Figure - available from: Frontiers in Plant Science
This content is subject to copyright.
Exonucleolytic mRNA degradation pathways in plants. mRNA deadenylation can be performed through three different pathways mediated by the PAN2/3 complex, the CCR4/CAF1/NOT complex, or the PARN enzyme. After deadenylation, mRNAs may be degraded in 3′-5′ direction (3′-5′ mRNA decay) or in 5′-3′ direction (5′-3′mRNA decay). In the 3′-5′ route, transcripts are degraded by the exosome or by SOV. In the case of the 5′-3′ route, it is imperative to remove the 5′ CAP structure of the transcripts by the decapping complex before their degradation by XRN4. Proteins in color represent proteins that participate in regulating plant tolerance to abiotic stress. DCP5 and VCS are positive regulators of plant tolerance to drought. SPI positively regulates Arabidopsis tolerance to high salt. The LSM1-7 complex attenuates tolerance to drought and the cold acclimation process, while promoting salt stress tolerance. Solid and dotted arrows represent established and theoretical pathways, respectively.
Source publication
It has long been assumed that the wide reprogramming of gene expression that modulates plant response to unfavorable environmental conditions is mainly controlled at the transcriptional level. A growing body of evidence, however, indicates that posttranscriptional regulatory mechanisms also play a relevant role in this control. Thus, the LSMs, a fa...
Citations
... An LSM domain-containing proteins (with an FDF domain of unknown role) are part of a complex in the mRNA de-capping machinery [70]. In Arabidopsis, the cytoplasmic LSM proteins are major regulators of abiotic stress responses including low temperature, salt, and drought stresses [71]. In addition, they regulate plant adaptation responses to adverse environmental conditions through stress-dependent regulation of mRNA turnover by targeting selected stress-inducible transcripts (LEA7, ZAT12, ABR1, ANAC019, AHK5, or ANAC092) for de-capping and degradation [71]. ...
... In Arabidopsis, the cytoplasmic LSM proteins are major regulators of abiotic stress responses including low temperature, salt, and drought stresses [71]. In addition, they regulate plant adaptation responses to adverse environmental conditions through stress-dependent regulation of mRNA turnover by targeting selected stress-inducible transcripts (LEA7, ZAT12, ABR1, ANAC019, AHK5, or ANAC092) for de-capping and degradation [71]. In our study, an LSM domain-containing protein and a late embryogenesis abundant protein (LEA-14) were associated with FHB resistance (Additional Table 1) suggesting that the LSM domain-containing proteins and their targets may also be involved in the regulation of plant biotic stress responses in the SHDW panel. ...
Fusarium head blight (FHB), caused by Fusarium graminearum, is one of the most destructive wheat diseases worldwide. FHB infection can dramatically reduce grain yield and quality due to mycotoxins contamination. Wheat resistance to FHB is quantitatively inherited and many low-effect quantitative trait loci (QTL) have been mapped in the wheat genome. Synthetic hexaploid wheat (SHW) represents a novel source of FHB resistance derived from Aegilops tauschii and Triticum turgidum that can be transferred into common wheat (T. aestivum). In this study, a panel of 194 spring Synthetic Hexaploid Derived Wheat (SHDW) lines from the International Maize and Wheat Improvement Center (CIMMYT) was evaluated for FHB response under field conditions over three years (2017–2019). A significant phenotypic variation was found for disease incidence, severity, index, number of Fusarium Damaged Kernels (FDKs), and deoxynivalenol (DON) content. Further, 11 accessions displayed < 10 ppm DON in 2017 and 2019. Genotyping of the SHDW panel using a 90 K Single Nucleotide Polymorphism (SNP) chip array revealed 31 K polymorphic SNPs with a minor allele frequency (MAF) > 5%, which were used for a Genome-Wide Association Study (GWAS) of FHB resistance. A total of 52 significant marker-trait associations for FHB resistance were identified. These included 5 for DON content, 13 for the percentage of FDKs, 11 for the FHB index, 3 for disease incidence, and 20 for disease severity. A survey of genes associated with the markers identified 395 candidate genes that may be involved in FHB resistance. Collectively, our results strongly support the view that utilization of synthetic hexaploid wheat in wheat breeding would enhance diversity and introduce new sources of resistance against FHB into the common wheat gene pool. Further, validated SNP markers associated with FHB resistance may facilitate the screening of wheat populations for FHB resistance.
