The DOI matches its Crossref record; 77 of the 77 references it cites were found in a registry or an index.
Single-cell RNA sequencing of developing maize ears facilitates functional analysis and trait candidate gene discovery
Open accessAbstract
SUMMARY Crop productivity depends on activity of meristems that produce optimized plant architectures, including that of the maize ear. A comprehensive understanding of development requires insight into the full diversity of cell types and developmental domains, and the gene networks required to specify them. Until now, these were identified primarily by morphology and insights from classical genetics, that are limited by genetic redundancy and pleiotropy. Here, we investigated the transcriptional profiles of 12,525 single cells from developing maize ears. The resulting developmental atlas provides a single-cell RNA sequencing (scRNA-seq) map of an inflorescence. We validated our results by mRNA in situ hybridization and by Fluorescence-Activated Cell Sorting (FACS) RNA-seq, and show how these data may facilitate genetic studies by predicting genetic redundancy, integrating transcriptional networks, and identifying candidate genes associated with crop yield traits.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Trimmomatic: a flexible trimmer for Illumina sequence data
Bolger, A. M., Lohse, M., & Usadel, B. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu170 · Cited by 65,548
Fast and accurate short read alignment with Burrows-Wheeler transform
Li, H., & Durbin, R. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp324 · Cited by 58,607
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709
Self-citationRobinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364
Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y. C., Laslo, P., Cheng, J. X., Murre, C., Singh, H., & Glass, C. K. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.05.004 · Cited by 13,382
Maps of random walks on complex networks reveal community structure
Rosvall, M., & Bergstrom, C. T. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706851105 · Cited by 4,583
McGinnis, C. S., Murrow, L. M., & Gartner, Z. J. (2019) · Cell Systems · doi:10.1016/j.cels.2019.03.003 · Cited by 4,521
Genetic screens in human cells using the CRISPR-Cas9 system
Wang, T., Wei, J. J., Sabatini, D. M., & Lander, E. S. (2014) · Science · doi:10.1126/science.1246981 · Cited by 2,856
McCarthy, D. J., Campbell, K. R., Lun, A. T. L., & Wills, Q. F. (2017) · Bioinformatics · doi:10.1093/bioinformatics/btw777 · Cited by 1,852
A step-by-step workflow for low-level analysis of single-cell RNA-seq data with Bioconductor
Lun, A. T. L., McCarthy, D. J., & Marioni, J. C. (2016) · F1000Research · doi:10.12688/f1000research.9501.2 · Cited by 1,574
Radial Patterning of Arabidopsis Shoots by Class III HD-ZIP and KANADI Genes
Emery, J. F., Floyd, S. K., Alvarez, J., Eshed, Y., Hawker, N. P., Izhaki, A., Baum, S. F., & Bowman, J. L. (2003) · Current Biology · doi:10.1016/j.cub.2003.09.035 · Cited by 1,143
Jamboree, P. I. T. 1. H. C. A., Lun, A. T. L., Riesenfeld, S., Andrews, T., Dao, T. P., Gomes, T., & Marioni, J. C. (2019) · Genome Biology · doi:10.1186/s13059-019-1662-y · Cited by 1,097
Jackson, D., Veit, B., & Hake, S. (1994) · Development · doi:10.1242/dev.120.2.405 · Cited by 754
Self-citationImproved Heritability Estimation from Genome-wide SNPs
