Abstract
We have analyzed the maize leaf transcriptome using Illumina sequencing. We mapped more than 120 million reads to define gene structure and alternative splicing events and to quantify transcript abundance along a leaf developmental gradient and in mature bundle sheath and mesophyll cells. We detected differential mRNA processing events for most maize genes. We found that 64% and 21% of genes were differentially expressed along the developmental gradient and between bundle sheath and mesophyll cells, respectively. We implemented Gbrowse, an electronic fluorescent pictograph browser, and created a two-cell biochemical pathway viewer to visualize datasets. Cluster analysis of the data revealed a dynamic transcriptome, with transcripts for primary cell wall and basic cellular metabolism at the leaf base transitioning to transcripts for secondary cell wall biosynthesis and C4 photosynthetic development toward the tip. This dataset will serve as the foundation for a systems biology approach to the understanding of photosynthetic development.
Similar content being viewed by others
Accession codes
References
Husbands, A.Y., Chitwood, D.H., Plavskin, Y. & Timmermans, M.C. Signals and prepatterns: new insights into organ polarity in plants. Genes Dev. 23, 1986–1997 (2009).
Hay, A. & Tsiantis, M.A. KNOX family TALE. Curr. Opin. Plant Biol. 12, 593–598 (2009).
Bayer, E.M. et al. Integration of transport-based models for phyllotaxis and midvein formation. Genes Dev. 23, 373–384 (2009).
Kirchanski, S.J. The ultrastructural development of the dimorphic plastids of Zea mays L. Am. J. Bot. 62, 695–705 (1975).
Leech, R.M., Rumsby, M.G. & Thomson, W.W. Plastid differentiation, acyl lipid, and fatty acid changes in develo** green maize leaves. Plant Physiol. 52, 240–245 (1973).
Lopez-Juez, E. & Pyke, K.A. Plastids unleashed: their development and their integration in plant development. Int. J. Dev. Biol. 49, 557–577 (2005).
Woodson, J.D. & Chory, J. Coordination of gene expression between organellar and nuclear genomes. Nat. Rev. Genet. 9, 383–395 (2008).
Esau, K. Ontogeny of the vascular bundle in Zea mays. Hilgardia 15, 327–368 (1943).
Evert, R.F., Russin, W.A. & Bosabalidis, A.M. Anatomical and ultrastructural changes associated with sink-to-source transition in develo** maize leaves. Int. J. Plant Sci. 157, 247–261 (1996).
Sharman, B.C. Developmental anatomy of the shoot of Zea mays L. Ann. Bot. (Lond.) 6, 245–284 (1942).
Poethig, R.S. & Szymkowiak, E.J. Clonal analysis of leaf development in maize. Maydica 40, 67–76 (1995).
Sylvester, A.W., Cande, W.Z. & Freeling, M. Division and differentiation during normal and liguleless-1 maize leaf development. Development 110, 985–1000 (1990).
Sheen, J. C4 gene expression. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 187–217 (1999).
Hatch, M.D. & Slack, C.R. Photosynthesis by sugar-cane leaves: A new carboxylation reaction and the pathway of sugar formation. Biochem. J. 101, 103–111 (1966).
Sage, R.F. The evolution of C4 photosynthesis. New Phytol. 161, 341–370 (2004).
Sawers, R.J., Liu, P., Anufrikova, K., Hwang, J.T. & Brutnell, T.P. A multi-treatment experimental system to examine photosynthetic differentiation in the maize leaf. BMC Genomics 8, 12 (2007).
Friso, G., Majeran, W., Huang, M., Sun, Q. & van Wijk, K.J. Reconstruction of metabolic pathways, protein expression and homeostasis machineries across maize bundle sheath and mesophyll chloroplasts; large scale quantitative proteomics using the first maize genome assembly. Plant Physiol. 152, 1219–1250 (2010).
Majeran, W., Cai, Y., Sun, Q. & van Wijk, K.J. Functional differentiation of bundle sheath and mesophyll maize chloroplasts determined by comparative proteomics. Plant Cell 17, 3111–3140 (2005).
