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Title: Poplar PtabZIP1-like enhances lateral root formation and biomass growth under drought stress

Abstract

Summary Developing drought‐resistance varieties is a major goal for bioenergy crops, such as poplar ( Populus ), which will be grown on marginal lands with little or no water input. Root architecture can affect drought resistance, but few genes that affect root architecture in relation to water availability have been identified. Here, using activation tagging in the prime bioenergy crop poplar, we have identified a mutant that overcomes the block of lateral root ( LR ) formation under osmotic stress. Positioning of the tag, validation of the activation and recapitulation showed that the phenotype is caused by the poplar Ptab ZIP 1‐like ( Ptab ZIP 1L ) gene with highest homology to bZIP 1 from Arabidopsis. Ptab ZIP 1L is predominantly expressed in roots, particularly in zones where lateral root primordia ( LRP ) initiate and LR differentiate and emerge. Transgenics overexpressing Ptab ZIP 1L showed precocious LRP and LR development, while Ptab ZIP 1L suppression significantly delayed both LRP and LR formation. Transgenic overexpression and suppression of Ptab ZIP 1L also resulted in modulation of key metabolites like proline, asparagine, valine and several flavonoids. Consistently, expression of both of the poplar Proline Dehydrogenase orthologs and two of the Flavonolmore » Synthases genes was also increased and decreased in overexpressed and suppressed transgenics, respectively. These findings suggest that Ptab ZIP 1L mediates LR development and drought resistance through modulation of multiple metabolic pathways.« less

Authors:
 [1];  [1];  [1];  [2];  [1];  [1]
  1. Michigan Technological Univ., Houghton, MI (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Bioscience Division
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); US Department of Agriculture (USDA)
OSTI Identifier:
1349610
Alternate Identifier(s):
OSTI ID: 1401028
Grant/Contract Number:  
AC05-00OR22725; SC0008462; 2009-65504-05767
Resource Type:
Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Volume: 89; Journal Issue: 4; Journal ID: ISSN 0960-7412
Publisher:
Society for Experimental Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; PtabZIP1-like; lateral root growth; Flavonol Synthases; flavonoid biosynthesis; Populus tremula × P. alba; drought resistance

Citation Formats

Dash, Madhumita, Yordanov, Yordan S., Georgieva, Tatyana, Tschaplinski, Timothy J., Yordanova, Elena, and Busov, Victor. Poplar PtabZIP1-like enhances lateral root formation and biomass growth under drought stress. United States: N. p., 2017. Web. doi:10.1111/tpj.13413.
Dash, Madhumita, Yordanov, Yordan S., Georgieva, Tatyana, Tschaplinski, Timothy J., Yordanova, Elena, & Busov, Victor. Poplar PtabZIP1-like enhances lateral root formation and biomass growth under drought stress. United States. https://doi.org/10.1111/tpj.13413
Dash, Madhumita, Yordanov, Yordan S., Georgieva, Tatyana, Tschaplinski, Timothy J., Yordanova, Elena, and Busov, Victor. Fri . "Poplar PtabZIP1-like enhances lateral root formation and biomass growth under drought stress". United States. https://doi.org/10.1111/tpj.13413. https://www.osti.gov/servlets/purl/1349610.
@article{osti_1349610,
title = {Poplar PtabZIP1-like enhances lateral root formation and biomass growth under drought stress},
author = {Dash, Madhumita and Yordanov, Yordan S. and Georgieva, Tatyana and Tschaplinski, Timothy J. and Yordanova, Elena and Busov, Victor},
abstractNote = {Summary Developing drought‐resistance varieties is a major goal for bioenergy crops, such as poplar ( Populus ), which will be grown on marginal lands with little or no water input. Root architecture can affect drought resistance, but few genes that affect root architecture in relation to water availability have been identified. Here, using activation tagging in the prime bioenergy crop poplar, we have identified a mutant that overcomes the block of lateral root ( LR ) formation under osmotic stress. Positioning of the tag, validation of the activation and recapitulation showed that the phenotype is caused by the poplar Ptab ZIP 1‐like ( Ptab ZIP 1L ) gene with highest homology to bZIP 1 from Arabidopsis. Ptab ZIP 1L is predominantly expressed in roots, particularly in zones where lateral root primordia ( LRP ) initiate and LR differentiate and emerge. Transgenics overexpressing Ptab ZIP 1L showed precocious LRP and LR development, while Ptab ZIP 1L suppression significantly delayed both LRP and LR formation. Transgenic overexpression and suppression of Ptab ZIP 1L also resulted in modulation of key metabolites like proline, asparagine, valine and several flavonoids. Consistently, expression of both of the poplar Proline Dehydrogenase orthologs and two of the Flavonol Synthases genes was also increased and decreased in overexpressed and suppressed transgenics, respectively. These findings suggest that Ptab ZIP 1L mediates LR development and drought resistance through modulation of multiple metabolic pathways.},
doi = {10.1111/tpj.13413},
journal = {The Plant Journal},
number = 4,
volume = 89,
place = {United States},
year = {Fri Feb 10 00:00:00 EST 2017},
month = {Fri Feb 10 00:00:00 EST 2017}
}

