Current Season Photoassimilate Distribution in Sweet Cherry

in Journal of the American Society for Horticultural Science

Sweet cherry (Prunus avium) tree canopies comprise three types of leaf populations: fruiting spur (FS), nonfruiting spur (NFS), and extension shoot (ES) leaves. The contribution of each leaf population as sources of photoassimilate synthesis and distribution for sweet cherry fruit development has not been described previously. To determine how carbon fixed by different leaf populations is distributed to reproductive and vegetative sinks during fruit development, fruiting branches of 7-year-old ‘Ulster’ sweet cherry trees grown on ‘Gisela®6’ (Gi6) (Prunus cerasus × Prunus canescens) rootstock at Michigan State University’s Clarksville Research Center (Clarksville, MI) were exposed to 13CO2 labeling on five dates in 2003 [25, 40, 44, 56, and 75 days after full bloom (DAFB), which occurred on 30 Apr.], comprising the period from late Stage I (SI) to late Stage III (SIII) of fruit development. Forty-eight hours after labeling, whole branches were removed and separated into different organs for 13C analysis by gas chromatography–mass spectrometry (GC-MS). The organs analyzed included: FS leaves, NFS leaves, ES leaves, fruit, and wood + bark from the segment of the branch corresponding to each leaf population. Relative distribution of C from each leaf population source to each sink varied during fruit development. Overall, the proportion of 13C recovered in the fruit was highest for the FS leaf population (which included fruit exposure to 13CO2), followed by the NFS leaves, then ES leaves. From SI to SIII, ≈60% of the 13C recovered in the FS portion of the branch was found in the fruit, except during the exponential growth of fruit in mid-SIII (56 DAFB) when this proportion was nearly 80%. About 30% of the 13C fixed by NFS leaves was found in the fruit during Stage II (SII) (40 DAFB) and early (44 DAFB) and late (75 DAFB) SIII, with higher proportions at SI (45% at 25 DAFB) and mid-SIII (70%). About 25% of the 13C fixed by ES leaves was found in the fruit during SI, SII, and late SIII, with a lower proportion (17%) at early SIII when shoot growth was exponential, and a higher proportion (nearly 60%) at mid-SIII. The proportion of 13C fixed and translocated to ES growth was minimal from FS and NFS leaves throughout the sampling dates, but that by the ES leaves was significant, peaking at early SIII. The results illustrate the dynamics of C contribution from each leaf population between vegetative and reproductive sinks during growth in sweet cherry orchards, which provides useful physiological information for canopy pruning and crop load regulation.

Abstract

Sweet cherry (Prunus avium) tree canopies comprise three types of leaf populations: fruiting spur (FS), nonfruiting spur (NFS), and extension shoot (ES) leaves. The contribution of each leaf population as sources of photoassimilate synthesis and distribution for sweet cherry fruit development has not been described previously. To determine how carbon fixed by different leaf populations is distributed to reproductive and vegetative sinks during fruit development, fruiting branches of 7-year-old ‘Ulster’ sweet cherry trees grown on ‘Gisela®6’ (Gi6) (Prunus cerasus × Prunus canescens) rootstock at Michigan State University’s Clarksville Research Center (Clarksville, MI) were exposed to 13CO2 labeling on five dates in 2003 [25, 40, 44, 56, and 75 days after full bloom (DAFB), which occurred on 30 Apr.], comprising the period from late Stage I (SI) to late Stage III (SIII) of fruit development. Forty-eight hours after labeling, whole branches were removed and separated into different organs for 13C analysis by gas chromatography–mass spectrometry (GC-MS). The organs analyzed included: FS leaves, NFS leaves, ES leaves, fruit, and wood + bark from the segment of the branch corresponding to each leaf population. Relative distribution of C from each leaf population source to each sink varied during fruit development. Overall, the proportion of 13C recovered in the fruit was highest for the FS leaf population (which included fruit exposure to 13CO2), followed by the NFS leaves, then ES leaves. From SI to SIII, ≈60% of the 13C recovered in the FS portion of the branch was found in the fruit, except during the exponential growth of fruit in mid-SIII (56 DAFB) when this proportion was nearly 80%. About 30% of the 13C fixed by NFS leaves was found in the fruit during Stage II (SII) (40 DAFB) and early (44 DAFB) and late (75 DAFB) SIII, with higher proportions at SI (45% at 25 DAFB) and mid-SIII (70%). About 25% of the 13C fixed by ES leaves was found in the fruit during SI, SII, and late SIII, with a lower proportion (17%) at early SIII when shoot growth was exponential, and a higher proportion (nearly 60%) at mid-SIII. The proportion of 13C fixed and translocated to ES growth was minimal from FS and NFS leaves throughout the sampling dates, but that by the ES leaves was significant, peaking at early SIII. The results illustrate the dynamics of C contribution from each leaf population between vegetative and reproductive sinks during growth in sweet cherry orchards, which provides useful physiological information for canopy pruning and crop load regulation.

In most tree fruit, carbon for fruit and canopy structural growth is provided initially by storage pools, transitioning to current assimilates as leaves become photosynthetically competent (Corelli-Grappadelli et al., 1994; Roper et al., 1988; Teng et al., 2001, 2002; Wünsche et al., 2005). In sweet cherry, reproductive and vegetative growth occurs simultaneously during spring and early summer (Roper et al., 1987). FS and NFS leaf area (LA) is derived from preformed vegetative meristems and reaches a maximum within 3–4 weeks of budbreak (Lang, 2005). However, on well-managed trees, ES LA continues developing from budbreak through harvest, transitioning from preformed to neoformed vegetative meristem activity and leaf expansion. Actively growing aerial sinks (i.e., flowers, fruit, spurs, and ES) compete for the C provided by these different leaf populations (Ayala and Lang, 2008; Roper et al., 1988). Roper et al. (1987) suggested that import of photoassimilates synthesized by leaves distal to FSs may be required for optimal fruit development, and branch girdling and defoliation studies demonstrated negative effects on quality traits when fruit were isolated from the major sources of photoassimilates (Ayala and Lang, 2004).

Fruit trees can be considered as a collection of individual sinks (reproductive and vegetative) that compete with each other (DeJong, 1999; Wright, 1989). The sink demand of an organ and its competitive ability to attract assimilates varies by developmental stage during the season (Fischer et al., 2012; Flore and Layne, 1999; Wright, 1989). The C available to individual organs depends on the supply of photoassimilates from sources (i.e., leaves and storage reserves) and the organ’s sink demand (Ayala and Lang, 2015; Basile et al., 2002). Farrar (1996) and Minchin et al. (1997) suggested that the distribution of assimilates is controlled by the entire source–sink pathway in the plant system and is not a property of sinks alone. By contrast, dry weight (DW) partitioning among sinks is regulated by sink development (Li et al., 2015; Marcelis, 1996).

Fruit are major sinks for assimilates (DeJong and Walton, 1989). In Prunus species, fruit development follows a double sigmoidal curve, which is divided into three stages (Berman and DeJong, 1996; Flore, 1994). Following pollination and fruit set, SI is characterized by active cell division and rapid initial fruit growth. SII or “pit hardening” is associated with endocarp lignification and slower growth of the pericarp. SIII or “final swell” is a period of rapid fruit growth characterized by mesocarp cell enlargement and DW accumulation. The length of each phenological stage is influenced by the ripening characteristics of the variety, which may vary by up to 8–9 weeks in sweet cherry. The shortest stage of cherry fruit development is SII, and 50% to 80% of fruit growth occurs during SIII (Flore, 1994). Roper et al. (1988) suggested that because sweet cherry fruit development occurs during a relatively short timeframe (60–70 d), fruit might be high priority sinks. In peach (Prunus persica) and apple (Malus ×domestica), periods of resource limitation lead to a competition for photoassimilates between reproductive and vegetative organs (Grossman and DeJong, 1995; Pavel and DeJong, 1993; Reyes et al., 2016).

