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

Dash, Madhumita; Yordanov, Yordan S.; Georgieva, Tatyana; Tschaplinski, Timothy J.; Yordanova, Elena; Busov, Victor

doi:10.1111/tpj.13413

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

Journal Article · 09 February 2017 · The Plant Journal

DOI: https://doi.org/10.1111/tpj.13413 · OSTI ID:1349610

Dash, Madhumita ^[1]; Yordanov, Yordan S. ^[1]; Georgieva, Tatyana ^[1]; Tschaplinski, Timothy J. ^[2]; Yordanova, Elena ^[1]; Busov, Victor ^[1]

Michigan Technological Univ., Houghton, MI (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Bioscience Division

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 in this study, 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 PtabZIP1-like (PtabZIP1L) gene with highest homology to bZIP1 from Arabidopsis. PtabZIP1L is predominantly expressed in roots, particularly in zones where lateral root primordia (LRP) initiate and LR differentiate and emerge. Transgenics overexpressing PtabZIP1L showed precocious LRP and LR development, while PtabZIP1L suppression significantly delayed both LRP and LR formation. Transgenic overexpression and suppression of PtabZIP1L 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 PtabZIP1L mediates LR development and drought resistance through modulation of multiple metabolic pathways.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); US Department of Agriculture (USDA)

Grant/Contract Number:: AC05-00OR22725; SC0008462

OSTI ID:: 1349610

Alternate ID(s):: OSTI ID: 1401028

Journal Information:: The Plant Journal, Journal Name: The Plant Journal Journal Issue: 4 Vol. 89; ISSN 0960-7412

Publisher:: Society for Experimental BiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (90)

