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ScienceDirect Flowering time regulation in crops — what did we learn from Arabidopsis? M Blu¨mel1, N Dally1 and C Jung1 The change from vegetative to reproductive growth is a key developmental switch in flowering plants. In agriculture, flowering is a prerequisite for crop production whenever seeds or fruits are harvested. An intricate network with various (epi-) genetic regulators responding to environmental and endogenous triggers controls the timely onset of flowering. Changes in the expression of a single flowering time (FTi) regulator can suffice to drastically alter FTi. FTi regulation is of utmost importance for genetic improvement of crops. We summarize recent discoveries on FTi regulators in crop species emphasizing crop-specific genes lacking homologs in Arabidopsis thaliana. We highlight pleiotropic effects on agronomically important characters, impact on adaptation to new geographical/climate conditions and future perspectives for crop improvement. Addresses Plant Breeding Institute, Christian-Albrechts-University of Kiel, Olshausenstr. 40, D-24118 Kiel, Germany Corresponding author: Jung, C ([email protected]) These authors contributed equally to this work.

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Current Opinion in Biotechnology 2015, 32:121–129 This review comes from a themed issue on Plant biotechnology Edited by Inge Broer and George N Skaracis

http://dx.doi.org/10.1016/j.copbio.2014.11.023 0958-1669/# 2014 Elsevier Ltd. All rights reserved.

Introduction The reproductive success of flowering plants depends on a complex network of (epi-) genetic factors and their interaction with external stimuli. During domestication and breeding, crop plants underwent a plethora of modifications such as the adaptation to long days (LDs), requirement for vernalization and the shift from annual to biennial life cycle. Since the pioneering work of Koornneef et al. [1] who characterized numerous flowering time (FTi) mutants in the model species Arabidopsis (Arabidopsis thaliana), remarkable progress has been made in identifying new FTi regulators. New-omics techniques further led to the discovery of numerous regulatory factors in Arabidopsis. Today they also serve as a basis for www.sciencedirect.com

functional analysis of Arabidopsis FTi orthologs and crop-specific regulators in cultivated species. Here, we review recently published FTi regulators with conserved or diverged function in crops as elucidated by mutant/linkage analysis or genetic engineering. We will further focus on FTi regulators and pathways unique to crop species (Tables 1 and 2). We aim to enlighten the relevance of selected genes for domestication, local adaptation and breeding and will indicate possible prospects for detecting yet unknown FTi regulators in crops, and for modifying life time regimes in crops.

Flowering time regulation in A. thaliana The genetic, epigenetic and environmental factors triggering the transition from the vegetative to the generative phase are best understood in the annual long-day (LD) plant A. thaliana, due to its generally acknowledged status as a model plant. Signaling pathways reacting to differential endogenous (autonomous, gibberellin, circadian clock, age, sugar budget) and environmental cues (vernalization, ambient temperature, and photoperiod) [2–4] converge towards a few floral integrator genes (SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1), FLOWERING LOCUS T (FT), and AGAMOUSLIKE24 (AGL24), Figure 1). They activate the meristem identity genes LEAFY (LFY), APETALA1 (AP1), SEPALLATA3 (SEP3) and FRUITFULL (FUL), which irreversibly confer the transition from a vegetative to a floral meristem. FT has a specific role in the floral transition process, since it constitutes, first, the floral integrator of several pathways and second, the mobile signal moving from the leaves through the phloem and binds to FD in the meristem to promote flowering [5]. Since various comprehensive recent reviews [3,6,7] have summarized our understanding of Arabidopsis FTi regulation, it is beyond the scope of this work to extensively discuss all genetic and epigenetic FTi controlling factors. However, Arabidopsis FTi research has by no means come to an end as illustrated by latest discoveries, for example, by Wang et al. [8]. These authors demonstrated that the B-BOX (BBX) 19 protein represses FT expression by interaction with CO to precisely define the timing of flowering. Another landmark study [9] identified TREHALOSE6-PHOSPHATE SYNTHASE 1 (TPS1) as a regulatory factor of the new T6P pathway, linking FTi control to the sugar budget of a plant [3]. Richter et al. [10,11] elucidated the function of two GATA transcription factors as critical repressors of plant growth in the gibberellin Current Opinion in Biotechnology 2015, 32:121–129

