14 C‐allocation of flowering and deblossomed strawberry in response to elevated ozone
2001; Wiley; Volume: 152; Issue: 3 Linguagem: Inglês
10.1046/j.0028-646x.2001.00270.x
ISSN1469-8137
Autores Tópico(s)Plant Stress Responses and Tolerance
ResumoNew PhytologistVolume 152, Issue 3 p. 455-461 Free Access 14C-allocation of flowering and deblossomed strawberry in response to elevated ozone P. D. Drogoudi, P. D. Drogoudi T. H. Huxley School of the Environment, Earth Sciences and Engineering, Imperial College of Science, Technology and Medicine, Silwood Park, Ascot, Berks SL5 7PY, UK;Search for more papers by this authorM. R. Ashmore, Corresponding Author M. R. Ashmore Present address: Department of Environmental Science, University of Bradford, West Yorkshire BD7 1DP, UK; Present address: Department of Agricultural and Environmental Science, University of Newcastle upon Tyne, NE1 7RU, UKAuthor for correspondence: M. R. Ashmore Tel: +44 (0)1274 235 695 Fax: +44 (0)1274 235 699 Email: [email protected]Search for more papers by this author P. D. Drogoudi, P. D. Drogoudi T. H. Huxley School of the Environment, Earth Sciences and Engineering, Imperial College of Science, Technology and Medicine, Silwood Park, Ascot, Berks SL5 7PY, UK;Search for more papers by this authorM. R. Ashmore, Corresponding Author M. R. Ashmore Present address: Department of Environmental Science, University of Bradford, West Yorkshire BD7 1DP, UK; Present address: Department of Agricultural and Environmental Science, University of Newcastle upon Tyne, NE1 7RU, UKAuthor for correspondence: M. R. Ashmore Tel: +44 (0)1274 235 695 Fax: +44 (0)1274 235 699 Email: [email protected]Search for more papers by this author First published: 06 April 2002 https://doi.org/10.1046/j.0028-646X.2001.00270.xCitations: 8AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Summary • A direct assessment of carbon distribution was made in fruiting and deblossomed strawberry (Fragaria × ananassa) in order to investigate the mechanisms of ozone (O3) action on fruit yield. • Fruiting and deblossomed strawberry plants were treated with 92 ppb ozone or filtered air in open-top chambers for 69 d. Either leaf 1 or leaf 3 (from the most recent fully expanded) were exposed to a 30-min 14CO2 pulse. The sink strength and relative specific uptake of sink tissues were determined after 24 h and 48 h. • Ozone did not affect the sink strength of fruits, but there was a trend to decreasing relative specific uptake of fruits when leaf 1, but not when leaf 3, was labelled. Ozone increased the sink strength of leaf blades younger than the source leaf when leaf 3 was labelled. Leaf 3, but not leaf 1, distributed assimilates mostly to the fruit. Ozone increased the sink strength of petioles in deblossomed plants. • There were important differences between source leaves of different age, both in overall carbon allocation to different sinks and the effects of ozone, which influenced the relative importance for fruit yield of effects of ozone on photosynthesis and on carbon allocation. Introduction Ozone (O3) is known to reduce fruit yield in many vegetable and fruit species (Cooley & Manning, 1987; Olszyk et al., 1990; Retzlaff et al., 1997). Photosynthesis, respiration and carbon allocation are physiological processes directly related to fruit yield. While effects of O3 on photosynthesis have been studied intensively, relatively little research has been done on the effect of ozone on carbon allocation. O3 is known to inhibit carbon export, as suggested by a build up of carbohydrates (Mulchi et al., 1992; Balaguer et al., 1995; Meyer et al., 1997) or retention of labelled assimilates in source leaves (McCool & Menge, 1983; McLaughlin & McConathy, 1983; Pausch et al., 1996; Samuelson & Kelly, 1996; Renaud et al., 1998; Grantz & Farrar, 1999). O3 has also been shown to induce changes in allocation patterns in 14C studies in bean plants (Okano et al., 1984) and forest species (Spence et al., 1990; Coleman et al., 1995). However, it is not known whether O3 alters the allocation of exported assimilates directed to the fruiting structures. In plants at a reproductive growth-stage, a direct assessment of the response of carbon allocation to O3 has been made only in bean (Phaseolus