Reduced expression of CDP-DAG synthase changes lipid composition and leads to male sterility in Drosophila.

Barbara Laurinyecz,Viktor Vedelek,Péter Maróy,Gábor Juhász,László Vígh,Attila L Kovács,Gábor Balogh,Mária Péter,Rita Sinka

doi:10.1098/rsob.150169

Abstract

Drosophila spermatogenesis is an ideal system to study the effects of changes in lipid composition, because spermatid elongation and individualization requires extensive membrane biosynthesis and remodelling. The bulk of transcriptional activity is completed with the entry of cysts into meiotic division, which makes post-meiotic stages of spermatogenesis very sensitive to even a small reduction in gene products. In this study, we describe the effect of changes in lipid composition during spermatogenesis using a hypomorphic male sterile allele of the Drosophila CDP-DAG synthase (CdsA) gene. We find that the CdsA mutant shows defects in spermatid individualization and enlargement of mitochondria and the axonemal sheath of the spermatids. Furthermore, we could genetically rescue the male sterile phenotype by overexpressing Phosphatidylinositol synthase (dPIS) in a CdsA mutant background. The results of lipidomic and genetic analyses of the CdsA mutant highlight the importance of correct lipid composition during sperm development and show that phosphatidic acid levels are crucial in late stages of spermatogenesis.

Highlights

Many developmental processes rely on controlled membrane growth, but the precise regulation of this process has yet to be characterized
We focused on a key enzyme in lipid metabolism, cytidine–diphosphate– diacyglycerol (CDP-DAG) synthase, and investigated its importance in spermatogenesis
CDP-DAG synthase (CdsA) function is not required for individualization complex formation, it may play an indirect role in its movement

Summary

Introduction

Many developmental processes rely on controlled membrane growth, but the precise regulation of this process has yet to be characterized. The meiotic divisions produce a cyst with 64 round spermatids, where cells are still connected by intercellular cytoplasmic bridges [1,2]. The nebenkern forms after meiosis by the aggregation, fusion and wrapping of mitochondria, divides into two parts (figure 1a) [3]. Both mitochondrial derivatives elongate together with the microtubule array that is formed around the mitochondrial surface [4]. Mature elongated sperm develop from approximately 12 mm spermatids through a process of intensive morphological changes. The spermatids increase their length 150-fold, producing spermatids approximately 1.8 mm long after elongation. The fully elongated spermatids undergo a synchronized individualization, in

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Conclusion