122 Plant biotechnology

Table 1 Functional orthologs of Arabidopsis thaliana FTi genes in crops with conserved function. Functional characterization was demonstrated by mutant analysis, sequencing and complementation analysis or heterologous expression, RNA interference, or clear linkage with a major QTL. CI, central integrator; PH, photoperiod; CC, circadian clock; VE, vernalization; AT, autonomous pathway. Arabidopsis gene name abbreviations are explained in Supplementary Table 1, cited references are given in the Supplementary Information Crop species Antirrhinum sp. Apple (Malus  domestica) Arabis alpina Banana (Musa sp.) Barley (Hordeum vulgare)

Brassica rapa

Common bean (Phaseolus vulgaris) Grapevine (Vitis vinifera) Jatropha curcas Maize (Zea mays) Lemon (Citrus sp.) Medicago truncatula Mustard (Sinapis alba) Oilseed rape (Brassica napus) Onion (Allium cepa) Pea (Pisum sativum)

Perennial ryegrass (Lolium perenne) Pepper (Piper nigrum) Poplar (Populus sp.)

Potato (Solanum tuberosum)

Rice (Oryza sativa)

Rose (Rosa sp.) Soybean (Glycine max)

Spring orchid (Cymbidium goeringii) Sugar beet (Beta vulgaris ssp. vulgaris) Tobacco (Nicotiana tabaccum) Tomato (Solanum lycopersicum)

Wheat (Triticum aestivum)

Woodland strawberry (Fragaria vesca)

Gene name CEN MdFT1, MdFT2 MdTFL1 PEP1 MaCOL1 HvFT1/Vrn3 HvCO1 EAM8 HvELF3/Mat-a BrFLC1 BrFLC2 BrFLC3 PvTFL1y VvFT JcFT ZCN8 ZCN6 CiFT CsTFL MtFTa1 SaFLC BnFLC.A3-b BnA.FRI.a AcFT2 LATE BLOOMER 1 HR DIE NEUTRALIS STERILE NODES LpCO FASCICULATE LAP1 PFT1 PnFTL1, PnFTL3 PtCO2 StSP3D StCO StCDF1 Hd3a RCN1, RCN2 RFL OsGI Hd1 OsELF3-1 OsMADS50 RoKSN GmFT2a, GmFT5a GmTFL1 GmGIa GmFLD CgFT BvFT2 BvFLK NtFT4 SP3D/SFT FALSIFLORA SP TaFT1/Vrn3 TaHd1-1 TaGI1 FvKSN

Current Opinion in Biotechnology 2015, 32:121–129

Ortholog in A. thaliana

Pathway/function

Reference

TFL1 FT TFL1 FLC CO FT CO ELF3 ELF3 FLC FLC FLC TFL1 FT FT FT TFL1 FT TFL1 FT FLC FLC FRI FT GI ELF3 ELF4 LUX CO TFL1 AP1 FT TFL1 CO FT CO CDF1 FT TFL1 LFY GI CO ELF3 SOC1 TFL1 FT TFL1 GI FLD FT FT FLK FT FT LFY TFL1 FT CO GI TFL1

CI CI CI VE PH CI PH CC CC CI CI CI CI CI CI CI CI CI CI CI VE VE VE CI PH CC CC CC PH CI

[72] [73] [74] [75] [76] [77,78] [79] [52,80] [52] [81] [81] [81] [57] [82] [83] [84,85] [86] [87] [88] [89] [90] [91] [92] [93] [94] [53] [95] [96] [97] [98] [99] [100,101] [102] [100] [37] [103] [60] [104] [105] [106] [107] [108] [109] [110] [67] [111] [56,112] [55] [113] [114] [115] [116] [117] [118] [119] [120] [78] [121] [122] [67]

