An expanded maize gene expression atlas based on RNA sequencing and its use to explore root development

Stelpflug, Scott C.; Sekhon, Rajandeep S.; Vaillancourt, Brieanne; Hirsch, Candice N.; Buell, C. Robin; de Leon, Natalia; Kaeppler, Shawn M.

doi:10.3835/plantgenome2015.04.0025

Title: An expanded maize gene expression atlas based on RNA sequencing and its use to explore root development

Journal Article · Wed Dec 30 00:00:00 EST 2015 · The Plant Genome

DOI:https://doi.org/10.3835/plantgenome2015.04.0025· OSTI ID:1363961

Stelpflug, Scott C. ^[1]; Sekhon, Rajandeep S. ^[2]; Vaillancourt, Brieanne ^[3]; Hirsch, Candice N. ^[4]; Buell, C. Robin ^[3]; de Leon, Natalia ^[5]; Kaeppler, Shawn M. ^[5]

Univ. of Wisconsin, Madison, WI (United States)
Clemson Univ., Clemson, SC (United States)
Michigan State Univ., East Lansing, MI (United States); DOE Great Lakes Bioenergy Research Center, East Lansing, MI (United States)
Univ. of Minnesota, St. Paul, MN (United States)
Univ. of Wisconsin, Madison, WI (United States); DOE Great Lakes Bioenergy Research Center, Madison, WI (United States)

Comprehensive and systematic transcriptome profiling provides valuable insight into biological and developmental processes that occur throughout the life cycle of a plant. We have enhanced our previously published microarray-based gene atlas of maize (Zea mays L.) inbred B73 to now include 79 distinct replicated samples that have been interrogated using RNA sequencing (RNA-seq). The current version of the atlas includes 50 original array-based gene atlas samples, a time-course of 12 stalk and leaf samples postflowering, and an additional set of 17 samples from the maize seedling and adult root system. The entire dataset contains 4.6 billion mapped reads, with an average of 20.5 million mapped reads per biological replicate, allowing for detection of genes with lower transcript abundance. As the new root samples represent key additions to the previously examined tissues, we highlight insights into the root transcriptome, which is represented by 28,894 (73.2%) annotated genes in maize. Additionally, we observed remarkable expression differences across both the longitudinal (four zones) and radial gradients (cortical parenchyma and stele) of the primary root supported by fourfold differential expression of 9353 and 4728 genes, respectively. Among the latter were 1110 genes that encode transcription factors, some of which are orthologs of previously characterized transcription factors known to regulate root development in Arabidopsis thaliana (L.) Heynh., while most are novel, and represent attractive targets for reverse genetics approaches to determine their roles in this important organ. As a result, this comprehensive transcriptome dataset is a powerful tool toward understanding maize development, physiology, and phenotypic diversity.

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Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: FC02-07ER64494

OSTI ID:: 1363961

Journal Information:: The Plant Genome, Vol. 9, Issue 1; ISSN 1940-3372

Publisher:: Alliance of Crop, Soil, and Environmental Science SocietiesCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 210 works

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References (98)

