Regulatory Networks of lncRNAs, miRNAs, and mRNAs in Response to Heat Stress in Wheat (Triticum Aestivum L.): An Integrated Analysis

Climate change has become a major source of concern, particularly in agriculture, because it has a significant impact on the production of economically important crops such as wheat, rice, and maize. In the present study, an attempt has been made to identify differentially expressed heat stress-responsive long non-coding RNAs (lncRNAs) in the wheat genome using publicly available wheat transcriptome data (24 SRAs) representing two conditions, namely, control and heat-stressed. A total of 10,965 lncRNAs have been identified and, among them, 153, 143, and 211 differentially expressed transcripts have been found under 0 DAT, 1 DAT, and 4 DAT heat-stress conditions, respectively. Target prediction analysis revealed that 4098 lncRNAs were targeted by 119 different miRNA responses to a plethora of environmental stresses, including heat stress. A total of 171 hub genes had 204 SSRs (simple sequence repeats), and a set of target sequences had SNP potential as well. Furthermore, gene ontology analysis revealed that the majority of the discovered lncRNAs are engaged in a variety of cellular and biological processes related to heat stress responses. Furthermore, the modeled three-dimensional (3D) structures of hub genes encoding proteins, which had an appropriate range of similarity with solved structures, provided information on their structural roles. The current study reveals many elements of gene expression regulation in wheat under heat stress, paving the way for the development of improved climate-resilient wheat cultivars.

[1]  Yingqiu Li,et al.  Role of long non-coding RNA in plant responses to abiotic stresses , 2022, Acta Physiologiae Plantarum.

[2]  D. Calderini,et al.  Transcriptomic and Physiological Response of Durum Wheat Grain to Short-Term Heat Stress during Early Grain Filling , 2021, Plants.

[3]  S. Kaur,et al.  Transcriptome based identification and validation of heat stress transcription factors in wheat progenitor species Aegilops speltoides , 2021, Scientific Reports.

[4]  Anuj Kumar,et al.  Discovery of miRNAs and Development of Heat-Responsive miRNA-SSR Markers for Characterization of Wheat Germplasm for Terminal Heat Tolerance Breeding , 2021, Frontiers in Genetics.

[5]  Xiaohan Yang,et al.  Recent Advances in the Roles of HSFs and HSPs in Heat Stress Response in Woody Plants , 2021, Frontiers in Plant Science.

[6]  Jia Liu,et al.  High-Throughput SSR Marker Development and the Analysis of Genetic Diversity in Capsicum frutescens , 2021, Horticulturae.

[7]  V. K. Mishra,et al.  Crosses with spelt improve tolerance of South Asian spring wheat to spot blotch, terminal heat stress, and their combination , 2021, Scientific Reports.

[8]  R R Mir,et al.  Development and use of miRNA-derived SSR markers for the study of genetic diversity, population structure, and characterization of genotypes for breeding heat tolerant wheat varieties , 2021, PloS one.

[9]  C. Foyer,et al.  Heat-Induced Oxidation of the Nuclei and Cytosol , 2021, Frontiers in Plant Science.

[10]  Bingru Huang,et al.  Protein phosphorylation associated with drought priming-enhanced heat tolerance in a temperate grass species , 2020, Horticulture research.

[11]  K. K. Chaturvedi,et al.  Weighted gene co-expression analysis for identification of key genes regulating heat stress in wheat , 2020, Cereal Research Communications.

[12]  Majed A. Alotaibi,et al.  Selection criteria for high-yielding and early-flowering bread wheat hybrids under heat stress , 2020, PloS one.

[13]  Anuj Kumar,et al.  Homology modeling and molecular dynamics based insights into Chalcone synthase and Chalcone isomerase in Phyllanthus emblica L. , 2020, 3 Biotech.

[14]  N. Singh,et al.  Population structure, marker-trait association and identification of candidate genes for terminal heat stress relevant traits in bread wheat (Triticum aestivum L. em Thell) , 2020, Plant Genetic Resources: Characterization and Utilization.

[15]  A. Mishra,et al.  Identification and characterization of long non-coding RNAs regulating resistant starch biosynthesis in bread wheat (Triticum aestivum L.). , 2020, Genomics.

[16]  M. Islam,et al.  Morpho-molecular screening of wheat genotypes for heat tolerance , 2020 .

