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1.
Chromosome Res ; 13(5): 443-53, 2005.
Article in English | MEDLINE | ID: mdl-16132810

ABSTRACT

Telomeres across the genus Drosophila are maintained, not by telomerase, but by two non-LTR retrotransposons, HeT-A and TART, that transpose specifically to chromosome ends. Successive transpositions result in long head-to-tail arrays of these elements. Thus Drosophila telomeres, like those produced by telomerase, consist of repeated sequences reverse transcribed from RNA templates. The Drosophila repeats, complete and 5'-truncated copies of HeT-A and TART, are more complex than telomerase repeats; nevertheless, these evolutionary variants have functional similarities to the more common telomeres. Like other telomeres, the Drosophila arrays are dynamic, fluctuating around an average length that can be changed by changes in the genetic background. Several proteins that interact with telomeres in other species have been found to have homologues that interact with Drosophila telomeres. Although they have hallmarks of non-LTR retrotransposons, HeT-A and TART appear to have a special relationship to Drosophila. Their Gag proteins are efficiently transported into diploid nuclei where HeT-A Gag recruits TART Gag to chromosome ends. Gags of other non-LTR elements remain predominantly in the cytoplasm. These studies provide intriguing evolutionary links between telomeres and retrotransposable elements.


Subject(s)
Drosophila/genetics , Retroelements/genetics , Telomere/genetics , Animals , Cell Nucleus/genetics , Chromosomes/genetics , Drosophila Proteins/genetics , Drosophila Proteins/metabolism , Evolution, Molecular , Gene Products, gag/genetics , Gene Products, gag/metabolism , Green Fluorescent Proteins/genetics , Green Fluorescent Proteins/metabolism , Microscopy, Fluorescence , Protein Structure, Tertiary/genetics , Recombinant Fusion Proteins/genetics , Recombinant Fusion Proteins/metabolism , Retroelements/physiology , Telomere/metabolism
2.
Cytogenet Genome Res ; 110(1-4): 152-9, 2005.
Article in English | MEDLINE | ID: mdl-16093667

ABSTRACT

Drosophila telomeres have been maintained by retrotransposition for at least 60 MY, which predates the separation of extant species of this genus. Studies of D. melanogaster, D. yakuba, and D. virilis show that, in Drosophila, telomeres are composed of two non-LTR retrotransposons, HeT-A and TART. Far from being static, HeT-A and TART evolve faster than Drosophila euchromatic genes. In spite of their high rate of sequence change, HeT-A and TART maintain their basic structures and unusual individual features. The maintenance of their separate identities suggests that HeT-A and TART cooperate either in the process of retrotransposition onto the chromosome end, or in the formation of telomere chromatin by transposed DNA copies. The telomeric retrotransposons and the Drosophila genome constitute an example of a robust symbiotic relationship between mobile elements and the genome.


Subject(s)
Chromosome Mapping , Drosophila/genetics , Evolution, Molecular , Retroelements , Animals , Base Sequence , DNA/chemistry , DNA/genetics , Molecular Sequence Data
3.
J Virol ; 77(11): 6376-84, 2003 Jun.
Article in English | MEDLINE | ID: mdl-12743295

ABSTRACT

Drosophila has two non-long-terminal-repeat (non-LTR) retrotransposons that are unique because they have a defined role in chromosome maintenance. These elements, HeT-A and TART, extend chromosome ends by successive transpositions, producing long arrays of head-to-tail repeat sequences. These arrays appear to be analogous to the arrays produced by telomerase on chromosomes of other organisms. While other non-LTR retrotransposons transpose to many chromosomal sites, HeT-A and TART transpose only to chromosome ends. Although HeT-A and TART belong to different subfamilies of non-LTR retrotransposons, they encode very similar Gag proteins, which suggests that Gag proteins are involved in their unique transposition targeting. We have recently shown that both Gags localize efficiently to nuclei where HeT-A Gag forms structures associated with telomeres. TART Gag does not associate with telomeres unless HeT-A Gag is present, suggesting a symbiotic relationship in which HeT-A Gag provides telomeric targeting. We now report studies to identify amino acid regions responsible for different aspects of the intracellular targeting of these proteins. Green fluorescent protein-tagged deletion derivatives were expressed in cultured Drosophila cells. The intracellular localization of these proteins shows the following. (i) Several regions that direct subcellular localizations or cluster formation are found in both Gags and are located in equivalent regions of the two proteins. (ii) Regions important for telomere association are present only in HeT-A Gag. These are present at several places in the protein, are not redundant, and cannot be complemented in trans. (iii) Regions containing zinc knuckle and major homology region motifs, characteristic of retroviral Gags, are involved in protein-protein interactions of the telomeric Gags, as they are in retroviral Gags.


