Extensive translational regulation during seed germination revealed by polysomal profiling

Summary This work investigates the extent of translational regulation during seed germination. The polysome occupancy of each gene is determined by genome‐wide profiling of total mRNA and polysome‐associated mRNA. This reveals extensive translational regulation during Arabidopsis thaliana seed germination. The polysome occupancy of thousands of individual mRNAs changes to a large extent during the germination process. Intriguingly, these changes are restricted to two temporal phases (shifts) during germination, seed hydration and germination. Sequence features, such as upstream open reading frame number, transcript length, mRNA stability, secondary structures, and the presence and location of specific motifs correlated with this translational regulation. These features differed significantly between the two shifts, indicating that independent mechanisms regulate translation during seed germination. This study reveals substantial translational dynamics during seed germination and identifies development‐dependent sequence features and cis elements that correlate with the translation control, uncovering a novel and important layer of gene regulation during seed germination.

• Publication year

  2016

• Venue

  New Phytologist

• Publication date

  2016-12-09

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1111/nph.14355PMID 27935038PMCID 5347915
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• A Predictive Coexpression Network Identifies Novel Genes Controlling the Seed-to-Seedling Phase Transition in Arabidopsis thaliana1[OPEN]

  2016influential reference
• Germination Potential of Dormant and Nondormant Arabidopsis Seeds Is Driven by Distinct Recruitment of Messenger RNAs to Polysomes

  2015influential reference
• Translatome analyses capture of opposing tissue-specific brassinosteroid signals orchestrating root meristem differentiation

  2015cited by this paper
• Assessing the translational landscape of myogenic differentiation by ribosome profiling

  2015cited by this paper
• Increased sucrose levels mediate selective mRNA translation in Arabidopsis

  2014cited by this paper
• Profiling of Translatomes of in Vivo–Grown Pollen Tubes Reveals Genes with Roles in Micropylar Guidance during Pollination in Arabidopsis[W][OPEN]

  2014influential reference
• REDUCED DORMANCY5 Encodes a Protein Phosphatase 2C That Is Required for Seed Dormancy in Arabidopsis[C][W][OPEN]

  2014cited by this paper
• Translatome profiling in dormant and nondormant sunflower (Helianthus annuus) seeds highlights post-transcriptional regulation of germination.

  2014cited by this paper
• Selective mRNA sequestration by OLIGOURIDYLATE-BINDING PROTEIN 1 contributes to translational control during hypoxia in Arabidopsis

  2014cited by this paper
• Transcriptome analysis during seed germination of elite Chinese bread wheat cultivar Jimai 20

  2014cited by this paper
• Polysome profiling reveals broad translatome remodeling during endoplasmic reticulum (ER) stress in the pathogenic fungus Aspergillus fumigatus

  2014influential reference
• Dynamic Proteomics Emphasizes the Importance of Selective mRNA Translation and Protein Turnover during Arabidopsis Seed Germination*

  2013cited by this paper
• Sounds of silence: synonymous nucleotides as a key to biological regulation and complexity

  2013cited by this paper
• Transcriptional Dynamics of Two Seed Compartments with Opposing Roles in Arabidopsis Seed Germination1[W][OPEN]

  2013cited by this paper
• An improved implementation of effective number of codons (nc).

  2013cited by this paper
• Translational Landscape of Photomorphogenic Arabidopsis[W]

  2013cited by this paper
• Title: Transcriptional Dynamics of Two Seed Compartments with Opposing Roles in Arabidopsis Seed Germination

  2013cited by this paper
• Translational dynamics revealed by genome-wide profiling of ribosome footprints in Arabidopsis

  2013influential reference
• Regulatory Impact of RNA Secondary Structure across the

  2012cited by this paper
• PRMD: an integrated database for plant RNA modifications

  2012influential reference
• Identification of an intronic splicing regulatory element involved in auto-regulation of alternative splicing of SCL33 pre-mRNA.

  2012cited by this paper
• On the Discordance of Metabolomics with Proteomics and Transcriptomics: Coping with Increasing Complexity in Logic, Chemistry, and Network Interactions Scientific Correspondence

  2012cited by this paper
• Transcriptome analysis.

