Scots pine has been reported recently (Hansen and Beck .... mâ2 sâ1. During summer, maximal photosynthetic rates were considerably higher but the saturating light intensities ..... Jarvis PG, James GB, Landsberg JJ (1976) Coniferous Forest.
Springer-Verlag 1996
Trees (1996) 11: 83 – 90
O R I G I N A L A RT I C L E
Jens Hansen
?
Gerd Vogg
?
Erwin Beck
Assimilation, allocation and utilization of carbon by 3-year-old Scots pine
Pinus sylvestris
(
L .) trees during winter and early spring
Received: 3 November 1995 / Accepted: 1 March 1996
AbstractmThe photosynthetic capacity of frost-hardy and frost-sensitive needles of 3-year-old Scots pines and the allocation and utilization of assimilated carbon was examined during winter and early spring. The photosynthates of the whole trees were labelled by 14CO2 fixation and after chase periods of from 7 days to 4 months under natural climatic conditions, the distribution of radiocarbon in the various tissues of the trees was determined. During winter maximal photosynthetic rates of 1-year-old needles were considerably lower than in summer when calculated on a leaf area basis. However, when related to the chlorophyll content these discrepancies disappeared. The decrease of the photosynthetic capacity upon frost-hardening could be attributed to a two- to three-fold reduction in the chlorophyll content of the needles. The pulse-chase experiments showed that photosynthesis during the cold season preferentially provides substrates for respiration. Half of the assimilated 14C was respired during the first week, and after chase periods of 3 – 4 months the trees contained not more than 10 – 20% of the radiocarbon. The carbon, which was exported by the needles, was translocated basipetally via the twigs and the stem to the roots. Whereas in the axial system incorporation of radiocarbon into storage compounds, like starch, and into cell wall material was almost negligible during the cold season, in the roots one-third of the radiocarbon was recovered from starch 2 months after the 14C-pulse. In contrast to the above-ground parts of the trees, where starch content was very low during winter, in the roots considerable amounts of starch, up to 450 µmol hexose units ? g– 1 DW, were found even during mid-winter. In early spring the radiocarbon in the cell wall-, lipid-, and starch-fraction accounted for more than 80% of the 14C recovered at that time from the axial system. Incorporation of minor quantities into the cell wall fraction of the roots during winter and early spring indicate continuous root
J. Hansen ( ) ? G. Vogg ? E. Beck Lehrstuhl Pflanzenphysiologie, Universita¨t Bayreuth, Universita¨tsstrasse 30, D-95440 Bayreuth, Germany
growth during the cold period as well as in early spring. Whereas during winter the buds did not attract freshly assimilated carbon, in spring just before bud break substantial amounts of carbon were translocated from the needles into the buds. In contrast, remobilization of carbon, which had been assimilated during autumn of the previous year, and import into the sprouting buds could not be demonstrated. Key wordsmPhotosynthesis ? 14C-labelling ? Carbon allocation ? Starch ? Pinus sylvestris
Introduction
Evergreen conifers exhibit photosynthetic capacity during the whole year. However, during the cold season photosynthetic production may be seriously curtailed. In montane regions of central Europe photosynthesis has been described to be completely inhibited for several months or overridden by respiration (Schulze et al. 1967; Pisek and Winkler 1958). In areas with a more moderate winter climate a positive photosynthetic production has been reported (Helms 1965; Fry and Phillips 1977; Ludlow and Jarvis 1971). However, a positive carbon balance of spruce trees during the cold season may be less important for the annual carbon budget because the production of new needles appears not to be dependent on that carbon (Schulze et al. 1977): In evergreen conifers carbon supply to the sprouting buds is mainly provided by the latest photosynthetic gain of the previous year’s needles (Ursino et al. 1968; Gordon and Larson 1968; Schier 1970; Ziemer 1971). Similarly, in Scots pine, reserve material deposited during autumn of the previous year is of negligible significance for growth of the new shoot and needle generation (Hansen and Beck 1990). However, during the cold season conifers, due to their evergreen leaf biomass, respire at a significantly higher rate than leafless deciduous trees (Pisek and Tranquillini 1954). Whereas photosynthesis stops at a minimum temperature of – 7 °C, respiration continues at
84
much lower temperatures (Ungerson and Scherdin 1965; Pisek and Tranquillini 1954). The root system of evergreen conifers reveals a bimodal pattern of growth activity with maxima in autumn and early spring (cf. Sutton 1969) which is paralleled by an equally bimodal pattern of assimilate import (Shiroya et al. 1966; Smith and Paul 1988; Hansen and Beck 1994). During winter the roots are better protected by the soil against severe frost than the shoot and therefore growth of the roots was observed until mid-winter and growth may continue throughout the cold period (cf. Sutton 1969). Thus, root growth during winter has to be supplied with carbon and the question arises whether the observed root growth activity during the cold season is provided with carbon which is derived directly from winter photosynthesis or from stored reserves. Redistribution of carbon stored in autumn by Scots pine has been reported recently (Hansen and Beck 1990, 1994); however, photosynthetic production and the utilization of carbon assimilated during the cold season has received less attention. In the present study we assessed the carbon gain of Scots pine during the cold season and analysed the distribution and utilization of the recent assimilates in relation to the carbon reserves. Seasonal changes in the photosynthetic performance of young Scots pine trees were investigated under natural climatic conditions and the distribution of assimilates in the whole tree was studied by 14CO2-pulse labelling experiments with chase periods between 1 week and 4 months during winter and early spring.
