Open AccessSpecialized eRpL22 paralogue-specific ribosomes regulate specific mRNA translation in spermatogenesis inDrosophila melanogaster
Author(s) -
Catherine M. Mageeney,
Vassie C. Ware
Publication year - 2019
Publication title -
molecular biology of the cell
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 2.463
H-Index - 225
eISSN - 1939-4586
pISSN - 1059-1524
DOI - 10.1091/mbc.e19-02-0086
Subject(s) - biology , polysome , translation (biology) , ribosome , germline , drosophila melanogaster , microbiology and biotechnology , genetics , messenger rna , protein biosynthesis , ribosomal rna , rna , gene
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.