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Splicing events (A) Overview of splicing events that can occur. Alternative events are depicted in red, conventional events are depicted in black. Boxes represent exons, lines represent introns. (B) Distribution of the differential splicing events upon shifts to higher or lower ambient temperature, compared to the events in the total dataset. The asterisk * indicates a significant difference of the abundance of the event compared to the overall abundance (Using Pearson’s Chi-square test, for data used for significance test, see S2 Table).
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Plants adjust their development and architecture to small variations in ambient temperature. In a time in which temperatures are rising world-wide, the mechanism by which plants are able to sense temperature fluctuations and adapt to it, is becoming of special interest. By performing RNA-sequencing on two Arabidopsis accession and one Brassica spec...
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Citations
... Moreover, AtU2AF65b has been reported to participate in the ABA flowering pathway by regulating the AS of ABI5 in plants (Verhage et al., 2017;Xiong et al., 2019). Environmental temperature also affects the AS of the AtU2AF65a gene itself, and this AS variation pattern further regulates the splicing of downstream genes (such as MAF1) to control the flowering process in plants (Cavallari et al., 2018;Verhage et al., 2017). ...
... Moreover, AtU2AF65b has been reported to participate in the ABA flowering pathway by regulating the AS of ABI5 in plants (Verhage et al., 2017;Xiong et al., 2019). Environmental temperature also affects the AS of the AtU2AF65a gene itself, and this AS variation pattern further regulates the splicing of downstream genes (such as MAF1) to control the flowering process in plants (Cavallari et al., 2018;Verhage et al., 2017). However, the regulatory mechanisms upstream of AtU2AF65a are still poorly understood. ...
Alternative splicing (AS) is an important regulatory mode at the post‐transcriptional level, through which many flowering genes regulate floral transition by producing multiple transcripts, and splicing factors have essential roles in this process. Hydrogen sulphide (H 2 S) is a newly found gasotransmitter that has critical physiological roles in plants, and one of its potential modes of action is via persulfidation of target proteins at specific cysteine sites. Previously, it has been shown that both the splicing factor AtU2AF65a and H 2 S are involved in the regulation of plant flowering. This study found that, in Arabidopsis , the promoting effect of H 2 S on flowering was abolished in atu2af65a‐4 mutants. Transcriptome analyses showed that when AtU2AF65a contained mutations, the regulatory function of H 2 S during the AS of many flowering genes (including SPA1 , LUH , LUG and MAF3 ) was inhibited. The persulfidation assay showed that AtU2AF65a can be persulfidated by H 2 S, and the RNA immunoprecipitation data indicated that H 2 S could alter the binding affinity of AtU2AF65a to the precursor messenger RNA of the above‐mentioned flowering genes. Overall, our results suggest that H 2 S may regulate the AS of flowering‐related genes through persulfidation of splicing factor AtU2AF65a and thus lead to early flowering in plants.
... Loss-of-function mutants of the two isoforms of AtU2AF65 also reveal their functional roles in floral transition [24,25,33]. atu2af65a and atu2af65b mutants showed late-and early-flowering phenotypes, respectively, which correlated with altered expression levels of the flowering time genes, including FLC and FLOWERING LOCUS T (FT) in the leaves [24]. ...
... Thus, the meristem region, which continuously generates new lateral organs under various environmental conditions, is an important site for developmental plasticity, where the underlying molecular mechanisms, such as AS, provide diversity and fine-tune gene expression. In particular, previous studies have shown that small fluctuations in the temperature, such as ambient temperature, directly influence the AS processes and that these changes affect the downstream genes associated with adaptation for plant development in response to changing temperatures [33,62]. ...
Plants, as sessile organisms, show a high degree of plasticity in their growth and development and have various strategies to cope with these alterations under continuously changing environments and unfavorable stress conditions. In particular, the floral transition from the vegetative and reproductive phases in the shoot apical meristem (SAM) is one of the most important developmental changes in plants. In addition, meristem regions, such as the SAM and root apical meristem (RAM), which continually generate new lateral organs throughout the plant life cycle, are important sites for developmental plasticity. Recent findings have shown that the prevailing type of alternative splicing (AS) in plants is intron retention (IR) unlike in animals; thus, AS is an important regulatory mechanism conferring plasticity for plant growth and development under various environmental conditions. Although eukaryotes exhibit some similarities in the composition and dynamics of their splicing machinery, plants have differences in the 3’ splicing characteristics governing AS. Here, we summarize recent findings on the roles of 3’ splicing factors and their interacting partners in regulating the flowering time and other developmental plasticities in Arabidopsis thaliana.
