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FT and florigen long-distance flowering control in plants
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ScienceDirect FT and florigen long-distance flowering control in plants Joanna Putterill1 and Erika Varkonyi-Gasic2 The great hunt for florigen, the universal, long distance flowering regulator proposed by Chailakhan in the 1930s, resulted in the discovery a decade ago that FT-like proteins fulfilled the predictions for florigen. They are small (175 amino acids), globular, phosphatidylethanolamine-binding (PEBP) proteins, phloem-expressed, graft-transmissible and able to move to the shoot apex to act as potent stimulators of flowering in many plants. Genes that regulate Arabidopsis FT protein movement and some features of Arabidopsis FT protein that make it an effective florigen have recently been identified. Although floral promotion via graft transmission of FT has not been demonstrated in trees, FT-like genes have been successfully applied to reducing the long juvenile (pre-flowering) phase of many trees enabling fast track breeding. Addresses 1 The Flowering Lab, School of Biological Sciences, University of Auckland, Auckland, New Zealand 2 The New Zealand Institute for Plant & Food Research Limited (Plant & Food Research) Mt Albert, Private Bag 92169, Auckland Mail Centre, Auckland 1142, New Zealand Corresponding author: Putterill, Joanna ([email protected])
i. Plants usually have several FT-like genes that play overlapping and/or distinct roles in promoting flowering. For example, FT and TSF promote Arabidopsis flowering, as do Hd3a and RFT1 in rice and GmFT2a and GmFT5a in soybean [9–16]. ii. Some FT-like genes repress flowering (antiflorigens). For example, sugar beet has two FT-like genes, FT1 that represses flowering and FT2 that promotes flowering [17]. iii. The balance of activity of florigens and antiflorigens is important for overall growth, architecture, and/or flowering. This was first elucidated for FT and TFL1like genes in the tomato model [18–20]. iv. Not all FT-like genes regulate flowering. For example, FT gene family members in potato and onion have roles in storage organ differentiation [21,22] and poplar FT genes have diverse roles in seasonal phenology [23]. v. There is diversity in the regulators of FT. For example, CO promotes long day photoperiodic flowering control of Arabidopsis FT and rice CO (Hd1) functions in short day induction of rice FT (Hd3a) and flowering [7]. However, CO-like genes do not regulate FT in all plants including the temperate long day legumes pea and Medicago [10,11,24].
Current Opinion in Plant Biology 2016, 33:77–82 This review comes from a themed issue on Cell signalling and gene regulation Edited by Kimberley Snowden and Dirk Inze´
Building on recent reviews on FT and flowering time control [9–11,19,23,25–28], here we provide an update on two important aspects of FT research; first, how FT functions as a mobile florigen and second the applications of FT/TFL1-like genes to flowering control in woody perennial plants.
http://dx.doi.org/10.1016/j.pbi.2016.06.008 1369-5266/# 2016 Elsevier Ltd. All rights reserved.
Introduction The timing of flowering is critical for successful sexual reproduction, crop productivity and yield [1,2]. A decade ago FT, a gene first described in the pioneering Koornneef paper on late flowering Arabidopsis mutants and then identified as a major integrator of flowering signals, was discovered to encode a protein that functioned as a major florigen — a universal, long distance flowering activator in different plants including tomato, rice and Arabidopsis [3–8]. Today, FT research is progressing in many directions. Some major insights from studies in different plants are: www.sciencedirect.com
Update on FT protein as a major florigen
FT protein was identified in the vascular stream of several annual plants and key proof that mobile FT protein, rather than its RNA, was the major florigen came from experiments performed in tomato, Arabidopsis, rice and cucurbits [3,15,19,29–34]. Once FT protein enters the sieve elements from the phloem companion cells, it travels with the phloem translocation stream to the shoot apex. FT unloads from the phloem and moves cell-to-cell to interact with the bZIP transcription factor FD and switch on the floral development program [6]. An important advance in FT biology in 2011 was the crystal structure of the proposed florigen activation complex (FAC) at the rice shoot apex comprised of two of each FT, FD and 14-3-3 proteins [26,27,35]. The complex stimulates flowering by activating transcription of OsMASDS15 and in Arabidopsis the floral integrator gene SOC1 and the floral meristem identity gene AP1 [6,35]. Current Opinion in Plant Biology 2016, 33:77–82
