Subgroup-specific intrinsic disorder profiles of Arabidopsis NAC transcription factors: Identification of functional hotspots.
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ABSTRACT:
SUBMITTER: Stender EG
PROVIDER: S-EPMC4622513 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Intrinsic disorder (ID) is highly abundant in eukaryotes, which reflect the greater need for disorder-associated signaling and transcriptional regulation in nucleated cells. Although several well-characterized examples of intrinsically disordered proteins in transcriptional regulation have been reported, no systematic analysis has been reported so far. To test for the general prevalence of intrinsic disorder in transcriptional regulation, we used the predictor of natural disorder regions (PONDR) to analyze the abundance of intrinsic disorder in three transcription factor datasets and two control sets. This analysis revealed that from 94.13 to 82.63% of transcription factors possess extended regions of intrinsic disorder, relative to 54.51 and 18.64% of the proteins in two control datasets, which indicates the significant prevalence of intrinsic disorder in transcription factors. This propensity of transcription factors to intrinsic disorder was confirmed by cumulative distribution function analysis and charge-hydropathy plots. The amino acid composition analysis showed that all three transcription factor datasets were substantially depleted in order-promoting residues and significantly enriched in disorder-promoting residues. Our analysis of the distribution of disorder within the transcription factor datasets revealed that (a) the AT-hooks and basic regions of transcription factor DNA-binding domains are highly disordered; (b) the degree of disorder in transcription factor activation regions is much higher than that in DNA-binding domains; (c) the degree of disorder is significantly higher in eukaryotic transcription factors than in prokaryotic transcription factors; and (d) the level of alpha-MoRF (molecular recognition feature) prediction is much higher in transcription factors. Overall, our data reflected the fact that eukaryotes with well-developed gene transcription machinery require transcription factor flexibility to be more efficient.
| S-EPMC2538555 | biostudies-literature
Project description:Pre-exposing (priming) plants to mild, non-lethal elevated temperature improves their tolerance to a later higher-temperature stress (triggering stimulus), which is of great ecological importance. 'Thermomemory' is maintaining this tolerance for an extended period of time. NAM/ATAF1/2/CUC2 (NAC) proteins are plant-specific transcription factors (TFs) that modulate responses to abiotic stresses, including heat stress (HS). Here, we investigated the potential role of NACs for thermomemory. We determined the expression of 104 Arabidopsis NAC genes after priming and triggering heat stimuli, and found ATAF1 expression is strongly induced right after priming and declines below control levels thereafter during thermorecovery. Knockout mutants of ATAF1 show better thermomemory than wild type, revealing a negative regulatory role. Differential expression analyses of RNA-seq data from ATAF1 overexpressor, ataf1 mutant and wild-type plants after heat priming revealed five genes that might be priming-associated direct targets of ATAF1: AT2G31260 (ATG9), AT2G41640 (GT61), AT3G44990 (XTH31), AT4G27720 and AT3G23540. Based on co-expression analyses applied to the aforementioned RNA-seq profiles, we identified ANAC055 to be transcriptionally co-regulated with ATAF1. Like ataf1, anac055 mutants show improved thermomemory, revealing a potential co-control of both NAC TFs over thermomemory. Our data reveals a core importance of two NAC transcription factors, ATAF1 and ANAC055, for thermomemory.
| S-EPMC9253118 | biostudies-literature
Project description:Eukaryotic cells are complex biological systems that depend on highly connected molecular interaction networks with intrinsically disordered proteins as essential components. Through specific examples, we relate the conformational ensemble nature of intrinsic disorder (ID) in transcription factors to functions in plants. Transcription factors contain large regulatory ID-regions with numerous orphan sequence motifs, representing potential important interaction sites. ID-regions may affect DNA-binding through electrostatic interactions or allosterically as for the bZIP transcription factors, in which the DNA-binding domains also populate ensembles of dynamic transient structures. The flexibility of ID is well-suited for interaction networks requiring efficient molecular adjustments. For example, Radical Induced Cell Death1 depends on ID in transcription factors for its numerous, structurally heterogeneous interactions, and the JAZ:MYC:MED15 regulatory unit depends on protein dynamics, including binding-associated unfolding, for regulation of jasmonate-signaling. Flexibility makes ID-regions excellent targets of posttranslational modifications. For example, the extent of phosphorylation of the NAC transcription factor SOG1 regulates target gene expression and the DNA-damage response, and phosphorylation of the AP2/ERF transcription factor DREB2A acts as a switch enabling heat-regulated degradation. ID-related phase separation is emerging as being important to transcriptional regulation with condensates functioning in storage and inactivation of transcription factors. The applicative potential of ID-regions is apparent, as removal of an ID-region of the AP2/ERF transcription factor WRI1 affects its stability and consequently oil biosynthesis. The highlighted examples show that ID plays essential functional roles in plant biology and has a promising potential in engineering.