... For example, atu2af35 mutants show a late flowering phenotype [14], whereas atsf1 mutants show an early flowering phenotype [13]. In addition, atu2af65a and atu2af65b mutants exhibit late and early flowering phenotypes, respectively [12,19,20]. ...
... This suggests that functional deficiency of AtU2AF65b and AtSF1 proteins may cause an increase in AtU2AF65a protein levels to compensate for their loss in pre-mRNA splicing machinery. Because differences in ambient temperature affect the splicing patterns of splicing factors [19], the expression of the three AtU2AF65a spliced forms (At4g36690.1, At4g36690.2, ...
We investigated the transcriptomic changes in the shoot apices during floral transition in Arabidopsis mutants of two closely related splicing factors: AtU2AF65a (atu2af65a) and AtU2AF65b (atu2af65b). The atu2af65a mutants exhibited delayed flowering, while the atu2af65b mutants showed accelerated flowering. The underlying gene regulatory mechanism of these phenotypes was unclear. We performed RNA-seq analysis using shoot apices instead of whole seedlings and found that the atu2af65a mutants had more differentially expressed genes than the atu2af65b mutants when they were compared to wild type. The only flowering time gene that was significantly up- or down-regulated by more than two-fold in the mutants were FLOWERING LOCUS C (FLC), a major floral repressor. We also examined the expression and alternative splicing (AS) patterns of several FLC upstream regulators, such as COOLAIR, EDM2, FRIGIDA, and PP2A-b’ɤ, and found that those of COOLAIR, EDM2, and PP2A-b’ɤ were altered in the mutants. Furthermore, we demonstrated that AtU2AF65a and AtU2AF65b genes partially influenced FLC expression by analyzing these mutants in the flc-3 mutant background. Our findings indicate that AtU2AF65a and AtU2AF65b splicing factors modulate FLC expression by affecting the expression or AS patterns of a subset of FLC upstream regulators in the shoot apex, leading to different flowering phenotypes.
... In this study, SME1 mutation dependent AS was overrepresented in genes involved in metabolic pathways and encoding RNA-binding proteins (Fig. 5C). Cross-or auto-regulation via AS of pre-mRNA splicing genes has been described before under temperature changes [70]. Also in animals, splicing factors, such as SR proteins, are known to exert auto-regulatory feedback by unproductive splicing and hence regulate the fate of their own mRNAs [71]. ...
Alternative splicing is a key posttranscriptional gene regulatory process, acting in diverse adaptive and basal plant processes. Splicing of precursor-messenger RNA (pre-mRNA) is catalyzed by a dynamic ribonucleoprotein complex, designated the spliceosome. In a suppressor screen, we identified a nonsense mutation in the Smith (Sm) antigen protein SME1 to alleviate photorespiratory H2O2-dependent cell death in catalase deficient plants. Similar attenuation of cell death was observed upon chemical inhibition of the spliceosome, suggesting pre-mRNA splicing inhibition to be responsible for the observed cell death alleviation. Furthermore, the sme1-2 mutants showed increased tolerance to the reactive oxygen species inducing herbicide methyl viologen. Both an mRNA-seq and shotgun proteomic analysis in sme1-2 mutants displayed a constitutive molecular stress response, together with extensive alterations in pre-mRNA splicing of transcripts encoding metabolic enzymes and RNA binding proteins, even under unstressed conditions. Using SME1 as a bait to identify protein interactors, we provide experimental evidence for almost 50 homologs of mammalian spliceosome-associated protein to reside in the Arabidopsis thaliana spliceosome complexes and propose roles in pre-mRNA splicing for four uncharacterized plant proteins. Furthermore, like in sme1-2, a mutant in the Sm core assembly protein ICLN resulted in a decreased sensitivity to methyl viologen. Taken together, these data show that both a perturbed Sm core composition and assembly results in the activation of a defense response and enhanced resilience to oxidative stress.
... Common AS regulators are RNA binding proteins (RBPs), such as Ser/Arg-rich (SR) proteins, which then interact with the spliceosome (Kornblihtt et al., 2013). The level and activity of hundreds of these splicing regulators, also known as splicing factors (SFs), change in response to temperature, suggesting they are crucial elements in thermal-stress AS regulation (Verhage et al., 2017;Calixto et al., 2018;Vitoriano and Calixto, 2021). Our knowledge of the true scale and function of SFs involved in heat-induced AS are limited and need to be addressed (Rosenkranz et al., 2022). ...
