Transcription factor bHLH121 regulates root cortical aerenchyma formation in maize

Schneider, Hannah M.; Lor, Vai S.; Zhang, Xia; Saengwilai, Patompong; Hanlon, Meredith T.; Klein, Stephanie P.; Davis, Jayne L.; Borkar, Aditi N.; Depew, Cody L.; Bennett, Malcolm J.; Kaeppler, Shawn M.; Brown, Kathleen M.; Bhosale, Rahul; Lynch, Jonathan P.

doi:10.1073/pnas.2219668120

Title: Transcription factor bHLH121 regulates root cortical aerenchyma formation in maize

Journal Article · 16 March 2023 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.2219668120 · OSTI ID:1961903

Schneider, Hannah M. ^[1]; Lor, Vai S. ^[2]; Zhang, Xia ^[2]; Saengwilai, Patompong ^[3]; Hanlon, Meredith T. ^[4];

^[4];

^[5];

^[5]; Depew, Cody L. ^[4];

^[5];

^[2];

^[4];

^[5];

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Pennsylvania State Univ., University Park, PA (United States); Wageningen Univ. (Netherlands)
Univ. of Wisconsin, Madison, WI (United States)
Pennsylvania State Univ., University Park, PA (United States); Mahidol University, Bangkok (Thailand)
Pennsylvania State Univ., University Park, PA (United States)
Univ. of Nottingham (United Kingdom)

Root anatomical phenotypes present a promising yet underexploited avenue to deliver major improvements in yield and climate resilience of crops by improving water and nutrient uptake. For instance, the formation of root cortical aerenchyma (RCA) significantly increases soil exploration and resource capture by reducing the metabolic costs of root tissue. A key bottleneck in studying such phenotypes has been the lack of robust high-throughput anatomical phenotyping platforms. We exploited a phenotyping approach based on laser ablation tomography, termed Anatomics, to quantify variation in RCA formation of 436 diverse maize lines in the field. Results revealed a significant and heritable variation for RCA formation. Genome-wide association studies identified a single-nucleotide polymorphism mapping to a root cortex-expressed gene-encoding transcription factor bHLH121. Functional studies identified that the bHLH121 Mu transposon mutant line and CRISPR/Cas9 loss-of-function mutant line showed reduced RCA formation, whereas an overexpression line exhibited significantly greater RCA formation when compared to the wild-type line. Characterization of these lines under suboptimal water and nitrogen availability in multiple soil environments revealed that bHLH121 is required for RCA formation developmentally as well as under studied abiotic stress. Overall functional validation of the bHLH121 gene’s importance in RCA formation provides a functional marker to select varieties with improved soil exploration and thus yield under suboptimal conditions.

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Research Organization:: Pennsylvania State Univ., University Park, PA (United States)

Sponsoring Organization:: USDOE Advanced Research Projects Agency - Energy (ARPA-E); USDA

Grant/Contract Number:: AR0000821; PEN04732

OSTI ID:: 1961903

Alternate ID(s):: OSTI ID: 2418415

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 120, Issue 12; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (90)

