skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Abstract

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 (VvCEB1 opt) 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 VvCEB1 opt-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 VvCEB1 opt 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 VvCEB1 opt-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 andmore » organ number proliferation were likely an auxin-mediated process. VvCEB1 opt 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.« less

Authors:
 [1];  [1]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [1]
  1. Univ. of Nevada, Reno, NV (United States). Department of Biochemistry and Molecular Biology
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1435181
Grant/Contract Number:  
AC05-00OR22725; SC0008834
Resource Type:
Accepted Manuscript
Journal Name:
Plant Biotechnology Journal
Additional Journal Information:
Journal Volume: 16; Journal Issue: 9; Journal ID: ISSN 1467-7644
Publisher:
Society for Experimental Biology; Association of Applied Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; basic helix-loop-helix transcription factor; cell expansion; auxin; delayed flowering; biomass production; Arabidopsis thaliana

Citation Formats

Lim, Sung Don, Yim, Won Choel, Liu, Degao, Hu, Rongbin, Yang, Xiaohan, and Cushman, John C. A Vitis vinifera basic helix-loop-helix transcription factor enhances plant cell size, vegetative biomass and reproductive yield. United States: N. p., 2018. Web. doi:10.1111/pbi.12898.
Lim, Sung Don, Yim, Won Choel, Liu, Degao, Hu, Rongbin, Yang, Xiaohan, & Cushman, John C. A Vitis vinifera basic helix-loop-helix transcription factor enhances plant cell size, vegetative biomass and reproductive yield. United States. doi:10.1111/pbi.12898.
Lim, Sung Don, Yim, Won Choel, Liu, Degao, Hu, Rongbin, Yang, Xiaohan, and Cushman, John C. Mon . "A Vitis vinifera basic helix-loop-helix transcription factor enhances plant cell size, vegetative biomass and reproductive yield". United States. doi:10.1111/pbi.12898. https://www.osti.gov/servlets/purl/1435181.
@article{osti_1435181,
title = {A Vitis vinifera basic helix-loop-helix transcription factor enhances plant cell size, vegetative biomass and reproductive yield},
author = {Lim, Sung Don and Yim, Won Choel and Liu, Degao and Hu, Rongbin and Yang, Xiaohan and Cushman, John C.},
abstractNote = {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.},
doi = {10.1111/pbi.12898},
journal = {Plant Biotechnology Journal},
number = 9,
volume = 16,
place = {United States},
year = {2018},
month = {4}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 5 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

FIT, the FER-LIKE IRON DEFICIENCY INDUCED TRANSCRIPTION FACTOR in Arabidopsis
journal, May 2007


Araport: the Arabidopsis Information Portal
journal, November 2014

  • Krishnakumar, Vivek; Hanlon, Matthew R.; Contrino, Sergio
  • Nucleic Acids Research, Vol. 43, Issue D1
  • DOI: 10.1093/nar/gku1200

Auxin metabolism and homeostasis during plant development
journal, February 2013


The Gene Controlling the Quantitative Trait Locus EPITHIOSPECIFIER MODIFIER1 Alters Glucosinolate Hydrolysis and Insect Resistance in Arabidopsis
journal, May 2006

  • Zhang, Zhiyong; Ober, James A.; Kliebenstein, Daniel J.
  • The Plant Cell, Vol. 18, Issue 6
  • DOI: 10.1105/tpc.105.039602

A Bacterial Effector Acts as a Plant Transcription Factor and Induces a Cell Size Regulator
journal, October 2007


BT2, a BTB Protein, Mediates Multiple Responses to Nutrients, Stresses, and Hormones in Arabidopsis
journal, June 2009

  • Mandadi, Kranthi K.; Misra, Anjali; Ren, Shuxin
  • Plant Physiology, Vol. 150, Issue 4
  • DOI: 10.1104/pp.109.139220

Origin and Diversification of Basic-Helix-Loop-Helix Proteins in Plants
journal, November 2009


Cytosolic calcium and pH signaling in plants under salinity stress
journal, March 2010

  • Kader, Md Abdul; Lindberg, Sylvia
  • Plant Signaling & Behavior, Vol. 5, Issue 3
  • DOI: 10.4161/psb.5.3.10740

