JXB Advance Access originally published online on August 30, 2005
Journal of Experimental Botany 2005 56(420):2713-2719; doi:10.1093/jxb/eri264
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RESEARCH PAPER |
13C-photosynthate accumulation in Japanese pear fruit during the period of rapid fruit growth is limited by the sink strength of fruit rather than by the transport capacity of the pedicel
1Laboratory of Horticultural Science, Faculty of Agriculture, Tottori University, Tottori, 680-8533, Japan
2Department of Plant Science, College of Agriculture and Biology, Shanghai Jiaotong University, Shanghai, 201101, China
3Tottori Horticultural Experiment station, Tottori, 689-2221, Japan
* To whom correspondence should be addressed. Fax: +81 857 31674. E-mail: tanabe{at}muses.tottori-u.ac.jp
Received 13 May 2005; Accepted 5 July 2005
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Abstract |
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In Japanese pear, the application of GA3+4 during the period of rapid fruit growth resulted in a marked increase in pedicel diameter and bigger fruit at harvest. To elucidate the relationship between pedicel capacity and fruit growth and to determine the main factor responsible for larger fruit size at harvest, fruit growth and pedicel vascularization after GA application were examined and the carbohydrate fluxes were monitored in a spur unit by non-invasive techniques using 13C tracer. Histological studies of fruit revealed that GA increased the cell size of the mesocarp but not the cell number and core size. The investigation of carbon partitioning showed that an increase in the specific rate of carbohydrate accumulation in fruit or the strength of fruit should be responsible for an increase of fruit weight in GA-treated trees. Observation of pedicel vascularization showed that an increase in pedicel cross-sectional area (CSA) by GA application mainly resulted from phloem and xylem CSA, but it is unlikely that an increase in the transport system is the direct factor for larger fruit size. Therefore, it can be concluded that larger fruit size resulting from GA application during the period of rapid fruit growth caused an increase in the cell size of the mesocarp and increased carbon partitioning to the fruit. Although GA is closely involved with pedicel vascularization, it seems that photosynthate accumulation in fruit is limited by the sink strength of fruit rather than by the transport capacity of the pedicel.
Key words: 13C labelling, fruit growth, gibberellins, Japanese pear, pedicel vascularization, Pyrus pyrifolia Nakai, sink strength
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Regulation of fruit size is a major economical factor for many horticultural plants, including Japanese pear (Gillaspy et al., 1993
; Zhang et al., 2005a, b). For the purpose of producing larger fruit, a range of techniques has been developed for the manipulation of balance between the tree and the environment in practical culture, in particular, the application of plant growth regulators has received much attention during the past few years (Hayashi and Tanabe, 1991; Jackson, 2003).
It is well known that, in many fruits, size is largely a function of cell division in the early stages and cell enlargement in the final stages of fruit growth (Gillaspy et al., 1993). However, final fruit size in a number of species is a function of cell number, which is determined during the early stages of fruit growth (Bohner and Bangerth, 1988; Scorza et al., 1991; Zhang et al., 2005b). Consequently, cytokinins, gibberellins (GAs), and auxin have been applied to promote cell division during the early stages of fruit growth in many species (Ozga and Dennis, 2003). Alternatively, GA is effective in maintaining cell expansion (Gillaspy et al., 1993; Ozga and Dennis, 2003) and therefore exogenous gibberellins have been widely used for fruit enlargement in the production of grape and Japanese pear (Hayashi and Tanabe, 1991). In Japanese pear, it has been proposed that the application of GA4 about 40 d after anthesis (DAA) could significantly increase the final fruit size (Hayashi and Tanabe, 1991). However, there is little information about its physiological mechanism and the role of GA in fruit development is still rather obscure.
