Tudor-SN, a component of stress granules, regulates growth under salt stress by modulating GA20ox3 mRNA levels in Arabidopsis

Yan, Cheng; Yan, Zongyun; Wang, Yizheng; Yan, Xiaowen; Han, Yuzhu

doi:10.1093/jxb/eru334

Cited by 67 publications

(80 citation statements)

References 57 publications

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“…Similar to previous studies of time-resolved SG disassembly in plant tissues recovering from hypoxia (Sorenson and BaileySerres, 2014) and related heat stress (Gutierrez-Beltran et al, 2015), the CML38 foci disassemble upon reoxygenation. Second, MS analysis of immunoprecipitates of CML38 from hypoxic root samples reveals the presence of established SG-associated proteins, including poly(A)-binding protein (Kedersha et al, 2002;Kimball et al, 2003;Sorenson and Bailey-Serres, 2014), eukaryotic initiation factors (Li et al, 2010), eukaryotic elongation factors (Hafrén et al, 2013), RNA helicase (Koroleva et al, 2009), small ribosomal subunit proteins (Kedersha et al, 2002;Sorenson and Bailey-Serres, 2014), and others (Mazroui et al, 2007;Buchan et al, 2013;Yan et al, 2014, GutierrezBeltran et al, 2015. Third, coexpression of the core SG-nucleating RNA-binding protein RBP47 (Weber et al, 2008) with CML38 shows that, under hypoxia conditions, the two proteins colocalize to cytosolic granules.…”

Section: Discussionmentioning

confidence: 99%

Arabidopsis CML38, a Calcium Sensor That Localizes to Ribonucleoprotein Complexes under Hypoxia Stress

et al. 2015

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During waterlogging and the associated oxygen deprivation stress, plants respond by the induction of adaptive programs, including the redirected expression of gene networks toward the synthesis of core hypoxia-response proteins. Among these core response proteins in Arabidopsis (Arabidopsis thaliana) is the calcium sensor CML38, a protein related to regulator of gene silencing calmodulin-like proteins (rgsCaMs). CML38 transcripts are up-regulated more than 300-fold in roots within 6 h of hypoxia treatment. Transfer DNA insertional mutants of CML38 show an enhanced sensitivity to hypoxia stress, with lowered survival and more severe inhibition of root and shoot growth. By using yellow fluorescent protein (YFP) translational fusions, CML38 protein was found to be localized to cytosolic granule structures similar in morphology to hypoxia-induced stress granules. Immunoprecipitation of CML38 from the roots of hypoxia-challenged transgenic plants harboring CML38pro::CML38: YFP followed by liquid chromatography-tandem mass spectrometry analysis revealed the presence of protein targets associated with messenger RNA ribonucleoprotein (mRNP) complexes including stress granules, which are known to accumulate as messenger RNA storage and triage centers during hypoxia. This finding is further supported by the colocalization of CML38 with the mRNP stress granule marker RNA Binding Protein 47 (RBP47) upon cotransfection of Nicotiana benthamiana leaves. Ruthenium Red treatment results in the loss of CML38 signal in cytosolic granules, suggesting that calcium is necessary for stress granule association. These results confirm that CML38 is a core hypoxia response calcium sensor protein and suggest that it serves as a potential calcium signaling target within stress granules and other mRNPs that accumulate during flooding stress responses.

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Section: Discussionmentioning

confidence: 99%

Arabidopsis CML38, a Calcium Sensor That Localizes to Ribonucleoprotein Complexes under Hypoxia Stress

et al. 2015

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“…34 SGs contain translationally repressed mRNA but also eukaryotic translation initiation factor (eiF4G) or Tudor-SN involved in stress adaptation. 35,36 Studies in lupine cells in comparison to A. thaliana allowed better visualization of SGs after the in situ hybridization of poly (A) RNA, including transcripts encoding proteins. We showed that the poly(A) RNA in SG-like structures represented a pool that was not co-localized with ribosomes, which suggests that they do not participate in translation.…”

Section: Discussionmentioning

confidence: 99%

Regulation of poly(A) RNA retention in the nucleus as a survival strategy of plants during hypoxia

2016

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Last finding indicates that post-transcriptional processes are significant in low-oxygen conditions, but their nature is poorly understood. Here, we localized poly(A) RNA and mRNA coding proteins involved and not involved with resistance to hypoxia in Lupinus luteus and Arabidopsis thaliana during submergence and after recovery of aerobic conditions. We showed a strong nuclear accumulation of poly(A) RNA and 6 of 7 studied mRNAs with a concurrent strong reduction in RNA polymerase II transcription during hypoxia. In this study, the nucleus did not accumulate mRNA of the ADH1 (alcohol dehydrogenase 1) gene, which is a core hypoxia gene. The RNA accumulation in the nucleus is among the mechanisms of post-transcriptional gene regulation that prevents translation. However re-aeration was accompanied by a strong increase in the amount of the mRNAs in the cytoplasm and a simultaneous decrease in nuclear mRNAs. This finding indicates that the nucleus is a storage site for those of mRNAs which are not involved in the response to hypoxia for use by the plants after the hypoxic stress. In this study, the highest intensity of RNA accumulation occurred in Cajal bodies (CBs); the intensity of accumulation was inversely correlated with transcription. Under hypoxia, ncb-1 mutants of Arabidopsis thaliana with a complete absence of CBs died sooner than wild type (WT), accompanied by a strong reduction in the level of poly(A) RNA in the nucleus. These results suggest that the CBs not only participate in the storage of the nuclear RNA, but they also could take part in its stabilization under low-oxygen conditions.

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“…22,23 Arabidopsis genome has 2 partly redundant TSN genes (TSN1 and TSN2) which were shown to confer stress tolerance through the stabilization of mRNAs encoding secreted proteins 24 and gibberellin 20-oxidase 3, a key enzyme in gibberellin biosynthesis. 25 Unlike animal TSN, in Arabidopsis TSN1 and TSN2 are exclusively cytoplasmic. 11,26 However, the role of TSN in plants seems to be extended to also encompass an opposite process, viz.…”

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Tudor Staphylococcal Nuclease plays two antagonistic roles in RNA metabolism under stress

Gutiérrez-Beltrán

Bozhkov

Moschou

2015

Plant Signaling & Behavior

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Tudor-SN, a component of stress granules, regulates growth under salt stress by modulating GA20ox3 mRNA levels in Arabidopsis

Abstract: SummaryTudor-SN protein accumulates in stress granules in response to salt stress in Arabidopsis. It binds GA20ox3 mRNA in vivo and up-regulates GA20ox3 levels to maintain plant growth under salt stress.

Cited by 67 publications

References 57 publications

Arabidopsis CML38, a Calcium Sensor That Localizes to Ribonucleoprotein Complexes under Hypoxia Stress

Arabidopsis CML38, a Calcium Sensor That Localizes to Ribonucleoprotein Complexes under Hypoxia Stress

Regulation of poly(A) RNA retention in the nucleus as a survival strategy of plants during hypoxia

Tudor Staphylococcal Nuclease plays two antagonistic roles in RNA metabolism under stress

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