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Fruit weight is related to ovary weight in olive (Olea europaea L.)
Scientia Horticulturae 122 (2009) 399–403
Contents lists available at ScienceDirect
Scientia Horticulturae journal homepage: www.elsevier.com/locate/scihorti
Fruit weight is related to ovary weight in olive (Olea europaea L.) Adolfo Rosati *, Marija Zipanc´icˇ, Silvia Caporali, Giuseppe Padula CRA – OLI, via Nursina 2, 06049 Spoleto (PG), Italy
A R T I C L E I N F O
A B S T R A C T
Article history: Received 23 March 2009 Received in revised form 14 May 2009 Accepted 16 May 2009
Fruit size is an important parameter both for scientific understanding and for commercial purposes. In many species, mature fruit size is often related to floral ovary size, but no literature exists in olive that demonstrates such a relationship. Previous work suggests that olive cultivars with different fruit sizes have similar cell number and size in the ovary transectional area, but ovary and fruit dry weight was not measured. In the present study, ovary dry weight and fruit dry weight during the whole fruit development season until harvest were measured in olive cultivars with different fruit size, over three years. Flower dry weight was also measured. Fruit weight at harvest was strongly correlated to ovary weight at bloom, both in single-year data and when data from three years were pooled. Flower dry weight, excluding the ovary, was also correlated to ovary dry weight. Ovary dry weight was strongly correlated not only to the fruit dry weight at maturity, but also at any date during fruit development. The mature fruit/ovary dry weight ratio ranged between 1000 and 4000 among cultivars, but was not correlated to the fruit dry weight at maturity. These results suggest that, in olive, fruit weight is genetically controlled through the ovary weight at bloom. This knowledge may have implications in the understanding of fruit set and source-sink relationships in olive. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Ovary Fruit Flower Size Weight Olea europaea Genetic control
1. Introduction Fruit size is a very important parameter both for scientific understanding and for commercial purposes. Much research has been carried out in several species to understand the mechanisms that control fruit size (Westwood and Blaney, 1963; Scorza et al., 1991; Grossman and DeJong, 1995; Famiani et al., 2000; Nesbitt and Tanksley, 2001; Jackson, 2003; Zhang et al., 2005a,b). Fruit size is determined by the interaction of the environmental factors with the genetically determined growth potential of the fruits. Among these factors photosynthate availability, which depends on the source-sink balance, is very important. The interaction between genetic growth potential and source-sink relationship has been widely studied and implemented in growth models, such as the ‘‘Peach’’ model (Grossman and DeJong, 1994). Fruit size is determined by cell number and size (McPherson et al., 2001). Fruits from early opening flowers are larger at harvest than those from later blooms in several species such as apple (Marguery and Sangwan, 1993), persimmon (Hasegawa and Nakajima, 1990), citrus (Praloran et al., 1981), peach (Scorza et al., 1991), grape (Coombe, 1973), and strawberry (Cheng and Breen, 1992). In kiwifruit, early flowers had larger ovaries than late flowers on the same vine, and produced larger fruits with a higher cell number in the outer pericarp than fruits from late flowers,
* Corresponding author. Tel.: +39 0743 49743; fax: +39 0743 43634. E-mail addresses: [email protected], [email protected] (A. Rosati). 0304-4238/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.scienta.2009.05.034
while cell size was the same (Lai et al., 1990; Lawes et al., 1990; Cruz-Castillo et al., 1991). The high number of cells was already found in the ovary tissues of early flowers. Similarly, peach cultivars with larger fruits had fruits with more cells than in fruits from small-fruited cultivars, and this difference appeared early in the growth of the ovary (Scorza et al., 1991). In strawberry, cultivars with larger/heavier flowers had bigger fruits (Handley and Dill, 2003). These findings suggest that final fruit size in some species is determined, at least in part, by the characteristics of the flower, particularly the ovarian tissues and cells. This hypothesis was tested in tomatoes where two nearly isogenic lines, differing for one gene affecting ovary cell division in the ovary primordia, and leading to ovaries of different size at bloom, had proportional variation in fruit size, independent of the source-sink balance (Nesbitt and Tanksley, 2001). In olive, Rapoport and Martins (2006) stated that, although it stands to reason that the initial size and growth potential of each ovarian tissues could be a factor in its growth as part of the fruit, little experimental information is available. Martins (2006) reported a strong correlation (R2 = 0.67) between the pulp/pit and ovary mesocarp/endocarp tissue ratios, among nine cultivars, but no data exist to correlate fruit size at harvest and ovary size at bloom. On the contrary, Rapoport et al. (2004) reported that while fruit size was mostly related to cell number among eight olive cultivars with different fruit size, at four weeks after bloom, cell size and number were similar in the ovary at bloom. This indicates that olive cultivars with different fruit sizes start out with similar ovaries, but have different rates of fruit development.
