tables 4 and 5, the recovery values of the X and second chromosomes from the homozygous and heterozygous stock were determined. The Sco male progeny in both sets of crosses share common sex and second chromosomes (see Figure 1). Therefore, this was used as a common reference class to determine the recovery values of the X and the second chromosomes from both sets of crosses. The equations used to determine the recovery values are shown below: X chromosome recovery Second chromosome recovery X and second chromosome recovery Esco??/E~codd X Cs,dd/Cs,?? E+dd/Es,,dd X C,,dd/C+dd E+??/Es,dd X Cs,,Sd/C+E
3 MODIFIERS OF HOMOZYGOUS AB0 STOCKS 887 In the text and Table 4, we describe an alternate method used to determine the recovery values of the X and second chromosomes. The equations for these determinations are shown below: X chromosome recovery Second chromosome recovery E+??/E+M X C+dd/C+oO E+99/Es,99 x CS,,99/C+9Q In Table 6, the recovery values of the Y and third chromosomes from the heterozygous and the homozygous stocks are determined. In these crosses, the Glued (GI) females share a common set of sex and third chromosomes in both sets of crosses. The equations used to calculate the recovery of the Y and third chromosomes are shown below: Y chromosome recovery E&/EGi$? X c&/cgdd Chromosome 3 recovery E+??/E& X c&/c+% Y and chromosome 3 recovery E+dd/E&Q X C&?/C+dd Statistical analysis: To determine whether the recovery values obtained in the homozygous and heterozygous sets of crosses were significantly different, we applied a statistical procedure known as the Mantel-Haenzel estimate of the odds ratio. From this estimate, we were able to obtain fitted or expected matrix values to which we could compare our observed values using x2 analysis. For a more complete discussion of this method, see BISHOP, FIENBERC and HOLLAND (1975). RESULTS The amelioration of the maternally induced abo lethality in a homozygous abo stock: abo is normally maintained in the heterozygous state using the second-chromosome balancer, ln(2lr)cy. The abo mutation is completely recessive (SANDLER 1970); thus, in the heterozygous condition there should be no selection for modifiers. In January, 1982, homozygous abo males and females were crossed, and the resulting homozygous stock has been maintained to the present. Therefore, when we initiated the present studies, the stock had been homozygous for abo for well over 30 generations. An increase in fertility of the homozygous stock over time indicated that the abo defect must have been at least partially suppressed. Interestingly, the increased fertility appeared to occur mainly in one or two generations, rather than gradually over many generations; that is, after a number of generations of very low fertility, the fertility of this homozygous stock suddenly increased, and, since then, has remained high. To confirm KRIDER S observations that the abo defect had in fact been alleviated, we crossed homozygous abo females to YSX.YL,ln(l)EN, y B/O males and recorded the sex ratio of the progeny. Table 1 shows that homozygous abo females from the stock that has been maintained in the heterozygous condition produced a male/female ratio of 0.36, whereas abo/cy females produced the control value of The excess of males in the control is expected because YSX.YL,ln(l )EN,y B/O;+/+ males will consistently lose a fraction of their attached-= chromosomes during spermiogenesis (SANDLER and BRAVER 1954; HARDY 1975). However, females from the homozygous stock produced a male/female ratio of Thus, it is clear that the strength of the abo maternally induced lethality, as measured by the disparity in the sex ratio of its progeny, is reduced in the stock maintained in the homozygous condition.