Speed, D., Hemani, G., Johnson, M. R., & Balding, D. J. (2012) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2012.10.010 · Cited by 720
Zhong, R., Richardson, E. A., & Ye, Z.-H. (2007) · The Plant Cell · doi:10.1105/tpc.107.053678 · Cited by 683
Single-cell RNA sequencing for the study of development, physiology and disease
Potter, S. S. (2018) · Nature Reviews Nephrology · doi:10.1038/s41581-018-0021-7 · Cited by 622
Denyer, T., Ma, X., Klesen, S., Scacchi, E., Nieselt, K., & Timmermans, M. C. P. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.02.022 · Cited by 608
Integration of omic networks in a developmental atlas of maize
Walley, J. W., Sartor, R. C., Shen, Z., Schmitz, R. J., Wu, K. J., Urich, M. A., Nery, J. R., Smith, L. G., Schnable, J. C., Ecker, J. R., et al. (2016) · Science · doi:10.1126/science.aag1125 · Cited by 484
Self-citationNuccio, M. L., Wu, J., Mowers, R., Zhou, H.-P., Meghji, M., Primavesi, L. F., Paul, M. J., Chen, X., Gao, Y., Haque, E., et al. (2015) · Nature Biotechnology · doi:10.1038/nbt.3277 · Cited by 473
A trehalose metabolic enzyme controls inflorescence architecture in maize
Satoh-Nagasawa, N., Nagasawa, N., Malcomber, S., Sakai, H., & Jackson, D. (2006) · Nature · doi:10.1038/nature04725 · Cited by 459
Self-citationWidespread long-range cis-regulatory elements in the maize genome
Ricci, W. A., Lu, Z., Ji, L., Marand, A. P., Ethridge, C. L., Murphy, N. G., Noshay, J. M., Galli, M., Mejía-Guerra, M. K., Colomé-Tatché, M., et al. (2019) · Nature Plants · doi:10.1038/s41477-019-0547-0 · Cited by 388
Self-citationHandbook of Maize: Its Biology
(2009) · Springer eBooks · doi:10.1007/978-0-387-79418-1 · Cited by 378
Crow, M., Paul, A., Ballouz, S., Huang, Z. J., & Gillis, J. (2018) · Nature Communications · doi:10.1038/s41467-018-03282-0 · Cited by 365
Self-citationThe role of barren stalk1 in the architecture of maize
Gallavotti, A., Zhao, Q., Kyozuka, J., Meeley, R. B., Ritter, M. K., Doebley, J. F., Enrico Pè, M., & Schmidt, R. J. (2004) · Nature · doi:10.1038/nature03148 · Cited by 365
Beyond bulk: a review of single cell transcriptomics methodologies and applications
Kulkarni, A., Anderson, A. G., Merullo, D. P., & Konopka, G. (2019) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2019.03.001 · Cited by 356
Characterization of the Class IV Homeodomain-Leucine Zipper Gene Family in Arabidopsis
Nakamura, M., Katsumata, H., Abe, M., Yabe, N., Komeda, Y., Yamamoto, K. T., & Takahashi, T. (2006) · Plant Physiology · doi:10.1104/pp.106.077388 · Cited by 346
Combining ATAC-seq with nuclei sorting for discovery of cis-regulatory regions in plant genomes
Lu, Z., Hofmeister, B. T., Vollmers, C., DuBois, R. M., & Schmitz, R. J. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkw1179 · Cited by 318
Self-citationUnraveling the KNOTTED1 regulatory network in maize meristems
Bolduc, N., Yilmaz, A., Mejia-Guerra, M. K., Morohashi, K., O'Connor, D., Grotewold, E., & Hake, S. (2012) · Genes & Development · doi:10.1101/gad.193433.112 · Cited by 295
The Control of Spikelet Meristem Identity by the branched silkless1 Gene in Maize
Chuck, G., Muszynski, M., Kellogg, E., Hake, S., & Schmidt, R. J. (2002) · Science · doi:10.1126/science.1076920 · Cited by 289
Plant vascular development: from early specification to differentiation
De Rybel, B., Mähönen, A. P., Helariutta, Y., & Weijers, D. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2015.6 · Cited by 279
