Cytoplasmic dynein-dynactin complex is required for spermatid growth but not axoneme assembly in Drosophila.
Spermatids derived from a single gonial cell remain interconnected within a cyst and elongate by synchronized growth inside the testis in Drosophila. Cylindrical spectrin-rich elongation cones form at their distal ends during the growth. The mechanism underlying this process is poorly understood. We found that developing sperm tails were abnormally coiled at the growing ends inside the cysts in the Drosophila Dynein light chain 1 (ddlc1) hemizygous mutant testis. A quantitative assay showed that average number of elongation cones was reduced, they were increasingly deformed, and average cyst lengths were shortened in ddlc1 hemizygous testes. These phenotypes were further enhanced by additional partial reduction of Dhc64C and Glued and rescued by Myc-PIN/LC8 expression in the gonial cells in ddlc1 backgrounds. Furthermore, DDLC1, DHC, and GLUED were enriched at the distal ends of growing spermatids. Finally, ultrastructure analysis of ddlc1 testes revealed abnormally formed interspermatid membrane, but the 9 + 2 microtubule organization, the radial spoke structures, and the Dynein arms of the axoneme were normal. Together, these findings suggest that axoneme assembly and spermatid growth involve independent mechanisms in Drosophila and DDLC1 interacts with the Dynein-Dynactin complex at the distal ends of spermatids to maintain the spectrin cytoskeleton assembly and cell growth.
Ghosh-Roy
Anindya
A
Tata Institute of Fundamental Research, Mumbai 400 005, India.
Kulkarni
Madhura
M
Kumar
Vikash
V
Shirolikar
Seema
S
Ray
Krishanu
K
D000483:Alleles; D000818:Animals; D002352:Carrier Proteins / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D003593:Cytoplasm / Q000378:metabolism; D003598:Cytoskeletal Proteins / Q000032:analysis / Q000378:metabolism; D004330:Drosophila / Q000235:genetics / Q000254:growth & development* / Q000648:ultrastructure*; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D000072159:Dynactin Complex; D004398:Dyneins / Q000378:metabolism / Q000502:physiology*; D005816:Genetic Complementation Test; D007248:Infertility, Male / Q000235:genetics; D008297:Male; D008869:Microtubule-Associated Proteins / Q000032:analysis / Q000378:metabolism / Q000502:physiology*; D013081:Sperm Motility / Q000235:genetics; D013082:Sperm Tail / Q000378:metabolism / Q000648:ultrastructure; D013087:Spermatids / Q000254:growth & development* / Q000648:ultrastructure*; D013737:Testis / Q000166:cytology / Q000378:metabolism
D002352:Carrier Proteins; D003598:Cytoskeletal Proteins; C105393:DCTN1-p150 protein, Drosophila; D029721:Drosophila Proteins; D000072159:Dynactin Complex; D008869:Microtubule-Associated Proteins; C542608:ctp protein, Drosophila; D004398:Dyneins