The objective of this study was to determine how C assimilated by FS, NFS, and ES leaf populations on fruiting sweet cherry branches is distributed to competing sinks. It was hypothesized that the distribution of C fixed by each leaf population would be differentially influenced by dynamic changes in competing reproductive and vegetative sink demands from fruit set to ripening. The contribution of each leaf population as sources of photoassimilate synthesis and distribution for sweet cherry fruit development has not been described previously.

Materials and Methods

Plant material and environment.

The experiment was conducted at Michigan State University’s Clarksville Research Center, Clarksville, MI (lat. 42.8°N, long. 85.2°W). In 2003, mature (7 years old) ‘Ulster’ sweet cherry trees on Gi6 rootstock were selected for pulse-labeling with 13CO2. Two rows of ‘Ulster’ alternated with two rows of ‘Hedelfingen’ on ‘Gisela®5’ (Gi5) as the cross-pollen source. The trees were grown in a coarse-loamy, mixed, mesic Typic Hapludalf soil of the Lapeer series, trained to a central leader and had similar height (3.0 m), trunk cross-sectional area, and canopy LA (12.8 ± 0.5 m2). The trees were planted 2.5 m within the row (maintained weed-free with herbicide) and 4.6 m between rows (with grass alleys), and were not pruned or thinned during the experiment. Trees were not protected against rain or birds. Fertilizer, drip irrigation, and plant protection pesticides were applied following standard commercial practices. Growing degree days [GDD (base 4.4 °C)], a measure of heat accumulation for plant growth, was used to associate phenological stages and developmental rates of fruit, leaves, and shoots from budbreak to the end of SIII. Full bloom (FB) occurred on Apr. 30.

Phenological characterization before 13CO2 pulsing.

Six hundred 2-year-old fruiting branches having similar vigor, crop load, length, and diameter were selected for 13CO2 pulse-labeling and growth measurements. Morphological measurement range means for the selected branches were: length (97.4–100.8 cm), diameter (18.1–22.1 mm), number of FS and NFS (12–14), FS and NFS leaf number (4.7–6.0), and fruit number (two to three fruit per spur). Most of the branches were located in the middle to upper sections of the canopy, 1.5–2.5 m above the ground. Terminal ES growth (i.e., length and leaf number) was measured weekly from budbreak until terminal budset for all branches. LA for each experimental branch was estimated by counting the total spur number (FS and NFS) and number of ES nodes before each 13C-pulse, and measuring the LA of 15 FS, NFS, and ES using detached leaves and a LA meter (LI-3100; LI-COR, Lincoln, NE). Leaf area per spur (FS and NFS) ranged from 68.1 ± 5.3 to 134.4 ± 5.2 cm2. Leaf area of ES at terminal budset ranged between 785 ± 7.3 and 876 ± 9.3 cm2.

Twenty fruit (F) per branch were measured for fresh weight [FW (grams)] and DW (grams), diameter (millimeters), and soluble solids content [SSC (percent)]. Thirty FS, NFS, and ES were measured for FW, DW, leaf number, and LA.

Treatments (T) and 13C labeling.

From the 600-branch population previously characterized, a group of 200 branches were selected randomly for growth measurements, and a group of 400 branches were selected randomly for labeling (or as nonlabeled controls). For each leaf population (T = 3) and pulse date (Date = 5), 10 single branch replications (n = 10) were used for each sampling date (immediately and 48 h after pulsing). Branch sections corresponding to FS (leaves plus fruit), NFS (leaves only), and ES (leaves plus new shoot) leaf populations were labeled with short pulses of 13CO2 at 25 d (SI), 40 d (SII), 44 d (early SIII), 56 d (mid-SIII), or 75 d [late SIII (terminal budset)] DAFB. Each labeling date corresponded to the noted phenological stage during fruit development and was a sunny day with the following mean daily temperatures: SI at 11 °C, SII at 16 °C, early SIII at 18 °C, mid-SIII at 27 °C, and late SIII at 21 °C. There was no rain between pulse date and sampling 48 h later except following the mid-SIII pulse, which had 2.8 mm of rain in between pulsing and sampling. Three additional nonlabeled branches were removed at each date to quantify natural 13C abundance in leaves.

For each labeled branch, one complete section (FS leaves plus fruit, NFS leaves, or ES leaves plus new shoot) was enclosed in a transparent polyester film (Mylar®; DuPont, Wilmington, DE) balloon chamber of appropriate volume and pulsed for 15–20 min with 13CO2 when assimilation rates were positive, between 1000 and 1200 hr. 13CO2 was generated by injecting 80% lactic acid into a 1-L wash bottle containing barium carbonate (98 atom percent 13C), and swirling and pumping the bottle to deliver a total of 3.9 mmol of 13CO2 into each chamber. The average rate of CO2 uptake for each date was calculated. Photosynthetically active radiation ranged between 1456 and 1835 μmol·m−2·s−1 during 13C labeling. Single leaf gas exchange was measured with an IR gas analyzer (CIRAS-2; PP-Systems, Haverhill, MA) for FS, NFS, and ES leaves on selected branches before and during the pulse-labeling. Net assimilation rate (A) varied between 15.7 and 20.4 μmol·m−2·s−1 CO2 among the three leaf populations and dates.

Sampling and 13C analysis.

Immediately after labeling, three fully expanded leaves were sampled from each leaf type to estimate the initial total 13C fixed by each leaf population. When FS were the labeled population, individual fruit were also sampled to estimate the 13C fixed because of fruit photosynthesis.

At 48 h after each pulse-labeling, each branch was removed at its base to measure FW and DW of different organs and prepare them for 13C enrichment analysis by GC-MS (20–20 mass spectrometer and ANCA-GSL sample combustion unit; PDZ Europa, Sandbach, UK). The organs analyzed included: FS leaves, NFS leaves, ES leaves, fruit, and wood + bark from the segment of the branch corresponding to each leaf population. Extension shoots were divided further into mature fully expanded leaves, developing leaves, young leaves, and wood. In addition, 10 single fruit from the FS section that had been labeled directly with 13C were divided into pericarp (epicarp + mesocarp) and endocarp. All plant materials were oven-dried at 70 °C for 72–96 h and ground using a Wiley mill (20 and 40 mesh; Thomas Scientific, Swedesboro, NJ). Additional samples were prepared from unlabeled branches for natural abundance calculations. 13C enrichment for different organs was calculated according to Boutton (1991) and Vivin et al. (1996).

Statistical analysis.

Analysis of variance was conducted by using PROC MIXED procedures of the SAS statistical analysis program (SAS Institute, Cary, NC). The statistical model for the overall experiment was a three-way factorial design with three factors: leaf type (T = 3), date (Date = 5), and organ (O = 8). As extremely high levels of 13C enrichment were expected in directly labeled leaves, these were not considered for statistical analysis.

