Evolutionary Landscape of Tea Circular RNAs and Its Contribution to Chilling Tolerance of Tea Plant

Chilling stress threatens the yield and distribution pattern of global crops, including the tea plant (Camellia sinensis), one of the most important cash crops around the world. Circular RNA (circRNA) plays roles in regulating plant growth and biotic/abiotic stress responses. Understanding the evolutionary characteristics of circRNA and its feedbacks to chilling stress in the tea plant will help to elucidate the vital roles of circRNAs. In the current report, we systematically identified 2702 high-confidence circRNAs under chilling stress in the tea plant, and interestingly found that the generation of tea plant circRNAs was associated with the length of their flanking introns. Repetitive sequences annotation and DNA methylation analysis revealed that the longer flanking introns of circRNAs present more repetitive sequences and higher methylation levels, which suggested that repeat-elements-mediated DNA methylation might promote the circRNAs biogenesis in the tea plant. We further detected 250 differentially expressed circRNAs under chilling stress, which were functionally enriched in GO terms related to cold/stress responses. Constructing a circRNA-miRNA-mRNA interaction network discovered 139 differentially expressed circRNAs harboring potential miRNA binding sites, which further identified 14 circRNAs that might contribute to tea plant chilling responses. We further characterized a key circRNA, CSS-circFAB1, which was significantly induced under chilling stress. FISH and silencing experiments revealed that CSS-circFAB1 was potentially involved in chilling tolerance of the tea plant. Our study emphasizes the importance of circRNA and its preliminary role against low-temperature stress, providing new insights for tea plant cold tolerance breeding.

[1]  L. Fan,et al.  PlantcircBase 7.0: Full-length transcripts and conservation of plant circRNAs , 2022, Plant communications.

[2]  Hua Zhao,et al.  A rapid and efficient transient expression system for gene function and subcellular localization studies in the tea plant (Camellia sinensis) leaves , 2022, Scientia Horticulturae.

[3]  W. Tong,et al.  Characterization of CsWRKY29 and CsWRKY37 transcription factors and their functional roles in cold tolerance of tea plant , 2022, Beverage Plant Research.

[4]  L. Fan,et al.  Recent origination of circular RNAs in plants. , 2021, The New phytologist.

[5]  A. Fernie,et al.  CsbZIP1-CsMYB12 mediates the production of bitter-tasting flavonols in tea plants (Camellia sinensis) through a coordinated activator–repressor network , 2021, Horticulture research.

[6]  W. Tong,et al.  Divergent DNA methylation contributes to duplicated gene evolution and chilling response in tea plants. , 2021, The Plant journal : for cell and molecular biology.

[7]  S. Jacobsen,et al.  Whole genome characterization of chronological age-associated changes in methylome and circular RNAs in moso bamboo (Phyllostachys edulis) from vegetative to floral growth. , 2021, The Plant journal : for cell and molecular biology.

[8]  S. Gill,et al.  Understanding the role of miRNAs for improvement of tea quality and stress tolerance. , 2021, Journal of biotechnology.

[9]  Peng Guo,et al.  Genome-Wide Identification of Copper Stress-Regulated and Novel MicroRNAs in Mulberry Leaf , 2021, Biochemical Genetics.

[10]  OUP accepted manuscript , 2021, Plant Physiology.

[11]  G. Zinta,et al.  Genome-Wide Identification of Circular RNAs in Response to Low-Temperature Stress in Tomato Leaves , 2020, Frontiers in Genetics.

[12]  A. Hasi,et al.  Genome-wide identification of microRNAs involved in the regulation of fruit ripening and climacteric stages in melon (Cucumis melo) , 2020, Horticulture Research.

[13]  W. Tong,et al.  The reference genome of tea plant and resequencing of 81 diverse accessions provide insights into genome evolution and adaptation of tea plants. , 2020, Molecular plant.

[14]  Jietang Zhao,et al.  Integrated sRNAome and RNA-Seq analysis reveals miRNA effects on betalain biosynthesis in pitaya , 2020, BMC Plant Biology.

[15]  Xinyuan Hao,et al.  ABA-dependent bZIP transcription factor, CsbZIP18, from Camellia sinensis negatively regulates freezing tolerance in Arabidopsis , 2020, Plant Cell Reports.

[16]  F. Zhao,et al.  Accurate quantification of circular RNAs identifies extensive circular isoform switching events , 2020, Nature Communications.

[17]  W. Schwab,et al.  Sesquiterpene glucosylation mediated by glucosyltransferase UGT91Q2 is involved in the modulation of cold stress tolerance in tea plants. , 2019, The New phytologist.

[18]  Chi-Tang Ho,et al.  Chemistry and Biological Activities of Processed Camellia sinensis Teas: A Comprehensive Review. , 2019, Comprehensive reviews in food science and food safety.

[19]  Sebastian Kadener,et al.  Past, present, and future of circRNAs , 2019, The EMBO journal.

[20]  J. Bennetzen,et al.  Comparative transcriptomic analysis reveals gene expression associated with cold adaptation in the tea plant Camellia sinensis , 2019, BMC Genomics.

[21]  Liping Zhao,et al.  Characterization and Cloning of Grape Circular RNAs Identified the Cold Resistance-Related Vv-circATS11 , 2019, Plant Physiology.

[22]  Tongbao Lin,et al.  Identification and characterization of CircRNAs involved in the regulation of wheat root length , 2019, Biological Research.

[23]  W. Terzaghi,et al.  A large-scale circular RNA profiling reveals universal molecular mechanisms responsive to drought stress in maize and Arabidopsis. , 2019, The Plant journal : for cell and molecular biology.

[24]  Ana Kozomara,et al.  miRBase: from microRNA sequences to function , 2018, Nucleic Acids Res..

