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Title: A Vitis vinifera basic helix-loop-helix transcription factor enhances plant cell size, vegetative biomass and reproductive yield

Journal Article · · Plant Biotechnology Journal
DOI: https://doi.org/10.1111/pbi.12898 · OSTI ID:1435181

Strategies for improving plant size are critical targets for plant biotechnology to increase vegetative biomass or reproductive yield. To improve biomass production, a codon-optimized helix–loop–helix transcription factor (VvCEB1opt) from wine grape was overexpressed in Arabidopsis thaliana resulting in significantly increased leaf number, leaf and rosette area, fresh weight and dry weight. Cell size, but typically not cell number, was increased in all tissues resulting in increased vegetative biomass and reproductive organ size, number and seed yield. Ionomic analysis of leaves revealed the VvCEB1opt-overexpressing plants had significantly elevated, K, S and Mo contents relative to control lines. Increased K content likely drives increased osmotic potential within cells leading to greater cellular growth and expansion. To understand the mechanistic basis of VvCEB1opt action, one transgenic line was genotyped using RNA-Seq mRNA expression profiling and revealed a novel transcriptional reprogramming network with significant changes in mRNA abundance for genes with functions in delayed flowering, pathogen–defence responses, iron homeostasis, vesicle-mediated cell wall formation and auxin-mediated signalling and responses. Direct testing of VvCEB1opt-overexpressing plants showed that they had significantly elevated auxin content and a significantly increased number of lateral leaf primordia within meristems relative to controls, confirming that cell expansion and organ number proliferation were likely an auxin-mediated process. VvCEB1opt overexpression in Nicotiana sylvestris also showed larger cells, organ size and biomass demonstrating the potential applicability of this innovative strategy for improving plant biomass and reproductive yield in crops.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE
Grant/Contract Number:
AC05-00OR22725; SC0008834
OSTI ID:
1435181
Journal Information:
Plant Biotechnology Journal, Journal Name: Plant Biotechnology Journal Journal Issue: 9 Vol. 16; ISSN 1467-7644
Publisher:
Society for Experimental Biology; Association of Applied BiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (181)

GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. journal December 1987
Microwave-stimulated glutaraldehyde and osmium tetroxide fixation of plant tissue: ultrastructural preservation in seconds journal May 1992
Expression analysis of the AtMLO Gene Family Encoding Plant-Specific Seven-Transmembrane Domain Proteins journal March 2006
Molecular dissection of a rice microtubule-associated RING finger protein and its potential role in salt tolerance in Arabidopsis journal September 2015
Rapid Synthesis of Auxin via a New Tryptophan-Dependent Pathway Is Required for Shade Avoidance in Plants journal April 2008
Iron- and Ferritin-Dependent Reactive Oxygen Species Distribution: Impact on Arabidopsis Root System Architecture journal March 2015
SAUR Proteins as Effectors of Hormonal and Environmental Signals in Plant Growth journal August 2015
Making bigger plants: key regulators of final organ size journal February 2009
Diversity and specificity: auxin perception and signaling through the TIR1/AFB pathway journal October 2014
FIT, the FER-LIKE IRON DEFICIENCY INDUCED TRANSCRIPTION FACTOR in Arabidopsis journal May 2007
Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids journal November 2008
A combinatorial TIR1/AFB–Aux/IAA co-receptor system for differential sensing of auxin journal April 2012
Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs journal August 2016
ER-localized auxin transporter PIN8 regulates auxin homeostasis and male gametophyte development in Arabidopsis journal January 2012
Fast gapped-read alignment with Bowtie 2 journal March 2012
BIGPETALp, a bHLH transcription factor is involved in the control of Arabidopsis petal size journal August 2006
Model for the regulation of Arabidopsis thaliana leaf margin development journal February 2011
Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana journal August 2000
The Biochemical Mechanism of Auxin Biosynthesis by an Arabidopsis YUCCA Flavin-containing Monooxygenase journal November 2012
Arabidopsis Ferritin 1 ( AtFer1 ) Gene Regulation by the Phosphate Starvation Response 1 (AtPHR1) Transcription Factor Reveals a Direct Molecular Link between Iron and Phosphate Homeostasis journal June 2013
