Differential mRNA translation contributes to gene regulation under non‐stress and dehydration stress conditions in <i>Arabidopsis thaliana</i>

Kawaguchi, Riki; Girke, Thomas; Bray, Elizabeth A.; Bailey‐Serres, Julia

doi:10.1111/j.1365-313x.2004.02090.x

Cited by 281 publications

(282 citation statements)

References 59 publications

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“…Selective translation mediated by changes in ribosome preferences may also contribute. This increase in synthesis of ribosomal proteins after UV-B irradiation is not the result of a general stress response in plants, as other abiotic stresses such as dehydration cause the coordinate down-regulation of the translation of the ribosomal protein gene mRNAs in Arabidopsis (Kawaguchi et al, 2004). The phosphorylation status of the S6 ribosomal protein has been implicated as one of the ribosome constituents that modulates translational selectivity (Thomas, 2002).…”

Section: Discussionmentioning

confidence: 99%

Crosslinking of Ribosomal Proteins to RNA in Maize Ribosomes by UV-B and Its Effects on Translation

Casati

Walbot

2004

Plant Physiology

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Ultraviolet-B (UV-B) photons can cause substantial cellular damage in biomolecules, as is well established for DNA. Because RNA has the same absorption spectrum for UV as DNA, we have investigated damage to this cellular constituent. In maize (Zea mays) leaves, UV-B radiation damages ribosomes by crosslinking cytosolic ribosomal proteins S14, L23a, and L32, and chloroplast ribosomal protein L29 to RNA. Ribosomal damage accumulated during a day of UV-B exposure correlated with a progressive decrease in new protein production; however, de novo synthesis of some ribosomal proteins is increased after 6 h of UV-B exposure. After 16 h without UV-B, damaged ribosomes were eliminated and translation was restored to normal levels. Ribosomal protein S6 and an S6 kinase are phosphorylated during UV-B exposure; these modifications are associated with selective translation of some ribosomal proteins after ribosome damage in mammalian fibroblast cells and may be an adaptation in maize. Neither photosynthesis nor pigment levels were affected significantly by UV-B, demonstrating that the treatment applied is not lethal and that maize leaf physiology readily recovers.The evolution of terrestrial life was made possible by formation of a stratosphere that screens solar UV radiation, absorbing UV-C (,280 nm) and the most energetic UV-B (280-315 nm). Recent depletion of stratospheric ozone by chlorofluorocarbons and other pollutants has increased terrestrial UV-B levels with potentially deleterious consequences for all living organisms and particularly for plant development and physiology (Ballaré et al., 2001;Searles et al., 2001;Paul and Gwynn-Jones, 2003). In response to the inevitable exposure to damaging terrestrial UV-B, plants have evolved UV-induced mechanisms of protection and repair, such as accumulation of UVabsorbing pigments and use of UV-A photons to repair UV-B induced DNA damage (Stapleton and Walbot, 1994;Britt, 1996). Because of its absorption spectrum, DNA is a major target of UV-B radiation (Britt, 1996). This radiation can also damage proteins and lipids directly (Gerhardt et al., 1999); RNA molecules strongly absorb UV-B, but less is known about UV-B mediated damage to this cellular constituent.Experimentally, UV has been extensively used to analyze ribosome structure in vitro, because crosslinks can be introduced at points of close contact between proteins, within ribosomal RNA (rRNA), and between proteins and rRNA, tRNA, or mRNA Noah et al., 2000). Furthermore, in vivo crosslinks are generated in rRNA by UV treatment of bacterial cells (Stiege et al., 1986). In mammalian cells, UV-C and UV-B cause specific damage to the 3#-end of the 28S rRNA activating a response called ribotoxic stress (Iordanov et al., 1997(Iordanov et al., , 1998. Protein synthesis in plant cells is also sensitive to UV-C. Murphy et al. (1973) demonstrated that 254 nm radiation disrupted amino acid incorporation into protein in a wheat germ in vitro synthesis reaction and that the most sensitive target was mRNA. Subsequent studies in cult...

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Section: Discussionmentioning

confidence: 99%

Crosslinking of Ribosomal Proteins to RNA in Maize Ribosomes by UV-B and Its Effects on Translation

Casati

Walbot

2004

Plant Physiology

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“…The analysis of the features in mRNA sequences responsible for translational regulation in Arabidopsis showed important determinants in the 5# UTR, although probably other unknown mRNA sequence motifs also contribute to differential mRNA translation in plants (Kawaguchi and Bailey-Serres, 2005). Furthermore, it is well known that the amount of mRNA does not necessarily correlate with the abundance of the protein present in plant cells (Kawaguchi et al, 2004;Branco-Price et al, 2008, Mustroph et al, 2009. The translation process is primarily regulated at the initiation step involving the recruitment of the 43S preinitiation complex to the mRNA (Proud, 2007).…”

