Transcriptomics of cryophilic Saccharomyces kudriavzevii reveals the key role of gene translation efficiency in cold stress adaptations

Long non-coding RNAs (lncRNAs) have been considered to be important regulators of gene expression in a range of biological processes in plants. A large number of lncRNAs have been identified in plants. However, most of their biological functions still remain to be determined. Here, we identified total 3 004 lncRNAs in cassava under normal or cold-treated conditions from Iso-seq data. We further characterized a lincRNA, CRIR1, as a novel positive regulator of the plant response to cold stress. CRIR1 can be significantly induced by cold treatment. Overexpression of CRIR1 in cassava enhanced the cold tolerance of transgenic plants. Transcriptome analysis demonstrated that CRIR1 regulates a range of cold stress-related genes in a CBF-independent pathway. We further found that CRIR1 RNA can interact with MeCSP5, a homolog of the cold shock protein that acts as RNA chaperones, indicating that CRIR1 may recruit MeCSP5 to improve the translation efficiency of mRNA. In summary, our study greatly extends the repertoire of lncRNAs in plants as well as its responding to cold stress. Moreover, it reveals a sophisticated mechanism by which CRIR1 regulates plant cold stress response by modulating the expression of stress-responsive genes and increasing the translational yield.

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Arabidopsis Disulfide Reductase, Trx-h2, Functions as an RNA Chaperone under Cold Stress

Applied Sciences ◽

10.3390/app11156865 ◽

2021 ◽

Vol 11 (15) ◽

pp. 6865

Author(s):

Eun Seon Lee ◽

Joung Hun Park ◽

Seong Dong Wi ◽

Ho Byoung Chae ◽

Seol Ki Paeng ◽

...

Keyword(s):

Cold Stress ◽

Wild Type ◽

Rna Chaperone ◽

E Coli ◽

Cold Sensitive ◽

Thioredoxin H ◽

Functional Rnas

The thioredoxin-h (Trx-h) family of Arabidopsis thaliana comprises cytosolic disulfide reductases. However, the physiological function of Trx-h2, which contains an additional 19 amino acids at its N-terminus, remains unclear. In this study, we investigated the molecular function of Trx-h2 both in vitro and in vivo and found that Arabidopsis Trx-h2 overexpression (Trx-h2OE) lines showed significantly longer roots than wild-type plants under cold stress. Therefore, we further investigated the role of Trx-h2 under cold stress. Our results revealed that Trx-h2 functions as an RNA chaperone by melting misfolded and non-functional RNAs, and by facilitating their correct folding into active forms with native conformation. We showed that Trx-h2 binds to and efficiently melts nucleic acids (ssDNA, dsDNA, and RNA), and facilitates the export of mRNAs from the nucleus to the cytoplasm under cold stress. Moreover, overexpression of Trx-h2 increased the survival rate of the cold-sensitive E. coli BX04 cells under low temperature. Thus, our data show that Trx-h2 performs function as an RNA chaperone under cold stress, thus increasing plant cold tolerance.

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Loss of Ftsj1 perturbs codon-specific translation efficiency in the brain and is associated with X-linked intellectual disability

Science Advances ◽

10.1126/sciadv.abf3072 ◽

2021 ◽

Vol 7 (13) ◽

pp. eabf3072

Author(s):

Y. Nagayoshi ◽

T. Chujo ◽

S. Hirata ◽

H. Nakatsuka ◽

C.-W. Chen ◽

...

Keyword(s):

Intellectual Disability ◽

State Level ◽

Memory Deficits ◽

Ribosome Profiling ◽

Translation Efficiency ◽

Trna Modification ◽

Synaptic Organization ◽

Transfer Rnas ◽

The Brain

FtsJ RNA 2′-O-methyltransferase 1 (FTSJ1) gene has been implicated in X-linked intellectual disability (XLID), but the molecular pathogenesis is unknown. We show that Ftsj1 is responsible for 2′-O-methylation of 11 species of cytosolic transfer RNAs (tRNAs) at the anticodon region, and these modifications are abolished in Ftsj1 knockout (KO) mice and XLID patient–derived cells. Loss of 2′-O-methylation in Ftsj1 KO mouse selectively reduced the steady-state level of tRNAPhe in the brain, resulting in a slow decoding at Phe codons. Ribosome profiling showed that translation efficiency is significantly reduced in a subset of genes that need to be efficiently translated to support synaptic organization and functions. Ftsj1 KO mice display immature synaptic morphology and aberrant synaptic plasticity, which are associated with anxiety-like and memory deficits. The data illuminate a fundamental role of tRNA modification in the brain through regulation of translation efficiency and provide mechanistic insights into FTSJ1-related XLID.

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The AaCBF4-AaBAM3.1 module enhances freezing tolerance of kiwifruit (Actinidia arguta)

Horticulture Research ◽

10.1038/s41438-021-00530-1 ◽

2021 ◽

Vol 8 (1) ◽

Author(s):

Shihang Sun ◽

Chungen Hu ◽

Xiujuan Qi ◽

Jinyong Chen ◽

Yunpeng Zhong ◽

...

