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A trehalose metabolic enzyme controls inflorescence architecture in maize

Nature volume 441, pages 227–230 (2006)Cite this article

Abstract

Inflorescence branching is a major yield trait in crop plants controlled by the developmental fate of axillary shoot meristems1. Variations in branching patterns lead to diversity in flower-bearing architectures (inflorescences) and affect crop yield by influencing seed number or harvesting ability2,3. Several growth regulators such as auxins, cytokinins and carotenoid derivatives regulate branching architectures4. Inflorescence branching in maize is regulated by three RAMOSA genes5. Here we show that one of these genes, RAMOSA3 (RA3), encodes a trehalose-6-phosphate phosphatase expressed in discrete domains subtending axillary inflorescence meristems. Genetic and molecular data indicate that RA3 functions through the predicted transcriptional regulator RAMOSA1 (RA1)5. We propose that RA3 regulates inflorescence branching by modification of a sugar signal that moves into axillary meristems. Alternatively, the fact that RA3 acts upstream of RA1 supports a hypothesis that RA3 itself may have a transcriptional regulatory function.

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Figure 1: ra3 mutant phenotypes.
Figure 2: Developmental expression of RA3 and SRA.
Figure 3: ra3 enhances a weak ra1 mutant, and RA1 expression is reduced in ra3 mutants.

References

  1. Ward, S. P. & Leyser, O. Shoot branching. Curr. Opin. Plant Biol. 7, 73–78 (2004)

    Article  CAS  PubMed  Google Scholar 

  2. Doebley, J. Mapping the genes that made maize. Trends Genet. 8, 302–307 (1992)

    Article  CAS  PubMed  Google Scholar 

  3. Bommert, P., Satoh-Nagasawa, N., Jackson, D. & Hirano, H. Genetics and evolution of inflorescence and flower development in grasses. Plant Cell Physiol. 46, 69–78 (2005)

    Article  CAS  PubMed  Google Scholar 

  4. Schmitz, G. & Theres, K. Shoot and inflorescence branching. Curr. Opin. Plant Biol. 8, 506–511 (2005)

    Article  CAS  PubMed  Google Scholar 

  5. Vollbrecht, E., Springer, P. S., Goh, L., Buckler, E. S. & Martienssen, R. Architecture of floral branch systems in maize and related grasses. Nature 436, 1119–1126 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  6. Strom, A. R. & Kaasen, I. Trehalose metabolism in Escherichia coli: stress protection and stress regulation of gene expression. Mol. Microbiol. 8, 205–210 (1993)

    Article  CAS  PubMed  Google Scholar 

  7. Thevelein, J. M. & Hohmann, S. Trehalose synthase: guard to the gate of glycolysis in yeast? Trends Biochem. Sci. 20, 3–10 (1995)

    Article  CAS  PubMed  Google Scholar 

  8. Goddijn, O. J. & van Dun, K. Trehalose metabolism in plants. Trends Plant Sci. 4, 315–319 (1999)

    Article  CAS  PubMed  Google Scholar 

  9. Leyman, B., Van Dijck, P. & Thevelein, J. M. An unexpected plethora of trehalose biosynthesis genes in Arabidopsis thaliana. Trends Plant Sci. 6, 510–513 (2001)

    Article  CAS  PubMed  Google Scholar 

  10. Eastmond, P. J., Li, Y. & Graham, I. A. Is trehalose-6-phosphate a regulator of sugar metabolism in plants? J. Exp. Bot. 54, 533–537 (2003)

    Article  CAS  PubMed  Google Scholar 

  11. Schluepmann, H., Pellny, T., van Dijken, A., Smeekens, S. & Paul, M. Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 100, 6849–6854 (2003)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  12. Cabib, E. & Leloir, L. F. The biosynthesis of trehalose phosphate. J. Biol. Chem. 231, 259–275 (1958)

    CAS  PubMed  Google Scholar 

  13. Schluepmann, H. et al. Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose-6-phosphate accumulation. Plant Physiol. 135, 879–890 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. van Dijken, A. J., Schluepmann, H. & Smeekens, S. C. Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol. 135, 969–977 (2004)

    Article  CAS  PubMed  Google Scholar 

  15. Perry, H. S. Maize Genetics/Genomics Database [online] http://www.maizegdb.org/.

  16. Michelmore, R. W., Paran, I. & Kesseli, R. V. Identification of markers linked to disease-resistance genes by bulked segregant analysis: A rapid method to detect markers in specific genomic regions by using segregating populations. Proc. Natl Acad. Sci. USA 88, 9828–9832 (1991)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  17. Thaller, M. C., Schippa, S. & Rossolini, G. M. Conserved sequence motifs among bacterial, eukaryotic, and archaeal phosphatases that define a new phosphohydrolase superfamily. Protein Sci. 7, 1647–1652 (1998)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Plant Genome DataBase. [online] http://www.plantgdb.org/prj/GSSAssembly/.

