Conserved function of FLOWERING LOCUS T (FT) homologues as signals for storage organ differentiation

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ScienceDirect Conserved function of FLOWERING LOCUS T (FT) homologues as signals for storage organ differentiation Cristina Navarro1, Eduard Cruz-Oro´1 and Salome´ Prat Due to their high carbohydrate content and relative low farming demands, tuber-bearing species are an important contribution to human dietary needs in many climatic zones, and interest in these staple crops for processed food and other industrial uses is increasing. Over the past years we have seen remarkable advances in our understanding of the signalling mechanisms involved in the differentiation of these organs, partly aided by their conservation with the well-characterized photoperiodic control of flowering in Arabidopsis. Recent studies have led to the identification of members of the FT gene family as major component of the tuber-inducing signal and the characterization of circadian and photoperiodic components involved in the regulation of these genes. A relevant role of microRNAs in the control of storage organ formation has been established, and hormonal balance requirements similar to those controlling shoot branching were shown to be implicated in the activation of stolon meristem cells. Hence, the recent finding that FT controls branching through direct interaction with the TCP factors holds great promise for the identification of genes acting as FT signal integrators in the stolon. Addresses Dpt. Plant Molecular Genetics, Centro Nacional de Biotecnologı´a-CSIC, Darwin 3, 28049 Madrid, Spain Corresponding author: Prat, Salome´ ([email protected]) These authors equally contributed to this work.

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Current Opinion in Plant Biology 2015, 23:45–53 This review comes from a themed issue on Growth and development Edited by Niko Geldner and Sigal Savaldi-Goldstein

http://dx.doi.org/10.1016/j.pbi.2014.10.008 1369-5266/# 2014 Elsevier Ltd. All right reserved.

Introduction During evolution, a number of plant species have acquired the ability to differentiate their leaves, stems or roots into storage organs, as observed in onion and garlic bulbs, potato and kohlrabi tubers, sugar beet taproots, sweet potato and cassava tuberous roots, or ginger rhizomes. Formation of these organs is induced during drought and freezing conditions that compromise plant viability, often serving as a mechanism for asexual propagation that provides a survival strategy to the plant. As www.sciencedirect.com

such, these organs remain dormant in soil during the adverse cold and dry periods, to be reactivated in the next favourable season and generate a new plant. Initial growth of the new shoot depends on the metabolic resources accumulated in these organs, mostly in the form of starch or soluble sugars, which makes them an excellent caloric supplementation to the human dietary needs. Iterative breeding selection for larger organs and adaptation to different latitudes gave rise to the modern cultivated genotypes, of high economic relevance and strategic in terms of food security. Sugar beet for instance accounts for 20% of the world’s sugar production, while potato is the third most important food crop, after wheat and rice. Cassava is, in addition, highly drought-tolerant and capable of growing on marginal soils, representing one of the main staple food crops in much of tropical Africa. Thus, understanding the mechanisms used by the plant to signal differentiation of these organs is an important goal to meet the nutritional demands of the rising world population, besides being a fundamental question in developmental biology. This developmental switch has been most studied in potato, where the availability of a reference genome sequence [1], easy generation of transgenic plants and availability of significant germplasm resources, largely facilitated these studies. The finding that members of the FLOWERING LOCUS T (FT) gene family, which in Arabidopsis encode the mobile flowering signal produced in the leaves, are responsible for triggering tuber formation in the underground stolon provided an important breakthrough in our understanding of how differentiation of these organs is regulated [2]. More recent studies in onion showed that different FT genes also regulate flowering and bulb formation [3], highlighting the evolutionary functional conservation of FT proteins as main triggers of the storage switch. Moreover, the discovery that expression of the LONELY GUY (LOG1) gene, encoding a cytokinin (CK)-activating enzyme, confers axillary tomato meristems the ability of de novo formation of tuber-like organs [4], suggest that CKs may function as universal regulators of storage-organ fate in plants. This also points to secondary meristems at the axillary buds and vascular cambium as the initials for this developmental transition.

