Fruit Attached on the Vine
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1 J. Japan. Soc. Hort. Sci. 59 (4) : Relationships between Growth in Volume and Respiration of Cucumber Fruit Attached on the Vine Akio Tazuke * and Ryozo Sakiyama Faculty of Agriculture, Universityof Tokyo, Bunkyo-ku, Tokyo 113 Summary Studies on the relationships between growth rate in volume and respiration rate of cucumber fruits attached on the vine were begun when they were about 9 cm in length. As fruits grew, those held in individual constant temperature chamber in which the temperature was maintained between 10 to 35 C showed a decrease in respiration rate per fruit volume (RIV) without exhibiting an apparent diurnal fluctuation. The R/V for the first day increased linearly as the fruit temperature became higher. Daily mean values of R/V for the whole measurement period were linear to the relative growth rate (RGR) in volume with the same regression line irrespective of fruit temperature (r=0.95). The intercept of R/V at RGR = 0 was comparataively small. The amount of respired CO2 (AR) from fruit, which varied at different temperatures and age of fruit, was proportional to the increment of fruit volume which occurred during the same period (AV), with a regression equation having a proportionality constant of 13.2 mg CO2 cm-3 irrespective of fruit temperature (R2=0.95). Overall conversion efficiency estimated using the proportionality constant obtained above was 86% and it was influenced little by fruit temperature. The proportionality between 0 R and A V indicated that the respiration rate of fruit can be used to monitor nondestructively the fruit growth in dry weight. Consequently, in modeling fruit growth of cucumber, separation of fruit respiration into growth and maintenance components is practically unnecessary. There was no difference in the relationship between growth in volume and respiration in two cucumber cultivars, i. e., AR/AV was nearly constant. Introduction Respiration rate of plant organs reflects physiological activity. It is traditional to separate respiration rate into two components relating growth and maintenance processes (7). This concept was given a biochemical basis by the work of Penning de Vries (8, 9). In fleshy fruit, 85-95% of the fresh weight is occupied by water (4). Water influx as related to cell expansion processes is a feature of growth of those fruits. Thus, growth of fruit may be characterized by the increase in volume rather than that in dry weight. There are some studies on the rela- Received for publication April 10, *present address: College of Agriculture, University Osaka Prefecture, Sakai, Osaka 591. of tionship between growth and respiration in fleshy fruit (5, 6,19). But they are mainly concerned with growth in dry matter. Growth in volume of cucumber fruit is very rapid and exponential at the younger stage (14). Relative growth rate in volume changes depending largely on the fruit conditions, especially fruit temperature (15). We investigated in this report how this rapid growth in volume is related to respiration. Materials 1. Growth condition and Methods In the spring of 1984, cucumber plants (Cucumis sativus L.) of `Tokiwa Hikari 3 Go A Gata' and `Kurume Ochiai H Gata' were grown in a glasshouse. Both cultivars were grafted onto figleaf 745
2 746 A. TAZUKE AND R. SAKIYAMA gourd stocks (Cucurbita ficifolia Bouche). Two rows were planted 50 cm apart on the bed, with 50 cm between plants. Basal fertilizer was applied to the soil at a recommended rate. After planting, liquid fertilizer was applied at intervals of about 2 weeks. All lateral shoots were removed. The height of a plant was kept at about 2 m from the bed by adjusting a hanging hook to an upper node as the plant grew. Plants were irrigated every morning. Female flowers were usually openpollinated, otherwise hand-pollinated. 2. Temperature control of fruit Fruits about 9 cm in length were used. In order to exclude competition between a treated fruit and the adjacent ones, fruits and female flowers on two upper and lower nodes were removed. Each fruit, attached on the vine, was put into a double-layered cylindrical chamber (6 cm in internal diameter, 12 cm in external diameter, and 30 cm in length) made of acrylic resin. The chamber was insulated with polyurethane foam resin and covered with aluminum foil to keep out incident light. The opening of the fruit chamber was sealed with a rubber cap. The cap had a small hole at its center and a radial cut from the center to the margin, so that the peduncle of the attached fruit could be held through the hole. The small space between peduncle and rubber cap was sealed carefully with plastic resin so as not to damage the peduncle. The chambers were maintained at 10, 15, 20, 25, 30 and 35 C for `Tokiwa Hikari 3 Go A Gata' and 15, 20, 25 and 30 C for `Kurume Ochiai H Gata' by circulating temperature-controlled water between the double walls of the acrylic chamber. The temperature near the fruit surface in the chamber, monitored by a thermocouple and recorded continuously, was kept within 1 C from the set temperature. A treatment without temperature regulation was also included as a control. 