CI CI PH CI PH PH CI CI CI PH PH CC CI CI CI CI PH AT CI CI AT CI CI CI CI CI PH PH CI

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Crop flowering time regulation compared to Arabidopsis Blu¨mel, Dally and Jung 123

Table 2 Homologs of Arabidopsis thaliana FTi genes in crops with pleiotropic or diverged function. Arabidopsis gene name abbreviations are explained in Supplementary Table 1, cited references are given in the Supplementary Information Crop species Barley (Hordeum vulgare)

Brassica rapa Onion (Allium cepa) Poplar (Populus sp.) Potato (Solanum tuberosum) Rice (Oryza sativa)

Root chicory (Cichorium intybus) Soybean (Glycine max) Sugar beet (Beta vulgaris ssp. vulgaris)

Tobacco (Nicotiana tabaccum) Tomato (Solanum lycopersicum) Wheat (Triticum aestivum)

Gene name

Homolog in A. thaliana

Ppd-H1

PRR7

Ppd-H2

FT

Vrn1

AP1/CAL/FUL

Vrn2 HvCEN (Eps2 locus) BrFLC2

COL gene TFL1

AcFT1 AcFT4 PFT2 StSP6A Hd1

FT

CiFL1 GmFT4 BvFT1

FLC

FT FT CO

Determinant of photoperiodic sensitivity/flowering time Floral promoter under non-inductive conditions, affects grain yield Floral promoter in response to vernalization, affects growth rate, spike length, yield Floral repressor, affects growth rate, spike length, yield Flowering time variation, affects yield and thousand kernel weight Differentiation between oil-type and vegetable-type B. rapa Bulb formation

Reference [123] [35,124] [42,125] [42] [32] [59] [93] [126] [37] [34,108]

FLC FT FT

Growth cessation, bud set Tuber formation Floral repressor in LD, floral promoter in SD, affects plant height, number of spikelets/panicle, number of grains/panicle, grain yield/plant No stable down-regulation after vernalization Floral repressor Floral repressor

BTC1 BvBBX19 BvFL1 NtFT1, NtFT2, NtFT3 SFT Ppd1

PRR7 BBX19 FLC FT

Regulator of bolting Floral promoter No stable down-regulation after vernalization Floral repressors

[36,66] [127] [20] [117]

FT PRR7

[38,118] [128]

Vrn1 Vrn2

AP1/CAL/FUL COL gene

Inflorescence architecture, yield heterosis Determinant of photoperiodic sensitivity and flowering time Floral promoter in response to vernalization Floral repressor

pathway and further described their interaction with the floral integrator SOC1.

Conservation and functional diversification of floral transition pathways between Arabidopsis and crop species The presence of orthologous genes in non-related species (Table 1) suggests a certain degree of evolutionary conservation of FTi genes. However, research within the past revealed also clear differences between the molecular mechanisms underlying floral transition (Table 2). Dally et al. [12] identified BvBBX19 in sugar beet (Beta vulgaris L.) as a floral promoter involved in bolting regulation by fine-tuning the two beet FT paralogs. Soon afterwards, BBX19 was functionally characterized in Arabidopsis and described as a direct interaction partner of CO and a repressor of FT [13]. Since no true CO ortholog has been identified in beet so far [12,13], a divergent, CO-independent pathway may be active in which BvBBX19 interacts with the bolting promoting gene BOLTING TIME CONTROL 1 (BTC1) to regulate the beet FT paralogs [12]. www.sciencedirect.com

Function/observation

[18] [28] [115]

[129] [130]