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The predicted spatio-temporal aspects of the proposed FAC and targets in the rice shoot apex were recently confirmed [36]. FT, as a PEBP protein might also be expected to bind lipids. A recent report demonstrated that FT also binds to the phospholipid phosphatidylcholine in vitro, and in vivo manipulation of phosphatidylcholine availability and type at the Arabidopsis shoot apex affects flowering time, in a partly FT-dependant manner [37]. In addition, 2014 saw the most comprehensive functional mutagenesis on FT protein to date built on previous structural and mutagenesis studies of FT and TFL1 proteins [38]. The effect of overexpression of hundreds of FT point mutations on flowering time was determined. The majority of the mutants remained functional, but inactive and neomorphic mutants were obtained; four new point mutations affected the surface charge of FT, potentially impacting on docking of regulatory ligands such as TCP proteins, converting FT to a TFL1-like repressor. The mechanisms controlling FT movement are not well understood overall. However, in 2013 the first FT mutagenesis to focus on mobility was reported [39]. Triple FT movement mutants carrying mutations at the following residues; V69A, S75A and R82A in pumpkin FTL2 or V70A, S76A and R83A in Arabidopsis FT entered the pumpkin sieve tube system, but did not move beyond the terminal phloem and were unable to stimulate flowering. However, they promoted flowering when expressed throughout the plant. In addition, two mutants in adjacent FT residues in a different region, D17K and V18A, did not accelerate flowering nearly as well from the phloem-specific SUC2 promoter than the CaMV35S or FD (shoot apex specific) promoters, implying a defect in movement [38]. A recent study using micrografting showed that two highly related (82% identical) Arabidopsis FT proteins that promote flowering, FT and TSF, were not equal with regard to their florigenic ability [40]. When over expressed from the CaMV35S promoter, both genes caused transgenic plants to flower very early. However, only CaMV35S:FT rootstocks (donors) could stimulate flowering of grafted ft tsf scions, while CaMV35S:TSF rootstocks virtually lacked activity (Figure 1). Swapping Region 2 of FT (L28-G98) into TSF imbued it with better florigenic activity and chimeric proteins were detectable in the shoot apex. However, insertion of TSF Region 2 into FT did not block FT movement, indicating the influence of other FT regions. Turning to other regulators of FT movement, the Arabidopsis genes FTIP1 and FE both promote flowering in long days and are expressed in the phloem [41,42]. Less FT protein was present in the shoot apex of ftip1 mutant plants because of a reduction in the amount of FT protein entering the sieve elements from the phloem companion Current Opinion in Plant Biology 2016, 33:77–82
cells, while single-leaf induction of FT protein, saw fe mutants accumulating less FT protein in their shoot apices than wild type plants. FTIP1 [41] was first identified as a FT interactor in yeast two hybrid experiments. An in situ Proximity Ligation Assay (PLA) indicated that FTIP1 and FT proteins also interact in phloem companion cells. FTIP1 protein localises to the phloem companion cells and plasmodesmata connecting companion cells and sieve elements. It is an ER-localised membrane protein with a PRT_C membrane-targeting domain and predicted C2 domains reminiscent of membrane-trafficking synaptotagmins and may function as a movement chaperone for FT [19,41]. FE, the last of the classical flowering time genes [5] to be molecularly characterised, encodes a MYB-like transcription factor expressed in the phloem [42]. By promoting the transcription of both FTIP and FT in long days, FE positively influenced the production and transport of FT and the transition to flowering. Genetic analysis found that the fe-1 ftip1-1 double mutant was slightly later flowering than either of the single mutants and it was described as more-than-additive, indicating independent and common functions. Application of FT genes to flowering regulation in trees
Much less is known about regulation of flowering time in woody perennial plants. However, flowering control is of particular interest because of their long juvenile period before they become competent to flower, followed by seasonal vegetative and reproductive growth and coexistence of vegetative and floral meristems on the same shoot. Shortened juvenility and precocious flowering are important breeding goals in fruit trees and vines; on the other hand, understanding flowering-time regulation can provide practical means to prevent flowering to improve the biomass and quality of wood in forestry and biofuel crops. Here, we focus on regulation of flowering with FT genes and their perceived role as florigen in woody perennials. Ample evidence confirms the role of some FT genes as activators of flowering in woody perennial plants. For example, constitutive expression of endogenous FT genes in poplar and citrus resulted in early flowering [43,44]. Similarly constitutive expression of Arabidopsis FT promoted flowering in Eucalyptus [45] as did expression from a heat-inducible promoter in juvenile poplar [43] (Figure 2) or by viral delivery into cotton, apple and pear [46,47,48,49]. Constitutive expression of poplar FT1 also gave early maturity and continuous flowering in plum [50] and its inducible expression promoted flowering in apple [51] (Figure 2). Studies in woody perennials also highlight the importance of TFL1-like repressor genes in flowering. Down regulation of TFL1 accelerated the onset of first flowering in www.sciencedirect.com
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Greater florigenic activity of FT compared to TSF demonstrated by grafting in Arabidopsis. Very late flowering Arabidopsis ft tsf double mutant, homo-grafted, produces a high number of leaves before flowering (left), a grafted plant with CaMV35S:TSF rootstock and ft tsf scion flowers slightly more rapidly (middle), but is still very delayed compared to the very early flowering grafted plant with CaMV35S:AtFT rootstock and ft tsf scion (right).
poplar, apple and pear [52–54]. Using virus delivery, simultaneous down regulation of TFL1 combined with over expression of Arabidopsis FT greatly increased the efficiency of floral promotion in apple and pear and led to continuous flowering [48,49].
