We have examined the developmental consequences for larval and imaginal segmental cuticular structure of a chromosomal translocation involving a breakpoint in the abdominal region of the bithorax complex (BX-C). This complex makes an essential contribution to the development of metameric differences in part of the thorax and in all abdominal segments. The breakpoint is proximal to the most distal (iab-7) homeobox, and results in the translocation to the Y chromosome of the Ultrabithorax (Ubx) and abdominal-A (abd-A) domains. The genotype deficient for the distal part of the complex shows normal function for Ubx and abd-A but has a phenotype typical for severe Abd-B mutations. Conversely, the distal fragment retains a segment identity function which must represent a contribution from Abd-B in parasegments 13 and 14; the latter metamere is wild type, indicating that it does not require the contribution of Ubx or abd-A.

We also constructed a genotype comprising the proximal fragment of this translocation together with an overlapping distal fragment of the BX-C derived from Df(3R)Ubx109. It therefore contained all sequences of the BX-C though in the abdominal region the abd-A and Abd-B domains were not adjacent to each other in the chromosome. This genotype was phenotypically normal and demonstrates that DNA sequences in the abd-A and Abd-B regions do not require cis-arrangement for their activity.

Differentiation of the unique array of metameres during Drosophila embryogenesis depends upon correct spatial expression of the antennapedia (ANT-C) and bithorax (BX-C) gene complexes (Kaufman, Lewis & Wakimoto, 1980; Lawrence & Morata, 1983; Lewis, 1978). The activation of these gene complexes begins at cellular blastoderm (Akam, 1983; Akam & Martinez-Arias, 1985) and is dependent upon positional cues established by the activities of the gap and pair-rule genes (for instance, see Ingham & Martinez-Arias, 1986; White & Lehmann, 1986) so that by the extended germ band stage there is clear evidence of spatial complexity in the accumulation of RNA transcripts (Akam, Martinez-Arias, Weinzierl & Wilde, 1985) and protein products from the ANT-C and BX-C, prior to the appearance of morphological differences between metameres. We shall here use the term parasegment (PS) (Martinez-Arias & Lawrence, 1985) to identify and describe metameric units.

Normal function of two copies of the BX-C is necessary to establish differences between ten parasegments (PS5 to PS14) in the embryo (Lawrence & Morata, 1983; Sanchez-Herrero, Vernos, Marco & Morata, 1985b; Morata, Sanchez-Herrero & Casanova, 1986). Beginning with the pioneering research of Lewis (1978), extensive genetic analysis has predicted the existence of considerable functional complexity within the BX-C. Complementation analysis and phenotypic descriptions of the cuticular changes produced by a large number of adult-viable dominant and recessive homoeotic mutations mapping to the BX-C (Lewis, 1982), together with the complementation map produced from zygotic recessive lethal mutations (Sanchez-Herrero et al. 1985; Tiong, Bone & Whittle, 1985; Sanchez-Herrero, Casanova, Kerridge & Morata, 1985a) and the behaviour of chromosomal deletions extending into this region (Morata, Botas, Kerridge & Struhl, 1983) suggest that a hierarchy of genetic functional units may exist within this complex. On the one hand, it has been suggested that the difference between each successive parasegment from PS5 to PS14 might reflect the function of an identifiable genetic unit with predominant activity in that metamere. Alternatively, each metamere or compartment may result from a unique combination of products from active units of the complex. The three lethal complementation groups of the BX-C (Ultrabithorax Ubx; abdominal-A, abd-A, and Abdominal-B Abd-B) (Sanchez-Herrero et al. 1985b;Tiong et al. 1985) offer insufficient combinations to specify nine parasegmental identities. The Ubx domain contains a hierarchy of genetic subfunctions and the effect of chromosomal rearrangements suggests that to function correctly the Ubx and bxd units must remain adjacent in cis arrangement (Lewis, 1978; Hogness et al. 1985). The Ubx domain can be separated by translocation from the abdominal region without phenotypic change (Struhl, 1984), but it remains unclear whether the chromosomal integrity of the abdominal domain is important for its function.

We have recovered a translocation breakpoint within Abdominal-B (Tp(3;Y)Abd-BS10) with which we have examined the effect upon embryonic and adult cuticular structures of translocation of the Ubx and abd-A regions to the Y chromosome. We conclude that the abdominal domains of the complex defined by embryonic lethal complementation analysis (abdominal-A and Abdominal-B) can contribute to a normal metameric pattern without requiring to be in cis-arrangement with each other.