[17]  Daowen Wang,et al.  Genomic and functional genomics analyses of gluten proteins and prospect for simultaneous improvement of end-use and health-related traits in wheat , 2020, Theoretical and Applied Genetics.

[18]  H. Nguyen,et al.  Molecular and genetic bases of heat stress responses in crop plants and breeding for increased resilience and productivity , 2020, Journal of experimental botany.

[19]  J. Bunce,et al.  Roles of heat shock protein and reprogramming of photosynthetic carbon metabolism in thermotolerance under elevated CO2 in maize , 2019 .

[20]  M. Seki,et al.  Histone Modifications Form Epigenetic Regulatory Networks to Regulate Abiotic Stress Response1[OPEN] , 2019, Plant Physiology.

[21]  K. Singh,et al.  Genome-wide identification, characterization, and expression profiling of SPX gene family in wheat. , 2019, International journal of biological macromolecules.

[22]  Birbal Singh,et al.  Bioinformatic Exploration of Metal-Binding Proteome of Zoonotic Pathogen Orientia tsutsugamushi , 2019, Front. Genet..

[23]  Shi-rong Guo,et al.  Systematic identification and analysis of heat-stress-responsive lncRNAs, circRNAs and miRNAs with associated co-expression and ceRNA networks in cucumber (Cucumis sativus L.). , 2019, Physiologia plantarum.

[24]  M. Domaratzki,et al.  MicroRNA-guided regulation of heat stress response in wheat , 2019, BMC Genomics.

[25]  A. Mason,et al.  Non-coding RNAs and transposable elements in plant genomes: emergence, regulatory mechanisms and roles in plant development and stress responses , 2019, Planta.

[26]  Selene L. Fernandez-Valverde,et al.  Splicing conservation signals in plant long noncoding RNAs , 2019, bioRxiv.

[27]  Liping Song,et al.  Genome-wide analysis of long non-coding RNAs unveils the regulatory roles in the heat tolerance of Chinese cabbage (Brassica rapa ssp.chinensis) , 2019, Scientific Reports.

[28]  K. Singh,et al.  Functional and structural insights into candidate genes associated with nitrogen and phosphorus nutrition in wheat (Triticum aestivum L.). , 2018, International journal of biological macromolecules.

[29]  Xiaofeng Cao,et al.  The seekers: how epigenetic modifying enzymes find their hidden genomic targets in Arabidopsis. , 2018, Current opinion in plant biology.

[30]  T. Mohapatra,et al.  Genome-wide identification and characterization of lncRNAs and miRNAs in cluster bean (Cyamopsis tetragonoloba). , 2018, Gene.

[31]  Zhimin Wang,et al.  Effects of water deficit on breadmaking quality and storage protein compositions in bread wheat (Triticum aestivum L.). , 2018, Journal of the science of food and agriculture.

[32]  Niranjan Singh,et al.  Developing a Selection Criterion for Terminal Heat Tolerance in Bread Wheat Based on Various Mopho-Physiological Traits , 2018, International Journal of Current Microbiology and Applied Sciences.

[33]  Y. Xiang,et al.  An Overview of Biomembrane Functions in Plant Responses to High-Temperature Stress , 2018, Front. Plant Sci..

[34]  X. Dai,et al.  psRNATarget: a plant small RNA target analysis server (2017 release) , 2018, Nucleic Acids Res..

[35]  Surinder Kumar,et al.  Identification, expression analysis, and molecular modeling of Iron-deficiency-specific clone 3 (Ids3)-like gene in hexaploid wheat , 2018, bioRxiv.

[36]  N. Mantri,et al.  Emerging roles of long non-coding RNAs in plant response to biotic and abiotic stresses , 2018, Critical reviews in biotechnology.

[37]  X. Tao,et al.  Identification and Expression Profile of CYPome in Perennial Ryegrass and Tall Fescue in Response to Temperature Stress , 2017, Front. Plant Sci..

[38]  C. Xie,et al.  Differential effects of a post-anthesis heat stress on wheat (Triticum aestivum L.) grain proteome determined by iTRAQ , 2017, Scientific Reports.

[39]  Shivi Tyagi,et al.  Survey of High Throughput RNA-Seq Data Reveals Potential Roles for lncRNAs during Development and Stress Response in Bread Wheat , 2017, Front. Plant Sci..