In general, the partitioning of assimilates from source leaves is a key factor for fruit development as any limitation of assimilate supply affects the final fruit size. However, the question is what kind of limitation is relevant to fruit growth; is it source limitation, sink limitation, or the capacity of translocation? In a previous report (Zhang et al., 2005a), it was shown that the movement of photosynthates into the fruit was determined by sink strength, while sink strength closely depends on sink activity. Sink activity is determined by many processes such as phloem transport, metabolism, and compartmentation (Ho, 1988), but little attention has been paid to phloem transport as a factor limiting sink organ growth and development. Several lines of evidence suggest a correlation between pedicel diameter and fruit size at harvest (Bustan et al., 1995; Nii, 1998), and it has been proposed that the fruit adjusts the development of vascular connections by the export of growth substances (Aloni, 1987). In addition, the application of exogenous plant growth regulators affected the vascular development of pedicel and resulted in a larger fruit (Aloni, 1987; Guardiola et al., 1993). These observations indicate the possibility of transport limitation during fruit growth. However, the relationship between phloem capacity and fruit growth is still a matter of controversy. In some earlier work on translocation with Citrus, where measurements and estimates were made of the specific mass transfer of dry matter through the phloem, the results suggested that phloem capacity may be a factor limiting fruit growth (Canny, 1973). On the contrary, some studies have shown that assimilate transport is controlled by the sink (Kallarackel and Milburn, 1984; Bruchou and Genard, 1999). The capacity of the transport system is not regarded as a limiting factor for fruit growth (Marcelis, 1996).
Although there are numerous descriptions of the vascular system in the pedicels of many fruit-bearing species (Nii, 1980, 1998; Bustan et al., 1995; Garcia-Luis et al., 2002), the influence that the capacity of the transport system may have on fruit growth is still not fully understood. In this study, fruit growth and pedicel vascularization after GA treatment during the period of rapid fruit growth were examined and the carbohydrate fluxes were monitored in a spur unit by non-invasive techniques using 13C tracer to elucidate the relationship between pedicel capacity and fruit growth and to determine the main factor responsible for larger fruit size at harvest in Japanese pear.
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Materials and methods |
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Plant material and GA3+4 applications
All experiments were performed on 20-year-old Japanese pear ‘Kousui’ (Pyrus pyrifolia Nakai), grafted on Pyrus betulaefolia Bunge rootstocks. ‘Kousui’ is an early-maturing cultivar with medium-sized fruit and one of three dominant cultivars of Japanese pear cultured in Japan. The cultivar was cultured with a flat-canopied pergola system as described by Zhang et al. (2005b)
and hand-pollinated with pollen of ‘Chojuro’ at anthesis. Fruit were hand-thinned to one per spur at 30 DAA according to commercial practice. The pedicel portion closed to current shoot of spur was treated with 20–30 mg gibberellins paste per fruit (concentration of GA3+4: 2.7%, W/W, Kyowa Hakko Chemical, Co. Ltd., Tokyo, Japan) at 42 DAA and the fruit were harvested 91 d after treatment (DAT). The GA-untreated fruit trees were used for the control.
Fruit growth
Ten fruit were sampled after GA application for the determination of fruit fresh weight. The dry weight of fruit was then determined after freeze drying. The water content was obtained from the difference between the fresh weight and the dry weight of fruit.
Core diameter, cell number, and cell length of mesocarp
The fruit in both GA-treated and GA-untreated groups at 14 DAT and at harvest were selected for the determination of core diameter, cell number, and cell length within the mesocarp. The fruit were cut along the equatorial region, then the diameter of the core was measured, and mesocarp width was calculated from the difference between the longest width of a transverse section of fruit and core. Slices of the mesocarp were preserved in formalin:acetic:alcohol (80% ethanol:acetic acid:formalin, 90:5:5 by vol.) for later histological analysis. The measurement of cell number and cell length of the mesocarp was conducted according to Zhang et al. (2005b). A transverse slice of mesocarp was taken along the equatorial region and stained by rubbing softly with a cloth soaked in blue ink. The stained surface was observed under a digital HF microscope system (VH-8000, Keyence, Tokyo, Japan) and an image from a CCD camera displayed on a monitor. Cell length, as an indicator of cell size, was measured from the length of seven contiguous cells from the core to the fruit surface: from these, the average cell length was calculated. Ten observation zones per section were measured. Cell number of the mesocarp along the equatorial region was then calculated by dividing the mesocarp width by the average cell length, and this was taken as an indicator of total cell number per fruit.