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Indirect evidence on possible mobility of FT protein over long distances in woody perennials is very scarce. There are no reports on detection of FT in the phloem or xylem sap in perennials. Some answers have been provided by a recent study of mobility of pear FT-like protein PcFT2 in tobacco and apple [56]. Ectopic expression of PcFT2 fused to YFP promoted flowering in tobacco, this effect was graft-transmissible and the fusion protein, but not PcFT2 RNA, was identified in the non-transgenic scion. In a similar experiment in apple, movement of the fusion protein was detected. Although it did not promote flowering, this indicated the presence of the mechanism for FT movement in the vascular tissue in woody perennials. The accessibility of signal conduits provides one possible regulatory mechanism for intercellular signal delivery in trees; reopening of conduits and transcription of FT are www.sciencedirect.com
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Remarkably, there is little evidence that any FT protein (or RNA) moves in trees. One exception is graft-transmissible early flowering in a small woody shrub Jatropha [55]. Expression of Jatropha JcFT under the control of the relatively weak synthetic G10-90 promoter reduced flowering time from 8 months to 1–2 months and induced early flowering in non-transgenic scions (Figure 3). By contrast, grafting experiments in poplar and apple with rootstocks expressing FT transgenes under the control of a heat-shock inducible promoter did not result in flowering in receptor scions [43,51] (Figure 2).
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FT induced by heat shock promotes flowering in transgenic apple and poplar but not by grafting. Upper panel: Poplar plants; wild type (left), early flowering heat-shocked pHSP:AtFT plants with Arabidopsis FT expressed from the heat shock promoter (middle) and non-flowering heat-induced grafted plants with pHSP:AtFT rootstock and wild type scion (right). Lower panel: Apple plants; wild type (left), early flowering plants after heat shock induction of pHSP:PtFT1 (Populus trichocarpa (poplar) FT), (middle) and non-flowering heat-shocked grafted plants with pHSP:PtFT1 rootstock grafted to a wild type scion (right). Double lines indicate the graft junction.
believed to jointly regulate growth and dormancy cycles in poplar [57]. Perspectives
In annual plants, there has been recent progress on the mechanisms of long distance FT protein transport and FT floral promotion at the shoot apex. FT stability [40,58], shape, size, ability to pass through plasmodesmata or interact with the phloem transport machinery, such as FTIP1, and/or other regulators including the justdescribed NaKR1 [59] are all likely to contribute to florigenic potential. The specifics of how FT movement is controlled beyond the terminal phloem into the shoot apex remains a gap in knowledge. Current Opinion in Plant Biology 2016, 33:77–82
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Figure 3
Acknowledgements We thank Andrew Allan and Karine David for interesting discussions and apologise to authors not cited due to word and reference limits. The research on flowering in our labs was funded by the New Zealand Foundation for Research Science and Technology (http://www.msi.govt.nz/) contract number C10X0816 MeriNET and in addition for JP the New Zealand Marsden Fund (http://www.royalsociety.org.nz/programmes/funds/ marsden/) contracts 10-UOA-200 and 14-UOA-125.
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References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as: of special interest of outstanding interest
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Florigenic activity of Jatropha FT demonstrated by grafting in the woody shrub Jatropha. Jatropha curcus plants; wild type-flowering of grafted plant with wild type rootstock and high oleic acid (X8-34) transgenic Jatropha scion (left), earlier flowering transgenic plant with pG10-90:JcFT construct (middle) and earlier flowering grafted plant with pG10-90:JcFT rootstock and high oleic acid (X8-34) transgenic Jatropha scion (right). Double lines indicate the graft junction.
In trees, some FT transgenes strongly activate flowering and greatly reduce the juvenile stage. However, these traits cannot be transmitted by grafting. The most feasible explanation for these observations is the difference in size and physiology of annual plants and shrubs compared to trees, may impact on the long-distance signal speed and effectiveness. Alternatively, FT protein may not be transported from source leaf into the shoot apex, but into other, closer or stronger sinks. Turning to applications, the hope is that detailed knowledge and testing of FT and TFL1-like genes will allow customisation of aspects of plant flowering, architecture, growth and yield from annuals to woody perennials [1,2,19,27]. For example, this has been demonstrated with fruit yield in tomato [60]. One aim is a Fast Track Tree Breeding scheme [50,51] where FT-induced rapid flowering trees are crossed with trees with High Value Traits (HVT). HVT trees that flower rapidly and continuously can then be readily crossed with other HVT trees enabling rapid breeding and selections. Future general challenges in investigating the biology of FT and flowering include understanding the functional diversification of the multiple FT-like genes in plants, of regulators of FT genes, of proteins that regulate or interact with FT/TFL1-like proteins and/or potential target genes. For example, the FT–FD complex in poplar is involved in photoperiodic control of seasonal growth, but has not yet been associated with flowering [61]. Current Opinion in Plant Biology 2016, 33:77–82