SNARE VTI13 plays a unique role in endosomal trafficking pathways associated with the vacuole and is essential for cell wall organization and root hair growth in arabidopsis journal April 2014
Principal component analysis based methods in bioinformatics studies journal January 2011
The Sequence Alignment/Map format and SAMtools journal June 2009
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data journal November 2009
The grape berry-specific basic helix–loop–helix transcription factor VvCEB1 affects cell size journal January 2013
Comprehensive Transcriptome Analysis of Auxin Responses in Arabidopsis journal March 2008
P-Loop-Dependent NLR SNC1 Can Oligomerize and Activate Immunity in the Nucleus journal December 2014
AGRIS: the Arabidopsis Gene Regulatory Information Server, an update journal November 2010
Araport: the Arabidopsis Information Portal journal November 2014
The BioGRID interaction database: 2015 update journal November 2014
ROTS: reproducible RNA-seq biomarker detector—prognostic markers for clear cell renal cell cancer journal August 2015
Molecular Cloning and Characterization of Aldehyde Oxidases in Arabidopsis thaliana journal April 1998
Tissue-Specific Expression of SMALL AUXIN UP RNA41 Differentially Regulates Cell Expansion and Root Meristem Patterning in Arabidopsis journal March 2013
Pseudomonas syringae Effector AvrPphB Suppresses AvrB-Induced Activation of RPM1 but Not AvrRpm1-Induced Activation journal June 2015
Auxin at the Shoot Apical Meristem journal March 2010
Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis journal July 2006
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks journal November 2003
Genome-Wide Identification and Testing of Superior Reference Genes for Transcript Normalization in Arabidopsis journal September 2005
Specialized Zones of Development in Roots journal November 1995
SAUR36, a SMALL AUXIN UP RNA Gene, Is Involved in the Promotion of Leaf Senescence in Arabidopsis journal December 2012
The Leucine-Rich Repeat Receptor-Like Kinase BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1 and the Cytochrome P450 PHYTOALEXIN DEFICIENT3 Contribute to Innate Immunity to Aphids in Arabidopsis journal February 2014
The Arabidopsis Auxin-Inducible Gene ARGOS Controls Lateral Organ Size journal August 2003
Characterization of an Arabidopsis Enzyme Family That Conjugates Amino Acids to Indole-3-Acetic Acid journal January 2005
The Gene Controlling the Quantitative Trait Locus EPITHIOSPECIFIER MODIFIER1 Alters Glucosinolate Hydrolysis and Insect Resistance in Arabidopsis journal May 2006
Global Analysis of DELLA Direct Targets in Early Gibberellin Signaling in Arabidopsis journal October 2007
AUXIN RESPONSE FACTOR8 Regulates Arabidopsis Petal Growth by Interacting with the bHLH Transcription Factor BIGPETALp journal March 2011
Ion Exchangers NHX1 and NHX2 Mediate Active Potassium Uptake into Vacuoles to Regulate Cell Turgor and Stomatal Function in Arabidopsis journal March 2012
Soluble Carbohydrates Regulate Auxin Biosynthesis via PIF Proteins in Arabidopsis journal December 2012
Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. journal November 1997
The Arabidopsis ARGOS-LIKE gene regulates cell expansion during organ growth journal July 2006
Arabidopsis ORGAN SIZE RELATED1 regulates organ growth and final organ size in orchestration with ARGOS and ARL journal April 2011
Auxin influx importers modulate serration along the leaf margin journal July 2015
A Bacterial Effector Acts as a Plant Transcription Factor and Induces a Cell Size Regulator journal October 2007
Photoexcited CRY2 Interacts with CIB1 to Regulate Transcription and Floral Initiation in Arabidopsis journal December 2008
Developmentally Regulated Systemic Endopolyploid in Succulents with Small Genomes journal October 1990
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome journal August 2011
jvenn: an interactive Venn diagram viewer journal January 2014
Protocol: High-throughput and quantitative assays of auxin and auxin precursors from minute tissue samples journal January 2012
Auxin metabolism and homeostasis during plant development journal February 2013
LEAFY expression and flower initiation in Arabidopsis journal October 1997
Improved Gateway Binary Vectors: High-Performance Vectors for Creation of Fusion Constructs in Transgenic Analysis of Plants journal August 2007
Multiple bHLH Proteins form Heterodimers to Mediate CRY2-Dependent Regulation of Flowering-Time in Arabidopsis journal October 2013