Characterization, costs, cues and future perspectives of phenotypic plasticity Schneider, Hannah M. Annals of Botany, Vol. 130, Issue 2 https://doi.org/10.1093/aob/mcac087	journal	June 2022
Molecular and Cellular Adaptations of Maize to Flooding Stress Subbaiah, C. C. Annals of Botany, Vol. 91, Issue 2 https://doi.org/10.1093/aob/mcf210	journal	January 2003
Large Root Cortical Cell Size Improves Drought Tolerance in Maize Chimungu, Joseph G.; Brown, Kathleen M.; Lynch, Jonathan P. Plant Physiology, Vol. 166, Issue 4 https://doi.org/10.1104/pp.114.250449	journal	October 2014
Root Phenes for Enhanced Soil Exploration and Phosphorus Acquisition: Tools for Future Crops Lynch, Jonathan P. Plant Physiology, Vol. 156, Issue 3 https://doi.org/10.1104/pp.111.175414	journal	May 2011
Distinguishing between yield advances and yield plateaus in historical crop production trends Grassini, Patricio; Eskridge, Kent M.; Cassman, Kenneth G. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3918	journal	December 2013
Marker assisted breeding for transformability in maize Lowe, Brenda A.; Way, Melissa M.; Kumpf, Jennifer M. Molecular Breeding, Vol. 18, Issue 3 https://doi.org/10.1007/s11032-006-9031-4	journal	September 2006
Insights into the Maize Pan-Genome and Pan-Transcriptome Hirsch, Candice N.; Foerster, Jillian M.; Johnson, James M. The Plant Cell, Vol. 26, Issue 1 https://doi.org/10.1105/tpc.113.119982	journal	January 2014
Root Architecture and Plant Productivity Lynch, J. Plant Physiology, Vol. 109, Issue 1 https://doi.org/10.1104/pp.109.1.7	journal	September 1995
Transcript profiles in cortical cells of maize primary root during ethylene-induced lysigenous aerenchyma formation under aerobic conditions Takahashi, Hirokazu; Yamauchi, Takaki; Rajhi, Imene Annals of Botany, Vol. 115, Issue 6 https://doi.org/10.1093/aob/mcv018	journal	April 2015
Reduced root cortical burden improves growth and grain yield under low phosphorus availability in maize: Root cortical burden and phosphorus capture Galindo-Castañeda, Tania; Brown, Kathleen M.; Lynch, Jonathan P. Plant, Cell & Environment, Vol. 41, Issue 7 https://doi.org/10.1111/pce.13197	journal	May 2018
Root phenotypes for improved nutrient capture: an underexploited opportunity for global agriculture Lynch, Jonathan P. New Phytologist, Vol. 223, Issue 2 https://doi.org/10.1111/nph.15738	journal	March 2019
Aerenchyma formation and radial O₂loss along adventitious roots of wheat with only the apical root portion exposed to O₂deficiency Malik, A. I.; Colmer, T. D.; Lambers, H. Plant, Cell & Environment, Vol. 26, Issue 10 https://doi.org/10.1046/j.1365-3040.2003.01089.x	journal	September 2003
Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field Trachsel, Samuel; Kaeppler, Shawn M.; Brown, Kathleen M. Plant and Soil, Vol. 341, Issue 1-2 https://doi.org/10.1007/s11104-010-0623-8	journal	November 2010
Root cortical aerenchyma improves the drought tolerance of maize ( Zea mays L.) Zhu, Jinming; Brown, Kathleen M.; Lynch, Jonathan P. Plant, Cell & Environment https://doi.org/10.1111/j.1365-3040.2009.02099.x	journal	February 2010
Diversity and Evolution of Coral Fluorescent Proteins Alieva, Naila O.; Konzen, Karen A.; Field, Steven F. PLoS ONE, Vol. 3, Issue 7 https://doi.org/10.1371/journal.pone.0002680	journal	July 2008
The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches Hirel, B.; Le Gouis, J.; Ney, B. Journal of Experimental Botany, Vol. 58, Issue 9 https://doi.org/10.1093/jxb/erm097	journal	March 2007
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
Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 49, Issue W1 https://doi.org/10.1093/nar/gkab301	journal	April 2021
Roots of the Second Green Revolution Lynch, Jonathan P. Australian Journal of Botany, Vol. 55, Issue 5 https://doi.org/10.1071/BT06118	journal	January 2007
Root Cortical Aerenchyma Enhances the Growth of Maize on Soils with Suboptimal Availability of Nitrogen, Phosphorus, and Potassium Postma, Johannes Auke; Lynch, Jonathan Paul Plant Physiology, Vol. 156, Issue 3 https://doi.org/10.1104/pp.111.175489	journal	May 2011