Materials and methods
16 h before it was returned to the natural environment for time periods between 7 and 131 days.
Sampling At the end of the chase period the trees were dissected into individual annual increments of stem and twigs. The twigs were further separated into axis and needles. Adhering soil particles were carefully removed from the root system which was separated into fine roots and main roots ( 5 mm diameter). The individual fractions were immediately frozen in liquid nitrogen and freeze-dried for 4 days. The plant material was milled to a particle size of 120 µm and aliquot portions were combusted in a sample oxidizer (Canberra-Packard mod. 307, Frankfurt/M., Germany). The 14C content was determined by liquid scintillation counting in a Tri-Carb 2500 TR counter (Canberra-Packard, Frankfurt/M., Germany).
4
Extraction of soluble compounds, lipids and starch Aliquot samples of 50 mg dry weight were extracted twice with 1 ml 70% ethanol containing 5 mM Hepes (N-2-hydroxyethylpiperazine N92-ethanesulphonic acid, pH 7.0) to prevent acidification of the extract. Extraction was performed at +80 °C for 10 min and repeated with 50% ethanol and 5 mM Hepes pH 7.0. For the separation of lipids, the pooled extracts were thoroughly mixed with 4 ml chloroform and subsequently centrifuged for 10 min until two phases appeared. The lower organic phase was washed twice with 2 ml 5 mM Hepes pH 7.0. The upper phases containing the water-soluble compounds were pooled and their 14C content was determined. For an exhaustive extraction of lipophilic compounds the residue from the ethanol extraction was freeze-dried overnight and resuspended in 1 ml benzene (boiling point: 60 – 80 °C). Extraction was performed for 3 h in an ultrasonic bath and repeated once with 1 ml benzene/ether (1:1). The 14C-content of the chloroform- and benzene-/ether-fraction were determined after evaporation of the solvents. The summarized 14C-content of the chloroform- and the benzene-/ether-fractions represent the total labelled lipids. Starch was determined enzymatically using the procedure described by Hansen and Beck (1994).
Trees
Determination of the
Potted 3-year-old Scots pine (Pinus sylvestris L.) trees which grew under ambient climatic conditions in the Botanical Garden of the University of Bayreuth were used for the experiments.
After extraction of the starch the residue was designated as cell wall material. The material was dried at +105 °C for 16 h and analyzed for their 14C content by combustion and liquid scintillation counting as described above.