Je, B. I., Gruel, J., Lee, Y. K., Bommert, P., Arevalo, E. D., Eveland, A. L., Wu, Q., Goldshmidt, A., Meeley, R., Bartlett, M., et al. (2016) · Nature Genetics · doi:10.1038/ng.3567 · Cited by 264
Self-citationMobile PEAR transcription factors integrate positional cues to prime cambial growth
Miyashima, S., Roszak, P., Sevilem, I., Toyokura, K., Blob, B., Heo, J.-O., Mellor, N., Help-Rinta-Rahko, H., Otero, S., Smet, W., et al. (2019) · Nature · doi:10.1038/s41586-018-0839-y · Cited by 264
Quantitative variation in maize kernel row number is controlled by the FASCIATED EAR2 locus
Bommert, P., Nagasawa, N. S., & Jackson, D. (2013) · Nature Genetics · doi:10.1038/ng.2534 · Cited by 256
Self-citationHuffaker, A., Dafoe, N. J., & Schmelz, E. A. (2011) · Plant Physiology · doi:10.1104/pp.110.166710 · Cited by 222
Chuck, G. S., Brown, P. J., Meeley, R., & Hake, S. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1407401112 · Cited by 211
Architecture of gene regulatory networks controlling flower development in Arabidopsis thaliana
Chen, D., Yan, W., Fu, L.-Y., & Kaufmann, K. (2018) · Nature Communications · doi:10.1038/s41467-018-06772-3 · Cited by 205
Krizek, B. (2009) · Plant Physiology · doi:10.1104/pp.109.141119 · Cited by 202
Funk, V., Kositsup, B., Zhao, C., & Beers, E. P. (2002) · Plant Physiology · doi:10.1104/pp.010514 · Cited by 200
Single-Cell Transcriptomics: A High-Resolution Avenue for Plant Functional Genomics
Rich-Griffin, C., Stechemesser, A., Finch, J., Lucas, E., Ott, S., & Schäfer, P. (2020) · Trends in Plant Science · doi:10.1016/j.tplants.2019.10.008 · Cited by 198
Plantacyanin Plays a Role in Reproduction in Arabidopsis
Dong, J., Kim, S. T., & Lord, E. M. (2005) · Plant Physiology · doi:10.1104/pp.105.063388 · Cited by 186
Ha, C. M., Jun, J. H., Nam, H. G., & Fletcher, J. C. (2007) · The Plant Cell · doi:10.1105/tpc.107.051938 · Cited by 186
Randomized Matrix Decompositions Using R
Erichson, N. B., Voronin, S., Brunton, S. L., & Kutz, J. N. (2019) · Journal of Statistical Software · doi:10.18637/jss.v089.i11 · Cited by 183
Evolution of buffering in a genetic circuit controlling plant stem cell proliferation
Rodriguez-Leal, D., Xu, C., Kwon, C.-T., Soyars, C., Demesa-Arevalo, E., Man, J., Liu, L., Lemmon, Z. H., Jones, D. S., Van Eck, J., et al. (2019) · Nature Genetics · doi:10.1038/s41588-019-0389-8 · Cited by 183
Self-citationA Comprehensive Dataset of Genes with a Loss-of-Function Mutant Phenotype in Arabidopsis
Lloyd, J., & Meinke, D. (2012) · Plant Physiology · doi:10.1104/pp.111.192393 · Cited by 168
Chang, Y.-M., Liu, W.-Y., Shih, A. C.-C., Shen, M.-N., Lu, C.-H., Lu, M.-Y. J., Yang, H.-W., Wang, T.-Y., Chen, S. C.-C., Chen, S. M., et al. (2012) · Plant Physiology · doi:10.1104/pp.112.203810 · Cited by 168
Regulatory modules controlling maize inflorescence architecturePreprint
Eveland, A. L., Goldshmidt, A., Pautler, M., Morohashi, K., Liseron-Monfils, C., Lewis, M. W., Kumari, S., Hiraga, S., Yang, F., Unger‐Wallace, E., et al. (2013) · Genome Research · doi:10.1101/gr.166397.113 · Cited by 160
Self-citationMaize YABBY Genes drooping leaf1 and drooping leaf2 Regulate Plant Architecture
Strable, J., Wallace, J. G., Unger‐Wallace, E., Briggs, S. A., Bradbury, P. J., Buckler, E. S., & Vollbrecht, E. (2017) · The Plant Cell · doi:10.1105/tpc.16.00477 · Cited by 158
Liu, J., Fernie, A. R., & Yan, J. (2019) · Plant Communications · doi:10.1016/j.xplc.2019.100010 · Cited by 143
