Trends in Plant Science
Volume 14, Issue 9, September 2009, Pages 512-519
Journal home page for Trends in Plant Science

Review
A role for the ribosome in development

https://doi.org/10.1016/j.tplants.2009.06.009Get rights and content

Development of a multicellular organism involves coordinated cell division, growth and specialization to generate different cell types that contribute to organized tissues, distinct organs and a higher order body plan. This coordinated process requires tight regulation of gene expression, which is mediated by multiple transcriptional, post-transcriptional, translational and post-translational control mechanisms. As I discuss here, recent studies on ribosomal protein genes and ribosome assembly genes indicate that the basic translational machinery of the cell, the ribosome, has a regulatory role in plant development. A comparison between plants and animals reveals both divergent trends in the genome content of ribosomal proteins and intriguing potential overlaps in the role of the ribosome in development.

Section snippets

The eukaryotic ribosome

Ribosomes are ribonucleoprotein complexes comprising a large and a small subunit. In eukaryotes, the large subunit is composed of 25–28S, 5.8S and 5S rRNA together with ∼47 ribosomal proteins, whereas the small subunit is composed of 18S rRNA and ∼33 ribosomal proteins (reviewed in Ref. [1]). Ribosomes are responsible for translating mRNA into protein and, as such, are generally perceived as the housekeeping components of the cell, with a non-selective role in polypeptide synthesis. However, in

Ribosomal protein genes in Arabidopsis

In plants, ribosomal proteins are encoded by small gene families. Arabidopsis thaliana has 80 cytoplasmic ribosomal proteins, each encoded by two to seven family members, with different genes within a family sharing between 65% and 100% amino acid sequence identity [2]. The occurrence of multiple copies of each ribosomal protein gene might be, in part, a consequence of ancient polyploidization events and could reflect a need to retain stoichiometric levels of ribosomal proteins that make up the

Developmental phenotypes of Arabidopsis ribosomal protein mutants

The presence of multiple gene families for each ribosomal protein in plants might be necessary to maintain equivalent ribosomal protein doses or there might be some degree of ribosome heterogeneity and functional specialization. Mutations in ribosomal protein genes in Arabidopsis have not differentiated fully between these possibilities. However, phenotypes resulting from mutations in several different ribosomal protein genes provide strong evidence that ribosomes participate as regulatory

Mutations affecting ribosome biogenesis

Ribosome biogenesis occurs largely in the nucleolus (Figure 2). In addition to rRNA and ribosomal proteins, the nucleolus contains many non-ribosomal RNAs and proteins that contribute to ribosome production. In Arabidopsis, two genes, OLIGOCELLULA2 (OLI2) and AtNUC-L1/PARALELL1 (PARL1), which are potentially required for ribosome biogenesis, have roles in development that overlap with those of the ribosomal proteins. OLI2 encodes a Nop2 protein, which is a predicted RNA methyltransferase

Differences and parallels between plants and animals

In contrast with plants, most ribosomal proteins in animals are encoded by single-copy genes. Also unlike plants, which have few ribosomal protein pseudogenes, mammalian genomes have a large number of ribosomal protein pseudogenes, from 1800 in humans to 2000 in mice [64 65]. Comparative studies suggest that these ribosomal protein pseudogenes are relatively recent in origin 64, 65. Although some ribosomal protein pseudogenes are expressed, the significance of the greatly amplified copy number

Prospects

There remain many questions about the role of the ribosome in the development of multicellular eukaryotes, including establishing the influence of ribosome dose on development, the extent and functional significance of ribosome heterogeneity, the means of coordinating rRNA synthesis with ribosomal protein function and determining targets of selective ribosome function. Developmental phenotypes could involve sensitivity of some transcripts to ribosome levels or to ribosome heterogeneity

Acknowledgements

I thank Lars Ostergaard, Robert Sablowski and anonymous reviewers for valuable comments on the manuscript. I also thank Colleen Sweeney and David Meinke in the Department of Botany, Oklahoma State University, Stillwater, Oklahoma, USA for providing Nomarski images in Figure 1. This work was supported by grants from the Biotechnological and Biological Sciences Research Council (BBSRC) to M.E.B.

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