Results and Discussion

Growth and fruiting of 2-year-old branches

Extension shoot growth on ‘Ulster’/Gi6 commenced around FB and terminal budset occurred at 75 DAFB, with an average length of 34 cm and 19 leaves per ES (Table 1), and six leaves per spur (FS or NFS). Mean LA per spur was ≈10% larger for NFS compared with FS [129 vs. 118 cm2 (data not shown)]. Mean area per leaf was greatest for ES leaves (44 cm2), which were just over twice the mean size of spur leaves [22 cm2 for NFS and 21 cm2 for FS leaves (data not shown)]. The ES proportion of the total branch LA increased from 8% at 25 DAFB to 21% at 75 DAFB. The LA:F of ES almost doubled from 25 to 75 DAFB (Table 1).

Table 1.

‘Ulster’/‘Gisela®6’ sweet cherry fruit fresh weight (FW) and growth data for 2-year-old branches (n = 10) at each 13CO2 pulse-labeling date [25, 40, 44, 56, and 75 d after full bloom (DAFB)]. Full bloom was on 30 Apr.

Table 1.

Fruit set occurred between 5 and 12 DAFB [256–312 GDD (FB = 30 Apr.)], and fruit growth at SI continued until 32 DAFB (319–483 GDD). Stage II occurred from 33 to 46 DAFB (492–604 GDD), with the greatest increase in fruit FW between 44 and 56 DAFB, continuing through 75 DAFB (Table 1). Between 44 and 56 DAFB, fruit FW gain averaged 0.2 g·d−1, and between 56 and 75 DAFB, fruit FW gain averaged 0.13 g·d−1. The end of SIII coincided with terminal budset at 75 DAFB (618–1135 GDD). The number of fruit per branch varied from 95 to 66, decreasing over time because of natural fruit drop. This resulted in a maximum LA:F ratio of 60.4 cm2 at the end of SIII. This low LA:F value explains the relatively low fruit FW attained at maturity for these branches. Whiting and Lang (2004) reported that a LA:F ratio of around 210 cm2 is required to produce sweet cherry fruit weights of 9–10 g, depending on the growing location. Therefore, the branches in this experiment were source-limited for the competition between fruit and shoot growth (Grossman and DeJong, 1995; Pavel and DeJong, 1993).

During the 25–75 DAFB sampling period, the total branch DW increased 178% as shown in Fig. 1. Most of this increase was attributed to fruit DW, which increased 534% over the sampling period. The proportional DW increases in the other organs–tissues was 448% for ES leaves and shoot growth, 69% for NFS leaves and wood, and 49% for FS leaves and wood. More than 50% of the total DW for the individual branch was attributed to fruit at harvest. These data imply proportional sink activities that were highest for fruit, followed by new shoots.

Fig. 1.
Fig. 1.

Total ‘Ulster’/‘Gisela®6’ sweet cherry dry weight (DW) accumulation (mean ± se) per 2-year-old branch, partitioned into organ types, at each 13CO2 pulse-labeling date (see arrows). Full bloom was on 30 Apr. (n = 30).

Citation: Journal of the American Society for Horticultural Science J. Amer. Soc. Hort. Sci. 143, 2; 10.21273/JASHS04200-17

13C Translocation patterns in 2-year-old branches

Total 13C in leaves and fruit immediately after pulsing.

All experimental branches labeled were highly enriched by each 13CO2 pulse, as indicated by total 13C content immediately after pulsing (Table 2). Total 13C content was highest at 75 DAFB, when fruit were fully ripe and ES growth was essentially complete. The greatest enrichment generally occurred from labeling the FS branch section, especially during SI and the most rapid phase of fruit growth during mid-SIII. All three-branch sections were comparably enriched at 40, 44, and 75 DAFB. Twenty-five ES were shorter and with fewer leaves resulting in lower enrichment levels than spur leaves.

Table 2.

Total 13C content recovered in 2-year-old branches of ‘Ulster’/‘Gisela®6’ sweet cherry immediately (after chamber removal) following 13C pulse-labeling to fruiting spur (FS), nonfruiting spur (NFS), and extension shoot (ES) branch sections (n = 10) at 25, 40, 44, 56, and 75 d after full bloom (DAFB). Calculations were made based on total dry weight (DW) of branches. Full bloom was on 30 Apr.

Table 2.

Fruit on the FS branch section were directly exposed to 13CO2 and the presence of significant levels of 13C in fruit immediately after pulsing indicated that fruit were actively photosynthesizing (Table 3). The 13C content in fruit was highest at 25 DAFB. Fruit fixation was significant but less at 40 and 44 DAFB, and became minimal at 56 and 75 DAFB, corresponding to the later stages of ripening with loss of chlorophyll and increased anthocyanin synthesis. Fruit photosynthesis has been reported for sour cherry [P. cerasus (Kappes and Flore, 1986, 1989)]. It is likely that 13C fixed directly by fruit mainly affect the C budget of individual fruit (DeJong and Walton, 1989; Hansen, 1970; Kappes, 1985). In sour cherry, fruit gross photosynthesis contributed 19%, 30%, and 1.5% of the carbohydrates (CH2O) used during SI, SII, and SIII, respectively. Seventy percent of the CH2O is incorporated into fruit DW, whereas the rest is used in dark respiration (Flore and Layne, 1999). In apple, fruit photosynthesis constituted <15% of the total C supply during the season (Jones, 1981), although it may contribute to early fruit growth (Lakso et al., 1999).

Table 3.

Total 13C content recovered in ‘Ulster’/‘Gisela®6’ sweet cherry fruit sampled from 2-year-old branches (n = 10) immediately (after chamber removal) following 13C pulse-labeling of the fruiting spur (FS) section at 25, 40, 44, 56, and 75 d after full bloom (DAFB). Full bloom was on 30 Apr.

Table 3.

Total 13C in leaves and fruit 48 h after pulsing.

Across all labeling dates, the total amount of 13C recovered in the branches 48 h after pulsing was lower than the amount of 13C fixed initially (Table 2 vs. Tables 46), indicating likely export of 13C to other parts of the tree and respiratory loss. Loescher et al. (1986) estimated that 16% to 23% of the total CH2O requirements for sweet cherry fruit growth are used in respiration, whereas in peach 16% to 20% of the seasonal CH2O requirements are respired by developing fruit (DeJong and Walton, 1989). A large proportion of the 13C remained in the pulsed leaves (Tables 46). The exception to this was at 56 DAFB, when the 13C remaining in all of the pulsed leaf populations was at the lowest relative levels compared with all other pulse dates. High sink activity related to rapid fruit growth and reduced leaf CH2O levels has been reported previously in sweet cherry (Roper et al., 1987, 1988) and japanese pear [Pyrus pyrifolia (Teng et al., 2001)].

Table 4.

Total 13C recovered per branch and relative 13C distribution among organs on 2-year-old branches of ‘Ulster’/‘Gisela®6’ sweet cherry trees 48 h after 13CO2 pulsing of the fruiting spur (FS) branch section (n = 10). Percentages are based on absolute amounts of 13C recovered for each organ at each 13CO2 pulse-labeling date [25, 40, 44, 56, and 75 d after full bloom (DAFB)]. Full bloom was on 30 Apr.

Table 4.
Table 5.

Total 13C recovered and relative 13C distribution among organs on 2-year-old branches (n = 10) of ‘Ulster’/‘Gisela®6’ sweet cherry trees 48 h after 13CO2 pulsing of the nonfruiting spur (NFS) branch section. Percentages are based on absolute amounts of 13C recovered for each organ at each pulse-labeling date [25, 40, 44, 56, and 75 d after full bloom (DAFB)]. Full bloom was on 30 Apr.