The translocation T(3;Y) Abd-BS10 was recovered in the progeny of a multiple wing hairs stock, subjected to 45 Grays gamma-irradiation, as a male showing a weak Abdominal-B phenotype. Complementation tests with recessive lethal mutations mapping proximal to the BX-C (Tiong et al. 1985) place the proximal breakpoint of this translocation in cytogenetic region 89C, proximal to spineless-aristapedia, and this large fragment has become inserted into the Y chromosome. The distal breakpoint is within the abdominal region of the BX-C proximal to the iab-7 homeobox at 154 kb (Regulski et al. 1985); a 4·3 kb probe derived from an R1 fragment of the +154 kb to +158 kb region of the BX-C was found to hybridize to the third chromosome of polytene chromosomes from larvae of the genotype Df(3R)Abd-BS10/Df(3R)DfP115 (W. Bender, personal communication). Other Abdominal-B alleles used (designated B in this manuscript) were recovered in this laboratory following EMS or gamma-irradiation mutagenesis and detection in F2 screens against Df(3R)P115 (Tiong et al. 1985; Whittle, Tiong & Sunkel, 1986). The deletions Df(3R)Ubx109, Df(3R)P9 and Df(3R)P115 are described in Lewis (1978).

Embryonic cuticular preparations were made using the method of Van de Meer (1977) and were photographed in phase-contrast illumination using Kodak Technical Pan film. We have adopted the notation for caudal sense organs used by Jürgens (1987).

We first show that the rearrangement Tp(3;Y)Abd-BS10 can be classified as an Abdominal-B mutation genetically; then we report the use of the centromeric proximal fragment of this translocation (Ubx+abd-A+) together with an existing deletion (Ubxabd-A) to show that cis-arrangement of three lethal complementation groups is not required to produce a normal phenotype.

Classification of the translocation phenotype

Abdominal-B mutations have a domain of function within the region from parasegment 10 (PS10) to parasegment 14 (PS14) (Sanchez-Herrero et al. 1985; Tiong et al. 1985; Whittle et al. 1986) (Fig. 1). They map distally in the BX-C and the majority are recessive lethal mutations. We classify Abd-B mutations into four classes (I–IV) on the basis of their precise phenotypes. Class I Abdominal-B mutations allow normal development of the embryo and show only a very subtle transformation in sternite 6 in adult males; this usually bald sternite carries a small number of sternite bristles. The remaining classes all affect embryonic determination. The ventral cuticular phenotype of these mutants is compared with wild type in Fig. 2. Fig. 2A is from a wild-type first instar larva. The shape of the denticle belt (b) changes from trapezoid (PS12) to rectilinear (PS13). Posterior to PS13 are seven pairs of sense organs, the posterior spiracles (s), tuft (t), and anal plates (ap). The belt of PS 13 is separated posteriorly from the anal plates by a narrow bald area. The pair of sense organs DMSOp is surrounded by a patch of heavy dorsal spinules (dp) located at the base of the posterior spiracles. PS12 carries a prominent sensory structure known as the lateral hair. PS14 contains the posterior spiracles, dorsal spinule patch and sense organs. PLSOh, PLSOp, ALSOh, ALSOp, DMSOh and-DMSOp (Whittle et al. 1986). Fig. 2B is of a class II phenotype (BS12/D/BS10). Denticle belts of PS10-12 resemble that of PS9, but the belt of PS13 and all caudad structures are unaffected. Fig. 2C shows a class III phenotype (BS9/BX-C). Denticle belts of PS10–13 now resemble the belt of PS9 in being rectilinear. The posterior spiracles, dorsal spinule patch and sense organ ALSOp (and sometimes DMSOp) are absent. The denticle belt of PS13 is separated from the anal plates by an enlarged bald region (arrow in Fig. 2C). Fig. 2D shows the most extreme type, class IV, phenotype (BS1/BS4) that we have seen. PS10–13 possess a trapezoid denticle belt (and lateral hair) similar to that of PS9. In addition to the losses shown by class III animals, this group consistently lacks sense organs PLSOh, ALSOp, DMSOh and DMSOp (shown in their wild-type disposition in Fig. 2E) and sense organs PLSOp and ALSOh are grossly abnormal (Whittle et al. 1986). An enlarged bald area (arrow in Fig. 2D) posterior to the ventral denticle belt is juxtaposed by a pair of sclerotized plates (sc) as observed in embryos homozygous for a deletion of the BX-C, Df(3R)P9 (Fig. 3A). These are often associated with two lateral groups of fine denticles (the vestige of an extra denticle belt) (arrowhead in Fig. 2D). Dorsally, there is a supernumerary area of spinules posterior to the dorsal hairs of PS13 and distinct from the dorsal spinule patch now absent.