... LSm are grouped into two complexes: LSm 1-7, mainly involved in the decapping process [4,40] , and LSm 2-8, which makes up the core of U6 [24,28,30]. These proteins have been related to multiple regulatory functions, being considered in plants as a key piece in the adaptation and response to environmental changes [7,19]. Having to interact with two different components of the spliceosome, these donor sites might present characteristic patterns of specificity that echo evolutionary divergent processes [46]. ...
Despite the fact that the main steps of the splicing process are similar across eukaryotes, differences in splicing factors, gene architecture and sequence divergences in splicing signals suggest clade-specific features of splicing and its regulation.
In this work we study conserved and divergent signatures embedded in the sequence composition of eukaryotic 5’ splicing sites. We considered a regularized maximum entropy modeling framework to mine for non-trivial two-site correlations in donor sequences of 14 different eukaryote organisms. Our approach allowed us to accommodate and extend in a unified framework many of the regularities observed in previous works, like the relationship between the frequency of occurrence of natural sequences and the corresponding site’s strength, or the negative epistatic effects between exonic and intronic consensus sites. In addition, performing a systematic and comparative analysis of 5’ss we showed that lineage information could be traced not only from single-site frequencies but also from joint di-nucleotide probabilities of donor sequences. Noticeably, we could also identify specific two-site coupling patterns for plants and for animals and argue that these differences, in association with taxon-specific features involving U6 snRNP, could be the basis for differences in splicing regulation previously reported between these groups.
... The results showed that RNA degradation pathway was enriched in a total of 4 proteins, namely antiviral helicase (SKI2), snRNA-related Sm-like protein (LSM1), snRNA-related Sm-like protein (LSM6), and phosphopyruvate hydratase (ERR3). LSM1 promoted the assembly of the LSM1-7 complex in the cytoplasm, which was a key component of the decap machine and played a vital role in the 5'− 3' mRNA attenuation pathway (Catalá et al., 2019). Exosomes were crucial in the 3' to 5' mRNA degradation pathway. ...
Paraquat (PQ) is a non-selective herbicide with strong toxicity to humans and mammals. However, the proteome regulation of cells by PQ is still unclear, limiting the development of effective antidotes. Studies have shown that a slight excess of intracellular copper levels could be beneficial to the survival under exposure to PQ. In this study, Saccharomyces cerevisiae was used as a model to explore the regulation effect of copper ions on PQ poisoning by the approach of date independent acquisition proteomics. The results showed that toxic effect of PQ was primarily induced by oxidative damage in the mitochondria and the disorder of gene expression. The addition of Cu²⁺ involved a series of favorable reactions to cell survival under PQ stress, including activation of the mitogen-activated protein kinase signaling pathway, regulation of processes such as sulfur metabolism, carbon metabolism and gene expression in cells. The generation of glutathione, heme and steroids advantageous to cell growth under stress was also increased. These findings inferred that therapeutic concentration of copper ions could prolong the survival of cells under PQ stress.
... Interestingly, under salt stress conditions, mis-spliced genes, such as CALCIUM EXCHANGER1 and RARE-COLD-INDUCIBLE 2A (RCI2A), could be largely associated with the Gene Ontology terms related to ABA signalling, salt stress, and response to cold temperature (Cui et al., 2014). In addition, CALCIUM EXCHANGER1 and RCI2A have been shown to play an important role in drought stress response and cold acclimation (Nylander et al., 2001;Catalá et al., 2019). Furthermore, LSM5 also regulates the splicing of A. thaliana clock genes, including TIMING OF CAB EXPRESSION1 (Perez-Santángelo et al., 2014), which undergoes AS under low temperatures (James et al., 2012). ...