FT-like genes as major inducers of storage organ formation Potato tubers develop from specialized underground stems or stolons that, on induction, cease longitudinal Current Opinion in Plant Biology 2015, 23:45–53

46 Growth and development

growth and initiate radial expansion in the subapical region. These morphological changes are associated with a switch from apoplastic to symplastic phloem unloading, expression of a specific set of genes, and the accumulation of large amounts of starch [5]. Formation of these organs is favoured by long nights, cool temperatures and low rates of nitrogen fertilization, although this response varies with the geographic origin of the germplasm. Andigena genotypes originating from the highlands of South America, for example, are strictly dependent on short days (SDs) for tuberization, and this tight control entails an excellent system for the study of the signalling mechanisms involved in differentiation of these organs — reviewed in [6–8]. Grafting studies showed that day length is perceived in the leaves and that, in inductive SDs, a mobile signal or ‘tuberigen’ is synthesized in these organs and transported to the underground stems to induce tuber formation. Flowering tobacco scions promote tuber formation when grafted onto non-induced potato stocks, suggesting that the mobile florigen and tuberigen signals are related in nature [9]. In Arabidopsis, the small FT protein, which shares similarity to RAF-kinase inhibitors, is a major component of the florigen signal [10–12] and a member of the FT gene family, the StSP6A gene, was indeed found to act as a main inducer of tuberization in potato [2]. In the Solanaceae, this gene family appears to have undergone preferential expansion, with 13 FT/TFL-like members identified in potato, as compared to the six genes reported in Arabidopsis. The StSP3D gene, which corresponds to the ortholog of tomato SINGLE FLOWER TRUSS (SFT), regulates day-neutral flowering [2,13,14], while StSP6A is expressed in the leaves only under inductive SDs, and promotes tuber formation in a graft-transmissible manner. StSP6A expression also responds to an autoregulatory loop that drives amplification of this signal in the stolons [2], a mechanism that has not been described in Arabidopsis. An additional member of this gene family, StSP5G, is highly expressed in long days (LDs) and has been proposed to act as a repressor of tuberization by preventing StSP6A expression under non-inductive conditions [2,15]. Antagonistic function of these proteins is similar to that observed for the sugar beet FT homologues, BvFT1 and BvFT2 [16]. Sugar beet is a biennial root crop that grows vegetatively in the first year and flowers after exposure to cold temperatures over winter; therefore, avoidance of flowering is critical for high yields and good taproot quality. The BvFT1 floral repressor is highly expressed before vernalization and acts in the leaves to suppress expression of BvFT2, a second FT family member with a role in floral induction. Notably, BvFT1 differs from BvFT2 in several residues at the external Bloop region involved in protein partner interaction [16]. These amino acid substitutions are shared by StSP5G, thus supporting a related repressive role of this member of the potato FT clade. Members of the FT gene family were also recently reported to control onion bulb formation [3]. Like sugar Current Opinion in Plant Biology 2015, 23:45–53

beet, onion is a biennial crop that is planted in the early spring and forms a bulb during longer days of late spring– summer. The bulb overwinters and after vernalization, flowers and sets seed. Different FT-like genes were shown to control flowering (AcFT2) and bulb formation (AcFT1 and AcFT4) in this monocot species, as seen in potato. LD photoperiods downregulate AcFT4, which acts as an inhibitor of bulb formation by preventing expression of AcFT1, which encodes a mobile protein promoting bulbing. Upon vernalization, floral induction correlates with the upregulation of AcFT2 in the central bud tissue of the bulb that will give rise to the floral inflorescence, hence implicating this gene as a key flowering regulator [3]. However, AcFT2 complements the late flowering of the Arabidopsis ft-1 mutant when expressed under control of the constitutive 35S promoter but not the SUC2 promoter, which is indicative of a limited mobility of this protein. Actually, a similar direct activation of the FT homologue, NtFT, at the apical meristem and leaf primordia inside the bulb was also reported for Narcissus [17], suggesting that floral initiation control in bulbs does not require a mobile signal. Although genes involved in taproot formation in sugar beet have not been identified, it is tempting to speculate that members of the FT gene family will also play a role in triggering formation of this organ, as observed in onion and potato. Modern potato cultivars were generated by intercrossing of Andigena and Chilotanum genotypes, derived from lowland south-central Chile and more adapted to LD conditions. Recurrent selection against photoperiodic control led to the Neo-tuberosum genotypes, able to tuberize in LDs. Recent transcriptomic analyses of this germplasm identified a second StSP6A-a2 allele that differs from StSP6A in intron size and a number of nucleotide polymorphisms, and is expressed in LDs [18]. Remarkably, this allele is absent in Andigena genotypes, suggesting that it plays a pivotal role in tuber formation under non-permissive day length conditions, although additional studies are needed to confirm this function.