Subject(s)
DNA Transposable Elements , Drosophila Proteins/metabolism , Drosophila/genetics , Gene Products, gag , Insect Proteins/metabolism , Retroelements/genetics , Telomere/metabolism , Amino Acid Sequence , Animals , Cell Nucleus/metabolism , Cells, Cultured , Drosophila Proteins/chemistry , Drosophila Proteins/genetics , Green Fluorescent Proteins , Insect Proteins/chemistry , Insect Proteins/genetics , Luminescent Proteins/genetics , Luminescent Proteins/metabolism , Molecular Sequence Data , Recombinant Fusion Proteins/metabolism , Telomere/genetics , Transfection
4.
Proc Natl Acad Sci U S A ; 99(6): 3621-6, 2002 Mar 19.
Article in English | MEDLINE | ID: mdl-11891280

ABSTRACT

Many Drosophila non-long terminal repeat (LTR) retrotransposons actively transpose into internal, gene-rich regions of chromosomes but do not transpose onto chromosome ends. HeT-A and TART are remarkable exceptions; they form telomeres of Drosophila by repeated transpositions onto the ends of chromosomes and never transpose to internal regions of chromosomes. Both telomeric and nontelomeric, non-LTR elements transpose by target-primed reverse transcription, and their targets are not determined simply by DNA sequence, so it is not clear why these two kinds of elements have nonoverlapping transposition patterns. To explore roles of retrotransposon-encoded proteins in transposition, we analyzed intracellular targeting of Gag proteins from five non-LTR retrotransposons, HeT-A, TART, jockey, Doc, and I factor. All were expressed as green fluorescent protein-tagged proteins in cultured Drosophila cells. These Gag proteins have high levels of sequence similarity, but they have dramatic differences in intracellular targeting. As expected, HeT-A and TART Gags are transported efficiently to nuclei, where they show specific patterns of localization. These patterns are cell cycle-dependent, disappearing during mitosis. In contrast, only a fraction of jockey Gag moves into nuclei, whereas neither Doc nor I factor Gag is detected in the nucleus. Gags of the nontelomeric retrotransposons form characteristic clusters in the cytoplasm. These experiments demonstrate that closely related retrotransposon Gag proteins can have different intracellular localizations, presumably because they interact differently with cellular components. We suggest that these interactions reflect mechanisms by which the cell influences the level of transposition of an element.


Subject(s)
Cell Nucleus/metabolism , Cytoplasm/metabolism , Drosophila Proteins/metabolism , Drosophila/cytology , Drosophila/metabolism , Recombination, Genetic/genetics , Retroelements/genetics , Animals , Cell Cycle , Cell Line , Drosophila/genetics , Drosophila Proteins/genetics , Protein Transport , Recombinant Fusion Proteins/genetics , Recombinant Fusion Proteins/metabolism , Terminal Repeat Sequences/genetics , Time Factors
7.
Genetica ; 109(1-2): 45-52, 2000.
Article in English | MEDLINE | ID: mdl-11293794

ABSTRACT

In Drosophila two non-LTR retrotransposons, HeT-A and TART, offer a novel experimental system for the study of heterochromatin. These elements, found only in heterochromatin, form Drosophila telomeres by repeated transposition onto chromosome ends. Their transposition yields arrays of repeats larger and more irregular than the repeats produced by telomerase; nevertheless, the transpositions are, in principle, equivalent to the telomere-building action of telomerase. The identification of the HeT-A promoter has given the first view of the molecular structure of a promoter active in heterochromatin. These telomere-specific elements are unusual in having a large amount of non-coding sequence. Like many other heterochromatic sequences, the HeT-A non-coding sequence has a repetitive organization strongly conserved within the species, although the sequence itself can undergo significant change between species (a typical example of concerted evolution). Such heterochromatic sequences could be important for the cell, perhaps as docking stations for essential proteins.


