The Flowering Hormone Florigen Accelerates Secondary Cell Wall Biogenesis to Harmonize Vascular Maturation with Reproductive Development

Abstract

The protein hormone florigen is a universal systemic inducer of flowering and a generic growth terminator across meristems. To understand the developmental rational for its pleiotropic functions and to uncover the deep cellular systems mobilized by florigen beyond flowering we explored termination of radial expansion of stems. Employing the power of tomato genetics along with RNAseq and histological validations we show that endogenous, mobile, or induced florigen accelerates secondary cell wall biogenesis (SCWB), and hence vascular maturation, independently of flowering. This finding is supported by a systemic florigen antagonist from the non-flowering Ginkgo biloba, which arrests SCWB and by MADS and MIF genes downstream of florigen that similarly suppress or enhance, respectively, vascular maturation independent of flowering. We also show that florigen is remarkably stable and distributed to all organs regardless of existing endogenous levels. By accelerating SCWB, florigen reprograms the distribution of resources, signals and mechanical loads required for the ensuing reproductive phase it had originally set into motion.\n\nDevelopmental HighlightsO_LIFlorigen accelerates SCWB: A prime case for a long-range regulation of a complete metabolic network by a plant hormone.\nC_LIO_LIThe dual acceleration of flowering and vascular maturation by Florigen provides a paradigm for a dynamic regulation of global, independent, developmental programs.\nC_LIO_LIThe growth termination functions of florigen and the auto-regulatory mechanism for its production and distribution provide a communication network enveloping the shoot system.\nC_LIO_LIA stable florigen provides a possible mechanism for the quantitative regulation of flowering\nC_LIO_LILateral stimulation of xylem differentiation links the phloem-travelling florigen with the annual rings in trunks.\nC_LIO_LIMADS genes are common relay partners in Florigen circuits; vascular maturation in stems and reproductive transition in apical meristems.\nC_LI