Control of FT expression: CO, photoperiod and circadian clock components In Arabidopsis, the B-box zinc finger CCT-domain transcription factor CONSTANS (CO) activates FT expression in the phloem companion cells, in inductive LDs. Circadian clock control of CO transcription and regulation of protein stability by light ensures correct timing of flowering — reviewed in [10–12]. Likewise, the CO-homologue rice Hd1 protein induces SD flowering by upregulating expression of the Hd3a FT-homologue, providing evidence that the day length pathway is conserved between taxa [11,12]. However, function of Hd1 differs from that of CO in Arabidopsis, as Hd1 activates Hd3a in SDs, while it www.sciencedirect.com

FT genes as signals for storage organ formation Navarro, Cruz-Oro´ and Prat 47

represses expression of this gene in LDs. Notably, Hd1 and CO show a similar oscillation pattern so that, in noninductive LDs, Hd1 transcription coincides with light. In contrast, in SDs, when Hd1 is presumed to activate Hd3a, expression is low during daytime. The Hd1 switch from activator to repressor is mediated by the red light photoreceptor PHYB, via a mechanism that is not yet well understood — reviewed in [19]. The recent identification of PHYTOCHROME-DEPENDENT LATE-FLOWERING (PHL), shown in Arabidopsis to bridge PHYB and CO in a red light-dependent manner, may shed some light on how this regulation is achieved [20]. A CO homologue (BvCOL1) was also identified in sugar beet through sequence similarity, but so far there is no functional information concerning a possible role of this gene in flowering [21]. Instead, cloning of the dominant early bolting B locus identified BOLTING TIME CONTROL 1 (BTC1) encoding a homologue of the PRR7 Arabidopsis clock and barley PPD-H1 gene, a pseudoresponse regulator with a pseudo-receiver and CCT domain, shown in this temperate grass species to play a major role in LD flowering via induction of HvFT [22]. BTC1 promotes bolting and flowering through repression of BvFT1 and activation of the floral integrator BvFT2, whereas in biennials carrying the btc1 recessive allele, BvFT1 is not repressed requiring vernalization for bolting. Interestingly, cloning of the flowering B2 locus identified the BvBBX19 gene, which includes two Bbox zinc finger conserved domains [23]. BvBBX19 is diurnally regulated and acts together with BTC1 to control BvFT1 and BvFT2 expression and bolting. It has been proposed that association of BTC1 and BvBBX19 would link the B-box and CCT1 domains, allowing these proteins to acquire a CO function [23]. CO is involved in day length control of tuberization in potato, where it represses tuber formation under noninductive LDs, by inhibiting production of the mobile tuberizing signal in the leaves [2,15,24,25]. Three CO genes organized in tandem were identified in this species, although transcripts for only two of these genes (StCO1 and StCO2) have been detected, suggesting that the third gene copy may be inactive. Functional studies have been performed with the StCO2 gene, which is expressed at higher levels [2,25]. StCO2-RNAi plants were shown to tuberize in LDs, providing evidence of a role of this COhomologue in repressing tuberization. Consistent with this function, StSP6A expression is induced in these plants, while StSP5G is strongly suppressed [2], indicating that StCO2 may directly regulate transcription of the StSP5G tuberization repressor. Interestingly, StCO2 does not show the same diurnal oscillation as CO or Hd1, but peaks at dawn [2,25]. In LDs, this peak of expression coincides with the light period, while in SDs it is shifted towards the night, which stimulates speculation that light is required to stabilize the StCO2 protein. Consistent www.sciencedirect.com

with this hypothesis, PHYB-silenced lines show a similar tuberization phenotype to StCO2-RNAi plants [26]. Therefore, assessing StCO2 protein levels in these lines will be essential to provide experimental evidence of this regulatory mechanism. A further remarkable discovery has been the finding that the potato earliness locus, a major quantitative trait locus for timing of tuber initiation and maturation, encodes a member of the CYCLING DOF FACTOR (CDF) gene family (StCDF1), shown in Arabidopsis to bind the CO promoter and suppress expression of this gene [15,27]. StCDF1 forms a complex with the circadian clock components, GIGANTEA and FKF1, responsible for targeting this DOF factor for proteasomal degradation and reverse inhibition of StCO1/StCO2 expression. Notably, StCDF1 effects on StCO1 are stronger than on StCO2, suggesting that this gene plays also an important role in day length tuberization control. Early tuberizing genotypes carry allelic StCDF1 variants that encode truncated forms of the protein, lacking the StFKF1 interacting domain at the C-terminal region [15]. In these cultivars, StCDF1 is stabilized and StCO1/2 expression is repressed in LD, such that peaks of these genes no longer coincide with the light. Therefore, StSP5G is not induced, allowing StSP6A activation and tuber induction (Figure 1). Consistent with this model, Neo-tuberosum genotypes tuberizing in LDs, contain alleles for both, the full-length and the C-terminal modified protein that evades StFKF1 regulation, while in SD-obligate Andigena genotypes, these truncated alleles are absent [18].