vulgaris) and rice plants. An increase in 13C-labelled assimilate allocation to the panicles, together with an increase in dry matter allocation to the panicles, was found in rice plants (Nouchi et al., 1995). In bean plants, O3 reduced the accumulation of 14C-labelled assimilates in large pods and increased leaf retention (McLaughlin & McConathy, 1983). However, whole-plant carbon allocation was measured in these studies, and it is unclear whether these allocation responses are due to altered carbon export from the source leaves, altered patterns of allocation of exported carbon to the various plant parts, a source leaf age-dependent response to ozone, or to sink changes. In an earlier paper, we showed that there are changes in the effect of O3 on partitioning priorities during the growth cycle of strawberry (Fragaria × ananassa) due to reproductive development and to the cumulative effects of O3 (Drogoudi & Ashmore, 2000). There was an acceleration in the inflorescence production at the beginning of the fumigation period that occurred before, or simultaneously with, a reduction in the relative growth rate of leaf area. This was followed by a reduction in the inflorescence numbers and fruit set, which coincided with reduced photosynthetic rate. A reduction in the individual fruit weight occurred in the later harvested fruits in particular and coincided with a cumulative effect of O3 on the photosynthetic rate. In a destructive harvest at the end of the fumigation period the above-ground, but not root, biomass was reduced in O3. Immediately before this destructive harvest, a direct assessment of the response of carbon allocation to ozone was made, which we present in this paper. The main objective of the study was to test whether this reduction in individual fruit weight was due to changes in carbon allocation. The effect of O3 on carbon allocation parameters in deblossomed strawberry was also reported in our earlier paper; removal of the fruit reduced the effect of O3 on the relative growth rate of leaf area and final biomass, but not on net photosynthetic rate (Drogoudi & Ashmore, 2000). Therefore, the study of carbon allocation reported in the current paper also considered differences between fruiting and deblossomed plants, as well as whether the effect of ozone on carbon allocation is dependent on leaf age. Coleman et al. (1995) found an age-dependent response of carbon allocation to O3 in poplar clones; O3 decreased the percentage of carbon allocated from mature leaves to roots and increased the percentage of carbon allocated to the lower stem, whereas allocation from recently matured leaves to roots increased. However, in bean plants the effect of O3 on the allocation of exported carbon did not differ when the primary or first trifoliate leaf was labelled (Okano et al., 1984). The objectives of the present study were to study the effects of O3 on the allocation of 14C-labelled assimilates in fruiting strawberry plants using leaves of different age and postlabelling periods, and to assess the effect of fruiting on the response to O3 of 14C distribution. Materials and Methods Growth and ozone fumigation conditions Strawberry (Fragaria × ananassa Duch.) crowns from the cultivar Cambridge Favourite (RW Walpole Ltd, Norfolk, UK) were planted in 7.5-l pots containing a 9 : 1 : 1 : 1 peat : perlite : sand : vermiculite compost and were grown in a glasshouse for 2 wk at a temperature of approx. 20°C. The treatments applied were air quality, which included exposure to filtered air or ozone, and fruiting level, which included fruiting and deblossomed plants. The fumigation system consisted of eight open-top chambers (OTCs) arranged in pairs, four receiving O3 and four receiving filtered air. Each chamber was 1.5 m high and 1.5 m in diameter. Ambient air was pumped through charcoal filters into each pair of chambers. O3 was distributed to four chambers, entering the air supply after the filters. Air samples were taken from the centre of all O3 fumigation chambers and one of the filtered air chambers and O3 concentration was recorded for 10-min each hour. The fumigation period lasted for 69 d (June 25–September 1, 1998), during which O3 was not applied on a total of 9 d spread over the fumigation period, due