Prediction of conserved and variable heat and cold stress response in maize using cis-regulatory information.
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ABSTRACT:
SUBMITTER: Zhou P
PROVIDER: S-EPMC8773969 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:The Heat Shock Factor (HSF) transcription factor family is a central and required component of plant heat stress responses and acquired thermotolerance. The HSF family has dramatically expanded in plant lineages, often including a repertoire of 20 or more genes. Here we assess and compare the composition, heat responsiveness, and chromatin profiles of the HSF families in maize and Setaria viridis (Setaria), two model C4 panicoid grasses. Both species encode a similar number of HSFs, and examples of both conserved and variable expression responses to a heat stress event were observed between the two species. Chromatin accessibility and genome-wide DNA-binding profiles were generated to assess the chromatin of HSF family members with distinct responses to heat stress. We observed significant variability for both chromatin accessibility and promoter occupancy within similarly regulated sets of HSFs between Setaria and maize, as well as between syntenic pairs of maize HSFs retained following its most recent genome duplication event. Additionally, we observed the widespread presence of TF binding at HSF promoters in control conditions, even at HSFs that are only expressed in response to heat stress. TF-binding peaks were typically near putative HSF-binding sites in HSFs upregulated in response to heat stress, but not in stable or not expressed HSFs. These observations collectively support a complex scenario of expansion and subfunctionalization within this transcription factor family and suggest that within-family HSF transcriptional regulation is a conserved, defining feature of the family.
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Project description:Gene expression differences between divergent lineages caused by modification of cis regulatory elements are thought to be important in evolution. We assayed genome-wide cis and trans regulatory differences between maize and its wild progenitor, teosinte, using deep RNA sequencing in F1 hybrid and parent inbred lines for three tissue types (ear, leaf and stem). Pervasive regulatory variation was observed with approximately 70% of ∼17,000 genes showing evidence of regulatory divergence between maize and teosinte. However, many fewer genes (1,079 genes) show consistent cis differences with all sampled maize and teosinte lines. For ∼70% of these 1,079 genes, the cis differences are specific to a single tissue. The number of genes with cis regulatory differences is greatest for ear tissue, which underwent a drastic transformation in form during domestication. As expected from the domestication bottleneck, maize possesses less cis regulatory variation than teosinte with this deficit greatest for genes showing maize-teosinte cis regulatory divergence, suggesting selection on cis regulatory differences during domestication. Consistent with selection on cis regulatory elements, genes with cis effects correlated strongly with genes under positive selection during maize domestication and improvement, while genes with trans regulatory effects did not. We observed a directional bias such that genes with cis differences showed higher expression of the maize allele more often than the teosinte allele, suggesting domestication favored up-regulation of gene expression. Finally, this work documents the cis and trans regulatory changes between maize and teosinte in over 17,000 genes for three tissues.
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Project description:MotivationThe accurate discovery and annotation of regulatory elements remains a challenging problem. The growing number of sequenced genomes creates new opportunities for comparative approaches to motif discovery. Putative binding sites are then considered to be functional if they are conserved in orthologous promoter sequences of multiple related species. Existing methods for comparative motif discovery usually rely on pregenerated multiple sequence alignments, which are difficult to obtain for more diverged species such as plants. As a consequence, misaligned regulatory elements often remain undetected.ResultsWe present a novel algorithm that supports both alignment-free and alignment-based motif discovery in the promoter sequences of related species. Putative motifs are exhaustively enumerated as words over the IUPAC alphabet and screened for conservation using the branch length score. Additionally, a confidence score is established in a genome-wide fashion. In order to take advantage of a cloud computing infrastructure, the MapReduce programming model is adopted. The method is applied to four monocotyledon plant species and it is shown that high-scoring motifs are significantly enriched for open chromatin regions in Oryza sativa and for transcription factor binding sites inferred through protein-binding microarrays in O.sativa and Zea mays. Furthermore, the method is shown to recover experimentally profiled ga2ox1-like KN1 binding sites in Z.mays.Availability and implementationBLSSpeller was written in Java. Source code and manual are available at http://bioinformatics.intec.ugent.be/blsspellerContactKlaas.Vandepoele@psb.vib-ugent.be or jan.fostier@intec.ugent.be.Supplementary informationSupplementary data are available at Bioinformatics online.