14C
content of the residue
Gas-exchange measurements Net photosynthesis was measured with an open flow system by use of an infrared gas-analyzer (BINOS-IR, Leybold-Heraeus, Germany). The cuvette system consisted of an assimilation chamber, in which twig sections of the previous year were enclosed. Humidity and temperature inside the cuvette were automatically adjusted to the ambient temperature and relative humidity. The CO2 concentration was at the ambient level. Measurements were accomplished under outdoor climatic conditions on a typical winter and summer day, from the onset of positive net carbon uptake in the morning and evening. Application of
14CO2
One day prior to labelling the trees were brought to controlled climatic conditions in the laboratory. The frozen trees were thawed for 10 h in a climate chamber at +4 °C, and subsequently adapted to room temperature overnight. For the application of the 14CO2 the whole tree was enclosed in an air-tight polyethylene bag together with a vial containing Ba14CO3. 14CO2 in the bag was produced by injection of phosphoric acid (85%) into the vial with a syringe. At the end of the 14CO2pulse the bag was removed and the tree was kept at +4 °C for another
Results Photosynthetic capacity of frost-hardy and frost-sensitive needles of Scots pine Rates of net photosynthesis of 3-year-old Scots pine plants were measured in the field under various ambient light intensities at the end of the winter and during summer. When related to leaf area, rates of net photosynthesis were considerably lower in early March compared to July (Fig. 1B). Even at the low light intensities of the winter months, rates of photosynthesis reached light saturation which was found at a photon flux rate of about 800 µmol m–2 s–1. During summer, maximal photosynthetic rates were considerably higher but the saturating light intensities were only slightly higher. However, when the photosynthetic rates were calculated on a chlorophyll basis noticeable
85 Fig. 1mDependence of net photosynthesis based on chlorophyll content (A) and leaf area (B) on photon fluence density of 1-yearold needles of Scots pine trees under outdoor climatic conditions. Measurements were taken on 2 March 1994 ( ) and 22 July 1994 (●). The leaf temperatures during measurements ranged from 6.0 °C to 7.5 °C ( ), and 27.2 °C to 30.1 °C (●)
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!
differences in net photosynthesis were found only above 800 µmol quanta m–2 s–1 (Fig. 1A). Frost-hardening of the trees during autumn and early winter was accompanied by a two- to three-fold reduction in the chlorophyll content of the needles on fresh weight as well as on leaf area basis (Table 1). Since the chlorophyll a/b ratio did not change during frost-hardening both photosystems appear to become similarly affected by the degradation processes. Therefore, the lower photosynthetic capacity of the frost-hardy needles may be explained by the decreased chlorophyll content. Accordingly, in Scots pine trees frost-hardening of the needles does not result in a reduced photosynthetic performance of the single photosynthetic unit.
Photosynthates of the cold season are mainly consumed by respiration To examine the degree of utilization of the carbon assimilated during the cold season whole Scots pine trees were 14C-labelled by photosynthesis in early winter (December), mid-winter (January and February), and in early spring prior to bud sprouting (April). The distribution of radiocarbon in the whole trees was determined after chase periods of between 7 and 131 days, i.e. before and after bud sprouting. Typically, more than 50% of the assimilated radiocarbon was lost by respiration during the first week after the 14CO2-pulse (Table 2). The rate of respiratory
Table 1mChlorophyll content of 1-year-old needles of unhardened and frost-hardened 3-year-old Scots pine (Pinus sylvestris L.) trees as related to fresh weight (FW) and chlorophyll Chlorophyll content mg Frost-hardened tree Unhardened tree Data = mean
?
0.79 2.01
g–1 FW
+0.08 +0.26
+ SD (n = 23)
mg
?
Chlorophyll a/b ratio m–2
+ +
142 14 369 48
+0.31 +0.20
3.05 3.22
losses of 14C expectedly decreased with increasing chase periods. After chase periods of 95 and 131 days, the trees had retained only 10 – 20% of the assimilated 14C. Thus it is obvious from the pulse-chase experiments that photosynthesis during the cold season provides substrate to respiration rather than serving the formation of storage products. The degree of carbon loss by respiration is strongly affected by the climatic conditions. The pulse-chase experiment in January 1993 was performed during a period of severe frost (Fig. 2). Under these conditions carbon losses after 2 months were considerably lower (tree 3: 39%, Table 2) compared to a similar situation with higher temperatures (tree 8: 73%).