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Works referenced in this record:

Auxin and Ethylene Induce Flavonol Accumulation through Distinct Transcriptional Networks
journal, March 2011

  • Lewis, Daniel R.; Ramirez, Melissa V.; Miller, Nathan D.
  • Plant Physiology, Vol. 156, Issue 1
  • DOI: 10.1104/pp.111.172502

Arabidopsis H+-PPase AVP1 Regulates Auxin-Mediated Organ Development
journal, October 2005


A DNA Transformation–Competent Arabidopsis Genomic Library in Agrobacterium
journal, October 1991

  • Lazo, Gerard R.; Stein, Pascal A.; Ludwig, Robert A.
  • Bio/Technology, Vol. 9, Issue 10
  • DOI: 10.1038/nbt1091-963

Hormonal Regulation of Lateral Root Development in Arabidopsis Modulated by MIZ1 and Requirement of GNOM Activity for MIZ1 Function
journal, September 2011

  • Moriwaki, Teppei; Miyazawa, Yutaka; Kobayashi, Akie
  • Plant Physiology, Vol. 157, Issue 3
  • DOI: 10.1104/pp.111.186270

Transcription factors that directly regulate the expression of CSLA9 encoding mannan synthase in Arabidopsis thaliana
journal, November 2013


Plant Flavonoids—Biosynthesis, Transport and Involvement in Stress Responses
journal, July 2013

  • Petrussa, Elisa; Braidot, Enrico; Zancani, Marco
  • International Journal of Molecular Sciences, Vol. 14, Issue 7
  • DOI: 10.3390/ijms140714950

MetaboAnalyst 3.0—making metabolomics more meaningful
journal, April 2015

  • Xia, Jianguo; Sinelnikov, Igor V.; Han, Beomsoo
  • Nucleic Acids Research, Vol. 43, Issue W1
  • DOI: 10.1093/nar/gkv380

Overexpression of MIZU-KUSSEI1 Enhances the Root Hydrotropic Response by Retaining Cell Viability Under Hydrostimulated Conditions in Arabidopsis thaliana
journal, September 2012

  • Miyazawa, Yutaka; Moriwaki, Teppei; Uchida, Mayumi
  • Plant and Cell Physiology, Vol. 53, Issue 11
  • DOI: 10.1093/pcp/pcs129

Food and fuel for all: realistic or foolish?
journal, January 2007

  • G. Cassman, Kenneth; Liska, Adam J.
  • Biofuels, Bioproducts and Biorefining, Vol. 1, Issue 1
  • DOI: 10.1002/bbb.3

Breeding for high water-use efficiency
journal, September 2004

  • Condon, A. G.
  • Journal of Experimental Botany, Vol. 55, Issue 407
  • DOI: 10.1093/jxb/erh277

Activation Tagging of a Dominant Gibberellin Catabolism Gene ( GA 2-oxidase ) from Poplar That Regulates Tree Stature
journal, June 2003

  • Busov, Victor B.; Meilan, Richard; Pearce, David W.
  • Plant Physiology, Vol. 132, Issue 3
  • DOI: 10.1104/pp.103.020354

Role of proline under changing environments: A review
journal, November 2012

  • Hayat, Shamsul; Hayat, Qaiser; Alyemeni, Mohammed Nasser
  • Plant Signaling & Behavior, Vol. 7, Issue 11
  • DOI: 10.4161/psb.21949

Interactions among enzymes of the Arabidopsis flavonoid biosynthetic pathway
journal, October 1999

  • Burbulis, I. E.; Winkel-Shirley, B.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 22
  • DOI: 10.1073/pnas.96.22.12929

