Specialized eRpL22 paralogue-specific ribosomes regulate specific mRNA translation in spermatogenesis in Drosophila melanogaster. 2019

Catherine M Mageeney, and Vassie C Ware
Department of Biological Sciences, Lehigh University, Bethlehem, PA 18015.

The functional significance of ribosome heterogeneity in development and differentiation is relatively unexplored. We present the first in vivo evidence of ribosome heterogeneity playing a role in specific mRNA translation in a multicellular eukaryote. Eukaryotic-specific ribosomal protein paralogues eRpL22 and eRpL22-like are essential in development and required for sperm maturation and fertility in Drosophila. eRpL22 and eRpL22-like roles in spermatogenesis are not completely interchangeable. Flies depleted of eRpL22 and rescued by eRpL22-like overexpression have reduced fertility, confirming that eRpL22-like cannot substitute fully for eRpL22 function, and that paralogues have functionally distinct roles, not yet defined. We investigated the hypothesis that specific RNAs differentially associate with eRpL22 or eRpL22-like ribosomes, thereby establishing distinct ribosomal roles. RNA-seq identified 12,051 transcripts (mRNAs/noncoding RNAs) with 50% being enriched on specific polysome types. Analysis of ∼10% of the most abundant mRNAs suggests ribosome specialization for translating groups of mRNAs expressed at specific stages of spermatogenesis. Further, we show enrichment of "model" eRpL22-like polysome-associated testis mRNAs can occur outside the germline within S2 cells transfected with eRpL22-like, indicating that germline-specific factors are not required for selective translation. This study reveals specialized roles in translation for eRpL22 and eRpL22-like ribosomes in germline differentiation.

UI MeSH Term Description Entries
D008297 Male Males
D011132 Polyribosomes A multiribosomal structure representing a linear array of RIBOSOMES held together by messenger RNA; (RNA, MESSENGER); They represent the active complexes in cellular protein synthesis and are able to incorporate amino acids into polypeptides both in vivo and in vitro. (From Rieger et al., Glossary of Genetics: Classical and Molecular, 5th ed) Polysomes,Polyribosome,Polysome
D004331 Drosophila melanogaster A species of fruit fly frequently used in genetics because of the large size of its chromosomes. D. melanogaster,Drosophila melanogasters,melanogaster, Drosophila
D005298 Fertility The capacity to conceive or to induce conception. It may refer to either the male or female. Fecundity,Below Replacement Fertility,Differential Fertility,Fecundability,Fertility Determinants,Fertility Incentives,Fertility Preferences,Fertility, Below Replacement,Marital Fertility,Natural Fertility,Subfecundity,World Fertility Survey,Determinant, Fertility,Determinants, Fertility,Fertility Determinant,Fertility Incentive,Fertility Preference,Fertility Survey, World,Fertility Surveys, World,Fertility, Differential,Fertility, Marital,Fertility, Natural,Preference, Fertility,Preferences, Fertility,Survey, World Fertility,Surveys, World Fertility,World Fertility Surveys
D005854 Germ Cells The reproductive cells in multicellular organisms at various stages during GAMETOGENESIS. Gamete,Gametes,Germ-Line Cells,Germ Line,Cell, Germ,Cell, Germ-Line,Cells, Germ,Cells, Germ-Line,Germ Cell,Germ Line Cells,Germ Lines,Germ-Line Cell
D000818 Animals Unicellular or multicellular, heterotrophic organisms, that have sensation and the power of voluntary movement. Under the older five kingdom paradigm, Animalia was one of the kingdoms. Under the modern three domain model, Animalia represents one of the many groups in the domain EUKARYOTA. Animal,Metazoa,Animalia
D012269 Ribosomal Proteins Proteins found in ribosomes. They are believed to have a catalytic function in reconstituting biologically active ribosomal subunits. Proteins, Ribosomal,Ribosomal Protein,Protein, Ribosomal
D012270 Ribosomes Multicomponent ribonucleoprotein structures found in the CYTOPLASM of all cells, and in MITOCHONDRIA, and PLASTIDS. They function in PROTEIN BIOSYNTHESIS via GENETIC TRANSLATION. Ribosome
D012333 RNA, Messenger RNA sequences that serve as templates for protein synthesis. Bacterial mRNAs are generally primary transcripts in that they do not require post-transcriptional processing. Eukaryotic mRNA is synthesized in the nucleus and must be exported to the cytoplasm for translation. Most eukaryotic mRNAs have a sequence of polyadenylic acid at the 3' end, referred to as the poly(A) tail. The function of this tail is not known for certain, but it may play a role in the export of mature mRNA from the nucleus as well as in helping stabilize some mRNA molecules by retarding their degradation in the cytoplasm. Messenger RNA,Messenger RNA, Polyadenylated,Poly(A) Tail,Poly(A)+ RNA,Poly(A)+ mRNA,RNA, Messenger, Polyadenylated,RNA, Polyadenylated,mRNA,mRNA, Non-Polyadenylated,mRNA, Polyadenylated,Non-Polyadenylated mRNA,Poly(A) RNA,Polyadenylated mRNA,Non Polyadenylated mRNA,Polyadenylated Messenger RNA,Polyadenylated RNA,RNA, Polyadenylated Messenger,mRNA, Non Polyadenylated
D013091 Spermatogenesis The process of germ cell development in the male from the primordial germ cells, through SPERMATOGONIA; SPERMATOCYTES; SPERMATIDS; to the mature haploid SPERMATOZOA. Spermatocytogenesis,Spermiogenesis

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