... The expression of LSM8 is induced by exposure to cold ambient temperatures, and its mutation causes a cold-sensitive phenotype, with splicing defects enriched in IR (Carrasco-López et al., 2017). Moreover, the GC content and length of LSM8-targeted introns differ greatly between abiotic stress conditions (Carrasco- López et al., 2017;Catalá et al., 2019). A current hypothesis is that GC content and intron length could alter the secondary RNA structure, in this way determining splice site accessibility after cold acclimation (Carrasco-López et al., 2017;Catalá et al., 2019). ...
... Moreover, the GC content and length of LSM8-targeted introns differ greatly between abiotic stress conditions (Carrasco- López et al., 2017;Catalá et al., 2019). A current hypothesis is that GC content and intron length could alter the secondary RNA structure, in this way determining splice site accessibility after cold acclimation (Carrasco-López et al., 2017;Catalá et al., 2019). ...
Alternative splicing occurs in all eukaryotic organisms. Since the first description of multiexon genes and the splicing machinery, the field has expanded rapidly, especially in animals and yeast. However, our knowledge about splicing in plants is still quite fragmented. Though eukaryotes show some similarity in the composition and dynamics of the splicing machinery, observations of unique plant traits are only starting to emerge. For instance, plant alternative splicing is closely linked to their ability to perceive various environmental stimuli. Due to their sessile lifestyle, temperature is a central source of information allowing plants to adjust their development to match current growth conditions. Hence, seasonal temperature fluctuations and day-night cycles can strongly influence plant morphology across developmental stages. Here we discuss the available data about temperature-dependent alternative splicing in plants. Given its fragmented state it is not always possible to fit specific observations into a coherent picture, yet it is sufficient to estimate the complexity of this field and the need of further research. Better understanding of alternative splicing as a part of plant temperature response and adaptation may also prove to be a powerful tool for both, fundamental and applied sciences.
... This pattern indicates that the occurrence of the alternative transcript could be involved on modulation of caffeine synthase expression. In plants, the LSM gene family is involved in posttranscriptional events, specifically selecting RNA targets for processing, splicing or degradation, frequently in response to abiotic stress (Catalá et al., 2019). Also, Arabidopsis plants with mutations on LSM genes have defective development patterns, suggesting the importance of active LSMs to control development-related gene expression (Perea-Resa et al., 2012). ...
Differential gene expression profiles and metabolic networks are valuable tools for the genetic characterization of agronomic traits. In this study, we used large-scale expression analyses to identify modified biological processes in caffeine-free coffee plants. The first step was the large-scale sequencing of RNA from young and developing tissues of caffeine-free plants (AC1) and plants with normal concentrations of the compound (MN). The resulting 65,000 sequences were analyzed in silico for identification of 171 genes with differential expression between treatments, and establishment of metabolic networks associated with levels of caffeine. Few genes were mapped onto metabolic pathways, indicating that low caffeine has no major effects on physiological processes. The differential expression observed in silico was validated for 12 selected genes in field experiments using qPCR. The expression profile of 5 genes differed on the analyses, and the rest confirmed the in silico profile. Among the validated genes two of them, FIG and LSM-l, may control other agronomic traits associated with low caffeine content in coffee tissues. These genes are potential markers for use in association with other current markers for assisted selection of low-caffeine coffee. Therefore, they may improve the efficiency and effectiveness of coffee breeding programs.
... As part of the LSM complexes, LSM2 plays roles in RNA surveillance and regulates decay of AUrich elements (AREs) containing mRNAs, which encode many genes involved in immunity and inflammation [62]. As described above for DDX39B, LSM rings also play important roles in regulating the stress response in plants [63]. ...
Here we review data suggestive of a role for RBPs in vertebrate immunity. We focus on the products of genes found in the class III region of the Major Histocompatibility Complex. Six of these genes, DDX39B (aka BAT1), DXO, LSM2, NELFE, PRRC2A (aka BAT2), and SKIV2L, encode RNA binding proteins with clear roles in post-transcriptional gene regulation and RNA surveillance. These genes are likely to have important functions in immunity and are associated with autoimmune diseases.
