Regulatory regions of plant genes tend to be more compact than those of animal genes, but the complement of transcription factors encoded in plant genomes is as large or larger than that found in those of animals1. Plants therefore provide an opportunity to study how transcriptional programs control multicellular development. We analyzed global gene expression during development of the reference plant Arabidopsis thaliana in samples covering many stages, from embryogenesis to senescence, and diverse organs. Here, we provide a first analysis of this data set, which is part of the AtGenExpress expression atlas. We observed that the expression levels of transcription factor genes and signal transduction components are similar to those of metabolic genes. Examining the expression patterns of large gene families, we found that they are often more similar than would be expected by chance, indicating that many gene families have been co-opted for specific developmental processes.
Subscribe to Journal
Get full journal access for 1 year
only $18.75 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
NOTES: In the version of Supplementary Table 4 online that originally accompanied this article, the number of gene families appeared smaller than was truly the case. This error has been corrected online.
NOTES: In the version of Supplementary Table 2 online that originally accompanied this article, the values for the A/C pairs were incorrect. This error has been corrected online.
The Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815 (2000).
Yamada, K. et al. Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 302, 842–846 (2003).
Birnbaum, K. et al. A gene expression map of the Arabidopsis root. Science 302, 1956–1960 (2003).
Becker, J.D., Boavida, L.C., Carneiro, J., Haury, M. & Feijo, J.A. Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome. Plant Physiol. 133, 713–725 (2003).
Wellmer, F., Riechmann, J.L., Alves-Ferreira, M. & Meyerowitz, E.M. Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell 16, 1314–1326 (2004).
Lippman, Z. & Martienssen, R. The role of RNA interference in heterochromatic silencing. Nature 431, 364–370 (2004).
Gagne, J.M., Downes, B.P., Shiu, S.H., Durski, A.M. & Vierstra, R.D. The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc. Natl. Acad. Sci. USA 99, 11519–11524 (2002).
Spellman, P.T. & Rubin, G.M. Evidence for large domains of similarly expressed genes in the Drosophila genome. J. Biol. 1, 5 (2002).
Cohen, B.A., Mitra, R.D., Hughes, J.D. & Church, G.M. A computational analysis of whole-genome expression data reveals chromosomal domains of gene expression. Nat. Genet. 26, 183–186 (2000).
Lercher, M.J., Urrutia, A.O. & Hurst, L.D. Clustering of housekeeping genes provides a unified model of gene order in the human genome. Nat. Genet. 31, 180–183 (2002).
Williams, E.J. & Bowles, D.J. Coexpression of neighboring genes in the genome of Arabidopsis thaliana. Genome Res. 14, 1060–1067 (2004).
Lercher, M.J., Blumenthal, T. & Hurst, L.D. Coexpression of neighboring genes in Caenorhabditis elegans is mostly due to operons and duplicate genes. Genome Res. 13, 238–243 (2003).
Copenhaver, G.P. et al. Genetic definition and sequence analysis of Arabidopsis centromeres. Science 286, 2468–2474 (1999).
Fransz, P.F. et al. Integrated cytogenetic map of chromosome arm 4S of A. thaliana: structural organization of heterochromatic knob and centromere region. Cell 100, 367–376 (2000).
Czechowski, T., Bari, R.P., Stitt, M., Scheible, W.R. & Udvardi, M.K. Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant J. 38, 366–379 (2004).
Beyer, A., Hollunder, J., Nasheuer, H.P. & Wilhelm, T. Post-transcriptional expression regulation in the yeast Saccharomyces cerevisiae on a genomic scale. Mol. Cell. Proteomics 3, 1083–1092 (2004).
Eisen, M.B., Spellman, P.T., Brown, P.O. & Botstein, D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95, 14863–14868 (1998).
Jansen, R., Greenbaum, D. & Gerstein, M. Relating whole-genome expression data with protein-protein interactions. Genome Res. 12, 37–46 (2002).
Force, A. et al. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531–1545 (1999).
Blanc, G. & Wolfe, K.H. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16, 1679–1691 (2004).
Haberer, G., Hindemitt, T., Meyers, B.C. & Mayer, K.F. Transcriptional similarities, dissimilarities, and conservation of cis-elements in duplicated genes of Arabidopsis. Plant Physiol. 136, 3009–3022 (2004).