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A. Rosati et al. / Scientia Horticulturae 122 (2009) 399–403
However, in the work of Rapoport et al. (2004), cell number and size were measured in olive fruit/ovary transections (not in the endocarp of the mature fruit, however), while fruit and ovary volumes were not considered. Given that different cultivars have different proportions between transection area and fruit/ovary volume, and different pulp to pit ratio, the hypothesis that final fruit size is related to initial ovary size in olive, cannot be ruled out. Surprisingly, no studies yet have measured directly ovary and fruit dry weight. As Rapoport and Martins (2006) stated, the critical tests to determine the degree of dependence still need to be performed. Testing whether fruit size is related to ovary size at bloom, or whether different cultivars start out with similar sized ovaries is important since it has implications in the understanding of fruit set and development and, ultimately, on productivity.
Fig. 1. Seasonal pattern of fruit dry weight for many olive cultivars with different fruit size, during 2006–2008.
The aim of the present study was to test whether fruit weight at maturity is correlated to ovary weight at bloom among olive cultivars with different fruit size. 2. Materials and methods Ovaries and fruits from several olive (Olea europaea L.) cultivars were collected from bloom to harvest in 2006–2008. Cultivars were chosen on the basis of the different fruit size, including table and oil cultivars. In 2006 the following cultivars were chosen: Koroneiki, Canino, Nocellara del Belice, Ascolana tenera, Arbequina, Moraiolo and Frantoio. In 2007 few more cultivars (Carolea, Leccino, Rosciola) were added while Arbequina did not set fruits. In 2008, the same cultivars as in 2007 were chosen, except for Nocellara del Belice, which did not set enough fruits for the
Fig. 2. Relationship between fruit dry weight at maturity and ovary dry weight at bloom for many olive cultivars with different fruit size, in 2006–2008. All fits are statistically significant (P < 0.001).
A. Rosati et al. / Scientia Horticulturae 122 (2009) 399–403
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sampling. For each cultivar, 10 ovaries in 2006 and 30 ovaries in 2007 and 2008 were collected from three to five 25-year-old trees that are part of a germplasm collection planted at the experimental farm of the CRA – OLI, near Spoleto in central Italy (428 480 4800 N, 128 390 1500 E, 356 m above see level). Flowers that had just opened were collected and immediately taken to the laboratory where the ovaries were isolated from the other parts of the flower. The ovaries were then dried in a ventilated oven at 60 8C for 48 h and then weighed. All 10 or 30 ovaries per cultivar were weighed together in a single measurement, to allow for sufficient precision of the scale reading. After bloom, 10–30 developing fruits were sampled periodically until harvest in November. Fruits were oven-dried and weighed similar to the ovaries, but kept in the oven until constant weight. Additionally, 15 whole flowers were collected just after opening in 2007 and 2008, and the corollas + stamens were separated from the pistils and oven-dried as with the ovaries to determine their dry weight. As for the ovaries, all 10–30 fruits or whole flowers were weighed together in a single measurement. Trees were not irrigated as is normal practice for olive growing in the area. Statistical analyses of the linear fits was carried out using the R Development Core Team (2006) software. 3. Results and discussion 3.1. Flower, ovary and fruit weight As expected, fruit weight (i.e. dry weight) differed considerably among cultivars (Fig. 1). In 2006, there was about a six-fold difference in fruit dry weight between the biggest (Nocellara del Belice, 2.3 g) and the smallest (Koroneiki, 0.4 g) fruits (Fig. 1). In 2007 the difference was again about six-fold, while in 2008 it was about five-fold. Ovary weight was also very variable among cultivars, with a five-fold difference between the biggest and the smallest ovaries in 2006, and a slightly smaller difference in the following years (Fig. 2). Hence, the initial difference between ovary weights among cultivars remained consistent up to harvest. The ratio between fruit dry weight at maturity and ovary dry weight at bloom ranged between 1000 and 4000 in the different years and cultivars, with most values around 2000 (Fig. 6). This result agrees with data from Rapoport et al. (2004) who found that cell size (i.e. transection area) in the mature fruit was, on average, 40 times that in the ovary (thus about 250 times the volume) while cell number was on average 8.5 times greater. Cultivars with larger ovaries also had larger flowers, with the corolla + stamen dry weight being correlated to the ovary dry weight (Fig. 3). Cuevas and Polito (2004) reported significant correlations between parts of the olive flower (i.e. stamen and pistil, stamen and petal, pistil and petal), but that study regarded only flowers within the same variety. Similar results were found in peach (Kozai et al., 2004). The present results demonstrate that large fruited olive cultivars have large flowers, with large ovaries.