Transcription factors that directly regulate the expression of CSLA9 encoding mannan synthase in Arabidopsis thaliana Kim, Won-Chan; Reca, Ida-Barbara; Kim, YongSig Plant Molecular Biology, Vol. 84, Issue 4-5 https://doi.org/10.1007/s11103-013-0154-9	journal	November 2013
Transgenic Populus Trees for Forest Products, Bioenergy, and Functional Genomics Ye, Xia; Busov, Victor; Zhao, Nan Critical Reviews in Plant Sciences, Vol. 30, Issue 5 https://doi.org/10.1080/07352689.2011.605737	journal	September 2011
Genotypic variation in seedling root architectural traits and implications for drought adaptation in wheat (Triticum aestivum L.) Manschadi, Ahmad M.; Hammer, Graeme L.; Christopher, John T. Plant and Soil, Vol. 303, Issue 1-2 https://doi.org/10.1007/s11104-007-9492-1	journal	November 2007
Meta-analysis of constitutive and adaptive QTL for drought tolerance in maize Hao, Zhuanfang; Li, Xinhai; Liu, Xiulin Euphytica, Vol. 174, Issue 2 https://doi.org/10.1007/s10681-009-0091-5	journal	December 2009
Plant Flavonoids—Biosynthesis, Transport and Involvement in Stress Responses Petrussa, Elisa; Braidot, Enrico; Zancani, Marco International Journal of Molecular Sciences, Vol. 14, Issue 7 https://doi.org/10.3390/ijms140714950	journal	July 2013
Total phenolic contents and free radical scavenging activity of certain Egyptian Ficus species leaf samples Abdel-Hameed, El-Sayed Saleh Food Chemistry, Vol. 114, Issue 4 https://doi.org/10.1016/j.foodchem.2008.11.005	journal	June 2009
Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants Park, S.; Li, J.; Pittman, J. K. Proceedings of the National Academy of Sciences, Vol. 102, Issue 52 https://doi.org/10.1073/pnas.0509512102	journal	December 2005
A new mathematical model for relative quantification in real-time RT-PCR Pfaffl, M. W. Nucleic Acids Research, Vol. 29, Issue 9 https://doi.org/10.1093/nar/29.9.e45	journal	May 2001
Water relations and gas exchange of tropical saplings during a prolonged drought in a Bornean heath forest, with reference to root architecture Cao, Kun-fang Journal of Tropical Ecology, Vol. 16, Issue 1 https://doi.org/10.1017/S0266467400001292	journal	January 2000
Breeding for high water-use efficiency Condon, A. G. Journal of Experimental Botany, Vol. 55, Issue 407 https://doi.org/10.1093/jxb/erh277	journal	September 2004
Food and fuel for all: realistic or foolish? G. Cassman, Kenneth; Liska, Adam J. Biofuels, Bioproducts and Biorefining, Vol. 1, Issue 1 https://doi.org/10.1002/bbb.3	journal	January 2007
Overexpression of MIZU-KUSSEI1 Enhances the Root Hydrotropic Response by Retaining Cell Viability Under Hydrostimulated Conditions in Arabidopsis thaliana Miyazawa, Yutaka; Moriwaki, Teppei; Uchida, Mayumi Plant and Cell Physiology, Vol. 53, Issue 11 https://doi.org/10.1093/pcp/pcs129	journal	September 2012
Marker assisted selection in crop plants Francia, E.; Tacconi, G.; Crosatti, C. Plant Cell, Tissue and Organ Culture, Vol. 82, Issue 3 https://doi.org/10.1007/s11240-005-2387-z	journal	September 2005
The role of root architectural traits in adaptation of wheat to water-limited environments Manschadi, Ahmad M.; Christopher, John; deVoil, Peter Functional Plant Biology, Vol. 33, Issue 9 https://doi.org/10.1071/FP06055	journal	January 2006
Rooting depth and water use efficiency of tropical maize inbred lines, differing in drought tolerance Hund, Andreas; Ruta, Nathinee; Liedgens, Markus Plant and Soil, Vol. 318, Issue 1-2 https://doi.org/10.1007/s11104-008-9843-6	journal	December 2008
Hormonal Regulation of Lateral Root Development in Arabidopsis Modulated by MIZ1 and Requirement of GNOM Activity for MIZ1 Function Moriwaki, Teppei; Miyazawa, Yutaka; Kobayashi, Akie Plant Physiology, Vol. 157, Issue 3 https://doi.org/10.1104/pp.111.186270	journal	September 2011