The BioGRID interaction database: 2015 update
journal, November 2014

  • Chatr-aryamontri, Andrew; Breitkreutz, Bobby-Joe; Oughtred, Rose
  • Nucleic Acids Research, Vol. 43, Issue D1
  • DOI: 10.1093/nar/gku1204

Intracellular auxin transport in pollen: PIN8, PIN5 and PILS5
journal, November 2012

  • Dal Bosco, Cristina; Dovzhenko, Alexander; Palme, Klaus
  • Plant Signaling & Behavior, Vol. 7, Issue 11
  • DOI: 10.4161/psb.21953

Molybdenum as an essential element for improving total yield in seawater-grown Salicornia europaea L.
journal, September 2010


Leaf epinasty and auxin: A biochemical and molecular overview
journal, December 2016


Molecular dissection of a rice microtubule-associated RING finger protein and its potential role in salt tolerance in Arabidopsis
journal, September 2015


Ion Exchangers NHX1 and NHX2 Mediate Active Potassium Uptake into Vacuoles to Regulate Cell Turgor and Stomatal Function in Arabidopsis
journal, March 2012

  • Barragán, Verónica; Leidi, Eduardo O.; Andrés, Zaida
  • The Plant Cell, Vol. 24, Issue 3
  • DOI: 10.1105/tpc.111.095273

Estimation of nuclear DNA content of plants by flow cytometry
journal, August 1991

  • Arumuganathan, K.; Earle, E. D.
  • Plant Molecular Biology Reporter, Vol. 9, Issue 3
  • DOI: 10.1007/BF02672073

SAMBA, a plant-specific anaphase-promoting complex/cyclosome regulator is involved in early development and A-type cyclin stabilization
journal, August 2012

  • Eloy, N. B.; Gonzalez, N.; Van Leene, J.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 34
  • DOI: 10.1073/pnas.1211418109

Identification and Characterization of Transcription Factors Regulating Arabidopsis HAK5
journal, July 2013

  • Hong, Jong-Pil; Takeshi, Yoshizumi; Kondou, Youichi
  • Plant and Cell Physiology, Vol. 54, Issue 9
  • DOI: 10.1093/pcp/pct094

Auxin Synthesized by the YUCCA Flavin Monooxygenases Is Essential for Embryogenesis and Leaf Formation in Arabidopsis
journal, August 2007


Combining growth-promoting genes leads to positive epistasis in Arabidopsis thaliana
journal, April 2014

  • Vanhaeren, Hannes; Gonzalez, Nathalie; Coppens, Frederik
  • eLife, Vol. 3
  • DOI: 10.7554/eLife.02252

Auxin Influx Carriers Control Vascular Patterning and Xylem Differentiation in Arabidopsis thaliana
journal, April 2015


Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis
journal, January 2000

  • Mizukami, Y.; Fischer, R. L.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 2
  • DOI: 10.1073/pnas.97.2.942

Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana
journal, August 2000

  • Cho, H. -T.; Cosgrove, D. J.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 17
  • DOI: 10.1073/pnas.160276997

Higher Activity of an Aldehyde Oxidase in the Auxin-Overproducing superroot1 Mutant of Arabidopsis thaliana
journal, February 1998

  • Seo, Mitsunori; Akaba, Shuichi; Oritani, Takayuki
  • Plant Physiology, Vol. 116, Issue 2
  • DOI: 10.1104/pp.116.2.687

Production of transgenic Nicotiana sylvestris plants expressing melatonin synthetase genes and their effect on UV-B-induced DNA damage
journal, October 2011

  • Zhang, LaiJun; Jia, JingFen; Xu, Yao
  • In Vitro Cellular & Developmental Biology - Plant, Vol. 48, Issue 3
  • DOI: 10.1007/s11627-011-9413-0

Iron- and Ferritin-Dependent Reactive Oxygen Species Distribution: Impact on Arabidopsis Root System Architecture
journal, March 2015


Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs
journal, August 2016

  • Campos, Marcelo L.; Yoshida, Yuki; Major, Ian T.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms12570

Brassinosteroid perception in the epidermis controls root meristem size
journal, January 2011