Majeran, W. et al. Consequences of C4 differentiation for chloroplast membrane proteomes in maize mesophyll and bundle sheath cells. Mol. Cell. Proteomics 7, 1609–1638 (2008).
Schnable, P.S. et al. The B73 maize genome: complexity, diversity, and dynamics. Science 326, 1112–1115 (2009).
Filichkin, S.A. et al. Genome-wide map** of alternative splicing in Arabidopsis thaliana. Genome Res. 20, 45–58 (2010).
Wang, B.B., O′Toole, M., Brendel, V. & Young, N.D. Cross-species EST alignments reveal novel and conserved alternative splicing events in legumes. BMC Plant Biol. 8, 17 (2008).
Wang, B.B. & Brendel, V. Genomewide comparative analysis of alternative splicing in plants. Proc. Natl. Acad. Sci. USA 103, 7175–7180 (2006).
Barbazuk, W.B., Fu, Y. & McGinnis, K.M. Genome-wide analyses of alternative splicing in plants: opportunities and challenges. Genome Res. 18, 1381–1392 (2008).
Severing, E.I., van Dijk, A.D., Stiekema, W.J. & van Ham, R.C. Comparative analysis indicates that alternative splicing in plants has a limited role in functional expansion of the proteome. BMC Genomics 10, 154 (2009).
Thimm, O. et al. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37, 914–939 (2004).
Wingler, A., Walker, R.P., Chen, Z.H. & Leegood, R.C. Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle sheath of maize. Plant Physiol. 120, 539–546 (1999).
Juarez, M.T., Kui, J.S., Thomas, J., Heller, B.A. & Timmermans, M.C. microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428, 84–88 (2004).
Juarez, M.T., Twigg, R.W. & Timmermans, M.C. Specification of adaxial cell fate during maize leaf development. Development 131, 4533–4544 (2004).
Liu, T., Ohashi-Ito, K. & Bergmann, D.C. Orthologs of Arabidopsis thaliana stomatal bHLH genes and regulation of stomatal development in grasses. Development 136, 2265–2276 (2009).
Lee, W.Y., Lee, D., Chung, W.I. & Kwon, C.S. Arabidopsis ING and Alfin1-like protein families localize to the nucleus and bind to H3K4me3/2 via plant homeodomain fingers. Plant J. 58, 511–524 (2009).
Hall, L.N., Rossini, L., Cribb, L. & Langdale, J.A. GOLDEN 2: a novel transcriptional regulator of cellular differentiation in the maize leaf. Plant Cell 10, 925–936 (1998).
Yanagisawa, S. & Sheen, J. Involvement of maize Dof zinc finger proteins in tissue-specific and light-regulated gene expression. Plant Cell 10, 75–89 (1998).
Stein, L.D. et al. The generic genome browser: a building block for a model organism system database. Genome Res. 12, 1599–1610 (2002).
Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
Winter, D. et al. An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2, e718 (2007).
Lycett, G. The role of Rab GTPases in cell wall metabolism. J. Exp. Bot. 59, 4061–4074 (2008).
Gou, J.Y., Yu, X.H. & Liu, C.J. A hydroxycinnamoyltransferase responsible for synthesizing suberin aromatics in Arabidopsis. Proc. Natl. Acad. Sci. USA 106, 18855–18860 (2009).
Molina, I., Li-Beisson, Y., Beisson, F., Ohlrogge, J.B. & Pollard, M. Identification of an Arabidopsis feruloyl-coenzyme A transferase required for suberin synthesis. Plant Physiol. 151, 1317–1328 (2009).
Ohtsu, K. et al. Global gene expression analysis of the shoot apical meristem of maize (Zea mays L.). Plant J. 52, 391–404 (2007).
Xu, T., Purcell, M., Zucchi, P., Helentjaris, T. & Bogorad, L. TRM1, a YY1-like suppressor of rbcS-m3 expression in maize mesophyll cells. Proc. Natl. Acad. Sci. USA 98, 2295–2300 (2001).
Hannemann, J. et al. Xeml Lab: a tool that supports the design of experiments at a graphical interface and generates computer-readable metadata files, which capture information about genotypes, growth conditions, environmental perturbations and sampling strategy. Plant Cell Environ. 32, 1185–1200 (2009).
