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Title: Decoding co-/post-transcriptional complexities of plant transcriptomes and epitranscriptome using next-generation sequencing technologies

Journal Article · · Biochemical Society Transactions
DOI:https://doi.org/10.1042/bst20190492· OSTI ID:1851428
ORCiD logo [1];  [2];  [3];  [4];  [2];  [5]
  1. Department of Biology and Program in Cell and Molecular Biology, Colorado State University, Fort Collins, CO 80523, U.S.A.
  2. Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China
  3. School of Human and Life Sciences, Canterbury Christ Church University, Canterbury CT1 1QU, U.K.
  4. Computer Science Department, Colorado State University, Fort Collins, CO 80523, U.S.A
  5. Basic Forestry and Proteomics Research Center, College of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, China

Next-generation sequencing (NGS) technologies - Illumina RNA-seq, Pacific Biosciences isoform sequencing (PacBio Iso-seq), and Oxford Nanopore direct RNA sequencing (DRS) - have revealed the complexity of plant transcriptomes and their regulation at the co-/post-transcriptional level. Global analysis of mature mRNAs, transcripts from nuclear run-on assays, and nascent chromatin-bound mRNAs using short as well as full-length and single-molecule DRS reads have uncovered potential roles of different forms of RNA polymerase II during the transcription process, and the extent of co-transcriptional pre-mRNA splicing and polyadenylation. These tools have also allowed mapping of transcriptome-wide start sites in cap-containing RNAs, poly(A) site choice, poly(A) tail length, and RNA base modifications. The emerging theme from recent studies is that reprogramming of gene expression in response to developmental cues and stresses at the co-/post-transcriptional level likely plays a crucial role in eliciting appropriate responses for optimal growth and plant survival under adverse conditions. Although the mechanisms by which developmental cues and different stresses regulate co-/post-transcriptional splicing are largely unknown, a few recent studies indicate that the external cues target spliceosomal and splicing regulatory proteins to modulate alternative splicing. In this review, we provide an overview of recent discoveries on the dynamics and complexities of plant transcriptomes, mechanistic insights into splicing regulation, and discuss critical gaps in co-/post-transcriptional research that need to be addressed using diverse genomic and biochemical approaches.

Research Organization:
Colorado State Univ., Fort Collins, CO (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
DOE Contract Number:
SC0010733
OSTI ID:
1851428
Journal Information:
Biochemical Society Transactions, Vol. 48, Issue 6; ISSN 0300-5127
Publisher:
Portland Press
Country of Publication:
United States
Language:
English

References (107)