GAPIT: genome association and prediction integrated tool Lipka, Alexander E.; Tian, Feng; Wang, Qishan Bioinformatics, Vol. 28, Issue 18 https://doi.org/10.1093/bioinformatics/bts444	journal	July 2012
Aerenchyma Formed Under Phosphorus Deficiency Contributes to the Reduced Root Hydraulic Conductivity in Maize Roots Fan, Mingshou; Bai, Ruiqin; Zhao, Xuefeng Journal of Integrative Plant Biology, Vol. 49, Issue 5 https://doi.org/10.1111/j.1744-7909.2007.00450.x	journal	May 2007
Root Cortical Senescence Improves Growth under Suboptimal Availability of N, P, and K Schneider, Hannah M.; Postma, Johannes A.; Wojciechowski, Tobias Plant Physiology, Vol. 174, Issue 4 https://doi.org/10.1104/pp.17.00648	journal	June 2017
A multiple testing correction method for genetic association studies using correlated single nucleotide polymorphisms Gao, Xiaoyi; Starmer, Joshua; Martin, Eden R. Genetic Epidemiology, Vol. 32, Issue 4 https://doi.org/10.1002/gepi.20310	journal	May 2008
Verification of QTL controlling root aerenchyma formation in a maize * teosinte "Zea nicaraguensis" advanced backcross population Mano, Yoshiro; Omori, Fumie Breeding Science, Vol. 58, Issue 3 https://doi.org/10.1270/jsbbs.58.217	journal	January 2008
Root angle in maize influences nitrogen capture and is regulated by calcineurin B‐like protein (CBL) ‐interacting serine/threonine‐protein kinase 15 ( ZmCIPK15 ) Schneider, Hannah M.; Lor, Vai Sa Nee; Hanlon, Meredith T. Plant, Cell & Environment, Vol. 45, Issue 3 https://doi.org/10.1111/pce.14135	journal	July 2021
QTL mapping of root aerenchyma formation in seedlings of a maize × rare teosinte “Zea nicaraguensis” cross Mano, Y.; Omori, F.; Takamizo, T. Plant and Soil, Vol. 295, Issue 1-2 https://doi.org/10.1007/s11104-007-9266-9	journal	May 2007
A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta Curtis, Mark D.; Grossniklaus, Ueli Plant Physiology, Vol. 133, Issue 2, p. 462-469 https://doi.org/10.1104/pp.103.027979	journal	September 2003
Too much of a good thing Sutton, Mark A.; Oenema, Oene; Erisman, Jan Willem Nature, Vol. 472, Issue 7342 https://doi.org/10.1038/472159a	journal	April 2011
Fitting Linear Mixed-Effects Models Using lme4 Bates, Douglas; Mächler, Martin; Bolker, Ben Journal of Statistical Software, Vol. 67, Issue 1 https://doi.org/10.18637/jss.v067.i01	journal	January 2015
Laser ablation tomography for visualization of root colonization by edaphic organisms Strock, Christopher F.; Schneider, Hannah M.; Galindo-Castañeda, Tania Journal of Experimental Botany, Vol. 70, Issue 19 https://doi.org/10.1093/jxb/erz271	journal	June 2019
lmerTest Package: Tests in Linear Mixed Effects Models Kuznetsova, Alexandra; Brockhoff, Per B.; Christensen, Rune H. B. Journal of Statistical Software, Vol. 82, Issue 13 https://doi.org/10.18637/jss.v082.i13	journal	January 2017
Genome-wide atlas of transcription during maize development Sekhon, Rajandeep S.; Lin, Haining; Childs, Kevin L. The Plant Journal, Vol. 66, Issue 4, p. 553-563 https://doi.org/10.1111/j.1365-313X.2011.04527.x	journal	March 2011
Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants Christensen, Alan H.; Quail, Peter H. Transgenic Research, Vol. 5, Issue 3 https://doi.org/10.1007/BF01969712	journal	May 1996
Reduced Root Cortical Cell File Number Improves Drought Tolerance in Maize Chimungu, Joseph G.; Brown, Kathleen M.; Lynch, Jonathan P. Plant Physiology, Vol. 166, Issue 4 https://doi.org/10.1104/pp.114.249037	journal	October 2014
Anatomical features of an African sorghum landrace adapted to flooded conditions Jaffuel, Sylvie; Brocke, Kirsten vom Australian Journal of Crop Science, Vol. 10, Issue 10 https://doi.org/10.21475/ajcs.2016.10.10.p7867	journal	October 2016
Root anatomy and soil resource capture Lynch, Jonathan P.; Strock, Christopher F.; Schneider, Hannah M. Plant and Soil, Vol. 466, Issue 1-2 https://doi.org/10.1007/s11104-021-05010-y	journal	July 2021
Aerenchyma formation: Tansley review Evans, David E. New Phytologist, Vol. 161, Issue 1 https://doi.org/10.1046/j.1469-8137.2003.00907.x	journal	October 2003