3. Respiration rate of fruit Respiration rate of fruit was measured by an open system using IRGA (Shimazu-Seisakusho). Air was passed through soda lime to remove CO2, and through a humidifier to saturate it with water vapor at room temperature. Then the air was led into the fruit chamber at a constant flow rate of 2.00 liter min-1 controlled by a thermal mass flow controller (Ueshima-Brooks). The air of the chamber was drawn at a rate of about 1 liter min-1 and dehumidified for the measurement of CO2 concentration. Eight channels provided with a fruit chamber for each and one channel without a chamber were prepared. Each channel was selected consecutively at an interval of 5 min by means of a rotary solenoid switch. A series of the measurement was cycled once an hour. 4. Estimation of fruit volume Volume of each fruit was estimated nondestructively twice a day. At first, "fruit volume index (FVI)" was computed by FVI = l x (a12 + a22 + a32) x 10-6 where l (mm) is fruit length and al, a2 and a3 (mm) are the girths at three positions. Then volume (V) (cm3) of the fruit was calculated as follows (14). V=22.61 x FVI The, standard deviation of V was computed to be 3%. Fresh weight and dry weight were also estimated from FVI with standard deviations of 3 % and 0.23 g, respectively (14). A preliminary experiment showed that frequent measurement of fruit volume appeared to disturb the physiological state of the fruit. So we calculated the volume of fruit at hourly intervals using the two measured values of a day, on the assumption that growth of a younger cucumber fruit was exponential during this period as shown in the previous paper (14). The measurement of growth and respiration of fruit continued until the fruit elongated to about 20 cm. Results 1. Changes in respiration rate of fruit and the growth in volume 1) Respiration of fruits without regulation of temperature.' The temperature inside a fruit chamber changed diurnally, depending on the room temperature with a lag of 1 to 2 hr. Respiration rate of fruit (R) was high during the day and low at night, and increased as the fruit grew. R showed a small decline immediately after measurement of the girth, although it recovered within 1 to 2 hr (Fig. la). Respiration rate on the basis of fruit volume
3 GROWTH IN VOLUME AND RESPIRATION OF CUCUMBER FRUIT 747 (R/V) was high during the day, low at night and gradually decreased as the fruit grew (Fig. ib). R/V had a smaller variation among the fruits than R did. 2) Respiration of fruit at constant temperatures. Since there was no difference in the respiration rate between the two cultivars, data of both cultivars were pooled and analyzed. R increased linearly as the fruit grew at any Fig. 1. Changes in fruit respiration rate of cucumber `Kurume Ochiai H Gata' grown in a glasshouse in spring without control of temperature. (a) Respiration rate (R). (b) Respiration rate on the basis of fruit volume (R/V). Arrows indicate the time when fruit volume was measured. temperature and tended to be higher at higher temperatures (Fig. 2a). R showed a temporal decline after handling fruits in the measurement of the girth. Such a decline was also observed on fruits which were held without temperature regulation. Variation among fruits was smaller in R/V than in R. R/V of fruit at a higher temperature decreased steadily at a higher rate for two days (Fig. 2b). On the first day when the size of fruit was smaller and was not yet affected remarkably by temperature treatments, R/V showed a linear relationship with fruit temperature (r = 0.93, Fig.3). Arrhenius plot of R/V could be fitted well to a linear line between 15 to 30 C (r=0.91) (data not shown). QIo of R/V calculated from the slope of the line was about Relationships between respiration of fruit and the growth in volume The amount of CO2 respired (AR) (mg C02) from fruit and the increment in fruit volume (AV) (cm3) between two consecutive measurements of fruit girth were calculated for fruits at different temperatures (Fig. 4). The regression line of 0 R against A V was expressed as follows, irrespective of fruit temperature. OR=12.4AV+21.9 (r=0.98) eq.1 Taking into account of the range of L R of this experiment, the intercept of this line was so small Fig. 2. Changes in fruit respiration rate of cucumber `Kurume Ochiai H Gata' grown in a glasshouse in spring. Fruits were held at a temperature of 15 ( ), 20 (0), 25 ( ) and 30 C (o). (a) Respiration rate (R). (b) Respiration rate on the basis of fruit volume (R/V). Arrows indicate the time when fruit volume was measured. Fig. 3. Relationships between fruit temperature and daily mean respiration rate on the basis of fruit volume (R/V) in cucumber fruit on the first day of temperature treatment.