4 888 W. SULLIVAN AND S. PIMPINELLI
5 MODIFIERS OF HOMOZYGOUS AB0 STOCKS TABLE 2 Egg-to-adult counts demonstrating the partial suppression of the obo maternal effect in homozygous d o females derived from the d o stock maintained in the homozygous condition Origin of the female 889 Heterozygous stock Homozygous stock C E C E Total no. of eggs No. of females No. of males No. of exceptional F, Total survival Female survival Male survival Male/female ratio Sister females derived from the heterozygous stock, either heterozygous (C) or homozygous (E) for abo, and homozygous abo females derived from the homozygous stock were crossed to YSX.YL,In(I)EN, y B/O males. (See MATERIALS AND MJCTHODS for survival values.) KRIDER (1975) found in his homozygous ab0 stock that the sex ratio approximated that of the control values. Although we have never observed the skewed sex ratio to be completely eliminated, it is evident that the severity of the abo maternal defect is markedly reduced when the ab0 stock is maintained in the homozygous state. The progeny-per-mother values (also shown in Table 1) suggest that the change in the sex ratio of the progeny from ab0 mothers derived from the homozygous ab0 stock is the result of an increase in the survival of XO males. As shown in Table 2, egg-to-adult counts confirm this result. These data demonstrate that eggs of ab0 mothers derived from the homozygous stock survive better than those originating from the heterozygous stock (0.31 compared to 0.23; x2 = 10.12; d.f. = 1; P < 0.05). In confirmation of the progeny-permother values, these egg-count data also show that the increase in overall survival is solely the result of an increase in the survival of the males. Chromosomes from the homozygous stock rescue the abo maternally induced lethality better than do chromosomes from the stock maintained in the heterozygous condition: To determine whether there is a zygotic component to the reduction of the ah-induced lethality. Homozygous ab0 males derived from either the homozygous or the heterozygous stock were mated to females from the heterozygous stock, and eggs and adults were scored. As the data from Table 3 show, chromosomes from males from the homozygous stock are more effective at rescuing the abo maternally induced lethality than are those from males from the heterozygous stock (20% VS. 7%; x2 = 60.4; d.f. = 1; P < 0.05). These results demonstrate that the factors which are responsible for the amelioration of the ab0 maternal effect in homozygous abo stocks are capable of acting zygotically and dominantly. It should be noted that the lower survival values recorded in Table 3 com-
6 890 W. SULLIVAN AND S. PIMPINELLI TABLE 3 Egg-to-adult counts demonstrating the increased rescue of the abo maternal effect by chromosomes derived from the abo stock maintained in the homozygous condition relative to those derived from the abo stock maintained in the heterozygous condition Paternal genotype XIY; abolabo (derived from the homozygous stock) XIY; abolabo (derived from the heterozygous stock) C E C E Total no. of eggs No. of females No. of males Total survival Female survival male survival Sister females, from the abo stock maintained in the heterozygous condition, either heterozygous (C) or homozygous (E) for abo were crossed to homozygous abo males from either the stock maintained in the heterozygous or the stock in the homozygous condition. (See MATERIALS AND METHODS for calculation of survival values). X/X abolabo X X/Y; Sco/Cy 4 X/X; abolabo X/F abo/sco X X/X abo/cy X*/X*; abo*/abo* X X/Y; ScolCy.1 X/X abolabo X*/V; abo*/sco X XIX; abo/cy FIGURE 1.-The mating scheme used to compare the ability of paternally inherited X and second chromosomes from the homozygous and heterozygous stocks to rescue the maternal aboinduced lethality. The chromosomes marked with an asterisk identify those derived from the homozygous stock. The tester males were crossed to heterozygous and homozygous abo females derived from the heterozygous abo stock. pared with those in Table 2 result because the zygotes in the latter experiments were do+, whereas those in Table 3 were abo. The normal allele of abo also rescues the abo-induced maternal effect (PIMPINELLI et al. 1985). Factors on both the X chromosome and chromosome 2 are responsible for the amelioration of the abo defect in the homozygous stock: To determine which chromosomes in the homozygous stock are responsible for the increased rescue, females from both the homozygous and the heterozygous stocks were outcrossed to a common, Sco/Cy, stock. Sco male offspring were collected from both crosses and were mated to both homozygous and heterozygous abo females from the heterozygous stock. This crossing scheme, diagrammed in Figure 1, allows us to compare independently the recovery values of the X and second chromosomes derived from the homozygous and the heterozygous stocks. The recovery values, calculated relative to the common Sco male genotype, reflect the relative ability of these chromosomes to rescue the abo maternal effect. Because the Sco males derived from both the heterozygous and
