Alternative Splicing Substantially Diversifies the Transcriptome during Early Photomorphogenesis and Correlates with the Energy Availability in Arabidopsis

Hartmann, Lisa; Drewe-Boß, Philipp; Wießner, Theresa; Wagner, Gerd K.; Geue, Sascha; Lee, Hsin-Chieh; Obermüller, Dominik M; Kahles, André; Behr, Jonas; Sinz, Fabian H.; Rätsch, Gunnar; Wachter, Andreas

doi:10.1105/tpc.16.00508

Cited by 80 publications

(109 citation statements)

References 109 publications

(163 reference statements)

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“…Transcriptome-wide AS profiling of etiolated Arabidopsis seedlings either exposed to different light qualities for 6 h or retained in darkness revealed several hundred AS event changes in response to illumination (Hartmann et al, 2016). Interestingly, the majority of regulated AS events display a switch from a presumably unproductive transcript in darkness to a likely protein-coding variant in light (Hartmann et al, 2016).…”

Section: Light Induces a Rapid And Transient As Shift For The Splicinmentioning

confidence: 99%

“…Interestingly, the majority of regulated AS events display a switch from a presumably unproductive transcript in darkness to a likely protein-coding variant in light (Hartmann et al, 2016). To understand the regulation and potential impact of this apparently frequent mode of AS shift, AS of SR30 was functionally characterized.…”

Section: Light Induces a Rapid And Transient As Shift For The Splicinmentioning

confidence: 99%

“…Interestingly, their data also support a role of coordinated AS programs in cell differentiation, while no evidence for AS-mediated celltype specification has been observed. Furthermore, transcriptome analyses in the course of photomorphogenesis have revealed widespread AS changes within few hours of light exposure of etiolated Arabidopsis seedlings (Shikata et al, 2014;Hartmann et al, 2016). Interestingly, more than 60% of the regulated AS events show a switch from a presumably nonproductive variant in darkness to a probably protein-coding variant in light (Hartmann et al, 2016), thereby allowing to ramp up expression of critical factors.…”

mentioning

confidence: 99%

“…Furthermore, transcriptome analyses in the course of photomorphogenesis have revealed widespread AS changes within few hours of light exposure of etiolated Arabidopsis seedlings (Shikata et al, 2014;Hartmann et al, 2016). Interestingly, more than 60% of the regulated AS events show a switch from a presumably nonproductive variant in darkness to a probably protein-coding variant in light (Hartmann et al, 2016), thereby allowing to ramp up expression of critical factors. Experimental evidence for such regulation has been provided for the positive light signaling component REDUCED RED-LIGHT RESPONSES IN CRY1CRY2 BACKGROUND1 (Shikata et al, 2012), which displays an AS switch from an NMD target in darkness to a protein-coding transcript variant in light (Hartmann et al, 2016).…”

mentioning

confidence: 99%

“…Interestingly, more than 60% of the regulated AS events show a switch from a presumably nonproductive variant in darkness to a probably protein-coding variant in light (Hartmann et al, 2016), thereby allowing to ramp up expression of critical factors. Experimental evidence for such regulation has been provided for the positive light signaling component REDUCED RED-LIGHT RESPONSES IN CRY1CRY2 BACKGROUND1 (Shikata et al, 2012), which displays an AS switch from an NMD target in darkness to a protein-coding transcript variant in light (Hartmann et al, 2016). Furthermore, evidence was provided that photomorphogenesis is promoted by light-dependent AS of SPA1-RELATED3 (Shikata et al, 2014) due to light-triggered formation of a dominant-negative version of this repressor of photomorphogenesis.…”

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confidence: 99%

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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: Light Induces a Rapid And Transient As Shift For The Splicinmentioning

confidence: 99%

Section: Light Induces a Rapid And Transient As Shift For The Splicinmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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

2018

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Alternative Splicing Underpins the ALMT9 Transporter Function for Vacuolar Malic Acid Accumulation in Apple

Li,

Krishnan,

Zhang

et al. 2024

Advanced Science

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Vacuolar malic acid accumulation largely determines fruit acidity, a key trait for the taste and flavor of apple and other fleshy fruits. Aluminum‐activated malate transporter 9 (ALMT9/Ma1) underlies a major genetic locus, Ma, for fruit acidity in apple, but how the protein transports malate across the tonoplast is unclear. Here, it is shown that overexpression of the coding sequence of Ma1 (Ma1α) drastically decreases fruit acidity in “Royal Gala” apple, leading to uncovering alternative splicing underpins Ma1's function. Alternative splicing generates two isoforms: Ma1β is 68 amino acids shorter with much lower expression than the full‐length protein Ma1α. Ma1β does not transport malate itself but interacts with the functional Ma1α to form heterodimers, creating synergy with Ma1α for malate transport in a threshold manner (When Ma1β/Ma1α ≥ 1/8). Overexpression of Ma1α triggers feedback inhibition on the native Ma1 expression via transcription factor MYB73, decreasing the Ma1β level well below the threshold that leads to significant reductions in Ma1 function and malic acid accumulation in fruit. Overexpression of Ma1α and Ma1β or genomic Ma1 increases both isoforms proportionally and enhances fruit malic acid accumulation. These findings reveal an essential role of alternative splicing in ALMT9‐mediated malate transport underlying apple fruit acidity.

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Regulation of Alternative Splicing by Phytochrome

Matsushita

2019

Methods in Molecular Biology

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Alternative Splicing Substantially Diversifies the Transcriptome during Early Photomorphogenesis and Correlates with the Energy Availability in Arabidopsis

Cited by 80 publications

References 109 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

Alternative Splicing Underpins the ALMT9 Transporter Function for Vacuolar Malic Acid Accumulation in Apple

Regulation of Alternative Splicing by Phytochrome

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