Subject(s)
DNA Transposable Elements , Drosophila/genetics , Heterochromatin/genetics , Telomere , Animals , Promoter Regions, Genetic
8.
Chromosoma ; 108(2): 73-82, 1999 May.
Article in English | MEDLINE | ID: mdl-10382069

ABSTRACT

Early studies of telomerase suggested that telomeres are maintained by an elegant but relatively simple and highly conserved mechanism of telomerase-medicated replication. As we learn more, it has become clear that the mechanism is elegant but not as simple as first thought. It is also evident that, although many species use similar, sometimes identical, DNA sequences for telomeres, these species express their own individuality in the way they regulate these sequences and, perhaps, in the additional tasks that they have imposed on their telomeric DNA. The striking similarities between telomeres in different species have revealed much about chromosome ends; the differences are proving to be equally informative. In addition to the differences between species that use telomerase, there are also a few exceptional organisms with atypical telomeres for which no telomerase activity has been detected. This review addresses recent studies, the insights they offer, and, perhaps more importantly, the questions they raise.


Subject(s)
Telomerase/metabolism , Telomere , Aging/genetics , Animals , Humans , Neoplasms/genetics
10.
Mol Cell Biol ; 19(1): 873-81, 1999 Jan.
Article in English | MEDLINE | ID: mdl-9858610

ABSTRACT

The transposable elements HeT-A and TART constitute the telomeres of Drosophila chromosomes. Both are non-long terminal repeat (LTR) retrotransposons, sharing the remarkable property of transposing only to chromosome ends. In addition, strong sequence similarity of their gag proteins indicates that these coding regions share a common ancestor. These findings led to the assumption that HeT-A and TART are closely related. However, we now find that these elements produce quite different sets of transcripts. HeT-A produces only sense-strand transcripts of the full-length element, whereas TART produces both sense and antisense full-length RNAs, with antisense transcripts in more than 10-fold excess over sense RNA. In addition, features of TART sequence organization resemble those of a subclass of non-LTR elements characterized by unequal terminal repeats. Thus, the ancestral gag sequence appears to have become incorporated in two different types of elements, possibly with different functions in the telomere. HeT-A transcripts are found in both nuclear and cytoplasmic cell fractions, consistent with roles as both mRNA and transposition template. In contrast, both sense and antisense TART transcripts are almost entirely concentrated in nuclear fractions. Also, TART open reading frame 2 probes detect a cytoplasmic mRNA for reverse transcriptase (RT), with no similarity to TART sequence 5' or 3' of the RT coding region. This RNA could be a processed TART transcript or the product of a "free-standing" RT gene. Either origin would be novel. The distinctive transcription patterns of both HeT-A and TART are conserved in Drosophila yakuba, despite significant sequence divergence. The conservation argues that these sets of transcripts are important to the function(s) of HeT-A and TART.


Subject(s)
DNA Transposable Elements , Drosophila melanogaster/genetics , Genes, Insect , Telomere , Transcription, Genetic , Animals , Base Sequence , Conserved Sequence , DNA, Complementary , Intracellular Fluid , Molecular Sequence Data , Nucleic Acid Hybridization , RNA, Antisense , RNA-Directed DNA Polymerase/genetics , Retroelements , Terminal Repeat Sequences
11.
Genetica ; 107(1-3): 189-96, 1999.
Article in English | MEDLINE | ID: mdl-10952212

ABSTRACT

Telomeres in Drosophila melanogaster are composed of multiple copies of two retrotransposable elements, HeT-A and TART instead of the short DNA repeats generated by telomerase in most organisms. Transpositions of HeT-A and TART yield arrays of repeats larger and more irregular than the repeats produced by telomerase; nevertheless, these transpositions are, in principle, equivalent to the telomere-building action of telomerase. Both telomerase and transposition of HeT-A and TART extend chromosomes by RNA-templated addition of specific sequences. We have proposed that HeT-A has evolved from genes encoding telomerase components. Although both HeT-A and TART share some novel features, TART probably has a different origin from HeT-A. HeT-A and TART are clearly identifiable as non-long terminal repeat (non-LTR) retrotransposons. Both telomere elements transpose only to the ends of chromosomes (apparently to any chromosome end in D. melanogaster) and each contains a large segment of untranslated sequence. HeT-A and TART are the first examples of transposable elements with a clear role in chromosome structure. This has interesting implications for the evolution of both chromosomes and transposable elements. The finding also raises the possibility that other transposable elements with bona fide roles in the cell will be detected, not only in Drosophila, but also in other organisms.