... Pre-mRNA processing is carried out by the spliceosome, which is formed by the association of several snRNPs, each one including a snRNA (U1, U2, U4, U5 and U6) and numerous associated proteins. Among them, the Sm and Sm-like (LSM) proteins form two core nuclear heteroheptameric complexes, the Sm and the LSM2-8, each one directly binding a snRNA (19). The Sm complex associates to the U1, U2, U4 and U5 snRNAs, while LSM2-8 binds specifically the U6 snRNA. ...
Although originally identified as the components of the complex aiding the cytosolic chaperonin CCT in the folding of actins and tubulins in the cytosol, prefoldins (PFDs) are emerging as novel regulators influencing gene expression in the nucleus. Work conducted mainly in yeast and animals showed that PFDs act as transcriptional regulators and participate in the nuclear proteostasis. To investigate new functions of PFDs, we performed a co-expression analysis in Arabidopsis thaliana. Results revealed co-expression between PFD and the Sm-like (LSM) genes, which encode the LSM2-8 spliceosome core complex, in this model organism. Here, we show that PFDs interact with and are required to maintain adequate levels of the LSM2-8 complex. Our data indicate that levels of the LSM8 protein, which defines and confers the functional specificity of the complex, are reduced in pfd mutants and in response to the Hsp90 inhibitor geldanamycin. We provide biochemical evidence showing that LSM8 is a client of Hsp90 and that PFD4 mediates the interaction between both proteins. Consistent with our results and with the role of the LSM2-8 complex in splicing through the stabilization of the U6 snRNA, pfd mutants showed reduced levels of this snRNA and altered pre-mRNA splicing patterns.
... -SL-miRNA-K1 managed to specifically enrich, among others, the helicase DHX15 (Treiber et al., 2017), a component of the tri-snRNP complex LSM2 (Catala et al., 2019), a major nucleolar protein involves in pre-rRNA maturation NUCL (Woo et al., 2017), a splicing protein SUGP1 (Treiber et al., 2017), and TADBP (Bhardwaj et al., 2013) a protein involves in various RNA biogenesis. ...
MicroRNAs arepost-transcriptional regulators of gene expression. Shared by all eukaryotes and some virus, deciphering their regulation is essential to understand cellular physiology. microRNA precursors can be expressed individually or in cluster within a so-called primary transcript. However, structural and sequence features of these precursors are not sufficient to describe their differential maturation. This project involves the search for a protein cofactor involved in the specific maturation of miRNA expressed by the human herpesvirus type 8 within a primary transcript possessing 10 microRNA precursors. RNA chromatographies have been carried out to identify potential proteins involved in the specific maturation of virus micoRNAs. Screening, expression and analysis tools have been put in place to begin describing the molecular mechanism underlying specific miRNA precursor maturation.
Plants undergo transcriptome reprogramming to adapt to daily and seasonal fluctuations in light and temperature conditions. While most efforts have focused on the role of master transcription factors, the importance of splicing factors modulating these processes is now emerging. Efficient pre-mRNA splicing depends on proper spliceosome assembly, which in plants and animals requires the methylosome complex. Ion Chloride nucleotide-sensitive protein (PICLN) is part of the methylosome complex in both humans and Arabidopsis (Arabidopsis thaliana), and we show here that the human PICLN ortholog rescues phenotypes of Arabidopsis picln mutants. Altered photomorphogenic and photoperiodic responses in Arabidopsis picln mutants are associated with changes in pre-mRNA splicing that partially overlap with those in PROTEIN-ARGININE METHYL TRANSFERASE5 (prmt5) mutants. Mammalian PICLN also acts in concert with the Survival Motor Neuron (SMN) complex component GEMIN2 to modulate the late steps of UsnRNP assembly, and many alternative splicing events regulated by PICLN but not PRMT5, the main protein of the methylosome, are controlled by Arabidopsis GEMIN2. As with GEMIN2 and SM PROTEIN E1/PORCUPINE (SME1/PCP), low temperature, which increases PICLN expression, aggravates morphological and molecular defects of picln mutants. Taken together, these results establish a key role for PICLN in the regulation of pre-mRNA splicing and in mediating plant adaptation to daily and seasonal fluctuations in environmental conditions.
