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The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA

Abstract

Retention of juvenile traits in the adult reproductive phase characterizes a process known as neoteny, and speculation exists over whether it has contributed to the evolution of new species. The dominant Corngrass1 (Cg1) mutant of maize is a neotenic mutation that results in phenotypes that may be present in the grass-like ancestors of maize. We cloned Cg1 and found that it encodes two tandem miR156 genes that are overexpressed in the meristem and lateral organs. Furthermore, a target of Cg1 is teosinte glume architecture1 (tga1)1, a gene known to have had a role in the domestication of maize from teosinte. Cg1 mutant plants overexpressing miR156 have lower levels of mir172, a microRNA that targets genes controlling juvenile development2. By altering the relative levels of both microRNAs, it is possible to either prolong or shorten juvenile development in maize, thus providing a mechanism for how species-level heterochronic changes can occur in nature.

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Figure 1: Analysis of the Cg1 phenotype.
Figure 2: Cloning of the Cg1 gene.
Figure 3: Analysis of Cg1 target genes.
Figure 4: Expression of MIR156 and target genes.

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References

  1. Wang, H. et al. The origin of the naked grains of maize. Nature 436, 714–719 (2005).

    Article  CAS  Google Scholar 

  2. Lauter, N., Kampani, A., Carlson, S., Goebel, M. & Moose, S.P. microRNA172 down-regulates glossy15 to promote vegetative phase change in maize. Proc. Natl. Acad. Sci. USA 102, 9412–9417 (2005).

    Article  CAS  Google Scholar 

  3. Steeves, T.A. & Sussex, I.M. Patterns in Plant Development (Cambridge Univ. Press, Cambridge, UK, 1989).

    Book  Google Scholar 

  4. Allsopp, A. Land and water forms: Physiological aspects. Handb. Pflugers Physiol. 15, 1236–1255 (1965).

    Google Scholar 

  5. Goliber, T.E. & Feldman, L.J. Developmental analysis of leaf plasticity in the heterophyllous aquatic plant Hippurus vulgaris. Am. J. Bot. 77, 399–412 (1990).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. Moose, S.P. & Sisco, P.H. Glossy15 controls the epidermal juvenile-to-adult phase transition in maize. Plant Cell 6, 1343–1355 (1994).

    Article  CAS  Google Scholar 

  8. Evans, M.M.S., Passas, H.J. & Poethig, R.S. Heterochronic effects of glossy15 mutations on epidermal cell identity in maize. Development 120, 1971–1981 (1994).

    CAS  PubMed  Google Scholar 

  9. Moose, S.P. & Sisco, P.H. glossy15, an APETELA2-like gene from maize that regulates leaf epidermal cell identity. Genes Dev. 10, 3018–3027 (1996).

    Article  CAS  Google Scholar 

  10. Poethig, R.S. Heterochronic mutations affecting shoot development in maize. Genetics 119, 959–973 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Whaley, W.G. & Leech, J.H. The developmental morphology of the mutant “Corn grass”. Bull. Torrey Bot. Club 77, 274–286 (1950).

    Article  Google Scholar 

  12. Galinat, W.C. Corn grass. I. Corn grass as a prototype or a false progenitor of maize. Am. Nat. 88, 101–104 (1954).

    Article  Google Scholar 

  13. Singleton, W.R. Inheritance of Corn grass, a macromutation in maize, and its possible significance as an ancestral type. Am. Nat. 305, 81–96 (1951).

    Article  Google Scholar 

  14. 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 

  15. Galinat, W.C. Corn grass. II. Effect of the Corn grass gene on the development of the maize inflorescence. Am. J. Bot. 41, 803–806 (1954).

    Article  Google Scholar 

  16. Bortiri, E. et al. ramosa2 encodes a Lateral Organ Boundary domain protein that determines the fate of stem cells in branch meristems of maize. Plant Cell 18, 574–585 (2006).