to rain or strong winds. The O3 fumigation was carried out for a mean of 7.8 ± 0.2 h (chamber mean ± SE) per day with a mean daily concentration of 92.0 ± 0.4 ppb. The accumulated exposure above a threshold concentration of 40 ppb (AOT40) was 24591 ± 305 ppb h−1. In filtered air chambers, the mean 8 h O3 concentration was 17.4 ± 0.5 ppb. Inflorescences were removed from the nonfruiting batch as soon as they appeared during the plant growth cycle. Stolons were also removed when they appeared through the whole experimental period. Further details of the growth and fumigation conditions are given in Drogoudi & Ashmore (2000). Translocation of 14C-labelled assimilates 14C assimilate labelling Translocation parameters (sink strength and relative specific uptake) were determined in the first and the third most recent fully expanded leaves (leaf 1 and 3) in fruiting and deblossomed plants, exposed to O3 and filtered air, after a 48-h postlabelling period. In fruiting plants, the effect of post labelling period (24 and 48 h) treatment was also studied, using leaf 1 as the source leaf. Plants were labelled with 14CO2 at the end of the fumigation period, on days 65, 66 and 67. Fruiting and deblossomed plants from each air quality treatment were arranged according to their leaf area, and distributed evenly between each leaf age and post labelling period treatment. There were five or six replicate plants for each of the two air quality treatments, for the two fruiting levels and for the two leaf ages. However, the effect of postlabelling period was tested only for fruiting plants and leaf 1; thus a total of 33 fruiting and 22 deblossomed plants were used. The 14CO2 fumigations took place four times a day. In each exposure, one O3 and one filtered air treated plant from a fruiting level, leaf age or post labelling period treatment was labelled, so that up to six plants were exposed at a time. Exposures with 14CO2 took place in an enclosed system consisting of a Perspex box (70 × 70 × 80 cm) inside a controlled environment chamber (Sanyo Gallenkamp, Leicestershire, UK) at 250 mmol m−2 s−1 PAR, 20°C, and 75% rh. The chamber was divided into two, using a transparent Perspex sheet. The top part of the chamber received circulated air containing 14CO2 and two fans attached to the top of the chamber provided air circulation. The bottom part of the chamber received air from the outside environment of the controlled chamber and the room (temperature 20°C), and air circulation was provided with one fan. The plant pots were placed in the bottom half of the chamber and the source trifoliate leaf, which was previously tagged, was folded and placed through a hole (7 cm2) in the horizontal middle sheeting, into the top part of the chamber and sealed with tape. Plants were acclimatized in the fumigation chamber for 2 h. 14CO2 was injected into the main air inlet in the top part of the chamber from a cylinder containing 14CO2, providing a total of 1570 KBq during a 30-min fumigation. After the 14CO2 injection was halted, air was circulated for an additional 30-min and then the chamber was vented. Two leaf disks (4.52 cm2) were taken immediately after the exposure from the source trifoliate leaf so the amount of 14C fixed could be determined, and then the plants were replaced in their previous positions in the OTCs and harvested 24 or 48-h later. Determination and calculation of translocation parameters At harvest, each plant was separated into root and two above-ground components. In deblossomed plants, the first above-ground component included the crown with leaves that contained the source leaf, and the second contained the subtended crowns with leaves. The first component was divided into crown, petioles, the source leaf, leaf blades younger than the source leaf and leaf blades older than the source leaf. The second component was divided into crowns, petioles and leaf blades. In fruiting plants, fruits with the flowers added were additionally separated from the crown that contained the source leaf and from the subtended crowns. The peduncles were summed with the petioles of the two plant components. The plant parts were freeze-dried, weighed and machine ground. Approx. 