Fig. 3. Relationship between the dry weight of petals + stamens and ovary dry weight for many olive cultivars, 2007 and 2008. All fits are statistically significant (P < 0.001).
genetically through the ovary size as was found in tomato (Nesbitt and Tanksley, 2001), peach (Scorza et al., 1991) and kiwi (Lai et al., 1990; Lawes et al., 1990; Cruz-Castillo et al., 1991). Particularly in tomato, it was found that sink competition was stronger between the big fruits of the nearly isogenic line carrying the gene for larger ovaries (and larger fruits) than among the small fruits of the wild type. This demonstrated that the wild type had small fruits due to genetic control and not due to competition for sources. Higher fruit set was the consequence of small fruit size, rather the cause. The
3.2. Correlation between ovary and fruit dry weight Fruit dry weight at harvest was strongly correlated to ovary dry weight at bloom in both years (Fig. 2), demonstrating that the difference in fruit weight among the olive cultivars was already present at bloom as a difference in ovary weight. The greater weight of both ovaries and mature fruits is probably due to a greater number of cells, rather than to larger cell size, in olive (Rapoport et al., 2004) as well as in other species (Smith, 1950; Cheng and Breen, 1992). The strong correlation between ovary and fruit dry weight among different olive cultivars with different fruit sizes suggests that, in olive, fruit growth potential is largely determined
Fig. 4. Relationship between fruit dry weight at maturity and ovary dry weight at bloom as in Fig. 2, but pooling all data from three years. The fit is statistically significant (P < 0.001).
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present results suggest that fruit size is genetically controlled through the ovary size also in olive. This hypothesis agrees with findings by Padula et al. (2008) who found that fruit size had high heritability in olive, even though this character was also strongly affected by the environment. Banilas et al. (2003) found that a RAPD marker could distinguish accessions according to fruit size, suggesting a genetic basis for fruits size. However specific DNA sequences relative to fruit size have yet to be identified in olive (Banilas et al., 2003). The correlation between fruit and ovary dry weight was also strong when all data from the three years were pooled (Fig. 4), despite the year-to-year variation in both ovary and fruit dry weight (Figs. 1 and 2). This suggests that ovary weight in olive changes between years and that the largest fruits are obtained in years with larger ovaries. The causes of the year-to-year variation in ovary weight should be further investigated.
Fig. 5. Coefficient of determination (R2) of the regression between ovary dry weight and fruit dry weight during the fruit development season, in 2006–2008.
The correlation between fruit and ovary dry weight was also good at all stages of fruit development as shown in Fig. 5 where the coefficient of determination (R2) of this relationship was shown for the different sampling dates. This suggests that fruit growth pattern and rate were similar in all cultivars and that the difference in final fruit weight was not related to differences in the rate of fruit development. This interpretation is further supported by the fact that fruit dry weight at maturity was not related to the ratio between fruit dry weight at maturity and ovary dry weight (Fig. 6). If the greater fruit weight of large fruited cultivars had derived from a faster rate of fruit development, fruit dry weight at maturity should have been consistently related to the fruit/ovary dry weight ratio. This ratio (i.e. fruit/ovary dry weight) may be more reflective of the growing conditions (i.e. the environmental effects on fruit size) than the genetic potential for fruit growth, which appeared to be controlled mainly by ovary weight at bloom. In fact, ovary weight is not the sole determinant of fruit weight at harvest, which is affected also by nutrient (Grossman and DeJong, 1995) and water (Lavee et al., 1990; Proietti and Antognozzi, 1996; Inglese et al., 1996) availability as well as temperature and growing conditions in general. In olive, alternate bearing also has a strong effect on fruit weight (Hartmann, 1952; Lavee and Spiegel-Roy, 1967; Troncoso et al., 1978), probably via nutrient competition (Suarez et al., 1984; Cuevas et al., 1994). All these factors tend to mask the relationship between ovary weight and final fruit weight. In the present study, this relationship was apparent probably because extremely large as well as extremely small fruited cultivars were included in the study. With a smaller range of fruit weights, the variation in fruit weight due to environmental conditions is more likely to override the effect of ovary weight. Another factor that affects the ovary weight/fruit weight relationship is harvest time. In some species, harvest time differs among cultivars, affecting fruit growth potential. In peach, for instance, it has been demonstrated that early-maturing cultivars have lower fruit growth potential (i.e. in terms of dry weight), due to the shorter fruit-growing season (Berman et al., 1998). This makes the relationship between final fruit weight and ovary weight, across cultivars, even less apparent. In olives, however, at least in this experiment, all cultivars were harvested at the same time, giving similar duration for fruit development among cultivars. This eliminates one variable that can affect fruit weight, allowing the relationship between ovary weight and fruit weight to be more evident than in other species with different fruit maturation time.
Fig. 6. Relationship between fruit dry weight at maturity and the ratio between fruit dry weight at maturity and ovary dry weight at bloom. Data from three years are pooled. No statistically significant fit was found.