Flavonoids and auxin transport: modulators or regulators? Peer, Wendy Ann; Murphy, Angus S. Trends in Plant Science, Vol. 12, Issue 12 https://doi.org/10.1016/j.tplants.2007.10.003	journal	December 2007
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
Members of the LATERAL ORGAN BOUNDARIES DOMAIN Transcription Factor Family Are Involved in the Regulation of Secondary Growth in Populus Yordanov, Yordan S.; Regan, Sharon; Busov, Victor The Plant Cell, Vol. 22, Issue 11 https://doi.org/10.1105/tpc.110.078634	journal	November 2010
Evaluation of Aluminium Complexation Reaction for Flavonoid Content Assay Pękal, Anna; Pyrzynska, Krystyna Food Analytical Methods, Vol. 7, Issue 9 https://doi.org/10.1007/s12161-014-9814-x	journal	February 2014
Integrated analyses of the transcriptome and small RNA of the hemiparasitic plant Monochasma savatieri before and after establishment of parasite-host association Chen, Lanlan; Guo, Qiaosheng; Zhu, Zaibiao BMC Plant Biology, Vol. 21, Issue 1 https://doi.org/10.1186/s12870-021-02861-6	journal	February 2021
Frenemies: Antagonistic bHLH/bZIP Transcription Factors Integrate Light and Reactive Oxygen Species Signaling in Arabidopsis Lockhart, Jennifer The Plant Cell, Vol. 25, Issue 5 https://doi.org/10.1105/tpc.113.250510	journal	May 2013
Water security for a planet under pressure: interconnected challenges of a changing world call for sustainable solutions Bogardi, Janos J.; Dudgeon, David; Lawford, Richard Current Opinion in Environmental Sustainability, Vol. 4, Issue 1 https://doi.org/10.1016/j.cosust.2011.12.002	journal	February 2012
Nitrogen deprivation promotes Populus root growth through global transcriptome reprogramming and activation of hierarchical genetic networks Wei, Hairong; Yordanov, Yordan S.; Georgieva, Tatyana New Phytologist, Vol. 200, Issue 2 https://doi.org/10.1111/nph.12375	journal	June 2013
Insertional mutagenesis in Populus: relevance and feasibility Busov, Victor; Fladung, Matthias; Groover, Andrew Tree Genetics & Genomes, Vol. 1, Issue 4 https://doi.org/10.1007/s11295-005-0019-8	journal	November 2005
Heterodimers of the Arabidopsis Transcription Factors bZIP1 and bZIP53 Reprogram Amino Acid Metabolism during Low Energy Stress Dietrich, Katrin; Weltmeier, Fridtjof; Ehlert, Andrea The Plant Cell, Vol. 23, Issue 1 https://doi.org/10.1105/tpc.110.075390	journal	January 2011
Analysis of strain and regional variation in gene expression in mouse brain Pavlidis, Paul; Noble, William S. Genome Biology, Vol. 2, Issue 10 https://doi.org/10.1186/gb-2001-2-10-research0042	journal	September 2001
Plant bZIP Protein DNA Binding Specificity Izawa, Takeshi; Foster, Randy; Chua, Nam-Hai Journal of Molecular Biology, Vol. 230, Issue 4 https://doi.org/10.1006/jmbi.1993.1230	journal	April 1993
Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids Nakabayashi, Ryo; Yonekura-Sakakibara, Keiko; Urano, Kaoru The Plant Journal, Vol. 77, Issue 3 https://doi.org/10.1111/tpj.12388	journal	December 2013
More from less: plant growth under limited water Skirycz, Aleksandra; Inzé, Dirk Current Opinion in Biotechnology, Vol. 21, Issue 2 https://doi.org/10.1016/j.copbio.2010.03.002	journal	April 2010
Root traits contributing to plant productivity under drought Comas, Louise H.; Becker, Steven R.; Cruz, Von Mark V. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00442	journal	January 2013
Activation Tagging of a Dominant Gibberellin Catabolism Gene ( GA 2-oxidase ) from Poplar That Regulates Tree Stature Busov, Victor B.; Meilan, Richard; Pearce, David W. Plant Physiology, Vol. 132, Issue 3 https://doi.org/10.1104/pp.103.020354	journal	June 2003