Modeling the global effect of the basic-leucine zipper transcription factor 1 (bZIP1) on nitrogen and light regulation in Arabidopsis
journal, January 2010

  • Obertello, Mariana; Krouk, Gabriel; Katari, Manpreet S.
  • BMC Systems Biology, Vol. 4, Issue 1
  • DOI: 10.1186/1752-0509-4-111

The MYB96 Transcription Factor Mediates Abscisic Acid Signaling during Drought Stress Response in Arabidopsis
journal, July 2009

  • Seo, Pil Joon; Xiang, Fengning; Qiao, Meng
  • Plant Physiology, Vol. 151, Issue 1
  • DOI: 10.1104/pp.109.144220

Heterodimers of the Arabidopsis Transcription Factors bZIP1 and bZIP53 Reprogram Amino Acid Metabolism during Low Energy Stress
journal, January 2011

  • Dietrich, Katrin; Weltmeier, Fridtjof; Ehlert, Andrea
  • The Plant Cell, Vol. 23, Issue 1
  • DOI: 10.1105/tpc.110.075390

More from less: plant growth under limited water
journal, April 2010


Identification, characterization of an AP2/ERF transcription factor that promotes adventitious, lateral root formation in Populus
journal, May 2013


Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants
journal, December 2005

  • Park, S.; Li, J.; Pittman, J. K.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 52
  • DOI: 10.1073/pnas.0509512102

GATEWAY™ vectors for Agrobacterium-mediated plant transformation
journal, May 2002


The role of root architectural traits in adaptation of wheat to water-limited environments
journal, January 2006

  • Manschadi, Ahmad M.; Christopher, John; deVoil, Peter
  • Functional Plant Biology, Vol. 33, Issue 9
  • DOI: 10.1071/FP06055

Flavonoids as Important Molecules of Plant Interactions with the Environment
journal, October 2014


Flavonoid Accumulation Patterns of Transparent Testa Mutants of Arabidopsis
journal, June 2001

  • Peer, Wendy Ann; Brown, Dana E.; Tague, Brian W.
  • Plant Physiology, Vol. 126, Issue 2
  • DOI: 10.1104/pp.126.2.536

Quantitative Trait Loci and Crop Performance under Abiotic Stress: Where Do We Stand?: Table I.
journal, June 2008

  • Collins, Nicholas C.; Tardieu, François; Tuberosa, Roberto
  • Plant Physiology, Vol. 147, Issue 2
  • DOI: 10.1104/pp.108.118117

Meta-analysis of constitutive and adaptive QTL for drought tolerance in maize
journal, December 2009


Soil structure and the effect of management practices
journal, December 2004


EARLY BUD-BREAK 1 ( EBB1 ) is a regulator of release from seasonal dormancy in poplar trees
journal, June 2014

  • Yordanov, Yordan S.; Ma, Cathleen; Strauss, Steven H.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 27
  • DOI: 10.1073/pnas.1405621111

The Arabidopsis bZIP1 Transcription Factor Is Involved in Sugar Signaling, Protein Networking, and DNA Binding
journal, March 2010

  • Kang, Shin Gene; Price, John; Lin, Pei-Chi
  • Molecular Plant, Vol. 3, Issue 2
  • DOI: 10.1093/mp/ssp115

Flavonoid oxidation in plants: from biochemical properties to physiological functions
journal, January 2007


Insertional mutagenesis in Populus: relevance and feasibility
journal, November 2005


Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on flavonol biosynthesis
journal, January 2012

  • Grunewald, W.; De Smet, I.; Lewis, D. R.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 5
  • DOI: 10.1073/pnas.1121134109

Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids
journal, December 2013

  • Nakabayashi, Ryo; Yonekura-Sakakibara, Keiko; Urano, Kaoru
  • The Plant Journal, Vol. 77, Issue 3
  • DOI: 10.1111/tpj.12388

Transgenics are imperative for biofuel crops
journal, March 2008


NIH Image to ImageJ: 25 years of image analysis
journal, June 2012

  • Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W.
  • Nature Methods, Vol. 9, Issue 7
  • DOI: 10.1038/nmeth.2089

An Agrobacterium tumefaciens transformation protocol effective on a variety of cottonwood hybrids (genus Populus)
journal, January 2000

  • Han, K.-H.; Meilan, R.; Ma, C.
  • Plant Cell Reports, Vol. 19, Issue 3, p. 315-320
  • DOI: 10.1007/s002990050019