Transcriptional profiling of Arabidopsis root hairs and pollen defines an apical cell growth signature Becker, Jörg D.; Takeda, Seiji; Borges, Filipe BMC Plant Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12870‐014‐0197‐3	journal	August 2014
EIN3-Dependent Regulation of Plant Ethylene Hormone Signaling by Two Arabidopsis F Box Proteins Potuschak, Thomas; Lechner, Esther; Parmentier, Yves Cell, Vol. 115, Issue 6, p. 679-689 https://doi.org/10.1016/S0092-8674(03)00968-1	journal	December 2003
EIN3-Dependent Regulation of Plant Ethylene Hormone Signaling by Two Arabidopsis F Box Proteins Potuschak, Thomas; Lechner, Esther; Parmentier, Yves Cell, Vol. 115, Issue 6 https://doi.org/10.1016/S0092‐8674(03)00968‐1	journal	December 2003
Reactive oxygen species mediate growth and death in submerged plants Steffens, Bianka; Steffen-Heins, Anja; Sauter, Margret Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00179	journal	January 2013
mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes Thimm, Oliver; Bläsing, Oliver; Gibon, Yves The Plant Journal, Vol. 37, Issue 6 https://doi.org/10.1111/j.1365‐313X.2004.02016.x	journal	March 2004
A Sorghum bicolor expression atlas reveals dynamic genotype-specific expression profiles for vegetative tissues of grain, sweet and bioenergy sorghums Shakoor, Nadia; Nair, Ramesh; Crasta, Oswald BMC Plant Biology, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2229-14-35	journal	January 2014
The phenylpropanoid pathway and plant defence-a genomics perspective Dixon, Richard A.; Achnine, Lahoucine; Kota, Parvathi Molecular Plant Pathology, Vol. 3, Issue 5 https://doi.org/10.1046/j.1364-3703.2002.00131.x	journal	September 2002
GRASSIUS: A Platform for Comparative Regulatory Genomics across the Grasses Yilmaz, Alper; Nishiyama, Milton Y.; Fuentes, Bernardo Garcia Plant Physiology, Vol. 149, Issue 1 https://doi.org/10.1104/pp.108.128579	journal	November 2008
Development of the Inflorescences Vollbrecht, Erik; Schmidt, Robert J. Handbook of Maize: Its Biology https://doi.org/10.1007/978-0-387-79418-1_2	book	January 2009
Hybridization interactions between probesets in short oligo microarrays lead to spurious correlations Okoniewski, Michał J.; Miller, Crispin J. BMC Bioinformatics, Vol. 7, Issue 1 https://doi.org/10.1186/1471‐2105‐7‐276	journal	June 2006
The effects of redox controls mediated by glutathione peroxidases on root architecture in Arabidopsis thaliana Passaia, Gisele; Queval, Guillaume; Bai, Juan Journal of Experimental Botany, Vol. 65, Issue 5 https://doi.org/10.1093/jxb/ert486	journal	January 2014
Root System Regulation of Whole Plant Growth Aiken, R. M.; Smucker, A. J. M. Annual Review of Phytopathology, Vol. 34, Issue 1 https://doi.org/10.1146/annurev.phyto.34.1.325	journal	September 1996
Root hair-specific expansins modulate root hair elongation in rice: Rice root hair elongation requires expansins ZhiMing, Yu; Bo, Kang; XiaoWei, He The Plant Journal, Vol. 66, Issue 5 https://doi.org/10.1111/j.1365‐313X.2011.04533.x	journal	March 2011
Auxin and ethylene promote root hair elongation inArabidopsis Pitts, R. Jason; Cernac, Alex; Estelle, Mark The Plant Journal, Vol. 16, Issue 5 https://doi.org/10.1046/j.1365-313x.1998.00321.x	journal	December 1998
An “Electronic Fluorescent Pictograph” Browser for Exploring and Analyzing Large-Scale Biological Data Sets Winter, Debbie; Vinegar, Ben; Nahal, Hardeep PLoS ONE, Vol. 2, Issue 8 https://doi.org/10.1371/journal.pone.0000718	journal	August 2007
Full-length transcriptome assembly from RNA-Seq data without a reference genome Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran Nature Biotechnology, Vol. 29, Issue 7 https://doi.org/10.1038/nbt.1883	journal	May 2011
Specification of Cortical Parenchyma and Stele of Maize Primary Roots by Asymmetric Levels of Auxin, Cytokinin, and Cytokinin-Regulated Proteins Saleem, Muhammad; Lamkemeyer, Tobias; Schützenmeister, André Plant Physiology, Vol. 152, Issue 1 https://doi.org/10.1104/pp.109.150425	journal	November 2009
Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis Mustroph, A.; Zanetti, M. E.; Jang, C. J. H. Proceedings of the National Academy of Sciences, Vol. 106, Issue 44 https://doi.org/10.1073/pnas.0906131106	journal	October 2009
An integrated transcriptome atlas of the crop model Glycine max, and its use in comparative analyses in plants: Soybean transcriptome atlas Libault, Marc; Farmer, Andrew; Joshi, Trupti The Plant Journal https://doi.org/10.1111/j.1365‐313X.2010.04222.x	journal	April 2010
