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The maize tasselseed4 microRNA controls sex determination and meristem cell fate by targeting Tasselseed6/indeterminate spikelet1

Abstract

In maize (Zea mays), sex determination occurs through abortion of female carpels in the tassel and arrest of male stamens in the ear. The Tasselseed6 (Ts6) and tasselseed4 (ts4) mutations permit carpel development in the tassel while increasing meristem branching, showing that sex determination and acquisition of meristem fate share a common pathway. We show that ts4 encodes a mir172 microRNA that targets APETALA2 floral homeotic transcription factors. Three lines of evidence suggest that indeterminate spikelet1 (ids1), an APETALA2 gene required for spikelet meristem determinacy, is a key target of ts4. First, loss of ids1 suppresses the ts4 sex determination and branching defects. Second, Ts6 mutants phenocopy ts4 and possess mutations in the microRNA binding site of ids1. Finally, IDS1 protein is expressed more broadly in ts4 mutants compared to wild type. Our results demonstrate that sexual identity in maize is acquired by limiting floral growth through negative regulation of the floral homeotic pathway.

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Figure 1: The ts4 mutant phenotype.
Figure 2: ts4 encodes a microRNA.
Figure 3: Expression of ts4.
Figure 4: Identification of ids1 as a target gene.
Figure 5: Immunolocalization of IDS1 in wild-type ears, tassels and ts4 tassels.

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References

  1. Phipps, I.F. Heritable characters in maize. XXXI. Tassel-seed4. J. Hered. 19, 399–404 (1928).

    Article  Google Scholar 

  2. 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 

  3. DeLong, A., Calderon-Urrea, A. & Dellaporta, S.L. Sex determination gene TASSELSEED2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 74, 757–768 (1993).

    Article  CAS  Google Scholar 

  4. Irish, E.E., Langdale, J.A. & Nelson, T.M. Interactions between tasselseed genes and other sex determining genes in maize. Dev. Genet. 15, 155–171 (1994).

    Article  Google Scholar 

  5. 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 

  6. 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 

  7. Moore, G., Devos, K.M., Wang, Z. & Gale, M.D. Cereal genome evolution - grasses, line up and form a circle. Curr. Biol. 7, 737–739 (1995).

    Article  Google Scholar 

  8. Irish, E.E. Class II tassel seed mutations provide evidence for multiple types of inflorescence meristems in maize (Poaceae). Am. J. Bot. 84, 1502–1515 (1997).

    Article  CAS  Google Scholar 

  9. Xie, Z. et al. Expression of Arabidopsis MIRNA genes. Plant Physiol. 138, 2145–2154 (2005).

    Article  CAS  Google Scholar 

  10. Reeves, R. & Wolffe, A.P. Substrate structure influences binding of the non-histone protein HMG-I(Y) to free nucleosomal DNA. Biochemistry 35, 5063–5074 (1996).

    Article  CAS  Google Scholar 

  11. Bensen, R.J. et al. Cloning and characterization of the maize An1 gene. Plant Cell 7, 75–84 (1995).

    Article  CAS  Google Scholar 

  12. 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 

  13. Chuck, G., Meeley, R. & Hake, S. The control of maize spikelet meristem fate by the APETALA2-like gene indeterminate spikelet1. Genes Dev. 12, 1145–1154 (1998).

    Article  CAS  Google Scholar 

  14. Simons, K.J. et al. Molecular characterization of the major wheat domestication gene Q. Genetics 172, 547–555 (2006).

    Article  CAS  Google Scholar 

  15. Schwab, R., Palatnik, J., Riester, M., Schommer, C., Schmid, M. & Weigel, D. Specific effects of microRNAs on the plant transcriptome. Dev. Cell 8, 517–527 (2005).

    Article  CAS  Google Scholar 

  16. Chen, X. A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303, 2022–2025 (2004).

    Article  CAS  Google Scholar 

  17. Aukerman, M.J. & Sakai, H. Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15, 2730–2741 (2003).

    Article  CAS  Google Scholar 

  18. Mizukami, Y. & Ma, H. Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71, 119–131 (1992).

    Article  CAS  Google Scholar 

  19. Zhao, L., Kim, Y., Dinh, T.T. & Chen, X. miR172 regulates stem cell fate and defines the inner boundary of APETALA3 and PISTILLATA expression domain in Arabidopsis floral meristems. Plant J. 51, 840–849 (2007).

    Article  CAS  Google Scholar 

  20. Nickerson, N.H. Sustained treatment with gibberellin acid of five different kinds of maize. Ann. Mo. Bot. Gard. 46, 19–37 (1959).

    Article  CAS  Google Scholar 

  21. Okamuro, J.K., Szeto, W., Lotys-Prass, C. & Jofuku, K.D. Photo and hormonal control of meristem identity in the Arabidopsis flower mutants apetala2 and apetala1. Plant Cell 9, 37–47 (1997).

    Article  CAS  Google Scholar 

  22. 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 

  23. 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 

  24. 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 

  25. Kaplinsky, N.J. & Freeling, M. Combinatorial control of meristem identity in maize inflorescences. Development 130, 1149–1158 (2003).

    Article  CAS  Google Scholar 

  26. 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 work was supported by National Science Foundation (NSF) grant DBI-0604923, by USDA-ARS Current Research Information System (CRIS) grant 5335-21000-018-00D to S.H. and by Cooperative State Research, Education, and Extension Service (CSREES) grant 2004-35301-14507 to G.C. We thank D. Irvine for the use of the scanning electron microscopy facility; D. Hantz for greenhouse maintenance; T. Peterson for the gift of the ts4-TP allele; M. Sachs for determining the genealogy of ts4-ref; B. Thompson, C. Lunde and E. Bortiri for helpful comments on the manuscript and L. Bartling and K. Saeturn for technical assistance.

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Contributions

R.M. contributed the ts4-mum1 allele, E.I. contributed the ts4-TP and ts4-A alleles and H.S. carried out BAC sequencing. G.C. designed this study and wrote the manuscript with help from S.H.

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Correspondence to George Chuck.

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Supplementary Figures 1–3, Supplementary Table 1 (PDF 1522 kb)

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Chuck, G., Meeley, R., Irish, E. et al. The maize tasselseed4 microRNA controls sex determination and meristem cell fate by targeting Tasselseed6/indeterminate spikelet1. Nat Genet 39, 1517–1521 (2007). https://doi.org/10.1038/ng.2007.20

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