Live imaging of Drosophila gonad formation reveals roles for Six4 in regulating germline and somatic cell migration.
BACKGROUND
Movement of cells, either as amoeboid individuals or in organised groups, is a key feature of organ formation. Both modes of migration occur during Drosophila embryonic gonad development, which therefore provides a paradigm for understanding the contribution of these processes to organ morphogenesis. Gonads of Drosophila are formed from three distinct cell types: primordial germ cells (PGCs), somatic gonadal precursors (SGPs), and in males, male-specific somatic gonadal precursors (msSGPs). These originate in distinct locations and migrate to associate in two intermingled clusters which then compact to form the spherical primitive gonads. PGC movements are well studied, but much less is known of the migratory events and other interactions undergone by their somatic partners. These appear to move in organised groups like, for example, lateral line cells in zebra fish or Drosophila ovarian border cells.


RESULTS
We have used time-lapse fluorescence imaging to characterise gonadal cell behaviour in wild type and mutant embryos. We show that the homeodomain transcription factor Six4 is required for the migration of the PGCs and the msSGPs towards the SGPs. We have identified a likely cause of this in the case of PGCs as we have found that Six4 is required for expression of Hmgcr which codes for HMGCoA reductase and is necessary for attraction of PGCs by SGPs. Six4 affects msSGP migration by a different pathway as these move normally in Hmgcr mutant embryos. Additionally, embryos lacking fully functional Six4 show a novel phenotype in which the SGPs, which originate in distinct clusters, fail to coalesce to form unified gonads.


CONCLUSIONS
Our work establishes the Drosophila gonad as a model system for the analysis of coordinated cell migrations and morphogenesis using live imaging and demonstrates that Six4 is a key regulator of somatic cell function during gonadogenesis. Our data suggest that the initial association of SGP clusters is under distinct control from the movements that drive gonad compaction.
Clark
Ivan B N
IB
Centres for Integrative Physiology and Neuroscience Research, University of Edinburgh, George Square, Edinburgh, UK. ivan.clark@dundee.ac.uk <ivan.clark@dundee.ac.uk>
Jarman
Andrew P
AP
Finnegan
David J
DJ
D000818:Animals; D002465:Cell Movement / Q000235:genetics*; D004330:Drosophila / Q000196:embryology / Q000235:genetics*; D029721:Drosophila Proteins / Q000235:genetics*; D004625:Embryo, Nonmammalian; D018507:Gene Expression Regulation, Developmental; D005854:Germ Cells / Q000166:cytology*; D006066:Gonads / Q000196:embryology*; D018398:Homeodomain Proteins / Q000235:genetics*; D007150:Immunohistochemistry; D008856:Microscopy, Fluorescence; D009419:Nerve Tissue Proteins / Q000235:genetics*; D038081:Organogenesis / Q000235:genetics; D014157:Transcription Factors / Q000235:genetics*
D029721:Drosophila Proteins; D018398:Homeodomain Proteins; D009419:Nerve Tissue Proteins; C434485:Six4 protein, Drosophila; D014157:Transcription Factors