Due to their suggested tropical origin, today’s winter annual cereals may have acquired their vernalization requirement as a result of convergent evolution or domestication [14]. Interestingly, FLC-like genes were recently identified in monocots based on genome synteny studies [15], but no functional FLC orthologs have been identified in cereals so far [16]. The vernalization response in wheat (Triticum spp.) and barley (Hordeum vulgare L.) is — in contrast to Arabidopsis — conferred by high expression levels of the zinc finger and CCT domain containing gene VRN2, which represses the FT ortholog VRN3 and thus, flowering before vernalization is prevented [17]. During cold exposure, VRN2 is repressed by the MADS box transcription factor VRN1, which shows homology to AP1/FUL/CAL. VRN2 is activated by epigenetic modification. Differential modes of vernalization response may be common, since almost no FLC orthologs have yet been characterized in non-Brassica species with the only two exceptions CiFL1 from root chicory [18] and BvFL1 from sugar beet, the latter being subject of a current scientific debate as regulator of vernalization response [19,20]. Current Opinion in Biotechnology 2015, 32:121–129

124 Plant biotechnology

Figure 1

vernalization

circadian clock DET1

PAF1-like complex CDC73/PHP

SWR1/SRCAP-like complex

VIP2/ELF7 VIP4,5 VIP6/ELF8

PIE1 ARP6/SUF3 SEF

PRR3

VRN2 complexVIN3

ATX1,2,7 EFS EMF2 ELF5

RNA binding

autonomous RNA processing

FCA FPA FLK

PRR9 PRR7 PRR5

VRN2 FIE CLF/SWN MSI1

GRP7

EBI LHP1/ ZTL TFL2 HDA9

PEP BBX24

REF6

-responsive miRNAs 163 169 398 399

AGL19

VOZ1,2

TEM1,2 miR824

BBX19

SVP

CBF/NF-Y HAP2,3,5

CO

AS1

FT

OBF4

ICE1

ambient temperature

FBH1-4 EDL3

DNF

AGL24

GA20ox GA3ox

AGL17

TSF TOE1,2 AP2 SNZ, SMZ

SOC1

SPL9

GID1 RGA GAI RGL1-3

phyD phyE

phyA

PFT1

PHO2

DELLA

phyB HOS1

FD

SLY1

photoperiod

CIB1

CDF1-3,5 PIF4

MAF2-5 FLM SPA1

AGL16

Gibberellin (GA4)

CRY2 FKF1

GI

HUA2

FLC SWP1/LDL1 CZS

COP1 SPAs

LKP2

Histone modification

CUL4

CRY1

FRI

FRL1,2 SUF4 FES

Chromatin modification LD FLD FVE/MSI4

ELF3 ELF4 LUX DDB1

TOC1

LHY/CCA1 CHE

VRN1

FY

RVE8

PIFs

GNC/ GNL

FUL CAL SEPs

LFY

age

miRNA172

TFL1

FPF1

miRNA156

AP1

SPL9,10

SPL3-5 TPS1

Activation and/or stabilization Inhibition and/or degradation

Genetic and/or physical interaction Indirect interaction

Current Opinion in Biotechnology

Flowering time gene network with known genetic and epigenetic regulators in Arabidopsis thaliana. Arrows indicate a promoting, T-ends indicate an inhibiting genetic interaction. Round dots at both ends mark an interaction without a known direction. Dashed lines denote an indirect interaction. Genes attributed as major regulators in the different flowering time pathways are written in bold. Red writing indicates the functional characterization of a gene as a flowering time regulator in cultivated species — although not necessarily with the same function as in Arabidopsis — by mutant analysis, sequencing and complementation analysis or heterologous expression, RNA interference, or clear linkage with a major QTL. Full gene names are provided in Supplementary Table 1.

FTi regulators in crops lacking homologs in A. thaliana

genes but share a certain degree of sequence conservation within functional protein domains.

