Spatiotemporal analysis identifies ABF2 and ABF3 as key hubs of endodermal response to nitrate

Contreras-López, Orlando; Vidal, Elena A.; Riveras, Eleodoro; Alvarez, José M.; Moyano, Tomás C.; Sparks, Erin E.; Medina, Joaquín; Pasquino, Angelo; Benfey, Philip N.; Coruzzi, Gloria M.; Gutiérrez, Rodrigo A.

doi:10.1073/pnas.2107879119

Title: Spatiotemporal analysis identifies ABF2 and ABF3 as key hubs of endodermal response to nitrate

Journal Article · 18 January 2022 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.2107879119 · OSTI ID:2480611

^[1];

^[2];

^[3]; Alvarez, José M. ^[2]; Moyano, Tomás C. ^[3];

^[4];

^[5];

^[6];

^[7];

^[6];

^[3]

Fondo de Desarrollo de Areas Prioritarias, Santiago (Chile); Pontificia Universidad Católica de Chile, Santiago (Chile)
Millennium Institute for Integrative Biology, Santiago (Chile); Universidad Mayor, Santiago (Chile)
Fondo de Desarrollo de Areas Prioritarias, Santiago (Chile); Pontificia Universidad Católica de Chile, Santiago (Chile); Millennium Institute for Integrative Biology, Santiago (Chile)
University of Delaware, Newark, DE (United States)
Universidad Politécnica de Madrid (Spain)
New York University (NYU), NY (United States)
Duke University, Durham, NC (United States)

Nitrate is a nutrient and a potent signal that impacts global gene expression in plants. However, the regulatory factors controlling temporal and cell type–specific nitrate responses remain largely unknown. We assayed nitrate-responsive transcriptome changes in five major root cell types of the Arabidopsis thaliana root as a function of time. We found that gene-expression response to nitrate is dynamic and highly localized and predicted cell type–specific transcription factor (TF)–target interactions. Among cell types, the endodermis stands out as having the largest and most connected nitrate-regulatory gene network. ABF2 and ABF3 are major hubs for transcriptional responses in the endodermis cell layer. We experimentally validated TF–target interactions for ABF2 and ABF3 by chromatin immunoprecipitation followed by sequencing and a cell-based system to detect TF regulation genome-wide. Validated targets of ABF2 and ABF3 account for more than 50% of the nitrate-responsive transcriptome in the endodermis. Moreover, ABF2 and ABF3 are involved in nitrate-induced lateral root growth. Our approach offers an unprecedented spatiotemporal resolution of the root response to nitrate and identifies important components of cell-specific gene regulatory networks.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: New York University (NYU), NY (United States)

Sponsoring Organization:: ANID Fondo de Desarrollo de Areas Prioritarias; ANID–Millennium Science Initiative Program; Agencia Nacional de Investigación y Desarrollo (ANID) National Fund for Scientific and Technological Development; Comisión Nacional de Investigación Científica y Tecnológica (CONICYT)-MPG; HHMI and NIH Maximizing Investigator’s Research; NIH National Institute of General Medical Sciences; National Institute for Agriculture and Food Research and Technology; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0014377

OSTI ID:: 2480611

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 4 Vol. 119; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (81)

