Requirement of teashirt (tsh) function during cell fate specification in developing head structures in Drosophila

Abstract The homeotic gene teashirt (tsh) is known to regulate segmental identity of the trunk region of the Drosophila embryo. Here we report a requirement for tsh function in the development of adult head structures. Animals homozygous for a viable tsh allele or heterozygous for various embryonic recessive lethal alleles displayed miniaturized maxillary palps, a phenotype characteristically induced by dominant gain-of-function mutations of Antennapedia (Antp) homeotic gene. Animals transheterozygous for tsh and Antp mutations displayed an enhanced antenna-to-leg and a striking reduced-eye phenotype suggesting aggravated ANTP misexpression in eye-antennal discs of these animals. In agreement with this, in the developing eye-antennal discs of the tsh mutant animals a significant amount of ANTP protein was detected overlapping the domains where tsh is normally expressed. These results suggest that tsh specifies adult head segments by repressing Antp expression.

[1]  M. Scott,et al.  Setting limits on homeotic gene function: restraint of Sex combs reduced activity by teashirt and other homeotic genes. , 1994, The EMBO journal.

[2]  J. Whittle.  Pattern formation in imaginal discs. , 1990, Seminars in cell biology.

[3]  Bernard Jacq,et al.  The gene teashirt is required for the development of Drosophila embryonic trunk segments and encodes a protein with widely spaced zinc finger motifs , 1991, Cell.

[4]  A. Ghysen,et al.  Neural enhancer-like elements as specific cell markers in Drosophila. , 1989, Development.

[5]  G. Struhl.  Genes controlling segmental specification in the Drosophila thorax. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[6]  D. Lindsley,et al.  The Genome of Drosophila Melanogaster , 1992 .

[7]  T. Kaufman,et al.  Analysis of larval segmentation in lethal genotypes associated with the antennapedia gene complex in Drosophila melanogaster. , 1981, Developmental biology.

[8]  J. Rempel.  The Evolution of the Insect Head: the Endless Dispute , 1975 .

[9]  S. Kerridge,et al.  Homeotic complex and teashirt genes co-operate to establish trunk segmental identities in Drosophila. , 1994, Development.

[10]  A. Schier,et al.  The specificities of sex combs reduced and Antennapedia are defined by a distinct portion of each protein that includes the homeodomain , 1990, Cell.

[11]  K. G. Coleman,et al.  Expression of engrailed proteins in arthropods, annelids, and chordates. , 1989, Cell.

[12]  W. Gehring,et al.  Redesigning the body plan of Drosophilaby ectopic expression of the homoeotic gene Antennapedia , 1987, Nature.

[13]  W. Gehring,et al.  Molecular analysis of the dominant homeotic Antennapedia phenotype , 1987, The EMBO journal.

[14]  N. Perrimon,et al.  The molecular genetics of head development in Drosophila melanogaster. , 1991, Development.

[15]  M. Scott,et al.  Role of the teashirt gene in Drosophila midgut morphogenesis: secreted proteins mediate the action of homeotic genes. , 1994, Development.

[16]  G. Struhl,et al.  A homoeotic mutation transforming leg to antenna in Drosophila , 1981, Nature.

[17]  T. Kaufman,et al.  Cytogenetic Analysis of Chromosome 3 in DROSOPHILA MELANOGASTER: The Homoeotic Gene Complex in Polytene Chromosome Interval 84a-B. , 1980, Genetics.

[18]  W. Gehring,et al.  Functional specificity of the Antennapedia homeodomain. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[19]  P. Talbert,et al.  The Drosophila homeotic mutation Nasobemia (AntpNs) and its revertants: an analysis of mutational reversion. , 1994, Genetics.

[20]  S. Kerridge,et al.  The role of the teashirt gene in trunk segmental identity in Drosophila. , 1992, Development.

[21]  W. Gehring,et al.  Homeotic transformation of thorax into head: Developmental analysis of a new Antennapedia allele in Drosophila melanogaster , 1985 .

[22]  L. Misquitta,et al.  Search for Drosophila genes based on patterned expression of mini-white reporter gene of a P lacW vector in adult eyes , 1995, Roux's archives of developmental biology.

[23]  M. Scott,et al.  Homeotic response elements are tightly linked to tissue-specific elements in a transcriptional enhancer of the teashirt gene. , 1995, Development.

[24]  Michael Akam,et al.  Homeotic genes and the control of segment diversity , 1988 .

[25]  J. Postlethwait,et al.  Pattern formation and determination in the antenna of the homoeotic mutant Antennapedia of Drosophila melanogaster. , 1971, Developmental biology.

[26]  C. Wilson,et al.  Identification of target genes of the homeotic gene Antennapedia by enhancer detection. , 1991, Genes & development.

[27]  S. Cohen,et al.  Specification of the wing by localized expression of wingless protein , 1996, Nature.