[25]  J. Bennetzen,et al.  Circular RNA architecture and differentiation during leaf bud to young leaf development in tea (Camellia sinensis) , 2018, Planta.

[26]  Brent S. Pedersen,et al.  GOATOOLS: A Python library for Gene Ontology analyses , 2018, Scientific Reports.

[27]  Yuchun Wang,et al.  Transcriptome sequencing dissection of the mechanisms underlying differential cold sensitivity in young and mature leaves of the tea plant (Camellia sinensis). , 2018, Journal of plant physiology.

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

[29]  Patrick S. Schnable,et al.  Circular RNAs mediated by transposons are associated with transcriptomic and phenotypic variation in maize. , 2018, The New phytologist.

[30]  Jian Wang,et al.  SOAPnuke: a MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data , 2017, GigaScience.

[31]  G. C. da Fonseca,et al.  Circular RNAs and Plant Stress Responses. , 2018, Advances in experimental medicine and biology.

[32]  Honghui Lin,et al.  Heat stress alters genome-wide profiles of circular RNAs in Arabidopsis , 2018, Plant Molecular Biology.

[33]  Xueying Guan,et al.  Characterization of conserved circular RNA in polyploid Gossypium species and their ancestors , 2017, FEBS letters.

[34]  Yizan Ma,et al.  microRNAs involved in auxin signalling modulate male sterility under high‐temperature stress in cotton (Gossypium hirsutum) , 2017, The Plant journal : for cell and molecular biology.

[35]  En-Hua Xia,et al.  The Tea Tree Genome Provides Insights into Tea Flavor and Independent Evolution of Caffeine Biosynthesis. , 2017, Molecular plant.

[36]  Hongwen Huang,et al.  Identification of Circular RNAs in Kiwifruit and Their Species-Specific Response to Bacterial Canker Pathogen Invasion , 2017, Front. Plant Sci..

[37]  C. De-la-Peña,et al.  Localization of miRNAs by In Situ Hybridization in Plants Using Conventional Oligonucleotide Probes. , 2017, Methods in molecular biology.

[38]  I. Kovalchuk.  Plant Epigenetics , 2017, Methods in Molecular Biology.

[39]  Yunbo Luo,et al.  Deciphering the roles of circRNAs on chilling injury in tomato. , 2016, Biochemical and biophysical research communications.

[40]  Liwang Liu,et al.  Identification of microRNAs and Their Target Genes Explores miRNA-Mediated Regulatory Network of Cytoplasmic Male Sterility Occurrence during Anther Development in Radish (Raphanus sativus L.) , 2016, Front. Plant Sci..

[41]  Ping Liu,et al.  Tracing the expression of circular RNAs in human pre-implantation embryos , 2016, Genome Biology.

[42]  Qi Feng,et al.  Transcriptome-wide investigation of circular RNAs in rice , 2015, RNA.

[43]  Qian-Hao Zhu,et al.  Widespread noncoding circular RNAs in plants. , 2015, The New phytologist.

[44]  O. Kohany,et al.  Repbase Update, a database of repetitive elements in eukaryotic genomes , 2015, Mobile DNA.

[45]  Yinfei Zhang,et al.  Integrated RNA-Seq and sRNA-Seq Analysis Identifies Chilling and Freezing Responsive Key Molecular Players and Pathways in Tea Plant (Camellia sinensis) , 2015, PloS one.

[46]  Christoph Dieterich,et al.  Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. , 2015, Cell reports.

[47]  Mingle Wang,et al.  Identification and characterization of cold-responsive microRNAs in tea plant (Camellia sinensis) and their targets using high-throughput sequencing and degradome analysis , 2014, BMC Plant Biology.

[48]  Dongming Liang,et al.  Short intronic repeat sequences facilitate circular RNA production , 2014, Genes & development.

[49]  N. Sharpless,et al.  Detecting and characterizing circular RNAs , 2014, Nature Biotechnology.

[50]  P. Brown,et al.  Circular RNA Is Expressed across the Eukaryotic Tree of Life , 2014, PloS one.

[51]  Ning Leng,et al.  EBSeq: an empirical Bayes hierarchical model for inference in RNA-seq experiments , 2013, Bioinform..

[52]  Sebastian D. Mackowiak,et al.  Circular RNAs are a large class of animal RNAs with regulatory potency , 2013, Nature.

[53]  Heng Li.  Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM , 2013, 1303.3997.

[54]  Zong-Hong Zhang,et al.  Global transcriptome profiles of Camellia sinensis during cold acclimation , 2013, BMC Genomics.

[55]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[56]  Colin N. Dewey,et al.  RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome , 2011, BMC Bioinformatics.

[57]  Yu Wang,et al.  CsICE1 and CsCBF1: two transcription factors involved in cold responses in Camellia sinensis , 2011, Plant Cell Reports.

[58]  Mark D. Robinson,et al.  edgeR: a Bioconductor package for differential expression analysis of digital gene expression data , 2009, Bioinform..

[59]  Xianwu Zheng,et al.  A R2R3 Type MYB Transcription Factor Is Involved in the Cold Regulation of CBF Genes and in Acquired Freezing Tolerance* , 2006, Journal of Biological Chemistry.

[60]  M. Flores-Vergara,et al.  A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethylammonium bromide , 2006, Nature Protocols.

[61]  Jianhua Zhu,et al.  Gene regulation during cold acclimation in plants , 2006 .

[62]  P. Shannon,et al.  Cytoscape: a software environment for integrated models of biomolecular interaction networks. , 2003, Genome research.

[63]  Yang Ya-jun.  Research Progress on Resistance Breeding of Tea Plant , 2003 .