Integration of root phenes for soil resource acquisition York, Larry M.; Nord, Eric A.; Lynch, Jonathan P. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00355	journal	January 2013
Characterization of Pearl Millet Root Architecture and Anatomy Reveals Three Types of Lateral Roots Passot, Sixtine; Gnacko, Fatoumata; Moukouanga, Daniel Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00829	journal	June 2016
Opportunities and challenges in the subsoil: pathways to deeper rooted crops Lynch, Jonathan P.; Wojciechowski, Tobias Journal of Experimental Botany, Vol. 66, Issue 8 https://doi.org/10.1093/jxb/eru508	journal	January 2015
Reduction in Root Secondary Growth as a Strategy for Phosphorus Acquisition Strock, Christopher F.; Morrow de la Riva, Laurie; Lynch, Jonathan P. Plant Physiology, Vol. 176, Issue 1 https://doi.org/10.1104/pp.17.01583	journal	November 2017
Phenotyping plants: genes, phenes and machines Pieruschka, Roland; Poorter, Hendrik Functional Plant Biology, Vol. 39, Issue 11 https://doi.org/10.1071/FPv39n11_IN	journal	January 2012
Genetic Transformation Using Maize Immature Zygotic Embryos Frame, Bronwyn; Main, Marcy; Schick, Rosemarie Methods in Molecular Biology https://doi.org/10.1007/978-1-61737-988-8_22	book	December 2010
Light-activated Cryptochrome Reacts with Molecular Oxygen to Form a Flavin–Superoxide Radical Pair Consistent with Magnetoreception Müller, Pavel; Ahmad, Margaret Journal of Biological Chemistry, Vol. 286, Issue 24 https://doi.org/10.1074/jbc.M111.228940	journal	June 2011
Characterization of Cestrum yellow leaf curling virus: a new member of the family Caulimoviridae Stavolone, Livia; Ragozzino, Antonio; Hohn, Thomas Journal of General Virology, Vol. 84, Issue 12 https://doi.org/10.1099/vir.0.19405-0	journal	December 2003
Blue‐light dependent reactive oxygen species formation by Arabidopsis cryptochrome may define a novel evolutionarily conserved signaling mechanism Consentino, Laurent; Lambert, Stefan; Martino, Carlos New Phytologist, Vol. 206, Issue 4 https://doi.org/10.1111/nph.13341	journal	February 2015
Multiple Integrated Root Phenotypes Are Associated with Improved Drought Tolerance Klein, Stephanie P.; Schneider, Hannah M.; Perkins, Alden C. Plant Physiology, Vol. 183, Issue 3 https://doi.org/10.1104/pp.20.00211	journal	April 2020
MaizeGDB 2018: the maize multi-genome genetics and genomics database Portwood, John L.; Woodhouse, Margaret R.; Cannon, Ethalinda K. Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1046	journal	November 2018
Switchgrass (Panicum virgatum L.) polyubiquitin gene (PvUbi1 and PvUbi2) promoters for use in plant transformation Mann, David GJ; King, Zachary R.; Liu, Wusheng BMC Biotechnology, Vol. 11, Issue 1 https://doi.org/10.1186/1472-6750-11-74	journal	July 2011
QTL mapping and phenotypic variation of root anatomical traits in maize (Zea mays L.) Burton, Amy L.; Johnson, James; Foerster, Jillian Theoretical and Applied Genetics, Vol. 128, Issue 1 https://doi.org/10.1007/s00122-014-2414-8	journal	October 2014
Gateway-compatible vectors for high-throughput gene functional analysis in switchgrass (Panicum virgatum L.) and other monocot species: Gateway-compatible vectors for monocot transformation Mann, David G. J.; LaFayette, Peter R.; Abercrombie, Laura L. Plant Biotechnology Journal, Vol. 10, Issue 2 https://doi.org/10.1111/j.1467-7652.2011.00658.x	journal	September 2011
Functional implications of root cortical senescence for soil resource capture Schneider, Hannah M.; Lynch, Jonathan P. Plant and Soil, Vol. 423, Issue 1-2 https://doi.org/10.1007/s11104-017-3533-1	journal	December 2017
Improved maize reference genome with single-molecule technologies Jiao, Yinping; Peluso, Paul; Shi, Jinghua Nature, Vol. 546, Issue 7659 https://doi.org/10.1038/nature22971	journal	June 2017
Construction of expression vectors based on the rice actin 1 (Act1) 5′ region for use in monocot transformation McElroy, David; Blowers, Alan D.; Jenes, Barnabás Molecular and General Genetics MGG, Vol. 231, Issue 1 https://doi.org/10.1007/BF00293832	journal	December 1991