Keyword(s):

Cold Stress ◽

Freezing Tolerance ◽

Luciferase Reporter ◽

Dna Interactions ◽

Functional Protein ◽

Actinidia Arguta ◽

Protein Dna Interactions ◽

Similar Phenotype ◽

Reporter Assays

AbstractBeta-amylase (BAM) plays an important role in plant resistance to cold stress. However, the specific role of the BAM gene in freezing tolerance is poorly understood. In this study, we demonstrated that a cold-responsive gene module was involved in the freezing tolerance of kiwifruit. In this module, the expression of AaBAM3.1, which encodes a functional protein, was induced by cold stress. AaBAM3.1-overexpressing kiwifruit lines showed increased freezing tolerance, and the heterologous overexpression of AaBAM3.1 in Arabidopsis thaliana resulted in a similar phenotype. The results of promoter GUS activity and cis-element analyses predicted AaCBF4 to be an upstream transcription factor that could regulate AaBAM3.1 expression. Further investigation of protein-DNA interactions by using yeast one-hybrid, GUS coexpression, and dual luciferase reporter assays confirmed that AaCBF4 directly regulated AaBAM3.1 expression. In addition, the expression of both AaBAM3.1 and AaCBF4 in kiwifruit responded positively to cold stress. Hence, we conclude that the AaCBF-AaBAM module is involved in the positive regulation of the freezing tolerance of kiwifruit.

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GRAS-domain transcription factor PAT1 regulates jasmonic acid biosynthesis in grape cold stress response

Plant Physiology ◽

10.1093/plphys/kiab142 ◽

2021 ◽

Author(s):

Zemin Wang ◽

Darren Chern Jan Wong ◽

Yi Wang ◽

Guangzhao Xu ◽

Chong Ren ◽

...

Keyword(s):

Stress Response ◽

Cold Stress ◽

Cold Tolerance ◽

Cold Treatment ◽

Ectopic Expression ◽

Bimolecular Fluorescence Complementation ◽

Luciferase Reporter ◽

Vitis Amurensis ◽

Mobility Shift

Abstract Cultivated grapevine (Vitis) is a highly valued horticultural crop, and cold stress affects its growth and productivity. Wild Amur grape (Vitis amurensis) PAT1 (Phytochrome A signal transduction 1, VaPAT1) is induced by low temperature, and ectopic expression of VaPAT1 enhances cold tolerance in Arabidopsis (Arabidopsis thaliana). However, little is known about the molecular mechanism of VaPAT1 during the cold stress response in grapevine. Here, we confirmed the overexpression of VaPAT1 in transformed grape calli enhanced cold tolerance. Yeast two-hybrid and bimolecular fluorescence complementation assays highlighted an interaction between VaPAT1 with INDETERMINATE-DOMAIN 3 (VaIDD3). A role of VaIDD3 in cold tolerance was also indicated. Transcriptome analysis revealed VaPAT1 and VaIDD3 overexpression and cold treatment coordinately modulate the expression of stress-related genes including lipoxygenase 3 (LOX3), a gene encoding a key jasmonate biosynthesis enzyme. Co-expression network analysis indicated LOX3 might be a downstream target of VaPAT1. Both electrophoretic mobility shift and dual luciferase reporter assays showed the VaPAT1-IDD3 complex binds to the IDD-box (AGACAAA) in the VaLOX3 promoter to activate its expression. Overexpression of both VaPAT1 and VaIDD3 increased the transcription of VaLOX3 and JA levels in transgenic grape calli. Conversely, VaPAT1-SRDX (dominant repression) and CRISPR/Cas9-mediated mutagenesis of PAT1-ED causing the loss of the C-terminus in grape calli dramatically prohibited the accumulation of VaLOX3 and JA levels during cold treatment. Together, these findings point to a pivotal role of VaPAT1 in the cold stress response in grape by regulating JA biosynthesis.

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The role of Pro-P5C Cycle in chs mutants of Arabidopsis under cold stress

Russian Journal of Plant Physiology ◽

10.1134/s1021443713020106 ◽

2013 ◽

Vol 60 (3) ◽

pp. 375-382 ◽

Cited By ~ 5

Author(s):

R. A. Khavari-Nejad ◽

R. Shekaste Band ◽

F. Najafi ◽

M. Nabiuni ◽

Z. Gharari

Keyword(s):

Cold Stress

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SIRT7 is a deacetylase of N4-acetylcytidine on ribosomal RNA

Genome Instability & Disease ◽

10.1007/s42764-021-00046-x ◽

2021 ◽

Author(s):

Chenzhong Xu ◽

Jin Zhang ◽

Jie Zhang ◽

Baohua Liu

Keyword(s):

Circadian Rhythms ◽

Ribosomal Rna ◽

Genome Stability ◽

Rna Stability ◽

Translation Efficiency ◽

Dependent Protein ◽

First Time ◽

Protein Deacetylase

AbstractN-acetyltransferase 10 catalyzes RNA N4-acetylcytidine (ac4C) modifications and thus regulates RNA stability and translation efficiency. However, the deacetylase for ac4C is unknown. SIRT7 was initially identified as an NAD+-dependent protein deacetylase and plays essential roles in genome stability, circadian rhythms, metabolism, and aging. In this study, we identified SIRT7 as a deacetylase of the ac4C of ribosomal (r)RNA for the first time and found it to be NAD+-independent. Our data highlight the important role of SIRT7 in rRNA ac4C modification and suggest an additional epitranscriptional regulation of aging.