Hormonal control of tuber formation Several plant hormones play an important role in driving the stolon-to-tuber transition — reviewed in [6,28]. It has been found that gibberellins (GAs) have an inhibitory effect on tuberization [29], and that a localized decrease in the levels of active GAs in the stolon is required for tuberization onset [30]. Additional studies support a role of auxins as promoters of tuberization, given that several auxin-related StPIN and StARF family genes are transcriptionally regulated during tuberization [31,32] and auxin levels strongly increase in the stolon upon tuber initiation, remaining relatively high during subsequent tuber growth [33]. These hormones together with strigolactones (SLs) regulate stolon architecture, by repressing axillary bud outgrowth, thus exerting a similar control as for shoot branching [33,34]. Silencing of the SL biosynthetic StCCD8 gene in potato results in enhanced shoot branching, fewer stolons that lack diageotropic growth, the formation of aerial tubers and increased secondary growth of the new developing tubers, indicating that SL have a dramatic effect not only in inhibiting shoot branching but also in maintaining tuber bud dormancy [34]. It has long been postulated that CKs may play a role in tuberization by promoting cell division during tuberization Current Opinion in Plant Biology 2015, 23:45–53

48 Growth and development

Figure 1

LDs SDs

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tuber induction tuber induction Current Opinion in Plant Biology

Regulation of tuber initiation in potato genotypes with strict or permissive photoperiodic requirements. The ssp. andigena is strictly dependent on short days to form tubers. In long days, StGI1 and StFKF1 interact with StCDF1, a negative regulator of StCO1/2, and target this DOF protein for degradation. StCO1/2 would be stabilized by PHYB and repress the FT-like gene StSP6A, likely through activation of StSP5G. In short days, the StGI1/StFKF1/StCDF1 complex would not be formed, StCO1/2 expression is repressed in the morning and the StCO1/2 protein is not stabilized by PHYB. Therefore StSP6A is activated and can be transported to the stolon, where it interacts with an unknown partner (X) to trigger tuber formation. An additional regulator (Y) is likely to activate StSP6A expression in short days. Neo-tuberosum genotypes, adapted to tuberize in long days, have truncated StCDF1 alleles that do not interact with StFKF1 allowing expression of StSP6A in long days. An additional allele of this gene (StSP6Aa2) is also present in these genotypes, although its role in tuberization has not yet been established. Arrows and blunted lines indicate activation and repression, respectively.

onset and creating a local sink [35]. Over-expression of the Arabidopsis CK catabolic enzyme, CK oxidase (CKX1), reduces tuber yield [35]. Recently, in a very elegant study it was proven that ectopic expression of the tomato LONELY GUY 1 gene (TLOG1), encoding a CK-activating enzyme, confers tomato basal axillary Current Opinion in Plant Biology 2015, 23:45–53

meristems the ability to generate aerial minitubers similar to potato tubers [4,36]. These findings suggest that CKs may act as universal regulators of storage-organ formation in plants and provide a framework for understanding the regulatory basis of this developmental process (Figure 2). www.sciencedirect.com

FT genes as signals for storage organ formation Navarro, Cruz-Oro´ and Prat 49

Figure 2

(a) auxins CKs

GAs

SLs sucrose StSUT4

stolon (b)

underground tuber

miR156 StLOG1 CKs

SLs in planta

axillary bud

aerial tuber

(c) sucrose CKs

GAs

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in vitro

aerial tuber Current Opinion in Plant Biology

Hormonal regulation of tuber formation. Tubers develop from underground stems or stolons and, under certain conditions, from axillary buds. Inductive (arrows) and repressive (blunted lines) effects of different plant regulators on tuberization (a) in stolons and (b and c) in axillary buds (green arrows) of plants (in planta) and stem node cuttings (in vitro). SLs and GAs have a repressive effect, while CKs and sucrose promote tuberization, reflecting a similar hormonal balance between tuber induction and axillary branching.