Morphological and physiological responses to burial depth and sediment type in the wetland macrophyte Miscanthus sacchariflorus Pan, Ying; Xie, Yonghong; Li, Feng Fundamental and Applied Limnology, Vol. 180, Issue 3 https://doi.org/10.1127/1863-9135/2012/0266	journal	April 2012
The Maize Genetics and Genomics Database. The Community Resource for Access to Diverse Maize Data Lawrence, Carolyn J.; Seigfried, Trent E.; Brendel, Volker Plant Physiology, Vol. 138, Issue 1 https://doi.org/10.1104/pp.104.059196	journal	May 2005
PLAZA 4.0: an integrative resource for functional, evolutionary and comparative plant genomics Van Bel, Michiel; Diels, Tim; Vancaester, Emmelien Nucleic Acids Research, Vol. 46, Issue D1 https://doi.org/10.1093/nar/gkx1002	journal	October 2017
Steady-state transposon mutagenesis in inbred maize: Maize steady-state transposon mutagenesis McCarty, Donald R.; Mark Settles, Andrew; Suzuki, Masaharu The Plant Journal, Vol. 44, Issue 1 https://doi.org/10.1111/j.1365-313X.2005.02509.x	journal	September 2005
Anatomics: High-throughput phenotyping of plant anatomy Strock, Christopher F.; Schneider, Hannah M.; Lynch, Jonathan P. Trends in Plant Science, Vol. 27, Issue 6 https://doi.org/10.1016/j.tplants.2022.02.009	journal	June 2022
Identification of aerenchyma formation-related QTL in barley that can be effective in breeding for waterlogging tolerance Zhang, Xuechen; Zhou, Gaofeng; Shabala, Sergey Theoretical and Applied Genetics, Vol. 129, Issue 6 https://doi.org/10.1007/s00122-016-2693-3	journal	February 2016
Gateway-compatible vectors for plant functional genomics and proteomics Earley, Keith W.; Haag, Jeremy R.; Pontes, Olga The Plant Journal, Vol. 45, Issue 4 https://doi.org/10.1111/j.1365-313X.2005.02617.x	journal	February 2006
Root biology and genetic improvement for drought avoidance in rice Gowda, Veeresh R. P.; Henry, Amelia; Yamauchi, Akira Field Crops Research, Vol. 122, Issue 1 https://doi.org/10.1016/j.fcr.2011.03.001	journal	April 2011
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
Bioconductor: open software development for computational biology and bioinformatics Gentleman, Robert C.; Carey, Vincent J.; Bates, Douglas M. Genome Biology, Vol. 5, Issue 10, p. R80 https://doi.org/10.1186/gb-2004-5-10-r80	journal	September 2004
Genetic control of root anatomical plasticity in maize Schneider, Hannah M.; Klein, Stephanie P.; Hanlon, Meredith T. The Plant Genome, Vol. 13, Issue 1 https://doi.org/10.1002/tpg2.20003	journal	March 2020
A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize Usadel, Bjorn; Poree, Fabien; Nagel, Axel Plant, Cell & Environment, Vol. 32, Issue 9, p. 1211-1229 https://doi.org/10.1111/j.1365-3040.2009.01978.x	journal	September 2009
Targeted genome editing in human cells with zinc finger nucleases constructed via modular assembly Kim, H. J.; Lee, H. J.; Kim, H. Genome Research, Vol. 19, Issue 7 https://doi.org/10.1101/gr.089417.108	journal	May 2009
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Theoretical evidence for the functional benefit of root cortical aerenchyma in soils with low phosphorus availability Postma, Johannes A.; Lynch, Jonathan P. Annals of Botany, Vol. 107, Issue 5 https://doi.org/10.1093/aob/mcq199	journal	October 2010
The control of endopolygalacturonase expression by the sugarcane RAV transcription factor during aerenchyma formation Tavares, Eveline Q. P.; De Souza, Amanda P.; Romim, Grayce H. Journal of Experimental Botany, Vol. 70, Issue 2 https://doi.org/10.1093/jxb/ery362	journal	January 2019
New insights into trophic aerenchyma formation strategy in maize (Zea mays L.) organs during sulfate deprivation Maniou, Filippa; Chorianopoulou, Styliani N.; Bouranis, Dimitris L. Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00581	journal	November 2014
FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix Price, M. N.; Dehal, P. S.; Arkin, A. P. Molecular Biology and Evolution, Vol. 26, Issue 7 https://doi.org/10.1093/molbev/msp077	journal	April 2009
