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First published online March 16, 2007; 10.1104/pp.107.095802 Plant Physiology 144:248-257 (2007) © 2007 American Society of Plant Biologists OPEN ACCESS ARTICLE
A Norway Spruce FLOWERING LOCUS T Homolog Is Implicated in Control of Growth Rhythm in Conifers1,[OA]Department of Evolutionary Functional Genomics, Evolutionary Biology Centre, Uppsala University, SE–752 36 Uppsala, Sweden (N.G., T.K., U.L.); and Department of Plant Biology and Forest Genetics, Swedish University of Agricultural Sciences, SE–750 07 Uppsala, Sweden (D.C.)
Growth in perennial plants possesses an annual cycle of active growth and dormancy that is controlled by environmental factors, mainly photoperiod and temperature. In conifers and other nonangiosperm species, the molecular mechanisms behind these responses are currently unknown. In Norway spruce (Picea abies L. Karst.) seedlings, growth cessation and bud set are induced by short days and plants from southern latitudes require at least 7 to 10 h of darkness, whereas plants from northern latitudes need only 2 to 3 h of darkness. Bud burst, on the other hand, is almost exclusively controlled by temperature. To test the possible role of Norway spruce FLOWERING LOCUS T (FT)-like genes in growth rhythm, we have studied expression patterns of four Norway spruce FT family genes in two populations with a divergent bud set response under various photoperiodic conditions. Our data show a significant and tight correlation between growth rhythm (both bud set and bud burst), and expression pattern of one of the four Norway spruce phosphatidylethanolamine-binding protein gene family members (PaFT4) over a variety of experimental conditions. This study strongly suggests that one Norway spruce homolog to the FT gene, which controls flowering in angiosperms, is also a key integrator of photoperiodic and thermal signals in the control of growth rhythms in gymnosperms. The data also indicate that the divergent adaptive bud set responses of northern and southern Norway spruce populations, both to photoperiod and light quality, are mediated through PaFT4. These results provide a major advance in our understanding of the molecular control of a major adaptive trait in conifers and a tool for further molecular studies of adaptive variation in plants.
Trees and other perennial plants must adapt their growth rhythm to seasonal changes in the environment. To a large extent, this adaptation is genetically controlled (Howe et al., 2003  ). A clear example is the strong clinal pattern of growth cessation and bud set in seedlings of the conifer Norway spruce (Picea abies L. Karst.; Ekberg et al., 1976).
Like most conifers, Norway spruce has a long juvenile phase of about 20 years before the first cones are formed. In first-year seedlings, the annual cycle (Fig. 1
) can be summarized as (1) shoot extension stops and terminal buds are set in late summer in response to a shortening photoperiod, after which the cambium ceases growth, needle primordia are initiated within the buds, and frost tolerance begins to increase; (2) rest dormancy (endodormancy) develops in the meristems during autumn after bud set and, with exposure to chilling temperatures (2°C–10°C), changes into quiescence dormancy (ectodormancy) by midwinter, when frost tolerance is maximal; and (3) opening of the bud scales (bud burst) occurs in spring after a temperature sum (TS) has been attained. The extension growth of first-year seedlings consists of the expansion of stem units formed in the current season. This free growth is in the following years (Fig. 1) successively replaced by predetermined growth (expansion of stem units initiated in the preceding growth period) and results in shortening of the period of extension growth. In older seedlings and trees, growth cessation and terminal bud set occur in early summer, presumably under endogenous rather than photoperiodic control (see Clapham et al., 2001a
Seedlings from northern latitudes cease to grow early in the summer, whereas those from more southern locations continue to grow later in the season. This difference is to a large extent determined by a genetically controlled response to photoperiod (Eriksson et al., 1978 ). Seedlings from populations from the Arctic Circle cease to grow and set terminal buds when length of the night exceeds 2 to 3 h, whereas populations from lowlands in central Europe and Romania require 7 to 10 h of darkness to cease growth (Dormling, 1973). Shorter critical night lengths apply when seedlings are raised in continuous light; longer night lengths apply when the seedlings are raised in cycles of light and darkness (Dormling, 1973). Further experiments adding populations from intermediate latitudes have shown that the variation displays a strong latitudinal cline (Clapham et al., 1998a).