4 748 A. TAZUKE AND R. SAKIYAMA that A R could be regarded as proportional to AV. Then eq. 1 was approximated by A R =13.2 A V (R2=0.95)) eq. 2 Daily mean values of R/V and those of RGR in volume were linearly correlated irrespective of fruit temperature (r = 0.95, Fig. 5). A regression line of R/V against RGR gave a small intercept of 0.9 g CO2min -1. cm - 3 at RGR =0. However, when data were analyzed for each experimental temperature, correlation coefficients between R V and RGR became lower. The intercepts of regression lines at RGR = 0 tended to be relatively small, but showed no consistent change with temperature (data not shown). 3. Change in R/V computed using V estimated from R By using eq. 2 on fruits which were kept untouched for two days at 30 C, A V per hr was estimated consecutively from the measurements of AR. V at a given time was V at the start of the measurement of respiration plus the sum of hourly AVs which were estimated subsequently from the respiration rate. These data were used to derive R/V (Fig. 6). The patterns of change in R/V were similar to those shown in Fig. 2. This indicate that the decline of R/V with the growth of fruit was not ascribed to putative physiological disturbance as a result of fruit handling during its girth measurement. Discussion R/V of cucumber fruit was highest at the younger stage and declined as the fruits grew. Similar results were reported for fruits of tomato (19), pea (5) and cotton (17). RAT was linearly related to fruit temperature over the range of 10 to 35 C, and Q10 was about 2. These results agreed with those reported for pea fruit (6). A R was found to be proportional to AV, irrespective of fruit temperature, fruit age, weather conditions or cultivar. AV was regarded approximately proportional to the increment in dry weight (A DW), as fruit volume showed an almost proportional relationship with the dry weight (r = 0.99) in the previous paper (14). Consequently 0 R is approximately proportional to A DW which indicates that the most part of respiration is related to growth. This will be useful information when mak- Fig. 4. Relationships between the increment in volume (AV) and the amount of C02 respired (AR) in cucumber fruit. Fruits were held at a temperature of 10 (4), 15 ( ), 20 (o), 25 ( ), 30 (o) and 35 C (x). Fig. 5. tion fruit. 20 Relationships between mean daily RGR and respirain cucumber rate on the basis of fruit volume (R/V) Fruits were held at a temperature of 10 (0), 15 ( ), (o), 25 (s), 30 (o) and 35 C (x). Fig. 6. Changes in respiration rate on the basis of fruit volume (RN) computed using fruit volume estimated from respiration rate of fruits of cucumber `Tokiwa Hikari 3 Go A Gata'. Fruits were held at 30 C. Each line indicates the value of a single fruit.
5 GROWTH IN VOLUME AND RESPIRATION OF CUCUMBER FRUIT 749 ing a model of fruit growth of cucumber in relation to respiratory activity. Percent dry matter of cucumber fruit was about 5% and specific gravity of a fruit was about 1(14). Analysis of `Asomidori' cucumber fruit revealed that the carbon content on a dry matter basis was 45%. Thus the increment in volume by 1 cm3 corresponds to 50 mg of carbohydrate, which is equivalent to 82.5 mg of C02, as calculated by 50 mg x 0.45 x C02/C. The amount of CO2 respired for the increment of volume is about 13 mg (eq. 2). Thus, overall conversion efficiency (Y), i.e., the percentage of carbon accumulated as dry matter in that incorporated into fruit, is computed as 82.5/( ) = 86%. This estimate is comparable to the value observed for tomato fruit (19), but is much higher than values reported for vegetative organs in which about half of the translocated carbon was respired (1, 2, 3,11,18). Thornley (16) pointed out that organs growing at higher RGR have higher values of Y. The value of Y in our experiment was not significantly affected by temperature. Therefore, higher fruit temperature may be profitable for fruit production, in that fruit can be harvested earlier without a decrease in conversion efficiency. However, the effect of temperature on fruit quality still needs to be studied. An intercept of a line of respiration rate on a dry weight basis plotted against RGR on the same basis gives an estimation of maintenance coefficient (m). In our experiment, the relationship between RAT and RGR revealed a relatively small intercept at RGR = 0 (Fig. 5). Taking into account of the fact that volume of fruit was almost