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A conserved microRNA module exerts homeotic control over Petunia hybrida and Antirrhinum majus floral organ identity


It is commonly thought that deep phylogenetic conservation of plant microRNAs (miRNAs) and their targets1,2 indicates conserved regulatory functions. We show that the blind (bl) mutant of Petunia hybrida3 and the fistulata (fis) mutant of Antirrhinum majus4,5, which have similar homeotic phenotypes, are recessive alleles of two homologous miRNA-encoding genes. The BL and FIS genes control the spatial restriction of homeotic class C genes6,7 to the inner floral whorls, but their ubiquitous early floral expression patterns are in contradiction with a potential role in patterning C gene expression. We provide genetic evidence for the unexpected function of the MIRFIS and MIRBL genes in the center of the flower and propose a dynamic mechanism underlying their regulatory role. Notably, Arabidopsis thaliana, a more distantly related species, also contains this miRNA module but does not seem to use it to confine early C gene expression to the center of the flower.

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Figure 1: Phenotypes of mutant and wild-type flowers.
Figure 2: The BL and FIS miRNAs and their targets.
Figure 3: miRBL, miRFIS and AmNF-YA expression during early flower development.
Figure 4: Enhanced PLE gene expression in the A. majus fis-1 mutant.
Figure 5: Rescue of organ identity defects of the fim mutant in the absence of miRFIS.
Figure 6: Regulatory mechanism governed by miRFIS and miRBL to maintain the C domain boundary by controlling early C gene expression.


  1. Axtell, M.J. & Bartel, D.P. Antiquity of microRNAs and their targets in land plants. Plant Cell 17, 1658–1673 (2005).

    Article  CAS  Google Scholar 

  2. Baulcombe, D. RNA silencing in plants. Nature 431, 356–363 (2004).

    Article  CAS  Google Scholar 

  3. Vallade, J., Maizonnier, D. & Cornu, A. La morphogenese florale chez le petunia. I. Analyze d'un mutant à corolle staminée. Can. J. Bot. 65, 761–764 (1987).

    Article  Google Scholar 

  4. McSteen, P.C.M., Vincent, C.A., Doyle, S., Carpenter, R. & Coen, E.S. Control of floral homeotic gene-expression and organ morphogenesis in Antirrhinum. Development 125, 2359–2369 (1998).

    CAS  PubMed  Google Scholar 

  5. Motte, P., Saedler, H. & Schwarz-Sommer, Z. STYLOSA and FISTULATA: regulatory components of the homeotic control of Antirrhinum floral organogenesis. Development 125, 71–84 (1998).

    CAS  PubMed  Google Scholar 

  6. Davies, B., Cartolano, M. & Schwarz-Sommer, Z. Flower development: The Antirrhinum perspective. Adv. Bot. Res. Inc. Adv. Plant Pathol. 44, 278–319 (2006).

    Google Scholar 

  7. Jack, T. Molecular and genetic mechanisms of floral control. Plant Cell 16, S1–S17 (2004).

    Article  CAS  Google Scholar 

  8. Navarro, C. et al. Molecular and genetic interactions between STYLOSA and GRAMINIFOLIA in the control of Antirrhinum vegetative and reproductive development. Development 131, 3649–3659 (2004).

    Article  CAS  Google Scholar 

  9. Kater, M.M. et al. Multiple AGAMOUS homologs from cucumber and petunia differ in their ability to induce reproductive organ fate. Plant Cell 10, 171–182 (1998).

    Article  CAS  Google Scholar 

  10. Davies, B. et al. PLENA and FARINELLI: redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. EMBO J. 18, 4023–4034 (1999).

    Article  CAS  Google Scholar 

  11. Maes, T. et al. Petunia Ap2-like genes and their role in flower and seed development. Plant Cell 13, 229–244 (2001).

    Article  CAS  Google Scholar 

  12. Keck, E., McSteen, P., Carpenter, R. & Coen, E. Separation of genetic functions controlling organ identity in flowers. EMBO J. 22, 1058–1066 (2003).

    Article  CAS  Google Scholar 

  13. Jones-Rhoades, M.W., Bartel, D.P. & Bartel, B. MicroRNAs and their regulatory roles in plants. Annu. Rev. Plant Biol. 57, 19–53 (2006).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  15. Gusmaroli, G., Tonellia, C. & Mantovani, R. Regulation of the CCAAT-Binding NF-Y subunits in Arabidopsis thaliana. Gene 283, 41–48 (2002).

