Long Noncoding RNA Modulates Alternative Splicing Regulators in Arabidopsis

Bardou, Florian; Ariel, Federico; Simpson, Craig G.; Romero-Barrios, Natali; Laporte, Philippe; Balzergue, Sandrine; Brown, John W.; Crespi, Martín

doi:10.1016/j.devcel.2014.06.017

Cited by 316 publications

(288 citation statements)

References 42 publications

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“…For example, this splicing variant may sequester or assemble splicing regulators and thereby affect the AS outcome of other pre-mRNAs, similar to what has been described for a long noncoding RNA in Arabidopsis. This long noncoding RNA can interact with nuclear speckle RNA-binding proteins and thereby alter the AS outcome of their target pre-mRNAs (Bardou et al, 2014). Further splicing of SR30.2 may also compete with nuclear decay of this splicing variant.…”

Section: Possible Alternative Routes For the Generation Of The Sr303mentioning

confidence: 99%

Subcellular Compartmentation of Alternatively Spliced Transcripts Defines SERINE/ARGININE-RICH PROTEIN30 Expression

2018

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Alternative splicing (AS) is prevalent in higher eukaryotes, and generation of different AS variants is tightly regulated. Widespread AS occurs in response to altered light conditions and plays a critical role in seedling photomorphogenesis, but despite its frequency and effect on plant development, the functional role of AS remains unknown for most splicing variants. Here, we characterized the light-dependent AS variants of the gene encoding the splicing regulator Ser/Arg-rich protein SR30 in Arabidopsis (Arabidopsis thaliana). We demonstrated that the splicing variant SR30.2, which is predominantly produced in darkness, is enriched within the nucleus and strongly depleted from ribosomes. Light-induced AS from a downstream 39 splice site gives rise to SR30.1, which is exported to the cytosol and translated, coinciding with SR30 protein accumulation upon seedling illumination. Constitutive expression of SR30.1 and SR30.2 fused to fluorescent proteins revealed their identical subcellular localization in the nucleoplasm and nuclear speckles. Furthermore, expression of either variant shifted splicing of a genomic SR30 reporter toward SR30.2, suggesting that an autoregulatory feedback loop affects SR30 splicing. We provide evidence that SR30.2 can be further spliced and, unlike SR30.2, the resulting cassette exon variant SR30.3 is sensitive to nonsense-mediated decay. Our work delivers insight into the complex and compartmentalized RNA processing mechanisms that control the expression of the splicing regulator SR30 in a light-dependent manner.Maturation of eukaryotic mRNAs involves intricate co-and posttranscriptional RNA processing, which has critical functions in regulating gene expression and diversifying the transcriptome. Among several mechanisms, alternative precursor mRNA splicing (AS) in particular generates many transcript variants by removing distinct intronic regions and joining the resulting exons. Deep analysis of transcriptomes via high-throughput RNA sequencing (RNA-seq) has revealed that a major fraction of all intron-containing genes from higher eukaryotes generates AS variants. In humans, more than 95% of multiexon genes display AS (Pan et al., 2008). The prevalence of AS has also been demonstrated for other eukaryotes including plants (Reddy et al., 2013;Staiger and Brown, 2013), with current estimates of ;61% and ;42% of intron-containing genes giving rise to AS variants in the model plants Arabidopsis (Arabidopsis thaliana;Marquez et al., 2012) and Brachypodium distachyon (Mandadi and Scholthof, 2015), respectively.Besides its pivotal role in increasing the coding and regulatory capacity of the transcriptome, AS finetunes gene expression by varying the output ratios of splicing variants. The full extent of AS regulation likely exceeds the current estimates, as the production of many transcript variants can be specifically controlled under certain conditions, such as cell and tissue types, developmental stages, and in response to stresses and other environmental factors (Reddy et al., 2013;Staige...

