Title: Prediction of conserved and variable heat and cold stress response in maize using cis-regulatory information
Abstract Changes in gene expression are important for responses to abiotic stress. Transcriptome profiling of heat- or cold-stressed maize genotypes identifies many changes in transcript abundance. We used comparisons of expression responses in multiple genotypes to identify alleles with variable responses to heat or cold stress and to distinguish examples of cis- or trans-regulatory variation for stress-responsive expression changes. We used motifs enriched near the transcription start sites (TSSs) for thermal stress-responsive genes to develop predictive models of gene expression responses. Prediction accuracies can be improved by focusing only on motifs within unmethylated regions near the TSS and vary for genes with different dynamic responses to stress. Models trained on expression responses in a single genotype and promoter sequences provided lower performance when applied to other genotypes but this could be improved by using models trained on data from all three genotypes tested. The analysis of genes with cis-regulatory variation provides evidence for structural variants that result in presence/absence of transcription factor binding sites in creating variable responses. This study provides insights into cis-regulatory motifs for heat- and cold-responsive gene expression and defines a framework for developing models to predict expression responses across multiple genotypes. more »« less
Many plant species exhibit genetic variation for coping with environmental stress. However, there are still limited approaches to effectively uncover the genomic region that regulates distinct responsive patterns of the gene across multiple varieties within the same species under abiotic stress.
Results
By analyzing the transcriptomes of more than 100 maize inbreds, we reveal manycis- andtrans-acting eQTLs that influence the expression response to heat stress. Thecis-acting eQTLs in response to heat stress are identified in genes with differential responses to heat stress between genotypes as well as genes that are only expressed under heat stress. Thecis-acting variants for heat stress-responsive expression likely result from distinct promoter activities, and the differential heat responses of the alleles are confirmed for selected genes using transient expression assays. Global footprinting of transcription factor binding is performed in control and heat stress conditions to document regions with heat-enriched transcription factor binding occupancies.
Conclusions
Footprints enriched near proximal regions of characterized heat-responsive genes in a large association panel can be utilized for prioritizing functional genomic regions that regulate genotype-specific responses under heat stress.
Azodi, Christina B; Lloyd, John P; Shiu, Shin-Han(
, NAR Genomics and Bioinformatics)
null
(Ed.)
Abstract 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.
Plants respond to abiotic stress through a variety of physiological, biochemical, and transcriptional mechanisms. Many genes exhibit altered levels of expression in response to abiotic stress, which requires concerted action of bothcis‐andtrans‐regulatory features. In order to study the variability in transcriptome response to abiotic stress,RNAsequencing was performed using 14‐day‐old maize seedlings of inbreds B73, Mo17, Oh43,PH207 and B37 under control, cold and heat conditions. Large numbers of genes that responded differentially to stress between parental inbred lines were identified.RNAsequencing was also performed on similar tissues of theF1hybrids produced by crossing B73 and each of the three other inbred lines. By evaluating allele‐specific transcript abundance in theF1hybrids, we were able to measure the abundance ofcis‐andtrans‐regulatory variation between genotypes for both steady‐state and stress‐responsive expression differences. Although examples oftrans‐regulatory variation were observed,cis‐regulatory variation was more common for both steady‐state and stress‐responsive expression differences. The genes withcis‐allelic variation for response to cold or heat stress provided an opportunity to study the basis for regulatory diversity.
The evolution of transcriptional regulatory mechanisms is central to how stress response and tolerance differ between species. However, it remains largely unknown how divergence in cis-regulatory sites and, subsequently, transcription factor (TF) binding specificity contribute to stress-responsive expression divergence, particularly between wild and domesticated spe-cies. By profiling wound-responsive gene transcriptomes in wild Solanum pennellii and do-mesticated S. lycopersicum, we found extensive wound-response divergence and identified 493 S. lycopersicum and 278 S. pennellii putative cis-regulatory elements (pCREs) that were predictive of wound-responsive gene expression. Only 24-52% of these wound-response pCREs (depending on wound-response patterns) were consistently enriched in the putative promoter regions of wound-responsive genes across species. In addition, between these two species, their differences in pCRE site sequences were significantly and positively correlated with differences in wound-responsive gene expression. Furthermore, ~11-39% of pCREs were specific to only one of the species and likely bound by TFs from different families. These findings indicate substantial regulatory divergence in these two plant species that di-verged ~3-7 million years ago. Our study provides insights into the mechanistic basis of how the transcriptional response to wounding is regulated and, importantly, the contribution of cis-regulatory components to variation in wound-responsive gene expression between a wild and a domesticated plant species.