Apart from genes with conserved and diverged functions, new FTi genes and even new regulatory pathways have been identified in crops lacking any functional equivalents in Arabidopsis. Environmental adaption has led to evolutionary diversification in many crop species and thus, Arabidopsis, despite its model status, may not always represent the most appropriate tool to functionally characterize or identify crop FTi regulators. Crop FTi candidate genes without Arabidopsis homologs have been found within major QTLs and their function has been uncovered by mutant analysis or genetic complementation; the complete genes do not show sequence similarity to Arabidopsis

The floral promoter gene ID1 of maize (Zea mays), encoding a C2H2 zinc finger protein without any known Arabidopsis homolog was cloned by transposon tagging [21]. Later, its functional rice (Oryza sativa) ortholog OsID1 was identified by domain homology search [22]. Rice heading time is conveyed by two independently acting pathways in response to different photoperiods [23]. Inductive SDs activate a conserved pathway between Arabidopsis and rice, in which the CO ortholog Hd1 promotes flowering via activation of the FT homolog Hd3a. For heading initiation under non-inductive LDs, a Hd1-independent pathway

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Crop flowering time regulation compared to Arabidopsis Blu¨mel, Dally and Jung 125

unique to rice has been described. This pathway acts by RFT1 activation via the Ehd3-Ghd7-Ehd1 module. All members of this pathway have no obvious homologs in Arabidopsis. OsID1 also acts in this pathway and promotes flowering through activation of Ehd1 [22], whose expression is also promoted by OsMADS51 [24]. Recently, Hd16, a casein kinase-I protein inhibiting flowering [25], and Ehd4, a CCCH-type zinc finger protein promoting flowering [26] were added to the rice flowering network as regulators of Ghd7 or Ehd1, respectively. In soybean (Glycine max L.), Xia et al. [27] have identified the major maturity gene E1 as a key flowering regulator which lacks any Arabidopsis homolog and regulates the antagonistically acting FT homologs GmFT2a/GmFT5a and GmFT4 [27,28]. In temperate cereals like wheat and barley, FTi loci which do not contain members of the vernalization or photoperiod response pathways are referred to as eps (earliness per se) genes [29,30]. Their function is incompletely understood and homologs from Arabidopsis have not been identified. Recently, an eps FTi QTL has been validated in winter wheat and candidate genes have been proposed [31]. In barley, HvCEN, a homolog of Antirrhinum CEN has been identified at the EPS2 locus. Resequencing HvCEN in a collection of spring and winter accessions revealed two haplotypes differing in a single non-synonymous polymorphism and corresponding to the respective growth type. Moreover, sequence analysis of HvCEN in a collection of flowering mutants confirmed that alterations within HvCEN are responsible for the observed FTi variation [32].

Yield or yield-related traits Evidently, allelic variation at FTi QTL or within major FTi genes is associated with growth vigor and yield characters. Several FTi gene candidates have been colocalized with yield and yield related QTL in crops. Seed yield in rapeseed (Brassica napus) is highly correlated with FTi and some seed yield or heterosis controlling QTL overlapped with FTi QTL, indicating their importance as components of heterosis in rapeseed [33]. Several studies further suggest that genes from photoperiod and cold responsive pathways and FT/TFL1 orthologs can have pleiotropic effects on growth characters. In rice, several FTi genes were shown to have strong pleiotropic effects on yield traits, for example Hd1 on plant height, number of spikelets/panicle, number of grains/panicle, and grain yield per plant under field conditions [34]. In barley, QTL for grain yield coincide with the positions of two major QTL for heading date, one associated with Ppd-H2, a FT homolog (Figure 1), and the other with Eam6 [35]. The mobile FT-like proteins and their antagonistic TFL proteins are involved in numerous signaling pathways and developmental processes which can also impact yield www.sciencedirect.com