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Project description:Genetic mapping studies on crops suggest that agronomic traits can be controlled by gene-distal intergenic loci. Despite the biological importance and the potential agronomic utility of these loci, they remain virtually uncharacterized in all crop species to date. Here, we provide genetic, epigenomic and functional molecular evidence to support the widespread existence of gene-distal (hereafter, distal) loci that act as long-range transcriptional cis-regulatory elements (CREs) in the maize genome. Such loci are enriched for euchromatic features that suggest their regulatory functions. Chromatin loops link together putative CREs with genes and recapitulate genetic interactions. Putative CREs also display elevated transcriptional enhancer activities, as measured by self-transcribing active regulatory region sequencing. These results provide functional support for the widespread existence of CREs that act over large genomic distances to control gene expression.
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Project description:Heat stress induced reactive oxygen species in maize silks are correlated with pollen tube growth arrest and sterility
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Project description:Adverse environmental conditions such as heat and salt stress create endoplasmic reticulum (ER) stress in maize and set off the unfolded protein response (UPR). A key feature of the UPR is the upregulation of ZmbZIP60 and the splicing of its messenger RNA. We conducted an association analysis of a recombinant inbred line (RIL) derived from a cross of a tropical founder line, CML52 with a standard temperate line, B73. We found a major QTL conditioning heat-induced ZmbZIP60 expression located cis to the gene. Based on the premise that the QTL might be associated with the ZmbZIP60 promoter, we evaluated various maize inbred lines for their ability to upregulate the expression of ZmbZIP60 in response to heat stress. In general, tropical lines with promoter regions similar to CML52 were more robust in upregulating ZmbZIP60 in response to heat stress. This finding was confirmed by comparing the strength of the B73 and CML52 ZmbZIP60 promoters in transient maize protoplast assays. We concluded that the upstream region of ZmbZIP60 is important in conditioning the response to heat stress and was under selection in maize when adapted to different environments. Summary: Heat stress has large negative effects on maize grain yield. Heat stress creates ER stress in maize and sets off the UPR. We searched for factors conditioning heat induction of the UPR in maize seedlings by conducting an association analysis based on the upregulation of unspliced and spliced forms of ZmbZIP60 mRNA (ZmbZIP60u and ZmbZIP60s, respectively). ZmbZIP60u was upregulated more robustly by heat stress in the tropical maize line, CML52, than in B73, and a major QTL derived from the analysis of RILs from a cross of these two lines mapped in the vicinity of ZmbZIP60. We conducted a cis/trans test to determine whether the QTL was acting as a cis regulatory element or in trans, as might be expected for a transcription factor. We found that the QTL was acting in cis, likely involving the ZmbZIP60 promoter. ZmbZIP60 promoters in other temperate and tropical lines similar to CML52 showed enhanced expression of ZmbZIP60u by heat. The contribution of the CML52 promoter to heat induction of ZmbZIP60 was confirmed by analyzing the CML52 and B73 promoters linked to a luciferase reporter and assayed in heat-treated maize protoplasts.
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Project description:Computational methods attempting to identify instances of cis-regulatory modules (CRMs) in the genome face a challenging problem of searching for potentially interacting transcription factor binding sites while knowledge of the specific interactions involved remains limited. Without a comprehensive comparison of their performance, the reliability and accuracy of these tools remains unclear. Faced with a large number of different tools that address this problem, we summarized and categorized them based on search strategy and input data requirements. Twelve representative methods were chosen and applied to predict CRMs from the Drosophila CRM database REDfly, and across the human ENCODE regions. Our results show that the optimal choice of method varies depending on species and composition of the sequences in question. When discriminating CRMs from non-coding regions, those methods considering evolutionary conservation have a stronger predictive power than methods designed to be run on a single genome. Different CRM representations and search strategies rely on different CRM properties, and different methods can complement one another. For example, some favour homotypical clusters of binding sites, while others perform best on short CRMs. Furthermore, most methods appear to be sensitive to the composition and structure of the genome to which they are applied. We analyze the principal features that distinguish the methods that performed well, identify weaknesses leading to poor performance, and provide a guide for users. We also propose key considerations for the development and evaluation of future CRM-prediction methods.