Fig. 1.

Domain of effect of Abdominal-B mutations that transform abdominal metameres. Beneath the array of parasegments forming the posterior abdomen (PS9–14) are shown the transformations found for each of the four phenotypic classes of Abdominal-B mutations, 1–IV. Only parasegments that show altered fates are drawn and their new identities are shown in the boxes. In class IV, PS14 has an identity unlike any wild-type metamere (see Fig. 2D).

Fig. 1.

Domain of effect of Abdominal-B mutations that transform abdominal metameres. Beneath the array of parasegments forming the posterior abdomen (PS9–14) are shown the transformations found for each of the four phenotypic classes of Abdominal-B mutations, 1–IV. Only parasegments that show altered fates are drawn and their new identities are shown in the boxes. In class IV, PS14 has an identity unlike any wild-type metamere (see Fig. 2D).

Fig. 2.

First instar larval cuticular phenotype of the posterior metameres of wild type and Abdominal-B mutants of classes I–IV. The ventral aspect of parasegments 12–14 are shown. (A-E) Wild-type embryos; (B) class II: denticle belt of PS12 is trapezoid but that of PS13 is wild-type; (C) class III: PS denticle belt is now trapezoid and no longer adjacent to the anal pads; (D) class IV: sclerotized plates appear posterior to the bald area caudad to PS13. ap, anal pad; b, ventral denticle belt; dp, dorsal spinules; sc, sclerotized cuticle; t, tuft of denticles. The sense organs (ASOh and p, PLSOh, PLSOp, ALSOh, ALSOp, DMSOh and DMSOp) are shown in their wild-type locations in E. Further details of these phenotypes are discussed in the text. Bar, 20 μm.

Fig. 2.

First instar larval cuticular phenotype of the posterior metameres of wild type and Abdominal-B mutants of classes I–IV. The ventral aspect of parasegments 12–14 are shown. (A-E) Wild-type embryos; (B) class II: denticle belt of PS12 is trapezoid but that of PS13 is wild-type; (C) class III: PS denticle belt is now trapezoid and no longer adjacent to the anal pads; (D) class IV: sclerotized plates appear posterior to the bald area caudad to PS13. ap, anal pad; b, ventral denticle belt; dp, dorsal spinules; sc, sclerotized cuticle; t, tuft of denticles. The sense organs (ASOh and p, PLSOh, PLSOp, ALSOh, ALSOp, DMSOh and DMSOp) are shown in their wild-type locations in E. Further details of these phenotypes are discussed in the text. Bar, 20 μm.

Fig. 3.

Ventral aspects of first instar larval cuticles of various bithorax complex deletion genotypes. (A) Df(3R)P9/Df(3R)P9, totally lacking BX-C functions: the denticle belts of PS12 and PS13 are small and fine, typical of thoracic belts. Sclerotized cuticle and a Keilin’s organ appear posterior to the belt of PS13. There are no posterior spiracles or dorsal spinule patch. (B) Dp Abd-BS10 Y/Df(3R)P9/Df(3R)P9. This phenotype is close to that of a class IV abdominal-B mutation (see Fig. 2D) but no extra denticles appear posterior to the belt of PS13. (C) Df(3R)Abd-BS10/Df(3R)P9. All seven sets of posterior sense organs and the posterior spiracles are present. Abbreviations are as in Fig. 2. Details of these phenotypes are discussed in the text. The lower frame of montage C is taken at a different focal plane to show terminal structures. Bar, 20 μm.

Fig. 3.