components [36]. In potato (Solanum tuberosum L.), tuberization is controlled by the FT ortholog StSP6A [37]. A gene from the locus EPS2 in barley showed stable pleiotropic effect on time to flowering, yield and thousandkernel weight [32]. The tomato (Solanum lycopersicum) SFT, an FT ortholog, accounts for remarkable yield heterosis in tomato F1 hybrids [38] depending on the prevalence of a second mutation in the tomato TFL1 ortholog SP. A recent study in rapeseed using BnTFL mutants as hybrid parents gave first evidence that TFL1-like gene driven heterosis may not be restricted to tomato [39]. However, a mechanistic link between FTi gene mutations and hybrid growth remains to be established. Wheat Vrn genes have various effects on grain yield and grain protein content [40]. Furthermore, QTLs for FTi and yield or yield-related traits were associated with barley photoperiod and vernalization genes [41]. The barley vernalization genes Vrn-H1 and Vrn-H2 determine growth and yield stability under dryland conditions [42]. This study impressively demonstrates that genotypes from different geographical origin can outperform local varieties due to variation in major FTi regulators.

Crop plant adaptation to different environments and growth conditions Adaptation of crop plants to different geographical regions is linked to mutations in major FTi regulators. As a general rule, seed crops when moving north lost their photoperiod sensitivity. Rice cultivars grown in northern latitudes are extremely early heading due to recessive mutations in four major genes, namely Ghd7, Hd2, Hd5 [43], and Hd16 [23]. Moreover, differences in the functional Hd1 alleles of indica and japonica cultivars have played an important role in the local adaptation of rice [44]. Analogously, maize lost its photoperiod sensitivity as a consequence of adaptation to LD growing conditions. Substantial impact is attributed to alterations in the promoter of the ZmCCT gene, that is, the insertion of a CACTA-like transposon, which suppressed its transcriptional activity resulting in photoperiod-insensitive flowering as a major post-domestication event [45,46]. Also ZCN8 plays a major role in maize adaptation to northern climates [47]. Interestingly, FTi alleles from tropical (SD) origin have recently been introduced into European silage maize breeding programs to breed late flowering energy maize with a high biomass potential [48]. Wheat and barley, in addition to day neutral behavior, gained a strong vernalization requirement as a prerequisite for cultivation as a winter crop. Alternatively, breeders selected genotypes completely devoid of vernalization requirement which could be cultivated as Current Opinion in Biotechnology 2015, 32:121–129

126 Plant biotechnology

short-seasoned spring crops. In either case, vernalization (VRN-1) and photoperiod responding genes were of major importance. Sequence variations in VRN1 genes [49] cause early flowering and spring growth habit in wheat and barley as illustrated for North American spring wheat varieties carrying Vrn-A1 mutations [50]. Likewise, VRN-1 in concert with Ppd-D1 genes has an effect on heading time in European bread wheat [51]. Moreover, Zakkhrabekova et al. [52] showed that the circadian clock regulator Mat-a has a strong impact on short-season adaptation in barley. The ELF3 ortholog HR from pea (Pisum sativum L.) is a key factor for the transition from photoperiod-sensitive to temperate legumes [53]. Clotault et al. [54] analyzed cultivated and wild accessions from pearl millet (Pennisetum glaucum L.) and they hypothesize that circadian clock-associated genes such as PgPHYC, PgPRR73, and PgGI were important for adaption to contrasting climates. In soybean, the GI homolog GmGIa was also found to be a major regulator for geographic adaptation [55]. Apart from FTi control, determinate growth is a major adaptive trait distinguishing cultivated from wild (indeterminate) legumes, which is governed by the TFL1 orthologs GmTfl1 and PvTFL1y from soybean [56] and common bean (Phaseolus vulgaris L.) [57], respectively. A strong vernalization requirement was also needed for oilseed rape for cultivation as a winter crop. Unlike cereals, Brassica crops possess a highly conserved FLCFRI module. A miniature inverted-repeat transposable element (MITE) inserted upstream of BnFLC.A10 is deemed to be a major adaptation event because it causes strong vernalization requirement of winter types grown in North-Western Europe [58]. Likewise, an insertion in the FLC ortholog BraA.FLC.b (BrFLC2) distinguishes between generative (oilseed) and vegetative (vegetable) B. rapa types [59]. Tuberization in potato is highly dependent on day length. After potato was introduced to Europe, very early maturing genotypes had been selected. Recently, non-functional alleles of the CDF homolog StCDF1 were reported to be the major factors responsible for potato cultivation in northern latitudes [60].