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40. Jin S, Jung HS, Chung KS, Lee JH, Ahn JH: FLOWERING LOCUS T has higher protein mobility than TWIN SISTER of FT. J Exp Bot 2015, 66:6109-6117. By directly comparing the florigenic potential of proteins by grafting, Arabidopsis FT and FT/TSF chimeric proteins are shown to function as superior florigens compared to TSF, a closely related paralogue of FT. 41. Liu L, Liu C, Hou X, Xi W, Shen L, Tao Z, Wang Y, Yu H: FTIP1 is an essential regulator required for florigen transport. PLoS Biol 2012:10. 42. Abe M, Kaya H, Watanabe-Taneda A, Shibuta M, Yamaguchi A, Sakamoto T, Kurata T, Ausı´n I, Araki T, Alonso-Blanco C: FE, a phloem-specific Myb-related protein, promotes flowering through transcriptional activation of FLOWERING LOCUS T and FLOWERING LOCUS T INTERACTING PROTEIN 1. Plant J 2015, 83:1059-1068. The FE gene promotes Arabidopsis flowering, the expression of FT and FTIP1 and FT protein transport to the shoot tip. This study provides insights into the coordination of FT transport by phloem factors. 43. Zhang HL, Harry DE, Ma C, Yuceer C, Hsu CY, Vikram V, Shevchenko O, Etherington E, Strauss SH: Precocious flowering in trees: the FLOWERING LOCUS T gene as a research and breeding tool in Populus. J Exp Bot 2010, 61:2549-2560. 44. Endo T, Shimada T, Fujii H, Kobayashi Y, Araki T, Omura M: Ectopic expression of an FT homolog from citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliata L. Raf.). Transgenic Res 2005, 14:703-712. 45. Klocko AL, Ma C, Robertson S, Esfandiari E, Nilsson O, Strauss SH: FT overexpression induces precocious flowering and normal reproductive development in Eucalyptus. Plant Biotechnol J 2016, 14:808-819. 46. Yamagishi N, Sasaki S, Yamagata K, Komori S, Nagase M, Wada M, Yamamoto T, Yoshikawa N: Promotion of flowering and reduction of a generation time in apple seedlings by ectopical expression of the Arabidopsis thaliana FT gene using the Apple latent spherical virus vector. Plant Mol Biol 2011, 75:193-204. 47. McGarry RC, Ayre BG: Geminivirus-mediated delivery of florigen promotes determinate growth in aerial organs and uncouples flowering from photoperiod in cotton. PLoS ONE 2012, 7:e36746. 48. Yamagishi N, Li C, Yoshikawa N: Promotion of flowering by Apple latent spherical virus vector and virus elimination at high temperature allow accelerated breeding of apple and pear. Front Plant Sci 2016:7. 49. Yamagishi N, Kishigami R, Yoshikawa N: Reduced generation time of apple seedlings to within a year by means of a plant virus vector: a new plant-breeding technique with no transmission of genetic modification to the next generation. Plant Biotechnol J 2014, 12:60-68. Infection of apple seed embryos with an ALSV vector (ALSV-AtFT/ MdTFL1) simultaneously expressing the Arabidopsis thaliana florigen (AtFT) gene and suppressing the apple MdTFL1-1 gene dramatically reduces juvenility and promotes continuous flowering. The results of this study together with Ref. [48] suggest a convenient way of reducing the breeding cycle of fruit trees and readily eliminating the viral vector by heat treatment. 50. Srinivasan C, Dardick C, Callahan A, Scorza R: Plum (Prunus domestica) trees transformed with poplar FT1 result in altered architecture, dormancy requirement, and continuous flowering. PLoS ONE 2012, 7:e40715. 51. Wenzel S, Flachowsky H, Hanke M-V: The Fast-track breeding approach can be improved by heat-induced expression of the FLOWERING LOCUS T genes from poplar (Populus trichocarpa) in apple (Malus domestica Borkh.). Plant Cell Tissue Organ Culture 2013, 115:127-137. Current Opinion in Plant Biology 2016, 33:77–82
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The authors have demonstrated movement of an FT–YFP fusion protein across the graft union in tobacco and apple, suggesting that FT may act as a mobile developmental signal in both annuals and trees. 57. Rinne PL, Welling A, Vahala J, Ripel L, Ruonala R, Kangasjarvi J, van der Schoot C: Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1,3-betaglucanases to reopen signal conduits and release dormancy in Populus. Plant Cell 2011, 23:130-146. 58. Kim S-J, Hong Sung M, Yoo Seong J, Moon S, Jung Hye S, Ahn Ji H: Post-translational regulation of FLOWERING LOCUS T protein in Arabidopsis. Mol Plant 2016, 9:308-311. 59. Zhu Y, Liu L, Shen L, Yu H: NaKR1 regulates long-distance movement of FLOWERING LOCUS T in Arabidopsis. Nat Plants 2016, 2:16075. 60. Park SJ, Jiang K, Tal L, Yichie Y, Gar O, Zamir D, Eshed Y, Lippman ZB: Optimization of crop productivity in tomato using induced mutations in the florigen pathway. Nat Genetics 2014, 46:1337-1342. 61. Tylewicz S, Tsuji H, Miskolczi P, Petterle A, Azeez A, Jonsson K, Shimamoto K, Bhalerao RP: Dual role of tree florigen activation complex component FD in photoperiodic growth control and adaptive response pathways. Proc Natl Acad Sci U S A 2015, 112:3140-3145.