Flavonoids and Isoflavonoids: From Plant Biology to Agriculture and Neuroscience Dixon, Richard A.; Pasinetti, Giulio M. Plant Physiology, Vol. 154, Issue 2 https://doi.org/10.1104/pp.110.161430	journal	October 2010
ROS as key players in plant stress signalling Baxter, A.; Mittler, R.; Suzuki, N. Journal of Experimental Botany, Vol. 65, Issue 5 https://doi.org/10.1093/jxb/ert375	journal	November 2013
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
A Global View of Gene Activity and Alternative Splicing by Deep Sequencing of the Human Transcriptome Sultan, M.; Schulz, M. H.; Richard, H. Science, Vol. 321, Issue 5891 https://doi.org/10.1126/science.1160342	journal	August 2008
Distinct Genetic Architectures for Male and Female Inflorescence Traits of Maize Brown, Patrick J.; Upadyayula, Narasimham; Mahone, Gregory S. PLoS Genetics, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pgen.1002383	journal	November 2011
Genetic Dissection of Root Formation in Maize (Zea mays) Reveals Root-type Specific Developmental Programmes Hochholdinger, F. Annals of Botany, Vol. 93, Issue 4 https://doi.org/10.1093/aob/mch056	journal	February 2004
Specialized Zones of Development in Roots: View from the Cellular Level Baluska, F.; Volkmann, D.; Barlow, P. W. Plant Physiology, Vol. 112, Issue 1 https://doi.org/10.1104/pp.112.1.3	journal	September 1996
mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes Thimm, Oliver; Bläsing, Oliver; Gibon, Yves The Plant Journal, Vol. 37, Issue 6, p. 914-939 https://doi.org/10.1111/j.1365-313X.2004.02016.x	journal	March 2004
A near complete snapshot of the Zea mays seedling transcriptome revealed from ultra-deep sequencing Martin, Jeffrey A.; Johnson, Nicole V.; Gross, Stephen M. Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep04519	journal	March 2014
A basic helix-loop-helix transcription factor controls cell growth and size in root hairs Yi, Keke; Menand, Benoît; Bell, Elizabeth Nature Genetics, Vol. 42, Issue 3 https://doi.org/10.1038/ng.529	journal	February 2010
RNA-Seq: a revolutionary tool for transcriptomics Wang, Zhong; Gerstein, Mark; Snyder, Michael Nature Reviews Genetics, Vol. 10, Issue 1 https://doi.org/10.1038/nrg2484	journal	January 2009
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
ARF7 and ARF19 Regulate Lateral Root Formation via Direct Activation of LBD/ASL Genes in Arabidopsis Okushima, Yoko; Fukaki, Hidehiro; Onoda, Makoto The Plant Cell, Vol. 19, Issue 1 https://doi.org/10.1105/tpc.106.047761	journal	January 2007
Establishment of the Lotus japonicus Gene Expression Atlas (LjGEA) and its use to explore legume seed maturation Verdier, Jerome; Torres-Jerez, Ivone; Wang, Mingyi The Plant Journal, Vol. 74, Issue 2 https://doi.org/10.1111/tpj.12119	journal	March 2013
Maize Gene Atlas Developed by RNA Sequencing and Comparative Evaluation of Transcriptomes Based on RNA Sequencing and Microarrays Sekhon, Rajandeep S.; Briskine, Roman; Hirsch, Candice N. PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061005	journal	April 2013
Auxin and ethylene promote root hair elongation inArabidopsis Pitts, R. Jason; Cernac, Alex; Estelle, Mark The Plant Journal, Vol. 16, Issue 5 https://doi.org/10.1046/j.1365‐313x.1998.00321.x	journal	December 1998
Nonsyntenic Genes Drive Highly Dynamic Complementation of Gene Expression in Maize Hybrids Paschold, Anja; Larson, Nick B.; Marcon, Caroline The Plant Cell, Vol. 26, Issue 10 https://doi.org/10.1105/tpc.114.130948	journal	October 2014
Dynamics of Aerenchyma Distribution in the Cortex of Sulfate-deprived Adventitious Roots of Maize Bouranis, Dimitris L.; Chorianopoulou, Styliani N.; Kollias, Charalambos Annals of Botany, Vol. 97, Issue 5 https://doi.org/10.1093/aob/mcl024	journal	February 2006
Temporal patterns of gene expression in developing maize endosperm identified through transcriptome sequencing Li, G.; Wang, D.; Yang, R. Proceedings of the National Academy of Sciences, Vol. 111, Issue 21 https://doi.org/10.1073/pnas.1406383111	journal	May 2014
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
agriGO: a GO analysis toolkit for the agricultural community Du, Zhou; Zhou, Xin; Ling, Yi Nucleic Acids Research, Vol. 38, Issue suppl_2 https://doi.org/10.1093/nar/gkq310	journal	April 2010
Specialized Zones of Development in Roots Ishikawa, H.; Evans, M. L. Plant Physiology, Vol. 109, Issue 3 https://doi.org/10.1104/pp.109.3.725	journal	November 1995