Fig. 2mMaximum and minimum air temperatures as calculated as mean values of periods of 3 days. The temperatures were measured 2 m and 5 cm above ground level. The climate data were recorded by the Deutscher Wetterdienst (Offenbach, Germany) at the Bayreuth climate station (330 m)
86 Table 2mAssimilation of 14CO2 by 1-year-old needles of 3-year-old Scots pine (Pinus sylvestris L.) trees during a 8 h pulse. Recovery and respiratory losses were determined after the indicated chase periods. the climatic conditions during the chase period are represented by the sum of daily mean temperatures below (I) and above (II) 0 °C. The Tree number
Date of pulse labelling
Chase period
(I)
(days)
(°C) 0 –59.5 –116.2
daily mean temperature (Tmean) was calculated as the weighted mean of the air temperature 2 m above ground measured at 7.30 a.m. (T1), 2.30 p.m. (T2), and 9.30 p.m. (T3) according to the following equation: Tmean = (T1 + T2 + 2 × T3)/4 (II)
14CO2
14C-loss
uptake
Recovery of 14C
(°C)
(µmol)
(%)
by respiration (%)
43.7 68.7 110.8
3.8 4.3 3.3
74.1 48.0 61.4
25.9 52.0 38.7
1 2 3
14 Jan 1993 14 Jan 1993 14 Jan 1993
7 23 60
4 5
22 Apr 1993 22 Apr 1993
7 11
0 0
132.3 190.6
4.8 5.2
21.7 17.2
78.3 82.8
6 7 8 9
30 25 26 1
Nov 1993 Nov 1993 Nov 1993 Dec 1993
8 26 59 131
–12.0 –39.1 –53.4 –67.0
24.0 86.1 181.0 504.2
7.3 10.1 8.1 16.4
34.4 53.4 26.9 33.6
65.6 46.6 73.1 66.4
10 11 12 13
1 23 3 24
Mar 1994 Feb 1994 Mar 1994 Feb 1994
7 28 40 95
0 0 0 0
59.4 172.9 240.3 839.8
4.2 6.3 6.6 8.0
22.0 18.0 17.8 11.6
78.0 82.0 82.2 88.4
The fate of non-respired carbon in needles, the axis system and roots Figure 3 shows the distribution pattern of photoassimilated radiocarbon within the trees. The bulk of the assimilated 14C was exported into the axial system of the tree (trees 6 – 8). Export of 14C continued until April. Analysis of the nature of the photosynthates revealed that during winter the export of carbon out of the needles is accomplished at the expense of soluble compounds, which transiently accumulated in the soluble fraction. In contrast, 14C retained in the needles was predominantly deposited as starch and lipids. This portion together with that fraction of radiocarbon which was incorporated into cell wall material accounted for maximally 10 – 20% of the recovered 14C. During winter 1- and 2-year-old needles exported only a minor portion of the assimilated radiocarbon and until early spring a stable 14C content of between 30 and 40% was observed. Whereas in spring the 1-year-old needles exhibit a renewed export of radiocarbon assimilated during winter (tree 9), accumulation of radiocarbon in the 2-year-old needles indicates import of recently produced assimilates (tree 5) and in part also of remobilized reserve compounds (tree 9). In contrast to the winter situation in early spring the storage pool of both age classes of needles represents a strong sink for recently produced photosynthate, since more than 50% of the radiocarbon recovered from the needles was incorporated into starch and to a minor extent into lipids. The carbon, which was exported by the assimilating needles, was translocated basipetally via the twig axis and the stem towards the roots. In the twig axis and the stem an increase in radiocarbon exported from the needles with rising length of the chase period occurred. During winter the incorporation of radiocarbon into cell wall components and storage compounds like lipids and starch was almost
negligible and never exceeded 0.5% of the radiocarbon recovered from the twigs and 4% from the stem (trees 1 – 3 and 6 – 8). Between winter and early spring the pulselabelling experiments revealed a dramatic change in the distribution pattern of the assimilated radiocarbon. In contrast to the situation in January (tree 8), in April (tree 9) the radiocarbon in the cell wall-, lipid- and starch-fraction accounted for more than 80% of the 14C recovered from the axial system. As early as March carbon was rapidly incorporated into starch, lipids and cell wall material (trees 11 – 13). The roots represented the major sink of the tree during the cold season (Fig. 3). With regard to the relatively protected situation of the roots in the soil significant differences in the carbon distribution between the shoots of the tree and the roots were observed during winter. In contrast to the 14C-distribution in the above-ground parts of the tree starch was heavily labelled in the roots: 35% of the radiocarbon recovered from the roots was found in the starch fraction 2 months after the 14C-pulse, indicating ongoing starch synthesis in the roots even during the cold season. These data are consistent with the results of starch quantification in the individual plant parts which show accumulation of large amounts of reserve starch in the root system during the cold season (Table 3). Between winter and early spring the distribution of the carbon in the roots changes significantly. More than 30% of the 14C assimilated at the beginning of March was translocated to the roots and to the main part deposited as reserve starch (Fig. 3: trees 10 – 12). Minor quantities of the carbon were incorporated into the cell wall fraction, but nevertheless indicate a continuing root growth activity in the cold period as well as in early spring. At any time during the winter the buds did not reveal strong sink strength for recently produced assimilates. Just before the beginning of bud sprouting the buds started to act
87 Fig. 3mDistribution (%) of recovered (=100%) 14C which was photoassimilated by 3-yearold Scots pine trees during an 8 h 14CO2-pulse ( ) in January 1993 (14-1-1993: trees 1 – 3), April 1993 (22-4-1993: trees 4 and 5), November 1993 (30-11-1993: trees 6 – 9), and March 1994 (1-3-1994: trees 10 – 13) as determined after chase periods between 7 to 131 days during winter and spring. Harvest of the trees: 1: 21-1-1993; 2: 6-2-1993; 3: 15-3-1993; 4: 29-4-1993; 5: 3-5-1993; 6: 8-12-1993; 7: 21-12-1993; 8: 24-1-1994; 9: 11-4-1994; 10: 8-3-1994; 11: 23-3-1994; 12: 12-4-1994; 13: 30-5-1994. Percent of recovered 14C in ethanol-soluble compounds ( ), lipids ( ), ), and cell wall mastarch ( terial (■■■). The beginning of bud sprouting is indicated by the triangle ( )
;
!