| S-EPMC7767404 | biostudies-literature
Project description:BackgroundPlants are continuously challenged by different environment stresses, and they vary widely in their adjustability. NAC (NAM, ATAF and CUC) transcription factors are known to be crucial in plants tolerance response to abiotic stresses, such as drought and salinity. ANAC019, ANAC055, and ANAC072, belong to the stress-NAC TFs, confer the Arabidopsis abiotic stress tolerance.ResultsHere we isolated two stress-responsive NACs, CiNAC3 and CiNAC4, from Caragana intermedia, which were induced by ABA and various abiotic stresses. Localization assays revealed that CiNAC3 and CiNAC4 localized in the nuclei, consistent with their roles as transcription factors. Histochemistry assay using Pro(CiNAC4)::GUS transgenic Arabidopsis showed that the expression of the GUS reporter was observed in many tissues of the transgenic plants, especially in the root vascular system. Overexpression of CiNAC3 and CiNAC4 reduced ABA sensitivity during seed germination, and enhanced salt tolerance of the transgenic Arabidopsis.ConclusionsWe characterised CiNAC3 and CiNAC4 and found that they were induced by numerous abiotic stresses and ABA. GUS histochemical assay of CiNAC4 promoter suggested that root, flower and local damaged tissues were the strongest stained tissues. Overexpression assay revealed that CiNAC4 play essential roles not only in promoting lateral roots formation, but also in responding to salinity and ABA treatment of Arabidopsis.
| S-EPMC4546137 | biostudies-literature
Project description:Transcription factors (TFs) regulate the expression of genes at the transcriptional level. Modification of TF activity dynamically alters the transcriptome, which leads to metabolic and phenotypic changes. Thus, functional analysis of TFs using 'omics-based' methodologies is one of the most important areas of the post-genome era. In this mini-review, we present an overview of Arabidopsis TFs and introduce strategies for the functional analysis of plant TFs, which include both traditional and recently developed technologies. These strategies can be assigned to five categories: bioinformatic analysis; analysis of molecular function; expression analysis; phenotype analysis; and network analysis for the description of entire transcriptional regulatory networks.
| S-EPMC2709548 | biostudies-literature
Project description:Controlled proteolytic cleavage of membrane-associated transcription factors (MTFs) is an intriguing activation strategy that ensures rapid transcriptional responses to incoming stimuli. Several MTFs are known to regulate diverse cellular functions in prokaryotes, yeast, and animals. In Arabidopsis, a few NAC MTFs mediate either cytokinin signaling during cell division or endoplasmic reticulum (ER) stress responses. Through genome-wide analysis, it was found that at least 13 members of the NAC family in Arabidopsis contain strong alpha-helical transmembrane motifs (TMs) in their C-terminal regions and are predicted to be membrane-associated. Interestingly, most of the putative NAC MTF genes are up-regulated by stress conditions, suggesting that they may be involved in stress responses. Notably, transgenic studies revealed that membrane release is essential for the function of NAC MTFs. Transgenic plants overexpressing partial-size NAC constructs devoid of the TMs, but not those overexpressing full-size constructs, showed distinct phenotypic changes, including dwarfed growth and delayed flowering. The rice genome also contains more than six NAC MTFs. Furthermore, the presence of numerous MTFs is predicted in the whole transcription factors in plants. We thus propose that proteolytic activation of MTFs is a genome-wide mechanism regulating plant genomes.
| S-EPMC1802569 | biostudies-literature
Project description:Target gene identification for transcription factors is a prerequisite for the systems wide understanding of organismal behaviour. NAM-ATAF1/2-CUC2 (NAC) transcription factors are amongst the largest transcription factor families in plants, yet limited data exist from unbiased approaches to resolve the DNA-binding preferences of individual members. Here, we present a TF-target gene identification workflow based on the integration of novel protein binding microarray data with gene expression and multi-species promoter sequence conservation to identify the DNA-binding specificities and the gene regulatory networks of 12 NAC transcription factors. Our data offer specific single-base resolution fingerprints for most TFs studied and indicate that NAC DNA-binding specificities might be predicted from their DNA-binding domain's sequence. The developed methodology, including the application of complementary functional genomics filters, makes it possible to translate, for each TF, protein binding microarray data into a set of high-quality target genes. With this approach, we confirm NAC target genes reported from independent in vivo analyses. We emphasize that candidate target gene sets together with the workflow associated with functional modules offer a strong resource to unravel the regulatory potential of NAC genes and that this workflow could be used to study other families of transcription factors.
