Stability of plant mRNAs depends on the length of the 3′-untranslated region

Abstract

Eukaryotic mRNAs that prematurely terminate translation are recognized and degraded by nonsense mediated decay (NMD). This degradation pathway is well studied in animal and yeast cells. The data available imply that NMD also takes place in plants. However, the molecular mechanism of recognition and degradation of plant RNAs containing premature terminator codon (PTC) is not known. Here we report that in plant cells this mechanism involves the recognition of the sizes of the 3'-untranslated regions (3'UTR). Plant 3'UTRs longer than 300 nucleotides induce mRNA instability. Contrary to mammalian and yeast cells, this destabilization does not depend on the presence of any specific sequences downstream of the terminator codon. Unlike nuclear-produced mRNAs, plant virus vector long 3'UTR-containing RNAs, which are synthesized directly in the cytoplasm, are stable and translated efficiently. This shows that RNAs produced in the cytoplasm by viral RNA-dependent RNA polymerase are able to avoid the proposed mechanism.

Aberrant mRNA Transcripts and the Nonsense-Mediated Decay Proteins UPF2 and UPF3 Are Enriched in theArabidopsisNucleolus

“…The mechanisms of PTC recognition vary among different species but can be summarized as relying on signals downstream of the PTC and, in particular 39 UTRs and associated proteins, or being splicing and EJC dependent (Bü hler et al, 2004(Bü hler et al, , 2006Amrani et al, 2006;Rehwinkel et al, 2006;Behm-Ansmant et al, 2007aChang et al, 2007;Isken and Maquat, 2007;Shyu et al, 2008;Stalder and Mü hlemann, 2008). In plants, NMD is also triggered by the distance between the PTC and 39 UTR (long 39 UTRs) and/or the presence of a downstream exon-exon junction (intron-based NMD) (Kerté sz et al, 2006;Schwartz et al, 2006;Hori and Watanabe, 2007;Keré nyi et al, 2008). These features are evident not only in NMD-sensitive protein-coding gene transcripts, but also in mRNA-like noncoding RNAs, which are also turned over by NMD in Arabidopsis (Kurihara et al, 2009).…”

“…By identifying the presence and position of premature termination codons (PTCs), 91% of the aberrantly spliced transcripts were found to be putative NMD substrates on the basis of current models of long 39 untranslated region (UTR)-and intron-based PTC recognition in plants (Kerté sz et al, 2006;Schwartz et al, 2006;Hori and Watanabe, 2007;Keré nyi et al, 2008) (Figure 3B; see Supplemental Table 1 online). All had an increased distance between the PTC and 39 UTR, and two-thirds also contained one or more splice junctions (and therefore EJCs) downstream of the PTC (Figures 2 and 3B).…”

Upf1 stimulates degradation of the product derived from aberrant messenger RNA containing a specific nonsense mutation by the proteasome

“…Drosophila melanogaster, Caenorhabditis elegans and plant cells (Kertesz et al, 2006;Schwartz et al, 2006;Behm-Ansmant et al, 2007;Longman et al, 2007), although not all mRNAs with an extended 3 0 -UTR are subjected to NMD. The poly(A)-binding protein 1 (Pab1) interacts with the translation termination factor, eukaryotic release factor 3, to enhance normal termination efficiency (Cosson et al, 2002;Uchida et al, 2002).…”

Expression Patterns of Convergently Overlapping Arabidopsis Thaliana Gene Pairs OHP-NDP1 and OHP2-MES14

“…Their 3'UTRs do not reach the length (>300 nt) documented to induce mRNA instability (Schwartz et al, 2006) and they do not contain the AU-rich sites for ARE-binding proteins that also influence mRNA stability (Barreau et al, 2005). The more likely roles played by overlapping 3'UTRs with APA sites include induction of ribosome binding and translation by 3'UTR shortening, as hypothesized by Andreassi and Riccio (2009).…”