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A gene expression map of Arabidopsis thaliana development

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Abstract

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.

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Figure 1: Expressed genes, expression dynamics and marker genes.
Figure 2: Global expression trends.
Figure 3: Sliding-window analysis of coexpression and expression levels along chromosome I.
Figure 4: Expression levels of Gene Ontology categories and relationship between different measures of expression.
Figure 5: Coexpression of genes encoding protein complexes and gene families.

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Change history

  • 23 May 2005

    Replaced Table 4

  • 02 June 2005

    Replaced Table 2

Notes

  1. 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.

  2. 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.

References

  1. The Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815 (2000).

  2. Yamada, K. et al. Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 302, 842–846 (2003).

    Article  CAS  PubMed  Google Scholar 

  3. Birnbaum, K. et al. A gene expression map of the Arabidopsis root. Science 302, 1956–1960 (2003).

    Article  CAS  PubMed  Google Scholar 

  4. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Lippman, Z. & Martienssen, R. The role of RNA interference in heterochromatic silencing. Nature 431, 364–370 (2004).

    Article  CAS  PubMed  Google Scholar 

  7. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Spellman, P.T. & Rubin, G.M. Evidence for large domains of similarly expressed genes in the Drosophila genome. J. Biol. 1, 5 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  9. 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).

    Article  CAS  PubMed  Google Scholar 

  10. 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).

    Article  CAS  PubMed  Google Scholar 

  11. Williams, E.J. & Bowles, D.J. Coexpression of neighboring genes in the genome of Arabidopsis thaliana. Genome Res. 14, 1060–1067 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Copenhaver, G.P. et al. Genetic definition and sequence analysis of Arabidopsis centromeres. Science 286, 2468–2474 (1999).

    Article  CAS  PubMed  Google Scholar 

  14. 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).

    Article  CAS  PubMed  Google Scholar 

  15. 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).

    Article  CAS  PubMed  Google Scholar 

  16. 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).

    Article  CAS  PubMed  Google Scholar 

  17. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Jansen, R., Greenbaum, D. & Gerstein, M. Relating whole-genome expression data with protein-protein interactions. Genome Res. 12, 37–46 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Force, A. et al. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531–1545 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Blanc, G. & Wolfe, K.H. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16, 1679–1691 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. 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).

    Article  CAS  PubMed  Google Scholar 

  23. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Eulgem, T., Rushton, P.J., Robatzek, S. & Somssich, I.E. The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5, 199–206 (2000).

    Article  CAS  PubMed  Google Scholar 

  25. 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).

    Article  CAS  PubMed  Google Scholar 

  26. Tornow, S. & Mewes, H.W. Functional modules by relating protein interaction networks and gene expression. Nucleic Acids Res. 31, 6283–6289 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Allemeersch, J. et al. Benchmarking the CATMA microarray. A novel tool for Arabidopsis transcriptome analysis. Plant Physiol. 137, 588–601 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. 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).

    Google Scholar 

  29. Schölkopf, B., Smola, A.J. & Müller, K.-R. Nonlinear component analysis as a kernel eigenvalue problem. Neural Comput. 10, 1299–1319 (1998).

    Article  Google Scholar 

  30. Hising, T., Attoor, S. & Dougherty, E. Relation between permutation-test P values and classifier error estimates. Machine Learning 52, 11–30 (2004).

    Article  Google Scholar 

Download references

Acknowledgements

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.

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Correspondence to Detlef Weigel.

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Supplementary information

Supplementary Fig. 1

Assessment of replicate quality for 79 samples probed in triplicate. (PDF 519 kb)

Supplementary Fig. 2

Examples of gene expression profiles. (PDF 911 kb)

Supplementary Fig. 3

Principal Component Analysis of entire organs and tissues and sorted root cells. (PDF 418 kb)

Supplementary Fig. 4

Fraction of genes detected in each sample. (PDF 1083 kb)

Supplementary Fig. 5

Sliding-window analysis of co-expression along each chromosome. (PDF 1235 kb)

Supplementary Fig. 6

Sliding-window analysis of co-expression using different window sizes. (PDF 1223 kb)

Supplementary Fig. 7

Genes encoding the PF02713 (DUF220) protein domain form a hot-spot of co-expression on chromosome I. (PDF 1003 kb)

Supplementary Fig. 8

Sliding window analysis of averaged expression levels along each chromosome. (PDF 796 kb)

Supplementary Fig. 9

Extent of correlated expression among duplicated genes. (PDF 1042 kb)

Supplementary Fig. 10

Hierarchical clustering of genes encoding WRKY and MADS domain transcription factors. (PDF 1555 kb)

Supplementary Table 1

Sample descriptions and growth conditions. (PDF 64 kb)

Supplementary Table 2

Summary statistics of replicate quality. (PDF 53 kb)

Supplementary Table 3

Significance of differences in combined expression levels along each chromosome. (PDF 41 kb)

Supplementary Table 4

Coexpression of gene families. (PDF 84 kb)

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Schmid, M., Davison, T., Henz, S. et al. A gene expression map of Arabidopsis thaliana development. Nat Genet 37, 501–506 (2005). https://doi.org/10.1038/ng1543

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