Previous experiments in Norway spruce have indicated that photoperiodic control of bud set can be achieved through two different processes, where one or the other dominates depending on the latitude of origin of the plants (for review, see Clapham et al., 1998b
The dark-dominant response is thought to be mediated through PHYP (PhyB type), whereas the light-dominant response is probably mainly mediated through PHYO (PhyA type; Clapham et al., 1998a
The PEBP/RKIP gene family is distinguished by a PEBP domain (Chardon and Damerval, 2005
Besides a role in induction of flowering (both as inducers [FT, MFT] and repressor [TFL1]), recent data also suggest that an FT gene is involved in the photoperiodic control of bud set in an angiosperm tree, Populus (Bohlenius et al., 2006 To test the possible role of Norway spruce PEBP-like genes in growth rhythm, we have now studied expression patterns of four PEBP family genes in seedlings from two populations with divergent bud set response under various photoperiodic conditions. Our data show significant and tight correlation between growth rhythm (both bud set and bud burst) and expression pattern of one of the four Norway spruce PEBP gene family members over a range of photoperiodic conditions.
Expression of PaFT4 Is Tightly Correlated with Bud Set in the Romanian Population Several PEBP family genes have been shown to exhibit diurnal rhythm in angiosperms. To test for diurnal expression of Norway spruce PEBP genes, seedlings from a Romanian population (from latitude 47) were raised in continuous light for 3 months. Seedlings were then transferred to an 8-h light/16-h dark photoperiod (hereafter denoted SD). Needles for RNA extraction were sampled every 4 h for 96 h and mRNA levels for the four Norway spruce PEBP genes (PaFT1–4) were estimated using real-time PCR. Under continuous light, expression levels for all four genes were consistently low, but transfer to SD resulted in a striking induction up to over 250-fold at some time points for one of the genes: PaFT4 (Fig. 2 ). The expression also displayed a diurnal rhythm with the highest expression levels occurring during the light period. PaFT3 also displayed diurnal rhythm, but expression levels were markedly lower and, in contrast to PaFT4, levels did not increase over time (Fig. 3 ). PaFT1 and PaFT2, on the other hand, showed steady expression over time at low levels similar to the average level of PaFT3 (data not shown).
Bud set in Norway spruce seedlings is induced by SDs in the sense that the seedlings set bud in response to one or a few cycles of long nights and SDs, even if they are returned to continuous light after the treatment. When grown up under continuous light, the Romanian population used in this experiment requires four cycles of SD to set terminal buds (Qamaruddin et al., 1995 ). To test whether PaFT4 expression was correlated with bud set, a series of experiments with different photoperiod treatments was conducted and bud set and PaFT4 expression were assayed. One group of seedlings from the Romanian population were again subjected to four cycles of SD and another group to four cycles of 19-h light/5-h dark (denoted LD treatment); both groups were then transferred back to continuous light. The former condition should result in a high frequency of bud set, whereas the latter should result in a low degree of bud set. Two additional groups of plants were transferred to a SD photoperiod with the addition of 1-h night breaks, either 5 h into the night (early night break [ENB]), or 12 h after lights off (late night break [LNB]). Night breaks are known to be efficient in preventing bud set in Romanian populations of Norway spruce when applied close to the critical night length of 7 h, even in an extended 40-h night, whereas a night break later in the night is less efficient (Clapham et al., 2001b). Repeated SD treatment gave a very similar expression profile to the initial SD experiment (Fig. 4 ; correlation coefficient 0.97). The treatment resulted in 82% of the plants setting bud (Fig. 5 ). The PaFT4 expression pattern after LD treatment was strikingly different, with expression constantly low at levels similar to those in constant light (Fig. 4). The low expression levels were paralleled by an almost complete suppression of bud set (2%; Fig. 5). The two night-break treatments resulted in intermediate levels of PaFT4 expression (Fig. 4) as well as bud set (24% and 55% for ENB and LNB, respectively; Fig. 5). Average PaFT4 expression levels (over time) for the different treatments are given in Table I . Expression levels are all significantly different (Wilcoxon paired-sample test, all multiple test corrected, P < 0.0013). There was also a striking correlation between expression level of PaFT4 and bud set in the different experiments (Fig. 5; R2 = 0.92; degrees of freedom = 2; P = 0.046).
