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1.
Plant Cell ; 36(6): 2219-2237, 2024 May 29.
Artigo em Inglês | MEDLINE | ID: mdl-38518124

RESUMO

Arabidopsis (Arabidopsis thaliana) PROTEIN ARGININE METHYLTRANSFERASE5 (PRMT5) post-translationally modifies RNA-binding proteins by arginine (R) methylation. However, the impact of this modification on the regulation of RNA processing is largely unknown. We used the spliceosome component, SM-LIKE PROTEIN 4 (LSM4), as a paradigm to study the role of R-methylation in RNA processing. We found that LSM4 regulates alternative splicing (AS) of a suite of its in vivo targets identified here. The lsm4 and prmt5 mutants show a considerable overlap of genes with altered AS raising the possibility that splicing of those genes could be regulated by PRMT5-dependent LSM4 methylation. Indeed, LSM4 methylation impacts AS, particularly of genes linked with stress response. Wild-type LSM4 and an unmethylable version complement the lsm4-1 mutant, suggesting that methylation is not critical for growth in normal environments. However, LSM4 methylation increases with abscisic acid and is necessary for plants to grow under abiotic stress. Conversely, bacterial infection reduces LSM4 methylation, and plants that express unmethylable-LSM4 are more resistant to Pseudomonas than those expressing wild-type LSM4. This tolerance correlates with decreased intron retention of immune-response genes upon infection. Taken together, this provides direct evidence that R-methylation adjusts LSM4 function on pre-mRNA splicing in an antagonistic manner in response to biotic and abiotic stress.


Assuntos
Processamento Alternativo , Proteínas de Arabidopsis , Arabidopsis , Arginina , Regulação da Expressão Gênica de Plantas , Proteína-Arginina N-Metiltransferases , Estresse Fisiológico , Arabidopsis/genética , Arabidopsis/metabolismo , Proteínas de Arabidopsis/genética , Proteínas de Arabidopsis/metabolismo , Processamento Alternativo/genética , Metilação , Proteína-Arginina N-Metiltransferases/metabolismo , Proteína-Arginina N-Metiltransferases/genética , Estresse Fisiológico/genética , Arginina/metabolismo , Ácido Abscísico/metabolismo , Proteínas de Ligação a RNA/metabolismo , Proteínas de Ligação a RNA/genética , Mutação/genética
2.
Plant Cell Physiol ; 63(11): 1709-1719, 2022 Nov 22.
Artigo em Inglês | MEDLINE | ID: mdl-36066193

RESUMO

Circadian rhythms enable organisms to anticipate and adjust their physiology to periodic environmental changes. These rhythms are controlled by biological clocks that consist of a set of clock genes that regulate each other's expression. Circadian oscillations in messenger RNA (mRNA) levels require the regulation of mRNA production and degradation. While transcription factors controlling clock function have been well characterized from cyanobacteria to humans, the role of factors controlling mRNA decay is largely unknown. Here, we show that mutations in SM-LIKE PROTEIN 1 (LSM1) and exoribonucleases 4 (XRN4), components of the 5'-3' mRNA decay pathway, alter clock function in Arabidopsis. We found that lsm1 and xrn4 mutants display long-period phenotypes for clock gene expression. In xrn4, these circadian defects were associated with changes in circadian phases of expression, but not overall mRNA levels, of several core-clock genes. We then used noninvasive transcriptome-wide mRNA stability analysis to identify genes and pathways regulated by XRN4. Among genes affected in the xrn4 mutant at the transcriptional and posttranscriptional level, we found an enrichment in genes involved in auxin, ethylene and drought recovery. Large effects were not observed for canonical core-clock genes, although the mRNAs of several auxiliary clock genes that control the pace of the clock were stabilized in xrn4 mutants. Our results establish that the 5'-3' mRNA decay pathway constitutes a novel posttranscriptional regulatory layer of the circadian gene network, which probably acts through a combination of small effects on mRNA stability of several auxiliary and some core-clock genes.