A new mathematical model for relative quantification in real-time RT-PCR
journal, May 2001


Plant bZIP Transcription Factors Responsive to Pathogens: A Review
journal, April 2013

  • Alves, Murilo; Dadalto, Silvana; Gonçalves, Amanda
  • International Journal of Molecular Sciences, Vol. 14, Issue 4
  • DOI: 10.3390/ijms14047815

Saturation mapping of QTL regions and identification of putative candidate genes for drought tolerance in rice
journal, June 2004

  • Nguyen, T. T. T.; Klueva, N.; Chamareck, V.
  • Molecular Genetics and Genomics, Vol. 272, Issue 1
  • DOI: 10.1007/s00438-004-1025-5

Root system architecture: opportunities and constraints for genetic improvement of crops
journal, October 2007


Genetic control of root development in rice, the model cereal
journal, April 2010


Quantitative trait loci influencing drought tolerance in grain sorghum (Sorghum bicolor L. Moench)
journal, August 2001

  • Kebede, H.; Subudhi, P. K.; Rosenow, D. T.
  • Theoretical and Applied Genetics, Vol. 103, Issue 2-3
  • DOI: 10.1007/s001220100541

Flavonoids Act as Negative Regulators of Auxin Transport in Vivo in Arabidopsis
journal, June 2001

  • Brown, Dana E.; Rashotte, Aaron M.; Murphy, Angus S.
  • Plant Physiology, Vol. 126, Issue 2
  • DOI: 10.1104/pp.126.2.524

Functional Analysis of a Predicted Flavonol Synthase Gene Family in Arabidopsis
journal, May 2008

  • Owens, Daniel K.; Alerding, Anne B.; Crosby, Kevin C.
  • Plant Physiology, Vol. 147, Issue 3
  • DOI: 10.1104/pp.108.117457

Dro1, a major QTL involved in deep rooting of rice under upland field conditions
journal, January 2011

  • Uga, Yusaku; Okuno, Kazutoshi; Yano, Masahiro
  • Journal of Experimental Botany, Vol. 62, Issue 8
  • DOI: 10.1093/jxb/erq429

Stress-Induced Phenylpropanoid Metabolism
journal, July 1995

  • Dixon, Richard A.; Paiva, Nancy L.
  • The Plant Cell, Vol. 7, Issue 7
  • DOI: 10.2307/3870059

A systems biology approach identifies new regulators of poplar root development under low nitrogen
journal, October 2015

  • Dash, Madhumita; Yordanov, Yordan S.; Georgieva, Tatyana
  • The Plant Journal, Vol. 84, Issue 2
  • DOI: 10.1111/tpj.13002

Nitrogen deprivation promotes Populus root growth through global transcriptome reprogramming and activation of hierarchical genetic networks
journal, June 2013

  • Wei, Hairong; Yordanov, Yordan S.; Georgieva, Tatyana
  • New Phytologist, Vol. 200, Issue 2
  • DOI: 10.1111/nph.12375

bZIP transcription factors in Arabidopsis
journal, March 2002


Marker assisted selection in crop plants
journal, September 2005

  • Francia, E.; Tacconi, G.; Crosatti, C.
  • Plant Cell, Tissue and Organ Culture, Vol. 82, Issue 3
  • DOI: 10.1007/s11240-005-2387-z

Stress-Induced Phenylpropanoid Metabolism.
journal, July 1995


MIZ1-regulated hydrotropism functions in the growth and survival of Arabidopsis thaliana under natural conditions
journal, May 2013

  • Iwata, Satoru; Miyazawa, Yutaka; Fujii, Nobuharu
  • Annals of Botany, Vol. 112, Issue 1
  • DOI: 10.1093/aob/mct098

GASA14 regulates leaf expansion and abiotic stress resistance by modulating reactive oxygen species accumulation
journal, February 2013

  • Sun, Shulan; Wang, Haoxiang; Yu, Hongmei
  • Journal of Experimental Botany, Vol. 64, Issue 6
  • DOI: 10.1093/jxb/ert021

Crop responses to drought and the interpretation of adaptation
journal, November 1996


Rooting depth and water use efficiency of tropical maize inbred lines, differing in drought tolerance
journal, December 2008


Flavonoids and auxin transport: modulators or regulators?
journal, December 2007


Evaluation of Aluminium Complexation Reaction for Flavonoid Content Assay
journal, February 2014