To identify novel solutions to improve rice yield under rising temperatures, molecular components of thermotolerance must be better understood. Alternative splicing (AS) is a major post-transcriptional mechanism impacting plant tolerance against stresses, including heat stress (HS). AS is largely regulated by splicing factors (SFs) and recent studies have shown their involvement in temperature response. However, little is known about the splicing networks between SFs and AS transcripts in the HS response. To expand this knowledge, we constructed a co-expression network based on a publicly available RNA-seq dataset that explored rice basal thermotolerance over a time-course. Our analyses suggest that the HS-dependent control of the abundance of specific transcripts coding for SFs might explain the widespread, coordinated, complex, and delicate AS regulation of critical genes during a plant’s inherent response to extreme temperatures. AS changes in these critical genes might affect many aspects of plant biology, from organellar functions to cell death, providing relevant regulatory candidates for future functional studies of basal thermotolerance.
... Recently, it was also found that the long-day photoperiod flowering pathway protein GIGANTEA (GI) mediates the photoperiodicity of thermal reversion by attenuating PIF4 function under long days (Park et al., 2020). Despite this progress in understanding thermal sensing, it is not known how thermal reversion intersects with the ambient flowering time pathway (see next section and "Outstanding Questions"), where higher ambient temperatures often promote faster flowering (but see Verhage et al., 2017;Del Olmo et al., 2019). Furthermore, the lack of evidence for phytochrome-regulated thermal reversion outside core eudicots, begs the question as to the conservation and number of origins of this sensing mechanism. ...
... A second major component of the ambient temperature pathway in both Arabidopsis and Brassica sp. is mediated by differential expression and splicing of transcription factors that regulate both repressors and promoters of flowering (Verhage et al., 2017). In the Arabidopsis Col-0 ecotype, FLOWERING CONTROL LOCUS A produces four alternative splice forms, one of which (lambda) becomes dominant at higher ambient temperatures to specifically repress the flowering repressor FLOWERING LOCUS C (FLC; Quesada et al., 2003). ...
Evidence suggests that anthropogenically-mediated global warming results in accelerated flowering for many plant populations. However, the fact that some plants are late flowering or unaffected by warming, underscores the complex relationship between phase change, temperature, and phylogeny. In this review, we present an emerging picture of how plants sense temperature changes, and then discuss the independent recruitment of ancient flowering pathway genes for the evolution of ambient, low, and high temperature-regulated reproductive development. As well as revealing areas of research required for a better understanding of how past thermal climates have shaped global patterns of plasticity in plant phase change, we consider the implications for these phenological thermal responses in light of climate change.
... In plants, as more forms and functions of AS are considered to modulate diverse biological mechanisms, including flowering time, circadian rhythms, and response to stress (Simpson et al., 2016;Ling et al., 2017;Verhage et al., 2017;Zhang and Xiao, 2018;Dikaya et al., 2021). lncRNAs in plants influence the gene expression and regulation both in direct and indirect ways. ...
Plants are sessile organisms affected by changing environment, especially biotic and abiotic stress. Long non-coding RNAs (lncRNAs) became prominent as crucial regulators in diverse biological mechanisms, including developmental processes and stress responses such as salinity. In this study, salinity related lncRNAs were sequenced and analyzed according to homology based on rice and maize lncRNA sequences. After sequencing, 72HASATROOT and 72TARMROOT were identified as 568 bp, additionally, 72HASATSHOOT and 72TARMSHOOT were also 568 bp according to reference sequence which are the member of the natural-antisense lncRNA with 565 bp. Besides, 77HASATROOT and 77TARMROOT were identified as 676 and 644 bp, additionally, 77HASATSHOOT and 77TARMSHOOT were 666 bp according to reference sequence alignment that reference sequence was 667 bp and the sno-lncRNA member. Sequencing studies demonstrated sequence alterations resulted in secondary structure changes which may affect the adaptation of varieties in response to stress. As a conclusion, rapid evolution of lncRNAs may be another force for adaptation to changing environment in plants.
... is recognized through base pairing with U1 snRNA, with the help of U1 snRNP (Lerner et al., 1980;Zhuang and Weiner, 1986;Verhage et al., 2017;Plaschka et al., 2018), while the 3 0 -SS is recognized by the U2 snRNP (Abovich and Rosbash, 1997). However, SS selection can be altered, resulting in the generation of two or more mRNA isoforms from the same pre-mRNA, a phenomenon that is termed alternative splicing (AS). ...
... The genes encoding splicing regulators often undergo intensive AS regulation themselves (Verhage et al., 2017). In the current Araport 11 annotation, PRP39a is represented by two major AS isoforms that differ in the incorporation of two alternative exons between exons 6 and 7 ( Figure 4A). ...