  2012cited by this paper
• The Ribosome Uses Two Active Mechanisms to Unwind mRNA During Translation

  2011cited by this paper
• In-Depth Temporal Transcriptome Profiling Reveals a Crucial Developmental Switch with Roles for RNA Processing and Organelle Metabolism That Are Essential for Germination in Arabidopsis1[W][OA]

  2011cited by this paper
• Translation Initiation: A Regulatory Role for Poly(A) Tracts in Front of the AUG Codon in Saccharomyces cerevisiae

  2011cited by this paper
• Length-dependent translation of messenger RNA by ribosomes.

  2011cited by this paper
• Expression profile of maize (Zea mays L.) embryonic axes during germination: translational regulation of ribosomal protein mRNAs.

  2011cited by this paper
• Genome-wide measurement of RNA secondary structure in yeast

  2010cited by this paper
• GERMINATOR: a software package for high-throughput scoring and curve fitting of Arabidopsis seed germination.

  2010cited by this paper
• Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis

  2009cited by this paper
• Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis

  2009cited by this paper
• MEME Suite: tools for motif discovery and searching

  2009influential reference
• General Rules for Optimal Codon Choice

  2009cited by this paper
• Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data

  2009cited by this paper
• Stress-Dependent Coordination of Transcriptome and Translatome in Yeast

  2009cited by this paper
• Genome-Wide Analysis in Vivo of Translation with Nucleotide Resolution Using Ribosome Profiling

  2009influential reference
• Isolation of plant polysomal mRNA by differential centrifugation and ribosome immunopurification methods.

  2009cited by this paper
• Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana.

  2008cited by this paper
• Selection on codon bias.

  2008cited by this paper
• Faculty Opinions recommendation of Genome-wide analysis of mRNA decay rates and their determinants in Arabidopsis thaliana.

  2008cited by this paper
• Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution.

  2008cited by this paper
• Genome-Scale Proteomics Reveals Arabidopsis thaliana Gene Models and Proteome Dynamics

  2008cited by this paper
• A Heteromeric Plastidic Pyruvate Kinase Complex Involved in Seed Oil Biosynthesis in Arabidopsis[W]

  2007cited by this paper
• Genome-Wide Analysis of mRNA Decay Rates and Their Determinants in Arabidopsis thaliana[W]

  2007cited by this paper
• Faculty Opinions recommendation of Large-scale analysis of mRNA translation states during sucrose starvation in arabidopsis cells identifies cell proliferation and chromatin structure as targets of translational control.

  2006cited by this paper
• Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes

  2006cited by this paper
• Seed dormancy and the control of germination.

  2006cited by this paper
• Large-Scale Analysis of mRNA Translation States during Sucrose Starvation in Arabidopsis Cells Identifies Cell Proliferation and Chromatin Structure as Targets of Translational Control1[W]

  2006cited by this paper
• Arabidopsis Seed Development and Germination Is Associated with Temporally Distinct Metabolic Switches1[W]

  2006cited by this paper
• Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation.

  2005cited by this paper
• Proteomic analysis and extensive protein identification from dry, germinating Arabidopsis seeds and young seedlings.

  2005cited by this paper
• Regulation of translation via mRNA structure in prokaryotes and eukaryotes.

  2005cited by this paper
• Structure of PTB Bound to RNA: Specific Binding and Implications for Splicing Regulation

  2005cited by this paper
• The Effect of α-Amanitin on the Arabidopsis Seed Proteome Highlights the Distinct Roles of Stored and Neosynthesized mRNAs during Germination1

  2004cited by this paper
• Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments

  2004influential reference
• affy - analysis of Affymetrix GeneChip data at the probe level

  2004influential reference
• Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae

  2003influential reference
• TM4: a free, open-source system for microarray data management and analysis.

  2003cited by this paper
• Exploration, normalization, and summaries of high density oligonucleotide array probe level data.

  2003cited by this paper
• Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes

  2002cited by this paper
• Seed Germination and Dormancy

  2002cited by this paper
• Proteomic analysis of arabidopsis seed germination and priming.