Gu, Z., Nicolae, D., Lu, H.H. & Li, W.H. Rapid divergence in expression between duplicate genes inferred from microarray data. Trends Genet. 18, 609–613 (2002).
Huminiecki, L. & Wolfe, K.H. Divergence of spatial gene expression profiles following species-specific gene duplications in human and mouse. Genome Res. 14, 1870–1879 (2004).
Eulgem, T., Rushton, P.J., Robatzek, S. & Somssich, I.E. The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5, 199–206 (2000).
Becker, A. & Theissen, G. The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol. Phylogenet. Evol. 29, 464–489 (2003).
Tornow, S. & Mewes, H.W. Functional modules by relating protein interaction networks and gene expression. Nucleic Acids Res. 31, 6283–6289 (2003).
Allemeersch, J. et al. Benchmarking the CATMA microarray. A novel tool for Arabidopsis transcriptome analysis. Plant Physiol. 137, 588–601 (2005).
Wu, Z., Irizarry, R.A., Gentleman, R., Murillo, F.M. & Spencer, F. A model based background adjustment for oligonucleotide expression arrays. in Dept. of Biostatistics Working Papers, Working Paper 1 (Johns Hopkins University, 2004).
Schölkopf, B., Smola, A.J. & Müller, K.-R. Nonlinear component analysis as a kernel eigenvalue problem. Neural Comput. 10, 1299–1319 (1998).
Hising, T., Attoor, S. & Dougherty, E. Relation between permutation-test P values and classifier error estimates. Machine Learning 52, 11–30 (2004).
We thank F. Mehrtens, B. Weisshaar, R. Heidstra, B. Scheres, M. Yoshikawa, S. Poethig, D. Twell and the CAGE consortium (M. Kuiper, M. Vuylsteke, J.P. Renou, F. Bitton and M. Luijten) for providing RNA samples; P. Benfey and A. Zien for discussion; and K. Bomblies, R. Clark and A. Maizel for comments on the manuscript. This work was supported by the Deutsche Forschungsgemeinschaft through a grant to L. Nover, T. Altmann and D.W. and by the Max Planck Society. D.W. is a director of the Max Planck Institute.
The authors declare no competing financial interests.
Assessment of replicate quality for 79 samples probed in triplicate. (PDF 519 kb)
Examples of gene expression profiles. (PDF 911 kb)
Principal Component Analysis of entire organs and tissues and sorted root cells. (PDF 418 kb)
Fraction of genes detected in each sample. (PDF 1083 kb)
Sliding-window analysis of co-expression along each chromosome. (PDF 1235 kb)
Sliding-window analysis of co-expression using different window sizes. (PDF 1223 kb)
Genes encoding the PF02713 (DUF220) protein domain form a hot-spot of co-expression on chromosome I. (PDF 1003 kb)
Sliding window analysis of averaged expression levels along each chromosome. (PDF 796 kb)
Extent of correlated expression among duplicated genes. (PDF 1042 kb)
Hierarchical clustering of genes encoding WRKY and MADS domain transcription factors. (PDF 1555 kb)
Sample descriptions and growth conditions. (PDF 64 kb)
Summary statistics of replicate quality. (PDF 53 kb)
Significance of differences in combined expression levels along each chromosome. (PDF 41 kb)
Coexpression of gene families. (PDF 84 kb)
About this article
Cite this article
Schmid, M., Davison, T., Henz, S. et al. A gene expression map of Arabidopsis thaliana development. Nat Genet 37, 501–506 (2005) doi:10.1038/ng1543
A CBL-interacting protein kinase AdCIPK5 confers salt and osmotic stress tolerance in transgenic tobacco
Scientific Reports (2020)
Biochimica et Biophysica Acta (BBA) - Bioenergetics (2020)
Non-canonical RNA-directed DNA methylation participates in maternal and environmental control of seed dormancy
Sugar transporters in Fabaceae, featuring SUT MST and SWEET families of the model plant Medicago truncatula and the agricultural crop Pisum sativum
PLOS ONE (2019)
Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication
BMC Evolutionary Biology (2019)