Transcriptome Analysis Revealed the Dynamic and Rapid Transcriptional Reprogramming Involved in Cold Stress and Related Core Genes in the Rice Seedling Stage

Cold damage is one of the most important environmental factors influencing crop growth, development, and production. In this study, we generated a pair of near-isogenic lines (NILs), Towada and ZL31, and Towada showed more cold sensitivity than ZL31 in the rice seedling stage. To explore the transcriptional regulation mechanism and the reason for phenotypic divergence of the two lines in response to cold stress, an in-depth comparative transcriptome study under cold stress was carried out. Our analysis uncovered that rapid and high-amplitude transcriptional reprogramming occurred in the early stage of cold treatment. GO enrichment and KEGG pathway analysis indicated that genes of the response to stress, environmental adaptation, signal transduction, metabolism, photosynthesis, and the MAPK signaling pathway might form the main part of the engine for transcriptional reprogramming in response to cold stress. Furthermore, we identified four core genes, OsWRKY24, OsCAT2, OsJAZ9, and OsRR6, that were potential candidates affecting the cold sensitivity of Towada and ZL31. Genome re-sequencing analysis between the two lines revealed that only OsWRKY24 contained sequence variations which may change its transcript abundance. Our study not only provides novel insights into the cold-related transcriptional reprogramming process, but also highlights the potential candidates involved in cold stress.

[1]  Wenzhu Jiang,et al.  The OsWRKY63-OsWRKY76-OsDREB1B module regulates chilling tolerance in rice. , 2022, The Plant journal : for cell and molecular biology.

[2]  Shuhua Yang,et al.  Surviving and thriving: How plants perceive and respond to temperature stress. , 2022, Developmental cell.

[3]  Hualong Liu,et al.  An integrated analysis of the rice transcriptome and lipidome reveals lipid metabolism plays a central role in rice cold tolerance , 2022, BMC Plant Biology.

[4]  Ruiqing Li,et al.  Melatonin Alleviates Low-Temperature Stress via ABI5-Mediated Signals During Seed Germination in Rice (Oryza sativa L.) , 2021, Frontiers in Plant Science.

[5]  Shanshan Zhu,et al.  Transcriptional Activation and Phosphorylation of OsCNGC9 Confer Enhanced Chilling Tolerance in Rice. , 2020, Molecular plant.

[6]  Margaret H. Frank,et al.  TBtools - an integrative toolkit developed for interactive analyses of big biological data. , 2020, Molecular plant.

[7]  Shan Lu,et al.  CYCLIC NUCLEOTIDE-GATED ION CHANNELs 14 and 16 Promote Tolerance to Heat and Chilling in Rice1[OPEN] , 2020, Plant Physiology.

[8]  Yiting Shi,et al.  Molecular Regulation of Plant Responses to Environmental Temperatures. , 2020, Molecular plant.

[9]  Steven L Salzberg,et al.  Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype , 2019, Nature Biotechnology.

[10]  Longping Yuan,et al.  Natural variation in the HAN1 gene confers chilling tolerance in rice and allowed adaptation to a temperate climate , 2019, Proceedings of the National Academy of Sciences.

[11]  Eun Woo Son,et al.  iDEP: an integrated web application for differential expression and pathway analysis of RNA-Seq data , 2018, BMC Bioinformatics.

[12]  Xiping Wang,et al.  Early selection of bZIP73 facilitated adaptation of japonica rice to cold climates , 2018, Nature Communications.

[13]  Rod A. Wing,et al.  The rice genome revolution: from an ancient grain to Green Super Rice , 2018, Nature Reviews Genetics.

[14]  Jia Gu,et al.  fastp: an ultra-fast all-in-one FASTQ preprocessor , 2018, bioRxiv.

[15]  Yingfang Zhu,et al.  MAP Kinase Cascades Regulate the Cold Response by Modulating ICE1 Protein Stability. , 2017, Developmental cell.

[16]  Zhanying Zhang,et al.  Natural variation in CTB4a enhances rice adaptation to cold habitats , 2017, Nature Communications.

[17]  Siqi Ma,et al.  The OsMYB30 Transcription Factor Suppresses Cold Tolerance by Interacting with a JAZ Protein and Suppressing β-Amylase Expression1[OPEN] , 2017, Plant Physiology.

[18]  Petr Danecek,et al.  BCFtools/csq: haplotype-aware variant consequences , 2016, bioRxiv.

[19]  Jukon Kim,et al.  Functional analysis of a cold-responsive rice WRKY gene, OsWRKY71 , 2016, Plant Biotechnology Reports.

[20]  Q. Shen,et al.  Three WRKY transcription factors additively repress abscisic acid and gibberellin signaling in aleurone cells. , 2015, Plant science : an international journal of experimental plant biology.

[21]  Jun Xiao,et al.  COLD1 Confers Chilling Tolerance in Rice , 2015, Cell.

[22]  Tao Zhang,et al.  OsJAZ9 acts as a transcriptional regulator in jasmonate signaling and modulates salt stress tolerance in rice. , 2015, Plant science : an international journal of experimental plant biology.

[23]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

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

[25]  Wei Shi,et al.  featureCounts: an efficient general purpose program for assigning sequence reads to genomic features , 2013, Bioinform..

[26]  Kazunori Okada,et al.  WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance , 2013, Journal of experimental botany.

[27]  D. Schwartz,et al.  Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data , 2013, Rice.

[28]  Jinjie Li,et al.  Characterization and identification of cold tolerant near-isogenic lines in rice , 2012, Breeding science.

[29]  Pablo Cingolani,et al.  © 2012 Landes Bioscience. Do not distribute. , 2022 .

[30]  Chungui Lu,et al.  Plant responses to cold: Transcriptome analysis of wheat. , 2010, Plant biotechnology journal.

[31]  Lizhong Xiong,et al.  Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice , 2009, Plant Molecular Biology.

[32]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[33]  Zhong-Lin Zhang,et al.  A negative regulator encoded by a rice WRKY gene represses both abscisic acid and gibberellins signaling in aleurone cells , 2009, Plant Molecular Biology.

[34]  Jianhua Zhu,et al.  Cold stress regulation of gene expression in plants. , 2007, Trends in plant science.

[35]  M. Kojima,et al.  Overexpression of a type-A response regulator alters rice morphology and cytokinin metabolism. , 2007, Plant & cell physiology.

[36]  A. Xiong,et al.  Isolation, optimization, and functional analysis of the cDNA encoding transcription factor OsDREB1B in Oryza Sativa L. , 2007, Molecular Breeding.

[37]  K. Shinozaki,et al.  Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. , 2006, Plant & cell physiology.

[38]  Jitendra P Khurana,et al.  Bmc Plant Biology Molecular Characterization and Differential Expression of Cytokinin-responsive Type-a Response Regulators in Rice (oryza Sativa) , 2005 .

[39]  K. Shinozaki,et al.  OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. , 2003, The Plant journal : for cell and molecular biology.

[40]  Michael F. Thomashow,et al.  PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms. , 1999, Annual review of plant physiology and plant molecular biology.

[41]  O. Junttila,et al.  Cold-induced freezing tolerance in Arabidopsis. , 1999, Plant physiology.

[42]  C. Guy,et al.  Altered gene expression during cold acclimation of spinach. , 1985, Proceedings of the National Academy of Sciences of the United States of America.