The Minimum Open Reading Frame, AUG-Stop, Induces Boron-Dependent Ribosome Stalling and mRNA Degradation

Tanaka, Mieko; Sotta, Naoyuki; Yamazumi, Yusuke; Yamashita, Yoshihisa; Miwa, Kyoko; Murota, Katsunori; Chiba, Yasuhiro; Hirai, Masami Yokota; Akiyama, Tetsu; Onouchi, Hitoshi; Naito, Shuichi; Fujiwara, Toru

doi:10.1105/tpc.16.00481

Cited by 120 publications

(145 citation statements)

References 70 publications

(97 reference statements)

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“…NIP55;1 encodes a boric acid channel that is required for efficient boron uptake by roots and is essential for growth under low‐boron conditions (Takano et al ., ). NIP5;1 carries two minimal uORFs (AUG‐Stop: AUGUAA) in its 5′ UTR that are responsible for the translational regulation of the mORF in a boron‐dependent manner (Tanaka et al ., ). Under high‐boron conditions, ribosomes stall at the AUG‐Stop sites inhibiting translation, with each of the two minimal uORFs being sufficient for this inhibition.…”

Section: Gene‐specific Translation Regulationmentioning

confidence: 97%

Translation regulation in plants: an interesting past, an exciting present and a promising future

2017

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SUMMARYChanges in gene expression are at the core of most biological processes, from cell differentiation to organ development, including the adaptation of the whole organism to the ever-changing environment. Although the central role of transcriptional regulation is solidly established and the general mechanisms involved in this type of regulation are relatively well understood, it is clear that regulation at a translational level also plays an essential role in modulating gene expression. Despite the large number of examples illustrating the critical role played by translational regulation in determining the expression levels of a gene, our understanding of the molecular mechanisms behind such types of regulation has been slow to emerge. With the recent development of high-throughput approaches to map and quantify different critical parameters affecting translation, such as RNA structure, protein-RNA interactions and ribosome occupancy at the genome level, a renewed enthusiasm toward studying translation regulation is warranted. The use of these new powerful technologies in well-established and uncharacterized translation-dependent processes holds the promise to decipher the likely complex and diverse, but also fascinating, mechanisms behind the regulation of translation.

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Section: Gene‐specific Translation Regulationmentioning

confidence: 97%

Translation regulation in plants: an interesting past, an exciting present and a promising future

2017

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“…Examination of 35 S‐Met/Cys incorporation after growth at high boron concentration showed a notable reduction in all gcn1 alleles examined ( gcn1 ‐ 3 , gcn1 ‐ 6 , and gcn1 ‐ 5 ) relative to wild type plants (Figure c). On the basis of the action of high boron concentration as a protein synthesis inhibitor (Tanaka et al, ; Uluisik et al, ), the lower 35 S‐Met/Cys incorporation in gcn1 alleles reflects a defect in translation regulation.…”

Section: Resultsmentioning

confidence: 99%

Arabidopsis nonresponding to oxylipins locus NOXY7 encodes a yeast GCN1 homolog that mediates noncanonical translation regulation and stress adaptation

Izquierdo

Kulasekaran

Benito

et al. 2018

Plant Cell & Environment

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Stress adaptation and translational regulation was studied using noxy7 (nonresponding to oxylipins7) from a series of Arabidopsis thaliana mutants. We identified the noxy7 mutation in At1g64790, which encodes a homolog of the yeast translational regulator General Control Nonderepressible1 (GCN1) that activates the GCN2 kinase; GCN2 in turn phosphorylates the α subunit of the translation initiation factor eIF2. This regulatory circuit is conserved in yeast and mammals, in which phosphorylated eIF2α (P-eIF2α) facilitates stress adaptation by inhibiting protein synthesis. In phenotypic and de novo protein synthesis studies with Arabidopsis mutants, we found that NOXY7/GCN1 and GCN2 mediate P-eIF2α formation and adaptation to amino acid deprivation; however, P-eIF2α formation is not linked to general protein synthesis arrest. Additional evidence suggested that NOXY7/GCN1 but not GCN2 regulates adaptation to mitochondrial dysfunction, high boron concentration, and activation of plant immunity to infection by Pseudomonas syringae pv tomato (Pst). In these responses, NOXY7/GCN1 acts with GCN20 to regulate translation in a noncanonical pathway independently of GCN2 and P-eIF2α. These results show the lesser functional relevance of GCN2 and P-eIF2α in plants relative to other eukaryotes and highlight the prominent role of NOXY7/GCN1 and GCN20 in regulation of translation and stress adaptation in plants.

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“…High B conditions enhance ribosome stalling at the minimum open reading frame, AUG‐stop, in the 5′UTR, while suppressing translation and inducing the degradation of NIP5 ; 1 mRNA (Tanaka et al ., ). This response is reportedly important for plant acclimation to high B conditions (Tanaka et al ., , ).…”

Section: Introductionmentioning

confidence: 97%

Establishment of genetically encoded biosensors for cytosolic boric acid in plant cells

et al. 2018

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Boron (B) is an essential micronutrient for plants. To maintain B concentration in tissues at appropriate levels, plants use boric acid channels belonging to the NIP subfamily of aquaporins and BOR borate exporters. To regulate B transport, these transporters exhibit different cell-type specific expression, polar localization, and B-dependent post-transcriptional regulation. Here, we describe the development of genetically encoded biosensors for cytosolic boric acid to visualize the spatial distribution and temporal dynamics of B in plant tissues. The biosensors were designed based on the function of the NIP5;1 5'-untranslated region (UTR), which promotes mRNA degradation in response to an elevated cytosolic boric acid concentration. The signal intensities of the biosensor coupled with Venus fluorescent protein and a nuclear localization signal (uNIP5;1-Venus) showed negative correlation with intracellular B concentrations in cultured tobacco BY-2 cells. When expressed in Arabidopsis thaliana, uNIP5;1-Venus enabled the quantification of B distribution in roots at single-cell resolution. In mature roots, cytosolic B levels in stele were maintained under low B supply, while those in epidermal, cortical, and endodermal cells were influenced by external B concentrations. Another biosensor coupled with a luciferase protein fused to a destabilization PEST sequence (uNIP5;1-Luc) was used to visualize changes in cytosolic boric acid concentrations. Thus, uNIP5;1-Venus/Luc enables visualization of B transport in various plant cells/tissues.

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The Minimum Open Reading Frame, AUG-Stop, Induces Boron-Dependent Ribosome Stalling and mRNA Degradation

Cited by 120 publications

References 70 publications

Translation regulation in plants: an interesting past, an exciting present and a promising future

Translation regulation in plants: an interesting past, an exciting present and a promising future

Arabidopsis nonresponding to oxylipins locus NOXY7 encodes a yeast GCN1 homolog that mediates noncanonical translation regulation and stress adaptation

Establishment of genetically encoded biosensors for cytosolic boric acid in plant cells

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