Root Endodermis and Exodermis: Structure, Function, and Responses to the Environment Enstone, Daryl E.; Peterson, Carol A.; Ma, Fengshan Journal of Plant Growth Regulation, Vol. 21, Issue 4 https://doi.org/10.1007/s00344-003-0002-2	journal	December 2002
The herbicide sensitivity gene CHL1 of arabidopsis encodes a nitrate-inducible nitrate transporter Tsay, Y. Cell, Vol. 72, Issue 5 https://doi.org/10.1016/0092-8674(93)90399-B	journal	March 1993
The SHORT-ROOT Gene Controls Radial Patterning of the Arabidopsis Root through Radial Signaling Helariutta, Yrjo; Fukaki, Hidehiro; Wysocka-Diller, Joanna Cell, Vol. 101, Issue 5 https://doi.org/10.1016/S0092-8674(00)80865-X	journal	May 2000
WEREWOLF, a MYB-Related Protein in Arabidopsis, Is a Position-Dependent Regulator of Epidermal Cell Patterning Lee, Myeong Min; Schiefelbein, John Cell, Vol. 99, Issue 5 https://doi.org/10.1016/S0092-8674(00)81536-6	journal	November 1999
CHL1 Functions as a Nitrate Sensor in Plants Ho, Cheng-Hsun; Lin, Shan-Hua; Hu, Heng-Cheng Cell, Vol. 138, Issue 6 https://doi.org/10.1016/j.cell.2009.07.004	journal	September 2009
Circuitry and Dynamics of Human Transcription Factor Regulatory Networks Neph, Shane; Stergachis, Andrew B.; Reynolds, Alex Cell, Vol. 150, Issue 6 https://doi.org/10.1016/j.cell.2012.04.040	journal	September 2012
Determination and Inference of Eukaryotic Transcription Factor Sequence Specificity Weirauch, Matthew T.; Yang, Ally; Albu, Mihai Cell, Vol. 158, Issue 6 https://doi.org/10.1016/j.cell.2014.08.009	journal	September 2014
Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape O’Malley, Ronan C.; Huang, Shao-shan Carol; Song, Liang Cell, Vol. 165, Issue 5 https://doi.org/10.1016/j.cell.2016.04.038	journal	May 2016
High-Throughput Single-Cell Transcriptome Profiling of Plant Cell Types Shulse, Christine N.; Cole, Benjamin J.; Ciobanu, Doina Cell Reports, Vol. 27, Issue 7 https://doi.org/10.1016/j.celrep.2019.04.054	journal	May 2019
Cell Identity Regulators Link Development and Stress Responses in the Arabidopsis Root Iyer-Pascuzzi, Anjali S.; Jackson, Terry; Cui, Hongchang Developmental Cell, Vol. 21, Issue 4 https://doi.org/10.1016/j.devcel.2011.09.009	journal	October 2011
Local Changes in Chromatin Accessibility and Transcriptional Networks Underlying the Nitrate Response in Arabidopsis Roots Alvarez, José M.; Moyano, Tomás C.; Zhang, Tao Molecular Plant, Vol. 12, Issue 12 https://doi.org/10.1016/j.molp.2019.09.002	journal	December 2019
A gateway with a guard: How the endodermis regulates growth through hormone signaling Dinneny, José R. Plant Science, Vol. 214 https://doi.org/10.1016/j.plantsci.2013.09.009	journal	January 2014
Auxin reflux between the endodermis and pericycle promotes lateral root initiation Marhavý, Peter; Vanstraelen, Marleen; De Rybel, Bert The EMBO Journal, Vol. 32, Issue 1 https://doi.org/10.1038/emboj.2012.303	journal	November 2012
A map of cell type‐specific auxin responses Bargmann, Bastiaan O. R.; Vanneste, Steffen; Krouk, Gabriel Molecular Systems Biology, Vol. 9, Issue 1 https://doi.org/10.1038/msb.2013.40	journal	January 2013
Discovery of nitrate–CPK–NLP signalling in central nutrient–growth networks Liu, Kun-hsiang; Niu, Yajie; Konishi, Mineko Nature, Vol. 545, Issue 7654 https://doi.org/10.1038/nature22077	journal	May 2017
Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants Marchive, Chloé; Roudier, François; Castaings, Loren Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms2650	journal	April 2013
AtNIGT1/HRS1 integrates nitrate and phosphate signals at the Arabidopsis root tip Medici, Anna; Marshall-Colon, Amy; Ronzier, Elsa Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7274	journal	February 2015