Genetic variability of drought-avoidance root traits in the mini-core germplasm collection of chickpea (Cicer arietinum L.).
journal, February 2006


Members of the LATERAL ORGAN BOUNDARIES DOMAIN Transcription Factor Family Are Involved in the Regulation of Secondary Growth in Populus
journal, November 2010

  • Yordanov, Yordan S.; Regan, Sharon; Busov, Victor
  • The Plant Cell, Vol. 22, Issue 11
  • DOI: 10.1105/tpc.110.078634

Sustainable bioenergy production from marginal lands in the US Midwest
journal, January 2013

  • Gelfand, Ilya; Sahajpal, Ritvik; Zhang, Xuesong
  • Nature, Vol. 493, Issue 7433
  • DOI: 10.1038/nature11811

Root traits contributing to plant productivity under drought
journal, January 2013

  • Comas, Louise H.; Becker, Steven R.; Cruz, Von Mark V.
  • Frontiers in Plant Science, Vol. 4
  • DOI: 10.3389/fpls.2013.00442

Plant bZIP Protein DNA Binding Specificity
journal, April 1993

  • Izawa, Takeshi; Foster, Randy; Chua, Nam-Hai
  • Journal of Molecular Biology, Vol. 230, Issue 4
  • DOI: 10.1006/jmbi.1993.1230

Variation in root system architecture and drought response in rice (Oryza sativa): Phenotyping of the OryzaSNP panel in rainfed lowland fields
journal, January 2011

  • Henry, Amelia; Gowda, Veeresh R. P.; Torres, Rolando O.
  • Field Crops Research, Vol. 120, Issue 2
  • DOI: 10.1016/j.fcr.2010.10.003

Transgenic Populus Trees for Forest Products, Bioenergy, and Functional Genomics
journal, September 2011


Kaempferol 3- O -rhamnoside-7- O -rhamnoside is an endogenous flavonol inhibitor of polar auxin transport in Arabidopsis shoots
journal, October 2013

  • Yin, Ruohe; Han, Kerstin; Heller, Werner
  • New Phytologist, Vol. 201, Issue 2
  • DOI: 10.1111/nph.12558

Transfection and transformation of Agrobacterium tumefaciens
journal, January 1978

  • Holsters, M.; de Waele, D.; Depicker, A.
  • Molecular and General Genetics MGG, Vol. 163, Issue 2
  • DOI: 10.1007/BF00267408

Soil salinity related to physical soil characteristics and irrigation management in four Mediterranean irrigation districts
journal, April 2011


Constraints and potentials of future irrigation water availability on agricultural production under climate change
journal, December 2013

  • Elliott, Joshua; Deryng, Delphine; Müller, Christoph
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 9
  • DOI: 10.1073/pnas.1222474110

Hit-and-run transcriptional control by bZIP1 mediates rapid nutrient signaling in Arabidopsis
journal, June 2014

  • Para, A.; Li, Y.; Marshall-Colon, A.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 28
  • DOI: 10.1073/pnas.1404657111

The anthocyanin reduced Tomato Mutant Demonstrates the Role of Flavonols in Tomato Lateral Root and Root Hair Development
journal, July 2014

  • Maloney, G. S.; DiNapoli, K. T.; Muday, G. K.
  • PLANT PHYSIOLOGY, Vol. 166, Issue 2
  • DOI: 10.1104/pp.114.240507

Multiple functional roles of flavonoids in photoprotection: Letters
journal, May 2010


Evidence of oxidative attenuation of auxin signalling
journal, May 2013

  • Peer, Wendy Ann; Cheng, Yan; Murphy, Angus S.
  • Journal of Experimental Botany, Vol. 64, Issue 9
  • DOI: 10.1093/jxb/ert152

Genotypic variation in seedling root architectural traits and implications for drought adaptation in wheat (Triticum aestivum L.)
journal, November 2007

  • Manschadi, Ahmad M.; Hammer, Graeme L.; Christopher, John T.
  • Plant and Soil, Vol. 303, Issue 1-2
  • DOI: 10.1007/s11104-007-9492-1

The Arabidopsis AtbZIP1 transcription factor is a positive regulator of plant tolerance to salt, osmotic and drought stresses
journal, September 2011


Water security for a planet under pressure: interconnected challenges of a changing world call for sustainable solutions
journal, February 2012