Additional sampling of needles after transfer back to constant light revealed that PaFT4 expression in needles returned to the same low levels as before transfer to SD conditions (data not shown). Similar, low PaFT4 levels were observed 5, 12, 18, and 25 d after transfer. During this time, bud set was initiated and completed in induced plants.
Bud set response to photoperiod is very different in Norway spruce populations from northern latitudes. Seedlings from populations north of the Arctic Circle raised in continuous light are induced to set terminal buds after one 16-h night. To study PaFT4 expression and bud set in seedlings from a population from latitude 67, the same four treatments were tested, except that the plants were transferred back to continuous light after two nights. Similar to the Romanian population, PaFT4 expression increased dramatically after transfer to SD conditions, but peak levels were even higher (Fig. 6 ). In contrast to southern populations, night breaks had no or limited effect on expression. Furthermore, expression patterns differed significantly in the LD treatments. Whereas expression remained virtually unchanged in the Romanian population, PaFT4 expression increased significantly in the Arctic population to levels even higher than those seen after night-break treatment in the Romanian one (compare with Figs. 4 and 6; Table I). Average PaFT4 expression for LD in the Arctic population was significantly higher than that for ENB in the Romanian one (Wilcoxon paired-sample test, P = 0.016). These differences were also reflected in the bud set response, with 100% bud set in all treatments, except LD. Bud set after LD treatment was 98% and occurred 1 week later than in the other treatments.
As Romanian and Artic populations differ in their requirement for FR light to prevent bud set, seedlings from both populations were subjected to day extensions with 16 h of FR-deficient cool-white illumination. Under these conditions, PaFT4 expression was strongly induced in northern seedlings, but remained at background level in Romanian seedlings (Fig. 7 ).
Expression Patterns of PaFT1, PaFT2, and PaFT3 Are Not Correlated with Bud Set Expression patterns of PaFT1 and PaFT2 that displayed low and steady expression throughout the experiment in SDs showed similar low and constant expression levels in the other photoperiodic treatments (data not shown). PaFT3, which showed a diurnal expression pattern in SDs, displayed a shift in phase in the short night treatment that was similar in both populations (data not shown). Thus, the shift in phase of PaFT3 was not associated with bud set in the Romanian population. These data suggest that neither PaFT1, PaFT2, nor PaFT3 participate in the control of vegetative bud set.
Air temperature is the major environmental factor regulating timing of bud burst in Norway spruce and many other tree species. A latitudinal trend in temperature response in Norway spruce has also been found in common garden experiments (Hannerz, 1994
Additional sampling of buds from adult trees in natural stands (from the Uppsala area, latitude 60) confirmed high PaFT4 expression levels in vegetative buds sampled in the autumn and low levels at early stages of bud burst in the spring. In samples from August 20, development of the leaf primordia had started with two to three rounds of primordia. On September 4, the shoots had initiated about two-thirds of the final number of needles, whereas on October 29, primordia initiation was complete. PaFT4 expression displayed peak expression around the time of active primordia development and declined thereafter (Fig. 9 ). In April, when bud burst was initiated (swollen buds; compare with. Fig. 1B), expression was very low.
These data corroborate that PaFT4 expression is high in buds during active development of needle primordia and that expression declines when the plants go from an endodormant to an ectodormant stage as an effect of exposure to chilling temperatures during early winter. Further decline in expression was associated with bud burst.