Dro1, a major QTL involved in deep rooting of rice under upland field conditions Uga, Yusaku; Okuno, Kazutoshi; Yano, Masahiro Journal of Experimental Botany, Vol. 62, Issue 8 https://doi.org/10.1093/jxb/erq429	journal	January 2011
Auxin and Ethylene Induce Flavonol Accumulation through Distinct Transcriptional Networks Lewis, Daniel R.; Ramirez, Melissa V.; Miller, Nathan D. Plant Physiology, Vol. 156, Issue 1 https://doi.org/10.1104/pp.111.172502	journal	March 2011
The role of ABF family bZIP class transcription factors in stress response Kim, Soo Young Physiologia Plantarum, Vol. 0, Issue 0 https://doi.org/10.1111/j.1399-3054.2005.00601.x	journal	November 2005
EARLY BUD-BREAK 1 ( EBB1 ) is a regulator of release from seasonal dormancy in poplar trees Yordanov, Yordan S.; Ma, Cathleen; Strauss, Steven H. Proceedings of the National Academy of Sciences, Vol. 111, Issue 27 https://doi.org/10.1073/pnas.1405621111	journal	June 2014
A DNA Transformation–Competent Arabidopsis Genomic Library in Agrobacterium Lazo, Gerard R.; Stein, Pascal A.; Ludwig, Robert A. Bio/Technology, Vol. 9, Issue 10 https://doi.org/10.1038/nbt1091-963	journal	October 1991
Interactions among enzymes of the Arabidopsis flavonoid biosynthetic pathway Burbulis, I. E.; Winkel-Shirley, B. Proceedings of the National Academy of Sciences, Vol. 96, Issue 22 https://doi.org/10.1073/pnas.96.22.12929	journal	October 1999
Activated Expression of an Arabidopsis HD-START Protein Confers Drought Tolerance with Improved Root System and Reduced Stomatal Density Yu, Hong; Chen, Xi; Hong, Yuan-Yuan The Plant Cell, Vol. 20, Issue 4 https://doi.org/10.1105/tpc.108.058263	journal	April 2008
Quantitative Trait Loci and Crop Performance under Abiotic Stress: Where Do We Stand?: Table I. Collins, Nicholas C.; Tardieu, François; Tuberosa, Roberto Plant Physiology, Vol. 147, Issue 2 https://doi.org/10.1104/pp.108.118117	journal	June 2008
Crop responses to drought and the interpretation of adaptation Blum, A. Drought Tolerance in Higher Plants: Genetical, Physiological and Molecular Biological Analysis https://doi.org/10.1007/978-94-017-1299-6_8	book	January 1996
The MYB96 Transcription Factor Mediates Abscisic Acid Signaling during Drought Stress Response in Arabidopsis Seo, Pil Joon; Xiang, Fengning; Qiao, Meng Plant Physiology, Vol. 151, Issue 1 https://doi.org/10.1104/pp.109.144220	journal	July 2009
Effective use of water (EUW) and not water-use efficiency (WUE) is the target of crop yield improvement under drought stress Blum, A. Field Crops Research, Vol. 112, Issue 2-3 https://doi.org/10.1016/j.fcr.2009.03.009	journal	June 2009
Down-regulation of the caffeic acid O-methyltransferase gene in switchgrass reveals a novel monolignol analog Tschaplinski, Timothy J.; Standaert, Robert F.; Engle, Nancy L. Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-71	journal	January 2012
Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on flavonol biosynthesis Grunewald, W.; De Smet, I.; Lewis, D. R. Proceedings of the National Academy of Sciences, Vol. 109, Issue 5 https://doi.org/10.1073/pnas.1121134109	journal	January 2012
Flavonoid Accumulation Patterns of Transparent Testa Mutants of Arabidopsis Peer, Wendy Ann; Brown, Dana E.; Tague, Brian W. Plant Physiology, Vol. 126, Issue 2 https://doi.org/10.1104/pp.126.2.536	journal	June 2001
Evidence of oxidative attenuation of auxin signalling Peer, Wendy Ann; Cheng, Yan; Murphy, Angus S. Journal of Experimental Botany, Vol. 64, Issue 9 https://doi.org/10.1093/jxb/ert152	journal	May 2013