Table 5.
Table 6.

Total 13C recovered and relative 13C distribution among organs on 2-year-old branches (n = 10) of ‘Ulster’/‘Gisela®6’ sweet cherry trees 48 h after 13CO2 pulsing of the extension shoot branch section. Percentages are based on absolute amounts of 13C recovered for each organ at each pulse-labeling date [25, 40, 44, 56, and 75 d after full bloom (DAFB)]. Full bloom was on 30 Apr.

Table 6.

At 48 h after pulsing, there were significant differences in 13C content among different organs of the branch, depending on the pulsed leaf population (Tables 46). For the three source leaf populations, the greatest proportion of translocated 13C was detected in fruit throughout SI, SII, and SIII. However, there were significant differences among leaf populations regarding the relative amount of 13C accumulated in fruit for each pulse-labeling date. The highest relative 13C levels in fruit were detected when FS leaves were the labeled source; these ranged from 57% to 63% across all labeling dates except at 56 DAFB when levels peaked at 79% (Table 4). The second most important C source for fruit was NFS leaves, with relative 13C levels ranging from around 32% at 40, 44, and 75 DAFB to 71% at 56 DAFB (Table 5). The lowest relative 13C levels recovered in fruit, around 22% to 28%, were from ES leaves as the source of photoassimilates, although again at 56 DAFB, relative 13C levels peaked at 59% (Table 6). These consistently high relative 13C levels recovered in fruit from all source leaf populations during mid-SIII suggest that this is the period of strongest fruit sink strength and the period when additional source LA is most needed to optimize fruit growth.

Fruiting spur, NFS, and ES leaves all supplied current photoassimilates to fruit and vegetative growth during SI, SII, and SIII of fruit development. Across all pulse-labeling dates, 13C fixed by FS leaves was translocated predominantly to fruit and wood subtending those leaves (Table 4). In 87% of 13C-enriched branches, very minor acropetal translocation of 13C was detected in NFS leaves, NFS wood, ES leaves, and wood. 13C fixed by NFS leaves was translocated predominantly basipetally to fruit and fruiting wood (Table 5). Significant amounts of 13C were detected in the wood subtending the NFS leaves. However, acropetal 13C translocation to ES wood and leaves also was observed. Only 12% of enriched branches did not exhibit translocation to either FS or ES. Bidirectional translocation from the NFS leaves has been shown previously for sweet cherry on the dwarfing rootstock Gi5, in which NFS leaves translocated 13C primarily to fruit during final swell, but also to ES growth (Ayala, 2004). Unidirectional and bidirectional transport from different leaf populations also have been reported for apple (Corelli Grappadelli et al., 1994; Hansen, 1969; Toselli et al., 2014; Wang et al., 2003; Zhou et al., 2015), sour cherry (Kappes and Flore, 1986; Toldam-Andersen, 1998), japanese pear (Zhang et al., 2005), pecan [Carya illinoinensis (Davis and Sparks, 1974)], persimmon [Diospyrus khaki (Nakano et al., 1998; Simkhada et al., 2007)], and grape [Vitis vinifera (Hale and Weaver, 1962)]. The highest total recoveries of 13C for both spur leaf populations occurred 56 DAFB, coincident with peak fruit growth as shown in Fig. 1.

ES growth was not a strong sink for assimilates during sweet cherry fruit development in these relatively heavily-cropped ‘Ulster’ trees on the semivigorous rootstock Gi6. Minimal amounts of 13C (<1%) were found in ES when FS and NFS leaves were labeled (Tables 4 and 5). Conversely, Kappel (1991) reported that, with ‘Lambert’ sweet cherry on vigorous P. avium seedling rootstocks, ES growth had a greater sink strength for photosynthates than fruit. Source–sink relationships and relative C distribution can be influenced by rootstock genotype (Caruso et al., 1997; Moing and Gaudillere, 1992). Fruit growth can affect ES development negatively in sweet cherry trees on dwarfing rootstocks (Whiting, 2005; Whiting and Lang, 2004). In ‘Bing’ on semidwarfing Gi5, heavy cropping reduced ES elongation and DW accumulation (Correa, 2008). Similarly in peach, the presence of fruit influenced primary and secondary growth (Costes et al., 2000), and stem length and DW accumulation, suggesting competition for C between vegetative growth and fruit (Grossman and DeJong, 1995). This competition requires orchard management strategies to adjust the LA:F ratio to avoid an imbalance between vegetative and reproductive sinks during fruit development (Ayala and Andrade, 2009; Lang, 2001a, 2001b; Whiting and Lang, 2004).

In this experiment, when terminal ES leaves were labeled directly, the basal and medial leaves had higher 13C enrichments than did young apical leaves (data not shown). Young ES apical leaves imported minimal amounts of 13C fixed by FS and NFS leaves. In sour cherry, ES become net CH2O exporters 17 d after budbreak (Kappes, 1985). ES of apple begin C export with 9–17 leaves (Corelli-Grappadelli et al., 1994; Lakso and Corelli-Grappadelli, 1992), whereas peach ES begin exporting to fruit 30 DAFB (Corelli-Grappadelli et al., 1996).

13C fixed by the ES leaf population was translocated basipetally to NFS leaves, NFS wood, FS leaves, FS wood, and fruit (Table 6). Several branches (16%) did not translocate 13C to either FS or NFS leaves. Most of the translocated 13C was in fruit, followed by either NFS wood or FS wood. The highest 13C contents in fruit were found at 56 DAFB, when ES were 30 cm (20 leaves) in length (Table 1), and the highest total recovery of 13C occurred at 75 DAFB, when shoots were 34 cm (i.e., 22 leaves) in length. The lowest total recovery of 13C was at 25 DAFB, when ES were 10 cm in length and had only 10 leaves. The lowest 13C export from ES was at the beginning of SIII (44 DAFB, 570 GDD), when shoots were elongating rapidly.

Translocation of 13C to, and within, fruit

When the total 13C translocation to the fruit, from all sources, is combined for each pulsing date, the extremely strong fruit sink activity at 56 DAFB is apparent with more than twice the total 13C content (65,055 μg/fruit) than for that found at any other date (Table 7). On a relative 13C distribution basis, the FS leaf population always contributed the most, around half of that recovered. At 25 DAFB, the NFS leaves were an important source for 13C, and during the period of greatest fruit sink demand, the NFS leaves were statistically similar to the FS leaves. As the ES leaf population reached its maximum LA (75 DAFB), the 13C provided by those leaves became statistically similar to that of the NFS leaf population, with each providing ≈25% of the 13C found in the mature fruit.

Table 7.

Total 13C content in sweet cherry fruit derived from all pulsed sources on 2-year-old branches (n = 10) of ‘Ulster’/‘Gisela®6’ trees 48 h after 13CO2 pulsing of fruiting spur (FS) leaves and fruit, nonfruiting spur (NFS) leaves, and extension shoot (ES) leaves. Percentages are based on absolute amounts of 13C recovered in fruit at each pulse-labeling date [25, 40, 44, 56, and 75 d after full bloom (DAFB)]. Full bloom was on 30 Apr.

Table 7.