    Article  CAS  Google Scholar 

  16. Schwab, R. et al. Specific effects of microRNAs on the plant transcriptome. Dev. Cell 8, 517–527 (2005).

    Article  CAS  Google Scholar 

  17. Hong, R.L., Hamaguchi, L., Busch, M.A. & Weigel, D. Regulatory elements of the floral homeotic gene AGAMOUS identified by phylogenetic footprinting and shadowing. Plant Cell 15, 1296–1309 (2003).

    Article  CAS  Google Scholar 

  18. Nikovics, K. et al. The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 18, 2929–2945 (2006).

    Article  CAS  Google Scholar 

  19. Hornstein, E. & Shomron, N. Canalization of development by microRNAs. Nat. Genet. 38, S20–S24 (2006).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  21. Gandikota, M. et al. The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J. 49, 683–693 (2007).

    Article  CAS  Google Scholar 

  22. Ingram, C.G. et al. Dual role for fimbriata in regulating floral homeotic genes and cell division in Antirrhinum. EMBO J. 16, 6521–6534 (1997).

    Article  CAS  Google Scholar 

  23. Gomez-Mena, C., de Folter, S., Costa, M.M.R., Angenent, G.C. & Sablowski, R. Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development 132, 429–438 (2005).

    Article  CAS  Google Scholar 

  24. Ingram, G.C. et al. Parallels between unusual floral organs and fimbriata, genes controlling flower development in Arabidopsis and Antirrhinum. Plant Cell 7, 1501–1510 (1995).

    Article  CAS  Google Scholar 

  25. Shigyo, M., Hasebe, M. & Ito, M. Molecular evolution of the AP2 subfamily. Gene 366, 256–265 (2006).

    Article  CAS  Google Scholar 

  26. Mlotshwa, S., Yang, Z., Kim, Y. & Chen, X. Floral patterning defects induced by Arabidopsis APETALA2 and microRNA172 expression in Nicotiana benthamiana. Plant Mol. Biol. 61, 781–793 (2006).

    Article  CAS  Google Scholar 

  27. Van den Broeck, D. et al. Transposon display identifies individual transposable elements in high copy number lines. Plant J. 13, 121–129 (1998).

    CAS  PubMed  Google Scholar 

  28. Valoczi, A., Varallyay, E., Kauppinen, S., Burgyan, J. & Havelda, Z. Spatio-temporal accumulation of microRNAs is highly coordinated in developing plant tissues. Plant J. 47, 140–151 (2006).

    Article  CAS  Google Scholar 

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We thank J. Burgyan for information on in situ analyses with miRNA; J. Stuurman and J. Moore (University of Berne) for the bl-2 allele and B. Davies, P. Huijser, H. Saedler and P. Schulze-Lefert for discussions and comments. This work was supported in part by a grant from the Deutsche Forschungsgemeinschaft/SFB572 (Z.S.-S.).

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Authors and Affiliations



All authors contributed to the experiments, which were conceptually designed mainly by M.V. and Z.S.-S. Z.S.-S. wrote the manuscript, with support from M.V., M.C. and T.G.

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Correspondence to Zsuzsanna Schwarz-Sommer.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Neighbor-joining tree of Antirrhinum, Petunia and Arabidopsis NF-YA family members. (PDF 957 kb)

Supplementary Fig. 2

Detection of the in situ expression patterns of Antirrhinum NF-YA genes by different methods. (PDF 117 kb)

Supplementary Fig. 3

RNA blot analysis of microRNA expression, and analysis of gene expression by qRT-PCR. (PDF 106 kb)

Supplementary Table 1

Position of cleavage sites in the MRE of Antirrhinum and Petunia NF-YA transcripts. (PDF 28 kb)

Supplementary Table 2

Oligonucleotide sequences. (PDF 60 kb)

Supplementary Methods (PDF 66 kb)

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Cartolano, M., Castillo, R., Efremova, N. et al. A conserved microRNA module exerts homeotic control over Petunia hybrida and Antirrhinum majus floral organ identity. Nat Genet 39, 901–905 (2007).

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