The Emerging Role of Reactive Oxygen Species Signaling during Lateral Root Development Manzano, Concepción; Pallero-Baena, Mercedes; Casimiro, Ilda Plant Physiology, Vol. 165, Issue 3 https://doi.org/10.1104/pp.114.238873	journal	May 2014
The B73 Maize Genome: Complexity, Diversity, and Dynamics Schnable, P. S.; Ware, D.; Fulton, R. S. Science, Vol. 326, Issue 5956, p. 1112-1115 https://doi.org/10.1126/science.1178534	journal	November 2009
The SCARECROW Gene Regulates an Asymmetric Cell Division That Is Essential for Generating the Radial Organization of the Arabidopsis Root Di Laurenzio, Laura; Wysocka-Diller, Joanna; Malamy, Jocelyn E. Cell, Vol. 86, Issue 3 https://doi.org/10.1016/S0092-8674(00)80115-4	journal	August 1996
Accumulation of the phytoalexin lettucenin a and changes in 3-hydroxy-3-methylglutaryl coenzyme a reductase activity in lettuce seedlings with the red spot disorder Bestwick, L.; Bennett, M. H.; Mansfield, J. W. Phytochemistry, Vol. 39, Issue 4 https://doi.org/10.1016/0031-9422(95)00089-P	journal	July 1995
Transcriptional and Metabolic Analysis of Senescence Induced by Preventing Pollination in Maize Sekhon, Rajandeep S.; Childs, Kevin L.; Santoro, Nicholas Plant Physiology, Vol. 159, Issue 4 https://doi.org/10.1104/pp.112.199224	journal	June 2012
POGs/PlantRBP: a resource for comparative genomics in plants Walker, Nigel S.; Stiffler, Nicholas; Barkan, Alice Nucleic Acids Research, Vol. 35, Issue suppl_1 https://doi.org/10.1093/nar/gkl795	journal	November 2006
The developmental dynamics of the maize leaf transcriptome Li, Pinghua; Ponnala, Lalit; Gandotra, Neeru Nature Genetics, Vol. 42, Issue 12, p. 1060-1067 https://doi.org/10.1038/ng.703	journal	October 2010
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
Translational Biology: From Arabidopsis Flowers to Grass Inflorescence Architecture Thompson, Beth E.; Hake, Sarah Plant Physiology, Vol. 149, Issue 1 https://doi.org/10.1104/pp.108.129619	journal	January 2009
Root hair-specific EXPANSIN A7 is required for root hair elongation in Arabidopsis Lin, Changfa; Choi, Hee-Seung; Cho, Hyung-Taeg Molecules and Cells, Vol. 31, Issue 4 https://doi.org/10.1007/s10059‐011‐0046‐2	journal	February 2011
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
Coupling and coordination in gene expression processes: a systems biology view Komili, Suzanne; Silver, Pamela A. Nature Reviews Genetics, Vol. 9, Issue 1 https://doi.org/10.1038/nrg2223	journal	January 2008
Ethylene is a positive regulator of root hair development in Arabidopsis thaliana: Root hair development in A. thaliana Tanimoto, Mimi; Roberts, Keith; Dolan, Liam The Plant Journal, Vol. 8, Issue 6 https://doi.org/10.1046/j.1365-313X.1995.8060943.x	journal	December 1995
POGs2: A Web Portal to Facilitate Cross-Species Inferences About Protein Architecture and Function in Plants Tomcal, Michael; Stiffler, Nicholas; Barkan, Alice PLoS ONE, Vol. 8, Issue 12 https://doi.org/10.1371/journal.pone.0082569	journal	December 2013
LATERAL ROOT PRIMORDIA 1 of maize acts as a transcriptional activator in auxin signalling downstream of the Aux/IAA gene rootless with undetectable meristem 1 Zhang, Yanxiang; Behrens, Inga von; Zimmermann, Roman Journal of Experimental Botany, Vol. 66, Issue 13 https://doi.org/10.1093/jxb/erv187	journal	April 2015
Root hair-specific expansins modulate root hair elongation in rice: Rice root hair elongation requires expansins ZhiMing, Yu; Bo, Kang; XiaoWei, He The Plant Journal, Vol. 66, Issue 5 https://doi.org/10.1111/j.1365-313X.2011.04533.x	journal	March 2011
Mapping and quantifying mammalian transcriptomes by RNA-Seq Mortazavi, Ali; Williams, Brian A.; McCue, Kenneth Nature Methods, Vol. 5, Issue 7, p. 621-628 https://doi.org/10.1038/nmeth.1226	journal	May 2008
Roothairless5 , which functions in maize ( Zea mays L.) root hair initiation and elongation encodes a monocot-specific NADPH oxidase Nestler, Josefine; Liu, Sanzhen; Wen, Tsui-Jung The Plant Journal, Vol. 79, Issue 5 https://doi.org/10.1111/tpj.12578	journal	July 2014
Regulatory modules controlling maize inflorescence architecture Eveland, A. L.; Goldshmidt, A.; Pautler, M. Genome Research, Vol. 24, Issue 3 https://doi.org/10.1101/gr.166397.113	journal	December 2013
