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The Flowering Hormone Florigen Functions As a General Systemic Regulator of Growth and Termination

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The Flowering Hormone Florigen Functions As a General Systemic Regulator of Growth and Termination The flowering hormone florigen functions as a general systemic regulator of growth and termination Akiva Shalita, Alexander Rozmana, Alexander Goldshmidtb, John P. Alvarezb, John L. Bowmanc, Yuval Eshedb, and Eliezer Lifschitza,1 aDepartment of Biology, Technion-Israel Institute of Technology, Haifa 32000, Israel; bDepartment of Plant Sciences, Weizmann Institute of Science, Rehovot 76100 Israel; and cSchool of Biological Sciences, Monash University, Melbourne, Victoria 3800, Australia Edited by Elliot M. Meyerowitz, California Institute of Technology, Pasadena, CA, and approved March 9, 2009 (received for review October 27, 2008) The florigen paradigm implies a universal flowering-inducing hor- The tomato plant presents unique opportunities to study multiple mone that is common to all flowering plants. Recent work identified aspects of florigen. Its shoots consist of developmental modules FT orthologues as originators of florigen and their polypeptides as the with homology to monopodial annuals but also feature regular likely systemic agent. However, the developmental processes tar- vegetative/reproductive oscillations typical of woody sympodial geted by florigen remained unknown. Here we identify local balances perennials. Unlike other systems, tomato is photoperiod insensitive, between SINGLE FLOWER TRUSS (SFT), the tomato precursor of thereby eliminating the influence of day length on the functional florigen, and SELF-PRUNING (SP), a potent SFT-dependent SFT inhib- analysis of florigen. Finally, the ease of grafting and a fortunate itor as prime targets of mobile florigen. The graft-transmissible battery of gene mutations can be used to monitor the effects of impacts of florigen on organ-specific traits in perennial tomato show florigen on diverse aspects of growth. Pivotal to the system are SFT, that in addition to import by shoot apical meristems, florigen is encoding florigen (6), and SP, a homologue of TFL1 that promotes imported by organs in which SFT is already expressed. By modulating growth and represses flowering (15–19). Being members of the local SFT/SP balances, florigen confers differential flowering re- same gene family, these 2 CETS (CEN, TFL, SP) genes encode sponses of primary and secondary apical meristems, regulates the signaling factors with multiple options for protein–protein interac- reiterative growth and termination cycles typical of perennial plants, tions (20). For example, the interaction with FD proved essential for accelerates leaf maturation, and influences the complexity of com- the floral-inducing function of FT (21, 22). The interaction of the pound leaves, the growth of stems and the formation of abscission 2 genes with the same proteins (20) and the contrasting flowering PLANT BIOLOGY zones. Florigen is thus established as a plant protein functioning as a modes of primary and sympodial apices of the self-pruning plants general growth hormone. Developmental interactions and a phylo- indicated to us that SP is a major component of the flowering genetic analysis suggest that the SFT/SP regulatory hierarchy is a response mechanism (7). Here we analyze the broad developmental recent evolutionary innovation unique to flowering plants. consequences of changes in the SFT/SP balances as modified, in a context-dependent manner, by the mobile, graft-transmissible form growth hormone ͉ SFT/SP ratio ͉ perennial ͉ compound leaf ͉ of SFT, florigen. Florigen is thus established as a plant protein abscission zone shown to function as a general growth hormone. Results he florigen paradigm was conceived from the study of Tphotoperiod-sensitive plants but implies, in its general form, Context-Specific Termination of Vegetative Growth in Shoot Apical a universal graft-transmissible flowering signal that although Meristems by Florigen. WT tomato plants terminate with a primary activated in leaves by species-specific stimuli is common to all inflorescence after forming 8 to 12 leaves, and subsequent sympo- plants (1–3). Unequivocal evidence for the critical tenets of graft dial units (SUs) consist of 3 leaves and a terminal inflorescence transmissibility and universality of the systemic mechanism was (Fig. 1A). Isogenic sp plants also terminate after 8 to 12 leaves, but obtained in tomato. SFT, the FT homologue encoding florigen subsequent SUs form progressively fewer leaves until the shoot is (4, 5), triggers graft-transmissible signals that complement late terminated by 2 consecutive inflorescences (SI Text, Fig. S1, and flowering in sft plants and substitutes for light dose stimuli in Table S1). It was inferred therefore that the flowering programs for day-neutral tomato and tobacco, for short days in Maryland the primary and sympodial shoots in tomato might be different (7). Mammoth tobacco and for long days in Arabidopsis (6). On the Here we describe the role of SFT and its mobile form, florigen, in the 2 flowering programs. We show that