Development of the fruit quality during cultivation

Of the factors that influence the quality of the product in cultivation (pre-harvest), the most determining factors are the genetics of the variety, the environmental conditions, the further interaction between genotype and environment, and the crop management strategies (^{Herrera, 2012}).

Environmental factors and quality

The environmental conditions of the site (climate and soil) are crucial for the process of crop quality formation, and are the basis for the development of commercial fruit growing in a country or region (^{Fischer and Miranda, 2012}; Fischer and Orduz-Rodríguez, 2012). The environment influences processes such as photosynthesis, transpiration, respiration, translocation of photoassimilates and the metabolism of the plant, which are decisive for the internal and external quality of the fruit and its longevity in post-harvest (^{Ladaniya, 2008}).

The effect of the physical, chemical and biotic environment on the physiological mechanisms of the plant is known as plant ecophysiology (^{Larcher, 2003}; ^{Lambers et al., 2008}). Different cultivated passion fruit species are found in Brazil, Colombia and, in general, in tropical America and Central America (^{Miranda, 2012}). The ecophysiological demands and climatic conditions of the different types of passion fruit are diverse, as shown in Table 1.

TABLE 1 Climatic factors of growth and production of passion fruits in Colombia. 

In Colombia, the altitude defines factors such as temperature. With an increase of 100 m the temperature decreases on average 0.6°C, while the UV radiation increases, and the atmospheric pressure and relative humidity decrease (^{Fischer and Orduz-Rodríguez, 2012}). As shown in Table 1, different Passifloraceae can be grown commercially between 0 and 3,000 m a.s.l.

Due to the increase in UV light with elevation, juicy fruits, as in the case of Passifloraceae, are more prone to sunburn (^{Fischer et al., 2016}) and, in addition, a high and prolonged solar radiation increases both the temperature of the irradiated cells that can cause the splitting of the epidermis and a subsequent entry of pathogens to these unprotected tissues (Fischer, 2000). For this reason, the plants need leaves to cover fruits. However, it is important that part of the UV light reaches the fruits during ripening to stimulate the production of antioxidants that improve their nutritional value (^{Fischer et al., 2016}).

At higher altitudes, due to the colder environment, production starts later and fruit development lasts longer than at lower sites, as ^{Mayorga (2017)} found in banana passion fruit. Outside their altitudinal range, crops can have a higher incidence of pests and diseases, and pollination processes are less effective (^{Fischer et al., 2009}; ^{Ocampo et al., 2015}). In banana passion fruit at higher altitudes, the epidermis of the fruit is thicker and more resistant to anthracnose (^{Campos and Quintero, 2012}). In sweet granadilla, at altitudes lower than 1,700 m a.s.l., fruit size is reduced producing 50% of second grade quality fruits (^{Castro, 2001}).

After assessing Passifloraceae fruits in a high altitudinal zone (2,498 m, average 14.9°C), ^{Mayorga (2017)} found that in Pasca (Cundinamarca, Colombia) the banana passion fruits had a higher weight, size, citric and ascorbic acid contents; in contrast, the total soluble solids content (TSS) was lower in the high zone compared to fruits produced in lower areas (2,006 m a.s.l. and 17.9°C). It is possible that the organic acids in the higher area were not metabolized at the same rate due to the colder environment (^{Tellez et al., 2007}) and the higher TSS at the lower elevation (2,006 m), leading to increase the transformation rate of starch in sugar by hydrolysis process. This was stated assuming that the TSS is basically a sugar dilution (80.95%) that does not depend directly on leaf photosynthesis rather than on the climatic conditions (^{Flórez et al., 2012}), considering that in this research the photosynthetic rate increased proportionally to the elevation rate.

For banana passion fruit located in foggy areas, the espalier and the conduction of the canopy were exposed with an angle of 45° and an orientation towards the east, increasing the capture of light by the leaves and the production of fruits. These features produce 90 fruits per m² of canopy in low radiation sites and up to 100-150 fruits per m² in those of high radiation with productions as high as 40 t ha^-1 year^-1,

Fischer, Melgarejo, and Cutler: Pre-harvest factors that influence the quality of passion with 2.5 cycles annually for the cv. Momix (O.C. Quintero, personal communication, 2004).