A High-Resolution Tissue-Specific Proteome and Phosphoproteome Atlas of Maize Primary Roots Reveals Functional Gradients along the Root Axes Marcon, Caroline; Malik, Waqas Ahmed; Walley, Justin W. Plant Physiology, Vol. 168, Issue 1 https://doi.org/10.1104/pp.15.00138	journal	March 2015
Ethylene is a positive regulator of root hair development in Arabidopsis thaliana: Root hair development in A. thaliana Tanimoto, Mimi; Roberts, Keith; Dolan, Liam The Plant Journal, Vol. 8, Issue 6 https://doi.org/10.1046/j.1365‐313X.1995.8060943.x	journal	December 1995
Tissue specificity of assimilation and transport of nitrogen in the root ofZea mays L. seedlings. I. Transformations of14C- sucrose and the nitrogen metabolism enzymes in cortex and stele Izmailov, S. F.; Piskorskaya, V. P.; Bruskova, R. K. Biologia Plantarum, Vol. 24, Issue 4 https://doi.org/10.1007/BF02879452	journal	July 1982
LACCASE Is Necessary and Nonredundant with PEROXIDASE for Lignin Polymerization during Vascular Development in Arabidopsis Zhao, Qiao; Nakashima, Jin; Chen, Fang The Plant Cell, Vol. 25, Issue 10 https://doi.org/10.1105/tpc.113.117770	journal	October 2013
Dynamic Transcriptome Landscape of Maize Embryo and Endosperm Development Chen, Jian; Zeng, Biao; Zhang, Mei Plant Physiology, Vol. 166, Issue 1 https://doi.org/10.1104/pp.114.240689	journal	July 2014
Cytokinins Act Directly on Lateral Root Founder Cells to Inhibit Root Initiation Laplaze, Laurent; Benkova, Eva; Casimiro, Ilda The Plant Cell, Vol. 19, Issue 12 https://doi.org/10.1105/tpc.107.055863	journal	December 2007
In the Early Response of Arabidopsis Roots to Ethylene, Cell Elongation Is Up- and Down-Regulated and Uncoupled from Differentiation Le, Jie; Vandenbussche, Filip; Van Der Straeten, Dominique Plant Physiology, Vol. 125, Issue 2 https://doi.org/10.1104/pp.125.2.519	journal	February 2001
A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize Usadel, BjÖRn; Poree, Fabien; Nagel, Axel Plant, Cell & Environment, Vol. 32, Issue 9 https://doi.org/10.1111/j.1365‐3040.2009.01978.x	journal	September 2009
Genetic and genomic dissection of maize root development and architecture Hochholdinger, Frank; Tuberosa, Roberto Current Opinion in Plant Biology, Vol. 12, Issue 2 https://doi.org/10.1016/j.pbi.2008.12.002	journal	April 2009
Utility of RNA Sequencing for Analysis of Maize Reproductive Transcriptomes Davidson, Rebecca M.; Hansey, Candice N.; Gowda, Malali The Plant Genome Journal, Vol. 4, Issue 3, p. 191-203 https://doi.org/10.3835/plantgenome2011.05.0015	journal	August 2011
A gene expression atlas of the model legume Medicago truncatula Benedito, Vagner A.; Torres-Jerez, Ivone; Murray, Jeremy D. The Plant Journal, Vol. 55, Issue 3 https://doi.org/10.1111/j.1365‐313X.2008.03519.x	journal	August 2008
PlantGSEA: a gene set enrichment analysis toolkit for plant community Yi, Xin; Du, Zhou; Su, Zhen Nucleic Acids Research, Vol. 41, Issue W1 https://doi.org/10.1093/nar/gkt281	journal	April 2013
Transcriptional profiling of Arabidopsis root hairs and pollen defines an apical cell growth signature Becker, Jörg D.; Takeda, Seiji; Borges, Filipe BMC Plant Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12870-014-0197-3	journal	August 2014
Reactive oxygen species produced by NADPH oxidase regulate plant cell growth Foreman, Julia; Demidchik, Vadim; Bothwell, John H. F. Nature, Vol. 422, Issue 6930 https://doi.org/10.1038/nature01485	journal	March 2003
Laccases Direct Lignification in the Discrete Secondary Cell Wall Domains of Protoxylem Schuetz, M.; Benske, A.; Smith, R. A. PLANT PHYSIOLOGY, Vol. 166, Issue 2 https://doi.org/10.1104/pp.114.245597	journal	August 2014
The bHLH Transcription Factor MYC3 Interacts with the Jasmonate ZIM-Domain Proteins to Mediate Jasmonate Response in Arabidopsis Cheng, Zhiwei; Sun, Li; Qi, Tiancong Molecular Plant, Vol. 4, Issue 2 https://doi.org/10.1093/mp/ssq073	journal	March 2011
Toward a universal microarray: prediction of gene expression through nearest-neighbor probe sequence identification Royce, T. E.; Rozowsky, J. S.; Gerstein, M. B. Nucleic Acids Research, Vol. 35, Issue 15 https://doi.org/10.1093/nar/gkm549	journal	July 2007
An atlas of gene expression from seed to seed through barley development Druka, Arnis; Muehlbauer, Gary; Druka, Ilze Functional & Integrative Genomics, Vol. 6, Issue 3 https://doi.org/10.1007/s10142‐006‐0025‐4	journal	March 2006
Reconstruction of protein networks from an atlas of maize seed proteotypes Walley, J. W.; Shen, Z.; Sartor, R. Proceedings of the National Academy of Sciences, Vol. 110, Issue 49 https://doi.org/10.1073/pnas.1319113110	journal	November 2013