  2001cited by this paper
• tRNA gene number and codon usage in the C. elegans genome are co-adapted for optimal translation of highly expressed genes.

  2000cited by this paper
• Selective translation of cytoplasmic mRNAs in plants.

  1999cited by this paper
• Seed Germination and Dormancy.

  1997cited by this paper
• Mutation of PTB binding sites causes misregulation of alternative 3' splice site selection in vivo.

  1997cited by this paper
• A complex of nuclear proteins mediates SR protein binding to a purine-rich splicing enhancer.

  1996cited by this paper
• Controlling the false discovery rate: a practical and powerful approach to multiple testing

  1995influential reference
• Distinct binding specificities and functions of higher eukaryotic polypyrimidine tract-binding proteins.

  1995cited by this paper
• Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy.

  1994cited by this paper
• Coevolution of codon usage and transfer RNA abundance

  1987cited by this paper
• Codon usage and tRNA content in unicellular and multicellular organisms.

  1985cited by this paper
• Polyribosome formation during early germination of bean embryonic axes.

  1978cited by this paper
• Codon--anticodon pairing: the wobble hypothesis.

  1966cited by this paper
• Molecular Systems Biology 6; Article number 419; doi:10.1038/msb.2010.76 Citation: Molecular Systems Biology 6:419

  year unknowninfluential reference
• Molecular Systems Biology Peer Review Process File Widespread Translational Control Contributes to the Regulation of Arabidopsis Photomorphogenesis Transaction Report

  year unknowncited by this paper

• Translational landscape during seed germination revealed by ribosome profiling

  2026cites this paper
• Unravelling the dynamics of seed‐stored mRNAs during seed priming

  2025cites this paper
• Control of seed-to-seedling transition by an upstream open reading frame in ABSCISIC ACID DEFICIENT2

  2025cites this paper
• Dynamic and spatial control of cellular activity during seed germination.

  2025cites this paper
• Translational landscape during Seed Germination at Sub-Codon resolution

  2025influential citation
• Holistic overview of regulatory networks governing seed dormancy and germination in plants.

  2025cites this paper
• Defying Death: A Multi-Omics Approach to Understanding Desiccation Tolerance and Senescence in Eragrostis nindensis

  2025cites this paper
• Translational regulation plasticity shapes wheat grain adaptation to heat stress

  2025cites this paper
• Translational and epitranscriptomic regulation of seed germination in Arabidopsis thaliana genotypes with contrasting dormancy phenotypes

  2025influential citation
• Boron Toxicity Modulates Hypocotyl Growth Through Brassinosteroid and Thermomorphogenic‐Like Mechanisms

  2025cites this paper
• Regulation of seed germination: ROS, epigenetic, and hormonal aspects

  2024cites this paper
• Morpho-Physiochemical Indices and Transcriptome Analysis Reveal the Role of Glucosinolate and Erucic Acid in Response to Drought Stress during Seed Germination of Rapeseed

  2024cites this paper
• Transcriptome analysis of green and purple fruited pepper provides insight into novel regulatory genes in anthocyanin biosynthesis

  2024cites this paper
• A commitment for life: Decades of unraveling the molecular mechanisms behind seed dormancy and germination

  2024cites this paper
• Enjoy the silence: Canonical and non-canonical RNA silencing activity during plant sexual reproduction.

  2024cites this paper
• Rapid and Robust Polysome Isolation and Fraction RNA Extraction for Studying the Seed Translatome

  2024cites this paper
• Aging and Germination of Long-term Stored Seeds: Can MicroRNAs Unlock the Secrets?

  2024cites this paper
• MALDI imaging unveils spatial lipidomics dynamics during jojoba seed germination and post-germination

  2024cites this paper
• Structure of plant photosystem I in a native assembly state defines PsaF as a regulatory checkpoint

  2024cites this paper
• Proteomic characterization of the different stages of seed germination in Cupressus gigantea

  2024cites this paper
• Dry side of the core: a meta-analysis addressing the original nature of the ABA signalosome at the onset of seed imbibition

  2023cites this paper
• Identification and Analysis of the Expression of microRNAs during the Low-Temperature Dormancy Release of Tulipa thianschanica Seeds

  2023cites this paper
• Implications of CO2 emissions on the main land and forest uses in the Brazilian Amazon.