  • Bogardi, Janos J.; Dudgeon, David; Lawford, Richard
  • Current Opinion in Environmental Sustainability, Vol. 4, Issue 1
  • DOI: 10.1016/j.cosust.2011.12.002

Down-regulation of the caffeic acid O-methyltransferase gene in switchgrass reveals a novel monolignol analog
journal, January 2012

  • Tschaplinski, Timothy J.; Standaert, Robert F.; Engle, Nancy L.
  • Biotechnology for Biofuels, Vol. 5, Issue 1
  • DOI: 10.1186/1754-6834-5-71

Activation tagging is an effective gene tagging system in Populus
journal, July 2010


Investigating the drought-stress response of hybrid poplar genotypes by metabolite profiling
journal, October 2013


Regulation of auxin transport by aminopeptidases and endogenous flavonoids
journal, August 2000


The role of ABF family bZIP class transcription factors in stress response
journal, November 2005


Plants with genetically encoded autoluminescence
journal, April 2020

  • Mitiouchkina, Tatiana; Mishin, Alexander S.; Somermeyer, Louisa Gonzalez
  • Nature Biotechnology, Vol. 38, Issue 8
  • DOI: 10.1038/s41587-020-0500-9

Rooting depth and water use efficiency of tropical maize inbred lines, differing in drought tolerance
text, January 2009


Crop responses to drought and the interpretation of adaptation
book, January 1996

  • Blum, A.
  • Drought Tolerance in Higher Plants: Genetical, Physiological and Molecular Biological Analysis
  • DOI: 10.1007/978-94-017-1299-6_8

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OsMADS25 regulates root system development via auxin signalling in rice
journal, July 2018

  • Zhang, Guopeng; Xu, Ning; Chen, Hongli
  • The Plant Journal, Vol. 95, Issue 6
  • DOI: 10.1111/tpj.14007

The Sugar-Signaling Hub: Overview of Regulators and Interaction with the Hormonal and Metabolic Network
journal, August 2018

  • Sakr, Soulaiman; Wang, Ming; Dédaldéchamp, Fabienne
  • International Journal of Molecular Sciences, Vol. 19, Issue 9
  • DOI: 10.3390/ijms19092506

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journal, December 2018


p-Aminobenzoate Organic Salts as Potential Plant Growth Regulators for Tomatoes
journal, April 2020


Overexpression of a developing xylem cDNA library in transgenic poplar generates high mutation rate specific to wood formation
journal, December 2019

  • Rauschendorfer, James; Yordanov, Yordan; Dobrev, Petre
  • Plant Biotechnology Journal, Vol. 18, Issue 6
  • DOI: 10.1111/pbi.13309

Contribution of methylation regulation of MpDREB2A promoter to drought resistance of Mauls prunifolia
journal, June 2019


PeCHYR1, a ubiquitin E3 ligase from Populus euphratica , enhances drought tolerance via ABA-induced stomatal closure by ROS production in Populus
journal, March 2018

  • He, Fang; Wang, Hou-Ling; Li, Hui-Guang
  • Plant Biotechnology Journal, Vol. 16, Issue 8
  • DOI: 10.1111/pbi.12893

A unique bZIP transcription factor imparting multiple stress tolerance in Rice
journal, August 2019


Auxin Controlled by Ethylene Steers Root Development
journal, November 2018

  • Qin, Hua; Huang, Rongfeng
  • International Journal of Molecular Sciences, Vol. 19, Issue 11
  • DOI: 10.3390/ijms19113656

A unique bZIP transcription factor imparting multiple stress tolerance in Rice
journal, August 2019


Gene network analysis of poplar root transcriptome in response to drought stress identifies a PtaJAZ3PtaRAP2.6-centered hierarchical network
journal, December 2018


GmWRKY45 Enhances Tolerance to Phosphate Starvation and Salt Stress, and Changes Fertility in Transgenic Arabidopsis
journal, January 2020


The Sugar-Signaling Hub: Overview of Regulators and Interaction with the Hormonal and Metabolic Network
journal, August 2018

  • Sakr, Soulaiman; Wang, Ming; Dédaldéchamp, Fabienne
  • International Journal of Molecular Sciences, Vol. 19, Issue 9
  • DOI: 10.3390/ijms19092506

Auxin Controlled by Ethylene Steers Root Development
journal, November 2018

  • Qin, Hua; Huang, Rongfeng
  • International Journal of Molecular Sciences, Vol. 19, Issue 11
  • DOI: 10.3390/ijms19113656