Drosophila Lysophospholipase Gene swiss cheese Is Required for Survival and Reproduction

SIMPLE SUMMARY: Biological evolution implies fitness of newly evolved organisms that have inherent adaptive traits because of mutations in genes. However, most mutations are detrimental, and they spoil the organism’s life, its survival and its ability to leave progeny. Some genes are extremely vital for an organism, and therefore, they tend to save their structure and do not mutate or do it very composedly. That is the case of the gene encoding PNPLA6 lysophospholipase domain that evolved in bacteria, and evolution obliged it to save its function in higher animals. In mammals, complete dysfunction of such a gene is lethal because of its high importance in placenta for early embryo development. Why is it conserved in other species, for instance insects, that have no placenta? Here we studied the role of the PNPLA6-encoding gene named swiss cheese in Drosophila melanogaster fitness. We have found that its dysfunction results in premature death of specimens and their inability to leave enough progeny. Thus, we provide the first evidence for significance of the gene that encodes the lysophospholipase enzyme in fitness of insects. ABSTRACT: Drosophila melanogaster is one of the most famous insects in biological research. It is widely used to analyse functions of different genes. The phosphatidylcholine lysophospholipase gene swiss cheese was initially shown to be important in the fruit fly nervous system. However, the role of this gene in non-nervous cell types has not been elucidated yet, and the evolutional explanation for the conservation of its function remains elusive. In this study, we analyse expression pattern and some aspects of the role of the swiss cheese gene in the fitness of Drosophila melanogaster. We describe the spatiotemporal expression of swiss cheese throughout the fly development and analyse the survival and productivity of swiss cheese mutants. We found swiss cheese to be expressed in salivary glands, midgut, Malpighian tubes, adipocytes, and male reproductive system. Dysfunction of swiss cheese results in severe pupae and imago lethality and decline of fertility, which is impressive in males. The latter is accompanied with abnormalities of male locomotor activity and courtship behaviour, accumulation of lipid droplets in testis cyst cells and decrease in spermatozoa motility. These results suggest that normal swiss cheese is important for Drosophila melanogaster fitness due to its necessity for both specimen survival and their reproductive success.