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

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

Journal Article · Tue Dec 29 23:00:00 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); Univ Wisconsin, Dept Agron, 1575 Linden Dr, Madison, WI 53706 USA
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.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: FC02-07ER64494

OSTI ID:: 1363961

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

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

Country of Publication:: United States

Language:: English

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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
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Genome-wide association analysis of stalk biomass and anatomical traits in maize Mazaheri, Mona; Heckwolf, Marlies; Vaillancourt, Brieanne BMC Plant Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12870-019-1653-x	journal	January 2019
A maize polygalacturonase functions as a suppressor of programmed cell death in plants He, Yijian; Karre, Shailesh; Johal, Gurmukh S. BMC Plant Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12870-019-1897-5	journal	July 2019
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
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
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, Sinead Preprints.org https://doi.org/10.20944/preprints201901.0035.v2	posted_content	January 2019
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
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
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
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
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
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
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
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
Additional file 1 of Transcriptomic and genome-wide association study reveal long noncoding RNAs responding to nitrogen deficiency in maize Ma, Peng; Zhang, Xiao; Luo, Bowen figshare https://doi.org/10.6084/m9.figshare.13979336	dataset	January 2021
Additional file 2 of Transcriptomic and genome-wide association study reveal long noncoding RNAs responding to nitrogen deficiency in maize Ma, Peng; Zhang, Xiao; Luo, Bowen figshare https://doi.org/10.6084/m9.figshare.13979342.v1	dataset	January 2021
Additional file 2 of Transcriptome analysis revealed the regulation of gibberellin and the establishment of photosynthetic system promote rapid seed germination and early growth of seedling in pearl millet Wu, Bingchao; Sun, Min; Zhang, Huan figshare https://doi.org/10.6084/m9.figshare.14399481	dataset	January 2021
Additional file 10 of Chromosome-level genome assembly of a regenerable maize inbred line A188 Lin, Guifang; He, Cheng; Zheng, Jun figshare https://doi.org/10.6084/m9.figshare.14759640.v1	dataset	January 2021
Additional file 11 of Chromosome-level genome assembly of a regenerable maize inbred line A188 Lin, Guifang; He, Cheng; Zheng, Jun figshare https://doi.org/10.6084/m9.figshare.14759643.v1	dataset	January 2021
Additional file 2 of Chromosome-level genome assembly of a regenerable maize inbred line A188 Lin, Guifang; He, Cheng; Zheng, Jun figshare https://doi.org/10.6084/m9.figshare.14759655.v1	dataset	January 2021
Additional file 3 of Chromosome-level genome assembly of a regenerable maize inbred line A188 Lin, Guifang; He, Cheng; Zheng, Jun figshare https://doi.org/10.6084/m9.figshare.14759658.v1	dataset	January 2021
Additional file 4 of Chromosome-level genome assembly of a regenerable maize inbred line A188 Lin, Guifang; He, Cheng; Zheng, Jun figshare https://doi.org/10.6084/m9.figshare.14759661	dataset	January 2021
Additional file 5 of Chromosome-level genome assembly of a regenerable maize inbred line A188 Lin, Guifang; He, Cheng; Zheng, Jun figshare https://doi.org/10.6084/m9.figshare.14759664.v1	dataset	January 2021
Additional file 6 of Chromosome-level genome assembly of a regenerable maize inbred line A188 Lin, Guifang; He, Cheng; Zheng, Jun figshare https://doi.org/10.6084/m9.figshare.14759667	dataset	January 2021
Additional file 8 of Chromosome-level genome assembly of a regenerable maize inbred line A188 Lin, Guifang; He, Cheng; Zheng, Jun figshare https://doi.org/10.6084/m9.figshare.14759673.v1	dataset	January 2021
Additional file 9 of Chromosome-level genome assembly of a regenerable maize inbred line A188 Lin, Guifang; He, Cheng; Zheng, Jun figshare https://doi.org/10.6084/m9.figshare.14759679	dataset	January 2021
Additional file 1 of Genome-wide association screening and verification of potential genes associated with root architectural traits in maize (Zea mays L.) at multiple seedling stages Moussa, Abdourazak Alio; Mandozai, Ajmal; Jin, Yukun figshare https://doi.org/10.6084/m9.figshare.15026746.v1	dataset	January 2021
Additional file 2 of Genome-wide association screening and verification of potential genes associated with root architectural traits in maize (Zea mays L.) at multiple seedling stages Moussa, Abdourazak Alio; Mandozai, Ajmal; Jin, Yukun figshare https://doi.org/10.6084/m9.figshare.15026749.v1	dataset	January 2021
Additional file 4 of Genome-wide association screening and verification of potential genes associated with root architectural traits in maize (Zea mays L.) at multiple seedling stages Moussa, Abdourazak Alio; Mandozai, Ajmal; Jin, Yukun figshare https://doi.org/10.6084/m9.figshare.15026755	dataset	January 2021
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
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
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
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
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
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
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
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
A plastidial pantoate transporter with a potential role in pantothenate synthesis Huang, Lili; Pyc, Michal; Alseekh, Saleh Biochemical Journal, Vol. 475, Issue 4 https://doi.org/10.1042/bcj20170883	journal	February 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
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
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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
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
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
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
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. https://doi.org/10.1101/343939	posted_content	November 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
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
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
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
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
qKW9 encodes a pentatricopeptide repeat protein affecting photosynthesis and grain filling in maize Huang, Juan; Lu, Gang; Liu, Lei https://doi.org/10.1101/847145	posted_content	November 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
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
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
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
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
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
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
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
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
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
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
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
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
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

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