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Architecture of floral branch systems in maize and related grasses

Nature volume 436, pages 1119–1126 (2005)Cite this article

Abstract

The external appearance of flowering plants is determined to a large extent by the forms of flower-bearing branch systems, known as inflorescences, and their position in the overall structure of the plant. Branches and branching patterns are produced by tissues called shoot apical meristems. Thus, inflorescence architecture reflects meristem number, arrangement and activity, and the duration of meristem activity correlates with branch length. The inflorescences of maize, unlike those of related grasses such as rice and sorghum, predominantly lack long branches, giving rise to the tassel and familiar corncob. Here we report the isolation of the maize ramosa1 gene and show that it controls inflorescence architecture. Through its expression in a boundary domain near the nascent meristem base, ramosa1 imposes short branch identity as branch meristems are initiated. A second gene, ramosa2, acts through ramosa1 by regulating ramosa1 gene expression levels. ramosa1 encodes a transcription factor that appears to be absent in rice, is heterochronically expressed in sorghum, and may have played an important role in maize domestication and grass evolution.

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Figure 1: Maize inflorescences.
Figure 2: Transposon tagging, expression and sequence of the ra1 gene.
Figure 3: ra1 gene expression pattern.
Figure 4: Developmental genetics of long branch pathways.
Figure 5: Comparative development and ra1 expression in Panicoid grasses.
Figure 6: A model for heterochronic modulation of inflorescence and plant architecture.

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References

  1. Weberling, F. Morphology of Flowers and Inflorescences (Cambridge Univ. Press, Cambridge, 1989)

    Google Scholar 

  2. Sussex, I. M. & Kerk, N. M. The evolution of plant architecture. Curr. Opin. Plant Biol. 4, 33–37 (2001)

    Article  CAS  Google Scholar 

  3. Clifford, H. in Grass Systematics and Evolution (eds Soderstrom, T., Hilu, K., Campbell, C. & Barkworth, M.) 21–30 (Smithsonian Institution Press, Washington DC, 1987)

    Google Scholar 

  4. Doust, A. N. & Kellogg, E. A. Inflorescence diversification in the panicoid “bristle grass” clade (Paniceae, Poaceae): evidence from molecular phylogenies and developmental morphology. Am. J. Bot. 89, 1203–1222 (2002)

    Article  Google Scholar 

  5. McSteen, P., Laudencia-Chingcuanco, D. & Colasanti, J. A floret by any other name: control of meristem identity in maize. Trends Plant Sci. 5, 61–66 (2000)

    Article  CAS  Google Scholar 

  6. Veit, B., Schmidt, R. J., Hake, S. & Yanofsky, M. F. Maize floral development: new genes and old mutants. Plant Cell 5, 1205–1215 (1993)

    Article  Google Scholar 

  7. Gernert, W. A new subspecies of Zea mays L. Am. Nat. 46, 616–622 (1912)

    Article  Google Scholar 

  8. Chuck, G., Muszynski, M., Kellogg, E., Hake, S. & Schmidt, R. J. The control of spikelet meristem identity by the branched silkless1 gene in maize. Science 298, 1238–1241 (2002)

    Article  ADS  CAS  Google Scholar 

  9. Postlethwait, S. N. & Nelson, O. E. Characterization of development in maize through the use of mutants. I. The polytypic (Pt) and ramosa-1 (ra1) mutants. Am. J. Bot. 51, 238–243 (1964)

    Article  Google Scholar 

  10. Emerson, R., Beadle, G. & Fraser, A. A summary of linkage studies in maize. Cornell Univ. Agric. Experiment Station Memoir 180, 3–83 (1935)

    Google Scholar 

  11. Cheng, P. C., Greyson, R. I. & Walden, D. B. Organ initiation and the development of unisexual flowers in the tassel and ear of Zea mays. Am. J. Bot. 70, 450–462 (1983)

    Article  Google Scholar 

  12. McClintock, B. Induction of instability at selected loci in maize. Genetics 38, 579–599 (1953)

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Dawe, R. K. & Freeling, M. Clonal analysis of the cell lineages in the male flower of maize. Dev. Biol. 142, 233–245 (1990)

    Article  CAS  Google Scholar 

  14. Takatsuji, H. Zinc-finger proteins: the classical zinc finger emerges in contemporary plant science. Plant Mol. Biol. 39, 1073–1078 (1999)

    Article  CAS  Google Scholar 

  15. Sakai, H., Medrano, L. J. & Meyerowitz, E. M. Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries. Nature 378, 199–203 (1995)

    Article  ADS  CAS  Google Scholar 

  16. Nickerson, N. H. & Dale, E. E. Tassel modifications in Zea mays. Ann. Mo. Bot. Gard. 42, 195–211 (1955)

    Article  Google Scholar 

  17. Walsh, J. & Freeling, M. The liguleless2 gene of maize functions during the transition from the vegetative to the reproductive shoot. Plant J. 19, 489–495 (1999)

    Article  CAS  Google Scholar 

  18. Kellogg, E. in Grasses: Systematics and Evolution (eds Jacobs, S. & Everett, J.) (CSIRO, Melbourne, 2000)

    Google Scholar 

  19. Kellogg, E. A. Plant evolution: the dominance of maize. Curr. Biol. 7, R411–R413 (1997)

    Article  CAS  Google Scholar 

  20. Whitt, S. R., Wilson, L. M., Tenaillon, M. I., Gaut, B. S. & Buckler, E. S. Genetic diversity and selection in the maize starch pathway. Proc. Natl Acad. Sci. USA 99, 12959–12962 (2002)