300 mg dry matter (measured to 3 decimal places) was then folded in ashless filter paper and oxidized for 1 min in an automatic sample oxidizer (Model 307; Canberra-Packard, Pangbourne, Berkshire, UK). 14CO2 was absorbed in a 20-ml scintillation cocktail (10 ml permafluor and 10 ml carbosorb) and trapped in polyethylene vials (Canberra-Packard). Standards of 5000 counts per min and blanks were also oxidized to determine the efficiency of the oxidizer. Scintillation counting was performed for 10 min using a ‘Rackbeta’ counter (model 1219 LKB, Pharmacia, UK). After the 24 or 48-h period, the 14C fixed would have been either lost to respiration, retained in the source leaf, or translocated to the various sinks. The amount of 14C recovered from each plant part was calculated as the product of tissue d. wt and specific activity. The percent 14C translocated during the chase period was calculated as the percentage of the total 14C recovered from all plant parts which was from the sink tissues. The sink strength was calculated as the percentage 14C recovered in each sink tissue as a percentage of the total translocated. Relative specific uptake (RSU) was calculated, as the percentage 14C recovered from a sink tissue divided by the percent of the total d. wt that the sink represents (excluding the source leaf contribution). It shows the capacity of a sink to take up 14C, taking into account the dry matter partitioned to that sink (Brun & Betts, 1984). The mean values of the percent 14C recovered (thus not respired) and the percentage translocated were estimated only in fruiting plants when leaf 1 was labelled. The mean value of the percent 14C recovered was calculated as the percentage of that fixed. The amount of 14C fixed was the product of the 14C activity of leaf discs taken immediately after exposure from the fed leaf (expressed per leaf area) and its leaf area. The percentage translocated, and thus not retained in the source leaf, was expressed as the percentage of the total recovered. Statistical analyses The experimental design was a randomized block design using air quality, fruiting level and age of the source leaf as treatments. In the case of fruiting plants, the effect of air quality and postlabelling period treatments when leaf 1 was labelled, and the effect of air quality and leaf age, were analysed separately. Statistical analyses were carried out using a multi factor ANOVA, based upon the replicate 14C exposures, using the Statsoft statistical package, Statistica (Statsoft, Tulsa OK, USA). Treatment means were separated using least significant difference (LSD) comparisons where ANOVA F-tests were significant, using a P-value of 0.05. Percentage data (sink strength) were arcsine transformed, and ratio data (relative specific uptake) were log-transformed, before analyses. Results Effects of air quality in fruiting plants The percentage 14C recovered and translocated were not significantly affected by O3 in fruiting plants when leaf 1 was labelled, the mean values being 65.4 ± 4.0 and 35.7 ± 3.9, respectively. The sink strength of fruit tissues was not significantly affected by O3, when analysed for leaf 1, across the 24-h and 48-h postlabelling periods, and for leaves 1 and 3, at the 48 h postlabelling period (data not shown). O3 induced only a decreasing trend (P = 0.070) in the relative specific uptake (RSU) of total fruit tissue, when calculated for leaf 1 across the 24-h and 48-h postlabelling periods (Fig. 1). RSU of total fruit tissue was not significantly affected by O3 for leaf 3 at the 48-h postlabelling period (Fig. 1). Figure 1Open in figure viewerPowerPoint Effect of ozone on relative specific uptake of fruit. Mean relative specific uptake (RSU) (%14C allocated/% dry matter) of total fruit tissue in response to 92 ppb O3 fumigation for 60 d in strawberry, when leaf 1 (from the most recent fully expanded) was the source leaf, 24 or 48 h after labelling, and when leaf 3 was the source leaf, 48 h after labelling. Values are means (± SE) of 5–6 replicate plants. Filtered air, closed columns; ozone, open columns. There was a significant interaction of air quality and chasing period on the RSU of the younger than source leaf tissue; it was greater (by 140%) in O3 compared with filtered air treated plants only at the 24 h chasing period (Fig. 