A transcriptome atlas of rice cell types uncovers cellular, functional and developmental hierarchies (original) (raw)

Nature Genetics volume 41, pages 258–263 (2009) Cite this article

Abstract

The functions of the plant body rely on interactions among distinct and nonequivalent cell types. The comparison of transcriptomes from different cell types should expose the transcriptional networks that underlie cellular attributes and contributions. Using laser microdissection and microarray profiling, we have produced a cell type transcriptome atlas that includes 40 cell types from rice (Oryza sativa) shoot, root and germinating seed at several developmental stages, providing patterns of cell specificity for individual genes and gene classes. Cell type comparisons uncovered previously unrecognized properties, including cell-specific promoter motifs and coexpressed cognate binding factor candidates, interaction partner candidates and hormone response centers. We inferred developmental regulatory hierarchies of gene expression in specific cell types by comparison of several stages within root, shoot and embryo.

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Figure 1: Global patterns of cellular gene expression.

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Figure 2: Cell-specific transcripts and selected metabolic pathways.

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Figure 3: Cellular distributions of transcripts from selected hormone-related genes.

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Figure 4: Identification of candidate cis and trans transcriptional control cognate partners on the basis of cellular coexpression.

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References

  1. Yu, H., Xia, Y., Trifonov, V. & Gerstein, M. Design principles of molecular networks revealed by global comparisons and composite motifs. Genome Biol. 7, R55 (2006).
    Article Google Scholar
  2. Birnbaum, K. et al. A gene expression map of the Arabidopsis root. Science 302, 1956–1960 (2003).
    Article CAS Google Scholar
  3. Brady, S.M. et al. A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318, 801–806 (2007).
    Article CAS Google Scholar
  4. Nelson, T., Gandotra, N. & Tausta, S.L. Plant cell types: reporting and sampling with new technologies. Curr. Opin. Plant Biol. 11, 567–573 (2008).
    Article CAS Google Scholar
  5. Nelson, T., Tausta, S.L., Gandotra, N. & Liu, T. Laser microdissection of plant tissue: what you see is what you get. Annu. Rev. Plant Biol. 57, 181–201 (2006).
    Article CAS Google Scholar
  6. Ishiwatari, Y. et al. Rice phloem thioredoxin h has the capacity to mediate its own cell-to-cell transport through plasmodesmata. Planta 205, 12–22 (1998).
    Article CAS Google Scholar
  7. Carland, F.M. & Nelson, T. Cotyledon vascular pattern2-mediated inositol (1,4,5) triphosphate signal transduction is essential for closed venation patterns of Arabidopsis foliar organs. Plant Cell 16, 1263–1275 (2004).
    Article CAS Google Scholar
  8. Petricka, J.J. & Nelson, T.M. Arabidopsis nucleolin affects plant development and patterning. Plant Physiol. 144, 173–186 (2007).
    Article CAS Google Scholar
  9. Zhan, S., Horrocks, J. & Lukens, L.N. Islands of co-expressed neighbouring genes in Arabidopsis thaliana suggest higher-order chromosome domains. Plant J. 45, 347–357 (2006).
    Article CAS Google Scholar
  10. Hurst, L.D., Pal, C. & Lercher, M.J. The evolutionary dynamics of eukaryotic gene order. Nat. Rev. Genet. 5, 299–310 (2004).
    Article CAS Google Scholar
  11. Lee, S., Jo, M., Lee, J., Koh, S.S. & Kim, S. Identification of novel universal housekeeping genes by statistical analysis of microarray data. J. Biochem. Mol. Biol. 40, 226–231 (2007).
    CAS PubMed Google Scholar
  12. Yang, G.X. et al. Microarray analysis of brassinosteroids- and gibberellin-regulated gene expression in rice seedlings. Mol. Genet. Genomics 271, 468–478 (2004).
    Article CAS Google Scholar
  13. Yazaki, J. et al. Transcriptional profiling of genes responsive to abscisic acid and gibberellin in rice: phenotyping and comparative analysis between rice and Arabidopsis. Physiol. Genomics 17, 87–100 (2004).
    Article CAS Google Scholar
  14. Liu, X. et al. A G protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid. Science 315, 1712–1716 (2007).
    Article CAS Google Scholar
  15. Razem, F.A., El-Kereamy, A., Abrams, S.R. & Hill, R.D. The RNA-binding protein FCA is an abscisic acid receptor. Nature 439, 290–294 (2006).
    Article CAS Google Scholar
  16. Shen, Y.Y. et al. The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443, 823–826 (2006).
    Article CAS Google Scholar
  17. Abe, H. et al. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15, 63–78 (2003).
    Article CAS Google Scholar
  18. Edwards, D., Murray, J.A. & Smith, A.G. Multiple genes encoding the conserved CCAAT-box transcription factor complex are expressed in Arabidopsis. Plant Physiol. 117, 1015–1022 (1998).
    Article CAS Google Scholar
  19. Lotan, T. et al. Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93, 1195–1205 (1998).
    Article CAS Google Scholar
  20. Coustry, F., Sinha, S., Maity, S.N. & Crombrugghe, B. The two activation domains of the CCAAT-binding factor CBF interact with the dTAFII110 component of the Drosophila TFIID complex. Biochem. J. 331, 291–297 (1998).
    Article CAS Google Scholar
  21. Gusmaroli, G., Tonelli, C. & Mantovani, R. Regulation of novel members of the Arabidopsis thaliana CCAAT-binding nuclear factor Y subunits. Gene 283, 41–48 (2002).
    Article CAS Google Scholar
  22. Ma, L. et al. A microarray analysis of the rice transcriptome and its comparison to Arabidopsis. Genome Res. 15, 1274–1283 (2005).
    Article CAS Google Scholar
  23. Churchill, G.A. Fundamentals of experimental design for cDNA microarrays. Nat. Genet. 32 Suppl, 490–495 (2002).
    Article CAS Google Scholar
  24. Kulldorff, M., Rand, K., Gherman, G., Williams, W. & DeFrancesco, D. SaTScan v2.1: software for the spatial and space-time scan statistics. US National Cancer Institutehttp://www.cancer.gov/prevention/BB/SaTScan.html##〉 (1998).
  25. 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 Google Scholar
  26. Saldanha, A.J. Java Treeview–extensible visualization of microarray data. Bioinformatics 20, 3246–3248 (2004).
    Article CAS Google Scholar
  27. Beissbarth, T. & Speed, T.P. GOstat: find statistically overrepresented Gene Ontologies within a group of genes. Bioinformatics 20, 1464–1465 (2004).
    Article CAS Google Scholar
  28. Du, L. et al. The two-component signal system in rice (Oryza sativa L.): a genome-wide study of cytokinin signal perception and transduction. Genomics 89, 697–707 (2007).
    Article CAS Google Scholar
  29. Ito, Y. & Kurata, N. Identification and characterization of cytokinin-signalling gene families in rice. Gene 382, 57–65 (2006).
    Article CAS Google Scholar
  30. Jain, M. et al. Structure and expression analysis of early auxin-responsive Aux/IAA gene family in rice (Oryza sativa). Funct. Integr. Genomics 6, 47–59 (2006).
    Article CAS Google Scholar