Subject(s)
Chromosomes , DNA Transposable Elements , Drosophila melanogaster/genetics , Telomere , Animals , Evolution, Molecular , Promoter Regions, Genetic , Retroviridae/genetics
13.
Proc Natl Acad Sci U S A ; 95(7): 3770-5, 1998 Mar 31.
Article in English | MEDLINE | ID: mdl-9520442

ABSTRACT

HeT-A was the first transposable element shown to have a bona fide role in chromosome structure, maintenance of telomeres in Drosophila melanogaster. HeT-A has hallmarks of non-long-terminal-repeat (non-LTR) retrotransposable elements but also has several unique features. We have now isolated HeT-A elements from Drosophila yakuba, showing that the retrotransposon mechanism of telomere maintenance predates the separation of D. melanogaster and D. yakuba (5-15 million years ago). HeT-A elements from the two species show significant sequence divergence, yet unusual features seen in HeT-Amel are conserved in HeT-Ayak. In both species, HeT-A elements are found in head-to-tail tandem arrays in telomeric heterochromatin. In both species, nearly half of the HeT-A sequence is noncoding and shows a distinctive imperfect repeat pattern of A-rich segments. Neither element encodes reverse transcriptase. The HeT-Amel promoter appears to be intermediate between the promoters of non-LTR and of LTR retrotransposons. The HeT-Ayak promoter shows similar features. HeT-Amel has a frameshift within the coding region. HeT-Ayak does not require a frameshift but shows conservation of the polypeptide sequence of the frameshifted product of D. melanogaster.


Subject(s)
DNA Transposable Elements/genetics , Drosophila Proteins , Drosophila melanogaster/genetics , Drosophila/genetics , Gene Products, gag , Insect Proteins/genetics , Telomere/genetics , Animals , Cloning, Molecular , Conserved Sequence , Molecular Sequence Data , Sequence Analysis
14.
Genetics ; 148(1): 233-42, 1998 Jan.
Article in English | MEDLINE | ID: mdl-9475735

ABSTRACT

HeT-A, a major component of Drosophila telomeres, is the first retrotransposon proposed to have a vital cellular function. Unlike most retrotransposons, more than half of its genome is noncoding. The 3' end contains > 2.5 kb of noncoding sequence. Copies of HeT-A differ by insertions or deletions and multiple nucleotide changes, which initially led us to conclude that HeT-A noncoding sequences are very fluid. However, we can now report, on the basis of new sequences and further analyses, that most of these differences are due to the existence of a small number of conserved sequence subfamilies, not to extensive sequence change during each transposition event. The high level of sequence conservation within subfamilies suggests that they arise from a small number of replicatively active elements. All HeT-A subfamilies show preservation of two intriguing features. First, segments of extremely A-rich sequence form a distinctive pattern within the 3' noncoding region. Second, there is a strong strand bias of nucleotide composition: The DNA strand running 5' to 3' toward the middle of the chromosome is unusually rich in adenine and unusually poor in guanine. Although not faced with the constraints of coding sequences, the HeT-A 3' noncoding sequence appears to be under other evolutionary constraints, possibly reflecting its roles in the telomeres.


Subject(s)
Drosophila/genetics , Retroelements/genetics , Telomere/genetics , Animals , Conserved Sequence , Sequence Alignment
15.
Cell ; 88(5): 647-55, 1997 Mar 07.
Article in English | MEDLINE | ID: mdl-9054504

ABSTRACT

HeT-A elements are non-long terminal repeat (non-LTR) retrotransposons found in head-to-tail arrays on Drosophila chromosome ends, where they form telomeres. We report that HeT-A promoter activity is located in the 3' end of the element, unlike the 5' location seen for other non-LTR retrotransposons. In HeT-A arrays the 3' sequence of one element directs transcription of its downstream neighbor. Because the upstream promoter has the same sequence as the 3' end of the transcribed element, the HeT-A promoter is effectively equivalent to a 5' LTR in both structure and function. Retroviruses and LTR retrotransposons have their promoters and transcription initiation sites in their 5' LTRs. Thus HeT-A appears to have the structure of an evolutionary intermediate between non-LTR and LTR retrotransposons.