Control of growth cessation in adult trees is poorly known, but numerous experiments have shown that photoperiod is the main cue for induction of bud set in Norway spruce seedlings (Dormling, 1973 ; Ekberg et al., 1976; Clapham et al., 1998a, 1998b). It is also clear that there is a strong genetically controlled latitudinal cline in this response, indicating strong selection on seedling growth rhythm (Clapham et al., 1998a). In Norway spruce seedlings, we found a striking correlation between the expression patterns in needles of one Norway spruce FT-like gene (PaFT4) and photoperiodic induction of bud set. The correlation between bud set and PaFT4 expression was particularly strong in a population from the south of the natural range, one reason being that treatments were chosen to maximize differences in bud set in that population. For comparative reasons, the same treatments were used for the northern population and these treatments caused almost complete bud set in all conditions. Still, the lower PaFT4 expression observed in the LD treatment correlated with a delay of bud set in the northern population. The strong association between the expression levels of PaFT4 and bud set, both between treatments in the Romanian population and between the two populations, clearly suggests that this gene plays a key role in the induction of growth cessation and bud set.
PaFT4 is a member of the plant PEBP gene family for which no functional information is currently available outside the angiosperms. Judging from sequence homology, PaFT4 is most similar to the FT subfamily that has been shown to control induction of reproduction in angiosperms (H. Hedman, T. Källman, D. Moore, M. Lascoux, U. Lagercrantz, and N. Gyllenstrand, unpublished data). Lifschitz and Eshed (2006)
Introduction in tomato (Solanum lycopersicum) of Arabidopsis FT under the filamentous flower promoter results in FT expression mainly in leaf primordia. Such FT expression in leaf primordia results in reduced stem and leaf growth and in frequent meristem arrest in addition to early flowering (Lifschitz et al., 2006
In Norway spruce, PaFT4 is strongly expressed in leaves under SD induction, but, when plants were transferred back to continuous light, expression levels returned to a low level in the leaves even though bud set was initiated. This suggests that expression of PaFT4 induced a transmissible signal directed to the apex. In angiosperms, FT genes are mainly expressed in leaves, particularly in vascular tissues. Current models in Arabidopsis state that FT expression is induced in leaves by the CONSTANS gene (Corbesier and Coupland, 2006
In plants where flowering is induced by LD photoperiods (e.g. Arabidopsis and Lolium), FT is induced in LDs (Kardailsky et al., 1999
In rice, night-break repression of Hd3a and subsequently of flowering requires phyB (Ishikawa et al., 2005
Interestingly, the PaFT4 response is rather different in the northern population, which fits with the hypothesis of light-dominant response (typical of LD plants) in high latitude populations of Norway spruce (Clapham et al., 1998b Our data also showed that PaFT4 expression was high in buds after bud set. In adult trees, the highest expression was seen in late August when growth is characterized by active development of new needle primordia for the coming season. Thus, high PaFT4 expression is associated with cessation of primordial extension and bud set, but not with complete arrest of meristem growth, as development of new leaf primordia is highly active in the presence of high PaFT4 expression. After completion of leaf primordia development, plants are in an endodormant stage so they remain dormant even if exposed to high temperature. Several weeks of low temperature during early winter then transfer the plants to an ectodormant stage, meaning that exposure to high temperature results in bud break (analogous to the effect of vernalization in flowering plants). The transfer to the ectodormant stage was paralleled by a decrease in PaFT4 expression. A further decrease to very low PaFT4 levels was evident during bud burst.
A more detailed phytotron study of bud burst induced by high temperature revealed a gradual decrease in PaFT4 expression. Temperature has also been shown to affect FT expression independently of light in Arabidopsis (Blazquez et al., 2003
Our data strongly suggest that PaFT4 is a key integrator of growth rhythm control in Norway spruce. Our data also support the hypothesis suggested by Lifschitz and Eshed (2006) that the primary and ancestral function of FT-like genes may be the induction and termination of growth. Previous studies have shown that pathways sensitive to R and FR light are important for bud set in southern and northern populations, respectively. Our results indicate that these two pathways controlling bud set and probably a temperature-sensitive pathway controlling bud burst all converge on PaFT4. A key question now is to identify these different pathways and to determine how the divergent responses of northern and southern populations are controlled. PaFT4 provides an essential tool in this quest.
Plant Materials Seedlings from two populations were used in the bud set experiment, a northern from 66.68°N, 150 m above sea level (Jock Valsjärv, Sweden), and a southern from 47.30°N, 750 m above sea level (Frasin, Romania).