In this study, the sink demand of sweet cherry fruit varied during development and fruit were stronger sinks for photoassimilates than shoots, as has been reported for peach (Grossman and DeJong, 1995). In sour cherry the highest fruit sink strength was during SIII (Flore and Layne, 1999). During SI, sink activity of a small sweet cherry fruit requires 13C assimilates for cell division. At this stage in our study, the highest 13C atom percent excess per unit basis was detected in fruit. Hansen (1987) indicated that increased sink activity of fruit promotes the uptake of assimilates, which in turn accelerates its growth rate. Sour cherry small fruit exhibit strong sink activity by removing C from the translocation system, which supports their high specific growth rate during early fruit development (Toldam-Andersen, 1998). Similarly, the sink activity of immature small grape berries is important for DW accumulation during the first week of growth when cell expansion is slow (Coombe, 1989).

The distribution of translocated 13C between the fruit pericarp (epicarp + mesocarp) and pit (endocarp + embryo) changed significantly during development (Table 8). From late SI through most of SII (25–40 DAFB), 74% to 79% of the total 13C in the fruit was recovered from the pit. The transition from SII to SIII (44 DAFB) marked the beginning of a shift in relative 13C distribution, from 2:1 pit:pericarp at 44 DAFB to 1:3 at 56 DAFB and 1:4 at 75 DAFB. Teng et al. (2001) reported that japanese pear fruit accumulated most of the 13C in the flesh during the period of active growth. Similar results have been reported for peach (Corelli-Grappadelli et al., 1996).

Table 8.

Relative 13C partitioning between ‘Ulster’/‘Gisela®6’ sweet cherry fruit pericarp and endocarp (n = 5) 48 h after 13CO2 pulsing of fruiting spur (FS) leaves and fruit at 25, 40, 44, 56, and 75 d after full bloom (DAFB). Calculations and statistical analyses are based on absolute amounts of 13C recovered at each pulse-labeling date. Full bloom was on 30 Apr.

Table 8.

Conclusions

This study examined how source–sink relationships at specific phenological stages influence the uptake and distribution of current season photosynthates in sweet cherry trees on highly productive rootstocks such as Gi6. On average, during fruit development, FS leaves contributed more 13C (60% to 80%) to fruit than did NFS (30% to 70%) and ES (18% to 60%) leaves. The exception was at 56 DAFB (mid-SIII, 812 GDD), a period of rapid cell enlargement and DW accumulation, when the amounts of 13C translocated to fruit were significantly higher from all 13C sources compared with the other pulse-labeling dates. In ‘Ulster’/Gi6 trees, SI (319–483 GDD) and mid-SIII (753–874 GDD) were the critical periods of potentially restricted C availability, because of limited ES LA during the former period and high fruit sink strength during the latter period.

Therefore, these results confirm the need to potentially reduce crop load during the early stages of fruit development to avoid negatively affecting fruit quality, particularly, size, SSC, firmness, and postharvest life. This has important implications for orchard management strategies such as dormant pruning, fruit thinning (i.e., intensity and type), and tree nutrition to maintain adequate LA to support fruit growth. To reduce the potential for resource limitations during fruit development, particularly in highly precocious dwarfing rootstock/scion combinations, more intensive dormant pruning could be imposed, with complementary flower or fruit thinning in orchards prone to excessively high yields. Heading cuts may be favored over thinning cuts to stimulate new ES LA and reduce the density of future spur flower bud formation. Fertilization strategies to build storage reserves for the promotion of larger FS and NFS leaf development in spring would also shift the LA:F ratio favorably. Additional studies of sweet cherry source–sink relationships at specific phenological stages would be valuable to further examine partitioning variations in relation to growing conditions and other rootstocks and varieties.

Literature Cited

  • AyalaM.2004Carbon partitioning in sweet cherry (Prunus avium L.) on dwarfing precocious rootstocks during fruit development. Michigan State Univ. East Lansing MI PhD Diss

  • AyalaM.AndradeP.2009Effects of fruiting spur thinning on fruit quality and vegetative growth of sweet cherry (Prunus avium)Revista Ciencia e Investigación Agraria36443450

    • Search Google Scholar
    • Export Citation
  • AyalaM.LangG.A.2004Examining the influence of different leaf populations in sweet cherry fruit qualityActa Hort.636481488

  • AyalaM.LangG.A.200813C-Photoassimilate partitioning in sweet cherry on dwarfing rootstocks during fruit developmentActa Hort.795625632

    • Search Google Scholar
    • Export Citation
  • AyalaM.LangG.A.201513C-Photoassimilate partitioning in sweet cherry (Prunus avium L.) during early springCiencia e Investigación Agraria42191203

    • Search Google Scholar
    • Export Citation
  • BasileB.MariscalM.J.DayK.R.JohnsonJ.S.DeJongT.M.2002Japanese plum (Prunus salicina L.) fruit growth: Seasonal pattern of source/sink limitationsJ. Amer. Pomol. Soc.568693

    • Search Google Scholar
    • Export Citation
  • BermanM.E.DeJongT.M.1996Water stress and crop load effects on fruit flesh weights in peach (Prunus persica L.)Tree Physiol.16859864

  • BouttonT.W.1991Stable carbon isotope ratios of natural materials: I. Sample preparation and mass spectrometric analysis p. 155–200. In: D.C. Coleman and B. Fry (eds.). Carbon isotope techniques. Academic Press New York NY

  • CarusoT.P.IngleseP.SidariM.SottileF.1997Rootstock influences seasonal dry matter and carbohydrate content and partitioning in above ground components of ‘Flordaprince’ peach treesJ. Amer. Soc. Hort. Sci.122673679

    • Search Google Scholar
    • Export Citation
  • CoombeB.G.1989The grape as a sinkActa Hort.239149159

  • Corelli-GrappadelliL.LaksoA.N.FloreJ.A.1994Early season patterns of carbohydrate partitioning in exposed and shaded apple branchesJ. Amer. Soc. Hort. Sci.119596603

    • Search Google Scholar
    • Export Citation
  • Corelli-GrappadelliL.RavagliaG.AsirelliA.1996Shoot type and light exposure influence carbon partitioning in peach cv. Elegant LadyJ. Hort. Sci.71533543

    • Search Google Scholar
    • Export Citation
  • CorreaJ.E.2008Effect of spur thinning on the photoassimilate translocation and the morphological characteristics of sweet cherry fruit (Prunus avium L.) in the combination ‘Bing’/‘Gisela®5’. Pontificia Universidad Católica de Chile Santiago Chile MSc Thesis

  • CostesE.FournierD.SallesJ.C.2000Changes in primary and secondary growth as influenced by crop load in ‘Fantasme’ apricot treeJ. Hort. Sci. Biotechnol.75510519

    • Search Google Scholar
    • Export Citation
  • DavisJ.T.SparksD.1974Assimilation and translocation patterns of carbon-14 in the shoots of fruiting pecan treesJ. Amer. Soc. Hort. Sci.99468480

    • Search Google Scholar
    • Export Citation
  • DeJongT.M.1999Developmental and environmental control of dry-matter partitioning in peachHortScience3410371040

  • DeJongT.M.WaltonE.F.1989Carbohydrate requirements of peach fruit growth and respirationTree Physiol.5329335

  • FarrarJ.F.1996Sinks-integral parts of a whole plantJ. Expt. Bot.4712731279

  • FischerG.Almanza-MerchánP.J.RamírezF.2012Source-sink relationships in fruit species: A reviewRevista Colombiana de Ciencias Horticolas6238253