[40]  Ge Gao,et al.  CPC2: a fast and accurate coding potential calculator based on sequence intrinsic features , 2017, Nucleic Acids Res..

[41]  Uwe Scholz,et al.  MISA-web: a web server for microsatellite prediction , 2017, Bioinform..

[42]  D. Adelson,et al.  Transposable elements (TEs) contribute to stress‐related long intergenic noncoding RNAs in plants , 2017, The Plant journal : for cell and molecular biology.

[43]  Garima Bhatia,et al.  Present Scenario of Long Non-Coding RNAs in Plants , 2017, Non-coding RNA.

[44]  Li Wang,et al.  Regulation of Non-coding RNAs in Heat Stress Responses of Plants , 2016, Front. Plant Sci..

[45]  Z. Fei,et al.  Comprehensive Transcriptome Profiling Reveals Long Noncoding RNA Expression and Alternative Splicing Regulation during Fruit Development and Ripening in Kiwifruit (Actinidia chinensis) , 2016, Front. Plant Sci..

[46]  Z. Gong,et al.  The Plant Heat Stress Transcription Factors (HSFs): Structure, Regulation, and Function in Response to Abiotic Stresses , 2016, Front. Plant Sci..

[47]  H. Walia,et al.  Drought stress delays endosperm development and misregulates genes associated with cytoskeleton organization and grain quality proteins in developing wheat seeds. , 2015, Plant science : an international journal of experimental plant biology.

[48]  D. Lv,et al.  Integrated Proteome Analysis of the Wheat Embryo and Endosperm Reveals Central Metabolic Changes Involved in the Water Deficit Response during Grain Development. , 2015, Journal of agricultural and food chemistry.

[49]  Michael J E Sternberg,et al.  The Phyre2 web portal for protein modeling, prediction and analysis , 2015, Nature Protocols.

[50]  Nan Li,et al.  Phosphoproteomic analysis of the response of maize leaves to drought, heat and their combination stress , 2015, Front. Plant Sci..

[51]  H. Nayyar,et al.  Temperature stress and redox homeostasis in agricultural crops , 2015, Front. Environ. Sci..

[52]  E. Mica,et al.  Post-transcriptional and post-translational regulations of drought and heat response in plants: a spider’s web of mechanisms , 2015, Front. Plant Sci..

[53]  J. Drenth,et al.  TaHsfA6f is a transcriptional activator that regulates a suite of heat stress protection genes in wheat (Triticum aestivum L.) including previously unknown Hsf targets , 2014, Journal of experimental botany.

[54]  C. Ye,et al.  Genome-wide identification and functional prediction of novel and drought-responsive lincRNAs in Populus trichocarpa , 2014, Journal of experimental botany.

[55]  R. Groß-Hardt,et al.  Heat shock factor HSFB2a involved in gametophyte development of Arabidopsis thaliana and its expression is controlled by a heat-inducible long non-coding antisense RNA , 2014, Plant Molecular Biology.

[56]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[57]  Matias D. Zurbriggen,et al.  Novel perspectives for the engineering of abiotic stress tolerance in plants. , 2014, Current opinion in biotechnology.

[58]  Steven R. Eichten,et al.  Genome-wide discovery and characterization of maize long non-coding RNAs , 2014, Genome Biology.

[59]  M. Seki,et al.  Arabidopsis Non-Coding RNA Regulation in Abiotic Stress Responses , 2013, International journal of molecular sciences.

[60]  Q. Lu,et al.  Chloroplast Small Heat Shock Protein HSP21 Interacts with Plastid Nucleoid Protein pTAC5 and Is Essential for Chloroplast Development in Arabidopsis under Heat Stress[W] , 2013, Plant Cell.

[61]  Md. Mahabubul Alam,et al.  Physiological, Biochemical, and Molecular Mechanisms of Heat Stress Tolerance in Plants , 2013, International journal of molecular sciences.

[62]  Meng Wang,et al.  Widespread Long Noncoding RNAs as Endogenous Target Mimics for MicroRNAs in Plants1[W] , 2013, Plant Physiology.

[63]  J. Hansen,et al.  Perception of climate change , 2012, Proceedings of the National Academy of Sciences.