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Section: Possible Alternative Routes For the Generation Of The Sr303mentioning

confidence: 99%

Subcellular Compartmentation of Alternatively Spliced Transcripts Defines SERINE/ARGININE-RICH PROTEIN30 Expression

2018

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“…lncRNAs commonly function to regulate target RNA alternative splicing or affect chromatin topology and regulate neighboring gene transcription Bardou et al, 2014). In addition, lncRNAs could function as precursors of miRNAs and other small RNAs (Pant et al, 2008).…”

Section: Drir Regulates Aba-mediated Responses To Drought and Salt Stmentioning

confidence: 99%

A Nucleus-Localized Long Non-Coding RNA Enhances Drought and Salt Stress Tolerance

Qin¹,

et al. 2017

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Long noncoding RNAs (lncRNAs) affect gene expression through a wide range of mechanisms and are considered as important regulators in many essential biological processes. A large number of lncRNA transcripts have been predicted or identified in plants in recent years. However, the biological functions for most of them are still unknown. In this study, we identified an Arabidopsis (Arabidopsis thaliana) lncRNA, DROUGHT INDUCED lncRNA (DRIR), as a novel positive regulator of the plant response to drought and salt stress. DRIR was expressed at a low level under nonstress conditions but can be significantly activated by drought and salt stress as well as by abscisic acid (ABA) treatment. We identified a T-DNA insertion mutant, drir D , which had higher expression of the DRIR gene than the wild-type plants. The drir D mutant exhibits increased tolerance to drought and salt stress. Overexpressing DRIR in Arabidopsis also increased tolerance to drought and salt stress of the transgenic plants. The drir D mutant and the overexpressing seedlings are more sensitive to ABA than the wild type in stomata closure and seedling growth. Genome-wide transcriptome analysis demonstrated that the expression of a large number of genes was altered in drir D and the overexpressing plants. These include genes involved in ABA signaling, water transport, and other stress-relief processes. Our study reveals a mechanism whereby DRIR regulates the plant response to abiotic stress by modulating the expression of a series of genes involved in the stress response.

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“…The size of these RNA species is in hundreds of nucleotides range and show mRNA-like characteristics. Investigations for discovery of these regulatory components and their various functions are more focused in the model plant Arabidopsis (Bardou et al 2014) and food crop plants such as maize (Li et al 2014a), rice (Ding et al 2012) and wheat (Xin et al 2011). Recently, Wu et al (2012) with the help of NGS platforms identified long non-coding RNA associated with the secondary metabolism in the medicinal plant Digitalis purpurea.…”

Section: Discovery Of Small and Long Non-coding Rna Speciesmentioning

confidence: 99%

Renaissance in phytomedicines: promising implications of NGS technologies

Sharma

Shrivastava

2016

Planta

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Medicinal plant research is growing significantly in faith to discover new and more biologically compatible phytomedicines. Deposition of huge genome/trancriptome sequence data assisted by NGS technologies has revealed the new possibilities for producing upgraded bioactive molecules in medicinal plants. Growing interest of investors and consumers in the herbal drugs raises the need for extensive research to open the facts and details of every inch of life canvas of medicinal plants to produce improved quality of phytomedicines. As in agriculture crops, knowledge emergence from medicinal plant's genome/transcriptome, can be used to assure their amended quality and these improved varieties are then transported to the fields for cultivation. Genome studies generate huge sequence data which can be exploited further for obtaining information regarding genes/gene clusters involved in biosynthesis as well as regulation. This can be achieved rapidly at a very large scale with NGS platforms. Identification of new RNA molecules has become possible, which can lead to the discovery of novel compounds. Sequence information can be combined with advanced phytochemical and bioinformatics tools to discover functional herbal drugs. Qualitative and quantitative analysis of small RNA species put a light on the regulatory aspect of biosynthetic pathways for phytomedicines. Inter or intra genomic as well as transcriptomic interactive processes for biosynthetic pathways can be elucidated in depth. Quality management of herbal material will also become rapid and high throughput. Enrichment of sequence information will be used to engineer the plants to get more efficient phytopharmaceuticals. The present review comprises of role of NGS technologies to boost genomic studies of pharmaceutically important plants and further, applications of sequence information aiming to produce enriched phytomedicines. Emerging knowledge from the medicinal plants genome/transcriptome can give birth to deep understanding of the processes responsible for biosynthesis of medicinally important compounds.

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Long Noncoding RNA Modulates Alternative Splicing Regulators in Arabidopsis

Cited by 316 publications

References 42 publications

Subcellular Compartmentation of Alternatively Spliced Transcripts Defines SERINE/ARGININE-RICH PROTEIN30 Expression

Subcellular Compartmentation of Alternatively Spliced Transcripts Defines SERINE/ARGININE-RICH PROTEIN30 Expression

A Nucleus-Localized Long Non-Coding RNA Enhances Drought and Salt Stress Tolerance

Renaissance in phytomedicines: promising implications of NGS technologies

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