    • Search Google Scholar
    • Export Citation
  • FloreJ.A.1994Stone fruit p. 233–270. In: B. Schaffer and P.C. Andersen (eds.). Handbook of environmental physiology of fruit crops Volume I: Temperate crops. CRC Press Boca Raton FL

  • FloreJ.A.LayneD.R.1999Photoassimilate production and distribution in cherryHortScience3410151019

  • GrossmanY.L.DeJongT.M.1995Maximum vegetative growth potential and seasonal partterns of resource dynamics during peach growthAnn. Bot.76473482

    • Search Google Scholar
    • Export Citation
  • HaleC.R.WeaverR.J.1962The effect of developmental stage on direction of translocation of photosynthates in Vitis viniferaHilgardia3389131

    • Search Google Scholar
    • Export Citation
  • HansenP.196914C studies on apple trees. IV. Photosynthate consumption in fruits in relation to the leaf-fruit ratio and to leaf-fruit positionPhysiol. Plant.22186198

    • Search Google Scholar
    • Export Citation
  • HansenP.197014C studies on apple trees. VI. The influence of the fruit on the photosynthesis of the leaves, and the relative photosynthetic yields of fruits and leavesPhysiol. Plant.23805810

    • Search Google Scholar
    • Export Citation
  • HansenP.1987Source/sink effects in fruits: An evaluation of various elements p. 29–37. In: C.J. Wright (ed.). Manipulation of fruiting. Butterworths London UK

  • JonesH.G.1981Carbon dioxide exchange of developing apple (Malus pumila Mill.) fruitsJ. Expt. Bot.3212031210

  • KappelF.1991Partitioning of above-ground dry matter in ‘Lambert’ sweet cherry trees with or without fruitJ. Amer. Soc. Hort. Sci.116201205

    • Search Google Scholar
    • Export Citation
  • KappesE.M.1985Carbohydrate production balance and translocation in leaves shoots and fruits of ‘Montmorency’ sour cherry. Michigan State Univ. East Lansing MI PhD Diss

  • KappesE.M.FloreJ.A.1986Carbohydrate balance models for ‘Montmorency’ sour cherry leaves, shoots and fruit during developmentActa Hort.184123127

    • Search Google Scholar
    • Export Citation
  • KappesE.M.FloreJ.A.1989Phyllotaxy and stage of leaf and fruit development influence initiation and direction of carbohydrate export from sour cherry leavesJ. Amer. Soc. Hort. Sci.114642648

    • Search Google Scholar
    • Export Citation
  • LaksoA.N.Corelli-GrappadelliL.1992Implications of pruning and training practices to carbon partitioning and fruit development in appleActa Hort.322231239

    • Search Google Scholar
    • Export Citation
  • LaksoA.N.WünscheJ.N.PalmerJ.W.Corelli-GrappadelliL.1999Measurement and modeling of carbon balance of the apple treeHortScience3410401047

    • Search Google Scholar
    • Export Citation
  • LangG.A.2001aCritical considerations for sweet cherry training systemsCompact Fruit Tree3437073

  • LangG.A.2001bIntensive sweet cherry orchard systems-rootstocks, vigor, precocity, productivity and managementCompact Fruit Tree3412326

  • LangG.A.2005Underlying principles of high density sweet cherry productionActa Hort.667325336

  • LiT.HeuvelinkE.MarcelisL.F.2015Quantifying the source-sink balance and carbohydrate content in three tomato cultivarsFront. Plant Sci.6416110

    • Search Google Scholar
    • Export Citation
  • LoescherW.RoperT.KellerJ.1986Carbohydrate partitioning in sweet cherriesProc. Washington State Hort. Assn.81240248

  • MarcelisL.F.M.1996Sink strength as determinant of dry matter partitioning in the whole plantJ. Expt. Bot.4712811291

  • MinchinP.E.H.ThorpeM.R.WünscheJ.N.PalmerJ.W.PictonR.F.1997Carbon partitioning between apple fruits: short- and long-term response to availability of photosynthateJ. Expt. Bot.4814011406

    • Search Google Scholar
    • Export Citation
  • MoingA.GaudillereJ.P.1992Carbon and nitrogen partitioning in peach/plum graftsTree Physiol.108192

  • NakanoR.YonemoriK.SugieraA.1998Fruit respiration for mantaining sink strength during final swell at growth stage III of persimmon fruitJ. Hort. Sci. Biotechnol.73341346

    • Search Google Scholar
    • Export Citation
  • PavelE.W.DeJongT.M.1993Source and sink-limited growth period of developing peach fruits indicated by relative growth rate analysisJ. Amer. Soc. Hort. Sci.118820824

    • Search Google Scholar
    • Export Citation
  • ReyesF.DeJongT.FranceschiP.TagliaviniM.GianelleD.2016Maximum growth potential and periods of resource limitation in apple treeFront. Plant Sci.7233112

    • Search Google Scholar
    • Export Citation
  • RoperT.KellerJ.D.LoescherW.H.RomC.R.1988Photosynthesis and carbohydrate partitioning in sweet cherry: Fruiting effectsPhysiol. Plant.724247

    • Search Google Scholar
    • Export Citation
  • RoperT.LoescherW.KellerJ.RomC.1987Sources of photosynthate for fruit growth in ‘Bing’ sweet cherryJ. Amer. Soc. Hort. Sci.112808812

    • Search Google Scholar
    • Export Citation
  • SimkhadaE.P.SekozawaY.SugayaS.GemmaH.2007Translocation and distribution of 13C-photosynthates in ʻFuyuʼ persimmon (Diospyros kaki) grafted onto different rootstocksJ. Food Agr. Environ.5184189

    • Search Google Scholar
    • Export Citation
  • TengY.TamuraF.TanabeK.2002Partitioning patterns of photosynthates from different shoot types in ʻNijisseikiʼ pear (Pyrus pyrifolia Nakai)J. Hort. Sci. Biotechnol.77758765

    • Search Google Scholar
    • Export Citation
  • TengY.TanabeK.TamuraF.OhmaeA.2001Fate of photosythates from spur leaves of ‘Nijisseiki’ pear during the period of rapid fruit growthJ. Hort. Sci. Biotechnol.76300304

    • Search Google Scholar
    • Export Citation
  • Toldam-AndersenT.B.1998The seasonal distribution of 14C-labelled photosynthates in sour cherry (Prunus cerasus)Acta Hort.48531540

  • ToselliM.MarcoliniG.FloreJ.LombardiniL.2014Leaf assimilation, carbon translocation and root respiration in ʻBudagovski 9ʼ apple cuttings grown in low soil moisture conditionEur. J. Hort. Sci.79241247

    • Search Google Scholar
    • Export Citation
  • VivinP.MartinF.GuehlJ.M.1996Acquisition and within plant allocation of 13C and 15N in CO2 enriched Quercus robur plantsPhysiol. Plant.988996

    • Search Google Scholar
    • Export Citation
  • WangL.Q.TangF.ZhangJ.ShuH.R.2003Effect of dwarfing rootstock on carbohydrate transportation and distribution of appleActa Agriculturae Nucleatae Sinica17212214

    • Search Google Scholar
    • Export Citation
  • WhitingM.D.2005Physiological principles for growing premium fruit p. 57–64. In: M.D. Whiting (ed.). Producing premium cherries: Pacific Northwest fruit school cherry short course proceedings. Good Fruit Grower Press Yakima WA