A. Rosati et al. / Scientia Horticulturae 122 (2009) 399–403
3.3. Implications of the ovary vs. fruit dry weight correlation Bigger ovaries at bloom probably imply stronger sink activity, as was found in nearly isogenic lines of tomatoes, carrying one gene difference for larger ovary size (Nesbitt and Tanksley, 2001). Stronger sink activity implies stronger competition among fruits. Competition among fruits is believed to occur already at bloom and to affect fruit set in olive (Suarez et al., 1984; Cuevas et al., 1994; Lavee et al., 1999; Seifi et al., 2008). This could explain the lower fruit set of table olives compared to small fruited cultivars, which notoriously set a greater number of fruits (Acebedo et al., 2002). If the total fruit-biomass carrying capacity of the tree, or ‘‘global fruiting potential’’ determines fruit set (Lavee et al., 1996), then the number of ovaries that set fruits should be inversely related to ovary weight, in order to achieve the same total ovary biomass (as well as the same fruit biomass at maturity). Testing the hypothesis that ovary weight strongly affects fruit set will be the subject of future work. 4. Conclusions The present results demonstrate that fruit weight at maturity is correlated to ovary weight at bloom in olive. Therefore, fruit weight appears genetically controlled through the ovary weight, even though this is not the sole factor determining final fruit weight, which depends strongly on environmental and tree conditions as well. The latter conditions may generate enough variability in fruit weight to mask the fruit/ovary relationship, unless cultivars of very contrasting fruit weight are compared, as in this study. Differences in ovary weight may contribute explaining different fruit set dynamic among cultivars. Acknowledgment The study was funded by the Italian Ministry for Agricultural, Food and Forestry Politics (MiPAAF), RIOM project. References Acebedo, M.M., Can˜ete, M.L., Cuevas, J., 2002. Processes affecting fruit distribution and its quality in the canopy of olive trees. Adv. Hort. Sci. 14, 169–175. Banilas, G., Minas, J., Gregoriou, C., Demoliou, C., Kourti, A., Hatzopoulos, P., 2003. Genetic diversity among accessions of an ancient olive variety of Cyprus. Genome 46 (3), 370–376. Berman, M.E., Rosati, A., Pace, L., Grossman, Y.L., DeJong, T.M., 1998. Using simulation modeling to estimate the relationship between date of fruit maturity and yield potential in peach. Fruit Varieties J. 52 (4), 229–235. Cheng, G.W., Breen, P.J., 1992. Cell count and size in relation to fruit size among strawberry cultivars. J. Am. Soc. Hort. Sci. 117, 946–950. Coombe, B.G., 1973. The regulation of set and development of the grape berry. Acta Hort. 34, 261–273. Cruz-Castillo, J.G., Lawes, G.S., Woolley, D.J., 1991. The influence of the time of anthesis, seed factors, and the application of a growth regulator mixture on the growth of kiwifruit. Acta Hort. 297, 475–480. Cuevas, J., Polito, V.S., 2004. The role of staminate flowers in the breeding system of Olea europaea (Oleaceae): an Andromonoecious, wind-pollinated taxon. Ann. Bot. 93, 547–553. Cuevas, J., Rallo, L., Rapoport, H.F., 1994. Crop load effects on floral quality in olive. Sci. Hort. 59, 123–130. Famiani, F., Proietti, P., Paliotti, A., Ferranti, F., Antognozzi, E., 2000. Effect of leaf to fruit ratios on fruit growth in chestnut. Sci. Hort. 85, 145–152. Grossman, Y.L., DeJong, T.M., 1994. Peach: a simulation model of reproductive and vegetative growth in peach trees. Tree Physiol. 14 (4), 329–345. Grossman, Y.L., DeJong, T.M., 1995. Maximum fruit growth potential following resource limitation during peach growth. Ann. Bot. 75, 561–567.
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Handley, D.T., Dill, J.F., 2003. Vegetative and floral characteristics of six strawberry cultivars associated with fruit size, yield and susceptibility to tarnished plant bug injury. Acta Hort. 626, 161–167. Hartmann, H.T., 1952. Spray thinning of Olives. Calif. Agric. 6, 7. Hasegawa, K., Nakajima, Y., 1990. Effects of bloom date, seediness, GA treatment and location of fruits in the foliar canopy on the fruit quality of persimmon (Diospyros kaki Thunb.). J. Jpn. Soc. Hort. Sci. 59, 263–270. Inglese, P., Barone, E., Gullo, G., 1996. The effect of complementary irrigation on fruit growth, ripening pattern and oil characteristics of olive (Olea europaea L.) cv. Carolea. J. Hort. Sci. 71 (2), 257–263. Jackson, J.E., 2003. Biology of Apples and Pears. Cambridge University Press, Cambridge, UK. Kozai, N., Beppu, K., Mochioka, R., Boonprakoi, U., Subhadrabandhu, S., Kataoka, I., 2004. Adverse effects of hight temperature on the development of reproductive organs in ‘Hakuho’ peach trees. J. 