Section: Discussionmentioning

confidence: 99%

“…The comparison of total and polysomal mRNA populations showed a significant decrease in polysomal abundance without a concomitant decrease in transcript levels. Transcripts for RPL10A to RPL10C, along with other mRNAs encoding for components of the machinery for the synthesis of cytosolic proteins, show minor changes in transcript accumulation but are decreased in polysomes after hypoxia; this indicates that ribosome biogenesis is restricted under the energy crisis caused by hypoxia and also other stresses such as mild dehydration and Suc starvation (Kawaguchi et al, 2004;Kawaguchi and Bailey-Serres, 2005;BrancoPrice et al, 2008). In conclusion, these observations indicate that RPL10 translation is highly regulated (Branco-Price et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

Plant L10 Ribosomal Proteins Have Different Roles during Development and Translation under Ultraviolet-B Stress

et al. 2010

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(J.B., A.L.B.) Ribosomal protein L10 (RPL10) proteins are ubiquitous in the plant kingdom. Arabidopsis (Arabidopsis thaliana) has three RPL10 genes encoding RPL10A to RPL10C proteins, while two genes are present in the maize (Zea mays) genome (rpl10-1 and rpl10-2). Maize and Arabidopsis RPL10s are tissue-specific and developmentally regulated, showing high levels of expression in tissues with active cell division. Coimmunoprecipitation experiments indicate that RPL10s in Arabidopsis associate with translation proteins, demonstrating that it is a component of the 80S ribosome. Previously, ultraviolet-B (UV-B) exposure was shown to increase the expression of a number of maize ribosomal protein genes, including rpl10. In this work, we demonstrate that maize rpl10 genes are induced by UV-B while Arabidopsis RPL10s are differentially regulated by this radiation: RPL10A is not UV-B regulated, RPL10B is down-regulated, while RPL10C is up-regulated by UV-B in all organs studied. Characterization of Arabidopsis T-DNA insertional mutants indicates that RPL10 genes are not functionally equivalent. rpl10A and rpl10B mutant plants show different phenotypes: knockout rpl10A mutants are lethal, rpl10A heterozygous plants are deficient in translation under UV-B conditions, and knockdown homozygous rpl10B mutants show abnormal growth. Based on the results described here, RPL10 genes are not redundant and participate in development and translation under UV-B stress.

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“…NT, No stress treatment. To isolate polysomal components, detergent-treated extracts were subjected to centrifugation through a 1.75 M Suc cushion, followed by fractionation in a 20% to 60% (w/v) Suc gradient (Kawaguchi et al, 2004;Mustroph et al, 2009). B, Polysome mRNA levels decrease under stress conditions.…”

Section: The Mrnas Of Photosynthetic Genes Remain Polysome Associatedmentioning

confidence: 99%

Posttranscriptional Control of Photosynthetic mRNA Decay under Stress Conditions Requires 3′ and 5′ Untranslated Regions and Correlates with Differential Polysome Association in Rice

et al. 2012

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Abiotic stress, including drought, salinity, and temperature extremes, regulates gene expression at the transcriptional and posttranscriptional levels. Expression profiling of total messenger RNAs (mRNAs) from rice (Oryza sativa) leaves grown under stress conditions revealed that the transcript levels of photosynthetic genes are reduced more rapidly than others, a phenomenon referred to as stress-induced mRNA decay (SMD). By comparing RNA polymerase II engagement with the steady-state mRNA level, we show here that SMD is a posttranscriptional event. The SMD of photosynthetic genes was further verified by measuring the half-lives of the small subunit of Rubisco (RbcS1) and Chlorophyll a/b-Binding Protein1 (Cab1) mRNAs during stress conditions in the presence of the transcription inhibitor cordycepin. To discern any correlation between SMD and the process of translation, changes in total and polysome-associated mRNA levels after stress were measured. Total and polysome-associated mRNA levels of two photosynthetic (RbcS1 and Cab1) and two stress-inducible (Dehydration Stress-Inducible Protein1 and Salt-Induced Protein) genes were found to be markedly similar. This demonstrated the importance of polysome association for transcript stability under stress conditions. Microarray experiments performed on total and polysomal mRNAs indicate that approximately half of all mRNAs that undergo SMD remain polysome associated during stress treatments. To delineate the functional determinant(s) of mRNAs responsible for SMD, the RbcS1 and Cab1 transcripts were dissected into several components. The expressions of different combinations of the mRNA components were analyzed under stress conditions, revealing that both 39 and 59 untranslated regions are necessary for SMD. Our results, therefore, suggest that the posttranscriptional control of photosynthetic mRNA decay under stress conditions requires both 39 and 59 untranslated regions and correlates with differential polysome association.

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Differential mRNA translation contributes to gene regulation under non‐stress and dehydration stress conditions in Arabidopsis thaliana

Cited by 281 publications

References 59 publications

Crosslinking of Ribosomal Proteins to RNA in Maize Ribosomes by UV-B and Its Effects on Translation

Crosslinking of Ribosomal Proteins to RNA in Maize Ribosomes by UV-B and Its Effects on Translation

Plant L10 Ribosomal Proteins Have Different Roles during Development and Translation under Ultraviolet-B Stress

Posttranscriptional Control of Photosynthetic mRNA Decay under Stress Conditions Requires 3′ and 5′ Untranslated Regions and Correlates with Differential Polysome Association in Rice

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