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Acknowledgements

We thank N. Li for valuable database advice and assistance and P. Wu (Zhejiang University) for the rice root micrograph in Figure 3. This work was supported by US National Science Foundation Plant Genome Program grant DBI-0325821 to T.N., X.-W.D. and H.Z. T.L. and M.C. were supported in part by Peking-Yale Monsanto Fellowships.

Author information

Author notes

  1. Yuling Jiao, Tie Liu, Nicole K Clay, Teresa Ceserani, Meiqin Chen, Ligeng Ma & Hui-yong Zhang
    Present address: Present addresses: Division of Biology, California Institute of Technology, Pasadena, California 91125, USA (Y.J.); Biology Department, Stanford University, Stanford, California 94305, USA (T.L.); Department of Molecular Biology, Massachusetts General Hospital, Boston, Massachusetts 02114, USA (N.K.C.); Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada (T.C.); Peking-Yale Joint Research Center of Plant Molecular Genetics and Agrobiotechnology, College of Life Sciences, Peking University, Beijing 100871, China (M.C.); National Institute of Biological Sciences, Zhongguancun Life Science Park, Beijing 102206, China (L.M. and H.-Y.Z.).,
  2. Yuling Jiao, S Lori Tausta, Neeru Gandotra, Ning Sun and Tie Liu: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, 06520, Connecticut, USA
    Yuling Jiao, S Lori Tausta, Neeru Gandotra, Tie Liu, Nicole K Clay, Teresa Ceserani, Meiqin Chen, Ligeng Ma, Hui-yong Zhang, Xing-Wang Deng & Timothy Nelson
  2. Peking-Yale Joint Research Center of Plant Molecular Genetics and Agrobiotechnology, College of Life Sciences, Peking University, Beijing, 100871, China
    Yuling Jiao, S Lori Tausta, Neeru Gandotra, Tie Liu, Nicole K Clay, Teresa Ceserani, Meiqin Chen, Ligeng Ma, Hui-yong Zhang, Xing-Wang Deng & Timothy Nelson
  3. Center for Statistical Genomics and Proteomics, Yale University, New Haven, 06520, Connecticut, USA
    Ning Sun, Matthew Holford & Hongyu Zhao

Authors

  1. Yuling Jiao
  2. S Lori Tausta
  3. Neeru Gandotra
  4. Ning Sun
  5. Tie Liu
  6. Nicole K Clay
  7. Teresa Ceserani
  8. Meiqin Chen
  9. Ligeng Ma
  10. Matthew Holford
  11. Hui-yong Zhang
  12. Hongyu Zhao
  13. Xing-Wang Deng
  14. Timothy Nelson

Contributions

T.N., X.-W.D. and H.Z. conceived and oversaw the research. S.L.T., N.G. and T.L. performed cell isolations, RNA isolations and informatic analysis. Y.J., H.Z. and L.M. performed microarray hybridizations and informatic analysis. T.C., N.K.C. and M.C. performed cell and RNA isolations. N.S. designed and performed statistical methods for data processing and analysis. M.H. designed and implemented the atlas database and analytical tools. T.N. prepared the manuscript, with assistance from all coauthors.

Note: Supplementary information is available on the Nature Genetics website.

Corresponding author

Correspondence toTimothy Nelson.

Supplementary information

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Jiao, Y., Lori Tausta, S., Gandotra, N. et al. A transcriptome atlas of rice cell types uncovers cellular, functional and developmental hierarchies.Nat Genet 41, 258–263 (2009). https://doi.org/10.1038/ng.282

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