Light Regulates Plant Alternative Splicing through the Control of Transcriptional Elongation

Herz, Micaela Amalia Godoy; Kubaczka, M. Guillermina; Brzyżek, Grzegorz; Servi, Lucas; Krzysztoń, Michał; Simpson, Craig G.; Brown, John W.; Świeżewski, Szymon; Petrillo, Ezequiel; Kornblihtt, Alberto R.

doi:10.1016/j.molcel.2018.12.005

Cited by 87 publications

(66 citation statements)

References 39 publications

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“…AS is common in plants; for example, in Arabidopsis thaliana, more than 60% of intron-containing genes undergo AS (Syed et al, 2012). Many environmental factors regulate AS events in plants, including CO 2 concentration (Huang et al, 2019), light (Godoy et al, 2019), salt stress (Ding et al, 2014), and nutrient deficiencies (Nishida et al, 2017). AS not only provides an important source of transcriptomic and proteomic diversity and plasticity for use in natural selection (Labadorf et al, 2010), but it also plays specific roles in the response (Chauhan et al, 2019) or adaptation to environmental stresses (Filichkin et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Investigation for a multi-silique trait in Brassica napus by alternative splicing analysis

Chai

Zhang

et al. 2020

PeerJ

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Background Flower and fruit development are vital stages of the angiosperm lifecycle. We previously investigated the multi-silique trait in the rapeseed (Brassica napus) line zws-ms on a genomic and transcriptomic level, leading to the identification of two genomic regions and several candidate genes associated with this trait. However, some events on the transcriptome level, like alternative splicing, were poorly understood. Methods Plants from zws-ms and its near-isogenic line (NIL) zws-217 were both grown in Xindu with normal conditions and a colder area Ma’erkang. Buds from the two lines were sampled and RNA was isolated to perform the transcriptomic sequencing. The numbers and types of alternative splicing (AS) events from the two lines were counted and classified. Genes with AS events and expressed differentially between the two lines, as well as genes with AS events which occurred in only one line were emphasized. Their annotations were further studied. Results From the plants in Xindu District, an average of 205,496 AS events, which could be sorted into five AS types, were identified. zws-ms and zws-217 shared highly similar ratios of each AS type: The alternative 5′ and 3′ splice site types were the most common, while the exon skipping type was observed least often. Eleven differentially expressed AS genes were identified, of which four were upregulated and seven were downregulated in zws-ms. Their annotations implied that five of these genes were directly associated with the multi-silique trait. While samples from colder area Ma’erkang generated generally reduced number of each type of AS events except for Intron Retention; but the number of differentially expressed AS genes increased significantly. Further analysis found that among the 11 differentially expressed AS genes from Xindu, three of them maintained the same expression models, while the other eight genes did not show significant difference between the two lines in expression level. Additionally, the 205 line-specific expressed AS genes were analyzed, of which 187 could be annotated, and two were considered to be important. Discussion This study provides new insights into the molecular mechanism of the agronomically important multi-silique trait in rapeseed on the transcriptome level and screens out some environment-responding candidate genes.

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Section: Introductionmentioning

confidence: 99%

Investigation for a multi-silique trait in Brassica napus by alternative splicing analysis

Chai

Zhang

et al. 2020

PeerJ

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“…In a recent publication (Godoy Herz et al., 2019), we show that the light control of alternative splicing responds to the kinetic coupling mechanism. Light promotes transcription elongation, while in darkness RNAPII elongation is lower.…”

Section: Light Regulation Of Alternative Splicing Through Transcriptimentioning

confidence: 73%

Alternative Splicing and Transcription Elongation in Plants

Herz

Kornblihtt

2019

Front. Plant Sci.

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Alternative splicing and transcription elongation by RNA polymerase II (RNAPII) are two processes which are tightly connected. Splicing is a co-transcriptional process, and different experimental approaches show that splicing is coupled to transcription in Drosophila , yeast and mammals. However, little is known about coupling of transcription and alternative splicing in plants. The kinetic coupling explains how changes in RNAPII elongation rate influence alternative splicing choices. Recent work in Arabidopsis shows that expression of a dominant negative transcription elongation factor, TFIIS, enhances exon inclusion. Furthermore, the Arabidopsis transcription elongation complex has been recently described, providing new information about elongation factors that interact with elongating RNAPII. Light regulates alternative splicing in plants through a chloroplast retrograde signaling. We have recently shown that light promotes RNAPII elongation in the affected genes, while in darkness elongation is lower. These changes in transcription are consistent with elongation causing the observed changes in alternative splicing. Altogether, these findings provide evidence that coupling between transcription and alternative splicing is an important layer of gene expression regulation in plants.

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“…Light causes wide-spread alternative splicing (AS) in plant transcriptome (Shikata et al, 2014; Hartmann et al, 2016; Xin et al, 2017; Godoy Herz et al, 2019). Although PIF3 has not been experimentally demonstrated to undergo light regulated AS, based on the information from Araport (Arabidopsis Information Portal: www.araport.org), transcripts with alternative splicing patterns at an intron of approximately 500 bp in PIF3 5’ untranslated region (UTR) have been found in the database (Figure 2A).…”

Section: Resultsmentioning

confidence: 99%

PhyB induces intron retention and uORF-mediated translational inhibition of PIF3

Dong

Chen

Deng

et al. 2019

Preprint

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The phytochrome B (phyB) photoreceptor stimulates light responses in plants in part by inactivating repressors of light responses such as phytochrome-interacting factor 3 (PIF3). It has been established that activated phyB inhibits PIF3 by rapid protein degradation and decreased transcription. PIF3 protein degradation has been shown to be mediated by EIN3-BINDING F-BOX PROTEIN (EBF) and LIGHT-RESPONSE BTB (LRB) E3 ligases, the latter simultaneously targeting phyB for degradation. In this study, we show that PIF3 level is additionally regulated by alternative splicing and protein translation. Overaccumulation of photo-activated phyB, which occur in the mutant defective for LRB genes under continuous red light (Rc), induces a specific alternative splicing of PIF3 that results in retention of an intron in the 5’UTR of PIF3 mRNA. In turn, the upstream opening reading frames (uORF) contained within this intron inhibit PIF3 protein synthesis. The phyB-dependent alternative splicing of PIF3 is diurnally regulated under the short-day light cycle. We hypothesize that this reversible regulatory mechanism may be utilized to fine-tune the level of PIF3 protein in light-grown plants, and may contribute to the oscillation of PIF3 protein abundance under the short-day environment.One Sentence SummaryLight down-regulates PIF3 by multiple mechanisms. We show that phyB induces an alternative splicing event that inhibits PIF3 protein translation, and that is regulated by short-day diurnal cycle.

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Light Regulates Plant Alternative Splicing through the Control of Transcriptional Elongation

Abstract: Highlights d Light increases Pol II elongation while in darkness elongation is lower d Light regulation of alternative splicing is controlled by Pol II elongation

Cited by 87 publications

References 39 publications

Investigation for a multi-silique trait in Brassica napus by alternative splicing analysis

Investigation for a multi-silique trait in Brassica napus by alternative splicing analysis

Alternative Splicing and Transcription Elongation in Plants

PhyB induces intron retention and uORF-mediated translational inhibition of PIF3

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