    Article  CAS  Google Scholar 

  17. 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  CAS  Google Scholar 

  18. Kellogg, E.A. Molecular and morphological evolution in Andropogoneae. in Proceedings of the Second International Conference on the Comparative Biology of the Monocotyledons. Vol. 2. Symposium on Grass Systematics and Evolution (eds. Everett, J.E. & Jacobs, S.W.L.) (CSIRO, Melbourne, 2000).

    Google Scholar 

  19. Wessler, S.R. & Varagona, M.J. Molecular basis of mutations at the waxy locus of maize: correlation with the fine structure genetic map. Proc. Natl. Acad. Sci. USA 82, 4177–4181 (1985).

    Article  CAS  Google Scholar 

  20. Rhoades, M.W. et al. Prediction of plant microRNA targets. Cell 110, 513–520 (2002).

    Article  CAS  Google Scholar 

  21. Goldschmidt, R.B. The Material Basis of Evolution, 436 (Yale Univ. Press, New Haven, Connnecticut, 1940).

    Google Scholar 

  22. Takhtajan, A. Neoteny and the Origin of Flowering Plants, 207–219 (Columbia Univ. Press, New York, 1976).

    Google Scholar 

  23. McClintock, B. The significance of responses of the genome to challenge. Science 226, 792–801 (1984).

    Article  CAS  Google Scholar 

  24. Doebley, J. & Stec, A. Genetic analysis of the morphological differences between maize and teosinte. Genetics 129, 285–295 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Unger, E. et al. A chimeric ecdysone receptor facilitates methoxyfenozide-dependent restoration of male fertility in ms45 maize. Transgenic Res. 11, 455–465 (2002).

    Article  CAS  Google Scholar 

  26. Cigan, A.M., Unger, E., Xu, R.-J., Kendall, T.L. & Fox, T.W. Phenotypic complementation of ms45 mutant maize requires tapetal expression of the Ms45 gene. Sex. Plant Reprod. 14, 135–142 (2001).

    Article  CAS  Google Scholar 

  27. Park, W., Li, J., Song, R., Messing, J. & Chen, X. CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol. 12, 1484–1495 (2002).

    Article  CAS  Google Scholar 

  28. Jackson, D. In situ hybridization in plants. in Molecular Plant Pathology: a Practical Approach (eds. Bowles, D.J., Gurr, S.J. & McPherson, M.) 163–174 (Oxford Univ. Press, Oxford, 1991).

    Google Scholar 

  29. Sunkar, R., Girke, T., Jain, P.K. & Zhu, J.K. Cloning and characterization of microRNAs from rice. Plant Cell 17, 1397–1411 (2005).

    Article  CAS  Google Scholar 

  30. 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 

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Acknowledgements

The authors thank B. Li for his assistance with the isolation of the flanking sequences for Cg1-Pio allele, E. Unger for her helpful discussions and C. Lunde and E. Bortiri for reviewing the manuscript. G.C. was supported by US Department of Agriculture National Research Initiative grant 2004-03387. S.H. was supported by the US Department of Agriculture-Agricultural Research Service. K.S. was supported by the University of California Leadership Excellence through Advanced Degrees (LEADS) research program.

Author information

Authors and Affiliations

Authors

Contributions

A.M.C. did the experiments described in Figure 2a,b and Supplementary Figure 1c. K.S. helped with positional cloning of Cg1-ref (Figs. 2c and 3b). G.C. carried out the analysis of Cg1-ref and analyzed the expression patterns of the microRNAs and target genes (Figs. 1, 2c–j, 3 and 4). G.C. wrote the manuscript with help from S.H. and A.M.C.

Corresponding author

Correspondence to George Chuck.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Corngrass1 epidermal peels and expression in transgenic lines. (PDF 815 kb)

Supplementary Table 1

Primers used in this study. (PDF 52 kb)

Supplementary Note (PDF 157 kb)

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Chuck, G., Cigan, A., Saeteurn, K. et al. The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39, 544–549 (2007). https://doi.org/10.1038/ng2001

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