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Lawes, G.S., Woolley, D.J., Lai, R., 1990. Seeds and other factors affecting fruit size in kiwifruit. Acta Hort. 282, 257–264. Marguery, P., Sangwan, B.S., 1993. Sources of variation between apple fruits within a season, and between seasons. J. Hort. Sci. 68, 309–315. Martins, P.C.S., 2006. Calidad de flor en variedades portuguesas del olivo Olea Europea. Master en Olivicultura y Elaiotecnia, Ciheam Mediterranean Istitute of Agronomy and University of Co`rdoba. McPherson, H.G., Richardson, A.C., Snelgark, W.P., Patterson, K.J., Currie, M.B., 2001. Flower quality and fruit size in kiwifruit (Actinidia deliciosa). N. Z. J. Crop Hort. Sci. 29, 93–101. Nesbitt, T.C., Tanksley, S.D., 2001. fw. 2.2. Directly affects the size of developing tomato fruit, with secondary effects on fruit number and photosynthate distribution. Plant Physiol. 127, 575–583. Padula, G., Giordani, E., Bellini, E., Rosati, A., Pandolfi, S., Paoletti, A., Pannelli, G., Ripa, V., De Rose, F., Perri, E., Buccoliero, A., Pennone, C., 2008. Field evaluation of new olive (Olea europaea) selections and effects of genotype and environment on productivity and fruit characteristics. Adv. Hort. Sci. 22 (2), 87–94. Praloran, J.C., Vullin, G., Jaquemond, C., Despierre, D., 1981. Observations sur la croissance des clementines en Corse. Fruits 36, 755–767. Proietti, P., Antognozzi, E., 1996. Effect of irrigation on fruit quality of table olives (Olea europea), cultivar ‘Ascolana tenera’. N. Z. J. Crop Hort. Sci. 24, 175–181. Rapoport, H.F., Manrique, T., Gucci, R., 2004. Cell division and expansion in the olive fruit. Acta Hort. 636, 461–465. Rapoport, H.F., Martins, P.C.S., 2006. Flower quality in the olive: broadening the concept. In: Proceedings of ‘‘Olivebioteq 2006’’ Second International Seminar ‘‘Recent Advances in Olive Industry’’, Marsala-Mazara del Vallo, Italy, 5–10 November 2006, pp. 397–402. Scorza, R., May, L.G., Purnell, B., Upchurch, B., 1991. Differences in number and area of mesocarp cells between small-and-large-fruited peach cultivars. J. Am. Soc. Hort. Sci. 116, 861–864. Seifi, E., Guerin, J., Kaiser, B., Sedgley, M., 2008. Inflorescence architecture of olive. Sci. Hort. 116, 273–279. Smith, W.H., 1950. Cell-multiplication and cell-enlargement in the development of the flesh of the apple fruit. Ann. Bot. 14, 23–38. Suarez, M.P., Fernandez-Escobar, R., Rallo, L., 1984. Competition among fruits in olive II. Influence of inflorescence or fruit thinning and cross-pollination on fruit set components and crop efficiency. Acta Hort. 149, 131–144. ˜ an, J., 1978. Aclareo quimico de frutos en el olivar Troncoso, A., Prieto, J., Lin Manzanillo de Sevilla. An. Edaf. Agrob. 37, 882–893. 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Contents lists available at ScienceDirect
Scientia Horticulturae journal homepage: www.elsevier.com/locate/scihorti
Fruit weight is related to ovary weight in olive (Olea europaea L.) Adolfo Rosati *, Marija Zipanc´icˇ, Silvia Caporali, Giuseppe Padula CRA – OLI, via Nursina 2, 06049 Spoleto (PG), Italy
A R T I C L E I N F O
A B S T R A C T
Article history: Received 23 March 2009 Received in revised form 14 May 2009 Accepted 16 May 2009
Fruit size is an important parameter both for scientific understanding and for commercial purposes. In many species, mature fruit size is often related to floral ovary size, but no literature exists in olive that demonstrates such a relationship. Previous work suggests that olive cultivars with different fruit sizes have similar cell number and size in the ovary transectional area, but ovary and fruit dry weight was not measured. In the present study, ovary dry weight and fruit dry weight during the whole fruit development season until harvest were measured in olive cultivars with different fruit size, over three years. Flower dry weight was also measured. Fruit weight at harvest was strongly correlated to ovary weight at bloom, both in single-year data and when data from three years were pooled. Flower dry weight, excluding the ovary, was also correlated to ovary dry weight. Ovary dry weight was strongly correlated not only to the fruit dry weight at maturity, but also at any date during fruit development. The mature fruit/ovary dry weight ratio ranged between 1000 and 4000 among cultivars, but was not correlated to the fruit dry weight at maturity. These results suggest that, in olive, fruit weight is genetically controlled through the ovary weight at bloom. This knowledge may have implications in the understanding of fruit set and source-sink relationships in olive. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Ovary Fruit Flower Size Weight Olea europaea Genetic control