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ScienceDirect FT and florigen long-distance flowering control in plants Joanna Putterill1 and Erika Varkonyi-Gasic2 The great hunt for florigen, the universal, long distance flowering regulator proposed by Chailakhan in the 1930s, resulted in the discovery a decade ago that FT-like proteins fulfilled the predictions for florigen. They are small (175 amino acids), globular, phosphatidylethanolamine-binding (PEBP) proteins, phloem-expressed, graft-transmissible and able to move to the shoot apex to act as potent stimulators of flowering in many plants. Genes that regulate Arabidopsis FT protein movement and some features of Arabidopsis FT protein that make it an effective florigen have recently been identified. Although floral promotion via graft transmission of FT has not been demonstrated in trees, FT-like genes have been successfully applied to reducing the long juvenile (pre-flowering) phase of many trees enabling fast track breeding. Addresses 1 The Flowering Lab, School of Biological Sciences, University of Auckland, Auckland, New Zealand 2 The New Zealand Institute for Plant & Food Research Limited (Plant & Food Research) Mt Albert, Private Bag 92169, Auckland Mail Centre, Auckland 1142, New Zealand Corresponding author: Putterill, Joanna ([email protected])
i. Plants usually have several FT-like genes that play overlapping and/or distinct roles in promoting flowering. For example, FT and TSF promote Arabidopsis flowering, as do Hd3a and RFT1 in rice and GmFT2a and GmFT5a in soybean [9–16]. ii. Some FT-like genes repress flowering (antiflorigens). For example, sugar beet has two FT-like genes, FT1 that represses flowering and FT2 that promotes flowering [17]. iii. The balance of activity of florigens and antiflorigens is important for overall growth, architecture, and/or flowering. This was first elucidated for FT and TFL1like genes in the tomato model [18–20]. iv. Not all FT-like genes regulate flowering. For example, FT gene family members in potato and onion have roles in storage organ differentiation [21,22] and poplar FT genes have diverse roles in seasonal phenology [23]. v. There is diversity in the regulators of FT. For example, CO promotes long day photoperiodic flowering control of Arabidopsis FT and rice CO (Hd1) functions in short day induction of rice FT (Hd3a) and flowering [7]. However, CO-like genes do not regulate FT in all plants including the temperate long day legumes pea and Medicago [10,11,24].
Current Opinion in Plant Biology 2016, 33:77–82 This review comes from a themed issue on Cell signalling and gene regulation Edited by Kimberley Snowden and Dirk Inze´
Building on recent reviews on FT and flowering time control [9–11,19,23,25–28], here we provide an update on two important aspects of FT research; first, how FT functions as a mobile florigen and second the applications of FT/TFL1-like genes to flowering control in woody perennial plants.
http://dx.doi.org/10.1016/j.pbi.2016.06.008 1369-5266/# 2016 Elsevier Ltd. All rights reserved.
Introduction The timing of flowering is critical for successful sexual reproduction, crop productivity and yield [1,2]. A decade ago FT, a gene first described in the pioneering Koornneef paper on late flowering Arabidopsis mutants and then identified as a major integrator of flowering signals, was discovered to encode a protein that functioned as a major florigen — a universal, long distance flowering activator in different plants including tomato, rice and Arabidopsis [3–8]. Today, FT research is progressing in many directions. Some major insights from studies in different plants are: www.sciencedirect.com
Update on FT protein as a major florigen
FT protein was identified in the vascular stream of several annual plants and key proof that mobile FT protein, rather than its RNA, was the major florigen came from experiments performed in tomato, Arabidopsis, rice and cucurbits [3,15,19,29–34]. Once FT protein enters the sieve elements from the phloem companion cells, it travels with the phloem translocation stream to the shoot apex. FT unloads from the phloem and moves cell-to-cell to interact with the bZIP transcription factor FD and switch on the floral development program [6]. An important advance in FT biology in 2011 was the crystal structure of the proposed florigen activation complex (FAC) at the rice shoot apex comprised of two of each FT, FD and 14-3-3 proteins [26,27,35]. The complex stimulates flowering by activating transcription of OsMASDS15 and in Arabidopsis the floral integrator gene SOC1 and the floral meristem identity gene AP1 [6,35]. Current Opinion in Plant Biology 2016, 33:77–82
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The predicted spatio-temporal aspects of the proposed FAC and targets in the rice shoot apex were recently confirmed [36]. FT, as a PEBP protein might also be expected to bind lipids. A recent report demonstrated that FT also binds to the phospholipid phosphatidylcholine in vitro, and in vivo manipulation of phosphatidylcholine availability and type at the Arabidopsis shoot apex affects flowering time, in a partly FT-dependant manner [37]. In addition, 2014 saw the most comprehensive functional mutagenesis on FT protein to date built on previous structural and mutagenesis studies of FT and TFL1 proteins [38]. The effect of overexpression of hundreds of FT point mutations on flowering time was determined. The majority of the mutants remained functional, but inactive and neomorphic mutants were obtained; four new point mutations