Ventral aspects of first instar larval cuticles of various bithorax complex deletion genotypes. (A) Df(3R)P9/Df(3R)P9, totally lacking BX-C functions: the denticle belts of PS12 and PS13 are small and fine, typical of thoracic belts. Sclerotized cuticle and a Keilin’s organ appear posterior to the belt of PS13. There are no posterior spiracles or dorsal spinule patch. (B) Dp Abd-BS10 Y/Df(3R)P9/Df(3R)P9. This phenotype is close to that of a class IV abdominal-B mutation (see Fig. 2D) but no extra denticles appear posterior to the belt of PS13. (C) Df(3R)Abd-BS10/Df(3R)P9. All seven sets of posterior sense organs and the posterior spiracles are present. Abbreviations are as in Fig. 2. Details of these phenotypes are discussed in the text. The lower frame of montage C is taken at a different focal plane to show terminal structures. Bar, 20 μm.

Our breakpoint in the BX-C does not behave as recessive-lethal. The two fragments of the transposition together (TpAbd-BS10) behave in outcrosses as a class II mutation; (Abd-B activity is lost in parasegments 10–12) and the combination is adult-viable with all our other Abd-B mutations except one (Abd-BS1). .

The deletion of the right-hand fragment has an extreme Abd-B phenotype (class IV) and it fails to complement the lethality of any lethal Abd-B allele. This is best shown by the genotype Dp Abd-BS10/Df P9/Df P9 in which the only portion of the BX-C present is a single copy of the fragment left of the breakpoint. It is embryonic-lethal and has an extreme transformation of PS10–14 (Fig. 3B), resembling a class IV Abd-B mutation (Fig. 2D), however, there is no evidence of an extra ventral denticle belt. Parasegments 5–9 are normal in this genotype, showing that the Ubx and abd-A regions function normally despite being inserted into the Y chromosome. The genotype possessing a single copy of both fragments of the translocation (TpAbd-BS10)/BX-C) ecloses as a male adult with transformations only of PS10, 11 and 12 corresponding to tergites 5, 6 and 7 and sternite 6.

The right-hand chromosomal fragment (Df3(R)-Abd-Bsw) which we are suggesting is Ubxabd-AAbd-B+, retains a genetic function in the BX-C despite failing to complement six of our lethal Abd-B alleles and only partially complementing three others. When this right-hand fragment is the sole component of the BX-C present, it produces an interesting embryonic-lethal phenotype (Fig. 3C) in that in PS13 and particularly in PS14, the metameric identity is clearly different from that of a total deletion of the BX-C (Fig. 3A); structures in PS14 that are lost when the BX-C is totally removed (BX-C/BX-C) persist when the distal region of the complex is retained (DfAbd-BS10/BX-C) and the abdominal belt of PS13 is not equivalent to that of an embryo lacking the BX-C. The denticle belt of this parasegment is closest to that of wild-type PS5. PS13 contains Keilin’s organs and sometimes sensory pits. A slightly enlarged bald region is found between the denticle belt and anal plates. There is no sclerotized cuticle. In contrast to total removal of the BX-C, this genotype does not affect structures of PS14; individuals possess posterior spiracles on a slanted protruberance, and the dorsal spinule patch and sense organs PLSOh, PLSOp, ALSOh, ALSOp, DMSOh and DMSOp are normal.

A bithorax complex genotype lacking cis arrangement of abd-A and Abd-B functions

The demonstration above that the centromeric proximal fragment TpAbd-Bsw carries a functional abdominal-A region allowed us to construct a genotype in which a functional Abdominal-B region did not lie in cis relationship to it. The genotype synthesized was DpAbd-BS10 (Ubx+abd-A+)Y; Df(3R) Ubx109/Df(3R) Ubx109 (Abd-B+), and it carried two copies of the abdominal region that is haplo-insufficient for imaginal cuticular structures (Fig. 4). This genotype eclosed as a wild-type male showing no transformation in pigmentation, trichome density or bristle distribution in tergites 4–6, no extra tergites or bristled sternites and did not differ phenotypically from sibs carrying a duplication of the BX-C in place of Df(3R)Ubx109 except that it displayed the Ubx phenotype in the halteres. These males had glazed eyes and ebony body colour, confirming that they were homozygous for the third chromosome glazed, ebony in which Df(3R)Ubx109 was originally induced.

Fig. 4.

Schematic genetic complementation and DNA maps of the BX-C to show the limits of the transposition Abd-BS10 and of the deletion Df(3R)Ubx109. The upper line indicates the sequence of the three lethal complementation groups Ubx, abd-A and Abd-B within the BX-C. The centromere is leftward in this diagram. The next three lines respectively show the deletion created by Df(3R)Abd-BS10 (Ubxabd-A) in the third chromosome, the Y-linked duplication Dp Abd-BS10 (Ubx+abd-A+) and the deletion Df(3R)Ubx109 (Ubxabd-AAbd-B+). The DNA map is shown below these, on which the locations of the three BX-C homeoboxes are indicated by H. The breakpoint of T(3;Y)/1M-SS10 is left of the iab-7 homeobox (see Materials and methods).