Pre-mRNA splicing is a crucial step in gene expression whereby the spliceosome produces constitutively and alternatively spliced transcripts. These transcripts not only diversify the transcriptome, but they also play essential roles in plant development and responses to environmental changes. Much evidence indicates that regulation at the pre-mRNA splicing step is important for flowering time control; however, the components and detailed mechanism underlying this process remain largely unknown. Here, we identified the splicing factor RNA BINDING PROTEIN 45d (RBP45d), a member of the RBP45/47 family in Arabidopsis thaliana. Using sequence comparison and biochemical analysis, we determined that RBP45d is a component of the U1 small nuclear ribonucleoprotein (U1 snRNP) with functions distinct from other family members. RBP45d associates with the U1 snRNP by interacting with pre-mRNA-processing factor 39a (PRP39a) and directly regulates alternative splicing (AS) for a specific set of genes. Plants with loss of RBP45d and PRP39a function exhibited defects in temperature-induced flowering, potentially due to the misregulation of temperature-sensitive AS of FLOWERING LOCUS M as well as the accumulation of the flowering repressor FLOWERING LOCUS C. Taken together, RBP45d is a U1 snRNP component in plants that functions with PRP39a in temperature-mediated flowering.
... Ген MAF2 предотвращает раннее цветение в ответ на короткие периоды холода, что позволяет избежать индукции цветения в теплый осенний период перед зимними холодами (66). Для MAF2 и MAF3 подобно FLM свойственен температурозависимый альтернативный сплайсинг (67,68). Низкотемпературная форма MAF2 кодирует белок, который взаимодействует с SVP, подавляя цветение; при повышенных температурах сплайсинг смещается в сторону варианта, который кодирует белок, не взаимодействующий с SVP; таким образом, при более низких температурах MAF2 и SVP подавляют цветение одновременно с FLM и SVP (68). ...
... In grapevine, like in other plant species, these different stress factors have previously been shown to regulate gene AS [22][23][24][25]. SR genes, which play a major role in gene splicing, are themselves subjected to AS modulation, especially under stress conditions, and may regulate the splicing of multiple downstream target pre-mRNAs, at the same time, to modify the transcriptome [26,27]. The extent of AS in grapevine has been first explored using cDNAs/ESTs collections available from public databases or merged RNAseq data to identify as many events as possible [22,28]. ...
... Furthermore, many SR transcript isoforms were found to be 'species-specific' in a study comparing maize and sorgho [66]. Several previous reports have also mentioned the overrepresentation of genes involved in RNA splicing among genes showing splicing variation depending on the developmental stage, the environment, or the genotype, in various plant species [27,39,67,68]. We found that a number of genes related to the response to nutritional or environmental stresses were among those with the most marked splicing differences between Gw and Ri. ...
Background
Alternative splicing (AS) produces transcript variants playing potential roles in proteome diversification and gene expression regulation. AS modulation is thus essential to respond to developmental and environmental stimuli. In grapevine, a better understanding of berry development is crucial for implementing breeding and viticultural strategies allowing adaptation to climate changes. Although profound changes in gene transcription have been shown to occur in the course of berry ripening, no detailed study on splicing modifications during this period has been published so far. We report here on the regulation of gene AS in developing berries of two grapevine (Vitis vinifera L.) varieties, Gewurztraminer (Gw) and Riesling (Ri), showing distinctive phenotypic characteristics. Using the software rMATS, the transcriptomes of berries at four developmental steps, from the green stage to mid-ripening, were analysed in pairwise comparisons between stages and varieties.
Results
A total of 305 differential AS (DAS) events, affecting 258 genes, were identified. Interestingly, 22% of these AS events had not been reported before. Among the 80 genes that underwent the most significant variations during ripening, 22 showed a similar splicing profile in Gw and Ri, which suggests their involvement in berry development. Conversely, 23 genes were subjected to splicing regulation in only one variety. In addition, the ratios of alternative isoforms were different in Gw and Ri for 35 other genes, without any change during ripening. This last result indicates substantial AS differences between the two varieties. Remarkably, 8 AS events were specific to one variety, due to the lack of a splice site in the other variety. Furthermore, the transcription rates of the genes affected by stage-dependent splicing regulation were mostly unchanged, identifying AS modulation as an independent way of shaping the transcriptome.
Conclusions
The analysis of AS profiles in grapevine varieties with contrasting phenotypes revealed some similarity in the regulation of several genes with developmental functions, suggesting their involvement in berry ripening. Additionally, many splicing differences were discovered between the two varieties, that could be linked to phenotypic specificities and distinct adaptive capacities. Together, these findings open perspectives for a better understanding of berry development and for the selection of grapevine genotypes adapted to climate change.