Enhanced Y1H assays for Arabidopsis Gaudinier, Allison; Zhang, Lifang; Reece-Hoyes, John S. Nature Methods, Vol. 8, Issue 12 https://doi.org/10.1038/nmeth.1750	journal	October 2011
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
Network Walking charts transcriptional dynamics of nitrogen signaling by integrating validated and predicted genome-wide interactions Brooks, Matthew D.; Cirrone, Jacopo; Pasquino, Angelo V. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-09522-1	journal	April 2019
Transient genome-wide interactions of the master transcription factor NLP7 initiate a rapid nitrogen-response cascade Alvarez, José M.; Schinke, Anna-Lena; Brooks, Matthew D. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14979-6	journal	March 2020
Transcriptional regulation of nitrogen-associated metabolism and growth Gaudinier, Allison; Rodriguez-Medina, Joel; Zhang, Lifang Nature, Vol. 563, Issue 7730 https://doi.org/10.1038/s41586-018-0656-3	journal	October 2018
ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis Signora, Laurent; De Smet, Ive; Foyer, Christine H. The Plant Journal, Vol. 28, Issue 6 https://doi.org/10.1046/j.1365-313x.2001.01185.x	journal	December 2001
Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots Lee, J. -Y.; Colinas, J.; Wang, J. Y. Proceedings of the National Academy of Sciences, Vol. 103, Issue 15 https://doi.org/10.1073/pnas.0510607103	journal	March 2006
Cell-specific nitrogen responses mediate developmental plasticity Gifford, M. L.; Dean, A.; Gutierrez, R. A. Proceedings of the National Academy of Sciences, Vol. 105, Issue 2 https://doi.org/10.1073/pnas.0709559105	journal	January 2008
Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana Vidal, E. A.; Araus, V.; Lu, C. Proceedings of the National Academy of Sciences, Vol. 107, Issue 9 https://doi.org/10.1073/pnas.0909571107	journal	February 2010
Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots Vidal, E. A.; Moyano, T. C.; Riveras, E. Proceedings of the National Academy of Sciences, Vol. 110, Issue 31 https://doi.org/10.1073/pnas.1310937110	journal	July 2013
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
Interacting TCP and NLP transcription factors control plant responses to nitrate availability Guan, Peizhu; Ripoll, Juan-José; Wang, Renhou Proceedings of the National Academy of Sciences, Vol. 114, Issue 9 https://doi.org/10.1073/pnas.1615676114	journal	February 2017
Temporal transcriptional logic of dynamic regulatory networks underlying nitrogen signaling and use in plants Varala, Kranthi; Marshall-Colón, Amy; Cirrone, Jacopo Proceedings of the National Academy of Sciences, Vol. 115, Issue 25 https://doi.org/10.1073/pnas.1721487115	journal	May 2018
Nutrient dose-responsive transcriptome changes driven by Michaelis–Menten kinetics underlie plant growth rates Swift, Joseph; Alvarez, Jose M.; Araus, Viviana Proceedings of the National Academy of Sciences, Vol. 117, Issue 23 https://doi.org/10.1073/pnas.1918619117	journal	May 2020
Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture Masclaux-Daubresse, Céline; Daniel-Vedele, Françoise; Dechorgnat, Julie Annals of Botany, Vol. 105, Issue 7 https://doi.org/10.1093/aob/mcq028	journal	March 2010
Using GOstats to test gene lists for GO term association Falcon, S.; Gentleman, R. Bioinformatics, Vol. 23, Issue 2 https://doi.org/10.1093/bioinformatics/btl567	journal	November 2006
TopHat: discovering splice junctions with RNA-Seq Trapnell, Cole; Pachter, Lior; Salzberg, Steven L. Bioinformatics, Vol. 25, Issue 9 https://doi.org/10.1093/bioinformatics/btp120	journal	March 2009
Precrec: fast and accurate precision–recall and ROC curve calculations in R Saito, Takaya; Rehmsmeier, Marc Bioinformatics, Vol. 33, Issue 1 https://doi.org/10.1093/bioinformatics/btw570	journal	September 2016