  19. The Institute for Genomic Research. The TIGR Maize Database [online] http://www.tigr.org/tdb/tgi/maize/.

  20. Emrich, S. J. et al. A strategy for assembling the maize (Zea mays L.) genome. Bioinformatics 20, 140–147 (2004)

    Article  CAS  PubMed  Google Scholar 

  21. Huelsenbeck, J. P. & Ronquist, F. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001)

    Article  CAS  PubMed  Google Scholar 

  22. Vogel, G., Aeschbacher, R. A., Muller, J., Boller, T. & Wiemken, A. Trehalose-6-phosphate phosphatases from Arabidopsis thaliana: identification by functional complementation of the yeast tps2 mutant. Plant J. 13, 673–683 (1998)

    Article  CAS  PubMed  Google Scholar 

  23. Klutts, S. et al. Purification, cloning, expression, and properties of mycobacterial trehalose-phosphate phosphatase. J. Biol. Chem. 278, 2093–2100 (2003)

    Article  CAS  PubMed  Google Scholar 

  24. De Virgilio, C. et al. Disruption of TPS2, the gene encoding the 100-kDa subunit of the trehalose-6-phosphate synthase/phosphatase complex in Saccharomyces cerevisiae, causes accumulation of trehalose-6-phosphate and loss of trehalose-6-phosphate phosphatase activity. Eur. J. Biochem. 212, 315–323 (1993)

    Article  CAS  PubMed  Google Scholar 

  25. Pellny, T. K. et al. Genetic modification of photosynthesis with E. coli genes for trehalose synthesis. Plant Biotechnol. J. 2, 71–82 (2004)

    Article  CAS  PubMed  Google Scholar 

  26. Kolbe, A. et al. Trehalose-6-phosphate regulates starch synthesis via posttranscriptional redox activation of ADP-glucose pyrophosphorylase. Proc. Natl Acad. Sci. USA 102, 11118–11123 (2005)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kim, J.-w. & Dang, C. V. Multifaceted roles of glycolytic enzymes. Trends Biochem. Sci. 30, 142–150 (2005)

    Article  CAS  PubMed  Google Scholar 

  28. Taguchi-Shiobara, F., Yuan, Z., Hake, S. & Jackson, D. The fasciated ear2 gene encodes a leucine rich repeat receptor like protein that regulates shoot meristem proliferation in maize. Genes Dev. 15, 2755–2766 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank C. Carson and E. Coe for initial molecular mapping of RA3; S. Hake for the fea1-Mu line; N. Inada, E. Irish, J. Linder and E. Vollbrecht for ra3 alleles; T. Mulligan for plant care; J. Andersen, N. Kobayashi-Simorowski and N. Tonks for help with phosphatase assays; V. Koroth Edavana for suggestions about the Mycobacterium TPP clone; P. Dahl, D. Goto, K. Noma and T. Phelps-Durr for suggestions for the yeast complementation test; J. Kossuth for help with DNA sequencing; and E. Kellogg, W. Lukowitz, J. Simorowski, E. Vollbrecht, and members of the Jackson laboratory for comments on the manuscript. Funding was provided by the National Science Foundation, Plant Genome Research Program, and the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service (to D.J.). Author Contributions N.S.-N. performed the SEM analyses, RA3 mapping, RT–PCRs, in situ hybridizations, double-mutant analyses, phosphatase assay and yeast complementation test. N.N. helped with RA3 mapping and provided the material for RT–PCR in rice. S.M. performed phylogenetic analyses and in situ hybridizations in rice. H.S. organized the collaboration. D.J. supervised the research and wrote the paper. All authors discussed the results and commented on the manuscript.

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  1. Simon Malcomber

    Present address: Department of Biological Sciences, California State University–Long Beach, Long Beach, California, 90840, USA

Authors and Affiliations

  1. Cold Spring Harbor Laboratory, 1 Bungtown Road, New York, 11724, Cold Spring Harbor, USA

    Namiko Satoh-Nagasawa & David Jackson

  2. DuPont Crop Genetics Experimental Station E353, Wilmington, Delaware, 19880, USA

    Nobuhiro Nagasawa & Hajime Sakai

  3. Department of Biology, University of Missouri–St Louis, St Louis, Missouri, 63121, USA

    Simon Malcomber

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  1. Namiko Satoh-Nagasawa
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Correspondence to David Jackson.

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Accession numbers for gene sequences are listed in Supplementary Fig. 2. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

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Supplementary Notes

This file contains Supplementary Figures 1–4, Supplementary Tables 1 and 2, Supplementary Methods and additional references. (DOC 336 kb)

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Satoh-Nagasawa, N., Nagasawa, N., Malcomber, S. et al. A trehalose metabolic enzyme controls inflorescence architecture in maize. Nature 441, 227–230 (2006). https://doi.org/10.1038/nature04725

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