Other mobile signals controlling potato tuberization Plants do not respond to photoperiodic inductive signals until they reach a certain age and become competent to flower or tuberize. The switch from the juvenile to adult vegetative phase is controlled by an age-dependent pathway that implicates sequential function of microRNAs miR156 and miR172 as main players — reviewed in [37– 39]. In Arabidopsis, miR156 is abundant in the juvenile phase and directs cleavage of transcripts of the SPL family of transcription factors, which facilitate floral transition by activating expression of the LFY, FUL, SOC1, AP1 and AGL24 genes in the shoot apex. In the leaves, these factors also activate expression of miR172 that shows a complementary pattern of expression to miR156, and accumulates during the adult phase. In Arabidopsis, miR172 was shown to promote early flowering via translational repression of members of the AP2-like family of transcription factors, which act as repressors of FT transcription. Hence, interplay between miR156/ miR172 and the SPL factors plays an important role in floral transition, by modulating expression of floral integrators and floral identity genes.miR156 and miR172 were www.sciencedirect.com

also implicated in tuberization control, with these miRNAs shown to move through the phloem and modulate tuber formation in a graft-transmissible manner [4,40,41]. In potato, expression of these miRNAs is controlled by photoperiodic conditions, with miR156 being high in leaves and stems in LDs, and found to accumulate in the stolons in SDs, while miR172 levels are higher in SDs, and upregulated in the stolon at the onset of tuberization (Figure 3). Thus, high levels of both microRNAs in the stolons differ from the complementary pattern observed in the leaves or in Arabidopsis, reflecting a specific mechanism of action of miR156 in this organ or a spatial exclusion of these two miRNAs [41]. miR156 over-expression leads to aerial tuber formation [4], although in Andigena plants this phenotype is only observed in SDs, suggesting a role of this miRNA as a tuberization facilitator rather than a tuberization inductive signal [41]. These plants exhibit altered plant architecture and reduced miR172 and SPL9 transcript levels, along with increased CK and reduced SL levels, and upregulated levels of expression of the StLOG1 transcript [41]. Andigena lines over-expressing miR172, by contrast, tuberize in LDs and promote tuber formation when grafted into wild-type potato stocks, with transcripts for the AP2related RAP1 gene found to be downregulated in these plants, suggesting a role of this miRNA in the regulation of the inducing tuberization signal [40]. Movement of transcripts such as StBEL5 [42,43] and POTATO HOMEOBOX1 (POTH1) [44] has also been demonstrated, with potato lines over-expressing these factors displaying enhanced tuberization and higher tuber yields [42]. These proteins were indeed shown to interact each other and bind the GA2oxidase1, YUCCA and IPT promoters to activate expression of these genes, hence it was proposed that they induce tuberization by regulating hormonal levels in the stolons [42,43]. However, direct evidence showing that these mobile RNAs are required for tuberization could not be obtained due to redundant function of members of these gene families [45,46]. Other metabolites, like sugars, are also recognized to have a promoting effect on flowering in the shoot apical meristem — reviewed in [47]. High sucrose likewise promotes tuberization of stem node cuttings, with the enhanced sucrose transport from the leaves caused by downregulation of the phloem StSUT4 transporter, leading to early flowering and tuberization under non-inductive LDs in Andigena potato genotypes. Tuberization effects were more pronounced in GA-treated plants, suggesting a reciprocal regulation of StSUT4 and GAs. Moreover, StCO expression is downregulated, while the StSP6A and StSOC1 transcripts are elevated in these plants, providing evidence of a link between enhanced sucrose transport and the day length pathway [48,49]. In this regard, sucrose was recently reported in Arabidopsis to modulate flowering via the signal metabolite trehalose 6-phosphate (T6P), that acts as a positive regulator of the Current Opinion in Plant Biology 2015, 23:45–53

50 Growth and development

Figure 3

miR172

LDs

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LDs

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expression

(a)

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StBEL5 POTH1 Current Opinion in Plant Biology

Role of miR156 and miR172 in tuber initiation. (a) Relative levels of miR156 and miR172 in the different plant organs in response to photoperiod. High levels of miR156 in induced stolons point to a positive role of this miRNA in tuber development. (b) Model for the regulation of tuber and flowering induction by these two complementary expressed miRNAs. StSPL9 is targeted by miR156 and activates miR172 that promotes flowering and tuberization likely through inhibition of the RAP1 repressor. BEL5 is induced by miR172 and thought to promote tuber formation through changes in hormonal levels via interaction with POTH1. miR156 has an additional role modulating the competence to form tubers in axillary buds. Black arrows indicate activation and red blunted lines indicate repression. Red arrow under PHYB indicates that PHYB induces miR172 transcription in leaves, but appears to inhibit its transport.

day length pathway in the leaves, while it promotes flowering at the shoot apex via the age pathway [50]. High sucrose and glucose levels were actually shown to inhibit miR156 expression at the transcriptional and posttranscriptional levels [51,52], and thereby it will be important to test if a related mechanism mediates also storage organ formation in response to high sucrose.