MaizeGDB, the community database for maize genetics and genomics Lawrence, C. J. Nucleic Acids Research, Vol. 32, Issue 90001 https://doi.org/10.1093/nar/gkh011	journal	January 2004
A Sorghum bicolor expression atlas reveals dynamic genotype-specific expression profiles for vegetative tissues of grain, sweet and bioenergy sorghums Shakoor, Nadia; Nair, Ramesh; Crasta, Oswald BMC Plant Biology, Vol. 14, Issue 1 https://doi.org/10.1186/1471‐2229‐14‐35	journal	January 2014
A transcriptome atlas of rice cell types uncovers cellular, functional and developmental hierarchies Jiao, Yuling; Lori Tausta, S.; Gandotra, Neeru Nature Genetics, Vol. 41, Issue 2 https://doi.org/10.1038/ng.282	journal	January 2009
under dependency Yekutieli, Daniel; Benjamini, Yoav The Annals of Statistics, Vol. 29, Issue 4 https://doi.org/10.1214/aos/1013699998	journal	August 2001
APL regulates vascular tissue identity in Arabidopsis Bonke, Martin; Thitamadee, Siripong; Mähönen, Ari Pekka Nature, Vol. 426, Issue 6963, p. 181-186 https://doi.org/10.1038/nature02100	journal	November 2003
The phenylpropanoid pathway and plant defence-a genomics perspective: Phenylpropanoids and plant defence Dixon, Richard A.; Achnine, Lahoucine; Kota, Parvathi Molecular Plant Pathology, Vol. 3, Issue 5 https://doi.org/10.1046/j.1364‐3703.2002.00131.x	journal	August 2002
A gene expression atlas of the model legume Medicago truncatula Benedito, Vagner A.; Torres-Jerez, Ivone; Murray, Jeremy D. The Plant Journal, Vol. 55, Issue 3 https://doi.org/10.1111/j.1365-313X.2008.03519.x	journal	August 2008
The role of reactive oxygen species in cell growth: lessons from root hairs Carol, R. J. Journal of Experimental Botany, Vol. 57, Issue 8 https://doi.org/10.1093/jxb/erj201	journal	May 2006
The Arabidopsis EIN3 Binding F-Box Proteins EBF1 and EBF2 Have Distinct but Overlapping Roles in Ethylene Signaling Binder, Brad M.; Walker, Joseph M.; Gagne, Jennifer M. The Plant Cell, Vol. 19, Issue 2 https://doi.org/10.1105/tpc.106.048140	journal	February 2007
A gene expression map of Arabidopsis thaliana development Schmid, Markus; Davison, Timothy S.; Henz, Stefan R. Nature Genetics, Vol. 37, Issue 5 https://doi.org/10.1038/ng1543	journal	April 2005
High-resolution metabolic mapping of cell types in plant roots Moussaieff, A.; Rogachev, I.; Brodsky, L. Proceedings of the National Academy of Sciences, Vol. 110, Issue 13 https://doi.org/10.1073/pnas.1302019110	journal	March 2013
An atlas of gene expression from seed to seed through barley development Druka, Arnis; Muehlbauer, Gary; Druka, Ilze Functional & Integrative Genomics, Vol. 6, Issue 3 https://doi.org/10.1007/s10142-006-0025-4	journal	March 2006
Genome-wide atlas of transcription during maize development: Maize gene atlas Sekhon, Rajandeep S.; Lin, Haining; Childs, Kevin L. The Plant Journal, Vol. 66, Issue 4 https://doi.org/10.1111/j.1365‐313X.2011.04527.x	journal	March 2011
Root hair-specific EXPANSIN A7 is required for root hair elongation in Arabidopsis Lin, Changfa; Choi, Hee-Seung; Cho, Hyung-Taeg Molecules and Cells, Vol. 31, Issue 4 https://doi.org/10.1007/s10059-011-0046-2	journal	February 2011
Role of Auxin-Induced Reactive Oxygen Species in Root Gravitropism Joo, Jung Hee; Bae, Yun Soo; Lee, June Seung Plant Physiology, Vol. 126, Issue 3 https://doi.org/10.1104/pp.126.3.1055	journal	July 2001
Hybridization interactions between probesets in short oligo microarrays lead to spurious correlations Okoniewski, Michał J.; Miller, Crispin J. BMC Bioinformatics, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2105-7-276	journal	June 2006
The SCARECROW Gene Regulates an Asymmetric Cell Division That Is Essential for Generating the Radial Organization of the Arabidopsis Root Di Laurenzio, Laura; Wysocka-Diller, Joanna; Malamy, Jocelyn E. Cell, Vol. 86, Issue 3 https://doi.org/10.1016/S0092‐8674(00)80115‐4	journal	August 1996
Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot Wysocka-Diller, J. W.; Helariutta, Y.; Fukaki, H. Development, Vol. 127, Issue 3 https://doi.org/10.1242/dev.127.3.595	journal	February 2000
Transcriptional profiling of two contrasting genotypes uncovers molecular mechanisms underlying salt tolerance in alfalfa Kaundal, Rakesh; Duhan, Naveen; Acharya, Biswa R. Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-84461-w	journal	March 2021