FASCIATED EAR4 Encodes a bZIP Transcription Factor That Regulates Shoot Meristem Size in Maize
Pautler, M., Eveland, A. L., LaRue, T., Yang, F., Weeks, R., Lunde, C. F., Je, B. I., Meeley, R. B., Komatsu, M., Vollbrecht, E., et al. (2015) · The Plant Cell · doi:10.1105/tpc.114.132506 · Cited by 141
Self-citationCell type boundaries organize plant development
Caggiano, M. P., Yu, X., Bhatia, N., Larsson, A., Ram, H., Ohno, C. K., Sappl, P. G., Meyerowitz, E. M., Jönsson, H., & Heisler, M. G. (2017) · eLife · doi:10.7554/elife.27421 · Cited by 127
Wu, Q., Xu, F., Liu, L., Char, S. N., Ding, Y., Je, B. I., Schmelz, E. A., Yang, B., & Jackson, D. P. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1917577116 · Cited by 125
Self-citationEstablishing leaf polarity: the role of small RNAs and positional signals in the shoot apex
Chitwood, D. H., Guo, M., Nogueira, F. T. S., & Timmermans, M. C. P. (2007) · Development · doi:10.1242/dev.000497 · Cited by 116
Javelle, M., Klein-Cosson, C., Vernoud, V., Boltz, V., Maher, C. G., Timmermans, M. C. P., Depège‐Fargeix, N., & Rogowsky, P. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.182147 · Cited by 116
A Comprehensive Toolkit for Inducible, Cell Type-Specific Gene Expression in Arabidopsis
Schürholz, A.-K., Lopéz-Salmerón, V., Li, Z., Forner, J., Wenzl, C., Gaillochet, C., Augustin, S., Barro, A. V., Fuchs, M., Gebert, M., et al. (2018) · PLANT PHYSIOLOGY · doi:10.1104/pp.18.00463 · Cited by 109
Claeys, H., Lang, S., Xu, X., Satoh‐Nagasawa, N., Eveland, A. L., Goldshmidt, A., Feil, R., Beggs, G. A., Sakai, H., Brennan, R. G., et al. (2019) · Nature Plants · doi:10.1038/s41477-019-0394-z · Cited by 99
Self-citationYasui, Y., Mukougawa, K., Uemoto, M., Yokofuji, A., Suzuri, R., Nishitani, A., & Kohchi, T. (2012) · The Plant Cell · doi:10.1105/tpc.112.101915 · Cited by 96
Ontogeny of the Maize Shoot Apical Meristem
Takacs, E. M., Li, J., Du, C., Ponnala, L., Janick‐Buckner, D., Yu, J., Muehlbauer, G. J., Schnable, P. S., Timmermans, M. C. P., Sun, Q., et al. (2012) · The Plant Cell · doi:10.1105/tpc.112.099614 · Cited by 82
Evidence of selection at the ramosa1 locus during maize domestication
Sigmon, B., & Vollbrecht, E. (2010) · Molecular Ecology · doi:10.1111/j.1365-294x.2010.04562.x · Cited by 75
Irish, E. E. (1997) · American Journal of Botany · doi:10.2307/2446611 · Cited by 75
EGAD: ultra-fast functional analysis of gene networks
Ballouz, S., Weber, M., Pavlidis, P., & Gillis, J. (2017) · Bioinformatics · doi:10.1093/bioinformatics/btw695 · Cited by 74
Self-citationDivergence in function and expression of the NOD26-like intrinsic proteins in plants
Liu, Q., Wang, H., Zhang, Z., Wu, J., Feng, Y., & Zhu, Z. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-313 · Cited by 73
A high-resolution gene expression atlas links dedicated meristem genes to key architectural traitsPreprint
Knauer, S., Javelle, M., Li, L., Li, X., Ma, X., Wimalanathan, K., Kumari, S., Johnston, R., Leiboff, S., Meeley, R. B., et al. (2019) · Genome Research · doi:10.1101/gr.250878.119 · Cited by 73
Self-citationDu, Y., Liu, L., Peng, Y., Li, M., Li, Y., Liu, D., Li, X., & Zhang, Z. (2020) · PLoS Genetics · doi:10.1371/journal.pgen.1008764 · Cited by 69
Self-citationmyo-Inositol-1-phosphate Synthase Is Required for Polar Auxin Transport and Organ Development
Chen, H., & Xiong, L. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.123661 · Cited by 65