  • Hacham, Y.; Holland, N.; Butterfield, C.
  • Development, Vol. 138, Issue 5
  • DOI: 10.1242/dev.061804

Contrasting Modes of Diversification in the Aux/IAA and ARF Gene Families
journal, July 2004

  • Remington, David L.; Vision, Todd J.; Guilfoyle, Thomas J.
  • Plant Physiology, Vol. 135, Issue 3
  • DOI: 10.1104/pp.104.039669

The Arabidopsis Auxin-Inducible Gene ARGOS Controls Lateral Organ Size
journal, August 2003

  • Hu, Yuxin; Xie, Qi; Chua, Nam-Hai
  • The Plant Cell, Vol. 15, Issue 9
  • DOI: 10.1105/tpc.013557

Colorimetric Method for Determination of Sugars and Related Substances
journal, March 1956

  • DuBois, Michel.; Gilles, K. A.; Hamilton, J. K.
  • Analytical Chemistry, Vol. 28, Issue 3, p. 350-356
  • DOI: 10.1021/ac60111a017

Expression of a rice OsARGOS gene in Arabidopsis promotes cell division and expansion and increases organ size
journal, January 2009


Miniaturization of three carbohydrate analyses using a microsample plate reader
journal, May 1991


RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome
journal, August 2011


Specialized Zones of Development in Roots
journal, November 1995


Diversity and specificity: auxin perception and signaling through the TIR1/AFB pathway
journal, October 2014


Global Analysis of DELLA Direct Targets in Early Gibberellin Signaling in Arabidopsis
journal, October 2007

  • Zentella, Rodolfo; Zhang, Zhong-Lin; Park, Mehea
  • The Plant Cell, Vol. 19, Issue 10
  • DOI: 10.1105/tpc.107.054999

Multiple bHLH Proteins form Heterodimers to Mediate CRY2-Dependent Regulation of Flowering-Time in Arabidopsis
journal, October 2013


Auxin influx importers modulate serration along the leaf margin
journal, July 2015

  • Kasprzewska, Ania; Carter, Ross; Swarup, Ranjan
  • The Plant Journal, Vol. 83, Issue 4
  • DOI: 10.1111/tpj.12921

Molecular Cloning and Characterization of Aldehyde Oxidases in Arabidopsis thaliana
journal, April 1998


Improved Gateway Binary Vectors: High-Performance Vectors for Creation of Fusion Constructs in Transgenic Analysis of Plants
journal, August 2007

  • Nakagawa, Tsuyoshi; Suzuki, Takamasa; Murata, Satoko
  • Bioscience, Biotechnology, and Biochemistry, Vol. 71, Issue 8
  • DOI: 10.1271/bbb.70216

Rapid Synthesis of Auxin via a New Tryptophan-Dependent Pathway Is Required for Shade Avoidance in Plants
journal, April 2008


Auxin-induced growth and its linkage to potassium channels
journal, January 1997

  • Claussen, Maike; L�the, Hartwig; Blatt, Michael
  • Planta, Vol. 201, Issue 2
  • DOI: 10.1007/BF01007708

P-Loop-Dependent NLR SNC1 Can Oligomerize and Activate Immunity in the Nucleus
journal, December 2014

  • Xu, Fang; Cheng, Yu Ti; Kapos, Paul
  • Molecular Plant, Vol. 7, Issue 12
  • DOI: 10.1093/mp/ssu097

Ward’s Hierarchical Agglomerative Clustering Method: Which Algorithms Implement Ward’s Criterion?
journal, October 2014


De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis
journal, July 2013

  • Haas, Brian J.; Papanicolaou, Alexie; Yassour, Moran
  • Nature Protocols, Vol. 8, Issue 8
  • DOI: 10.1038/nprot.2013.084

Principal component analysis based methods in bioinformatics studies
journal, January 2011


Arabidopsis ORGAN SIZE RELATED1 regulates organ growth and final organ size in orchestration with ARGOS and ARL
journal, April 2011


Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method
journal, June 2006

  • Zhang, Xiuren; Henriques, Rossana; Lin, Shih-Shun
  • Nature Protocols, Vol. 1, Issue 2
  • DOI: 10.1038/nprot.2006.97