2a). The sink strength of the younger than source leaf tissue was also significantly greater, by 215%, in O3 for leaf 3 at the 48 h chasing period (Fig. 2b). Figure 2Open in figure viewerPowerPoint Effects of ozone on sink strength and relative specific uptake of young leaves in fruiting plants. (a) Relative specific uptake (RSU) (%14C allocated/% dry matter), and (b) sink strength (%14C allocated), of the above source leaf tissue when leaf 1 (from the most recent fully expanded leaf) was the source leaf, 24 or 48 h after labelling, and when leaf 3 was the source leaf 48 h after labelling, in response to 92 ppb O3 fumigation for 60 d in fruiting strawberry plants. Values are means (± SE) of 5–6 replicate plants. Filtered air, closed columns; ozone, open columns. There was only one significant interaction between air quality and leaf age on the sink strength or RSU of the separated and total plant parts. The sink strength of the crowns, excluding the one containing the source leaf, showed a significant interaction between air quality and leaf age, at the 48-h chasing period. When leaf 1, but not leaf 3, was labelled it was greater in O3 (1.028 ± 0.373) compared with the filtered air (0.426 ± 0.085) treatment; however, this accounted for only a small proportion of the total exported carbon. Effects of air quality in fruiting and deblossomed plants There was no significant overall effect of air quality on the sink strength or RSU of total plant parts when analysed for fruiting and deblossomed plants (Table 1). Table 1. P-values for the effects of air quality (O3 and filtered air), fruiting level (fruiting and deblossomed) and leaf age (leaf 1 and 3) and their interactions, on the sink strength (%14C allocated within the plant), and relative specific uptake (%14C allocated within the plant/% dry matter) of total plant parts 48-h after labelling Parameter Plant part AQ1 Fruit2 Age3 AQ × fruit AQ × age Fruit × age AQ × fruit × age Sink strength Root 0.836 0.003 0.107 0.099 0.533 0.029 0.803 Crown 0.464 < 0.001 0.123 0.332 0.217 0.451 0.738 Petiole 0.374 0.001 0.012 0.041 0.758 0.265 0.606 Leaf 0.518 < 0.001 < 0.001 0.550 0.595 0.054 0.116 Fruit 0.497 – 0.004 – 0.917 – – RSU Root 0.664 0.160 0.185 0.190 0.611 0.012 0.585 Crown 0.810 0.002 0.250 0.202 0.244 0.408 0.868 Petiole 0.796 < 0.001 0.041 0.089 0.420 0.305 0.361 Leaf 0.414 < 0.001 < 0.001 0.372 0.305 0.029 0.040 Fruit 0.278 – 0.002 – 0.307 – – 1 AQ, air quality treatments (filtered air and ozone fumigation); 2 2 Fruit, fruiting and deblossomed plants; 3 3 Age, age of the source leaf (leaf 1 and 3). RSU, relative specific uptake. There was a significant interaction between air quality and fruiting presence in the sink strength of total petiole tissue; it increased by 31%, across the two leaf age source leaves, in response to ozone, only in deblossomed plants (Table 1; Fig. 3). In deblossomed plants, the sink strength of the petioles of the crown containing the source leaf was also significantly greater in O3 compared with filtered air treated plants (data not shown). Figure 3Open in figure viewerPowerPoint Effects of ozone on sink strengths of all plant parts in fruiting and deblossomed plants. Sink strength (%14C allocated) of total plant parts in (a) fruiting, and (b) deblossomed strawberry plants, when leaf 1 or leaf 3 were the source leaves, 48 h after labelling, in response to 92 ppb O3 fumigation for 60 d. Values are means (± SE) of 5–6 replicate plants. Leaf 1 (CF), open columns; leaf 1 (O3), cross hatched columns; leaf 3 (CF), hatched columns; leaf 3 (O3), closed columns. Air quality, fruiting level and leaf age showed a significant interaction term on the RSU of total leaf tissue (Table 1). This was attributed to a significant interaction between air quality and leaf age in deblossomed, but not in fruiting plants; RSU was similar in the two ages of source leaves in filtered air, but it was greater for leaf 1 compared with leaf 3 in the O3 treatment (data not shown). Effects of leaf age and fruiting level treatments In fruiting plants, the sink strength (Fig. 3a) and RSU (Fig. 1) of total fruit tissue were significantly greater across the two air quality treatments when leaf 3 was the source leaf compared with leaf 1 (Table 1). There was a