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Maize leaf PPDK regulatory protein isoform-2 is specific to bundle sheath chloroplasts and paradoxically lacks a Pi-dependent PPDK activation activity Chastain, Chris J.; Baird, Lisa M.; Walker, Mitchell T. Journal of Experimental Botany, Vol. 69, Issue 5 https://doi.org/10.1093/jxb/erx471	journal	December 2017
Shifting the limits in wheat research and breeding using a fully annotated reference genome Appels, Rudi; Eversole, Kellye; Stein, Nils Science, Vol. 361, Issue 6403 https://doi.org/10.1126/science.aar7191	journal	August 2018
Identification and characterization of genes encoding the nuclear envelope LINC complex in the monocot species Zea mays Gumber, Hardeep K.; McKenna, Joseph F.; Estrada, Amado L. Journal of Cell Science, Vol. 132, Issue 3 https://doi.org/10.1242/jcs.221390	journal	January 2019
A maize cytochrome b–c1 complex subunit protein ZmQCR7 controls variation in the hypersensitive response He, Yijian; Kim, Saet-Byul; Balint-Kurti, Peter Planta, Vol. 249, Issue 5 https://doi.org/10.1007/s00425-019-03092-8	journal	January 2019
Quantitative Genetic Analysis of the Maize Leaf Microbiome Wallace, Jason G.; Kremling, Karl A.; Buckler, Edward S. bioRxiv https://doi.org/10.1101/268532	posted_content	February 2018
Proteases Underground: Analysis of the Maize Root Apoplast Identifies Organ Specific Papain-Like Cysteine Protease Activity Schulze Hüynck, Jan; Kaschani, Farnusch; van der Linde, Karina Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00473	journal	April 2019
Control of Maize Vegetative and Reproductive Development, Fertility, and rRNAs Silencing by HISTONE DEACETYLASE 108 Forestan, Cristian; Farinati, Silvia; Rouster, Jacques Genetics, Vol. 208, Issue 4 https://doi.org/10.1534/genetics.117.300625	journal	January 2018
Dynamic Patterns of Transcript Abundance of Transposable Element Families in Maize Anderson, Sarah N.; Stitzer, Michelle C.; Zhou, Peng G3: Genes\|Genomes\|Genetics, Vol. 9, Issue 11 https://doi.org/10.1534/g3.119.400431	journal	September 2019
Besides and beyond Flowering: Other Roles of EuAP2 Genes in Plant Development Solomon, Charles U.; Drea, Sinéad Genes, Vol. 10, Issue 12 https://doi.org/10.3390/genes10120994	journal	December 2019
Maize nested introgression library provides evidence for the involvement of liguleless1 in resistance to northern leaf blight Kolkman, Judith M.; Strable, Josh; Harline, Kate G3: Genes\|Genomes\|Genetics https://doi.org/10.1101/818518	posted_content	October 2019
Drought-tolerant and drought-sensitive genotypes of maize (Zea mays L.) differ in contents of endogenous brassinosteroids and their drought-induced changes Tůmová, Lenka; Tarkowská, Danuše; Řehořová, Kateřina PLOS ONE, Vol. 13, Issue 5 https://doi.org/10.1371/journal.pone.0197870	journal	May 2018
Functions of maize genes encoding pyruvate phosphate dikinase in developing endosperm Lappe, Ryan R.; Baier, John W.; Boehlein, Susan K. Proceedings of the National Academy of Sciences, Vol. 115, Issue 1 https://doi.org/10.1073/pnas.1715668115	journal	December 2017
Interpretation of differential gene expression results of RNA-seq data: review and integration McDermaid, Adam; Monier, Brandon; Zhao, Jing Briefings in Bioinformatics, Vol. 20, Issue 6 https://doi.org/10.1093/bib/bby067	journal	August 2018
Dicer-like 5 deficiency confers temperature-sensitive male sterility in maize Teng, Chong; Zhang, Han; Hammond, Reza Nature Communications https://doi.org/10.1101/498410	posted_content	May 2020
Gene Expression Maps in Plants: Current State and Prospects Klepikova, Anna V.; Penin, Aleksey A. Plants, Vol. 8, Issue 9 https://doi.org/10.3390/plants8090309	journal	August 2019
Discovering and Constructing ceRNA-miRNA-Target Gene Regulatory Networks during Anther Development in Maize Li, Ziwen; An, Xueli; Zhu, Taotao International Journal of Molecular Sciences, Vol. 20, Issue 14 https://doi.org/10.3390/ijms20143480	journal	July 2019
Cloning and characterization of BES1/BZR1 transcription factor genes in maize Yu, Haoqiang; Feng, Wenqi; Sun, Fuai Plant Growth Regulation, Vol. 86, Issue 2 https://doi.org/10.1007/s10725-018-0424-2	journal	July 2018
The limited role of differential fractionation in genome content variation and function in maize ( Zea mays L .) inbred lines Brohammer, Alex B.; Kono, Thomas J. Y.; Springer, Nathan M. The Plant Journal, Vol. 93, Issue 1 https://doi.org/10.1111/tpj.13765	journal	December 2017
The genetic architecture of amylose biosynthesis in maize kernel Li, Changsheng; Huang, Yongcai; Huang, Ruidong Plant Biotechnology Journal, Vol. 16, Issue 2 https://doi.org/10.1111/pbi.12821	journal	September 2017
Genome-wide identification, systematic analysis and characterization of SRO family genes in maize (Zea mays L.) Jiang, Huanhuan; Xiao, Yao; Zhu, Suwen Acta Physiologiae Plantarum, Vol. 40, Issue 10 https://doi.org/10.1007/s11738-018-2738-0	journal	September 2018
Genome-wide association study of maize plant architecture using F1 populations Zhao, Yang; Wang, Hengsheng; Bo, Chen Plant Molecular Biology, Vol. 99, Issue 1-2 https://doi.org/10.1007/s11103-018-0797-7	journal	December 2018
Transcriptome analysis of maize seedling roots in response to nitrogen-, phosphorus-, and potassium deficiency Ma, Nana; Dong, Lina; Lü, Wei Plant and Soil, Vol. 447, Issue 1-2 https://doi.org/10.1007/s11104-019-04385-3	journal	January 2020
An updated gene atlas for maize reveals organ‐specific and stress‐induced genes Hoopes, Genevieve M.; Hamilton, John P.; Wood, Joshua C. The Plant Journal, Vol. 97, Issue 6 https://doi.org/10.1111/tpj.14184	journal	January 2019
Genomic-Enabled Prediction Kernel Models with Random Intercepts for Multi-environment Trials Cuevas, Jaime; Granato, Italo; Fritsche-Neto, Roberto G3: Genes\|Genomes\|Genetics, Vol. 8, Issue 4 https://doi.org/10.1534/g3.117.300454	journal	February 2018
MLKS2 is an ARM domain and F-actin-associated KASH protein that functions in stomatal complex development and meiotic chromosome segregation Gumber, Hardeep K.; McKenna, Joseph F.; Tolmie, Andrea F. Nucleus, Vol. 10, Issue 1 https://doi.org/10.1080/19491034.2019.1629795	journal	January 2019
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
A calcium-dependent protein kinase, ZmCPK32, specifically expressed in maize pollen to regulate pollen tube growth Li, Jie; Li, Yihao; Deng, Yanling PLOS ONE, Vol. 13, Issue 5 https://doi.org/10.1371/journal.pone.0195787	journal	May 2018
