Inhibiting the inhibitor to allow flowering in Citrus: the seasonal epigenetic resetting of CcMADS19

Citrus trees are polycarpic species that only produce single flowers or determinate inflorescences, so that vegetative growth is required at the axillary buds to renew the polycarpic habit. In addition, in some species/cultivars the presence of fruits inhibits sprouting and flower induction from nearby axillary buds in the current season. This results in low flowering intensity the following spring, thus giving rise to alternate bearing. Our previous results show that the presence of the fruit correlates with epigenetic changes in CcMADS19 (Citrus clementina FLC ortholog), which prevent the activation of the floral promoter CiFT3 (Citrus clementina FT ortholog) in the leaf, even in the presence of the floral inductive signals (i.e., cold temperatures). To reestablish the flowering ability, the axillary bud maintains a silenced version of CcMADS19 which is mitotically transmitted to the new vegetative shoots, thereby allowing the activation of CiFT3 during the following cold season. This mechanism operates through changes in H3K27me3 and methyltransferase activity. On the other hand, gibberellin (GAs) have always been considered the main flowering inhibitor in Citrus. But, how are GAs related to the CcMADS19 transcription factor? Our results show no relationship between GAs and CcMADS19 gene expression, and suggest that GAs act downstream of CcMADS19. In this paper, we converge the hormonal hypothesis with the genetic and epigenetic evidences in the control of Citrus flowering. In summary, we propose the view of flowering as a repressive process: new buds are competent to flower, but this default state is reversed -or transiently repressed- by inhibitory signals (due to fruit). And the promotion of flowering would involve the upstream repression of this inhibition. In other words, the so-called “promoters of flowering” might be “inhibitors of flowering inhibitors”.