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

Abstract

Developmental Highlights-Florigen accelerates SCWB: A prime case for a long-range regulation of a complete metabolic network by a plant hormone.-The dual acceleration of flowering and vascular maturation by Florigen provides a paradigm for a dynamic regulation of global, independent, developmental programs.-The growth termination functions of florigen and the auto-regulatory mechanism for its production and distribution provide a communication network enveloping the shoot system. -A stable florigen provides a possible mechanism for the quantitative regulation of flowering -Lateral stimulation of xylem differentiation links the phloem-travelling florigen with the annual rings in trunks. -MADS genes are common relay partners in Florigen circuits; vascular maturation in stems and reproductive transition in apical meristems. 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-floweringGinkgo 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.

FRUITFULL-like genes regulate flowering time and inflorescence architecture in tomato

“…Although previous overexpression studies suggested that MBP20 functions in leaf development and FUL2 in stem development and secondary growth (Burko et al, 2013; Wang et al, 2014a; Shalit-Kaneh et al, 2019), we did not observe aberrant phenotypes in these tissues in our knockout mutants. The most probable explanation for this discrepancy is the use of the Cauliflower 35S promoter in the previous experiments (Wang et al, 2014a; Shalit-Kaneh et al, 2019), resulting in ectopic expression and mis-regulation of target genes at a position where FUL2 and MBP20 are usually not expressed. Overexpressing MADS-domain proteins or dominant-negative forms of MADS proteins can also perturb complexes that involve their interaction partners, and the phenotype may thus reflect the phenotype of mutants impaired in other, interacting tomato MADS proteins.…”

Plant Inflorescence Architecture: The Formation, Activity, and Fate of Axillary Meristems

“…Mutations in the TFL1 homolog SELF PRUNING (SP) reduces the length of the sympodial unit (numbers of leaves produced) and leads to eventual termination in a cluster of flowers. Termination is more extreme in overexpressors of the tomato FT-homolog SINGLE FLOWER TRUSS (SFT) and near complete when SFT is overexpressed in sp mutants, consistent with the idea that the balance between TFL1 and FT homologs determines the switch between indeterminacy/branching and determinacy/ flower formation (Lifschitz et al 2014;Park et al 2014;Shalit-Kaneh et al 2018). An FT homolog that evolved to act as a flowering repressor, SP5G, also contributes to sympodial growth by repressing onset of reproductive development.…”

Moving on up – controlling internode growth

“…However in dicots, florigens were recently demonstrated to move directly into internodes to influence their development. Shalit‐Kaneh and colleagues showed that grafts overexpressing the tomato FT orthologue, SINGLE FLOWER TRUSS ( SFT ), accelerated vascular maturation in recipient stems, making them shorter and thinner (Shalit‐Kaneh et al , ). This phenotype is consistent with the involvement of florigens in terminal fate, and with FT overexpression in multiple species leading to short stems.…”

“…SINGLE FLOWER TRUSS control of stem growth was independent from its promotion of flowering in tomato (Shalit‐Kaneh et al , ). In fact, differences in rib and intercalary activity are not obligate outcomes of floral fate since these events, including those mediated by DELLAs, can be separated genetically and by responsiveness to seasonal cues (Mazzella et al , ; Serrano‐Mislata et al , ; Gómez‐Ariza et al , ; Kemi et al , ).…”