Drosophila FoxL1 non-autonomously coordinates organ placement during embryonic development

Dev Biol. 2016 Nov 15;419(2):273-284. doi: 10.1016/j.ydbio.2016.09.007. Epub 2016 Sep 13.

Abstract

Determining how organs attain precise positioning within an organism is a crucial facet of developmental biology. The Fox family winged-helix transcription factors are known to play key roles in development of multiple organs. Drosophila FoxL1 (aka Fd64A) is dynamically expressed in embryos but its function is completely uncharacterized. FoxL1 is expressed in a single group of body wall - muscles in the 2nd and 3rd thoracic segments, in homologous abdominal muscles at earlier stages, and in the hindgut mesoderm from early through late embryogenesis. We show that FoxL1 expression in T2 and T3 is in VIS5, which is not a single muscle spanning the entire thorax, as previously published, but is, instead, three individual muscles, each spanning a single thoracic segment. We generate mutations in foxL1 and show that, surprisingly, none of the tissues that express FoxL1 are affected by its loss. Instead, loss of foxL1 results in defects in salivary gland positioning and morphology, as well as defects in the migration of hemocytes, germ cells and Malpighian tubules. We also show that FoxL1-dependent expression of secreted Sema2a in T3 VIS5 is required for normal salivary gland positioning. Altogether, these findings suggest that Drosophila FoxL1 functions like its mammalian counterpart in non-autonomously orchestrating the behaviors of surrounding tissues.

Keywords: Drosophila; Embryogenesis; Fox proteins; FoxL1; Germ cells; Hemocytes; Malpighian tubules; Migration; Salivary gland; Somatic muscle.

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Body Patterning / genetics
  • Body Patterning / physiology
  • Cell Movement / genetics
  • Cell Movement / physiology
  • Drosophila Proteins / deficiency
  • Drosophila Proteins / genetics
  • Drosophila Proteins / physiology*
  • Drosophila melanogaster / embryology*
  • Drosophila melanogaster / genetics
  • Embryo, Nonmammalian / ultrastructure
  • Embryonic Germ Cells / cytology
  • Forkhead Transcription Factors / deficiency
  • Forkhead Transcription Factors / genetics
  • Forkhead Transcription Factors / physiology*
  • Gene Expression Regulation, Developmental
  • Hemocytes / cytology
  • Malpighian Tubules / embryology
  • Muscles / embryology
  • Muscles / ultrastructure
  • Organ Specificity
  • Organogenesis / genetics
  • Organogenesis / physiology*
  • RNA Interference
  • Recombinant Fusion Proteins / genetics
  • Salivary Glands / embryology
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • Thorax / embryology
  • Thorax / ultrastructure

Substances

  • Drosophila Proteins
  • Forkhead Transcription Factors
  • FoxL1 protein, Drosophila
  • Recombinant Fusion Proteins