[64]  David R. Kelley,et al.  Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks , 2012, Nature Protocols.

[65]  Jihua Ding,et al.  A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice , 2012, Proceedings of the National Academy of Sciences.

[66]  C. Lata,et al.  Role of DREBs in regulation of abiotic stress responses in plants. , 2011, Journal of experimental botany.

[67]  Patrick Xuechun Zhao,et al.  psRNATarget: a plant small RNA target analysis server , 2011, Nucleic Acids Res..

[68]  Mingming Xin,et al.  Identification and characterization of wheat long non-protein coding RNAs responsive to powdery mildew infection and heat stress by using microarray analysis and SBS sequencing , 2011, BMC Plant Biology.

[69]  Hideaki Sugawara,et al.  The Sequence Read Archive , 2010, Nucleic Acids Res..

[70]  H. Sakurai,et al.  Novel aspects of heat shock factors: DNA recognition, chromatin modulation and gene expression , 2010, The FEBS journal.

[71]  M. Fujita,et al.  Physiological and biochemical mechanisms of nitric oxide induced abiotic stress tolerance in plants. , 2010 .

[72]  Cole Trapnell,et al.  Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. , 2010, Nature biotechnology.

[73]  J. Rinn,et al.  Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression , 2009, Proceedings of the National Academy of Sciences.

[74]  Lior Pachter,et al.  Sequence Analysis , 2020, Definitions.

[75]  Michael F. Lin,et al.  Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals , 2009, Nature.

[76]  Kazuo Shinozaki,et al.  Functional analysis of an Arabidopsis heat-shock transcription factor HsfA3 in the transcriptional cascade downstream of the DREB2A stress-regulatory system. , 2008, Biochemical and biophysical research communications.

[77]  M. Todesco,et al.  Target mimicry provides a new mechanism for regulation of microRNA activity , 2007, Nature Genetics.

[78]  K. Shinozaki,et al.  Gene networks involved in drought stress response and tolerance. , 2006, Journal of experimental botany.

[79]  Gaetano T Montelione,et al.  Evaluating protein structures determined by structural genomics consortia , 2006, Proteins.

[80]  Juan Miguel García-Gómez,et al.  BIOINFORMATICS APPLICATIONS NOTE Sequence analysis Manipulation of FASTQ data with Galaxy , 2005 .

[81]  Kapil Bharti,et al.  Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors , 2004, Journal of Biosciences.

[82]  Wolfgang Busch,et al.  Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. , 2004, The Plant journal : for cell and molecular biology.

[83]  Burkhard Morgenstern,et al.  AUGUSTUS: a web server for gene finding in eukaryotes , 2004, Nucleic Acids Res..

[84]  P. Shannon,et al.  Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks , 2003 .

[85]  J. Thornton,et al.  PROCHECK: a program to check the stereochemical quality of protein structures , 1993 .

[86]  M. Rana,et al.  Genetic diversity for developing climate-resilient wheats to achieve food security goals , 2022, Advances in Agronomy.

[87]  Santosh Kumar Upadhyay,et al.  An overview of long noncoding RNA in plants , 2021 .

[88]  T. Chaudhuri,et al.  Molecular Chaperones: Structure-Function Relationship and their Role in Protein Folding , 2018 .

[89]  K. Shinozaki,et al.  Transcriptional Regulatory Network of Plant Heat Stress Response. , 2017, Trends in plant science.

[90]  Paul Kersey,et al.  Ensembl Plants: Integrating Tools for Visualizing, Mining, and Analyzing Plant Genomics Data. , 2016, Methods in molecular biology.

[91]  B. Tyagi,et al.  Enhancing wheat production- A global perspective , 2015, The Indian Journal of Agricultural Sciences.

[92]  M. Fujita,et al.  Plant Response and Tolerance to Abiotic Oxidative Stress: Antioxidant Defense Is a Key Factor , 2012 .

[93]  Sibum Sung,et al.  Long noncoding RNA: unveiling hidden layer of gene regulatory networks. , 2012, Trends in plant science.

[94]  A. Orellana,et al.  The physiological role of the unfolded protein response in plants. , 2011, Biological research.

[95]  V. Chinnusamy,et al.  SMALL RNAs: BIG ROLE IN ABIOTIC STRESS TOLERANCE OF PLANTS , 2007 .