Subject(s)
DNA Transposable Elements/genetics , Promoter Regions, Genetic/genetics , Retroviridae/genetics , Telomere/genetics , Animals , Base Sequence , Biological Evolution , Blotting, Northern , Cells, Cultured/physiology , Drosophila melanogaster , Genes, Viral/genetics , Molecular Sequence Data , RNA, Messenger/analysis , Sequence Analysis, DNA , Transcription, Genetic/genetics
16.
Genetica ; 100(1-3): 73-84, 1997.
Article in English | MEDLINE | ID: mdl-9440260

ABSTRACT

Transposable elements are abundant in the genomes of higher organisms but are usually thought to affect cells only incidentally, by transposing in or near a gene and influencing its expression. Telomeres of Drosophila chromosomes are maintained by two non-LTR retrotransposons, HeT-A and TART. These are the first transposable elements with identified roles in chromosome structure. We suggest that these elements may be evolutionarily related to telomerase; in both cases an enzyme extends the end of a chromosome by adding DNA copied from an RNA template. The evolution of transposable elements from chromosomal replication mechanisms may have occurred multiple times, although in other organisms the new products have not replaced the endogenous telomerase, as they have in Drosophila. This is somewhat reminiscent of the oncogenes that have arisen from cellular genes. Perhaps the viruses that carry oncogenes have also arisen from cellular genetic systems.


Subject(s)
Drosophila/genetics , Evolution, Molecular , Retroelements , Telomere , Amino Acid Sequence , Animals , Molecular Sequence Data , Repetitive Sequences, Nucleic Acid , Sequence Homology, Amino Acid , Telomerase/genetics
17.
J Mol Evol ; 43(6): 572-83, 1996 Dec.
Article in English | MEDLINE | ID: mdl-8995054

ABSTRACT

A major component of Drosophila telomeres is the retrotransposon HeT-A, which is clearly related to other retrotransposons and retroviruses. This retrotransposon is distinguished by its exclusively telomeric location, and by the fact that, unlike other retrotransposons, it does not encode its own reverse transcriptase. HeT-A coding sequences diverge significantly, even between elements within the same genome. Such rapid divergence has been noted previously in studies of gag genes from other retroelements. Sequence comparisons indicate that the entire HeT-A coding region codes for gag protein, with regions of similarity to other insect retrotransposon gag proteins found throughout the open reading frame (ORF). Similarity is most striking in the zinc knuckle region, a region characteristic of gag genes of most replication-competent retroelements. We identify a subgroup of insect non-LTR retrotransposons with three zinc knuckles of the form: (1) CX2CX4HX4C, (2) CX2CX3HX4C, (3) CX2CX3HX6C. The first and third knuckles are invariant, but the second shows some differences between members of this subgroup. This subgroup includes HeT-A and a second Drosophila telomeric retrotransposon, TART. Unlike other gag regions, HeT-A requires a -1 frameshift for complete translation. Such frameshifts are common between the gag and pol sequences of retroviruses but have not before been seen within a gag sequence. The frameshift allows HeT-A to encode two polypeptides; this mechanism may substitute for the post-translational cleavage that creates multiple gag polypeptides in retroviruses. D. melanogaster HeT-A coding sequences have a polymorphic region with insertions/deletions of 1-31 codons and many nucleotide changes. None of these changes interrupt the open reading frame, arguing that only elements with translatable ORFs can be incorporated into the chromosomes. Perhaps HeT-A translation products act in cis to target the RNA to chromosome ends.


Subject(s)
DNA Transposable Elements , Drosophila Proteins , Drosophila/genetics , Gene Products, gag , Insect Proteins/genetics , Polymorphism, Genetic , Retroelements/genetics , Telomere/genetics , Amino Acid Sequence , Animals , Binding Sites , Blotting, Northern , Conserved Sequence , Drosophila melanogaster/genetics , Insect Proteins/metabolism , Molecular Sequence Data , Open Reading Frames , Peptide Fragments/genetics , Peptide Fragments/metabolism , Protein Biosynthesis , Sequence Homology, Amino Acid , Telomere/metabolism , Transcription, Genetic , Zinc/metabolism
18.
Trends Genet ; 12(2): 48-52, 1996 Feb.
Article in English | MEDLINE | ID: mdl-8851970

ABSTRACT

In Drosophila, chromosome ends (telomeres) are composed of telomere-specific transposable elements (the retroposons HeT-A and TART). These elements are a bona fide part of the cellular machinery yet have many of the hallmarks of retrotransposable elements and retroviruses, raising the possibility that parasitic transposable elements and viruses might have evolved from mechanisms that the cell uses to maintain its chromosomes. It is striking that Drosophila, the model organism for many discoveries in genetics, development and molecular biology (including the classical concept of telomeres), should prove to have chromosome ends different from the generally accepted model. Studies of these telomere-specific retrotransposable elements raise questions about conventional wisdom concerning not only telomeres, but also transposable elements and heterochromatin.