affected the surface charge of FT, potentially impacting on docking of regulatory ligands such as TCP proteins, converting FT to a TFL1-like repressor. The mechanisms controlling FT movement are not well understood overall. However, in 2013 the first FT mutagenesis to focus on mobility was reported [39]. Triple FT movement mutants carrying mutations at the following residues; V69A, S75A and R82A in pumpkin FTL2 or V70A, S76A and R83A in Arabidopsis FT entered the pumpkin sieve tube system, but did not move beyond the terminal phloem and were unable to stimulate flowering. However, they promoted flowering when expressed throughout the plant. In addition, two mutants in adjacent FT residues in a different region, D17K and V18A, did not accelerate flowering nearly as well from the phloem-specific SUC2 promoter than the CaMV35S or FD (shoot apex specific) promoters, implying a defect in movement [38]. A recent study using micrografting showed that two highly related (82% identical) Arabidopsis FT proteins that promote flowering, FT and TSF, were not equal with regard to their florigenic ability [40]. When over expressed from the CaMV35S promoter, both genes caused transgenic plants to flower very early. However, only CaMV35S:FT rootstocks (donors) could stimulate flowering of grafted ft tsf scions, while CaMV35S:TSF rootstocks virtually lacked activity (Figure 1). Swapping Region 2 of FT (L28-G98) into TSF imbued it with better florigenic activity and chimeric proteins were detectable in the shoot apex. However, insertion of TSF Region 2 into FT did not block FT movement, indicating the influence of other FT regions. Turning to other regulators of FT movement, the Arabidopsis genes FTIP1 and FE both promote flowering in long days and are expressed in the phloem [41,42]. Less FT protein was present in the shoot apex of ftip1 mutant plants because of a reduction in the amount of FT protein entering the sieve elements from the phloem companion Current Opinion in Plant Biology 2016, 33:77–82
cells, while single-leaf induction of FT protein, saw fe mutants accumulating less FT protein in their shoot apices than wild type plants. FTIP1 [41] was first identified as a FT interactor in yeast two hybrid experiments. An in situ Proximity Ligation Assay (PLA) indicated that FTIP1 and FT proteins also interact in phloem companion cells. FTIP1 protein localises to the phloem companion cells and plasmodesmata connecting companion cells and sieve elements. It is an ER-localised membrane protein with a PRT_C membrane-targeting domain and predicted C2 domains reminiscent of membrane-trafficking synaptotagmins and may function as a movement chaperone for FT [19,41]. FE, the last of the classical flowering time genes [5] to be molecularly characterised, encodes a MYB-like transcription factor expressed in the phloem [42]. By promoting the transcription of both FTIP and FT in long days, FE positively influenced the production and transport of FT and the transition to flowering. Genetic analysis found that the fe-1 ftip1-1 double mutant was slightly later flowering than either of the single mutants and it was described as more-than-additive, indicating independent and common functions. Application of FT genes to flowering regulation in trees
Much less is known about regulation of flowering time in woody perennial plants. However, flowering control is of particular interest because of their long juvenile period before they become competent to flower, followed by seasonal vegetative and reproductive growth and coexistence of vegetative and floral meristems on the same shoot. Shortened juvenility and precocious flowering are important breeding goals in fruit trees and vines; on the other hand, understanding flowering-time regulation can provide practical means to prevent flowering to improve the biomass and quality of wood in forestry and biofuel crops. Here, we focus on regulation of flowering with FT genes and their perceived role as florigen in woody perennials. Ample evidence confirms the role of some FT genes as activators of flowering in woody perennial plants. For example, constitutive expression of endogenous FT genes in poplar and citrus resulted in early flowering [43,44]. Similarly constitutive expression of Arabidopsis FT promoted flowering in Eucalyptus [45] as did expression from a heat-inducible promoter in juvenile poplar [43] (Figure 2) or by viral delivery into cotton, apple and pear [46,47,48,49]. Constitutive expression of poplar FT1 also gave early maturity and continuous flowering in plum [50] and its inducible expression promoted flowering in apple [51] (Figure 2). Studies in woody perennials also highlight the importance of TFL1-like repressor genes in flowering. Down regulation of TFL1 accelerated the onset of first flowering in www.sciencedirect.com
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Greater florigenic activity of FT compared to TSF demonstrated by grafting in Arabidopsis. Very late flowering Arabidopsis ft tsf double mutant, homo-grafted, produces a high number of leaves before flowering (left), a grafted plant with CaMV35S:TSF rootstock and ft tsf scion flowers slightly more rapidly (middle), but is still very delayed compared to the very early flowering grafted plant with CaMV35S:AtFT rootstock and ft tsf scion (right).
poplar, apple and pear [52–54]. Using virus delivery, simultaneous down regulation of TFL1 combined with over expression of Arabidopsis FT greatly increased the efficiency of floral promotion in apple and pear and led to continuous flowering [48,49].