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Duck Hepatitis A Virus Type 1 Induces eIF2α Phosphorylation-Dependent Cellular Translation Shutoff via PERK/GCN2

Frontiers in Microbiology ◽

10.3389/fmicb.2021.624540 ◽

2021 ◽

Vol 12 ◽

Author(s):

Yuanzhi Liu ◽

Anchun Cheng ◽

Mingshu Wang ◽

Sai Mao ◽

Xumin Ou ◽

...

Keyword(s):

Virus Type ◽

Hepatitis A ◽

Hepatitis A Virus ◽

Translation Efficiency ◽

Eif2α Phosphorylation ◽

Duck Hepatitis ◽

Cellular Translation ◽

First Time

Duck hepatitis A virus type 1 (DHAV-1) is one of the most deadly pathogens that endanger the duck industry. Most viruses usually turn off host translation after infection to facilitate viral replication and translation. For the first time report to our knowledge, DHAV-1 can induce eIF2α phosphorylation and inhibit cellular translation in duck embryo fibroblasts (DEFs). Moreover, the activity of DHAV-1 in the cells caused obvious eIF2α phosphorylation, which has nothing to do with the viral protein. Subsequently, we screened two kinases (PERK and GCN2) that affect eIF2α phosphorylation through inhibitors and shRNA. Notably, the role of GCN2 in other picornaviruses has not been reported. In addition, when the phosphorylation of eIF2α induced by DHAV-1 is inhibited, the translation efficiency of DEFs restores to a normal level, indicating that DHAV-1 induced cellular translation shutoff is dependent on eIF2α phosphorylation.

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Seeking a Role for Translational Control by Alternative Polyadenylation in Saccharomyces cerevisiae

Microorganisms ◽

10.3390/microorganisms9091885 ◽

2021 ◽

Vol 9 (9) ◽

pp. 1885

Author(s):

Rachael E. Turner ◽

Traude H. Beilharz

Keyword(s):

Saccharomyces Cerevisiae ◽

Translational Control ◽

Model Organism ◽

Alternative Polyadenylation ◽

Ribosome Profiling ◽

Translation Efficiency ◽

Mrna Isoforms ◽

Cleavage And Polyadenylation ◽

Made In

Alternative polyadenylation (APA) represents an important mechanism for regulating isoform-specific translation efficiency, stability, and localisation. Though some progress has been made in understanding its consequences in metazoans, the role of APA in the model organism Saccharomyces cerevisiae remains a relative mystery because, despite abundant studies on the translational state of mRNA, none differentiate mRNA isoforms’ alternative 3′-end. This review discusses the implications of alternative polyadenylation in S. cerevisiae using other organisms to draw inferences. Given the foundational role that research in this yeast has played in the discovery of the mechanisms of cleavage and polyadenylation and in the drivers of APA, it is surprising that such an inference is required. However, because advances in ribosome profiling are insensitive to APA, how it impacts translation is still unclear. To bridge the gap between widespread observed APA and the discovery of any functional consequence, we also provide a review of the experimental techniques used to uncover the functional importance of 3′ UTR isoforms on translation.

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Codon usage and protein sequence pattern dependency in different organisms: A Bioinformatics approach

Journal of Bioinformatics and Computational Biology ◽

10.1142/s021972001550002x ◽

2015 ◽

Vol 13 (02) ◽

pp. 1550002

Author(s):

Mohammad-Hadi Foroughmand-Araabi ◽

Bahram Goliaei ◽

Kasra Alishahi ◽

Mehdi Sadeghi ◽

Sama Goliaei

Keyword(s):

Gene Regulation ◽

Codon Usage ◽

Protein Sequence ◽

Multinomial Logistic Regression ◽

Translation Efficiency ◽

Translation Rate ◽

Protein Levels ◽

Synonymous Codons ◽

First Time

Although it is known that synonymous codons are not chosen randomly, the role of the codon usage in gene regulation is not clearly understood, yet. Researchers have investigated the relation between the codon usage and various properties, such as gene regulation, translation rate, translation efficiency, mRNA stability, splicing, and protein domains. Recently, a universal codon usage based mechanism for gene regulation is proposed. We studied the role of protein sequence patterns on the codons usage by related genes. Considering a subsequence of a protein that matches to a pattern or motif, we showed that, parts of the genes, which are translated to this subsequence, use specific ratios of synonymous codons. Also, we built a multinomial logistic regression statistical model for codon usage, which considers the effect of patterns on codon usage. This model justifies the observed codon usage preference better than the classic organism dependent codon usage. Our results showed that the codon usage plays a role in controlling protein levels, for genes that participate in a specific biological function. This is the first time that this phenomenon is reported.

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