1. Introduction Fruit size is a very important parameter both for scientific understanding and for commercial purposes. Much research has been carried out in several species to understand the mechanisms that control fruit size (Westwood and Blaney, 1963; Scorza et al., 1991; Grossman and DeJong, 1995; Famiani et al., 2000; Nesbitt and Tanksley, 2001; Jackson, 2003; Zhang et al., 2005a,b). Fruit size is determined by the interaction of the environmental factors with the genetically determined growth potential of the fruits. Among these factors photosynthate availability, which depends on the source-sink balance, is very important. The interaction between genetic growth potential and source-sink relationship has been widely studied and implemented in growth models, such as the ‘‘Peach’’ model (Grossman and DeJong, 1994). Fruit size is determined by cell number and size (McPherson et al., 2001). Fruits from early opening flowers are larger at harvest than those from later blooms in several species such as apple (Marguery and Sangwan, 1993), persimmon (Hasegawa and Nakajima, 1990), citrus (Praloran et al., 1981), peach (Scorza et al., 1991), grape (Coombe, 1973), and strawberry (Cheng and Breen, 1992). In kiwifruit, early flowers had larger ovaries than late flowers on the same vine, and produced larger fruits with a higher cell number in the outer pericarp than fruits from late flowers,
* Corresponding author. Tel.: +39 0743 49743; fax: +39 0743 43634. E-mail addresses: [email protected], [email protected] (A. Rosati). 0304-4238/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.scienta.2009.05.034
while cell size was the same (Lai et al., 1990; Lawes et al., 1990; Cruz-Castillo et al., 1991). The high number of cells was already found in the ovary tissues of early flowers. Similarly, peach cultivars with larger fruits had fruits with more cells than in fruits from small-fruited cultivars, and this difference appeared early in the growth of the ovary (Scorza et al., 1991). In strawberry, cultivars with larger/heavier flowers had bigger fruits (Handley and Dill, 2003). These findings suggest that final fruit size in some species is determined, at least in part, by the characteristics of the flower, particularly the ovarian tissues and cells. This hypothesis was tested in tomatoes where two nearly isogenic lines, differing for one gene affecting ovary cell division in the ovary primordia, and leading to ovaries of different size at bloom, had proportional variation in fruit size, independent of the source-sink balance (Nesbitt and Tanksley, 2001). In olive, Rapoport and Martins (2006) stated that, although it stands to reason that the initial size and growth potential of each ovarian tissues could be a factor in its growth as part of the fruit, little experimental information is available. Martins (2006) reported a strong correlation (R2 = 0.67) between the pulp/pit and ovary mesocarp/endocarp tissue ratios, among nine cultivars, but no data exist to correlate fruit size at harvest and ovary size at bloom. On the contrary, Rapoport et al. (2004) reported that while fruit size was mostly related to cell number among eight olive cultivars with different fruit size, at four weeks after bloom, cell size and number were similar in the ovary at bloom. This indicates that olive cultivars with different fruit sizes start out with similar ovaries, but have different rates of fruit development.
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However, in the work of Rapoport et al. (2004), cell number and size were measured in olive fruit/ovary transections (not in the endocarp of the mature fruit, however), while fruit and ovary volumes were not considered. Given that different cultivars have different proportions between transection area and fruit/ovary volume, and different pulp to pit ratio, the hypothesis that final fruit size is related to initial ovary size in olive, cannot be ruled out. Surprisingly, no studies yet have measured directly ovary and fruit dry weight. As Rapoport and Martins (2006) stated, the critical tests to determine the degree of dependence still need to be performed. Testing whether fruit size is related to ovary size at bloom, or whether different cultivars start out with similar sized ovaries is important since it has implications in the understanding of fruit set and development and, ultimately, on productivity.
Fig. 1. Seasonal pattern of fruit dry weight for many olive cultivars with different fruit size, during 2006–2008.
The aim of the present study was to test whether fruit weight at maturity is correlated to ovary weight at bloom among olive cultivars with different fruit size. 2. Materials and methods Ovaries and fruits from several olive (Olea europaea L.) cultivars were collected from bloom to harvest in 2006–2008. Cultivars were chosen on the basis of the different fruit size, including table and oil cultivars. In 2006 the following cultivars were chosen: Koroneiki, Canino, Nocellara del Belice, Ascolana tenera, Arbequina, Moraiolo and Frantoio. In 2007 few more cultivars (Carolea, Leccino, Rosciola) were added while Arbequina did not set fruits. In 2008, the same cultivars as in 2007 were chosen, except for Nocellara del Belice, which did not set enough fruits for the
Fig. 2. Relationship between fruit dry weight at maturity and ovary dry weight at bloom for many olive cultivars with different fruit size, in 2006–2008. All fits are statistically significant (P < 0.001).