Arabidopsis H+-PPase AVP1 Regulates Auxin-Mediated Organ Development Li, J. Science, Vol. 310, Issue 5745 https://doi.org/10.1126/science.1115711	journal	October 2005
Soil structure and the effect of management practices Pagliai, M.; Vignozzi, N.; Pellegrini, S. Soil and Tillage Research, Vol. 79, Issue 2 https://doi.org/10.1016/j.still.2004.07.002	journal	December 2004
MetaboAnalyst 3.0—making metabolomics more meaningful Xia, Jianguo; Sinelnikov, Igor V.; Han, Beomsoo Nucleic Acids Research, Vol. 43, Issue W1 https://doi.org/10.1093/nar/gkv380	journal	April 2015
GATEWAY™ vectors for Agrobacterium-mediated plant transformation Karimi, Mansour; Inzé, Dirk; Depicker, Ann Trends in Plant Science, Vol. 7, Issue 5, p. 193-195 https://doi.org/10.1016/S1360-1385(02)02251-3	journal	May 2002
Stress-Induced Phenylpropanoid Metabolism. Dixon, R. A.; Paiva, N. L. The Plant Cell https://doi.org/10.1105/tpc.7.7.1085	journal	July 1995
Crop responses to drought and the interpretation of adaptation Blum, A. Plant Growth Regulation, Vol. 20, Issue 2 https://doi.org/10.1007/BF00024010	journal	November 1996
Modeling the global effect of the basic-leucine zipper transcription factor 1 (bZIP1) on nitrogen and light regulation in Arabidopsis Obertello, Mariana; Krouk, Gabriel; Katari, Manpreet S. BMC Systems Biology, Vol. 4, Issue 1 https://doi.org/10.1186/1752-0509-4-111	journal	January 2010
Genetic variability of drought-avoidance root traits in the mini-core germplasm collection of chickpea (Cicer arietinum L.). Kashiwagi, Junichi; Krishnamurthy, L.; Upadhyaya, Hari D. Euphytica, Vol. 146, Issue 3 https://doi.org/10.1007/s10681-005-9007-1	journal	February 2006
Variation in root system architecture and drought response in rice (Oryza sativa): Phenotyping of the OryzaSNP panel in rainfed lowland fields Henry, Amelia; Gowda, Veeresh R. P.; Torres, Rolando O. Field Crops Research, Vol. 120, Issue 2 https://doi.org/10.1016/j.fcr.2010.10.003	journal	January 2011
Quantitative trait loci influencing drought tolerance in grain sorghum (Sorghum bicolor L. Moench) Kebede, H.; Subudhi, P. K.; Rosenow, D. T. Theoretical and Applied Genetics, Vol. 103, Issue 2-3 https://doi.org/10.1007/s001220100541	journal	August 2001
Genetic control of root development in rice, the model cereal Coudert, Yoan; Périn, Christophe; Courtois, Brigitte Trends in Plant Science, Vol. 15, Issue 4 https://doi.org/10.1016/j.tplants.2010.01.008	journal	April 2010
Role of proline under changing environments: A review Hayat, Shamsul; Hayat, Qaiser; Alyemeni, Mohammed Nasser Plant Signaling & Behavior, Vol. 7, Issue 11 https://doi.org/10.4161/psb.21949	journal	November 2012
bZIP transcription factors in Arabidopsis Jakoby, Marc; Weisshaar, Bernd; Dröge-Laser, Wolfgang Trends in Plant Science, Vol. 7, Issue 3 https://doi.org/10.1016/S1360-1385(01)02223-3	journal	March 2002
An Agrobacterium tumefaciens transformation protocol effective on a variety of cottonwood hybrids (genus Populus) Han, K.-H.; Meilan, R.; Ma, C. Plant Cell Reports, Vol. 19, Issue 3, p. 315-320 https://doi.org/10.1007/s002990050019	journal	January 2000
Sustainable bioenergy production from marginal lands in the US Midwest Gelfand, Ilya; Sahajpal, Ritvik; Zhang, Xuesong Nature, Vol. 493, Issue 7433 https://doi.org/10.1038/nature11811	journal	January 2013
The Arabidopsis AtbZIP1 transcription factor is a positive regulator of plant tolerance to salt, osmotic and drought stresses Sun, Xiaoli; Li, Yong; Cai, Hua Journal of Plant Research, Vol. 125, Issue 3 https://doi.org/10.1007/s10265-011-0448-4	journal	September 2011
GASA14 regulates leaf expansion and abiotic stress resistance by modulating reactive oxygen species accumulation Sun, Shulan; Wang, Haoxiang; Yu, Hongmei Journal of Experimental Botany, Vol. 64, Issue 6 https://doi.org/10.1093/jxb/ert021	journal	February 2013