Les nématodes parasites de plante du genre Meloidogyne, ou nématodes à galles, constituent un problème phytosanitaire majeur à l’échelle mondiale. Ces parasites obligatoires des plantes ont élaboré des mécanismes de parasitisme originaux et complexes. Grâce à l’injection dans la plante hôte de protéines appelées « effecteurs », ils induisent une reprogrammation cellulaire et la transformation de cellules racinaires en cellules nourricières hypertrophiées et polynucléées, nommées « cellules géantes ». Le déterminisme de ces structures néoformées chez la plante reste très mal connu. Au cours de ma thèse, je me suis intéressé à deux protéines sécrétées par le nématode à galles M. incognita, l’effecteur 18 codé par un gène pionnier (MiEFF18) et une protéine disulfide isomérase (MiPDI). Nous avons identifié par une stratégie de double hybride en levures leurs cibles protéiques chez la plante et nous avons étudié leurs rôles dans l’interaction et la formation des cellules géantes. Des expériences d’immunolocalisation ont permis de démontrer que la protéine MiEFF18 est produite dans les glandes salivaires, s’accumule dans des granules de sécrétion indiquant qu’elle serait sécrétée in planta via le stylet. L’utilisation de fusions traductionnelles entre MiEFF18 et la GFP a montré que cet effecteur s’accumulait dans le noyau et le nucléole des cellules végétales. Les protéines SmD1 ont été identifié comme cibles de MiEFF18 chez la tomate, Arabidopsis et en N. benthamiana. Ces protéines SmD1 sont des composants conservés, essentiels du spliceosome et de la machinerie eucaryote d’épissage des ARN messagers. Le séquençage des transcrits (RNAseq) de plants sauvages d’Arabidopsis thaliana, de plantes surexprimant MiEFF18, ou mutantes (knock-out) pour le gène AtSmD1b, montre que cet effecteur est capable de moduler la fonction de régulateur de l’épissage alternatif de SmD1 et que sa surexpression modifie l'expression de gènes importants pour l'ontogenèse des cellules géantes. MiEFF18 module également la fonction de la protéine SmD1 dans le déclenchement d’une voie de « silencing » spécifique appelée S-PTGS (« sense transgene post-transcriptional gene silencing »). Nous avons pu montrer que des plantes d’Arabidopsis thaliana, de tomate (Solanum lycopersicum) et de Nicotiana benthamiana chez lesquelles l’expression de SmD1 est affectée présentent une résistance accrue aux nématodes à galles et que la fonction de l’effecteur EFF18 est conservée chez d’autres espèces de Meloidogyne. Les effecteurs EFF18 sont donc capables de manipuler les différentes fonctions de SmD1 afin de favoriser la formation des cellules géantes lors de l’infection chez Arabidopsis et deux Solanacées (tomate et N. benthamiana). Dans un second temps, nous avons pu démontrer la sécrétion de l’effecteur MiPDI-1 dans les cellules géantes. La stratégie de double hybride en levures a permis d’identifier sa cible végétale, la protéine associée au stress 12 (SAP12) chez la tomate et Arabidopsis. La protéine SAP12 est capable de déceler l’état d’oxydoréduction environnant et est impliquée dans la défense des plantes et la réponse à divers stress abiotiques. L’analyse fonctionnelle de ce couple effecteur-cible a permis de montrer que la manipulation de la protéine SAP12 par MiPDI-1 est indispensable au succès parasitaire de M. incognita, afin de (i) protéger les larves des espèces actives de l’oxygène produites au cours de la pénétration de l’hôte et (ii) de moduler l’expression de gènes impliqués dans la défense et la réponse aux stress au cours du parasitisme. L’ensemble de ces travaux montrent l’importance de l’étude du dialogue moléculaire entre le parasite et la plante et la caractérisation des protéines ciblées par ces bioagresseurs pour le développement de nouvelles formes de résistance contre ces ravageurs des cultures.