  2023cites this paper
• Integration of miRNA and mRNA analysis reveals the role of ribosome in to anti-artificial aging in sweetcorn.

  2023cites this paper
• A Travel through Landscapes of Seed Dormancy

  2023cites this paper
• Phytocannabinoids biosynthesis during early stages of development of young Cannabis sativa L. seedlings: Integrating biochemical and transcription data.

  2023cites this paper
• A Single-Nucleus Atlas of Seed-to-Seed Development in Arabidopsis

  2023cites this paper
• Proteomic Analysis of Pecan (Carya illinoinensis) Nut Development

  2023cites this paper
• What, where, and how: Regulation of translation and the translational landscape in plants.

  2023cites this paper
• The translational landscape of bread wheat during grain development.

  2023cites this paper
• A Miniature Sucrose Gradient for Polysome Profiling

  2023cites this paper
• Seed germination variability: Why do genetically identical seeds not germinate at the same moment?

  2023cites this paper
• Single seeds exhibit transcriptional heterogeneity during secondary dormancy induction

  2022cites this paper
• RNA-binding proteins and their role in translational regulation in plants.

  2022cites this paper
• Physiological and molecular changes in seeds of Hancornia speciosa Gomes stored in conservative solutions

  2022cites this paper
• Identification of the Potential Genes Regulating Seed Germination Speed in Maize

  2022cites this paper
• Exploring Breakthroughs in Three Traits Belonging to Seed Life

  2022cites this paper
• Variable selection in sparse multivariate GLARMA models: application to germination control by environment

  2022cites this paper
• SeedTransNet: a directional translational network revealing regulatory patterns during seed maturation and germination

  2022cites this paper
• Too little, too late: transcription during imbibition of lethally aged soybean seeds is weak and delayed, but not aberrant

  2021cites this paper
• Physiological-biochemical and genetic featuresof barley as a product for functionalnutrition

  2021cites this paper
• The mRNA‐binding proteome of a critical phase transition during Arabidopsis seed germination

  2021cites this paper
• Delayed Protein Changes During Seed Germination

  2021cites this paper
• Post-transcriptional regulation of seed dormancy and germination: Current understanding and future directions

  2021cites this paper
• Genome-Wide Association Mapping Unravels the Genetic Control of Seed Vigor under Low-Temperature Conditions in Rapeseed (Brassica napus L.)

  2021cites this paper
• Translational remodeling by RNA‐binding proteins and noncoding RNAs

  2021cites this paper
• Identification and characterization of CTP:phosphocholine cytidylyltransferase CpCCT1 in the resurrection plant Craterostigma plantagineum.

  2021cites this paper
• Characterization of the Heat-Stable Proteome during Seed Germination in Arabidopsis with Special Focus on LEA Proteins

  2021cites this paper
• Contribution of Stored mRNAs to Seed Germination

  2020cites this paper
• Seeds as Economical Production Platform for Recombinant Proteins.

  2020cites this paper
• Temporal tissue-specific regulation of transcriptomes during barley (Hordeum vulgare) seed germination.

  2020cites this paper
• Protein synthesis increases with photosynthesis via the stimulation of translation initiation.

  2020cites this paper
• Molecular and environmental factors regulating seed longevity.

  2020cites this paper
• Identifying the Translatome of Mouse NEBD-Stage Oocytes via SSP-Profiling; A Novel Polysome Fractionation Method

  2020cites this paper
• Lost in Translation: Physiological Roles of Stored mRNAs in Seed Germination

  2020cites this paper
• miRNA–mRNA Integrated Analysis Reveals Roles for miRNAs in a Typical Halophyte, Reaumuria soongorica, during Seed Germination under Salt Stress

  2020cites this paper
• Environmental and biophysical controls of evapotranspiration from Seasonally Dry Tropical Forests (Caatinga) in the Brazilian Semiarid