Subject(s)
Drosophila/genetics , Evolution, Molecular , Telomere/genetics , Animals , Base Sequence , Molecular Sequence Data , Retroelements
19.
Genetics ; 139(4): 1611-21, 1995 Apr.
Article in English | MEDLINE | ID: mdl-7540581

ABSTRACT

The Drosophila melanogaster Hsr-omega locus produces a nuclear RNA containing > 5 kb of tandem repeat sequences. These repeats are unique to Hsr-omega and show concerted evolution similar to that seen with classical satellite DNAs. In D. melanogaster the monomer is approximately 280 bp. Sequences of 19 1/2 monomers differ by 8 +/- 5% (mean +/- SD), when all pairwise comparisons are considered. Differences are single nucleotide substitutions and 1-3 nucleotide deletions/insertions. Changes appear to be randomly distributed over the repeat unit. Outer repeats do not show the decrease in monomer homogeneity that might be expected if homogeneity is maintained by recombination. However, just outside the last complete repeat at each end, there are a few fragments of sequence similar to the monomer. The sequences in these flanking regions are not those predicted for sequences decaying in the absence of recombination. Instead, the fragmentation of the sequence homology suggests that flanking regions have undergone more severe disruptions, possibly during an insertion or amplification event. Hsr-omega alleles differing in the number of repeats are detected and appear to be stable over a few thousand generations; however, both increases and decreases in repeat numbers have been observed. The new alleles appear to be as stable as their predecessors. No alleles of less than approximately 5 kb nor more than approximately 16 kb of repeats were seen in any stocks examined. The evidence that there is a limit on the minimum number of repeats is consistent with the suggestion that these repeats are important in the function of the unusual Hsr-omega nuclear RNA.


Subject(s)
Cell Nucleus/metabolism , Drosophila melanogaster/genetics , RNA/genetics , Repetitive Sequences, Nucleic Acid , Alleles , Animals , Base Sequence , Chromosome Mapping , Molecular Sequence Data , Oligodeoxyribonucleotides , Species Specificity
20.
J Cell Biol ; 128(3): 393-403, 1995 Feb.
Article in English | MEDLINE | ID: mdl-7844153

ABSTRACT

In Drosophila, the large muscle protein, projectin, has very different localizations in synchronous and asynchronous muscles, suggesting that projectin has different functions in different muscle types. The multiple projectin isoforms are encoded by a single gene; however they differ significantly in size (as detected by gel mobility) and show differences in some peptide fragments, presumably indicating alternative splicing or termination. We now report additional sequence of the projectin gene, showing a kinase domain and flanking regions highly similar to equivalent regions of twitchin, including a possible autoinhibitory region. In spite of apparent differences in function, all isoforms of projectin have the kinase domain and all are capable of autophosphorylation in vitro. The projectin gene is in polytene region 102C/D where the bentD phenotype maps. The recessive lethality of bentD is associated with a breakpoint that removes sequence of the projectin kinase domain. We find that different alleles of the highly mutable recessive lethal complementation group, l(4)2, also have defects in different parts of the projectin sequence, both NH2-terminal and COOH-terminal to the bentD breakpoint. These alleles are therefore renamed as alleles of the bent locus. Adults heterozygous for projectin mutations show little, if any, effect of one defective gene copy, but homozygosity for any of the defects is lethal. The times of death can vary with allele. Some alleles kill the embryos, others are larval lethal. These molecular studies begin to explain why genetic studies suggested that l(4)2 was a complex (or pseudoallelic) locus.


Subject(s)
Drosophila melanogaster/metabolism , Muscle Proteins/metabolism , Phosphotransferases/metabolism , Amino Acid Sequence , Animals , Catalysis , Conserved Sequence , Drosophila melanogaster/genetics , Genes, Lethal , Molecular Sequence Data , Muscle Contraction , Muscle Proteins/genetics , Phosphorylation , Phosphotransferases/genetics , Sequence Homology, Amino Acid
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