Auxin Import and Local Auxin Biosynthesis Are Required for Mitotic Divisions, Cell Expansion and Cell Specification during Female Gametophyte Development in Arabidopsis thaliana journal May 2015
Genetically modified crops for biomass increase. Genes and strategies journal May 2010
The Root Apex of Arabidopsis thaliana Consists of Four Distinct Zones of Growth Activities : Meristematic Zone, Transition Zone, Fast Elongation Zone and Growth Terminating Zone journal November 2006
Intracellular auxin transport in pollen: PIN8, PIN5 and PILS5 journal November 2012
Cytosolic calcium and pH signaling in plants under salinity stress journal March 2010
Early evolution of bHLH proteins in plants journal July 2010
Combining growth-promoting genes leads to positive epistasis in Arabidopsis thaliana journal April 2014
Ectopic expression ofAINTEGUMENTA inArabidopsis plants results in increased growth of floral organs journal January 1999
GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. journal December 1987
Vacuum-Microwave Combination for Processing Plant Tissues for Electron Microscopy book January 2001
Microwave-stimulated glutaraldehyde and osmium tetroxide fixation of plant tissue: ultrastructural preservation in seconds journal May 1992
Auxin-induced growth and its linkage to potassium channels journal January 1997
Estimation of nuclear DNA content of plants by flow cytometry journal August 1991
Estimation of nuclear DNA content of plants by flow cytometry journal November 1991
Ward’s Hierarchical Agglomerative Clustering Method: Which Algorithms Implement Ward’s Criterion? journal October 2014
Expression analysis of the AtMLO Gene Family Encoding Plant-Specific Seven-Transmembrane Domain Proteins journal March 2006
Molecular dissection of a rice microtubule-associated RING finger protein and its potential role in salt tolerance in Arabidopsis journal September 2015
Production of transgenic Nicotiana sylvestris plants expressing melatonin synthetase genes and their effect on UV-B-induced DNA damage journal October 2011
Miniaturization of three carbohydrate analyses using a microsample plate reader journal May 1991
Expression of a rice OsARGOS gene in Arabidopsis promotes cell division and expansion and increases organ size journal January 2009
Rapid Synthesis of Auxin via a New Tryptophan-Dependent Pathway Is Required for Shade Avoidance in Plants journal April 2008
Iron- and Ferritin-Dependent Reactive Oxygen Species Distribution: Impact on Arabidopsis Root System Architecture journal March 2015
SAUR Proteins as Effectors of Hormonal and Environmental Signals in Plant Growth journal August 2015
Making bigger plants: key regulators of final organ size journal February 2009
Diversity and specificity: auxin perception and signaling through the TIR1/AFB pathway journal October 2014
Leaf epinasty and auxin: A biochemical and molecular overview journal December 2016
FIT, the FER-LIKE IRON DEFICIENCY INDUCED TRANSCRIPTION FACTOR in Arabidopsis journal May 2007
Molybdenum as an essential element for improving total yield in seawater-grown Salicornia europaea L. journal September 2010
Colorimetric Method for Determination of Sugars and Related Substances journal March 1956
Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids journal November 2008
A combinatorial TIR1/AFB–Aux/IAA co-receptor system for differential sensing of auxin journal April 2012
Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs journal August 2016
ER-localized auxin transporter PIN8 regulates auxin homeostasis and male gametophyte development in Arabidopsis journal January 2012
Fast gapped-read alignment with Bowtie 2 journal March 2012
Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method journal June 2006
De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis journal July 2013
Antibiotic-resistant bacteria show widespread collateral sensitivity to antimicrobial peptides journal May 2018
Probiotic properties of a phytase producing Pediococcus acidilactici strain SMVDUDB2 isolated from traditional fermented cheese product, Kalarei journal February 2020
BIGPETALp, a bHLH transcription factor is involved in the control of Arabidopsis petal size journal August 2006
Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering: FLM is a MADS-box flowering repressor journal April 2001
Model for the regulation of Arabidopsis thaliana leaf margin development journal February 2011
SAMBA, a plant-specific anaphase-promoting complex/cyclosome regulator is involved in early development and A-type cyclin stabilization journal August 2012
Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana journal August 2000
Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis journal January 2000
The Biochemical Mechanism of Auxin Biosynthesis by an Arabidopsis YUCCA Flavin-containing Monooxygenase journal November 2012
Arabidopsis Ferritin 1 ( AtFer1 ) Gene Regulation by the Phosphate Starvation Response 1 (AtPHR1) Transcription Factor Reveals a Direct Molecular Link between Iron and Phosphate Homeostasis journal June 2013
Quality assurance for plant tissue analysis by ICP‐AES journal October 1984
SNARE VTI13 plays a unique role in endosomal trafficking pathways associated with the vacuole and is essential for cell wall organization and root hair growth in arabidopsis journal April 2014
Principal component analysis based methods in bioinformatics studies journal January 2011
The Sequence Alignment/Map format and SAMtools journal June 2009
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data journal November 2009
Three Redundant Brassinosteroid Early Response Genes Encode Putative bHLH Transcription Factors Required for Normal Growth journal November 2002
The grape berry-specific basic helix–loop–helix transcription factor VvCEB1 affects cell size journal January 2013
Leaf anatomical traits which accommodate the facultative engagement of crassulacean acid metabolism in tropical trees of the genus Clusia journal February 2014
Origin and Diversification of Basic-Helix-Loop-Helix Proteins in Plants journal November 2009
Comprehensive Transcriptome Analysis of Auxin Responses in Arabidopsis journal March 2008
P-Loop-Dependent NLR SNC1 Can Oligomerize and Activate Immunity in the Nucleus journal December 2014
AGRIS: the Arabidopsis Gene Regulatory Information Server, an update journal November 2010
Araport: the Arabidopsis Information Portal journal November 2014
The BioGRID interaction database: 2015 update journal November 2014
ROTS: reproducible RNA-seq biomarker detector—prognostic markers for clear cell renal cell cancer journal August 2015
Molecular Cloning and Characterization of Aldehyde Oxidases in Arabidopsis thaliana journal April 1998
Tissue-Specific Expression of SMALL AUXIN UP RNA41 Differentially Regulates Cell Expansion and Root Meristem Patterning in Arabidopsis journal March 2013
Identification and Characterization of Transcription Factors Regulating Arabidopsis HAK5 journal July 2013
Pseudomonas syringae Effector AvrPphB Suppresses AvrB-Induced Activation of RPM1 but Not AvrRpm1-Induced Activation journal June 2015
Auxin at the Shoot Apical Meristem journal March 2010
Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis journal July 2006
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks journal November 2003
Scanning Electron Microscopy (SEM) of Plant Tissues journal April 2008
Contrasting Modes of Diversification in the Aux/IAA and ARF Gene Families journal July 2004
Genome-Wide Identification and Testing of Superior Reference Genes for Transcript Normalization in Arabidopsis journal September 2005
BT2, a BTB Protein, Mediates Multiple Responses to Nutrients, Stresses, and Hormones in Arabidopsis journal June 2009
Specialized Zones of Development in Roots journal November 1995
SAUR36, a SMALL AUXIN UP RNA Gene, Is Involved in the Promotion of Leaf Senescence in Arabidopsis journal December 2012
The Leucine-Rich Repeat Receptor-Like Kinase BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1 and the Cytochrome P450 PHYTOALEXIN DEFICIENT3 Contribute to Innate Immunity to Aphids in Arabidopsis journal February 2014
Higher Activity of an Aldehyde Oxidase in the Auxin-Overproducing superroot1 Mutant of Arabidopsis thaliana journal February 1998
The Arabidopsis Auxin-Inducible Gene ARGOS Controls Lateral Organ Size journal August 2003
Characterization of an Arabidopsis Enzyme Family That Conjugates Amino Acids to Indole-3-Acetic Acid journal January 2005
The Gene Controlling the Quantitative Trait Locus EPITHIOSPECIFIER MODIFIER1 Alters Glucosinolate Hydrolysis and Insect Resistance in Arabidopsis journal May 2006
Auxin Synthesized by the YUCCA Flavin Monooxygenases Is Essential for Embryogenesis and Leaf Formation in Arabidopsis journal August 2007
Global Analysis of DELLA Direct Targets in Early Gibberellin Signaling in Arabidopsis journal October 2007
AUXIN RESPONSE FACTOR8 Regulates Arabidopsis Petal Growth by Interacting with the bHLH Transcription Factor BIGPETALp journal March 2011