7 MODIFIERS OF HOMOZYGOUS AB0 STOCKS TABLE 4 The results of crosses which assay X and second chromosome abo rescuing ability derived from stocks maintained in homozygous and heterozygous condition Phenotype of the progeny Recovery values Stock from which the X and second chromosomes of the X and secmale parent originated +Pp ScoPp +6d ScdS ond X Second C Heterozygous abo stock E (1.33) (0.44) C Homozygous abo stock E (1.64) (0.61) Females derived from heterozygous stock, either heterozygous (C) or homozygous (E) for abo, were crossed to males possessing the X and second chromosomes from the abo stocks maintained in either the heterozygous or the homozygous state. (See Figure 1 for crossing scheme and the text for calculations.) the homozygous set of crosses carry an identical set of sex and second chromosomes, they provide a common genotype between the homozygous and the heterozygous sets of crosses so that the recovery values, reflecting absolute survival values between the sets, may be directly compared. In Table 4, the progeny counts and recovery values from these crosses are shown. The X chromosome from the heterozygous stock has a recovery value of 1.26, whereas the X chromosome from the homozygous stock has a recovery value of This difference is significant at the 0.05 level (x2 = 5.2; d.f. = 1). This demonstrates that the X chromosome derived from the homozygous stock has an increased ability, relative to the X chromosome derived from a heterozygous stock, to rescue the abo maternal effect. Notice that we are calculating the recovery values of paternally introduced chromosomes into aboderived eggs. This is exactly the same procedure used to operationally define and map AB0 (PIMPINELLI et al. 1985). These data also show that the second chromosome derived from the homozygous stock is more effective at rescuing the abo maternal-effect defect than is the second chromosome derived from the heterozygous abo stock (x2 = 9.3; d.f. = 1; P < 0.05). The data also indicate that the X and second chromosomes derived from the homozygous stock produce a greater effect together than either would alone (x2 = 31.4; d.f. = 1; P < 0.05). To ask whether the elements on the X and second chromosomes were acting in an additive fashion, we calculated the recovery of the X and second chromosomes together compared to chromosome 2 alone. This should provide a value for the recovery value of the X alone if the X and second chromosomes act in an additive fashion and not synergistically. As shown by the values in parenthesis in Table 4, the recovery values of the X calculated by these two independent methods are not different E1.26 and 1.33 for the heterozygous stock (x2 = 0.34; d.f. = 1; P > 0.05) and 1.51 and 1.64 for the homozygous stock (x2 = 1.01, d.f. = 1, P > 0.05)]. This also obtains for the second- 89 1
8 892 W. SULLIVAN AND S. PIMPINELLI TABLE 5 The results of crosses which assay the X and second chromosome abo rescuing ability derived from stocks maintained in homozygous and heterozygous condition Phenotype of the progeny Recovery values Stocks from which the X and second chromosomes of X and the male parent originated +E SCOOP +88 ScoSd second X Second C Heterozygous abo stock E C Homozygous abo stock E Females derived from a heterozygous abo stock with a marked and unrelated set of X chromosomes, either heterozygous (C) or homozygous (E) for abo, were crossed to males possessing the X and second chromosomes from the abo stocks maintained in either the heterozygous or the homozygous state. chromosome recovery values; the differences are not significant at the 0.05 level. These identities are especially striking because the two methods of calculating the recovery values use different, and independent, sets of values. The simplest explanation for these results is that the X and second chromosomes act in an additive fashion to rescue the abo maternal-effect defect. A discrepancy exists between the values obtained here and those reported previously. Typically, X-recovery values are around 2; yet here, values of 1.5 and 1.3 were