Sugar‐inducible expression of the nucleolin‐1 gene of Arabidopsis thaliana and its role in ribosome synthesis, growth and development

Abstract

SummaryAnimal and yeast nucleolin function as global regulators of ribosome synthesis, and their expression is tightly linked to cell proliferation. Although Arabidopsis contains two genes for nucleolin, AtNuc-L1 is the predominant if not only form of the protein found in most tissues, and GFP-AtNuc-L1 fusion proteins were targeted to the nucleolus. Expression of AtNuc-L1 was strongly induced by sucrose or glucose but not by nonmetabolizable mannitol or 2-deoxyglucose. Sucrose also caused enhanced expression of genes for subunits of C/D and H/ACA small nucleolar ribonucleoproteins, as well as a large number of genes for ribosomal proteins (RPs), suggesting that carbohydrate availability regulates de novo ribosome synthesis. In sugar-starved cells, induction of AtNuc-L1 occurred with 10 mM glucose, which seemed to be a prerequisite for resumption of growth. Disruption of AtNuc-L1 caused an increased steady-state level of pre-rRNA relative to mature 25S rRNA, and resulted in various phenotypes that overlap those reported for several RP gene mutants, including a reduced growth rate, prolonged lifetime, bushy growth, pointed leaf, and defective vascular patterns and pod development. These results suggest that the rate of ribosome synthesis in the meristem has a strong impact not only on the growth but also the structure of plants. The AtNuc-L1 disruptant exhibited significantly reduced sugar-induced expression of RP genes, suggesting that AtNuc-L1 is involved in the sugar-inducible expression of RP genes.

Nuclear Ribosome Biogenesis Mediated by the DIM1A rRNA Dimethylase Is Required for Organized Root Growth and Epidermal Patterning in Arabidopsis

“…These phenotypes are similar to ones observed in other Arabidopsis ribosome assembly factor mutants, including nuc-l1/par1 (Kojima et al, 2007;Petricka and Nelson, 2007;Pontvianne et al, 2007), oligocellula2 (Fujikura et al, 2009), and apum23-1 (Abbasi et al, 2010), as well as the phenotypes of Arabidopsis ribosomal protein mutants, including rpl24b/stv1, rpl4a, and rps23a (Nishimura et al, 2005;Degenhardt and Bonham-Smith, 2008;Rosado et al, 2010). Interestingly, we did not detect a difference in leaf cell shape or stomatal development ( Figure 10E) as observed in other ribosomal mutants (Fujikura et al, 2009;Rosado et al, 2010).…”

Pumilio Puf domain RNA-binding proteins in Arabidopsis

“…2). In spite of the phenotypic similarity of apum23 mutant to the "loss of function" mutants of nucleolin 1 (AtNuc-L1) [46][47][48] and ribosomal protein (RP) [49][50][51][52] genes, our microarray data showed the transcriptional upregulation of a portion of the RP genes, although the expression level of the AtNuc-L1 transcript did not change. However, AtNuc-L2, which is not expressed under normal growth conditions in wild-type plants, was greatly upregulated.…”

“…AtNuc-L1 is also required in pre-rRNA processing, similar to APUM23. 46,48 Hence, AtNuc-L2 appears to be upregulated to compensate for the reduced supply rate of rRNA. Upregulation of RP gene expression in the apum23 mutant also may be a feed-back mechanism to compensate either the reduced rate of ribosome assembly or the imbalance of ribosome subunits due to a limited supply of integral rRNAs.…”

Expression of Sucrose Transporter cDNAs Specifically in Companion Cells Enhances Phloem Loading and Long-Distance Transport of Sucrose but Leads to an Inhibition of Growth and the Perception of a Phosphate Limitation

“…In a classic study of barley growing on limiting P supply, about 26% was in free P, 17% was in phospholipids, 26% was in P-containing metabolites, including sugar Ps and nucleotide Ps, and 30% was in nucleic acids (Chapin and Bieleski, 1982). The vast majority of nucleic acids are in ribosomes, which are especially abundant in growing tissues (Detchon and Possingham, 1972;Dean and Leech, 1982;Baerenfaller et al, 2012), where they may represent an even greater proportion of the total P. Suc is known to increase gene expression for nucleotide synthesis and coordinately induce genes for ribosomal proteins and ribosome assembly, especially those for cytosolic ribosomes (Contento et al, 2004;Price et al, 2004;Bläsing et al, 2005;Zrenner et al, 2006;Kojima et al, 2007;Osuna et al, 2007;Usadel et al, 2008;Pal et al, 2013). It is thus plausible that an increased supply of Suc may induce pathways for nucleotide synthesis and ribosome biogenesis, which, in turn, creates an increased demand for P in growing sink tissues.…”