    Article  ADS  CAS  Google Scholar 

  21. Hudson, R., Kreitman, M. & Aguade, M. A test of neutral molecular evolution based on nucleotide data. Genetics 116, 153–159 (1987)

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Tenaillon, M. I. et al. Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc. Natl Acad. Sci. USA 98, 9161–9166 (2001)

    Article  ADS  CAS  Google Scholar 

  23. Remington, D. L. et al. Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc. Natl Acad. Sci. USA 98, 11479–11484 (2001)

    Article  ADS  CAS  Google Scholar 

  24. Wilson, L. M. et al. Dissection of maize kernel composition and starch production by candidate gene association. Plant Cell 16, 2719–2733 (2004)

    Article  CAS  Google Scholar 

  25. Troll, W. Die Infloreszenzen: Typologie und Stellung im Aufbau des Vegetationskörpers (Fischer, Stuttgart, 1964)

    Google Scholar 

  26. Poethig, R. Phase change and the regulation of shoot morphogenesis in plants. Science 250, 923–930 (1990)

    Article  ADS  CAS  Google Scholar 

  27. Gallavotti, A. et al. The role of barren stalk1 in the architecture of maize. Nature 432, 630–635 (2004)

    Article  ADS  CAS  Google Scholar 

  28. Doebley, J., Stec, A. & Hubbard, L. The evolution of apical dominance in maize. Nature 386, 485–488 (1997)

    Article  ADS  CAS  Google Scholar 

  29. Chuck, G., Meeley, R. & Hake, S. The control of maize spikelet meristem identity by the APETALA-2-like gene indeterminate spikelet1. Genes Dev. 12, 1145–1154 (1998)

    Article  CAS  Google Scholar 

  30. 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  Google Scholar 

  31. Bommert, P. et al. thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase. Development 132, 1235–1245 (2005)

    Article  CAS  Google Scholar 

  32. Vollbrecht, E., Reiser, L. & Hake, S. Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene, knotted1. Development 127, 3161–3172 (2000)

    CAS  PubMed  Google Scholar 

  33. Collins, G. Hybrids of Zea tunicata and Zea ramosa. Proc. Natl Acad. Sci. USA 3, 345–349 (1917)

    Article  ADS  CAS  Google Scholar 

  34. Doebley, J. & Stec, A. Inheritance of the morphological differences between maize and teosinte: comparison of results for two F2 populations. Genetics 134, 559–570 (1993)

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Wang, R. L., Stec, A., Hey, J., Lukens, L. & Doebley, J. The limits of selection during maize domestication. Nature 398, 236–239 (1999)

    Article  ADS  CAS  Google Scholar 

  36. Takeda, T. et al. The OsTB1 gene negatively regulates lateral branching in rice. Plant J. 33, 513–520 (2003)

    Article  CAS  Google Scholar 

  37. Doebley, J. The genetics of maize evolution. Annu. Rev. Genet. 38, 37–59 (2004)

    Article  CAS  Google Scholar 

  38. Kellogg, E. A. Evolution of developmental traits. Curr. Opin. Plant Biol. 7, 92–98 (2004)

    Article  CAS  Google Scholar 

  39. Martienssen, R. The origin of maize branches out. Nature 386, 443–444 (1997)

    Article  ADS  CAS  Google Scholar 

  40. Sambrook, J. & Russell, D. W. Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, 2001)

    Google Scholar 

  41. Jackson, D., Veit, B. & Hake, S. Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120, 405–413 (1994)

    CAS  Google Scholar 

  42. Rozas, J. & Rozas, R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174–175 (1999)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank T. Mulligan for plant care, Z. Lippman and C. Kopec for help with in situ hybridization and SEM, R. J. Schmidt for producing and sharing the ra1-RS allele, D. Jackson for discussions and V. Irish for commenting on the manuscript. E.V. was a DOE-Energy Biosciences postdoctoral fellow of the Life Sciences Research Foundation. L.G. was supported by the Cold Spring Harbor Undergraduate Research Program. Grant support was provided by the Agricultural Research Service of the USDA (to E.S.B.), the National Research Initiative of the USDA CSREES (to R.M.), and by the NSF Plant Genome Research Program (to E.S.B. and R.M.).

Author information

Author notes

  1. Erik Vollbrecht

    Present address: Department of Genetics, Development and Cell Biology, Iowa State University, Ames, Iowa, 50011, USA

  2. Patricia S. Springer

    Present address: Department of Botany and Plant Science, Center for Plant Cell Biology, University of California, Riverside, California, 92521, USA

  3. Lindee Goh

    Present address: The Boston Consulting Group, 1 Exchange Place, Boston, Massachusetts, 02109, USA

Authors and Affiliations

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

    Erik Vollbrecht, Patricia S. Springer, Lindee Goh & Robert Martienssen

  2. USDA, ARS and Department of Plant Breeding, Cornell University, New York, 14850, Ithaca, USA

    Edward S. Buckler IV

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Corresponding author

Correspondence to Robert Martienssen.

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Competing interests

DNA sequences reported here have been deposited in GenBank under accession numbers AY957396–AY957399 and DQ013174–DQ013203. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Table S1

This Microsoft Word format file contains a table with statistics of nucleotide diversity and HKA tests. (DOC 30 kb)

Supplementary Methods

This Microsoft Word format file contains text that summarizes genetic methods for cosegregation analysis of mutable, Spm-induced alleles of ramosa1. (DOC 24 kb)

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Vollbrecht, E., Springer, P., Goh, L. et al. Architecture of floral branch systems in maize and related grasses. Nature 436, 1119–1126 (2005). https://doi.org/10.1038/nature03892

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