| S-EPMC4081100 | biostudies-literature
Project description:BackgroundNAC proteins contribute to diverse plant developmental processes as well as tolerances to biotic and abiotic stresses. The pear genome had been decoded and provided the basis for the genome-wide analysis to find the evolution, duplication, gene structures and predicted functions of PpNAC transcription factors.ResultsA total of 185 PpNAC genes were found in pear, of which 148 were mapped on chromosomes while 37 were on unanchored scaffolds. Phylogeny split the NAC genes into 6 clades (Group1- Group6) with their sub clades (~ subgroup A to subgroup H) and each group displayed common motifs with no/minor change. The numbers of exons in each group varied from 1 to 12 with an average of 3 while 44 pairs from all groups showed their duplication events. qPCR and RNA-Seq data analyses in different pear cultivars/species revealed some predicted functions of PpNAC genes i.e. PpNACs 37, 61, 70 (2A), 53, 151(2D), 10, 92, 130 and 154 (3D) were potentially involved in bud endodormancy, PpNACs 61, 70 (2A), 172, 176 and 23 (4E) were associated with fruit pigmentations in blue light, PpNACs 127 (1E), 46 (1G) and 56 (5A) might be related to early, middle and late fruit developments respectively. Besides, all genes from subgroups 2D and 3D were found to be related with abiotic stress (cold, salt and drought) tolerances by targeting the stress responsive genes in pear.ConclusionsThe present genome-wide analysis provided valuable information for understanding the classification, motif and gene structure, evolution and predicted functions of NAC gene family in pear as well as in higher plants. NAC TFs play diverse and multifunctional roles in biotic and abiotic stresses, growth and development and fruit ripening and pigmentation through multiple pathways in pear.
| S-EPMC6169067 | biostudies-literature
Project description:The membrane-bound NAC transcription (NTL) factors have been demonstrated to participate in the regulation of plant development and the responses to multiple environmental stresses. This study is aimed to functionally characterize soybean NTL transcription factors in response to Al-toxicity, which is largely uncharacterized. The qRT-PCR assays in the present study found that thirteen out of fifteen GmNTL genes in the soybean genome were up-regulated by Al toxicity. However, among the Al-up-regulated GmNTLs selected from six duplicate gene pairs, only overexpressing GmNTL1, GmNTL4, and GmNTL10 could confer Arabidopsis Al resistance. Further comprehensive functional characterization of GmNTL4 showed that the expression of this gene in response to Al stress depended on root tissues, as well as the Al concentration and period of Al treatment. Overexpression of GmNTL4 conferred Al tolerance of transgenic Arabidopsis in long-term (48 and 72 h) Al treatments. Moreover, RNA-seq assay identified 517 DEGs regulated by GmNTL4 in Arabidopsis responsive to Al stress, which included MATEs, ALMTs, PMEs, and XTHs. These results suggest that the function of GmNTLs in Al responses is divergent, and GmNTL4 might confer Al resistance partially by regulating the expression of genes involved in organic acid efflux and cell wall modification.
| S-EPMC8657865 | biostudies-literature
Project description:A model is presented describing the gene regulatory network surrounding three similar NAC transcription factors that have roles in Arabidopsis leaf senescence and stress responses. ANAC019, ANAC055 and ANAC072 belong to the same clade of NAC domain genes and have overlapping expression patterns. A combination of promoter DNA/protein interactions identified using yeast 1-hybrid analysis and modelling using gene expression time course data has been applied to predict the regulatory network upstream of these genes. Similarities and divergence in regulation during a variety of stress responses are predicted by different combinations of upstream transcription factors binding and also by the modelling. Mutant analysis with potential upstream genes was used to test and confirm some of the predicted interactions. Gene expression analysis in mutants of ANAC019 and ANAC055 at different times during leaf senescence has revealed a distinctly different role for each of these genes. Yeast 1-hybrid analysis is shown to be a valuable tool that can distinguish clades of binding proteins and be used to test and quantify protein binding to predicted promoter motifs.
| S-EPMC3781708 | biostudies-literature