Conclusions and perspectives In the past years, we have witnessed a considerable advancement in our understanding of the mechanisms controlling induction of storage organ formation in plants. Multiple genes were identified in potato, which, upon alteration of their expression levels, result in promotion or a delay of tuberization (see Table 1). Crucial discoveries have been the finding that clock components and a COFT module related to that reported in Arabidopsis, are implicated in day length control of storage organ formation, while high CKs de novo induce formation of these organs, in species in which this developmental process has been evolutionarily suppressed. Potato tubers can be induced in axillary buds of stem node cuttings and it is becoming increasingly clear that hormonal regulation plays an important role in axillary meristem activation Current Opinion in Plant Biology 2015, 23:45–53

and competence/commitment for tuber development. A still remaining question is what genes act at integration of the FT mobile signals to initiate the storage switch. In this regard, the recent finding that the florigen FT and TWIN SISTER OF FT (TSF) proteins modulate axillary shoot branching through direct interaction with the BRANCHED1 TCP factor [53,54] is very exciting, and it will be crucial to assess if additional TCP family members are likewise implicated in the storage-fate switch. It will be also of interest to investigate if tuber induction by cool temperatures shares common regulatory elements with the photoperiodic pathway, as this should impact in the design of novel strategies to improve tuber production in geographic areas in which warm temperatures compromise cultivation of this crop. The use of high throughput technologies will help in a better understanding of this process in potato and other tuber-bearing species, like cassava, a primary staple food crop in the tropics, with increasing industrial interest. International research consortia have boosted studies in this species in recent past years, partly thanks to the availability of most of its genome sequence [55] and the possibility of generating www.sciencedirect.com

FT genes as signals for storage organ formation Navarro, Cruz-Oro´ and Prat 51

Table 1 Genes affecting potato tuberization. Summary of genes reported to be involved in tuber development through different signalling pathways. Their positive (induction) or negative effect (repression) on tuberization is indicated. (*) Denotes genes whose function has been suggested but not fully tested. GAs, gibberellins; CKs, cytokinins; JA, jasmonic acid; SLs, strigolactones Gene

Effect on tuberization

Pathway

StSP6A StSP6Aa2 StSP5G StCO1 StCO2 StCDF1 StGI1 StFKF1 StPHYB StPHYA StTFL1 StGA2ox1 StGA20ox1 StPHOR1 StPOTLX-1 StPOTM1 TLOG1 StCCD8 StSUT4

Induction Induction* Repression* Repression* Repression Induction Repression* Repression* Repression Repression Induction Induction Repression Repression Induction Induction Induction Repression Repression

StmiR156

Repression/ Induction Induction Repression* Induction Induction

Photoperiod Photoperiod Photoperiod Photoperiod Photoperiod Photoperiod Photoperiod Photoperiod Photoperiod Photoperiod n.d. GAs GAs GAs JA CKs CKs SLs Photoperiod/ GAs/Sucrose Photoperiod/ Age/CKs/SLs Photoperiod/Age Photoperiod/Age Photoperiod/GAs/CKs Photoperiod/GAs/CKs

StmiR172 StRAP1 StBEL5 StPOTH1

Reference [2] [18] [2,15] [15] [2,25] [15] [15] [15] [26] [58] [59] [30] [60] [61] [62] [63] [4] [34] [48,49] [4,41] [40] [40] [42,43] [64,44]

transgenic plants, and are foreseen to lead to great progress in the near future [56,57].

Acknowledgements We apologize to all colleagues whose work could not be cited due to space restrictions. Research by the group is currently funded by the ERA-NET New-Indigo PIM2010ENI-00699 grant from the Spanish MINECO and financial support by KWS, MEIJER, HZPC and SOLANA Research in the frame of the FP7 ERA-CAPS 291864 proposal.

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2.

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3. 

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5.

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