Sperm-Leucylaminopeptidases are required for male fertility as structural components of mitochondrial paracrystalline material in Drosophila melanogaster sperm

Laurinyecz, Barbara; Vedelek, Viktor; Kovács, Attila; Szilasi, Kinga; Lipinszki, Zoltán; Slezák, Csilla; Darula, Zsuzsanna; Juhász, Gábor; Sinka, Rita

doi:10.1371/journal.pgen.1007987

Cited by 33 publications

(50 citation statements)

References 58 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In some insect species, the two mitochondrial derivatives in a single spermatozoon differ in ultrastructural features, such as their size and the material they contain 48,49 . In Drosophila, defects in the larger mitochondrial derivatives induce male sterility 50 . In lepidopteran insects, eupyrene and apyrene sperm contain distinctively different mitochondrial derivatives; nevertheless, the molecular constituents and precise functions of the two types of mitochondrial derivatives still remain to be determined 23,40 .…”

Section: Discussionmentioning

confidence: 99%

Dysfunction of dimorphic sperm impairs male fertility in the silkworm

Chen

Liu

et al. 2020

Cell Discov

View full text Add to dashboard Cite

Sperm, which have a vital role in sexual reproduction in the animal kingdom, can display heteromorphism in some species. The regulation of sperm dichotomy remains a longstanding puzzle even though the phenomenon has been widely documented for over a century. Here we use Bombyx mori as a model to study a form of sperm dimorphism (eupyrene and apyrene sperm), which is nearly universal among Lepidoptera. We demonstrate that B. mori Sex-lethal (BmSxl) is crucial for apyrene sperm development, and that B. mori poly(A)-specific ribonuclease-like domain-containing 1 (BmPnldc1) is required for eupyrene sperm development. BmSXL is distributed in the nuclei and cytoplasm of somatic cyst cells in a mesh-like pattern and in the cytoplasm of germ cells enclosed in spermatocysts and sperm bundles. Cytological analyses of dimorphic sperm in BmSxl mutants (∆BmSxl) showed deficient apyrene sperm with abnormal nuclei, as well as loss of motility associated with malformed mitochondrial derivatives. We define the crucial function of apyrene sperm in the process of fertilization as assisting the migration of eupyrene spermatozoa from bursa copulatrix to spermatheca. By contrast, BmPnldc1 deficiency (∆BmPnldc1) caused eupyrene sperm abnormalities and impaired the release of eupyrene sperm bundles during spermiation. Although apyrene or eupyrene sperm defects impaired fertility of the mutated males, double copulation of a wild-type female with ∆BmSxl and ∆BmPnldc1 males could rescue the sterility phenotypes induced by single copulation with either gene-deficient male. Our findings demonstrate the crucial functions of BmSxl and BmPnldc1 in the development of sperm dimorphism and the indispensable roles of nonfertile apyrene sperm in fertilization.

show abstract

Section: Discussionmentioning

confidence: 99%

Dysfunction of dimorphic sperm impairs male fertility in the silkworm

Chen

Liu

et al. 2020

Cell Discov

View full text Add to dashboard Cite

show abstract

“…The function of S-Lap is poorly studied, but a recent paper suggests that all S-Lap genes in D . melanogaster are structural components of the mitochondrial paracrystalline material in sperm tails [50]. Sperm tail morphology varies dramatically between D .…”

Section: Discussionmentioning

confidence: 99%

Recurrent gene co-amplification on Drosophila X and Y chromosomes

Bachtrog¹

2019

PLoS Genet

View full text Add to dashboard Cite

Y chromosomes often contain amplified genes which can increase dosage of male fertility genes and counteract degeneration via gene conversion. Here we identify genes with increased copy number on both X and Y chromosomes in various species of Drosophila, a pattern that has previously been associated with sex chromosome drive involving the Slx and Sly gene families in mice. We show that recurrent X/Y co-amplification appears to be an important evolutionary force that has shaped gene content evolution of sex chromosomes in Drosophila. We demonstrate that convergent acquisition and amplification of testis expressed gene families are common on Drosophila sex chromosomes, and especially on recently formed ones, and we carefully characterize one putative novel X/Y co-amplification system. We find that co-amplification of the S-Lap1 / GAPsec gene pair on both the X and the Y chromosome occurred independently several times in members of the D . obscura group, where this normally autosomal gene pair is sex-linked due to a sex chromosome—autosome fusion. We explore several evolutionary scenarios that would explain this pattern of co-amplification. Investigation of gene expression and short RNA profiles at the S-Lap1 / GAPsec system suggest that, like Slx/Sly in mice, these genes may be remnants of a cryptic sex chromosome drive system, however additional transgenic experiments will be necessary to validate this model. Regardless of whether sex chromosome drive is responsible for this co-amplification, our findings suggest that recurrent gene duplications between X and Y sex chromosomes could have a widespread effect on genomic and evolutionary patterns, including the epigenetic regulation of sex chromosomes, the distribution of sex-biased genes, and the evolution of hybrid sterility.

show abstract

“…Protein or peptide degradation, indicated, e.g., by a high abundance of leucine aminopeptidases in D . melanogaster mitochondrial derivatives 48,49 , are possible but likely not the sole mechanisms for energetic supply of sperm in males and females. Because these enzymes only partially clarify a predominance towards glycolytic or oxidative metabolism, two-photon FLIM presents itself as a promising method to analyse the structural composition and mechanistic functions of mitochondrial derivatives in insect sperm.…”

Section: Discussionmentioning

confidence: 99%

Distinct metabolic profiles in Drosophila sperm and somatic tissues revealed by two-photon NAD(P)H and FAD autofluorescence lifetime imaging

Wetzker

Reinhardt

2019

Sci Rep

View full text Add to dashboard Cite

Metabolic profiles vary across all levels of biological diversity, from cells to taxa. Two-photon fluorescence lifetime imaging microscopy (FLIM) facilitates metabolic characterisation of biological specimens by assaying the intrinsic autofluorescence of the ubiquitous coenzymes NAD(P)H and FAD. The potential of this method for characterising the diversity of organismal metabolism remains largely untapped. Using FLIM in Drosophila melanogaster, we show tissue-specificity in fluorescence lifetime that reflects variation in redox patterns. In particular, sperm cells exhibited elevated glycolysis relative to other tissues. We also show that sperm metabolism is phenotypically plastic: compared to male-stored sperm, sperm stored in the female’s storage organ showed a substantial reduction in the protein-bound FAD lifetime fraction but no change in the NAD(P)H profile. This study represents the first ex vivo investigation of sperm metabolism using FLIM.

show abstract

Sperm-Leucylaminopeptidases are required for male fertility as structural components of mitochondrial paracrystalline material in Drosophila melanogaster sperm

Cited by 33 publications

References 58 publications

Dysfunction of dimorphic sperm impairs male fertility in the silkworm

Dysfunction of dimorphic sperm impairs male fertility in the silkworm

Recurrent gene co-amplification on Drosophila X and Y chromosomes

Distinct metabolic profiles in Drosophila sperm and somatic tissues revealed by two-photon NAD(P)H and FAD autofluorescence lifetime imaging

Contact Info

Product

Resources

About