significant interaction between fruiting level and leaf age in the sink strength and RSU of root tissue (Table 1). In fruiting plants, the sink strength (Fig. 3) and RSU (data not shown) of roots were similar when leaf 1 and 3 were labelled, whereas in deblossomed plants, they were greater when leaf 3 was labelled. Also, there was an almost significant interaction between fruiting level and age of the source leaf on the sink strength (P = 0.054) (Fig. 3) and RSU (data not shown) of total leaf blade tissue (Table 1). They were greater when leaf 1, compared with leaf 3, was labelled in both fruiting and deblossomed plants, but the increase was greater in fruiting plants. Discussion The impairment of processes associated with phloem loading is often an early symptom of O3 toxicity (Balaguer et al., 1995; Renaud et al., 1998), which has been shown to precede (soybean, Pausch et al., 1996; spring wheat; Meyer et al., 1997; pima cotton, Grantz & Farrar, 1999) or not (loblolly pine, Spence et al., 1990) any O3 effect on net photosynthesis. O3 may also have a differential effect on carbon retention depending on the age of source leaf. For example, carbon retention increased in fully mature leaves of aspen clones (Coleman et al., 1995) and bean plants (Okano et al., 1984), whereas in recently mature leaves it was not affected in aspen clones and decreased in bean plants. In the present study, there was no significant effect of O3 on the percent of 14C retained in leaf 1, and there was no substantial decrease in net photosynthetic rate in leaf 1, as reported by Drogoudi & Ashmore (2000). Negative effects on yield parameters such as the number of inflorescences, fruit set and individual fruit weight were found in this experiment in the O3 treated plants (Drogoudi & Ashmore, 2000). The decrease in individual fruit weight occurred particularly during the harvest of the later fruits, which coincided with the 14C-labelling study. In order to elucidate the mechanism inducing the decrease in individual fruit weight, a comparison can be made between the effects of O3 on net photosynthetic rate, as reported by Drogoudi & Ashmore (2000), and distribution pattern of assimilates, as reported in this paper, in leaves differing in age. Ozone did not significantly affect the percentage allocation to total fruits, while there was only a decreasing trend in the relative specific uptake of total fruit when leaf 1, but not when leaf 3, was labelled. Furthermore, a greater proportion of assimilates were distributed to the fruiting structures from leaf 3 than leaf 1. Since the ozone-induced reduction in the photosynthetic rate was more pronounced in leaf 3 than leaf 1, it appears that the decrease in individual fruit yield resulted primarily from changes in the net photosynthetic rate, rather than carbon allocation. In the present study, strawberry exhibited an adaptive response to an O3-induced decrease in the photosynthetic rate in the source leaves, by increasing the proportion of assimilates sent to the younger leaves for repair purposes or growth. The 14C assimilate concentration (RSU) of the leaves younger than the source leaf (leaf 1) was significantly greater at the 24 h, but not 48 h, post labelling period, suggesting that assimilates were distributed earlier to the young leaves in ozone treated plants. In addition, a greater sink strength in the leaves younger than source leaf 3 was found. Similarly, after an acute O3 exposure (200 ppb O3 for 4 d, 24 h d−1) Okano et al. (1984) found that the assimilate distribution of 14C from the primary or trifoliate leaves favoured the newly expanding leaves in bean plants. However in loblolly pine seedlings (Spence et al., 1990) and aspen clones (Coleman et al., 1995), allocation of 13C or 14C was not altered towards the upper shoot by O3. Although there was no substantial effect of O3 on the allocation of 14C to the fruiting structures at this time of fruit expansion, O3 could have influenced translocation patterns earlier in the developmental process. For example, Drogoudi & Ashmore (2000) found that O3 exposure favoured inflorescence production at an earlier growth stage. Thus, further 14C label studies are required at earlier developmental stages to obtain a full picture of O3 