as sink organs and substantial amounts of the carbon fixed in April were allocated to the buds (trees 4, 5). Carbon, assimilated during autumn, which was already incorporated into insoluble materials, was not remobilized for the supply of sprouting buds: in April radiocarbon fixed in November was not incorporated into the buds (tree 9).
The starch content in the different organs during winter and spring In all above-ground organs of the trees the starch content was very low during winter (Table 3). However, during spring an augmented starch synthesis resulted in an accumulation of increasing amounts of reserve starch (trees 4, 5, 10 – 13), and until April starch concentrations of around 650 µmol hexose units ? g DW–1 were reached in the needles. The time of onset of the starch synthesis depends strongly on the climatic conditions. Although in mid-March 1993 starch accumulation had not yet been started due to
subfreezing temperatures (see Fig. 3), in 1994 starch synthesis had already commenced at the beginning of March and accumulation of starch continued until bud sprouting in May. In the roots a completely different situation was observed. Even in mid-winter considerable amounts of starch up to 450 µmol hexose units ? g DW–1 were found in large as well as in fine roots. Nevertheless, the appearance of a period with subfreezing temperatures during March 1993 resulted in a considerable reduction of the starch content in the root system. Therefore, the size of the starch pool in the roots apparently depends on the temperature conditions and freezing of the soil results in a dissolution of the deposited starch.
88 Table 3mStarch content (µmol hexose-units × g–1 DW) of the various organs of 3-year-old Scots pine (Pinus sylvestris L.) trees during winter and spring. (N = needles; A = twig axis. n.d. = not determined) Tree number
Date of harvest
Buds
1-year-old part of twig N
2-year-old part of twig A
N
Stem
Large roots
Fine roots
A
1 2 3
21 Jan 1993 6 Febr 1993 15 Mar 1993
31 10 233
51 21 40
50 19 15
47 26 49
n.d. n.d. n.d.
43 24 24
434 454 151
440 254 140
4 5
29 Apr 1993 3 May 1993
126 332
365 752
243 353
543 847
n.d. n.d.
260 442
702 809
502 671
6 7 8 9
8 Dec 1993 21 Dec 1993 24 Jan 1994 11 Apr 1994
n.d. n.d. 2 94
13 22 10 408
21 24 9 300
26 36 14 394
22 28 15 336
21 18 9 377
192 256 465 725
198 314 571 1262
8 23 12 30
262 76 123 275
160 207 666 622
95 196 315 391
241 414 967 635
78 192 324 476
355 244 326 432
473 778 1289 522
494 1403 1460 361
10 11 12 13
Mar 1994 Mar 1994 Apr 1994 May 1994
Discussion
The distribution of the photosynthate produced during winter and early spring
The contribution of winter time photosynthesis to the carbon balance of evergreen conifers
The allocation of the photosynthate in conifer trees during the growth period has previously been examined by many authors (Shiroya et al. 1966; Gordon and Larson 1968, 1970; Ziemer 1971; Loach and Little 1973). In the present study pulse-labelling experiments have been performed to investigate the dynamic of carbon allocation and assimilate utilization during winter and early spring prior to the onset of the growth period. During winter the young needle generation represents the most important source of photosynthate for the tree. Whereas these needles export the major portion of the labelled photosynthate, the 1-year-old needles retain considerable amounts of the assimilates, this property of the older needles being more pronounced in spring than in winter (Fig. 3). This finding is in accordance with results obtained from other conifers that the assimilate export capacity of the older needles decreases continuously with the progressive maturation of the current needles (Ursino et al. 1968). During winter labelling of the buds does not occur, and the assimilates exported by the needles are translocated basipetally as indicated by a pronounced sink activity of axes and roots (Fig. 3). The translocation of assimilates from the exporting needles to the locations of demand requires a functioning phloem even during winter. In gymnosperms the last-formed sieve cells overwinter in a mature stage (Alfieri and Evert 1968, 1973). As long as subzero temperatures do not prevent transport by freezing of cellular water, long-distance transport of assimilates is possible as it has been demonstrated in Picea abies by the translocation of radiolabelled photosynthate (BlechschmidtSchneider 1990). During winter the root system is by far the dominant sink in the tree. Seven weeks after pulse-labelling in December 25% of the radiocarbon was recovered from