The regulatory landscape of early maize inflorescence development
Parvathaneni, R. K., Bertolini, E., Shamimuzzaman, M., Vera, D. L., Lung, P.-Y., Rice, B. R., Zhang, J., Brown, P. J., Lipka, A. E., Bass, H. W., et al. (2020) · Genome biology · doi:10.1186/s13059-020-02070-8 · Cited by 62
Self-citationComparative analysis of binding patterns of MADS-domain proteins in Arabidopsis thaliana
Aerts, N., de Bruijn, S., van Mourik, H., Angenent, G. C., & van Dijk, A. D. J. (2018) · BMC Plant Biology · doi:10.1186/s12870-018-1348-8 · Cited by 59
Development of the Inflorescences
Vollbrecht, E., & Schmidt, R. J. (2009) · Springer eBooks · doi:10.1007/978-0-387-79418-1_2 · Cited by 58
Transcriptional switch for programmed cell death in pith parenchyma of sorghum stems
Fujimoto, M., Sazuka, T., Oda, Y., Kawahigashi, H., Wu, J., Takanashi, H., Ohnishi, T., Yoneda, J., Ishimori, M., Kajiya‐Kanegae, H., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1807501115 · Cited by 56
Bartlett, M. E., Williams, S. K., Taylor, Z., DeBlasio, S. L., Goldshmidt, A., Hall, D. H., Schmidt, R. J., Jackson, D. P., & Whipple, C. (2015) · The Plant Cell · doi:10.1105/tpc.15.00679 · Cited by 55
Self-citationPscB: A Browser to Explore Plant Single Cell RNA-Sequencing Data Sets
Ma, X., Denyer, T., & Timmermans, M. C. P. (2020) · PLANT PHYSIOLOGY · doi:10.1104/pp.20.00250 · Cited by 50
Rice, B. R., Fernandes, S. B., & Lipka, A. E. (2020) · Plant and Cell Physiology · doi:10.1093/pcp/pcaa039 · Cited by 47
Self-citationHorváth, E., Bela, K., Holinka, B., Riyazuddin, R., Gallé, Á., Hajnal, Á. B., Hurton, Á., Fehér, A., & Csiszár, J. (2019) · Plant Science · doi:10.1016/j.plantsci.2019.02.005 · Cited by 42
CoCoCoNet: conserved and comparative co-expression across a diverse set of species
Lee, J., Shah, M., Ballouz, S., Crow, M., & Gillis, J. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa348 · Cited by 40
Self-citationGuo, P., Zheng, Y., Peng, D., Liu, L., Dai, L., Chen, C., & Wáng, B. (2018) · Scientific Reports · doi:10.1038/s41598-018-28953-2 · Cited by 27
Self-citationelPrep: High-Performance Preparation of Sequence Alignment/Map Files for Variant Calling
Herzeel, C., Costanza, P., Decap, D., Fostier, J., & Reumers, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0132868 · Cited by 25
Arabidopsis RanBP2-Type Zinc Finger Proteins Related to Chloroplast RNA Editing Factor OZ1
Gipson, A. B., Giloteaux, L., Hanson, M. R., & Bentolila, S. (2020) · Plants · doi:10.3390/plants9030307 · Cited by 10
Management, Analyses, and Distribution of the MaizeCODE Data on the Cloud
Wang, L., Lu, Z., delaBastide, M., Buren, P. V., Wang, X., Ghiban, C., Regulski, M., Drenkow, J., Xu, X., Ortiz‐Ramírez, C., et al. (2020) · Frontiers in Plant Science · doi:10.3389/fpls.2020.00289 · Cited by 5
Self-citation
Metadata
- Authors
- Xu, X., Crow, M., Rice, B. R., Li, F., Harris, B., Liu, L., Demesa-Arevalo, E., Lu, Z., Wang, L., Fox, N., Wang, X., Drenkow, J., Luo, A., Char, S. N., Yang, B., Sylvester, A. W., Gingeras, T. R., Schmitz, R. J., Ware, D., Lipka, A. E., Gillis, J., & Jackson, D.
- Venue
- Developmental Cell
- Publisher
- Elsevier BV
- Published
- 2021-02
- Volume
- 56
- Issue
- 4
- Pages
- 557-568.e6
- ISSN
- 1534-5807 (ISSN-L)
- OpenAlex
- W3120987247
- Cited by
- 264
- References
- 77
- FWCI
- 12.75
- Type
- journal article
- Language
- en
- Open access
- bronze
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.