Assuntos
Proteínas de Arabidopsis , Arabidopsis , Relógios Circadianos , Humanos , Arabidopsis/metabolismo , Proteínas de Arabidopsis/genética , Proteínas de Arabidopsis/metabolismo , RNA Mensageiro/genética , RNA Mensageiro/metabolismo , Regulação da Expressão Gênica de Plantas , Relógios Circadianos/genética , Estabilidade de RNA/genética
3.
Plant J ; 103(2): 889-902, 2020 07.
Artigo em Inglês | MEDLINE | ID: mdl-32314836

RESUMO

The circadian clock of Arabidopsis thaliana controls many physiological and molecular processes, allowing plants to anticipate daily changes in their environment. However, developing a detailed understanding of how oscillations in mRNA levels are connected to oscillations in co/post-transcriptional processes, such as splicing, has remained a challenge. Here we applied a combined approach using deep transcriptome sequencing and bioinformatics tools to identify novel circadian-regulated genes and splicing events. Using a stringent approach, we identified 300 intron retention, eight exon skipping, 79 alternative 3' splice site usage, 48 alternative 5' splice site usage, and 350 multiple (more than one event type) annotated events under circadian regulation. We also found seven and 721 novel alternative exonic and intronic events. Depletion of the circadian-regulated splicing factor AtSPF30 homologue resulted in the disruption of a subset of clock-controlled splicing events. Altogether, our global circadian RNA-seq coupled with an in silico, event-centred, splicing analysis tool offers a new approach for studying the interplay between the circadian clock and the splicing machinery at a global scale. The identification of many circadian-regulated splicing events broadens our current understanding of the level of control that the circadian clock has over this co/post-transcriptional regulatory layer.


Assuntos
Processamento Alternativo , Arabidopsis/metabolismo , Ritmo Circadiano , Perfilação da Expressão Gênica , Processamento Alternativo/fisiologia , Arabidopsis/genética , Arabidopsis/fisiologia , Ritmo Circadiano/fisiologia , Genes de Plantas/genética , Transcriptoma
4.
Proc Natl Acad Sci U S A ; 112(30): 9382-7, 2015 Jul 28.
Artigo em Inglês | MEDLINE | ID: mdl-26170331

RESUMO

The mechanisms by which poikilothermic organisms ensure that biological processes are robust to temperature changes are largely unknown. Temperature compensation, the ability of circadian rhythms to maintain a relatively constant period over the broad range of temperatures resulting from seasonal fluctuations in environmental conditions, is a defining property of circadian networks. Temperature affects the alternative splicing (AS) of several clock genes in fungi, plants, and flies, but the splicing factors that modulate these effects to ensure clock accuracy throughout the year remain to be identified. Here we show that GEMIN2, a spliceosomal small nuclear ribonucleoprotein assembly factor conserved from yeast to humans, modulates low temperature effects on a large subset of pre-mRNA splicing events. In particular, GEMIN2 controls the AS of several clock genes and attenuates the effects of temperature on the circadian period in Arabidopsis thaliana. We conclude that GEMIN2 is a key component of a posttranscriptional regulatory mechanism that ensures the appropriate acclimation of plants to daily and seasonal changes in temperature conditions.


Assuntos
Proteínas de Arabidopsis/genética , Arabidopsis/genética , Regulação da Expressão Gênica de Plantas , Proteínas do Complexo SMN/fisiologia , Processamento Alternativo , Sequência de Aminoácidos , Arabidopsis/fisiologia , Proteínas de Arabidopsis/fisiologia , Ritmo Circadiano , Análise por Conglomerados , Evolução Molecular , Perfilação da Expressão Gênica , Regulação da Expressão Gênica , Teste de Complementação Genética , Estudo de Associação Genômica Ampla , Humanos , Íntrons , Dados de Sequência Molecular , Mutação , Proteínas do Tecido Nervoso/genética , Folhas de Planta/fisiologia , RNA Nuclear Pequeno/genética , Proteínas de Ligação a RNA/genética , Proteínas do Complexo SMN/genética , Homologia de Sequência de Aminoácidos , Spliceossomos/fisiologia , Temperatura , Transcrição Gênica
5.
Proc Natl Acad Sci U S A ; 111(42): 15166-71, 2014 Oct 21.
Artigo em Inglês | MEDLINE | ID: mdl-25288739

RESUMO

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.