Evergreen conifers have a pronounced seasonal variation in net photosynthesis, which is greatly decreased during winter (Schulze et al. 1967; Gordon and Larson 1968; Jarvis et al. 1976; Tranquillini 1957; Troeng and Linder 1982). Reduction in photosynthetic capacity has been attributed to the severe impact of winter climatic conditions on the photosynthetic apparatus (Senser and Beck 1977; ¨ quist and Martin 1980). However, Martin et al. 1978; O under favourable climatic conditions during winter a recovery of photosynthesis from the winter stress inhibition ¨ quist 1985). may take place within 1 to 2 days (Strand and O Frost-hardening of conifer needles results in a distinct reduction of the chlorophyll content, a feature which Pinus sylvestris shares (Table 1) with other conifers ¨ quist (Perry and Baldwin 1966; Senser et al. 1975; O ¨ 1986; Oquist and Strand 1986). Nevertheless, the measurement of net photosynthesis on a chlorophyll basis indicates that the efficiency of the photosynthetic apparatus is not impaired (Fig. 1A). In the pulse-labelling experiments the contribution of the photosynthetic activity of the evergreen needles to the carbon balance becomes obvious. The measured net carbon uptake represents the carbon yield of a single day and, assuming that the trees will gain carbon every day with mild climatic conditions, on a long-term basis the trees could maintain a positive carbon balance during winter. This is corroborated by the fact that respiration is lowered during periods when the photosynthetic carbon input is diminished under strong frost.
89
the roots (Fig. 3). During spring prior to bud-break the sink activity of the conifer root system further increases, and 32% of the assimilated radiocarbon was translocated to the roots within 6 weeks of chase (Fig. 3). The sink activity of the conifer root system fluctuates significantly during the course of the year. A bimodal course of carbon translocation to the roots with maxima in autumn and spring with a minor but substantial translocation during winter has been observed in several species (Shiroya et al. 1966; Smith and Paul 1988; Hansen and Beck 1994). Shortly prior to bud sprouting a powerful sink develops in the above-ground part of the tree resulting in a transient inversion from a basipetal assimilate flow to an acropetal flow into the developing shoots (Hansen and Beck 1994). In this earlier study a remobilization of reserve material stored during the last autumn for the supply of the growing parts of the shoot was not observed. This also holds true for the reserves which were produced during winter (Fig. 3).
The utilization of reserve compounds in the roots The strong sink activity of the roots during winter is accompanied by a pronounced metabolic activity; 24% (6% of 26%) of the carbon allocated to the roots is converted and deposited as starch (Fig. 3). In contrast to the above-ground parts of the tree, where cold-induced degradation of starch reduces the starch levels, in the roots the accumulation of starch continues throughout the cold period (Table 3). An increase in the starch content of the roots during winter has also been found by other investigators (Ericsson and Persson 1980; Adams et al. 1986). However, on the basis of the pulse-labelling experiments in this study the observed starch accumulation can physiologically be explained as a deposition of translocated assimilates which have been produced by photosynthesis during winter. Prior to bud-break, the sink activity of the roots is further enhanced (Fig. 3). Deposition of the incorporated material as starch prevents redistribution of the gained assimilates and warrants carbon supply for root growth. The deposited starch reserves may be of physiological significance in periods when the carbon demand by the shoot prevents carbon allocation into the roots (Hansen and Beck 1994). In accordance with these findings maxima of root-growth activity have been found in autumn and early spring separated by a period with more or less intensive root growth depending on the winter climatic conditions (cf. Sutton 1969). AcknowledgementsmThe skilful technical assistance of Mrs. S. Bourteele is gratefully acknowledged. Climatic data were kindly provided by the Deutscher Wetterdienst, Offenbach, Germany. This work was supported by the Deutsche Forschungsgemeinschaft.
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