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Project description:Among developmental control genes, transcription factor-target gene "linkages"--the direct connections between target genes and the factors that control their patterns of expression--can show remarkable evolutionary stability. However, the specific binding sites that mediate and define these regulatory connections are themselves often subject to rapid turnover. Here we describe several instances in which particular transcription factor binding motif combinations have evidently been conserved upstream of orthologous target genes for extraordinarily long evolutionary periods. This occurs against a backdrop in which other binding sites for the same factors are coming and going rapidly. Our examples include a particular Dpp Silencer Element upstream of insect brinker genes, in combination with a novel motif we refer to as the Downstream Element; combinations of a Suppressor of Hairless Paired Site (SPS) and a specific proneural protein binding site associated with arthropod Notch pathway target genes; and a three-motif combination, also including an SPS, upstream of deuterostome Hes repressor genes, which are also Notch targets. We propose that these stable motif architectures have been conserved intact from a deep ancestor, in part because they mediate a special mode of regulation that cannot be supplied by the other, unstable motif instances.
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Project description:Maize is an important cereal crop but is sensitive to heat stress, which significantly restricts its grain yield. To explore the molecular mechanism of maize heat tolerance, a heat-tolerant hybrid ZD309 and its parental lines (H39_1 and M189) were subjected to heat stress, followed by transcriptomic and metabolomic analyses. After six-day-heat treatment, the growth of ZD309 and its parental lines were suppressed, showing dwarf stature and rolled leaf compared with the control plants. ZD309 exhibited vigorous growth; however, M189 displayed superior heat tolerance. By transcriptomic and metabolomic analysis, hundreds to thousands of differentially expressed genes (DEGs) and metabolites (DEMs) were identified. Notably, the female parent H39 shares more DEGs and DEMs with the hybrid ZD309, indicating more genetic gain derived from the female instead of the male. A total of 299 heat shock genes detected among three genotypes were greatly aggregated in sugar transmembrane transporter activity, plasma membrane, photosynthesis, protein processing in the endoplasmic reticulum, cysteine, and methionine metabolism. A total of 150 heat-responsive metabolites detected among three genotypes were highly accumulated, including jasmonic acid, amino acids, sugar, flavonoids, coumarin, and organic acids. Integrating transcriptomic and metabolomic assays revealed that plant hormone signal transduction, cysteine, and methionine metabolism, and α-linolenic acid metabolism play crucial roles in heat tolerance in maize. Our research will be facilitated to identify essential heat tolerance genes in maize, thereby contributing to breeding heat resistance maize varieties.
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Project description:Plants respond to their environment by dynamically modulating gene expression. A powerful approach for understanding how these responses are regulated is to integrate information about cis-regulatory elements (CREs) into models called cis-regulatory codes. Transcriptional response to combined stress is typically not the sum of the responses to the individual stresses. However, cis-regulatory codes underlying combined stress response have not been established. Here we modeled transcriptional response to single and combined heat and drought stress in Arabidopsis thaliana. We grouped genes by their pattern of response (independent, antagonistic and synergistic) and trained machine learning models to predict their response using putative CREs (pCREs) as features (median F-measure = 0.64). We then developed a deep learning approach to integrate additional omics information (sequence conservation, chromatin accessibility and histone modification) into our models, improving performance by 6.2%. While pCREs important for predicting independent and antagonistic responses tended to resemble binding motifs of transcription factors associated with heat and/or drought stress, important synergistic pCREs resembled binding motifs of transcription factors not known to be associated with stress. These findings demonstrate how in silico approaches can improve our understanding of the complex codes regulating response to combined stress and help us identify prime targets for future characterization.
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