Ion Exchangers NHX1 and NHX2 Mediate Active Potassium Uptake into Vacuoles to Regulate Cell Turgor and Stomatal Function in Arabidopsis journal March 2012
Soluble Carbohydrates Regulate Auxin Biosynthesis via PIF Proteins in Arabidopsis journal December 2012
Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. journal November 1997
CYP90C1 and CYP90D1 are involved in different steps in the brassinosteroid biosynthesis pathway in Arabidopsis thaliana: ROT3 and CYP90D1 in brassinosteroid biosynthesis journal February 2005
Overexpression of COL9, a CONSTANS-LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana: Overexpression of COL9 delays flowering journal August 2005
The Arabidopsis ARGOS-LIKE gene regulates cell expansion during organ growth journal July 2006
BTB and TAZ domain scaffold proteins perform a crucial function in Arabidopsis development: Arabidopsis BT proteins and gametophyte development journal January 2009
LOV KELCH PROTEIN2 and ZEITLUPE repress Arabidopsis photoperiodic flowering under non-inductive conditions, dependent on FLAVIN-BINDING KELCH REPEAT F-BOX1: LKP2 and ZTL repress flowering, dependent on FKF1 journal July 2011
The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion: SAUR fusion proteins promote cell expansion journal March 2012
The endoplasmic reticulum localized PIN8 is a pollen-specific auxin carrier involved in intracellular auxin homeostasis: Endoplasmic reticulum localized PIN8 journal July 2012
Arabidopsis ORGAN SIZE RELATED1 regulates organ growth and final organ size in orchestration with ARGOS and ARL journal April 2011
Small auxin upregulated RNA ( SAUR ) gene family in maize: Identification, evolution, and its phylogenetic comparison with Arabidopsis , rice, and sorghum journal January 2014
Auxin influx importers modulate serration along the leaf margin journal July 2015
A Bacterial Effector Acts as a Plant Transcription Factor and Induces a Cell Size Regulator journal October 2007
Photoexcited CRY2 Interacts with CIB1 to Regulate Transcription and Floral Initiation in Arabidopsis journal December 2008
Developmentally Regulated Systemic Endopolyploid in Succulents with Small Genomes journal October 1990
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome journal August 2011
jvenn: an interactive Venn diagram viewer journal January 2014
Protocol: High-throughput and quantitative assays of auxin and auxin precursors from minute tissue samples journal January 2012
voom: precision weights unlock linear model analysis tools for RNA-seq read counts journal January 2014
OmicLoupe: facilitating biological discovery by interactive exploration of multiple omic datasets and statistical comparisons journal March 2021
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
Brassinosteroid perception in the epidermis controls root meristem size journal January 2011
Auxin metabolism and homeostasis during plant development journal February 2013
LEAFY expression and flower initiation in Arabidopsis journal October 1997
Improved Gateway Binary Vectors: High-Performance Vectors for Creation of Fusion Constructs in Transgenic Analysis of Plants journal August 2007
Multiple bHLH Proteins form Heterodimers to Mediate CRY2-Dependent Regulation of Flowering-Time in Arabidopsis journal October 2013
Auxin Influx Carriers Control Vascular Patterning and Xylem Differentiation in Arabidopsis thaliana journal April 2015
Does Ploidy Level Directly Control Cell Size? Counterevidence from Arabidopsis Genetics journal December 2013
Auxin Import and Local Auxin Biosynthesis Are Required for Mitotic Divisions, Cell Expansion and Cell Specification during Female Gametophyte Development in Arabidopsis thaliana journal May 2015
Aux/IAA Proteins Repress Expression of Reporter Genes Containing Natural and Highly Active Synthetic Auxin Response Elements journal November 1997
Genetically modified crops for biomass increase. Genes and strategies journal May 2010
The Root Apex of Arabidopsis thaliana Consists of Four Distinct Zones of Growth Activities : Meristematic Zone, Transition Zone, Fast Elongation Zone and Growth Terminating Zone journal November 2006
Intracellular auxin transport in pollen: PIN8, PIN5 and PILS5 journal November 2012
Cytosolic calcium and pH signaling in plants under salinity stress journal March 2010
Tissue-specific expression of SMALL AUXIN UP RNA41 differentially regulates cell expansion and root meristem patterning in Arabidopsis text January 2013
Combining growth-promoting genes leads to positive epistasis in Arabidopsis thaliana journal April 2014

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