Extensive signal integration by the phytohormone protein network journal July 2020
Plant signaling in biotic and abiotic stress journal March 2020
Coping with Stresses: Roles of Calcium- and Calcium/Calmodulin-Regulated Gene Expression journal June 2011
Does co-transcriptional regulation of alternative splicing mediate plant stress responses? journal February 2019
Thermopriming triggers splicing memory in Arabidopsis journal February 2018
Alternative Splicing and Protein Diversity: Plants Versus Animals journal June 2019
Perspective on Alternative Splicing and Proteome Complexity in Plants journal June 2019
Phytochrome B Induces Intron Retention and Translational Inhibition of PHYTOCHROME-INTERACTING FACTOR3 journal November 2019
Large-Scale Discovery of Non-conventional Peptides in Maize and Arabidopsis through an Integrated Peptidogenomic Pipeline journal July 2020
Nonsense-Mediated RNA Decay Factor UPF1 Is Critical for Posttranscriptional and Translational Gene Regulation in Arabidopsis journal July 2020
PlantAPAdb: A Comprehensive Database for Alternative Polyadenylation Sites in Plants journal November 2019
Wide‐ranging transcriptome remodelling mediated by alternative polyadenylation in response to abiotic stresses in Sorghum journal January 2020
Assessment of transcript reconstruction methods for RNA-seq journal November 2013
Analysis of Transcriptome and Epitranscriptome in Plants Using PacBio Iso-Seq and Nanopore-Based Direct RNA Sequencing journal March 2019
PacBio full-length cDNA sequencing integrated with RNA-seq reads drastically improves the discovery of splicing transcripts in rice journal December 2018
Analysis and comprehensive comparison of PacBio and nanopore-based RNA sequencing of the Arabidopsis transcriptome journal June 2020
New insights into Arabidopsis transcriptome complexity revealed by direct sequencing of native RNAs journal July 2020
Profiling of circular RNA N 6 ‐methyladenosine in moso bamboo ( Phyllostachys edulis ) using nanopore‐based direct RNA sequencing journal August 2020
Accurate detection of m6A RNA modifications in native RNA sequences journal September 2019
How Do You Identify m6 A Methylation in Transcriptomes at High Resolution? A Comparison of Recent Datasets journal May 2020
Nascent RNA sequencing reveals distinct features in plant transcription journal October 2016
RNA polymerase II activity revealed by GRO-seq and pNET-seq in Arabidopsis journal October 2018
Metabolic Labeling of RNAs Uncovers Hidden Features and Dynamics of the Arabidopsis Transcriptome journal February 2020
The Features and Regulation of Co-transcriptional Splicing in Arabidopsis journal February 2020
Global Co-transcriptional Splicing in Arabidopsis and the Correlation with Splicing Regulation in Mature RNAs journal February 2020
MAC3A and MAC3B, Two Core Subunits of the MOS4-Associated Complex, Positively Influence miRNA Biogenesis journal February 2018
Post-transcriptional splicing of nascent RNA contributes to widespread intron retention in plants journal June 2020
Splicing Kinetics and Coordination Revealed by Direct Nascent RNA Sequencing through Nanopores journal March 2020
Poly(A)-tail profiling reveals an embryonic switch in translational control journal January 2014
DNA Methylation Affects Gene Alternative Splicing in Plants: An Example from Rice journal February 2016
Position-specific intron retention is mediated by the histone methyltransferase SDG725 journal April 2018
Exploring the relationship between intron retention and chromatin accessibility in plants journal January 2018
Unraveling the Linkage between Retrograde Signaling and RNA Metabolism in Plants journal February 2020
Phytochrome Coordinates with a hnRNP to Regulate Alternative Splicing via an Exonic Splicing Silencer journal September 2019
Light Regulates Plant Alternative Splicing through the Control of Transcriptional Elongation journal March 2019
Organismal benefits of transcription speed control at gene boundaries journal February 2020
Histone Modifications Form Epigenetic Regulatory Networks to Regulate Abiotic Stress Response journal November 2019
Histone H3 lysine 36 methylation affects temperature-induced alternative splicing and flowering in plants journal June 2017
Native elongation transcript sequencing reveals temperature dependent dynamics of nascent RNAPII transcription in Arabidopsis journal December 2019
The chromatin remodeler ZmCHB101 impacts alternative splicing contexts in response to osmotic stress journal November 2018
Mediator Subunit MED25 Couples Alternative Splicing of JAZ Genes with Fine-Tuning of Jasmonate Signaling journal December 2019
The PROTEIN PHOSPHATASE4 Complex Promotes Transcription and Processing of Primary microRNAs in Arabidopsis journal January 2019
Serine/Arginine-rich protein family of splicing regulators: New approaches to study splice isoform functions journal June 2019
Messenger RNA Modifications in Plants journal April 2019
m6A in mRNA coding regions promotes translation via the RNA helicase-containing YTHDC2 journal November 2019
N 6 ‐methyladenosine and RNA secondary structure affect transcript stability and protein abundance during systemic salt stress in Arabidopsis journal July 2020
m6A enhances the phase separation potential of mRNA journal July 2019
Epigenetic Modifications of mRNA and DNA in Plants journal January 2020
New insights into the plant epitranscriptome journal July 2018
Natural Variation in RNA m 6 A Methylation and Its Relationship with Translational Status journal October 2019
Occurrence and Functions of m 6 A and Other Covalent Modifications in Plant mRNA journal November 2019
OsNSUN2-Mediated 5-Methylcytosine mRNA Modification Enhances Rice Adaptation to High Temperature journal May 2020
5-Methylcytosine RNA Methylation in Arabidopsis Thaliana journal November 2017
N6-Methyladenosine Inhibits Local Ribonucleolytic Cleavage to Stabilize mRNAs in Arabidopsis journal October 2018
The N 1 -Methyladenosine Methylome of Petunia mRNA journal May 2020
Limits in the detection of m6A changes using MeRIP/m6A-seq journal April 2020