Perspectives for crop improvement FTi genes are widely used as selectable markers in plant breeding programs. Since non-appropriate heading is a problem after crossing with non-adapted or wild material, for example, rice indica  japonica hybrids, breeding strategies for optimum heading date by pyramiding FTi QTL were proposed [61]. Selection against photoperiod sensitivity after crossing with tropical maize using FTi functional markers was suggested by Coles et al. [62]. Bentley et al. [63] found a new source of FTi variation by selecting for Ppd-A1a alleles in Current Opinion in Biotechnology 2015, 32:121–129

synthetic hexaploid wheat lines, representing an important example for the application of FTi markers in wheat breeding. Avoidance of flowering before winter (biennial life cycle) is a key trait for cultivating vegetative crops which were often derived from wild annual ancestors. This major domestication step is due to mutations in FTi genes such as FLC homologs in Brassica species [64]. The tendency of vegetative crops, for example, carrots, onion, cabbage, for early bolting upon exposure to low temperatures in early spring, thereby drastically reducing yield and quality have made bolting resistance an important breeding aim. FTi markers are employed for selecting bulb onion (Allium cepa L.) genotypes with adapted FTi after crossing with exotic material [65]. The key domestication step in sugar beet was the shift from an annual to a biennial life cycle (flowering after winter) which was conveyed by a mutation within the BTC1 gene [66]. Now, we are looking for mutations within BTC1 and its co-regulator BvBBX19 to turn the biennial into a winter beet which can be sown before winter but does not flower in the next year. Early or continuous flowering is desirable for some perennial crop species. In modern roses and woodland strawberries (Fragaria vesca L.) this trait is controlled by recessive TFL1 orthologs [67]. Long juvenile phases of fruit and forest tree species (up to 12 years in apple (Malus  domestica)), severely hamper the introgression of new alleles conferring, for example, disease resistance into existing varieties. Therefore, new breeding methods based on stable transformation or virus induced FTi gene silencing have been proposed. Coordinated transcriptional activation of Arabidopsis FT and silencing of MdTFL1-1 drastically reduced the juvenile phase in apple [68]. Since the offspring is non-transgenic, this method could be an interesting alternative for tree breeding.

Outlook Many FTi regulators that have been ignored so far may be identified by their sequence homology to Arabidopsis orthologs, such as members of hormone regulatory pathways, miRNAs, cryptochromes, age and ambient temperature dependent genes (Figure 1). Moreover, perception of environmental signals seems to be much more complicated in crops as indicated by a large phenotypic plasticity for FTi. Sequence based selection and targeted manipulation of FTi regulators offer new perspectives to further increase genetic variation. We can expect that gene-based modeling of phenological development will become reality, as recently proposed for wheat, sorghum and maize [69,70,71].

Acknowledgements We thank Siegbert Melzer for careful revision. We acknowledge funding by the German Research Foundation (DFG) via the priority program 1530: Flowering time control — from natural variation to crop improvement via the Grant JU205/18-1. www.sciencedirect.com

Crop flowering time regulation compared to Arabidopsis Blu¨mel, Dally and Jung 127

Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at http://dx.doi.org/10. 1016/j.copbio.2014.11.023.

References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as:  of special interest  of outstanding interest 1.

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Wang C-Q, Guthrie C, Sarmast MK, Dehesh K: BBX19 interacts with CONSTANS to repress FLOWERING LOCUS T transcription, defining a flowering time checkpoint in Arabidopsis. Plant Cell 2014, 26:3589-3602. BBX19 is introduced as a negative regulator of flowering time under inductive photoperiods in Arabidopsis. The authors demonstrate, that the B-Box 1 motif is essential for the protein–protein interaction with the floral promoter CONSTANS. They propose that FT expression is precisely timed based on the balance of BBX19/CO superimposed on their opposing expression rhythms.

9. 

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