Hormonal control of the inflated calyx syndrome, a morphological novelty, in Physalis

The 'Chinese lantern' phenotype or inflated calyx syndrome (ICS)--inflated sepals encapsulating the mature berry of Physalis floridana--is a morphological novelty within the Solanaceae. ICS is associated with heterotopic expression of MPF2, which codes for a MADS-box transcription factor otherwise involved in leaf formation and male fertility. In accordance with this finding, the MPF2 promoter sequence differs significantly from that of its orthologue STMADS16 in the related Solanum tuberosum, which does not exhibit ICS. However, heterotopic expression of MPF2 is not sufficient for ICS formation in P. floridana- fertilization is also important. Here we report that the hormones cytokinin and gibberellin are essential for ICS formation. MPF2 controls sepal cell division, but the resulting cells are small. Calyx size increases substantially only if gibberellin and cytokinin are available to promote cell elongation and further cell division. Transient expression of appropriate MPF2-/STMADS16-GFP fusions in leaf tissues in the presence of hormones revealed that cytokinin, but not gibberellin, facilitated transport of the transcription factor into the nucleus. Furthermore, an ICS-like structure can be induced in transgenic S. tuberosum by ectopic expression of STMADS16 and simultaneous treatment with cytokinin and gibberellin. Strikingly, transgenic Arabidopsis ectopically expressing solanaceous MPF2-like proteins display enhanced sepal growth when exposed to cytokinin only, while orthologous proteins from non-solanaceous plants did not require cytokinin for this function. These data are incorporated into a detailed model for ICS formation in P. floridana.