Plants are subjected to extreme environmental conditions and must adapt rapidly. The phytohormone abscisic acid (ABA) accumulates during abiotic stress, signaling transcriptional changes that trigger physiological responses. Epigenetic modifications often facilitate transcription, particularly at genes exhibiting temporal, tissue-specific and environmentally-induced expression. In maize ( Zea mays ), MEDIATOR OF PARAMUTATION 1 (MOP1) is required for progression of an RNA-dependent epigenetic pathway that regulates transcriptional silencing of loci genomewide. MOP1 function has been previously correlated with genomic regions adjoining particular types of transposable elements and genic regions, suggesting that this regulatory pathway functions to maintain distinct transcriptional activities within genomic spaces, and that loss of MOP1 may modify the responsiveness of some loci to other regulatory pathways. As critical regulators of gene expression, MOP1 and ABA pathways each regulate specific genes. To determine whether loss of MOP1 impacts ABA-responsive gene expression in maize, mop1-1 and Mop1 homozygous seedlings were subjected to exogenous ABA and RNA-sequencing. A total of 3,242 differentially expressed genes (DEGs) were identified in four pairwise comparisons. Overall, ABA-induced changes in gene expression were enhanced in mop1-1 homozygous plants. The highest number of DEGs were identified in ABA-induced mop1-1 mutants, including many transcription factors; this suggests combinatorial regulatory scenarios including direct and indirect transcriptional responses to genetic disruption ( mop1-1 ) and/or stimulus-induction of a hierarchical, cascading network of responsive genes. Additionally, a modest increase in CHH methylation at putative MOP1-RdDM loci in response to ABA was observed in some genotypes, suggesting that epigenetic variation might influence environmentally-induced transcriptional responses in maize.
Zhou, Peng, Enders, Tara A, Myers, Zachary A, Magnusson, Erika, Crisp, Peter A, Noshay, Jaclyn M, Gomez-Cano, Fabio, Liang, Zhikai, Grotewold, Erich, Greenham, Kathleen, and Springer, Nathan M. Prediction of conserved and variable heat and cold stress response in maize using cis-regulatory information. Retrieved from https://par.nsf.gov/biblio/10313985. The Plant Cell 34.1 Web. doi:10.1093/plcell/koab267.
Zhou, Peng, Enders, Tara A, Myers, Zachary A, Magnusson, Erika, Crisp, Peter A, Noshay, Jaclyn M, Gomez-Cano, Fabio, Liang, Zhikai, Grotewold, Erich, Greenham, Kathleen, & Springer, Nathan M. Prediction of conserved and variable heat and cold stress response in maize using cis-regulatory information. The Plant Cell, 34 (1). Retrieved from https://par.nsf.gov/biblio/10313985. https://doi.org/10.1093/plcell/koab267
Zhou, Peng, Enders, Tara A, Myers, Zachary A, Magnusson, Erika, Crisp, Peter A, Noshay, Jaclyn M, Gomez-Cano, Fabio, Liang, Zhikai, Grotewold, Erich, Greenham, Kathleen, and Springer, Nathan M.
"Prediction of conserved and variable heat and cold stress response in maize using cis-regulatory information". The Plant Cell 34 (1). Country unknown/Code not available. https://doi.org/10.1093/plcell/koab267.https://par.nsf.gov/biblio/10313985.
@article{osti_10313985,
place = {Country unknown/Code not available},
title = {Prediction of conserved and variable heat and cold stress response in maize using cis-regulatory information},
url = {https://par.nsf.gov/biblio/10313985},
DOI = {10.1093/plcell/koab267},
abstractNote = {Abstract Changes in gene expression are important for responses to abiotic stress. Transcriptome profiling of heat- or cold-stressed maize genotypes identifies many changes in transcript abundance. We used comparisons of expression responses in multiple genotypes to identify alleles with variable responses to heat or cold stress and to distinguish examples of cis- or trans-regulatory variation for stress-responsive expression changes. We used motifs enriched near the transcription start sites (TSSs) for thermal stress-responsive genes to develop predictive models of gene expression responses. Prediction accuracies can be improved by focusing only on motifs within unmethylated regions near the TSS and vary for genes with different dynamic responses to stress. Models trained on expression responses in a single genotype and promoter sequences provided lower performance when applied to other genotypes but this could be improved by using models trained on data from all three genotypes tested. The analysis of genes with cis-regulatory variation provides evidence for structural variants that result in presence/absence of transcription factor binding sites in creating variable responses. This study provides insights into cis-regulatory motifs for heat- and cold-responsive gene expression and defines a framework for developing models to predict expression responses across multiple genotypes.},
journal = {The Plant Cell},
volume = {34},
number = {1},
author = {Zhou, Peng and Enders, Tara A and Myers, Zachary A and Magnusson, Erika and Crisp, Peter A and Noshay, Jaclyn M and Gomez-Cano, Fabio and Liang, Zhikai and Grotewold, Erich and Greenham, Kathleen and Springer, Nathan M},
}
Warning: Leaving National Science Foundation Website
You are now leaving the National Science Foundation website to go to a non-government website.
Website:
NSF takes no responsibility for and exercises no control over the views expressed or the accuracy of
the information contained on this site. Also be aware that NSF's privacy policy does not apply to this site.