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sampling. For each cultivar, 10 ovaries in 2006 and 30 ovaries in 2007 and 2008 were collected from three to five 25-year-old trees that are part of a germplasm collection planted at the experimental farm of the CRA – OLI, near Spoleto in central Italy (428 480 4800 N, 128 390 1500 E, 356 m above see level). Flowers that had just opened were collected and immediately taken to the laboratory where the ovaries were isolated from the other parts of the flower. The ovaries were then dried in a ventilated oven at 60 8C for 48 h and then weighed. All 10 or 30 ovaries per cultivar were weighed together in a single measurement, to allow for sufficient precision of the scale reading. After bloom, 10–30 developing fruits were sampled periodically until harvest in November. Fruits were oven-dried and weighed similar to the ovaries, but kept in the oven until constant weight. Additionally, 15 whole flowers were collected just after opening in 2007 and 2008, and the corollas + stamens were separated from the pistils and oven-dried as with the ovaries to determine their dry weight. As for the ovaries, all 10–30 fruits or whole flowers were weighed together in a single measurement. Trees were not irrigated as is normal practice for olive growing in the area. Statistical analyses of the linear fits was carried out using the R Development Core Team (2006) software. 3. Results and discussion 3.1. Flower, ovary and fruit weight As expected, fruit weight (i.e. dry weight) differed considerably among cultivars (Fig. 1). In 2006, there was about a six-fold difference in fruit dry weight between the biggest (Nocellara del Belice, 2.3 g) and the smallest (Koroneiki, 0.4 g) fruits (Fig. 1). In 2007 the difference was again about six-fold, while in 2008 it was about five-fold. Ovary weight was also very variable among cultivars, with a five-fold difference between the biggest and the smallest ovaries in 2006, and a slightly smaller difference in the following years (Fig. 2). Hence, the initial difference between ovary weights among cultivars remained consistent up to harvest. The ratio between fruit dry weight at maturity and ovary dry weight at bloom ranged between 1000 and 4000 in the different years and cultivars, with most values around 2000 (Fig. 6). This result agrees with data from Rapoport et al. (2004) who found that cell size (i.e. transection area) in the mature fruit was, on average, 40 times that in the ovary (thus about 250 times the volume) while cell number was on average 8.5 times greater. Cultivars with larger ovaries also had larger flowers, with the corolla + stamen dry weight being correlated to the ovary dry weight (Fig. 3). Cuevas and Polito (2004) reported significant correlations between parts of the olive flower (i.e. stamen and pistil, stamen and petal, pistil and petal), but that study regarded only flowers within the same variety. Similar results were found in peach (Kozai et al., 2004). The present results demonstrate that large fruited olive cultivars have large flowers, with large ovaries.
Fig. 3. Relationship between the dry weight of petals + stamens and ovary dry weight for many olive cultivars, 2007 and 2008. All fits are statistically significant (P < 0.001).
genetically through the ovary size as was found in tomato (Nesbitt and Tanksley, 2001), peach (Scorza et al., 1991) and kiwi (Lai et al., 1990; Lawes et al., 1990; Cruz-Castillo et al., 1991). Particularly in tomato, it was found that sink competition was stronger between the big fruits of the nearly isogenic line carrying the gene for larger ovaries (and larger fruits) than among the small fruits of the wild type. This demonstrated that the wild type had small fruits due to genetic control and not due to competition for sources. Higher fruit set was the consequence of small fruit size, rather the cause. The
3.2. Correlation between ovary and fruit dry weight Fruit dry weight at harvest was strongly correlated to ovary dry weight at bloom in both years (Fig. 2), demonstrating that the difference in fruit weight among the olive cultivars was already present at bloom as a difference in ovary weight. The greater weight of both ovaries and mature fruits is probably due to a greater number of cells, rather than to larger cell size, in olive (Rapoport et al., 2004) as well as in other species (Smith, 1950; Cheng and Breen, 1992). The strong correlation between ovary and fruit dry weight among different olive cultivars with different fruit sizes suggests that, in olive, fruit growth potential is largely determined
Fig. 4. Relationship between fruit dry weight at maturity and ovary dry weight at bloom as in Fig. 2, but pooling all data from three years. The fit is statistically significant (P < 0.001).
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present results suggest that fruit size is genetically controlled through the ovary size also in olive. This hypothesis agrees with findings by Padula et al. (2008) who found that fruit size had high heritability in olive, even though this character was also strongly affected by the environment. Banilas et al. (2003) found that a RAPD marker could distinguish accessions according to fruit size, suggesting a genetic basis for fruits size. However specific DNA sequences relative to fruit size have yet to be identified in olive (Banilas et al., 2003). The correlation between fruit and ovary dry weight was also strong when all data from the three years were pooled (Fig. 4), despite the year-to-year variation in both ovary and fruit dry weight (Figs. 1 and 2). This suggests that ovary weight in olive changes between years and that the largest fruits are obtained in years with larger ovaries. The causes of the year-to-year variation in ovary weight should be further investigated.
Fig. 5. Coefficient of determination (R2) of the regression between ovary dry weight and fruit dry weight during the fruit development season, in 2006–2008.
The correlation between fruit and ovary dry weight was also good at all stages of fruit development as shown in Fig. 5 where the coefficient of determination (R2) of this relationship was shown for the different sampling dates. This suggests that fruit growth pattern and rate were similar in all cultivars and that the difference in final fruit weight was not related to differences in the rate of fruit development. This interpretation is further supported by the fact that fruit dry weight at maturity was not related to the ratio between fruit dry weight at maturity and ovary dry weight (Fig. 6). If the greater fruit weight of large fruited cultivars had derived from a faster rate of fruit development, fruit dry weight at maturity should have been consistently related to the fruit/ovary dry weight ratio. This ratio (i.e. fruit/ovary dry weight) may be more reflective of the growing conditions (i.e. the environmental effects on fruit size) than the genetic potential for fruit growth, which appeared to be controlled mainly by ovary weight at bloom. In fact, ovary weight is not the sole determinant of fruit weight at harvest, which is affected also by nutrient (Grossman and DeJong, 1995) and water (Lavee et al., 1990; Proietti and Antognozzi, 1996; Inglese et al., 1996) availability as well as temperature and growing conditions in general. In olive, alternate bearing also has a strong effect on fruit weight (Hartmann, 1952; Lavee and Spiegel-Roy, 1967; Troncoso et al., 1978), probably via nutrient competition (Suarez et al., 1984; Cuevas et al., 1994). All these factors tend to mask the relationship between ovary weight and final fruit weight. In the present study, this relationship was apparent probably because extremely large as well as extremely small fruited cultivars were included in the study. With a smaller range of fruit weights, the variation in fruit weight due to environmental conditions is more likely to override the effect of ovary weight. Another factor that affects the ovary weight/fruit weight relationship is harvest time. In some species, harvest time differs among cultivars, affecting fruit growth potential. In peach, for instance, it has been demonstrated that early-maturing cultivars have lower fruit growth potential (i.e. in terms of dry weight), due to the shorter fruit-growing season (Berman et al., 1998). This makes the relationship between final fruit weight and ovary weight, across cultivars, even less apparent. In olives, however, at least in this experiment, all cultivars were harvested at the same time, giving similar duration for fruit development among cultivars. This eliminates one variable that can affect fruit weight, allowing the relationship between ovary weight and fruit weight to be more evident than in other species with different fruit maturation time.