Making bigger plants: key regulators of final organ size
journal, February 2009


Model for the regulation of Arabidopsis thaliana leaf margin development
journal, February 2011

  • Bilsborough, G. D.; Runions, A.; Barkoulas, M.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 8
  • DOI: 10.1073/pnas.1015162108

Developmentally Regulated Systemic Endopolyploid in Succulents with Small Genomes
journal, October 1990


BIGPETALp, a bHLH transcription factor is involved in the control of Arabidopsis petal size
journal, August 2006


Small auxin upregulated RNA ( SAUR ) gene family in maize: Identification, evolution, and its phylogenetic comparison with Arabidopsis , rice, and sorghum
journal, January 2014

  • Chen, Yuzhu; Hao, Xi; Cao, Jun
  • Journal of Integrative Plant Biology, Vol. 56, Issue 2
  • DOI: 10.1111/jipb.12127

Pseudomonas syringae Effector AvrPphB Suppresses AvrB-Induced Activation of RPM1 but Not AvrRpm1-Induced Activation
journal, June 2015

  • Russell, Andrew R.; Ashfield, Tom; Innes, Roger W.
  • Molecular Plant-Microbe Interactions, Vol. 28, Issue 6
  • DOI: 10.1094/MPMI-08-14-0248-R

Auxin at the Shoot Apical Meristem
journal, March 2010


Expression analysis of the AtMLO Gene Family Encoding Plant-Specific Seven-Transmembrane Domain Proteins
journal, March 2006

  • Chen, Zhongying; Hartmann, H. Andreas; Wu, Ming-Jing
  • Plant Molecular Biology, Vol. 60, Issue 4
  • DOI: 10.1007/s11103-005-5082-x

AUXIN RESPONSE FACTOR8 Regulates Arabidopsis Petal Growth by Interacting with the bHLH Transcription Factor BIGPETALp
journal, March 2011

  • Varaud, Emilie; Brioudes, Florian; Szécsi, Judit
  • The Plant Cell, Vol. 23, Issue 3
  • DOI: 10.1105/tpc.110.081653

Leaf anatomical traits which accommodate the facultative engagement of crassulacean acid metabolism in tropical trees of the genus Clusia
journal, February 2014

  • Barrera Zambrano, V. A.; Lawson, T.; Olmos, E.
  • Journal of Experimental Botany, Vol. 65, Issue 13
  • DOI: 10.1093/jxb/eru022

jvenn: an interactive Venn diagram viewer
journal, January 2014

  • Bardou, Philippe; Mariette, Jérôme; Escudié, Frédéric
  • BMC Bioinformatics, Vol. 15, Issue 1
  • DOI: 10.1186/1471-2105-15-293

The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion: SAUR fusion proteins promote cell expansion
journal, March 2012


Genetically modified crops for biomass increase. Genes and strategies
journal, May 2010

  • Rojas, Cristian Antonio; Hemerly, Adrianna Silva; Ferreira, Paulo Cavalcanti Gomes
  • GM Crops, Vol. 1, Issue 3
  • DOI: 10.4161/gmcr.1.3.12615

Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering: FLM is a MADS-box flowering repressor
journal, April 2001


A combinatorial TIR1/AFB–Aux/IAA co-receptor system for differential sensing of auxin
journal, April 2012

  • Calderón Villalobos, Luz Irina A.; Lee, Sarah; De Oliveira, Cesar
  • Nature Chemical Biology, Vol. 8, Issue 5
  • DOI: 10.1038/nchembio.926

SAUR36, a SMALL AUXIN UP RNA Gene, Is Involved in the Promotion of Leaf Senescence 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


Genome-Wide Identification and Testing of Superior Reference Genes for Transcript Normalization in Arabidopsis
journal, September 2005

  • Czechowski, Tomasz; Stitt, Mark; Altmann, Thomas
  • Plant Physiology, Vol. 139, Issue 1
  • DOI: 10.1104/pp.105.063743

edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
journal, November 2009


AGRIS: the Arabidopsis Gene Regulatory Information Server, an update
journal, November 2010

  • Yilmaz, A.; Mejia-Guerra, M. K.; Kurz, K.
  • Nucleic Acids Research, Vol. 39, Issue Database
  • DOI: 10.1093/nar/gkq1120