Exploration, normalization, and summaries of high density oligonucleotide array probe level data Irizarry, Rafael A.; Hobbs, Bridget; Collin, Francois Biostatistics, Vol. 4, Issue 2, p. 249-264 https://doi.org/10.1093/biostatistics/4.2.249	journal	April 2003
A balancing act: how plants integrate nitrogen and water signals Araus, Viviana; Swift, Joseph; Alvarez, Jose M. Journal of Experimental Botany, Vol. 71, Issue 15 https://doi.org/10.1093/jxb/eraa054	journal	January 2020
Insights into the genomic nitrate response using genetics and the Sungear Software System Gutierrez, R. A.; Gifford, M. L.; Poultney, C. Journal of Experimental Botany, Vol. 58, Issue 9 https://doi.org/10.1093/jxb/erm079	journal	March 2007
The Primary Nitrate Response: a multifaceted signalling pathway Medici, Anna; Krouk, Gabriel Journal of Experimental Botany, Vol. 65, Issue 19 https://doi.org/10.1093/jxb/eru245	journal	June 2014
Nitrate regulation of lateral root and root hair development in plants Liu, Bohan; Wu, Junyu; Yang, Shuaiqi Journal of Experimental Botany, Vol. 71, Issue 15 https://doi.org/10.1093/jxb/erz536	journal	December 2019
TARGET: A Transient Transformation System for Genome-Wide Transcription Factor Target Discovery Bargmann, Bastiaan O. R.; Marshall-Colon, Amy; Efroni, Idan Molecular Plant, Vol. 6, Issue 3 https://doi.org/10.1093/mp/sst010	journal	May 2013
Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data Ruijter, J. M.; Ramakers, C.; Hoogaars, W. M. H. Nucleic Acids Research, Vol. 37, Issue 6 https://doi.org/10.1093/nar/gkp045	journal	February 2009
AGRIS: the Arabidopsis Gene Regulatory Information Server, an update Yilmaz, A.; Mejia-Guerra, M. K.; Kurz, K. Nucleic Acids Research, Vol. 39, Issue Database https://doi.org/10.1093/nar/gkq1120	journal	November 2010
SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem Sabatini, S. Genes & Development, Vol. 17, Issue 3 https://doi.org/10.1101/gad.252503	journal	February 2003
Targeted cell elimination reveals an auxin-guided biphasic mode of lateral root initiation Marhavý, Peter; Montesinos, Juan Carlos; Abuzeineh, Anas Genes & Development, Vol. 30, Issue 4 https://doi.org/10.1101/gad.276964.115	journal	February 2016
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Genomic Analysis of the Nitrate Response Using a Nitrate Reductase-Null Mutant of Arabidopsis Wang, Rongchen; Tischner, Rudolf; Gutiérrez, Rodrigo A. Plant Physiology, Vol. 136, Issue 1 https://doi.org/10.1104/pp.104.044610	journal	August 2004
Genome-Wide Identification and Testing of Superior Reference Genes for Transcript Normalization in Arabidopsis Czechowski, Tomasz; Stitt, Mark; Altmann, Thomas Plant Physiology, Vol. 139, Issue 1 https://doi.org/10.1104/pp.105.063743	journal	September 2005
Genetic Interactions of TGA Transcription Factors in the Regulation of Pathogenesis-Related Genes and Disease Resistance in Arabidopsis Kesarwani, Meenu; Yoo, Jungmin; Dong, Xinnian Plant Physiology, Vol. 144, Issue 1 https://doi.org/10.1104/pp.106.095299	journal	March 2007
Large Cellular Inclusions Accumulate in Arabidopsis Roots Exposed to Low-Sulfur Conditions Jackson, Terry L.; Baker, Ginger W.; Wilks, Floyd R. Plant Physiology, Vol. 168, Issue 4 https://doi.org/10.1104/pp.15.00465	journal	June 2015
AREB1 Is a Transcription Activator of Novel ABRE-Dependent ABA Signaling That Enhances Drought Stress Tolerance in Arabidopsis Fujita, Yasunari; Fujita, Miki; Satoh, Rie The Plant Cell, Vol. 17, Issue 12 https://doi.org/10.1105/tpc.105.035659	journal	November 2005
An Auxin Gradient and Maximum in the Arabidopsis Root Apex Shown by High-Resolution Cell-Specific Analysis of IAA Distribution and Synthesis Petersson, Sara V.; Johansson, Annika I.; Kowalczyk, Mariusz The Plant Cell, Vol. 21, Issue 6 https://doi.org/10.1105/tpc.109.066480	journal	June 2009