  • WhitingM.D.LangG.2004‘Bing’ sweet cherry on the dwarfing rootstock ‘Gisela 5’: Thinning affect fruit quality and vegetative growth but not net CO2 exchangeJ. Amer. Soc. Hort. Sci.129407415

    • Search Google Scholar
    • Export Citation
  • WrightC.J.1989Interactions between vegetative and reproductive growth p. 15–27. In: C.J. Wright (ed.). Manipulation of fruiting. Butterworths London UK

  • WünscheJ.N.GreerD.H.LaingW.A.PalmerJ.W.2005Physiological and biochemical leaf and tree responses to crop level in appleTree Physiol.2512531263

    • Search Google Scholar
    • Export Citation
  • ZhangC.TanabeK.TamuraF.ItaiA.WangS.2005Spur characteristics, fruit growth, and carbon partitioning in two late maturing Japanese pear (Pyrus pyrifolia Nakai.) cultivars con contrasting fruit sizeJ. Amer. Hort. Sci.130252260

    • Search Google Scholar
    • Export Citation
  • ZhouY.Q.QinS.J.MaX.X.ZhangJ.E.ZhouP.SunM.WangB.S.ZhouH.F.LyuD.G.2015Effect of interstocks on the photosynthetic characteristics and carbon distribution of young apple trees during the vigorous growth period of shootsEur. J. Hort. Sci.80296305

    • Search Google Scholar
    • Export Citation

If the inline PDF is not rendering correctly, you can download the PDF file here.

Contributor Notes

The research reported was funded in part by a grant from the Michigan Cherry Committee, and supported by Michigan Sate University’s AgBioResearch, the USDA National Institute of Food and Agriculture’s Hatch projects MICL02002 and MICL01305, and Pontificia Universidad Católica de Chile.

Corresponding author. E-mail: mayalaz@uc.cl.

  • View in gallery

    Total ‘Ulster’/‘Gisela®6’ sweet cherry dry weight (DW) accumulation (mean ± se) per 2-year-old branch, partitioned into organ types, at each 13CO2 pulse-labeling date (see arrows). Full bloom was on 30 Apr. (n = 30).

  • AyalaM.2004Carbon partitioning in sweet cherry (Prunus avium L.) on dwarfing precocious rootstocks during fruit development. Michigan State Univ. East Lansing MI PhD Diss

  • AyalaM.AndradeP.2009Effects of fruiting spur thinning on fruit quality and vegetative growth of sweet cherry (Prunus avium)Revista Ciencia e Investigación Agraria36443450

    • Search Google Scholar
    • Export Citation
  • AyalaM.LangG.A.2004Examining the influence of different leaf populations in sweet cherry fruit qualityActa Hort.636481488

  • AyalaM.LangG.A.200813C-Photoassimilate partitioning in sweet cherry on dwarfing rootstocks during fruit developmentActa Hort.795625632

    • Search Google Scholar
    • Export Citation
  • AyalaM.LangG.A.201513C-Photoassimilate partitioning in sweet cherry (Prunus avium L.) during early springCiencia e Investigación Agraria42191203

    • Search Google Scholar
    • Export Citation
  • BasileB.MariscalM.J.DayK.R.JohnsonJ.S.DeJongT.M.2002Japanese plum (Prunus salicina L.) fruit growth: Seasonal pattern of source/sink limitationsJ. Amer. Pomol. Soc.568693

    • Search Google Scholar
    • Export Citation
  • BermanM.E.DeJongT.M.1996Water stress and crop load effects on fruit flesh weights in peach (Prunus persica L.)Tree Physiol.16859864

  • BouttonT.W.1991Stable carbon isotope ratios of natural materials: I. Sample preparation and mass spectrometric analysis p. 155–200. In: D.C. Coleman and B. Fry (eds.). Carbon isotope techniques. Academic Press New York NY

  • CarusoT.P.IngleseP.SidariM.SottileF.1997Rootstock influences seasonal dry matter and carbohydrate content and partitioning in above ground components of ‘Flordaprince’ peach treesJ. Amer. Soc. Hort. Sci.122673679

    • Search Google Scholar
    • Export Citation
  • CoombeB.G.1989The grape as a sinkActa Hort.239149159

  • Corelli-GrappadelliL.LaksoA.N.FloreJ.A.1994Early season patterns of carbohydrate partitioning in exposed and shaded apple branchesJ. Amer. Soc. Hort. Sci.119596603

    • Search Google Scholar
    • Export Citation
  • Corelli-GrappadelliL.RavagliaG.AsirelliA.1996Shoot type and light exposure influence carbon partitioning in peach cv. Elegant LadyJ. Hort. Sci.71533543

    • Search Google Scholar
    • Export Citation
  • CorreaJ.E.2008Effect of spur thinning on the photoassimilate translocation and the morphological characteristics of sweet cherry fruit (Prunus avium L.) in the combination ‘Bing’/‘Gisela®5’. Pontificia Universidad Católica de Chile Santiago Chile MSc Thesis

  • CostesE.FournierD.SallesJ.C.2000Changes in primary and secondary growth as influenced by crop load in ‘Fantasme’ apricot treeJ. Hort. Sci. Biotechnol.75510519

    • Search Google Scholar
    • Export Citation
  • DavisJ.T.SparksD.1974Assimilation and translocation patterns of carbon-14 in the shoots of fruiting pecan treesJ. Amer. Soc. Hort. Sci.99468480

    • Search Google Scholar
    • Export Citation
  • DeJongT.M.1999Developmental and environmental control of dry-matter partitioning in peachHortScience3410371040

  • DeJongT.M.WaltonE.F.1989Carbohydrate requirements of peach fruit growth and respirationTree Physiol.5329335

  • FarrarJ.F.1996Sinks-integral parts of a whole plantJ. Expt. Bot.4712731279

  • FischerG.Almanza-MerchánP.J.RamírezF.2012Source-sink relationships in fruit species: A reviewRevista Colombiana de Ciencias Horticolas6238253

    • Search Google Scholar
    • Export Citation
  • FloreJ.A.1994Stone fruit p. 233–270. In: B. Schaffer and P.C. Andersen (eds.). Handbook of environmental physiology of fruit crops Volume I: Temperate crops. CRC Press Boca Raton FL

  • FloreJ.A.LayneD.R.1999Photoassimilate production and distribution in cherryHortScience3410151019

  • GrossmanY.L.DeJongT.M.1995Maximum vegetative growth potential and seasonal partterns of resource dynamics during peach growthAnn. Bot.76473482

    • Search Google Scholar
    • Export Citation
  • HaleC.R.WeaverR.J.1962The effect of developmental stage on direction of translocation of photosynthates in Vitis viniferaHilgardia3389131

    • Search Google Scholar
    • Export Citation
  • HansenP.196914C studies on apple trees. IV. Photosynthate consumption in fruits in relation to the leaf-fruit ratio and to leaf-fruit positionPhysiol. Plant.22186198

    • Search Google Scholar
    • Export Citation
  • HansenP.197014C studies on apple trees. VI. The influence of the fruit on the photosynthesis of the leaves, and the relative photosynthetic yields of fruits and leavesPhysiol. Plant.23805810

    • Search Google Scholar
    • Export Citation
  • HansenP.1987Source/sink effects in fruits: An evaluation of various elements p. 29–37. In: C.J. Wright (ed.). Manipulation of fruiting. Butterworths London UK

  • JonesH.G.1981Carbon dioxide exchange of developing apple (Malus pumila Mill.) fruitsJ. Expt. Bot.3212031210