Kaempferol 3- O -rhamnoside-7- O -rhamnoside is an endogenous flavonol inhibitor of polar auxin transport in Arabidopsis shoots Yin, Ruohe; Han, Kerstin; Heller, Werner New Phytologist, Vol. 201, Issue 2 https://doi.org/10.1111/nph.12558	journal	October 2013
Transfection and transformation of Agrobacterium tumefaciens Holsters, M.; de Waele, D.; Depicker, A. Molecular and General Genetics MGG, Vol. 163, Issue 2 https://doi.org/10.1007/BF00267408	journal	January 1978
Saturation mapping of QTL regions and identification of putative candidate genes for drought tolerance in rice Nguyen, T. T. T.; Klueva, N.; Chamareck, V. Molecular Genetics and Genomics, Vol. 272, Issue 1 https://doi.org/10.1007/s00438-004-1025-5	journal	June 2004
Flavonoids as Important Molecules of Plant Interactions with the Environment Mierziak, Justyna; Kostyn, Kamil; Kulma, Anna Molecules, Vol. 19, Issue 10 https://doi.org/10.3390/molecules191016240	journal	October 2014
Transgenics are imperative for biofuel crops Gressel, Jonathan Plant Science, Vol. 174, Issue 3 https://doi.org/10.1016/j.plantsci.2007.11.009	journal	March 2008
Stress-Induced Phenylpropanoid Metabolism Dixon, Richard A.; Paiva, Nancy L. The Plant Cell, Vol. 7, Issue 7 https://doi.org/10.2307/3870059	journal	July 1995
A systems biology approach identifies new regulators of poplar root development under low nitrogen Dash, Madhumita; Yordanov, Yordan S.; Georgieva, Tatyana The Plant Journal, Vol. 84, Issue 2 https://doi.org/10.1111/tpj.13002	journal	October 2015
Multiple functional roles of flavonoids in photoprotection: Letters Agati, Giovanni; Tattini, Massimiliano New Phytologist, Vol. 186, Issue 4 https://doi.org/10.1111/j.1469-8137.2010.03269.x	journal	May 2010
Investigating the drought-stress response of hybrid poplar genotypes by metabolite profiling Barchet, G. L. H.; Dauwe, R.; Guy, R. D. Tree Physiology, Vol. 34, Issue 11 https://doi.org/10.1093/treephys/tpt080	journal	October 2013
Functional Analysis of a Predicted Flavonol Synthase Gene Family in Arabidopsis Owens, Daniel K.; Alerding, Anne B.; Crosby, Kevin C. Plant Physiology, Vol. 147, Issue 3 https://doi.org/10.1104/pp.108.117457	journal	May 2008
Activation tagging is an effective gene tagging system in Populus Busov, Victor; Yordanov, Yordan; Gou, Jiqing Tree Genetics & Genomes, Vol. 7, Issue 1 https://doi.org/10.1007/s11295-010-0317-7	journal	July 2010
The anthocyanin reduced Tomato Mutant Demonstrates the Role of Flavonols in Tomato Lateral Root and Root Hair Development Maloney, G. S.; DiNapoli, K. T.; Muday, G. K. PLANT PHYSIOLOGY, Vol. 166, Issue 2 https://doi.org/10.1104/pp.114.240507	journal	July 2014
Alteration of flavonoid accumulation patterns in transparent testa mutants disturbs auxin transport, gravity responses, and imparts long-term effects on root and shoot architecture Buer, Charles S.; Kordbacheh, Farzanah; Truong, Thy T. Planta, Vol. 238, Issue 1 https://doi.org/10.1007/s00425-013-1883-3	journal	April 2013
Rooting depth and water use efficiency of tropical maize inbred lines, differing in drought tolerance Andreas, Hund,; Nathinee, Ruta,; Markus, Liedgens, ETH Zurich https://doi.org/10.3929/ethz-b-000021385	text	January 2009
The Arabidopsis bZIP1 Transcription Factor Is Involved in Sugar Signaling, Protein Networking, and DNA Binding Kang, Shin Gene; Price, John; Lin, Pei-Chi Molecular Plant, Vol. 3, Issue 2 https://doi.org/10.1093/mp/ssp115	journal	March 2010