Fig. 4.

Schematic genetic complementation and DNA maps of the BX-C to show the limits of the transposition Abd-BS10 and of the deletion Df(3R)Ubx109. The upper line indicates the sequence of the three lethal complementation groups Ubx, abd-A and Abd-B within the BX-C. The centromere is leftward in this diagram. The next three lines respectively show the deletion created by Df(3R)Abd-BS10 (Ubxabd-A) in the third chromosome, the Y-linked duplication Dp Abd-BS10 (Ubx+abd-A+) and the deletion Df(3R)Ubx109 (Ubxabd-AAbd-B+). The DNA map is shown below these, on which the locations of the three BX-C homeoboxes are indicated by H. The breakpoint of T(3;Y)/1M-SS10 is left of the iab-7 homeobox (see Materials and methods).

We have examined the genetic behaviour of a translocation (TpAbd-BS10) having a breakpoint in the abdominal region of the BX-C (W. Bender, personal communication, see Materials and methods) left of the iab-7 homeobox (Karch et al. 1985; Regulski et al. 1985). The breakpoint itself is adult-viable when combined with a deletion of the BX-C but shows cuticular transformation in derivatives of parasegments 10–12, suggesting that the breakpoint has resulted in the inactivation of Abdominal-B activity in these parasegments, which could be explained as the result of uncoupling a cis-regulatory element in Abd-B proximal to the breakpoint acting upon transcription including that from the iab-7 homeobox region to the right of the breakpoint (Karch et al. 1985).

The distal chromosomal fragment of this translocation (Df(3R)Abd-BS10) nevertheless apparently still exerts an effect upon metameric identity within PS14 because the genotype Df(3R)Abd-BS10/Df(3R)P9 differs from Df(3R)P9/Df(3R)P9 in the cuticular structures formed in parasegment 14. In the former genotype, the absence of Ubx and abd-A function is evident in the cephalad transformation of PS6–13 (they resemble those of an embryo totally lacking the BX-C), but correct metameric identity is established in PS14 (Fig. 3C) in the total absence of Ubx and abd-A. This confirms the earlier observation of Tiong et al. (1985) that Abdominal-B mutations have a domain of effect that extends into PS14, and that neither mutations in Ubx or abd-A affect the identity of PS14.

The detailed relationships between the domain of effect of individual Abd-B mutations, their complementation behaviour and the underlying organization in the DNA remain enigmatic. The increasing involvement of more posterior metameres in the transformation of class IV mutations compared to class III and of class III to class II may relate to the correspondence between chromosomal location of mutations and the particular metameric units affected, a phenomenon first recognized by Lewis (1978) and which has been clearly illustrated by the DNA mapping of mutations within the abdominal region (Karch et al. 1985). A molecular explanation may be offered as for the Ubx region (Akam, Moore & Cox, 1984; Beachy, Helfand & Hogness, 1985), i.e. there might be a large initial proximally directed RNA transcript spanning the region of the most distal homeobox (iab-7), which may be spliced differentially within different groups of cells in the embryo so as to establish their separate metameric identity. However, the failure of either the proximal or distal fragment of Abd-Bsl° to complement the lethality of many Abd-B alleles cautions us against any simple explanation.

The correct identity of PS13 requires the sum of several gene activities, including those of Ubx and abd-A. When both fragments of Abd-BS10 are present PS13 is normal but in the genotype having only the distal fragment, PS 13 does not resemble that of a BX-C- embryo (Fig. 3C c.f. Fig. 3A). The phenotype in PS13 therefore represents the contribution of Abd-B function alone, deriving therefore from sequences distal to the breakpoint. Our conclusion reinforces evidence recently presented by Casanova, Sanchez-Herrero & Morata, (1986) from mutational analysis for a distinct distal function in Abd-B, which must lie distal to the breakpoint of Abd-BSi0.

We acknowledge the very helpful suggestions of Philip Ingham, unpublished information from Welcome Bender, the assistance of Jillion Davey and Colin Atherton in preparing this manuscript, the diligence of tjie referees, and the financial support of the Science and Engineering Research Council.

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