Single-base mapping of m 6 A by an antibody-independent method journal July 2019
Deciphering the “m6A Code” via Antibody-Independent Quantitative Profiling journal July 2019
Counting the Cuts: MAZTER-Seq Quantifies m6A Levels Using a Methylation-Sensitive Ribonuclease journal July 2019
DART-seq: an antibody-free method for global m6A detection journal September 2019
Antibody-free enzyme-assisted chemical approach for detection of N6-methyladenosine journal April 2020
Direct RNA sequencing enables m 6 A detection in endogenous transcript isoforms at base-specific resolution journal October 2019
Decoding the epitranscriptional landscape from native RNA sequences journal July 2020
MasterOfPores: A Workflow for the Analysis of Oxford Nanopore Direct RNA Sequencing Datasets journal March 2020
A circRNA from SEPALLATA3 regulates splicing of its cognate mRNA through R-loop formation journal April 2017
The interplay between microRNA and alternative splicing of linear and circular RNAs in eleven plant species journal January 2019
m6A-dependent biogenesis of circular RNAs in male germ cells journal February 2020
Rapid and Dynamic Alternative Splicing Impacts the Arabidopsis Cold Response Transcriptome journal May 2018
Highly ABA-Induced 1 (HAI1)-Interacting protein HIN1 and drought acclimation-enhanced splicing efficiency at intron retention sites journal October 2019
Phytophthora Effectors Modulate Genome-wide Alternative Splicing of Host mRNAs to Reprogram Plant Immunity journal October 2020
Abiotic Stresses Modulate Landscape of Poplar Transcriptome via Alternative Splicing, Differential Intron Retention, and Isoform Ratio Switching journal February 2018
Environmental Stresses Modulate Abundance and Timing of Alternatively Spliced Circadian Transcripts in Arabidopsis journal February 2015
Genome-Wide Identification of Splicing Quantitative Trait Loci (sQTLs) in Diverse Ecotypes of Arabidopsis thaliana journal October 2019
Alternative Splicing and Cross-Talk with Light Signaling journal May 2018
Global transcriptome analysis reveals circadian control of splicing events in Arabidopsis thaliana journal May 2020
The circadian clock shapes the Arabidopsis transcriptome by regulating alternative splicing and alternative polyadenylation journal May 2020
Coordinated Regulation of Pre-mRNA Splicing by the SFPS-RRC1 Complex to Promote Photomorphogenesis journal July 2019
Alternative Splicing Regulation During Light-Induced Germination of Arabidopsis thaliana Seeds journal September 2019
Heterogeneous Nuclear Ribonucleoprotein H1 Coordinates with Phytochrome and the U1 snRNP Complex to Regulate Alternative Splicing in Physcomitrella patens journal August 2019
SPF45-related splicing factor for phytochrome signaling promotes photomorphogenesis by regulating pre-mRNA splicing in Arabidopsis journal July 2017
An oomycete plant pathogen reprograms host pre-mRNA splicing to subvert immunity journal December 2017
Alternative Splicing in the Regulation of Plant–Microbe Interactions journal May 2019
RNA-seq analysis reveals alternative splicing under salt stress in cotton, Gossypium davidsonii journal January 2018
Large-scale analysis of the cassava transcriptome reveals the impact of cold stress on alternative splicing journal November 2019
Alternative Splicing Plays a Critical Role in Maintaining Mineral Nutrient Homeostasis in Rice ( Oryza sativa ) journal September 2018
Identification of an intronic splicing regulatory element involved in auto-regulation of alternative splicing of SCL33 pre-mRNA journal October 2012
Transcriptome-Wide Identification of RNA Targets of Arabidopsis SERINE/ARGININE-RICH45 Uncovers the Unexpected Roles of This RNA Binding Protein in RNA Processing journal November 2015
Depletion of Arabidopsis SC35 and SC35-like serine/arginine-rich proteins affects the transcription and splicing of a subset of genes journal March 2017
The Arabidopsis splicing regulator SR45 confers salt tolerance in a splice isoform-dependent manner journal April 2019
Transcriptome analyses reveal SR45 to be a neutral splicing regulator and a suppressor of innate immunity in Arabidopsis thaliana journal October 2017
Genome-Wide Analysis of Alternative Splicing Landscapes Modulated during Plant-Virus Interactions in Brachypodium distachyon journal January 2015
Insect herbivory elicits genome-wide alternative splicing responses in Nicotiana attenuata journal October 2015
Comprehensive Transcriptome Analyses Reveal that Potato Spindle Tuber Viroid Triggers Genome-Wide Changes in Alternative Splicing, Inducible trans -Acting Activity of Phased Secondary Small Interfering RNAs, and Immune Responses journal June 2017
Functional Analysis of PsAvr3c Effector Family From Phytophthora Provides Probes to Dissect SKRP Mediated Plant Susceptibility journal July 2018
RALF1-FERONIA complex affects splicing dynamics to modulate stress responses and growth in plants journal May 2020
RNA-Binding Proteins Revisited – The Emerging Arabidopsis mRNA Interactome journal June 2017
Development of an in vitro pre-mRNA splicing assay using plant nuclear extract journal January 2018
A Collection of Pre-mRNA Splicing Mutants in Arabidopsis thaliana journal June 2020
Identifying proteins that bind to specific RNAs - focus on simple repeat expansion diseases journal September 2016
Transcriptome Engineering with RNA-Targeting Type VI-D CRISPR Effectors journal April 2018
Integrative genome-wide analysis reveals HLP1, a novel RNA-binding protein, regulates plant flowering by targeting alternative polyadenylation journal June 2015
Adaptation of iCLIP to plants determines the binding landscape of the clock-regulated RNA-binding protein AtGRP7 journal October 2017
A large-scale binding and functional map of human RNA-binding proteins journal July 2020
Identification of RNA-binding protein targets with HyperTRIBE journal July 2018
Cumulus provides cloud-based data analysis for large-scale single-cell and single-nucleus RNA-seq journal July 2020
RIC-seq for global in situ profiling of RNA–RNA spatial interactions journal May 2020
Integrated multi-omics framework of the plant response to jasmonic acid journal March 2020