Transcriptomic response to divergent selection for flowering times reveals convergence and key players of the underlying gene regulatory network Tenaillon, Maud I.; Seddiki, Khawla; Mollion, Maeva https://doi.org/10.1101/461947	preprint	June 2019
ZmRAP2.7, an AP2 Transcription Factor, Is Involved in Maize Brace Roots Development Li, Jieping; Chen, Fanjun; Li, Yanqing Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00820	journal	July 2019
A comparative transcriptional landscape of maize and sorghum obtained by single-molecule sequencing Wang, Bo; Regulski, Michael; Tseng, Elizabeth Genome Research, Vol. 28, Issue 6 https://doi.org/10.1101/gr.227462.117	journal	April 2018
Evolutionarily informed deep learning methods for predicting relative transcript abundance from DNA sequence Washburn, Jacob D.; Mejia-Guerra, Maria Katherine; Ramstein, Guillaume Proceedings of the National Academy of Sciences, Vol. 116, Issue 12 https://doi.org/10.1073/pnas.1814551116	journal	March 2019
A Comprehensive Analysis of Alternative Splicing in Paleopolyploid Maize Mei, Wenbin; Liu, Sanzhen; Schnable, James C. Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00694	journal	May 2017
Expansion and diversification of the gibberellin receptor GIBBERELLIN INSENSITIVE DWARF1 (GID1) family in land plants Gazara, Rajesh K.; Moharana, Kanhu C.; Bellieny-Rabelo, Daniel Plant Molecular Biology, Vol. 97, Issue 4-5 https://doi.org/10.1007/s11103-018-0750-9	journal	June 2018
MATRILINEAL, a sperm-specific phospholipase, triggers maize haploid induction Kelliher, Timothy; Starr, Dakota; Richbourg, Lee Nature, Vol. 542, Issue 7639 https://doi.org/10.1038/nature20827	journal	January 2017
The RNA-Seq-based high resolution gene expression atlas of chickpea ( Cicer arietinum L.) reveals dynamic spatio-temporal changes associated with growth and development: RNA-Seq based chickpea gene expression atlas Kudapa, Himabindu; Garg, Vanika; Chitikineni, Annapurna Plant, Cell & Environment https://doi.org/10.1111/pce.13210	journal	May 2018
Integration of quantitated expression estimates from polyA-selected and rRNA-depleted RNA-seq libraries Bush, Stephen J.; McCulloch, Mary E. B.; Summers, Kim M. BMC Bioinformatics, Vol. 18, Issue 1 https://doi.org/10.1186/s12859-017-1714-9	journal	June 2017
Using multiple reference genomes to identify and resolve annotation inconsistencies Monnahan, Patrick J.; Michno, Jean-Michel; O’Connor, Christine BMC Genomics, Vol. 21, Issue 1 https://doi.org/10.1186/s12864-020-6696-8	journal	April 2020
Genome-wide analysis of the basic Helix-Loop-Helix (bHLH) transcription factor family in maize Zhang, Tingting; Lv, Wei; Zhang, Haisen BMC Plant Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12870-018-1441-z	journal	October 2018
Utilization of Tissue Ploidy Level Variation in de Novo Transcriptome Assembly of Pinus sylvestris Ojeda, Dario I.; Mattila, Tiina M.; Ruttink, Tom G3: Genes\|Genomes\|Genetics, Vol. 9, Issue 10 https://doi.org/10.1534/g3.119.400357	journal	August 2019
Besides and Beyond Flowering: Other Roles of euAP2 Genes in Plant Development Solomon, Charles U.; Drea, Sinead Preprints.org https://doi.org/10.20944/preprints201901.0035.v1	posted_content	January 2019
Dynamic patterns of transcript abundance of transposable element families in maize Anderson, Sarah N.; Stitzer, Michelle C.; Zhou, Peng G3: Genes\|Genomes\|Genetics https://doi.org/10.1101/668558	posted_content	June 2019
Besides and Beyond Flowering: Other Roles of euAP2 Genes in Plant Development Solomon, Charles U.; Drea, Sinead Preprints.org https://doi.org/10.20944/preprints201901.0035.v2	posted_content	January 2019
Dicer-like 5 deficiency confers temperature-sensitive male sterility in maize Teng, Chong; Zhang, Han; Hammond, Reza Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16634-6	journal	June 2020
Stress-induced and epigenetic-mediated maize transcriptome regulation study by means of transcriptome reannotation and differential expression analysis Forestan, Cristian; Aiese Cigliano, Riccardo; Farinati, Silvia Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep30446	journal	July 2016
Expansion and diversification of the gibberellin receptor GIBBERELLIN INSENSITIVE DWARF1 (GID1) family in land plants Gazara, Rajesh K.; Moharana, Kanhu C.; Bellieny-Rabelo, Daniel bioRxiv https://doi.org/10.1101/221937	posted_content	November 2017
MLKS2 is an ARM domain and F-actin-associated KASH protein that functions in stomatal complex development and meiotic chromosome segregation Gumber, Hardeep K.; McKenna, Joseph F.; Tolmie, Andrea F. Nucleus https://doi.org/10.1101/609594	posted_content	May 2019
Characterization of the maize lipoxygenase gene family in relation to aflatoxin accumulation resistance Ogunola, Oluwaseun F.; Hawkins, Leigh K.; Mylroie, Erik PLOS ONE, Vol. 12, Issue 7 https://doi.org/10.1371/journal.pone.0181265	journal	July 2017
Genetic Diversity and Molecular Evolution of a Violaxanthin De-epoxidase Gene in Maize Xu, Jing; Li, Zhigang; Yang, Haorui Frontiers in Genetics, Vol. 7 https://doi.org/10.3389/fgene.2016.00131	journal	July 2016
Structural Characterization of Maize SIRK1 Kinase Domain Reveals an Unusual Architecture of the Activation Segment Aquino, Bruno; Couñago, Rafael M.; Verza, Natalia Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00852	journal	May 2017
Comparative Genomics, Whole-Genome Re-sequencing and Expression Profile Analysis of Nucleobase:Cation Symporter 2 (NCS2) Genes in Maize Chai, Wenbo; Peng, Xiaojian; Liu, Bin Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00856	journal	June 2018
Cell Type-Specific Transcriptomics of Lateral Root Formation and Plasticity Kortz, Annika; Hochholdinger, Frank; Yu, Peng Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00021	journal	February 2019
Seed Weight as a Covariate in Association and Prediction Studies for Biomass Traits in Maize Seedlings Galic, Vlatko; Mazur, Maja; Brkic, Andrija Plants, Vol. 9, Issue 2 https://doi.org/10.3390/plants9020275	journal	February 2020
Genome-wide identification of ZmHMAs and association of natural variation in ZmHMA2 and ZmHMA3 with leaf cadmium accumulation in maize Cao, Yanhua; Zhao, Xiongwei; Liu, Yajuan PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7877	journal	October 2019

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