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Comparative analyses of C4 and C3 photosynthesis in developing leaves of maize and rice

Nature Biotechnology volume 32, pages 1158–1165 (2014)Cite this article

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Abstract

C4 and C3 photosynthesis differ in the efficiency with which they consume water and nitrogen. Engineering traits of the more efficient C4 photosynthesis into C3 crops could substantially increase crop yields in hot, arid conditions. To identify differences between C4 and C3 photosynthetic mechanisms, we profiled metabolites and gene expression in the developing leaves of Zea mays (maize), a C4 plant, and Oryza sativa (rice), a C3 plant, using a statistical method named the unified developmental model (UDM). Candidate cis-regulatory elements and transcription factors that might regulate photosynthesis were identified, together with differences between C4 and C3 nitrogen and carbon metabolism. The UDM algorithms could be applied to analyze and compare development in other species. These data sets together with community viewers to access and mine them provide a resource for photosynthetic research that will inform efforts to engineer improvements in carbon fixation in economically valuable grass crops.

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Figure 1: Leaf gradients of maize and rice.
Figure 2: A unified developmental model to correlate developmental gradients.
Figure 3: Clusters enriched with photosynthesis GO annotations.
Figure 4: Candidate cis-regulatory elements for mesophyll and bundle sheath–specific expression.
Figure 5: Suberin biosynthesis and regulatory candidates.

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Gene Expression Omnibus

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Sequence Read Archive

Change history

  • 16 October 2014

    In the version of this article initially published online, reference 20 was incorrect. Instead of Piganeau et al., J. Mol. Evol. 69, 249–259 (2009), the correct reference is Vandepoele et al., Plant Physiol. 150, 535–546 (2009).The error has been corrected for the print, PDF and HTML versions of this article.

  • 26 October 2014

    The version of this article initially published online was incorrectly listed as an Article. It is a Resource. The error has been corrected for the print, PDF and HTML versions of this article.

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Acknowledgements

We thank J. Schnable for helpful comments and uploading the original sequencing data to the NCBI SRA (SRP018823). This research was supported by the National Science Foundation (IOS-1127017 to T.P.B., T.C.M., P. Liu and R.T.), the National Sciences and Engineering Research Council of Canada (to N.J.P.) and The Max-Planck Society and the European Union Framework 7 Program (3to4) (to A.R.F. and M.S.).

Author information

Author notes

  1. Lin Wang, Yaqing Si, Adriano Nunes-Nesi, Lauren K Dedow, Pinghua Li, Cankui Zhang & Ying Shao

    Present address: Present addresses: Monsanto Company, St. Louis, Missouri, USA (L.W.), Southwestern University of Finance & Economics, Chengdu, China (Y. Si), Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Minas Gerais, Brazil (A.N.-N.), Department of Botany and Plant Science, University of California at Riverside, Riverside, California, USA (L.K.D.), Shandong Agricultural University, Tai'an, Shandong, China (P.L.), Department of Agronomy, Purdue University, West Lafayette, Indiana, USA (C.Z.), and St. Jude Children's Research Hospital, Pediatric Cancer Genome Project, Memphis, Tennessee, USA (Y. Shao).,

Authors and Affiliations

  1. The Donald Danforth Plant Science Center, St. Louis, Missouri, USA

    Lin Wang, Rachel A Mertz, Lauren K Dedow, Douglas W Bryant, Sarit Weissmann, Anthony Studer, Ying Shao, Todd C Mockler & Thomas P Brutnell

  2. The Max Planck Institute for Molecular Plant Physiology, Wissenschaftspark Golm, Potsdam-Golm, Germany

    Angelika Czedik-Eysenberg, Takayuki Tohge, Adriano Nunes-Nesi, Stephanie Arrivault, Alisdair R Fernie & Mark Stitt

  3. Department of Statistics, Iowa State University, Ames, Iowa, USA

    Yaqing Si, Wen Zhou & Peng Liu

  4. The Chinese Academy of Sciences-Max Planck Society Partner Institute for Computational Biology, Shanghai Institute for Biological Sciences, Chinese Academy of Sciences, Shanghai, China

    Jiajia Xu & Xinguang Zhu

  5. The Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Hainan, Haikou, China.,

    Pinghua Li & Zehong Ding

  6. Department of Agronomy, Purdue University, West Lafayette, Indiana, USA

    Cankui Zhang & Robert Turgeon

  7. Department of Biology, Skidmore College, Saratoga Springs, New York, USA

    Therese LaRue

  8. Computational Biology Service Unit, Life Sciences Core Laboratories Center, Cornell University, Ithaca, New York, USA

    Qi Sun

  9. Department of Cell and Systems Biology/Center for the Analysis of Genome Evolution and Function, University of Toronto, Toronto, Ontario, Canada

    Rohan V Patel & Nicholas J Provart

  10. Collaborative Innovation Center of Henan Grain Crops and National Key Laboratory of Wheat and Maize Crop Science, Henan Agricultural University, Zhengzhou, China

    Thomas P Brutnell

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Contributions

L.W., M.S., A.R.F. and T.P.B. contributed to the design of the comparative transcriptomics and metabolic profiling, P.L., Y. Si, L.W. and T.P.B. to the design of the unified developmental model, and D.W.B. and T.C.M. to the design of the ELEMENT algorithm. Data visualization tools were developed by R.V.P. and N.J.P. All authors contributed to the design and execution of experiments and to the interpretation of data.

Corresponding author

Correspondence to Thomas P Brutnell.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–11, Supplementary Tables 4–6, 8–9 and 17 and Supplementary Note 1 (PDF 3598 kb)

Supplementary Table 1

Metabolic traits determined across the maize leaf developmental gradient (XLSX 66 kb)

Supplementary Table 2

Metabolic traits determined across the rice leaf developmental gradient (XLSX 21 kb)

Supplementary Table 3

Orthologous genes of maize and rice (XLSX 1145 kb)

Supplementary Table 7

Expression of major C4 carbon shuttle genes (XLSX 11 kb)

Supplementary Table 10

Lipophilic Cell Wall Biosynthesis candidates of maize and rice (XLSX 29 kb)

Supplementary Table 11

Candidate TFs for Suberin biosynthesis in cluster 25 (XLSX 12 kb)

Supplementary Table 12

Cis-elements of Arabidopsis and maize suberin regulatory candidate promoters (XLSX 12 kb)

Supplementary Table 13

RPKM values of maize and rice genes along the leaf gradients (XLSX 21087 kb)

Supplementary Table 14

TopGO enrichment results for Biological processes (XLSX 75 kb)

Supplementary Table 15

TopGO enrichment results for Molecular Functions (XLSX 73 kb)

Supplementary Table 16

TopGO enrichment results for Cellular Component (XLSX 69 kb)

Supplementary Table 18

Anchor genes used for UDM model (XLSX 1325 kb)

Supplementary Note 2

R codes used to construct UDM (ZIP 16 kb)

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Wang, L., Czedik-Eysenberg, A., Mertz, R. et al. Comparative analyses of C4 and C3 photosynthesis in developing leaves of maize and rice. Nat Biotechnol 32, 1158–1165 (2014). https://doi.org/10.1038/nbt.3019

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