New roots for agriculture: exploiting the root phenome Lynch, Jonathan P.; Brown, Kathleen M. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1595 https://doi.org/10.1098/rstb.2011.0243	journal	June 2012
Root phenes that reduce the metabolic costs of soil exploration: opportunities for 21st century agriculture: New roots for agriculture Lynch, Jonathan P. Plant, Cell & Environment, Vol. 38, Issue 9 https://doi.org/10.1111/pce.12451	journal	November 2014
Identification of genes expressed in maize root cortical cells during lysigenous aerenchyma formation using laser microdissection and microarray analyses Rajhi, Imene; Yamauchi, Takaki; Takahashi, Hirokazu New Phytologist, Vol. 190, Issue 2 https://doi.org/10.1111/j.1469-8137.2010.03535.x	journal	November 2010
Rightsizing root phenotypes for drought resistance Lynch, Jonathan P. Journal of Experimental Botany, Vol. 69, Issue 13 https://doi.org/10.1093/jxb/ery048	journal	February 2018
A Multipurpose Toolkit to Enable Advanced Genome Engineering in Plants Čermák, Tomáš; Curtin, Shaun J.; Gil-Humanes, Javier The Plant Cell, Vol. 29, Issue 6 https://doi.org/10.1105/tpc.16.00922	journal	May 2017
Root cortical burden influences drought tolerance in maize Jaramillo, Raúl E.; Nord, Eric A.; Chimungu, Joseph G. Annals of Botany, Vol. 112, Issue 2 https://doi.org/10.1093/aob/mct069	journal	April 2013
Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize( Zea mays L.) Gunawardena, Arunika H. L. A. N.; Pearce, Deborah M.; Jackson, Michael B. Planta, Vol. 212, Issue 2 https://doi.org/10.1007/s004250000381	journal	January 2001
Programmed cell death and aerenchyma formation in roots Drew, Malcolm C.; He, Chuan-Jiu; Morgan, Page W. Trends in Plant Science, Vol. 5, Issue 3 https://doi.org/10.1016/S1360-1385(00)01570-3	journal	March 2000
Three-dimensional analysis of biological systems via a novel laser ablation technique Hall, Benjamin; Lanba, Asheesh Journal of Laser Applications, Vol. 31, Issue 2 https://doi.org/10.2351/1.5096089	journal	May 2019
Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems Lynch, Jonathan P. Annals of Botany, Vol. 112, Issue 2 https://doi.org/10.1093/aob/mcs293	journal	January 2013
Utility of root cortical aerenchyma under water limited conditions in tropical maize (Zea mays L.) Chimungu, Joseph G.; Maliro, Moses F. A.; Nalivata, Patson C. Field Crops Research, Vol. 171 https://doi.org/10.1016/j.fcr.2014.10.009	journal	February 2015
Root cortical senescence decreases root respiration, nutrient content and radial water and nutrient transport in barley: Cortical senescence reduces respiration, nutrient content and radial transport Schneider, Hannah M.; Wojciechowski, Tobias; Postma, Johannes A. Plant, Cell & Environment, Vol. 40, Issue 8 https://doi.org/10.1111/pce.12933	journal	April 2017
EAT1 promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice Niu, Ningning; Liang, Wanqi; Yang, Xijia Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms2396	journal	February 2013
Genotypic variation and nitrogen stress effects on root anatomy in maize are node specific Yang, Jennifer T.; Schneider, Hannah M.; Brown, Kathleen M. Journal of Experimental Botany, Vol. 70, Issue 19 https://doi.org/10.1093/jxb/erz293	journal	June 2019
Genetic Diversity of a Maize Association Population with Restricted Phenology Hansey, Candice N.; Johnson, James M.; Sekhon, Rajandeep S. Crop Science, Vol. 51, Issue 2 https://doi.org/10.2135/cropsci2010.03.0178	journal	January 2011
Root Cortical Aerenchyma Enhances Nitrogen Acquisition from Low-Nitrogen Soils in Maize Saengwilai, P.; Nord, E. A.; Chimungu, J. G. PLANT PHYSIOLOGY, Vol. 166, Issue 2 https://doi.org/10.1104/pp.114.241711	journal	June 2014
RootScan: Software for high-throughput analysis of root anatomical traits Burton, Amy L.; Williams, Michael; Lynch, Jonathan P. Plant and Soil, Vol. 357, Issue 1-2 https://doi.org/10.1007/s11104-012-1138-2	journal	February 2012

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Title: Transcription factor bHLH121 regulates root cortical aerenchyma formation in maize

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