Differential contributions of ribosomal protein genes to Arabidopsis thaliana leaf development

Abstract

SUMMARYIn Arabidopsis thaliana, mutations in genes encoding ribosomal proteins (r-proteins) perturb various developmental processes. Whether these perturbations are caused by overall ribosome insufficiency or partial dysfunction of the ribosome caused by deficiency of a particular ribosomal protein is not known. To distinguish these possibilities, a comparative study using several r-protein mutants was required. Here, we identified mutations in 11 r-protein genes from previously isolated denticulata and pointed-leaves mutants. Most of these mutations were associated with pointed leaves, with reduced growth due to a decrease in the number or size of palisade mesophyll and pavement cells. In addition, leaf abaxialization was usually observed when these r-protein mutations were combined with asymmetric leaves1 (as1) and as2 mutations. These results suggest that the establishment of leaf polarity is highly sensitive to ribosome functionality in general. However, several r-protein mutants showed a preference towards a specific developmental defect. For example, rpl4d mutations did not affect cell proliferation but caused strong abaxialization of leaves in the as1 and as2 backgrounds. On the other hand, rps28b enhanced leaf abaxialization of as2 to a weaker extent than expected on the basis of its negative effect on cell proliferation. In addition, hypomorphic rps6a alleles had the strongest effects on most of the phenotypes examined. These findings suggest that deficiencies in these three r-protein genes lead to production of dysfunctional ribosomes. Depending on their structural abnormalities, dysfunctional ribosomes may affect translation of specific transcripts involved in the regulation of some leaf developmental processes.

atBRX1-1 and atBRX1-2 are involved in an alternative rRNA processing pathway in Arabidopsis thaliana

“…Interestingly, brx1-2 showed a slight pointed leaf phenotype (Fig. 3G) that has previously been observed in ribosomal proteins mutants (Byrne 2009;Horiguchi et al 2011). Development of all following rosette leaves as well as flowering was also more delayed in brx1-2 than in brx1-1.…”

“…3G) was previously observed for many RP mutants (Byrne 2009;Horiguchi et al 2011) and a delay in early growth and development was shown for multiple RBF mutants (Pontvianne et al 2007;Lange et al 2011;Weis et al 2014). These observations imply that ribosome biogenesis, in general, is closely coupled to early plant development, likely due to the high demand for newly synthesized ribosomes in this growth phase.…”

New Evidence for Differential Roles of L10 Ribosomal Proteins from Arabidopsis

“…Furthermore, it has been recently demonstrated that ribosomal proteins control auxinmediated developmental programs by translational regulation of auxin response factors (Rosado et al, 2012). In addition, the characterization of single, double, and, in certain cases, triple mutants as well as complementation by paralog genes have demonstrated full, partial, and no redundancy between members of ribosomal protein families (Briggs et al, 2006;Guo and Chen, 2008;Guo et al, 2011;Horiguchi et al, 2011;Stirnberg et al, 2012).…”

“…In this way, ribosomal heterogeneity would allow selective translation of specific mRNAs under particular cell conditions (Barakat et al, 2001;Szick-Miranda and BaileySerres, 2001;Giavalisco et al, 2005;Carroll et al, 2008;Carroll, 2013). Arabidopsis mutants in ribosomal proteins exhibit a large range of developmental phenotypes with extreme abnormalities, including embryonic lethality, suggesting that ribosomes also have specific functions regulating the expression of developmental genes (Van Lijsebettens et al, 1994;Degenhardt and Bonham-Smith, 2008;Byrne, 2009;Horiguchi et al, 2011Horiguchi et al, , 2012Szakonyi and Byrne, 2011). Furthermore, it has been recently demonstrated that ribosomal proteins control auxinmediated developmental programs by translational regulation of auxin response factors (Rosado et al, 2012).…”

Expression of rice <i>45S rRNA</i> promotes cell proliferation, leading to enhancement of growth in transgenic tobacco

“…However, the detailed mechanism underlying the determination of final leaf size has yet to be elucidated. Several Arabidopsis mutants for ribosomal protein genes have shown developmental changes in leaf size (Byrne 2009;Fujikura et al 2009;Horiguchi et al 2011;Horiguchi et al 2012;Ito et al 2000;Rosado et al 2012;Van Lijsebettens et al 1994;Zsogon et al 2014). Thus, some ribosome-related process might be involved in the co-ordination of cell-proliferation and cell-expansion in the leaf development.…”