Members of the LBD Family of Transcription Factors Repress Anthocyanin Synthesis and Affect Additional Nitrogen Responses in Arabidopsis Rubin, Grit; Tohge, Takayuki; Matsuda, Fumio The Plant Cell, Vol. 21, Issue 11 https://doi.org/10.1105/tpc.109.067041	journal	November 2009
Arabidopsis PYR/PYL/RCAR Receptors Play a Major Role in Quantitative Regulation of Stomatal Aperture and Transcriptional Response to Abscisic Acid Gonzalez-Guzman, Miguel; Pizzio, Gaston A.; Antoni, Regina The Plant Cell, Vol. 24, Issue 6 https://doi.org/10.1105/tpc.112.098574	journal	June 2012
Endodermal ABA Signaling Promotes Lateral Root Quiescence during Salt Stress in Arabidopsis Seedlings Duan, Lina; Dietrich, Daniela; Ng, Chong Han The Plant Cell, Vol. 25, Issue 1 https://doi.org/10.1105/tpc.112.107227	journal	January 2013
A Spatio-Temporal Understanding of Growth Regulation during the Salt Stress Response in Arabidopsis Geng, Y.; Wu, R.; Wee, C. W. The Plant Cell, Vol. 25, Issue 6 https://doi.org/10.1105/tpc.113.112896	journal	June 2013
Cell-Type-Specific Cytokinin Distribution within the Arabidopsis Primary Root Apex Antoniadi, Ioanna; Plačková, Lenka; Simonovik, Biljana The Plant Cell, Vol. 27, Issue 7 https://doi.org/10.1105/tpc.15.00176	journal	July 2015
Environmental Nitrate Stimulates Abscisic Acid Accumulation in Arabidopsis Root Tips by Releasing It from Inactive Stores Ondzighi-Assoume, Christine A.; Chakraborty, Sanhita; Harris, Jeanne M. The Plant Cell, Vol. 28, Issue 3 https://doi.org/10.1105/tpc.15.00946	journal	February 2016
Changes in Gene Expression in Space and Time Orchestrate Environmentally Mediated Shaping of Root Architecture Walker, Liam; Boddington, Clare; Jenkins, Dafyd The Plant Cell, Vol. 29, Issue 10 https://doi.org/10.1105/tpc.16.00961	journal	September 2017
Nitrate in 2020: Thirty Years from Transport to Signaling Networks Vidal, Elena A.; Alvarez, José M.; Araus, Viviana The Plant Cell, Vol. 32, Issue 7 https://doi.org/10.1105/tpc.19.00748	journal	March 2020
ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance Kim, Sunmi; Kang, Jung-youn; Cho, Dong-Im The Plant Journal, Vol. 40, Issue 1 https://doi.org/10.1111/j.1365-313X.2004.02192.x	journal	August 2004
AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation Yoshida, Takuya; Fujita, Yasunari; Sayama, Hiroko The Plant Journal, Vol. 61, Issue 4 https://doi.org/10.1111/j.1365-313X.2009.04092.x	journal	February 2010
NRT2.1 C‐terminus phosphorylation prevents root high affinity nitrate uptake activity in Arabidopsis thaliana Jacquot, Aurore; Chaput, Valentin; Mauries, Adeline New Phytologist, Vol. 228, Issue 3 https://doi.org/10.1111/nph.16710	journal	September 2020
Systems approach identifies TGA1 and TGA4 transcription factors as important regulatory components of the nitrate response of Arabidopsis thaliana roots Alvarez, José M.; Riveras, Eleodoro; Vidal, Elena A. The Plant Journal, Vol. 80, Issue 1 https://doi.org/10.1111/tpj.12618	journal	August 2014
Nitrate induction of root hair density is mediated by TGA1/TGA4 and CPC transcription factors in Arabidopsis thaliana Canales, Javier; Contreras-López, Orlando; Álvarez, José M. The Plant Journal, Vol. 92, Issue 2 https://doi.org/10.1111/tpj.13656	journal	August 2017
A Gene Expression Map of the Arabidopsis Root Birnbaum, K. Science, Vol. 302, Issue 5652 https://doi.org/10.1126/science.1090022	journal	December 2003
A High-Resolution Root Spatiotemporal Map Reveals Dominant Expression Patterns Brady, S. M.; Orlando, D. A.; Lee, J. -Y. Science, Vol. 318, Issue 5851 https://doi.org/10.1126/science.1146265	journal	November 2007
Cell Identity Mediates the Response of Arabidopsis Roots to Abiotic Stress Dinneny, J. R.; Long, T. A.; Wang, J. Y. Science, Vol. 320, Issue 5878 https://doi.org/10.1126/science.1153795	journal	May 2008