Fig. 6. Relationship between fruit dry weight at maturity and the ratio between fruit dry weight at maturity and ovary dry weight at bloom. Data from three years are pooled. No statistically significant fit was found.
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3.3. Implications of the ovary vs. fruit dry weight correlation Bigger ovaries at bloom probably imply stronger sink activity, as was found in nearly isogenic lines of tomatoes, carrying one gene difference for larger ovary size (Nesbitt and Tanksley, 2001). Stronger sink activity implies stronger competition among fruits. Competition among fruits is believed to occur already at bloom and to affect fruit set in olive (Suarez et al., 1984; Cuevas et al., 1994; Lavee et al., 1999; Seifi et al., 2008). This could explain the lower fruit set of table olives compared to small fruited cultivars, which notoriously set a greater number of fruits (Acebedo et al., 2002). If the total fruit-biomass carrying capacity of the tree, or ‘‘global fruiting potential’’ determines fruit set (Lavee et al., 1996), then the number of ovaries that set fruits should be inversely related to ovary weight, in order to achieve the same total ovary biomass (as well as the same fruit biomass at maturity). Testing the hypothesis that ovary weight strongly affects fruit set will be the subject of future work. 4. Conclusions The present results demonstrate that fruit weight at maturity is correlated to ovary weight at bloom in olive. Therefore, fruit weight appears genetically controlled through the ovary weight, even though this is not the sole factor determining final fruit weight, which depends strongly on environmental and tree conditions as well. The latter conditions may generate enough variability in fruit weight to mask the fruit/ovary relationship, unless cultivars of very contrasting fruit weight are compared, as in this study. Differences in ovary weight may contribute explaining different fruit set dynamic among cultivars. Acknowledgment The study was funded by the Italian Ministry for Agricultural, Food and Forestry Politics (MiPAAF), RIOM project. References Acebedo, M.M., Can˜ete, M.L., Cuevas, J., 2002. Processes affecting fruit distribution and its quality in the canopy of olive trees. Adv. Hort. Sci. 14, 169–175. Banilas, G., Minas, J., Gregoriou, C., Demoliou, C., Kourti, A., Hatzopoulos, P., 2003. Genetic diversity among accessions of an ancient olive variety of Cyprus. Genome 46 (3), 370–376. Berman, M.E., Rosati, A., Pace, L., Grossman, Y.L., DeJong, T.M., 1998. Using simulation modeling to estimate the relationship between date of fruit maturity and yield potential in peach. Fruit Varieties J. 52 (4), 229–235. Cheng, G.W., Breen, P.J., 1992. Cell count and size in relation to fruit size among strawberry cultivars. J. Am. Soc. Hort. Sci. 117, 946–950. Coombe, B.G., 1973. The regulation of set and development of the grape berry. Acta Hort. 34, 261–273. Cruz-Castillo, J.G., Lawes, G.S., Woolley, D.J., 1991. The influence of the time of anthesis, seed factors, and the application of a growth regulator mixture on the growth of kiwifruit. Acta Hort. 297, 475–480. Cuevas, J., Polito, V.S., 2004. The role of staminate flowers in the breeding system of Olea europaea (Oleaceae): an Andromonoecious, wind-pollinated taxon. Ann. Bot. 93, 547–553. Cuevas, J., Rallo, L., Rapoport, H.F., 1994. Crop load effects on floral quality in olive. Sci. Hort. 59, 123–130. Famiani, F., Proietti, P., Paliotti, A., Ferranti, F., Antognozzi, E., 2000. Effect of leaf to fruit ratios on fruit growth in chestnut. Sci. Hort. 85, 145–152. Grossman, Y.L., DeJong, T.M., 1994. Peach: a simulation model of reproductive and vegetative growth in peach trees. Tree Physiol. 14 (4), 329–345. Grossman, Y.L., DeJong, T.M., 1995. Maximum fruit growth potential following resource limitation during peach growth. Ann. Bot. 75, 561–567.
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