Observations of pedicel vascularization
The pedicels were separated from the fruit before measurement of fruit size at 7, 14, and 28 DAT and at harvest and were fixed in a formalin:propionic acid:alcohol (1:1:18 by vol.) until anatomical observation. The pedicel was hand-sectioned using a sharp blade to obtain a transverse section about 40 µm thick at its narrowest portion. These sections were stained with fast green and safranin. Measurements were obtained from 10 pedicels per treatment. The cross-sectional areas (CSA) of pedicel, xylem, primary phloem, secondary phloem, and pith were estimated through digital analysis of the microscope images with the above microscope system. The cross-sectional area of cortex was calculated from the differences between the cross-sectional area of pedicel and the total cross-sectional area of the other components of the tissue mentioned above.
Net photosynthesis
Net photosynthesis (Pn) measurement of individual mature leaves from fruiting spurs were taken using a Shimadzu portable photosynthesis system (Analytical Development Co. Ltd., Hoddesdon, Hertfordshire, UK). The third or fourth leaf from the base of the spur was used for Pn measurement within a spur. Each leaf was a single replication, and there were six replications per treatment.
13C labelling and sampling
The 13C labelling experiment was conducted according to Zhang et al. (2005a, b) and modified in this study. Healthy, uniform 2-year-old fruiting spurs without bourse shoots on a lateral branch were selected for 13C labelling at 7 d and 28 d after treatment. One spur per tree was applied for 13C labelling. Statistically, one tree represented a replicate and four trees were selected. The fruit were covered with aluminium foil to prevent them from fixing carbon dioxide. Individual spurs were exposed to 13CO2 enclosed in a polyethylene bag which contained a 25 ml glass vial fixed on the frame of the bag. The 13CO2 was generated by injecting 3 ml 70% lactic acid on to 0.8 g Ba13CO3 with an abundance of 99% 13C (Cambridge Isoptope Laboratories, Andover, Massachusetts, USA). To ensure an absolute utilization of 13CO2 for photosynthesis, 1.5 h after the start of 13C labelling, unlabelled CO2 was produced by injecting lactic acid into another vial containing 1 g of BaCO3 in the polyethylene bag. Labelling was under ambient field conditions with clear skies and lasted for 2 h between 08.00 h and 10.00 h. The four spurs of both GA-treated trees and untreated trees were harvested 2 h after 13C labelling. Harvested spurs were immediately separated into leaves, current shoot, old wood, and fruit, then stored on ice and brought to the laboratory. Fruit was further divided into pedicel, flesh (exocarp+mesocarp) and core (pith of receptacle+pericarp+seeds). The parts were freeze-dried and then weighed, except that the pedicel was used for anatomical observation according to the method described before. The dried material was finely ground in a coffee mill and stored in glass vials for 13C analyses.
Measurement of 13C
13C abundance and carbon contents were determined using an infrared 13CO2 analyser (Model EX-130S, Japan Spectroscopic Co. Ltd., Tokyo, Japan) after combustion of a sample at 900 °C in an O2 stream according to Okano et al. (1983) and Kouchi and Yoneyama (1984). The absolute amounts (mg) of labelled 13C recovered in each organ were calculated as total carbon in each organ x13C atom%. Since the losses by respiration and exported from the spur were extremely low after 2 h during the period of rapid fruit growth (Zhang et al., 2005a, b), the losses via respiration and export from the spurs were not estimated.
Specific rate of 13C accumulation in fruit
The specific rate of 13C accumulation in fruit (mg mm–2 h–1) was calculated by dividing the amount of 13C recovered in fruit (mg) by the phloem or pedicel cross-sectional area (mm2) during the period of 2 h 13C labelling at the same sampling date. In this case, the sink strength of fruit was defined as the specific rate of 13C accumulation in fruit (Doehlert, 1993; Farrar, 1993a).
Statistical analysis
The comparison of pairs of values was analysed by Student's t-test using Sigmaplot (Jandel Scientific, San Rafael, California) software. A probability of P >0.05 was considered non-significant.
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Results |
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Fruit growth and development
Examination of the dynamics of fruit growth showed that average fruit weight of control fruit was about 300 g while GA-treated trees had larger fruit, weighing up to 400 g (Fig. 1A). The increase in fresh weight at harvest induced by GA application mainly resulted from an increase in water content, as the increase in fruit dry weight only contributed around a 5% increase in total fresh fruit weight (Fig. 1B). On the other hand, histological analysis of fruit showed that there were no differences in cell number of the mesocarp and core size between GA-treated and control fruit (Fig. 2). However, the GA-treated fruit had a significantly larger final cell length at harvest.