Assuntos
Proteínas de Arabidopsis/fisiologia , Ritmo Circadiano , Proteínas de Ligação a RNA/fisiologia , Ribonucleoproteínas Nucleares Pequenas/fisiologia , Alelos , Processamento Alternativo , Animais , Arabidopsis/metabolismo , Proteínas de Arabidopsis/genética , Linhagem Celular Tumoral , Regulação da Expressão Gênica de Plantas , Genômica , Humanos , Camundongos , Camundongos Transgênicos , Mutação , Fenótipo , Folhas de Planta/metabolismo , Proteínas de Plantas/metabolismo , RNA Interferente Pequeno/metabolismo , Proteínas de Ligação a RNA/genética , Ribonucleoproteínas Nucleares Pequenas/genética , Análise de Sequência de RNA , Transdução de Sinais , Spliceossomos/metabolismo , Núcleo Supraquiasmático/metabolismo
6.
Plants (Basel) ; 11(3)2022 Jan 18.
Artigo em Inglês | MEDLINE | ID: mdl-35161220

RESUMO

Plants use seasonal cues to initiate flowering at an appropriate time of year to ensure optimal reproductive success. The circadian clock integrates these daily and seasonal cues with internal cues to initiate flowering. The molecular pathways that control the sensitivity of flowering to photoperiods (daylengths) are well described in the model plant Arabidopsis. However, much less is known for crop species, such as legumes. Here, we performed a flowering time screen of a TILLING population of Medicago truncatula and found a line with late-flowering and altered light-sensing phenotypes. Using RNA sequencing, we identified a nonsense mutation in the Phytochromobilin synthase (MtPΦBS) gene, which encodes an enzyme that carries out the final step in the biosynthesis of the chromophore required for phytochrome (phy) activity. The analysis of the circadian clock in the MtpΦbs mutant revealed a shorter circadian period, which was shared with the MtphyA mutant. The MtpΦbs and MtphyA mutants showed downregulation of the FT floral regulators MtFTa1 and MtFTb1/b2 and a change in phase for morning and night core clock genes. Our findings show that phyA is necessary to synchronize the circadian clock and integration of light signalling to precisely control the timing of flowering.

7.
Brief Funct Genomics ; 12(1): 13-24, 2013 Jan.
Artigo em Inglês | MEDLINE | ID: mdl-23165351

RESUMO

Circadian clocks, the molecular devices present in almost all eukaryotic and some prokaryotic organisms, phase biological activities to the most appropriate time of day. These devices are synchronized by the daily cycles of light and temperature, and control hundreds of processes, ranging from gene expression to behavior as well as reproductive development. For a long time, these clocks were considered to operate primarily through regulatory feedback loops that act at the transcriptional level. Recent studies, however, conclusively show that circadian rhythms can persist in the absence of transcription, and it is evident that robust and precise circadian oscillations require multiple regulatory mechanisms operating at the co-/post-transcriptional, translational, post-translational and metabolic levels. Furthermore, these different regulatory loops exhibit strong interactions, which contribute to the synchronization of biological rhythms with environmental changes throughout the day and year. Here, we describe recent advances that highlight the role of alternative splicing (AS) in the operation of circadian networks, focusing on molecular and genomic studies conducted in Arabidopsis thaliana. These studies have also enhanced our understanding of the mechanisms that control AS and of the physiological impact of AS.


Assuntos
Processamento Alternativo/genética , Relógios Circadianos/genética , Redes Reguladoras de Genes/genética , Genômica/métodos , Animais , Humanos , Plantas/genética , Transdução de Sinais/genética
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