ROTS: reproducible RNA-seq biomarker detector—prognostic markers for clear cell renal cell cancer
journal, August 2015

  • Seyednasrollah, Fatemeh; Rantanen, Krista; Jaakkola, Panu
  • Nucleic Acids Research, Vol. 44, Issue 1
  • DOI: 10.1093/nar/gkv806

Fast gapped-read alignment with Bowtie 2
journal, March 2012

  • Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 9, Issue 4
  • DOI: 10.1038/nmeth.1923

The grape berry-specific basic helix–loop–helix transcription factor VvCEB1 affects cell size
journal, January 2013

  • Nicolas, Philippe; Lecourieux, David; Gomès, Eric
  • Journal of Experimental Botany, Vol. 64, Issue 4
  • DOI: 10.1093/jxb/ers374

Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003


The Biochemical Mechanism of Auxin Biosynthesis by an Arabidopsis YUCCA Flavin-containing Monooxygenase
journal, November 2012

  • Dai, Xinhua; Mashiguchi, Kiyoshi; Chen, Qingguo
  • Journal of Biological Chemistry, Vol. 288, Issue 3
  • DOI: 10.1074/jbc.M112.424077

Soluble Carbohydrates Regulate Auxin Biosynthesis via PIF Proteins in Arabidopsis
journal, December 2012

  • Sairanen, Ilkka; Novák, Ondřej; Pěnčík, Aleš
  • The Plant Cell, Vol. 24, Issue 12
  • DOI: 10.1105/tpc.112.104794

Tissue-Specific Expression of SMALL AUXIN UP RNA41 Differentially Regulates Cell Expansion and Root Meristem Patterning in Arabidopsis
journal, March 2013

  • Kong, Yingying; Zhu, Yubin; Gao, Chen
  • Plant and Cell Physiology, Vol. 54, Issue 4
  • DOI: 10.1093/pcp/pct028

Quality assurance for plant tissue analysis by ICP‐AES
journal, October 1984

  • Munter, R. C.; Halverson, T. L.; Anderson, R. D.
  • Communications in Soil Science and Plant Analysis, Vol. 15, Issue 11
  • DOI: 10.1080/00103628409367559

Photoexcited CRY2 Interacts with CIB1 to Regulate Transcription and Floral Initiation in Arabidopsis
journal, December 2008


voom: precision weights unlock linear model analysis tools for RNA-seq read counts
journal, January 2014


Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis
journal, July 2006

  • Cheng, Youfa; Dai, Xinhua; Zhao, Yunde
  • Genes & Development, Vol. 20, Issue 13
  • DOI: 10.1101/gad.1415106

Comprehensive Transcriptome Analysis of Auxin Responses in Arabidopsis
journal, March 2008

  • Paponov, Ivan A.; Paponov, Martina; Teale, William
  • Molecular Plant, Vol. 1, Issue 2
  • DOI: 10.1093/mp/ssm021

ER-localized auxin transporter PIN8 regulates auxin homeostasis and male gametophyte development in Arabidopsis
journal, January 2012

  • Ding, Zhaojun; Wang, Bangjun; Moreno, Ignacio
  • Nature Communications, Vol. 3, Issue 1
  • DOI: 10.1038/ncomms1941

Characterization of an Arabidopsis Enzyme Family That Conjugates Amino Acids to Indole-3-Acetic Acid
journal, January 2005

  • Staswick, Paul E.; Serban, Bogdan; Rowe, Martha
  • The Plant Cell, Vol. 17, Issue 2
  • DOI: 10.1105/tpc.104.026690

Protocol: High-throughput and quantitative assays of auxin and auxin precursors from minute tissue samples
journal, January 2012


Does Ploidy Level Directly Control Cell Size? Counterevidence from Arabidopsis Genetics
journal, December 2013


The Sequence Alignment/Map format and SAMtools
journal, June 2009


SAUR Proteins as Effectors of Hormonal and Environmental Signals in Plant Growth
journal, August 2015


The Arabidopsis ARGOS-LIKE gene regulates cell expansion during organ growth
journal, July 2006


Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids
journal, November 2008