  2020cites this paper
• Translational gene regulation in plants: A green new deal

  2020cites this paper
• Regulatory Contexts in the 5'-Region of mRNA from Arabidopsis thaliana Plants and Their Role in Translation Efficiency

  2020cites this paper
• An Updated Overview on the Regulation of Seed Germination

  2020cites this paper
• Separation and Paired Proteome Profiling of Plant Chloroplast and Cytoplasmic Ribosomes

  2020cites this paper
• Low RIN Value for RNA-Seq Library Construction from Long-Term Stored Seeds: A Case Study of Barley Seeds

  2020cites this paper
• Desiccation Tolerance as the Basis of Long-Term Seed Viability

  2020cites this paper
• From the Outside to the Inside: New Insights on the Main Factors that Guide the Germination Process

  2020influential citation
• From the Outside to the Inside: New Insights on the Main Factors That Guide Seed Dormancy and Germination

  2020cites this paper
• Monitoring of XRN4 Targets Reveals the Importance of Cotranslational Decay during Arabidopsis Development1[OPEN]

  2020cites this paper
• Méthodes régularisées pour l’analyse de données multivariées en grande dimension : théorie et applications.

  2019cites this paper
• Transcriptome and translatome profiling and translational network analysis during seed maturation reveals conserved transcriptional and distinct translational regulatory patterns

  2019influential citation
• Seed-Stored mRNAs that Are Specifically Associated to Monosomes Are Translationally Regulated during Germination1[OPEN]

  2019influential citation
• Shotgun proteomic analysis highlights roles of long-lived mRNAs and de novo transcribed mRNAs upon imbibition in rice embryos.

  2019cites this paper
• Fine-Tuning the Expression of Duplicate Genes by Translational Regulation in Arabidopsis and Maize

  2019cites this paper
• Seeds: A Unique System to Study Translational Regulation.

  2019cites this paper
• Usability of reference-free transcriptome assemblies for detection of differential expression: a case study on Aethionema arabicum dimorphic seeds

  2019cites this paper
• Characterization of LRL5 as a key regulator of root hair growth in maize

  2019cites this paper
• Translatomics: The Global View of Translation

  2019cites this paper
• Fine Tuning of Translation: A Complex Web of Mechanisms and Its Relevance to Plant Functional Genomics and Biotechnology

  2019cites this paper
• Dormancy cycling: translation‐related transcripts are the main difference between dormant and non‐dormant seeds in the field

  2019cites this paper
• Metabolic and gene expression hallmarks of seed germination uncovered by sodium butyrate in Medicago truncatula.

  2018cites this paper
• Combined transcriptome and translatome analyses reveal a role for tryptophan-dependent auxin biosynthesis in the control of DOG1-dependent seed dormancy.

  2018cites this paper
• A Plant Biologist’s Toolbox to Study Translation

  2018cites this paper
• Estimation of large block structured covariance matrices: Application to ‘multi‐omic’ approaches to study seed quality

  2018cites this paper
• Exploring the fate of mRNA in aging seeds: protection, destruction, or slow decay?

  2018cites this paper
• An examination of Job's rule: protection and repair of the proteins of the translational apparatus in seeds

  2018cites this paper
• The kinetics of ageing in dry-stored seeds: a comparison of viability loss and RNA degradation in unique legacy seed collections.

  2018cites this paper
• Ribosome profiling reveals changes in translational status of soybean transcripts during immature cotyledon development

  2018cites this paper
• Decline in RNA integrity of dry-stored soybean seeds correlates with loss of germination potential

  2017cites this paper
• Translation regulation in plants: an interesting past, an exciting present and a promising future.

  2017cites this paper
• Regulation of Translation by TOR, eIF4E and eIF2α in Plants: Current Knowledge, Challenges and Future Perspectives

  2017cites this paper
• Emerging Roles and Landscape of Translating mRNAs in Plants

  2017influential citation
• Isolation of tissues and preservation of RNA from intact, germinated barley grain

  2017cites this paper
• Bioinformatics Group - Thesis projects

  year unknowncites this paper
• Elucidating the genetic factors underlying heavy metal accumulation and tolerance

  year unknowncites this paper