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Indirect evidence on possible mobility of FT protein over long distances in woody perennials is very scarce. There are no reports on detection of FT in the phloem or xylem sap in perennials. Some answers have been provided by a recent study of mobility of pear FT-like protein PcFT2 in tobacco and apple [56]. Ectopic expression of PcFT2 fused to YFP promoted flowering in tobacco, this effect was graft-transmissible and the fusion protein, but not PcFT2 RNA, was identified in the non-transgenic scion. In a similar experiment in apple, movement of the fusion protein was detected. Although it did not promote flowering, this indicated the presence of the mechanism for FT movement in the vascular tissue in woody perennials. The accessibility of signal conduits provides one possible regulatory mechanism for intercellular signal delivery in trees; reopening of conduits and transcription of FT are www.sciencedirect.com
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Remarkably, there is little evidence that any FT protein (or RNA) moves in trees. One exception is graft-transmissible early flowering in a small woody shrub Jatropha [55]. Expression of Jatropha JcFT under the control of the relatively weak synthetic G10-90 promoter reduced flowering time from 8 months to 1–2 months and induced early flowering in non-transgenic scions (Figure 3). By contrast, grafting experiments in poplar and apple with rootstocks expressing FT transgenes under the control of a heat-shock inducible promoter did not result in flowering in receptor scions [43,51] (Figure 2).
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FT induced by heat shock promotes flowering in transgenic apple and poplar but not by grafting. Upper panel: Poplar plants; wild type (left), early flowering heat-shocked pHSP:AtFT plants with Arabidopsis FT expressed from the heat shock promoter (middle) and non-flowering heat-induced grafted plants with pHSP:AtFT rootstock and wild type scion (right). Lower panel: Apple plants; wild type (left), early flowering plants after heat shock induction of pHSP:PtFT1 (Populus trichocarpa (poplar) FT), (middle) and non-flowering heat-shocked grafted plants with pHSP:PtFT1 rootstock grafted to a wild type scion (right). Double lines indicate the graft junction.
believed to jointly regulate growth and dormancy cycles in poplar [57]. Perspectives
In annual plants, there has been recent progress on the mechanisms of long distance FT protein transport and FT floral promotion at the shoot apex. FT stability [40,58], shape, size, ability to pass through plasmodesmata or interact with the phloem transport machinery, such as FTIP1, and/or other regulators including the justdescribed NaKR1 [59] are all likely to contribute to florigenic potential. The specifics of how FT movement is controlled beyond the terminal phloem into the shoot apex remains a gap in knowledge. Current Opinion in Plant Biology 2016, 33:77–82
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Figure 3
Acknowledgements We thank Andrew Allan and Karine David for interesting discussions and apologise to authors not cited due to word and reference limits. The research on flowering in our labs was funded by the New Zealand Foundation for Research Science and Technology (http://www.msi.govt.nz/) contract number C10X0816 MeriNET and in addition for JP the New Zealand Marsden Fund (http://www.royalsociety.org.nz/programmes/funds/ marsden/) contracts 10-UOA-200 and 14-UOA-125.
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References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as: of special interest of outstanding interest
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Florigenic activity of Jatropha FT demonstrated by grafting in the woody shrub Jatropha. Jatropha curcus plants; wild type-flowering of grafted plant with wild type rootstock and high oleic acid (X8-34) transgenic Jatropha scion (left), earlier flowering transgenic plant with pG10-90:JcFT construct (middle) and earlier flowering grafted plant with pG10-90:JcFT rootstock and high oleic acid (X8-34) transgenic Jatropha scion (right). Double lines indicate the graft junction.
In trees, some FT transgenes strongly activate flowering and greatly reduce the juvenile stage. However, these traits cannot be transmitted by grafting. The most feasible explanation for these observations is the difference in size and physiology of annual plants and shrubs compared to trees, may impact on the long-distance signal speed and effectiveness. Alternatively, FT protein may not be transported from source leaf into the shoot apex, but into other, closer or stronger sinks. Turning to applications, the hope is that detailed knowledge and testing of FT and TFL1-like genes will allow customisation of aspects of plant flowering, architecture, growth and yield from annuals to woody perennials [1,2,19,27]. For example, this has been demonstrated with fruit yield in tomato [60]. One aim is a Fast Track Tree Breeding scheme [50,51] where FT-induced rapid flowering trees are crossed with trees with High Value Traits (HVT). HVT trees that flower rapidly and continuously can then be readily crossed with other HVT trees enabling rapid breeding and selections. Future general challenges in investigating the biology of FT and flowering include understanding the functional diversification of the multiple FT-like genes in plants, of regulators of FT genes, of proteins that regulate or interact with FT/TFL1-like proteins and/or potential target genes. For example, the FT–FD complex in poplar is involved in photoperiodic control of seasonal growth, but has not yet been associated with flowering [61]. Current Opinion in Plant Biology 2016, 33:77–82