  • KappelF.1991Partitioning of above-ground dry matter in ‘Lambert’ sweet cherry trees with or without fruitJ. Amer. Soc. Hort. Sci.116201205

    • Search Google Scholar
    • Export Citation
  • KappesE.M.1985Carbohydrate production balance and translocation in leaves shoots and fruits of ‘Montmorency’ sour cherry. Michigan State Univ. East Lansing MI PhD Diss

  • KappesE.M.FloreJ.A.1986Carbohydrate balance models for ‘Montmorency’ sour cherry leaves, shoots and fruit during developmentActa Hort.184123127

    • Search Google Scholar
    • Export Citation
  • KappesE.M.FloreJ.A.1989Phyllotaxy and stage of leaf and fruit development influence initiation and direction of carbohydrate export from sour cherry leavesJ. Amer. Soc. Hort. Sci.114642648

    • Search Google Scholar
    • Export Citation
  • LaksoA.N.Corelli-GrappadelliL.1992Implications of pruning and training practices to carbon partitioning and fruit development in appleActa Hort.322231239

    • Search Google Scholar
    • Export Citation
  • LaksoA.N.WünscheJ.N.PalmerJ.W.Corelli-GrappadelliL.1999Measurement and modeling of carbon balance of the apple treeHortScience3410401047

    • Search Google Scholar
    • Export Citation
  • LangG.A.2001aCritical considerations for sweet cherry training systemsCompact Fruit Tree3437073

  • LangG.A.2001bIntensive sweet cherry orchard systems-rootstocks, vigor, precocity, productivity and managementCompact Fruit Tree3412326

  • LangG.A.2005Underlying principles of high density sweet cherry productionActa Hort.667325336

  • LiT.HeuvelinkE.MarcelisL.F.2015Quantifying the source-sink balance and carbohydrate content in three tomato cultivarsFront. Plant Sci.6416110

    • Search Google Scholar
    • Export Citation
  • LoescherW.RoperT.KellerJ.1986Carbohydrate partitioning in sweet cherriesProc. Washington State Hort. Assn.81240248

  • MarcelisL.F.M.1996Sink strength as determinant of dry matter partitioning in the whole plantJ. Expt. Bot.4712811291

  • MinchinP.E.H.ThorpeM.R.WünscheJ.N.PalmerJ.W.PictonR.F.1997Carbon partitioning between apple fruits: short- and long-term response to availability of photosynthateJ. Expt. Bot.4814011406

    • Search Google Scholar
    • Export Citation
  • MoingA.GaudillereJ.P.1992Carbon and nitrogen partitioning in peach/plum graftsTree Physiol.108192

  • NakanoR.YonemoriK.SugieraA.1998Fruit respiration for mantaining sink strength during final swell at growth stage III of persimmon fruitJ. Hort. Sci. Biotechnol.73341346

    • Search Google Scholar
    • Export Citation
  • PavelE.W.DeJongT.M.1993Source and sink-limited growth period of developing peach fruits indicated by relative growth rate analysisJ. Amer. Soc. Hort. Sci.118820824

    • Search Google Scholar
    • Export Citation
  • ReyesF.DeJongT.FranceschiP.TagliaviniM.GianelleD.2016Maximum growth potential and periods of resource limitation in apple treeFront. Plant Sci.7233112

    • Search Google Scholar
    • Export Citation
  • RoperT.KellerJ.D.LoescherW.H.RomC.R.1988Photosynthesis and carbohydrate partitioning in sweet cherry: Fruiting effectsPhysiol. Plant.724247

    • Search Google Scholar
    • Export Citation
  • RoperT.LoescherW.KellerJ.RomC.1987Sources of photosynthate for fruit growth in ‘Bing’ sweet cherryJ. Amer. Soc. Hort. Sci.112808812

    • Search Google Scholar
    • Export Citation
  • SimkhadaE.P.SekozawaY.SugayaS.GemmaH.2007Translocation and distribution of 13C-photosynthates in ʻFuyuʼ persimmon (Diospyros kaki) grafted onto different rootstocksJ. Food Agr. Environ.5184189

    • Search Google Scholar
    • Export Citation
  • TengY.TamuraF.TanabeK.2002Partitioning patterns of photosynthates from different shoot types in ʻNijisseikiʼ pear (Pyrus pyrifolia Nakai)J. Hort. Sci. Biotechnol.77758765

    • Search Google Scholar
    • Export Citation
  • TengY.TanabeK.TamuraF.OhmaeA.2001Fate of photosythates from spur leaves of ‘Nijisseiki’ pear during the period of rapid fruit growthJ. Hort. Sci. Biotechnol.76300304

    • Search Google Scholar
    • Export Citation
  • Toldam-AndersenT.B.1998The seasonal distribution of 14C-labelled photosynthates in sour cherry (Prunus cerasus)Acta Hort.48531540

  • ToselliM.MarcoliniG.FloreJ.LombardiniL.2014Leaf assimilation, carbon translocation and root respiration in ʻBudagovski 9ʼ apple cuttings grown in low soil moisture conditionEur. J. Hort. Sci.79241247

    • Search Google Scholar
    • Export Citation
  • VivinP.MartinF.GuehlJ.M.1996Acquisition and within plant allocation of 13C and 15N in CO2 enriched Quercus robur plantsPhysiol. Plant.988996

    • Search Google Scholar
    • Export Citation
  • WangL.Q.TangF.ZhangJ.ShuH.R.2003Effect of dwarfing rootstock on carbohydrate transportation and distribution of appleActa Agriculturae Nucleatae Sinica17212214

    • Search Google Scholar
    • Export Citation
  • WhitingM.D.2005Physiological principles for growing premium fruit p. 57–64. In: M.D. Whiting (ed.). Producing premium cherries: Pacific Northwest fruit school cherry short course proceedings. Good Fruit Grower Press Yakima WA

  • WhitingM.D.LangG.2004‘Bing’ sweet cherry on the dwarfing rootstock ‘Gisela 5’: Thinning affect fruit quality and vegetative growth but not net CO2 exchangeJ. Amer. Soc. Hort. Sci.129407415

    • Search Google Scholar
    • Export Citation
  • WrightC.J.1989Interactions between vegetative and reproductive growth p. 15–27. In: C.J. Wright (ed.). Manipulation of fruiting. Butterworths London UK

  • WünscheJ.N.GreerD.H.LaingW.A.PalmerJ.W.2005Physiological and biochemical leaf and tree responses to crop level in appleTree Physiol.2512531263

    • Search Google Scholar
    • Export Citation
  • ZhangC.TanabeK.TamuraF.ItaiA.WangS.2005Spur characteristics, fruit growth, and carbon partitioning in two late maturing Japanese pear (Pyrus pyrifolia Nakai.) cultivars con contrasting fruit sizeJ. Amer. Hort. Sci.130252260

    • Search Google Scholar
    • Export Citation
  • ZhouY.Q.QinS.J.MaX.X.ZhangJ.E.ZhouP.SunM.WangB.S.ZhouH.F.LyuD.G.2015Effect of interstocks on the photosynthetic characteristics and carbon distribution of young apple trees during the vigorous growth period of shootsEur. J. Hort. Sci.80296305

    • Search Google Scholar
    • Export Citation
All Time Past Year Past 30 Days
Abstract Views 206 58 0
Full Text Views 245 96 11
PDF Downloads 77 49 5