The flowering hormone florigen accelerates secondary cell wall biogenesis to harmonize vascular maturation with reproductive development

• Published in: Proceedings of the National Academy of Sciences - PNAS 2019-08, Vol.116 (32), p.16127-16136
• Main Authors: Shalit-Kaneh, Akiva, Eviatar-Ribak, Tamar, Horev, Guy, Suss, Naomi, Aloni, Roni, Eshed, Yuval, Lifschitz, Eliezer
• Format: Article
• Language: English
• Subjects: Acceleration; Arabidopsis - drug effects; Arabidopsis - physiology; Biological Sciences; Biosynthesis; Cell Wall - drug effects; Cell Wall - metabolism; Cell walls; Florigen - pharmacology; Flowering; Flowering plants; Flowers - physiology; Gene Expression Regulation, Plant - drug effects; Hot Temperature; Lycopersicon esculentum - drug effects; Lycopersicon esculentum - physiology; Maturation; Meristems; Organs; Phase transitions; Photoperiod; Plant Growth Regulators - pharmacology; Plant Proteins - genetics; Plant Proteins - metabolism; Plant Stems - drug effects; Plant Stems - physiology; Plant Vascular Bundle - drug effects; Plant Vascular Bundle - physiology; Plants (botany); PNAS Plus; Reproduction - drug effects; Ribonucleic acid; RNA; Signal processing; Stems; Tomatoes; Transcription; Up-Regulation - drug effects
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1906405116

Florigen, a proteinaceous hormone, functions as a universal long-range promoter of flowering and concurrently as a generic growth-attenuating hormone across leaf and stem meristems. In flowering plants, the transition from the vegetative phase to the reproductive phase entails the orchestration of new growth coordinates and a global redistribution of resources, signals, and mechanical loads among organs. However, the ultimate cellular processes governing the adaptation of the shoot system to reproduction remain unknown. We hypothesized that if the mechanism for floral induction is universal, then the cellular metabolic mechanisms underlying the conditioning of the shoot system for reproduction would also be universal and may be best regulated by florigen itself. To understand the cellular basis for the vegetative functions of florigen, we explored the radial expansion of tomato stems. RNA-Seq and complementary genetic and histological studies revealed that florigen of endogenous, mobile, or induced origins accelerates the transcription network navigating secondary cell wall biogenesis as a unit, promoting vascular maturation and thereby adapting the shoot system to the developmental needs of the ensuing reproductive phase it had originally set into motion. We then demonstrated that a remarkably stable and broadly distributed florigen promotes MADS and MIF genes, which in turn regulate the rate of vascular maturation and radial expansion of stems irrespective of flowering or florigen level. The dual acceleration of flowering and vascular maturation by florigen provides a paradigm for coordinated regulation of independent global developmental programs.