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Ribosome heterogeneity and specialization in development

Advanced Review

Karl Norris, Tayah Hopes, Julie Louise Aspden

Published Online: Feb 10 2021

DOI: 10.1002/wrna.1644

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Abstract Regulation of protein synthesis is a vital step in controlling gene expression, especially during development. Over the last 10 years, it has become clear that rather than being homogeneous machines responsible for mRNA translation, ribosomes are highly heterogeneous and can play an active part in translational regulation. These “specialized ribosomes” comprise of specific protein and/or rRNA components, which are required for the translation of particular mRNAs. However, while there is extensive evidence for ribosome heterogeneity, support for specialized functions is limited. Recent work in a variety of developmental model organisms has shed some light on the biological relevance of ribosome heterogeneity. Tissue‐specific expression of ribosomal components along with phenotypic analysis of ribosomal gene mutations indicate that ribosome heterogeneity and potentially specialization are common in key development processes like embryogenesis, spermatogenesis, oogenesis, body patterning, and neurogenesis. Several examples of ribosome specialization have now been proposed but strong links between ribosome heterogeneity, translation of specific mRNAs by defined mechanisms, and role of these translation events remain elusive. Furthermore, several studies have indicated that heterogeneous ribosome populations are a product of tissue‐specific expression rather than specialized function and that ribosomal protein phenotypes are the result of extra‐ribosomal function or overall reduced ribosome levels. Many important questions still need to be addressed in order to determine the functional importance of ribosome heterogeneity to development and disease, which is likely to vary across systems. It will be essential to dissect these issues to fully understand diseases caused by disruptions to ribosomal composition, such as ribosomopathies. This article is categorized under: Translation > Translation Regulation Translation > Ribosome Structure/Function RNA in Disease and Development > RNA in Development

Timeline of our understanding of specialized ribosomes. The theory of specialized ribosomes initially started back in 1950s but in the last 10 years more evidence and examples have been characterized

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Significant phenotypes of Arabidopsis thaliana ribosomal protein (RP) mutants. Defects in leaf morphology are common, including reduced tissue complexity (vasculature and photosynthetic cells) and polarity defects in the asymmetric leaves1 (as1) and as2 backgrounds (abaxialization; where the upper side of the leaf has the morphology of the underside of the leaf). Aberrant cell fate specification has also been observed in the female gametophyte (gynocium) and during development of the embryo (suspensor)

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Role of ribosome heterogeneity in gametogenesis. Schematic diagram highlighting the potential roles of ribosome heterogeneity in oocyte development (Drosophila melanogaster) and sperm cell development (D. melanogaster, Mus musculus) from studies using different model organisms

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Mechanisms of translation initiation and regulation. Schematic depiction of how specialized ribosomes could mechanistically affect translation

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Types of ribosome heterogeneity. Schematic illustrating the six different ways ribosome heterogeneity has been found to occur

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