AGRIS: Arabidopsis Gene Regulatory Information Server, an information resource of Arabidopsis cis-regulatory elements and transcription factors Davuluri, Ramana V.; Sun, Hao; Palaniswamy, Saranyan K. BMC Bioinformatics, Vol. 4, Issue 1 https://doi.org/10.1186/1471-2105-4-25	journal	June 2003
A system biology approach highlights a hormonal enhancer effect on regulation of genes in a nitrate responsive "biomodule" Nero, Damion; Krouk, Gabriel; Tranchina, Daniel BMC Systems Biology, Vol. 3, Issue 1 https://doi.org/10.1186/1752-0509-3-59	journal	January 2009
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
Qualitative network models and genome-wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis Gutiérrez, Rodrigo A.; Lejay, Laurence V.; Dean, Alexis Genome Biology, Vol. 8, Issue 1 https://doi.org/10.1186/gb-2007-8-1-r7	journal	January 2007
Predictive network modeling of the high-resolution dynamic plant transcriptome in response to nitrate Krouk, Gabriel; Mirowski, Piotr; LeCun, Yann Genome Biology, Vol. 11, Issue 12 https://doi.org/10.1186/gb-2010-11-12-r123	journal	January 2010
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
Regulation of ABI5 expression by ABF3 during salt stress responses in Arabidopsis thaliana Chang, Hui-Chun; Tsai, Min-Chieh; Wu, Sih-Sian Botanical Studies, Vol. 60, Issue 1 https://doi.org/10.1186/s40529-019-0264-z	journal	August 2019
Organization and cell differentiation in lateral roots of Arabidopsis thaliana Malamy, J. E.; Benfey, P. N. Development, Vol. 124, Issue 1 https://doi.org/10.1242/dev.124.1.33	journal	January 1997
Root Suberin Forms an Extracellular Barrier That Affects Water Relations and Mineral Nutrition in Arabidopsis Baxter, Ivan; Hosmani, Prashant S.; Rus, Ana PLoS Genetics, Vol. 5, Issue 5 https://doi.org/10.1371/journal.pgen.1000492	journal	May 2009
The Arabidopsis ABA-Activated Kinase OST1 Phosphorylates the bZIP Transcription Factor ABF3 and Creates a 14-3-3 Binding Site Involved in Its Turnover Sirichandra, Caroline; Davanture, Marlène; Turk, Benjamin E. PLoS ONE, Vol. 5, Issue 11 https://doi.org/10.1371/journal.pone.0013935	journal	November 2010
Systems analysis of transcriptome data provides new hypotheses about Arabidopsis root response to nitrate treatments Canales, Javier; Moyano, Tomás C.; Villarroel, Eva Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00022	journal	January 2014
Nitrate: A Crucial Signal during Lateral Roots Development Sun, Cui-Hui; Yu, Jian-Qiang; Hu, Da-Gang Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00485	journal	April 2017
Nitrate Signaling, Functions, and Regulation of Root System Architecture: Insights from Arabidopsis thaliana Asim, Muhammad; Ullah, Zia; Xu, Fangzheng Genes, Vol. 11, Issue 6 https://doi.org/10.3390/genes11060633	journal	June 2020

Similar Records

A suberized exodermis is required for tomato drought tolerance

Journal Article · 2024 · Nature Plants (Online) · OSTI ID:2282166

Cantó-Pastor, Alex; Kajala, Kaisa; Shaar-Moshe, Lidor; +21 more

A tissue‐resolved, network‐based transcriptomic framework for abiotic stress responses in sorghum

Journal Article · 2026 · The Plant Journal · OSTI ID:3024993

Ko, Dae Kwan; Brandizzi, Federica

Temporal change in chromatin accessibility predicts regulators of nodulation in Medicago truncatula

Journal Article · 2022 · BMC Biology · OSTI ID:1975673

Knaack, Sara A.; Conde, Daniel; Chakraborty, Sanhita; +11 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
cell-specific
nitrate signaling
transcriptional regulation

Title: Spatiotemporal analysis identifies ABF2 and ABF3 as key hubs of endodermal response to nitrate

Citation Formats

References (81)

Similar Records

Related Subjects