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Pedicel vascularization
The vascular routes in the pedicel and fruit were constructed of 10 bundles, which were separated in the pedicel of the flower as described by Nii (1980)
(data not shown). The pedicel cross-sectional area in GA-treated fruit was significantly greater than that in untreated fruit from 28 DAT (Fig. 3F). It is obvious that there is a close correlation between fruit size and fruit pedicel cross-sectional area (Figs 1, 3F). Further anatomical analysis of the pedicel revealed that, except for the cortex cross-sectional area (Fig. 3A), the cross-sectional area of the other components of the tissue was markedly increased by GA application at harvest, but that the patterns of cross-sectional area varied with the components of the tissue (Fig. 3B–E). A marked increase in primary phloem cross-sectional area was the response to GA application from 7 DAT. However, no differences in the cross-sectional area of xylem and secondary phloem between GA-treated and untreated fruit were observed until 14 DAT. Moreover, no significant differences in pith cross-sectional area between both treatments were measured, even at 28 DAT.
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Net photosynthesis and specific rate of 13C accumulation in fruit
Net rate of photosynthesis (Pn) of mature spur leaves displayed similar patterns in both GA-treated and untreated spurs as shown in Fig. 4. There were no significant differences in Pn until 28 DAT, but GA-treated spurs showed a higher Pn than untreated ones during later growth.
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On the basis of phloem cross-sectional area, the GA-treated spurs had a greater specific rate of 13C accumulation in fruit than untreated ones at 7 DAT and 28 DAT. A similar result was obtained even if expressed on the basis of pedicel cross-sectional area (Fig. 5A, C). The increase in the rate of 13C accumulation in fruit and phloem or pedicel cross-sectional area did not bear a 1:1 relationship (Fig. 5).
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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In Japanese pear, it has been proposed that the application of GA4 at about 40 DAA could effectively increase final fruit size (Hayashi and Tanabe, 1991
). In this study, the results (Fig. 1) confirmed the above suggestion and showed that the critical factor for larger fruit size that resulted from GA application should be contributed to the enlarged cell size of the mesocarp not to cell number and core size (Fig. 2).
In many previous reports, application of exogenous plant growth regulators could affect the vascular development of the pedicel and lead to a larger fruit at harvest in many species of fruit-bearing plants (Aloni, 1987; El-Otmani et al., 1993; Guardiola et al., 1993; Jackson, 2003). Furthermore, these results showed that fruit size was tightly correlated to both phloem and xylem cross-sectional area (Fig. 3) and supported the previous suggestion that there is a close correlation between pedicel diameter and fruit size at harvest (El-Otmani et al., 1993; Guardiola et al., 1993; Bustan et al., 1995). In addition, there is considerable evidence that plant hormones (GAs, auxins) are important regulators of cambial cell division and secondary xylem and phloem differentiation, including the mediation of environmental factors that influence wood formation (Little and Savidge, 1987). In the present study, the effect of GA on pedicel vascularization (Fig. 3) supported the above suggestions and further indicated that there is a possible dependence of fruit growth on the capacity of the vascular route to the fruit and that GA is the direct trigger and regulates the induction and formation of new vascular tissue.
However, the relationship between pedicel capacity and fruit growth still remains to be clarified because of the controversial results. For example, it has been suggested that secondary thickening of the pedicel, induced by auxin treatment, might have been the reason for the bigger size of fruit, in addition to the direct effect of auxin on fruit growth in Citrus (El-Otmani et al., 1993). By contrast, some evidence has shown that assimilate transport is controlled by the sink rather than by the translocation capacity (Kallarackel and Milburn, 1984; Marcelis, 1996; Bruchou and Genard, 1999). Guardiola et al. (1993) also suspected that vascular connections limit the growth of Citrus fruit, however, they concluded that growth substance effects on fruit size were more related to metabolic changes in fruit tissues. Garcia-Luis et al. (2002) demonstrated that the lower sink strength of fruit, rather than differences in phloem cross-sectional area, was a determining factor for the reduced transport to them. The removal of a significant proportion (up to 43%) of the pedicel phloem was matched by a compensatory increase in the specific mass transfer of dry matter, but it had no effect on transport to fruit (Bustan et al., 1995; Garcia-Luis et al., 2002). These observations proved that transport in the phloem occurred at a rate markedly lower than its transport capacity. Apparently, measurement of phloem offers a general indicator of phloem flow but the increase of the specific rate of 13C accumulation and phloem cross-sectional area did not bear a strict 1:1 relationship (Fig. 5). In addition, the specific rate of 13C accumulation in fruit, based on pedicel cross-sectional area, increased after GA application while there were no differences in pedicel cross-sectional area between GA-treated fruit and the control. Therefore, the results strongly indicated that pedicel capacity was not the critical factor for the enhanced transport of photosynthates.