obtained. The possibility existed that the reduced recovery may have been produced by deleterious factors, not part of the abo system, that had become homozygous. Further, the difference in recovery between the X chromosomes derived from the homozygous and the heterozygous stock might itself have been the consequence of homozygosis of many more recessive deleterious factors in the latter than in the former stock. To examine this possibility, we repeated the experiment, but used abo females bearing an unrelated set of X chromosomes. As shown in Table 5, in this set of crosses, female recoveries are greater than 2.0. However, the X and second chromosome from the homozygous stock rescued the abo defect better than did the X and second chromosomes derived from the heterozygous stock. Therefore, the low female recovery values found in the first set of crosses were most likely the result of recessive deleterious factors. However, regardless of the cause, the effect is indiscriminant and acts equivalently in progeny derived from fathers originating from the homozygous and heterozygous abo stocks. Thus, in spite of this reduced recovery, we are still able to reliably measure the relative differences in the ability of chromosomes derived from the homozygous and the heterozygous stock to rescue the abo-induced defect. There are no factors on the Y or the third chromosome responsible for the differences in the amelioration of the abo defect in the homozygous, compared to the heterozygous, stock: In a set of experiments analogous to those described above, we measured the abo rescuing activity of the Y and
9 MODIFIERS OF HOMOZYGOUS AB0 STOCKS X/X +/+; DIG1 X X/Y; abolabo; +/+.1 X/X abolabo X/Y; abo/+; GI/+ X X/X abolcy X/X +/+; DIG1 X X*/Y*; abo*/abo*; +*/+* 3- X/Y*; abo*l+; G1/+* X XIX abolabo X/X abolcy FIGURE 2.-The mating scheme used to compare the ability of paternally inherited Y and third chromosomes from the homozygous and heterozygous stocks to rescue the maternal abo-induced lethality. The chromosomes marked with an asterisk identify those derived from the homozygous stock. The tester males were crossed to heterozygous and homozygous abo females derived from the heterozygous abo stock. TABLE 6 The results of crosses which assay Y and third chromosome abo rescuing ability derived from stocks maintained in homozygous and heterozygous condition Phenotype of the progeny Recovery values Stock from which the Y and third chromosomes of the Y and male parent originated +# GlOP +M G166 third Y Third C Heterozygous abo stock E C Homozygous abo stock E Females derived from a heterozygous abo stock, either heterozygous (C) or homozygous (E) for abo, were crossed to males carrying the Y and third chromosomes from abo stocks maintained in either the heterozygous or the homozygous state. In these crosses, the Glued (GI) females share a common set of sex and third chromosomes in both sets of crosses. (See MATERIALS AND METHODS for calculation of recovery of the Y and third chromosomes.) third chromosomes derived from both the homozygous and the heterozygous stocks. To this end, we outcrossed abo males from both the homozygous and the heterozygous stocks to females bearing the dominant third-chromosome marker Glued (Gl). In this case, flies derived from the homozygous and heterozygous lines share common X and third chromosomes (see Figure 2). The results in Table 6, show that the Y from the homozygous stock has not increased its abo rescuing activity relative to the Y from the heterozygous stock (x2 = 1.26; d.f. = 1; P > 0.05). In addition, the third chromosome from the homozygous stock is not significantly better in rescuing the abo maternal defect relative to the third chromosome from the heterozygous stock (x2 = 0.48; d.f. = 1; P > 0.05). DISCUSSION In a series of studies, KRIDER and colleagues (KRIDER and LEVINE 1975; KRIDER, YEDVOBNICK and LEVINE 1979; YEDVOBNICK, KRIDER and LEVINE 1980) demonstrated that when an abo stock is maintained in homozygous con- 893