impacts on carbon allocation to the fruit and to new leaf production. Whether O3 induced any re-distribution of stored carbon to the fruiting structures has not been investigated in the present, or in any other previous, study. This would be unlikely to have contributed to fruit or leaf growth in the present study since a reduction in vegetative growth had already occurred in O3 treated plants. By contrast to fruiting plants, O3 increased the 14C concentration in the petioles of the crown containing the source leaf in deblossomed plants. Accumulation of labelled assimilates or starch in petioles or stems has been reported in other studies in response to O3 (ladino clover, Blum et al., 1983; loblolly pine trees, Spence et al., 1990, Northern red oak mature trees; Samuelson & Kelly, 1996). Assimilate accumulation in stems is commonly reported as a result of other stresses like shade, which reduces the source activities (Waring & Schlesinger, 1985). A carbohydrate accumulation in petioles of other species has been shown, which may be transient and connected with alternating source and sink activities (Oparka & Davies, 1985; Keller & Matile, 1989; Davis & Loescher, 1991). Minchin et al. (1993) used a model to show that a reduced amount of exported assimilates is expected to reach the adjacent sinks (e.g. petioles), at the expense of distant sinks (e.g. roots). However, the O3-induced reduction in the photosynthetic rate was similar between fruiting and deblossomed plants. Fruit removal may induce a reduction in the mass transfer rate in the sieve elements due to the absence of fruit producing phytohormones to attract assimilates (Patrick & Waring, 1981). Thus the lower carbon transport rate in the sieve elements of deblossomed plants, in addition to a lower amount of assimilates transported due to O3, may be responsible for the preferential carbon accumulation in petioles in deblossomed but not in fruiting plants. Coleman et al. (1995) reported that O3 increased the assimilate allocation to the stems, at the expense of the root, and substantially decreased the amount of exported carbon (due to both a decrease in the photosynthetic rate and increased carbon retention) in the mature leaf of aspen clones. In the present study, O3 similarly increased carbon allocation to the petioles in deblossomed plants, which did not coincide with a significant decrease in the proportional allocation of assimilates to the root. Since the reduction in photosynthetic rate caused by O3 was more pronounced in older leaves, which in deblossomed plants directed assimilates mostly to the root, and in fruiting plants to the fruits, these are the plant parts to which carbon export would be most affected by ozone. In conclusion, the effects of O3 on fruit yield appeared to be related more to a reduction in the photosynthetic rate, rather than to any specific effect of O3 on carbon allocation. O3 increased the allocation of exported 14C-labelled carbon to younger leaves, which may be a compensating response for O3 induced leaf damage. Removal of the flowers changed the response of carbon allocation to O3; in deblossomed, but not fruiting, plants the exported 14C-labelled carbon was accumulated to the petioles. There were important differences between source leaves of different age, both in overall carbon allocation patterns to different sinks, and in the effects of O3. Future mechanistic studies of ozone impacts on fruit production in strawberry and in other species need to consider in more detail the cumulative effects on both photosynthetic rate and carbon allocation in leaves of different age. Acknowledgements This study was supported by a postgraduate research fellowship from the Greek State Scholarship Foundation. References Balaguer L, Barnes JD, Panicucci A, Borland AM. 1995. Production and utilization of assimilates in wheat (Triticum aestivum L.) leaves exposed to elevated O3 and/or CO2. New Phytologist 152: 557– 568. Blum U, Mrozek E, Johnson E. 1983. Investigation of ozone effects on 14C distribution in ladino clover. Environmental and Experimental Botany 23: 369– 378. Brun WA, Betts KJ. 1984. Source/sink relations of abscising and non-abscising soybean flowers. Plant Physiology 75: 187– 191. Coleman MD, Dickson RE, Isebrands