Constraints and potentials of future irrigation water availability on agricultural production under climate change Elliott, Joshua; Deryng, Delphine; Müller, Christoph Proceedings of the National Academy of Sciences, Vol. 111, Issue 9 https://doi.org/10.1073/pnas.1222474110	journal	December 2013
Regulation of auxin transport by aminopeptidases and endogenous flavonoids Murphy, Angus; Peer, Wendy Ann; Taiz, Lincoln Planta, Vol. 211, Issue 3 https://doi.org/10.1007/s004250000300	journal	August 2000
MIZ1-regulated hydrotropism functions in the growth and survival of Arabidopsis thaliana under natural conditions Iwata, Satoru; Miyazawa, Yutaka; Fujii, Nobuharu Annals of Botany, Vol. 112, Issue 1 https://doi.org/10.1093/aob/mct098	journal	May 2013
Flavonoid oxidation in plants: from biochemical properties to physiological functions Pourcel, L.; Routaboul, J.; Cheynier, V. Trends in Plant Science, Vol. 12, Issue 1 https://doi.org/10.1016/j.tplants.2006.11.006	journal	January 2007
Hit-and-run transcriptional control by bZIP1 mediates rapid nutrient signaling in Arabidopsis Para, A.; Li, Y.; Marshall-Colon, A. Proceedings of the National Academy of Sciences, Vol. 111, Issue 28 https://doi.org/10.1073/pnas.1404657111	journal	June 2014
Identification, characterization of an AP2/ERF transcription factor that promotes adventitious, lateral root formation in Populus Trupiano, Dalila; Yordanov, Yordan; Regan, Sharon Planta, Vol. 238, Issue 2 https://doi.org/10.1007/s00425-013-1890-4	journal	May 2013
Flavonoids Act as Negative Regulators of Auxin Transport in Vivo in Arabidopsis Brown, Dana E.; Rashotte, Aaron M.; Murphy, Angus S. Plant Physiology, Vol. 126, Issue 2 https://doi.org/10.1104/pp.126.2.524	journal	June 2001
Root system architecture: opportunities and constraints for genetic improvement of crops de Dorlodot, Sophie; Forster, Brian; Pagès, Loïc Trends in Plant Science, Vol. 12, Issue 10 https://doi.org/10.1016/j.tplants.2007.08.012	journal	October 2007
Plant bZIP Transcription Factors Responsive to Pathogens: A Review Alves, Murilo; Dadalto, Silvana; Gonçalves, Amanda International Journal of Molecular Sciences, Vol. 14, Issue 4 https://doi.org/10.3390/ijms14047815	journal	April 2013
Soil salinity related to physical soil characteristics and irrigation management in four Mediterranean irrigation districts Aragüés, R.; Urdanoz, V.; Çetin, M. Agricultural Water Management, Vol. 98, Issue 6 https://doi.org/10.1016/j.agwat.2011.01.004	journal	April 2011
Plants with genetically encoded autoluminescence Mitiouchkina, Tatiana; Mishin, Alexander S.; Somermeyer, Louisa Gonzalez Nature Biotechnology, Vol. 38, Issue 8 https://doi.org/10.1038/s41587-020-0500-9	journal	April 2020

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Auxin Controlled by Ethylene Steers Root Development Qin, Hua; Huang, Rongfeng International Journal of Molecular Sciences, Vol. 19, Issue 11 https://doi.org/10.3390/ijms19113656	journal	November 2018
GmWRKY45 Enhances Tolerance to Phosphate Starvation and Salt Stress, and Changes Fertility in Transgenic Arabidopsis Li, Cheng; Liu, Xinyi; Ruan, Hui Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01714	journal	January 2020
A unique bZIP transcription factor imparting multiple stress tolerance in Rice Das, Priyanka; Lakra, Nita; Nutan, Kamlesh Kant Rice, Vol. 12, Issue 1 https://doi.org/10.1186/s12284-019-0316-8	journal	August 2019
Gene network analysis of poplar root transcriptome in response to drought stress identifies a PtaJAZ3PtaRAP2.6-centered hierarchical network Dash, Madhumita; Yordanov, Yordan S.; Georgieva, Tatyana PLOS ONE, Vol. 13, Issue 12 https://doi.org/10.1371/journal.pone.0208560	journal	December 2018

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

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