Zhu, X.G., Long, S.P. & Ort, D.R. What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Curr. Opin. Biotechnol. 19, 153–159 (2008).
Snyder, M. & Gallagher, J.E. Systems biology from a yeast omics perspective. FEBS Lett. 583, 3895–3899 (2009).
Brady, S.M. et al. A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318, 801–806 (2007).
Reidel, E.J., Rennie, E.A., Amiard, V., Cheng, L. & Turgeon, R. Phloem loading strategies in three plant species that transport sugar alcohols. Plant Physiol. 149, 1601–1608 (2009).
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300 (1995).
Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. & Wold, B. Map** and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621–628 (2008).
Trapnell, C., Pachter, L. & Salzberg, S.L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105–1111 (2009).
Li, P. et al. Arabidopsis transcript and metabolite profiles: ecotype-specific responses to open-air elevated. Plant Cell Environ. 31, 1673–1687 (2008).
Winnall, W.R. et al. Effects of chronic celecoxib on testicular function in normal and lipopolysaccharide-treated rats. Int. J. Androl. 32, 542–555 (2009).
Marioni, J.C., Mason, C.E., Mane, S.M., Stephens, M. & Gilad, Y. RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res. 18, 1509–1517 (2008).
Acknowledgements
This work was supported by grants from the National Science Foundation (IOS-0701736 to R.T., P.L., Q.S., T.N. and T.P.B.). C.R.M. acknowledges support from a grant to the International Rice Research Institute from the Bill and Melinda Gates Foundation and T.P.B. acknowledges support from the iPlant Collaborative for development of the eFP browser.
Author information
Authors and Affiliations
Contributions
T.P.B., T.N. and R.T. designed the experiments. P. Li, L.P., N.G., E.J.R. and T.H.K. optimized and performed the experiments. Q.S., L.P., P. Liu, P. Li, L.W., Y.S., R.P., T.P.B., N.P., N.G., S.L.T. and C.R.M. performed data analysis. P. Li, L.P., T.N., N.G., S.L.T. and T.P.B. wrote the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Text and Figures
Supplementary Table 1, Supplementary Figures 1–13 and Supplementary Note (PDF 8744 kb)
Supplementary Table 2
Verification of RNA-seq results by qRT-PCR. (XLS 35 kb)
Supplementary Table 3
List of the K-means clusters. (XLS 4141 kb)
Supplementary Table 4
List of genes exhibiting differential expression between bundle sheath and mesophyll cells. (XLS 1078 kb)
Supplementary Table 5
Correlation between RNA-seq and proteomics data in the bundle sheath and mesophyll cells. (XLS 268 kb)
Supplementary Table 6
List of C4 genes and their expression changes along developmental zones. (XLS 41 kb)
Supplementary Table 7
List of differentially expressed transcription factors in the developmental zones and bundle sheath and mesophyll cells. (XLS 725 kb)
Supplemenatry Table 8
List of gene ID?s and RPKM estimates for Supplementary Figs. 8-12. (XLS 52 kb)
Rights and permissions
About this article
Cite this article
Li, P., Ponnala, L., Gandotra, N. et al. The developmental dynamics of the maize leaf transcriptome. Nat Genet 42, 1060–1067 (2010). https://doi.org/10.1038/ng.703
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ng.703
- Springer Nature America, Inc.
This article is cited by
-
Genomic investigation of duplication, functional conservation, and divergence in the LRR-RLK Family of Saccharum
BMC Genomics (2024)
-
Delayed leaf greening involves a major shift in the expression of cytosolic and mitochondrial ribosomes to plastid ribosomes in the highly phosphorus-use-efficient Hakea prostrata (Proteaceae)
Plant and Soil (2024)
-
De novo transcriptome assemblies of C3 and C4 non-model grass species reveal key differences in leaf development
BMC Genomics (2023)
-
Characterization and expression profiles of the B-box gene family during plant growth and under low-nitrogen stress in Saccharum
BMC Genomics (2023)
-
A transcriptional activator effector of Ustilago maydis regulates hyperplasia in maize during pathogen-induced tumor formation
Nature Communications (2023)