JG, Karnosky DF. 1995. Carbon allocation and partitioning in aspen clones varying in sensitivity to tropospheric ozone. Tree Physiology 15: 593– 604. Cooley DR, Manning WJ. 1987. The impact of ozone on assimilate partitioning in plants: a review. Environmental Pollution 47: 95– 113. Davis JM, Loescher WH. 1991. Diurnal pattern of carbohydrates in celery leaves of various ages. Hortscience 26: 1404– 1406. Drogoudi PD, Ashmore MR. 2000. Does elevated ozone have differing effects in flowering and deblossomed strawberry? New Phytologist 147: 561– 569. Grantz DA, Farrar JF. 1999. Acute exposure to ozone inhibits rapid carbon translocation from source leaves of Pima cotton. Journal of Experimental Botany 50: 1253– 1262. Keller F, Matile P. 1989. Storage of sugars and manitol in petioles of celery leaves. New Phytologist 113: 291– 299. McCool PM, Menge JA. 1983. Influence of ozone on carbon partitioning in tomato: Potential role of carbon flow in regulation of the mycorrhizal symbiosis under conditions of stress. New Phytologist 94: 241– 247. McLaughlin SB, McConathy RK. 1983. Effects of SO2 and O3 on allocation of 14C-labelled photosynthate in Phaseolus vulgaris. Plant Physiology 73: 630– 635. Meyer U, Kollner B, Willenbrink J, Krause GHM. 1997. Physiological changes in agricultural crops induced by different ambient ozone exposure regimes I. Effects on photosynthesis and assimilate allocation in spring wheat. New Phytologist 136: 645– 652. Minchin PEH, Thorpe MR, Farrar JF. 1993. A simple mechanistic model of phloem transport which explains sink priority. Journal of Experimental Botany 44: 947– 955. Mulchi CL, Slaughter L, Saleem M, Lee EH, Pausch R, Rowland R. 1992. Growth and physiological characteristics of soybean in open-top chambers in response to ozone and increased atmospheric CO2. Agriculture, Ecosystem and Environment 38: 107– 118. Nouchi I, Ito O, Harazono Y, Kouchi H. 1995. Acceleration of 13C-labelled photosynthate partitioning from leaves to panicles in rice plants exposed to chronic ozone at the reproductive stage. Environmental Pollution 88: 253– 260. Okano K, Ito O, Takeba G, Shimizu A, Totsuka T. 1984. Alteration of C13-assimilate partitioning in plants of Phaseolus vulgaris exposed to ozone. New Phytologist 97: 155– 163. Olszyk DM, Kats G, Morrison CL, Dawson PJ, Gocka I, Wolf J, Thompson CR. 1990. ‘Valencia’ orange fruit yield with ambient oxidant or sulphur dioxide exposures. Journal of the American Society for Horticultural Sciences 115: 878– 883. Oparka KJ, Davies HV. 1985. Translocation of assimilates within and between potato stems. Annals of Botany 56: 45– 54. Patrick JW, Waring PF. 1981. Hormonal control of assimilate movement and distribution. In: B Jeffcoat, ed. Aspects and prospects of plant growth regulators, Proceedings Joint Symposium of British Crop Protection Council and British Plant Growth Regulator Group. Wantage, UK: Dutch Committee for Plant Growth Regulators and British Plant Growth Regulator Group, 65– 84. Pausch RC, Mulchi CL, Lee EH, Forseth IN, Slaughter LH. 1996. Use of 13C and 14N isotopes to investigate O3 effects on C and N metabolism in soybean. Part I. C fixation and translocation. Agriculture, Ecosystem and Environment 59: 69– 80. Renaud JP, Laitat E, Mauffette Y, Allard G. 1998. Photoassimilate allocation and photosynthetic and biochemical characteristics of two alfalfa (Medicago sativa) cultivars of different ozone sensitivities. Canadian Journal of Botany 76: 281– 289. Retzlaff WA, Williams LE, DeJong TM. 1997. Growth and yield response of commercial bearing-age ‘Casselman’ plum trees to various ozone partial pressures. Journal of Environmental Quality 26: 858– 865. Samuelson LJ, Kelly JM. 1996. Carbon partitioning and allocation in northern red oak seedlings and mature trees in response to ozone. Tree Physiology 16: 853– 858. Spence RD, Rykiel EJ, JrSharpe PJH. 1990. Ozone alters carbon allocation in Loblolly pine: Assessment with carbon-11 labelling. Environmental Pollution 64: 93– 106. Waring RH, Schlesinger WH. 1985. Forest ecosystems: concepts and management. Orlando, FL, USA: Academic Press. Citing Literature Volume152, Issue3December 2001Pages 455-461 FiguresReferencesRelatedInformation
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