10 894 W. SULLIVAN AND S. PIMPINELLI dition for a number of generations, the abo maternally induced lethality is reduced. By analogy with the changes in copy number observed in rdna under magnifying and compensating conditions, and because in homozygous abo individuals rdna copy number becomes unstable, the reduction in the severity of the abo-induced maternal-effect lethality in homozygous abo stocks was interpreted as a copy-number change in an abo-responsive heterochromatic factor. The data presented here examine the ability of the factors altered in the homozygous stock to rescue the abo maternally induced lethality when those factors are paternally inherited. This analysis enables us to examine the zygotic effects of the elements separately from their maternal effects. Thus, we could determine the chromosomes involved and directly compare the properties of these factors to those of the abo-responsive heterochromatic factors (ABO) which have been defined and mapped based on their paternal rescue of the abo maternally induced lethality. The results support the notion that the genetic factors altered in the homozygous stock responsible for the reduced lethality are the abo-responsive heterochromatic rescuing regions. They demonstrate that, like these heterochromatically mapped AB0 regions, the rescuing factors found in the homozygous abo stock act zygotically and dominantly. In addition, the factors map to the X and second chromosomes of the homozygous stock, as do the heterochromatically located abo-responsive elements. The increased rescue by the paternally derived second chromosome from the homozygous abo stock, in addition, genetically supports the molecular findings (YEDVOBNICK, KRIDER and LEVINE 1980) and cytological observations (PIMPINELLI et al. 1985) demonstrating that the factors responsible for rescue do not map to the rdna. The suggestion by KRIDER and LEVINE (1975) that it may be the increased replication of these heterochromatic abo-responding regions that is responsible for the reduced lethality in homozygous abo stocks also finds support in that the increased rescue by the X and second chromosomes derived from a homozygous stock act additively together. Such a result is expected if the degree of rescue is dependent primarily on the copy number of the rescuing elements. A final point to note is that, if this analysis has been correctly interpreted, then the Y-chromosome AB0 elements do not change copy number in homozygous abo stocks. Whether this is because Y-chromosome repeated elements in general do not increase or decrease copy number, or whether it is because these AB0 changes occur only in females, is not clear. We are grateful to RICK CARBER, KENT COLIC, GARY KARPEN, JOHN TOMKIEL, GLENN YASUDA, BARBARA WAKIMOTO and especially LARRY SANDLER for their helpful advice and critical reading of the manuscript. SERCIO PIMPINELLI was supported by a Fogarty International Fellowship during the academic year at the University of Washington. WILLIAM SULLIVAN was supported by a National Institutes of Health genetics training grant. The work was supported by National Institutes of Health grant RG LITERATURE CITED BISHOP, Y. M. M., S. E. FIENBERC and P. W. HOLLAND, 1975 Discrete Multivariate Analysis Theory and Practice. MIT Press, Cambridge, Massachusetts.
11 MODIFIERS OF HOMOZYGOUS AB0 STOCKS 895 CARPENTER, A. T. C. and L. SANDLER, 1974 On recombinationdefective meiotic mutants in Drosophila melanogaster. Genetics 76: HARDY, R. W., 1975 The influence of chromosome content on the size and shape of sperm heads in Drosophila melanoguster and the demonstration of chromosome loss during spermiogenesis. Genetics KRIDER, H. M. and B. I. LEVINE, 1975 Studies on the mutation abnormal oocyte and its interaction with the ribosomal DNA of Drosophila melanoguster. Genetics 81: KRIDER, H. M., B. YEDVOBNICK and B. I. LEVINE, 1979 The effect of ubo phenotypic expression on ribosomal DNA instabilities in Drosophila melanogaster. Genetics PARRY, D. M. and L. SANDLER, 1974 The genetic identification of a heterochromatic segment in the X chromosome of Drosophila melunogaster. Genetics 77: PIMPINELLI, S., W. SULLIVAN, M. PROUT and L. SANDLER, 1985 On biological functions mapping to the heterochromatin of Drosophila melunogaster. Genetics SANDLER, L., 1970 The regulation of sex-chromosome heterochromatic activity by an autosomal gene in Drosophila melanoguster. Genetics 64: SANDLER, L., 1975 Studies on the genetic control of heterochromatin in Drosophila melanogaster. Isr. J. Med. Sci. 11: SANDLER, L., 1977 Evidence for a set of closely linked autosomal genes that interact with sex chromosome heterochromatin in Drosophila melanogaster. Genetics SANDLER, L. and G. BRAVER, 1954 The meiotic loss of unpaired chromosomes in Drosophila melanogaster. Genetics 39: WRIGHT, T. R. F., 1970 The genetics of embryogenesis in Drosophila. Adv. Genet YEDVOBNICK, B., H. M. KRIDER and B. I. LEVINE, 1980 Analysis of the autosomal mutation abo and its interaction with the ribosomal DNA of Drosophila melunoguster: the role of X-chromosome heterochromatin. Genetics Communicating editor: A. CHOVNICK
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