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40. Jin S, Jung HS, Chung KS, Lee JH, Ahn JH: FLOWERING LOCUS T has higher protein mobility than TWIN SISTER of FT. J Exp Bot 2015, 66:6109-6117. By directly comparing the florigenic potential of proteins by grafting, Arabidopsis FT and FT/TSF chimeric proteins are shown to function as superior florigens compared to TSF, a closely related paralogue of FT. 41. Liu L, Liu C, Hou X, Xi W, Shen L, Tao Z, Wang Y, Yu H: FTIP1 is an essential regulator required for florigen transport. PLoS Biol 2012:10. 42. Abe M, Kaya H, Watanabe-Taneda A, Shibuta M, Yamaguchi A, Sakamoto T, Kurata T, Ausı´n I, Araki T, Alonso-Blanco C: FE, a phloem-specific Myb-related protein, promotes flowering through transcriptional activation of FLOWERING LOCUS T and FLOWERING LOCUS T INTERACTING PROTEIN 1. Plant J 2015, 83:1059-1068. The FE gene promotes Arabidopsis flowering, the expression of FT and FTIP1 and FT protein transport to the shoot tip. This study provides insights into the coordination of FT transport by phloem factors. 43. Zhang HL, Harry DE, Ma C, Yuceer C, Hsu CY, Vikram V, Shevchenko O, Etherington E, Strauss SH: Precocious flowering in trees: the FLOWERING LOCUS T gene as a research and breeding tool in Populus. J Exp Bot 2010, 61:2549-2560. 44. Endo T, Shimada T, Fujii H, Kobayashi Y, Araki T, Omura M: Ectopic expression of an FT homolog from citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliata L. Raf.). Transgenic Res 2005, 14:703-712. 45. Klocko AL, Ma C, Robertson S, Esfandiari E, Nilsson O, Strauss SH: FT overexpression induces precocious flowering and normal reproductive development in Eucalyptus. Plant Biotechnol J 2016, 14:808-819. 46. Yamagishi N, Sasaki S, Yamagata K, Komori S, Nagase M, Wada M, Yamamoto T, Yoshikawa N: Promotion of flowering and reduction of a generation time in apple seedlings by ectopical expression of the Arabidopsis thaliana FT gene using the Apple latent spherical virus vector. Plant Mol Biol 2011, 75:193-204. 47. McGarry RC, Ayre BG: Geminivirus-mediated delivery of florigen promotes determinate growth in aerial organs and uncouples flowering from photoperiod in cotton. PLoS ONE 2012, 7:e36746. 48. Yamagishi N, Li C, Yoshikawa N: Promotion of flowering by Apple latent spherical virus vector and virus elimination at high temperature allow accelerated breeding of apple and pear. Front Plant Sci 2016:7. 49. Yamagishi N, Kishigami R, Yoshikawa N: Reduced generation time of apple seedlings to within a year by means of a plant virus vector: a new plant-breeding technique with no transmission of genetic modification to the next generation. Plant Biotechnol J 2014, 12:60-68. Infection of apple seed embryos with an ALSV vector (ALSV-AtFT/ MdTFL1) simultaneously expressing the Arabidopsis thaliana florigen (AtFT) gene and suppressing the apple MdTFL1-1 gene dramatically reduces juvenility and promotes continuous flowering. The results of this study together with Ref. [48] suggest a convenient way of reducing the breeding cycle of fruit trees and readily eliminating the viral vector by heat treatment. 50. Srinivasan C, Dardick C, Callahan A, Scorza R: Plum (Prunus domestica) trees transformed with poplar FT1 result in altered architecture, dormancy requirement, and continuous flowering. PLoS ONE 2012, 7:e40715. 51. Wenzel S, Flachowsky H, Hanke M-V: The Fast-track breeding approach can be improved by heat-induced expression of the FLOWERING LOCUS T genes from poplar (Populus trichocarpa) in apple (Malus domestica Borkh.). Plant Cell Tissue Organ Culture 2013, 115:127-137. Current Opinion in Plant Biology 2016, 33:77–82
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The authors have demonstrated movement of an FT–YFP fusion protein across the graft union in tobacco and apple, suggesting that FT may act as a mobile developmental signal in both annuals and trees. 57. Rinne PL, Welling A, Vahala J, Ripel L, Ruonala R, Kangasjarvi J, van der Schoot C: Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1,3-betaglucanases to reopen signal conduits and release dormancy in Populus. Plant Cell 2011, 23:130-146. 58. Kim S-J, Hong Sung M, Yoo Seong J, Moon S, Jung Hye S, Ahn Ji H: Post-translational regulation of FLOWERING LOCUS T protein in Arabidopsis. Mol Plant 2016, 9:308-311. 59. Zhu Y, Liu L, Shen L, Yu H: NaKR1 regulates long-distance movement of FLOWERING LOCUS T in Arabidopsis. Nat Plants 2016, 2:16075. 60. Park SJ, Jiang K, Tal L, Yichie Y, Gar O, Zamir D, Eshed Y, Lippman ZB: Optimization of crop productivity in tomato using induced mutations in the florigen pathway. Nat Genetics 2014, 46:1337-1342. 61. Tylewicz S, Tsuji H, Miskolczi P, Petterle A, Azeez A, Jonsson K, Shimamoto K, Bhalerao RP: Dual role of tree florigen activation complex component FD in photoperiodic growth control and adaptive response pathways. Proc Natl Acad Sci U S A 2015, 112:3140-3145.
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