Dynamic regulation of genome-wide pre-mRNA splicing and stress tolerance by the Sm-like protein LSm5 in Arabidopsis

Cui, Peng; Zhang, Shoudong; Ding, Feng; Ali, Shahjahan; Xiong, Liming

doi:10.1186/gb-2014-15-1-r1

Cited by 1,653 publications

(119 citation statements)

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“…Among the AS events affected in the lsm4 and sad1/lsm5 mutants, we found an increase in the proportion of IR events relative to their frequency in wildtype plants, which is consistent with previous findings reported for the sad1/lsm5 mutant (Fig. 4C) (29,36). Representative examples of alterations in AS observed in the mutants using the Integrative Genome Browser (IGB) (37) are shown in Fig.…”

Section: A Mutation In Arabidopsis Lsm5 Confers a Long Period Phenotysupporting

confidence: 80%

“…These results provide strong evidence that LSM genes also regulate circadian rhythms in mammals. specific splicing defects (29). One of these studies analyzed splicing alterations at the genome-wide level using high-throughput RNA sequencing (RNA-seq) and found that LSM5 controls the splicing efficiency and splice-site recognition of many splicing events, but is particularly required for regulating the splicing efficiency of stress-responsive genes (29).…”

Section: A Mutation In Arabidopsis Lsm5 Confers a Long Period Phenotymentioning

confidence: 99%

“…LSM5, which encodes an Sm-like protein, was originally identified in a screen for genes that control abiotic stress responses, and was named supersensitive to abscisic acid and drought (sad1) (28). The sad1/lsm5 mutant has a point mutation that changes a conserved glutamic acid residue to lysine (29). We found that the period length in sad1/lsm5 mutants was more than 3 h longer than in wild-type plants (29.09 ± 1.83 h and 24.20 ± 0.32 h, respectively, P < 0.05) ( Fig.…”

Section: A Mutation In Arabidopsis Lsm5 Confers a Long Period Phenotymentioning

confidence: 99%

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Role for LSM genes in the regulation of circadian rhythms

Perez-Santángelo

Mancini

Francey

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Growing evidence suggests that core spliceosomal components differentially affect RNA processing of specific genes; however, whether changes in the levels or activities of these factors control specific signaling pathways is largely unknown. Here we show that some SM-like (LSM) genes, which encode core components of the spliceosomal U6 small nuclear ribonucleoprotein complex, regulate circadian rhythms in plants and mammals. We found that the circadian clock regulates the expression of LSM5 in Arabidopsis plants and several LSM genes in mouse suprachiasmatic nucleus. Further, mutations in LSM5 or LSM4 in Arabidopsis, or down-regulation of LSM3, LSM5, or LSM7 expression in human cells, lengthens the circadian period. Although we identified changes in the expression and alternative splicing of some core clock genes in Arabidopsis lsm5 mutants, the precise molecular mechanism causing period lengthening remains to be identified. Genome-wide expression analysis of either a weak lsm5 or a strong lsm4 mutant allele in Arabidopsis revealed larger effects on alternative splicing than on constitutive splicing. Remarkably, large splicing defects were not observed in most of the introns evaluated using RNA-seq in the strong lsm4 mutant allele used in this study. These findings support the idea that some LSM genes play both regulatory and constitutive roles in RNA processing, contributing to the fine-tuning of specific signaling pathways.posttranscriptional | alternative splicing | circadian clock | Arabidopsis | mammals C ircadian rhythms are persistent 24-h oscillations in biological processes that occur under constant environmental conditions. They allow organisms to coordinate multiple physiological processes with periodic or seasonal changes that occur in the environment. At the heart of the eukaryotic circadian system lies a complex set of interconnected transcriptional and translational feedback loops, in which a group of core clock genes regulate each other to ensure that their mRNA levels oscillate with a period of ∼24 h (1). The core oscillator in Arabidopsis thaliana involves two MYB domain-containing transcription factors, CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY), that repress the expression of TIMING OF CAB2 EXPRESSION 1 (TOC1) at the beginning of the day. In turn, TOC1, a member of the PSEUDO-RESPONSE REGULATOR (PRR) family, represses CCA1/LHY expression at the end of the day (2). Other clock components expressed throughout the day form multiple interconnected transcriptional feedback loops (2).Mounting evidence indicates that alternative splicing (AS), the process by which pre-mRNA molecules are differentially spliced to yield multiple mRNA isoforms from a single gene, plays a key role in the regulation of circadian networks in a variety of organisms, including Drosophila melanogaster (3), Neurospora crassa (4-6), and Arabidopsis (7-11). For example, the core clock genes period in Drosophila and frequency in Neurospora give rise to different mRNA isoforms through AS, which helps t...