Seedlings were raised in a growth room under continuous light from metal halogen lamps at 250 µmol m–2 s–1 (400–700 nm) with a ratio of irradiances at 660 and 730 nm (R:FR) of 2.0, at 20°C for 3 to 4 months. Plants were grown in pots 8.5 x 8.5 x 6 cm, four to a pot, in a mixture of peat and coarse sand, with watering every 1 to 2 d from a weak complete nutrient solution after Ingestad (1979)
The Romanian seedlings were exposed to four cycles of 8-h light/16-h dark (SD) before returning the seedlings to continuous light at 20°C as specified for raising the seedlings. Some of the plants were exposed to 1-h night breaks at 150 µmol m–2 s–1 (R:FR = 3.0), either from 5 to 6 h after lights off (ENB) or from 12 to 13 h after lights off (LNB). Seedlings of the northern population were given two cycles of 8-h light/16-h dark. Some of the plants were exposed to night breaks as described for the Romanian seedlings, but from 2 to 3 h after lights off (ENB) or from 12 to 13 h after lights off (LNB). The ENB was chosen to coincide with the critical night length of the respective populations, where it has been shown to be most effective (Clapham et al., 2001b
To test the response to day extensions with FR-deficient light, seedlings of the two populations were raised for 12 weeks in the growth room in continuous light as previously described and then exposed to the following conditions: (1) 16 h of FR-deficient illumination from Philips TL 40W/29RS fluorescent tubes of the cool-white type, with irradiance at a plant level of 40 µmol m–2 s–1 over the range 400 to 700 nm; the irradiance at 670 nm was 2.23 µmol m–2 s–1 and that at 730 nm was 0.21 µmol m–2 s–1, giving an R:FR ratio of 10.1; (2) 8 h of illumination from fluorescent tubes giving irradiance at a plant level of 200 µmol m–2 s–1, R:FR = 3.0; (3) a second 16-h period of FR-deficient illumination, all at 20°C. Needles were sampled at intervals of 4 h as previously described.
For the bud burst experiment, two clones were chosen that flush with about 2 weeks difference based on phenological observations in the field, one early flushing (1,709) originating from middle Sweden (60°N) and one late flushing (2,644) originating from Belarus (53°N). Clones of both genotypes were grown in a phytotron under controlled temperature and light (250 W, 300 µmol m–2 s–1, 400- to 700-nm spectrum). Plants were released from dormancy by increasing the temperature in steps from 5°C to 20°C. At each sampling, buds from four plants from each clone were collected for RNA extraction.
Total RNA was isolated from needles or buds according to the protocol described in Azevedo et al. (2003)
Data Analysis
Relative quantification using
We thank Kerstin Santesson for lab assistance. Received January 12, 2007; accepted March 10, 2007; published March 16, 2007.
1 This work was supported by the Swedish Research Council, the Swedish Research Council for Environment, Agricultural Sciences, and Spatial Planning, the Carl Tryggers Foundation, and the Philip-Sörensen Foundation. N.G. was supported by the European Union (grant no. QLRT–2001–01973 to Martin Lascoux).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Ulf Lagercrantz (ulf.lagercrantz{at}ebc.uu.se).
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.107.095802 * Corresponding author; e-mail ulf.lagercrantz{at}ebc.uu.se; fax 46–18–471–64 27.
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ABSTRACT
RESULTS
CT values (CTCTRL – CTPaFT4) ± SE are given from two real-time PCR amplifications using different control genes (
-tubulin and polyubiquitin). White and black bars at the top represent light and dark periods.
); SD (8-h light/16-h dark; 
); SD + ENB (
); and SD + LNB (
). White and black bars at the top represent light and dark periods in SD (top) and LD (bottom) conditions. Start points of early and late 1-h night breaks are indicated with double and single arrows, respectively. PaFT4 expression levels were normalized to the average expression level of the LD treatment.
) population during day extensions with R light. Plants were grown in continuous light and transferred to cycles of 16-h cool-white fluorescent light with a R:FR ratio of 10.1 (RL) and 8-h white light with a R:FR ratio of 3.0 (WL). Gray and white bars at the top represent RL and WL periods. PaFT4 expression levels were normalized to the average expression level of the Romanian population.
where 