proportional to dry weight at the younger stage of cucumber fruit (14), the small intercept at RGR = 0 could mean a small value of m. Our m value is much smaller than that reported elsewhere for cucumber fruit (10). However, further studies will be needed to get a more accurate estimate of m because a) in our experiment, m seems to be temperatureindependent contrary to other reports (10,19); and b) separation of maintenance from growth respiration rates is reported to be difficult for those organs which grow exponentially, e.g., at a constant RGR (7), as was approximately the case with young cucumber fruit. To overcome these problems, it may be useful to disturb the exponential feature of fruit growth at a constant temperature, e.g., by treating fruit so that the influx rate of carbon can be restricted. Accurate determination of maintenance respiration may give a reasonable explanation for the almost proportional relationship between A R and A DW. There are at least two cases which give rise to such a relation; one is when maintenance respiration occupies a very small part of the whole respiraiton rate, and another is when maintenance respiration is, even if not small, proportional to growth respiration. A high correlation between A R and A DW provides us with a method by which the growth rate of cucumber fruit can be estimated nondestructively from the measurement of respiration rate. Furthermore, this method will be useful for diminishing variations among test fruits because measurements are continually made on the same fruit. A comparable approach was used to estimate increases in dry matter by soy bean pods by calculating their respiration rates (12,13) Literature Cited Farrar, J. F The pattern of respiration rate in vegetative barley plant. Ann. Bot. 46: Farrar, J. F Respiration rate of barley roots: Its relation to growth, substrate supply and the illumination of the shoot. Ann. Bot. 48 : Gordon, A. J., G. J. A. Ryle, C. E. Powell and D. Mitchell Export, mobilization, and respiration of assimilates in uniculum barley during light and darkness. J. Exp. Bot. 31: Ho, L. C Control of import into tomato fruits. Ber..Deu. Bot. Ges. 93 : Hole, C. C. and A. Barnes Maintenance and growth components of carbon dioxide efflux from growing pea fruits. Ann. Bot. 45 : Hole, C. C. and P. A. Scott Pea fruit extention rate. II. Effect of temperature on the relationship with respiration. J. Exp. Bot. 35 : Lambers, H Respiration in intact plants and tissues: Its regulaiton and dependence on environmental factors, metabolism and invaded organisms. p In: R. Douce and D. A. Day (eds.). Encyclopedia of plant physiology. New series. Vol. 18. Springer, Berlin. Penning de Vries, F. W. T Use of assimilates in higher plants. p In: J. P. Cooper (ed.). Photosynthesis and productivity in different environments. Cambridge University Press, London. Penning de Vries, F. W. T The cost of maintenance processes in plant cells. Ann. Bot.
6 750 A. TAZUKE AND R. SAKIYAMA : Schapendonk, A. H. C. M. and H. Challa Assimilate requirements for growth and maintenance of the cucumber fruit. Acta Hortic. 118: Shishido, Y., H. Challa and J. Krupa Effect of temperature and light on the carbon budget of young cucumber plants studied by steady-state feeding with 14CO2. J. Exp. Bot. 38: Spaeth, S. C. and T. R. Sinclair Carbon exchange rate of intact individual soya bean pods. 1. Response to step changes in light and temperature. Ann. Bot. 51: Spaeth, S. C. and T. R. Sinclair Carbon exchange rate of intact individual soya bean pods. 2. Ontogeny of temperature sensitivity. Ann. Bot. 51: Tazuke, A. and R. Sakiyama Growth analysis of cucumber fruits on vine by use of the dimensions of fruit shape. J. Japan. Soc. Hort. Sci. 53 : (In Japanese with English summary). 15. Tazuke, A. and R. Sakiyama Effect of fruit temperature on the growth of cucumber fruits. J. Japan. Soc. Hort. Sci. 55: Thornley, J. H. M Mathematical models in plant physiology. p Academic Press, London. 17. Thornley, J. H. M. and J. D. Hesketh Growth and respiration in cotton balls. J. Appl. Ecol. 9 : Verkleij, F. N. and H. Challa Diurnal export and carbon economy in an expanding source leaf of cucumber at contrasting source and sink temperature. Physiol. Plant. 74 : Walker, A. J. and J. H. M. Thornley The tomato fruit: Import, growth, respiration and carbon metabolism at different fruit sizes and temperatures. Ann. Bot. 41:
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