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Section: A Mutation In Arabidopsis Lsm5 Confers a Long Period Phenotysupporting

confidence: 80%

Section: A Mutation In Arabidopsis Lsm5 Confers a Long Period Phenotymentioning

confidence: 99%

Section: A Mutation In Arabidopsis Lsm5 Confers a Long Period Phenotymentioning

confidence: 99%

See 1 more Smart Citation

Role for LSM genes in the regulation of circadian rhythms

Perez-Santángelo

Mancini

Francey

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…8 and 9). In Arabidopsis, overexpression of the salt stress-regulated splicing factor SAD1 was shown to increase splicing precision and confer salt tolerance (Cui et al, 2014). PRP18, therefore, may play a similar role in drought stress response and warrants further investigation.…”

Section: Changes In Splicing Correlate With Gene Expression Changes Imentioning

confidence: 99%

“…Gene expression changes in splicing factors are a major factor in determining stress-induced alternative splicing changes (Yan et al, 2012;Leviatan et al, 2013;Staiger and Brown, 2013). For example, Cui et al (2014) recently showed that overexpression of the splicing factor SAD1 conferred increased splicing precision and resulted in increased tolerance to salt stress in Arabidopsis (Arabidopsis thaliana). These and other findings highlight the importance of examining mRNA changes at both the transcriptional and posttranscriptional levels to obtain a more complete picture of both development and stress.…”

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confidence: 99%

Genome-Wide Analysis of Alternative Splicing during Development and Drought Stress in Maize

et al. 2015

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Alternative splicing plays a crucial role in plant development as well as stress responses. Although alternative splicing has been studied during development and in response to stress, the interplay between these two factors remains an open question. To assess the effects of drought stress on developmentally regulated splicing in maize (Zea mays), 94 RNA-seq libraries from ear, tassel, and leaf of the B73 public inbred line were constructed at four developmental stages under both well-watered and drought conditions. This analysis was supplemented with a publicly available series of 53 libraries from developing seed, embryo, and endosperm. More than 48,000 novel isoforms, often with stage-or condition-specific expression, were uncovered, suggesting that developmentally regulated alternative splicing occurs in thousands of genes. Drought induced large developmental splicing changes in leaf and ear but relatively few in tassel. Most developmental stage-specific splicing changes affected by drought were tissue dependent, whereas stage-independent changes frequently overlapped between leaf and ear. A linear relationship was found between gene expression changes in splicing factors and alternative spicing of other genes during development. Collectively, these results demonstrate that alternative splicing is strongly associated with tissue type, developmental stage, and stress condition.After transcription, the majority of eukaryotic premRNA is subjected to a series of posttranscriptional modifications, including the removal of introns to form a mature mRNA (Stamm et al., 2005). Although some introns are removed constitutively, many can be processed in a variety of alternative ways, including exon skipping, intron retention, alternative acceptor, alternative donor, and alternative position (change in both acceptor and donor positions; Lorkovic et al., 2000). These alternative splicing events form a crucial regulatory level and have the ability to alter an mRNA's stability, localization, and protein products. Alternative splicing events are controlled by a variety of cis-elements, including the presence of consensus splice sequences at the intron-exon border and intronic and exonic splicing enhancer sequences (Pertea et al., 2007). Trans-acting factors also exert a strong effect on splicing and are mostly composed of Ser/Arg-rich proteins, which typically promote intron removal, and heterogenous nuclear ribonucleoproteins, which typically inhibit it (Erkelenz et al., 2013). A host of other indirect factors can affect splicing, including transcription rate, methylation status, and any cellular conditions that alter RNA secondary structure (Kornblihtt et al

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The Transpeptidase Sortase A Binds Nucleic Acids and Mediates Mammalian Cell Labeling

Liu,

Lu,

et al. 2024

Advanced Science

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Wild‐type sortase A is an important virulence factor displaying a diverse array of proteins on the surface of bacteria. This protein display relies on the transpeptidase activity of sortase A, which is widely engineered to allow protein ligation and protein engineering based on the interaction between sortase A and peptides. Here an unknown interaction is found between sortase A from Staphylococcus aureus and nucleic acids, in which exogenously expressed engineered sortase A binds oligonucleotides in vitro and is independent of its canonical transpeptidase activity. When incubated with mammalian cells, engineered sortase A further mediates oligonucleotide labeling to the cell surface, where sortase A attaches itself and is part of the labeled moiety. The labeling reaction can also be mediated by many classes of wild‐type sortases as well. Cell surface GAG appears involved in sortase‐mediated oligonucleotide cell labeling, as demonstrated by CRISPR screening. This interaction property is utilized to develop a technique called CellID to facilitate sample multiplexing for scRNA‐seq and shows the potential of using sortases to label cells with diverse oligonucleotides. Together, the binding between sortase A and nucleic acids opens a new avenue to understanding the virulence of wild‐type sortases and exploring the application of sortases in biotechnology.

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Dynamic regulation of genome-wide pre-mRNA splicing and stress tolerance by the Sm-like protein LSm5 in Arabidopsis

Cited by 1,653 publications

References 49 publications

Role for LSM genes in the regulation of circadian rhythms

Role for LSM genes in the regulation of circadian rhythms

Genome-Wide Analysis of Alternative Splicing during Development and Drought Stress in Maize

The Transpeptidase Sortase A Binds Nucleic Acids and Mediates Mammalian Cell Labeling

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