both local SFT and florigen basis of the absence of SFT mRNA beyond the graft joints, we impact differential termination and flowering in the primary and suggested that florigenic signals are generated by cell- sympodial apices. autonomous SFT transcripts. This implicated the protein as a Unlike in sp, termination of the primary shoot in sft is delayed by likely systemic agent (7), which was supported by strong circum- 5 to 6 leaves resulting in a terminating vegetative inflorescence stantial evidence (8–14). However, the developmental mecha- shoot that arrests the sympodial branching, thereby replacing the nisms targeted by florigen to transform vegetative meristems normal sympodial shoot system (SI Text and Fig. S1). Surprisingly, into reproductive organs remain unknown, and their study, by despite the opposite effects of sp and sft on WT shoot architecture, and large, is indifferent to florigen being a protein or RNA. sft single mutants and sft sp double mutants are indistinguishable A clue as to the target of florigen was inferred from the (23). Furthermore, overexpression of SP delays primary termina- observation that overexpression of SFT induces, in addition to tion, increases the number of leaves per SU, and promotes leafy precocious flowering, an overall growth retardation (6). This seemingly trivial phenomenon associated with flowering in many plants might be the consequence of stress upon flowering, but Author contributions: A.S., Y.E., and E.L. designed research; A.S., A.R., A.G., J.P.A., Y.E., and because growth retardation and precocious flowering were trig- E.L. performed research; J.L.B., Y.E., and E.L. analyzed data; and Y.E. and E.L. wrote the gered by a single gene, we hypothesized that they represent 2 facets paper. of the same mechanism. In other words, boosting flowering is just The authors declare no conflict of interest. 1 of the pleiotropic functions of florigen (6). To identify the This article is a PNAS Direct Submission. developmental targets of florigen system-wide, we dissected its 1To whom correspondence should be addressed. E-mail: [email protected]. overall growth effects by using grafting in conjunction with mutants This article contains supporting information online at www.pnas.org/cgi/content/full/ that sensitize organ-specific responses to florigen. 0810810106/DCSupplemental. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0810810106 PNAS Early Edition ͉ 1of6 Downloaded by guest on September 30, 2021 A B CD F G B1 D1 H B2 E D2 Fig. 1. Florigen and SP-dependent termination of apical meristems. (A) A scheme of a WT main shoot of the tomato plant composed of the primary shoot (leaves 1–10) and reiterated SUs (SL1–3). LS, lateral shoot; PL, primary leaf; SL, sympodial leaf. (B) Precocious primary termination and modes of first sympodial branching in MM 35S:SFT transgenic plants. (B1) Normal resumption of sympodial branching, with the first inflorescence (arrow) positioned correctly between 2 leaves (SI Text). (B2) A prospective sympodial bud was permanently suppressed, and growth resumed from a more distal axillary bud. All subsequent SUs consisted of 3 leaves in both modes. (C) A robust 2-leaf sympodial cycling (numbered) in a receptor VFNT plant stimulated by a grafted 35S:SFT donor (arrow). (D and E) Florigen regulates 2 flowering programs in an SP-dependent manner. (D1) sp 35S:SFT plants terminate after 3 leaves, as do 35S:SFT plants, but the terminal inflorescence consists of just 1 or 2 flowers, and subsequent sympodial branching is completely arrested. (D2) Distal lateral shoots of sp 35S:SFT plants (arrow) form 1 or 2 leaves with ‘‘blind’’ apices as shown here, or with terminal flowers as in D1 (arrow). (E) Systemic induction of flowering and termination in a uf sp receptor shoot (boxes mark grafting joint). The induced shoot is terminated after 3 leaves with 2 consecutive flowers (arrow). (F) Florigen is epistatic to late-flowering inflorescence identity genes. mc bl sp plants terminate after more than 20 leaves with 1 abnormal flower with enlarged sepals, and complete arrest of laterals. mc bl sp 35S:SFT plants terminate prematurely with a similar flower (arrow) and serve as ideal donors of florigen (Fig. S4). (G) The main shoot (few laterals removed) of an ever-vegetative, 75-day-old, 2-m-tall uf sft double-mutant plant. (H) Flowering on a 35S:SFT//uf sft graft. The flowering shoot (circle) arose as a lateral from the axil of a receptor leaf below the graft joint. inflorescences (17), but these effects are essentially masked in sft cycles in WT plants, 2 doses are required to maintain it under excess plants (Fig. S2). Thus, the terminating effect of sp is largely relevant of SFT, as suggested by the fluctuation in leaf numbers (between only in the presence of a functional SFT. 1 and 3) per SUs in sp/ϩ35S:SFT plants (Table S1). Significantly, In cultivars such as Money Maker (MM) and VFNT (resistant to all features of sp 35S:SFT were also induced in sp receptors by verticillium wilt, fusarium wilt, nematodes, and tobacco mosaic florigenic SFT signals emanating from a grafted 35S:SFT donor virus), primary shoots of WT plants expressing the constitutive (Fig.
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