To understand the regulation of dry matter partitioning by the sinks, there has been substantial interest in a property of a sink, called the sink strength, that determines this regulation (Marcelis, 1996). The term sink strength can be defined as the competitive ability of an organ to receive or attract assimilates (Wareing and Patrick, 1975; Wolswinkel, 1985; Farrar, 1993b). In this study, the application of GA significantly increased the specific rate of 13C accumulation in fruit (Fig. 5) and this can be regarded as the sink strength of fruit (Farrar, 1993a; Doehlert, 1993). The result is in agreement with the statement that the movement of photosynthates into the fruit was determined by sink strength and confirmed the hypothesis that factors that increase the sink strength of fruit, such as plant growth regulators, may be expected to increase fruit size in Japanese pear (Zhang et al., 2005a).
It is generally accepted that the concentration gradient of assimilates between source and sink tissue is likely to be the primary regulator for the rate of transport and the pattern of partitioning (Ho, 1988). Moreover, hormones have been proposed for serving as mobilizers of assimilates to fruit and modulators for many of the rate-limiting components in the overall process of carbon partitioning (Kuiper, 1993; Brenner and Cheikh, 1995). Recently, it has been suggested that apoplasmic phloem unloading existed in developing apple fruit and invertase was critical for this process (Zhang et al., 2001, 2004). Studies on the activity of NAD-SDH (NAD+-dependent sorbitol dehydrogenase) and invertase in ‘Kousui’ fruit after GA application also confirmed the above suggestion (Zhang, 2005). Therefore, sink strength was established and regulated by plant growth regulators through stimulating nutrient transport and increasing phloem unloading, or acting on metabolism and compartmentalization of sucrose and sorbitol (Kuiper, 1993; Brenner and Cheikh, 1995).
During later fruit growth, enhanced leaf photosynthetic rate or strength of fruit supported the conclusion that, generally, photosynthesis and carbohydrate metabolism in source leaves respond to sink activity (Paul and Foyer, 2001). The enhanced sink activity and sink size (Fig. 1) can be attributed to an increase in the specific rate of 13C accumulation in fruit (Fig. 5) or the strength of fruit.
After GA application, therefore, it is likely that pedicel size and vascularization become adjusted to the forthcoming transport and mechanical requirements of the fruit. Greater phloem cross-sectional area will potentially enable greater mass transfer of dry matter to the more vigorously growing fruit. The mechanical strength of the woody xylem will allow the pedicels to hold the increasingly heavier fruit. This hypothesis could be supported by observations on apple, which demonstrated that the xylem formed in the pedicel after flowering is non-functional (Lang and Ryan, 1994). In addition, the xylem may not contribute directly to the transport of water and mineral elements to the fruit, since there is a net water backflow from the fruit into the xylem (Lang and Thorpe, 1989; Lang and Ryan, 1994; Goldschmidt and Koch, 1996).
In conclusion, larger fruit size at harvest resulting from GA application during the period of rapid fruit growth has been ascribed to the increase in cell size of the mesocarp, rate of carbohydrate accumulation in fruit or strength of fruit. On the other hand, GA is closely related with pedicel vascularization and the increased pedicel cross-sectional area mainly resulted from phloem and xylem cross-sectional areas after GA treatment. However, it seems that the primary action of GA is on fruit sink strength rather than through an increased phloem cross-sectional area for enhanced photoassimilate import into pear fruit.
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