Genetic material and quality

The highest genetic diversity of the passion fruit is found in Colombia, where ^{Ocampo et al. (2007)} observed 167 species, from which 165 were native, followed by Brazil with 127 and Ecuador with 90. According to ^{Ligarreto (2012)}, in the National System of Germplasm Banks administered by Corpoica (Colombia), there are 170 accessions of passion fruits, with 52 molecularly characterized, including details about their biochemical and agro-industrial properties. The quality enhancement is the most important objective of genetic breeding, improving the flavor and acidity of the fruit for the industrialized beverages manufacture, increasing the content of TSS and the size of the fruit (Ligarreto, 2012). In the case of yellow passion fruit, the same author mentions that oval shaped fruits are preferred because they contain up to 10% more juice than the round ones.

^{Ocampo et al. (2015)} collected and characterized sweet granadilla fruits in 35 municipalities of 11 provinces of the Andean region in Colombia to establish the degree of genetic variability as an important input for genetic improvement. Eleven physicochemical variables were characterized and seven elite accessions were identified through the quality parameters: fruit weight (>34 g), °Brix (>14.4) and pulp + seed (>52%).

Regarding the influence of the genetic material on the quality and production of the Passifloraceae, there are great differences between the species and the variety. In yellow passion fruit in Brazil, the kinetics of chlorophyll fluorescence allowed an accurate evaluation of the functional states of the photosynthetic apparatus in the different cultivars, which indicated that 'FB 300', 'BRS Sol do Cerrado' and 'BRS Ouro Vermelho' are photosynthetically more efficient and have better fruit quality (^{Gama et al., 2013}).

^{Ramaiya et al. (2013)} compared antioxidant contents (ascorbic acid, total phenols and total antioxidant activity) in four passion fruit species and found the highest content of ascorbic acid in purple passion fruit (0.32 g kg^-1 FW) and the lowest in sweet calabash (0.15 g kg^-1 FW). Regarding the total phenols, the highest content was found in sweet calabash (277.00 mg GAE/L FW) and the lowest in giant granadilla (272.96 mg GAE/L FW), while the highest total antioxidant activity was found in sweet calabash (1,685.00 μπω! Trolox/L FW) and the lowest in purple passion fruit (547.70 μmol Trolox/L FW); yellow passion fruit obtained intermediate values of these antioxidants (Tab. 2).

TABLE 2 Some antioxidants, predominant organic acids and sugars contained in the pulp of passion fruits. 

^{1Ramaiya et al. (2013)}; ^{2Espinosa et al. (2018)}; ^{3Chan et al. (1972)}; ^{4Sánchez et al. (2014)}; ^{5Ocampo et al. (2015)}. TAA - Total antioxidant activity

In a compilation by ^{Casierra-Posada and Jarma-Orozco (2016)} on the nutritive values of different passion fruits vary depending on the species. For example, according to the reports of ^{Chan et al. (1972)}, the highest content of organic acids in yellow passion fruit are: citric acid (55.0 meq/100 g fruit juice), malic acid (10.5 meq), lactic acid (0.5 meq) and malonic acid (0.1 meq). In purple passion fruit, citric acid also presented the highest content, but only with 13.1 meq followed by lactic (7.4 meq), malonic (4.9 meq) and malic (3.8 meq) acids (Tab. 2).

Moreover, the different commercial passion fruit species differ in the content of sugars in the fruit juice. ^{Ramaiya et al. (2013)} analyzed the highest sucrose content in purple passion fruit (45.5 g kg^-1 FW) and the lowest in sweet calabash (17.0 g), while the glucose content was the highest in giant granadilla (43.7 g) and the lowest in yellow passion fruit (14.1 g). Likewise, the lowest level of monosaccharide fructose was found in yellow passion fruit (14.6 g), and the highest one was reported in giant granadilla (39.0 g) (Tab. 2).

Some cultural practices and quality Nutrition

Good crop management increases the potential of the variety. Plant nutrition is one of the key factors for the development of the typical fruit quality (^{Fischer and Álvarez, 2008}), and due to its effect on the growth it highly influences the production and quality of the fruit (^{Aular et al., 2014}). Important practices can be lead to promote the development and quality of the fruit in purple passion fruit crop. For example, around 70 to 80 g of fertilizer 10-20-20 (NPK) should be applied seven times between 200 and 295 d after sowing (^{Jiménez et al., 2012}).

The absorption of nutrients increases at the beginning of the reproductive phase, for example in yellow passion fruit, the fertilizer demand increases at 250 to 280 d after transplanting, when the plants begin to grow exponentially. In this phenological stage, the absorption of nutrients such as nitrogen (N), potassium (K) and calcium (Ca) and the micronutrients rises, especially manganese (Mn) and iron (Fe) (^{Borges and Lima, 2007}). In addition, the same authors reported that temperatures below 18°C decrease passion fruit growth which, consequently, reduces nutrient absorption and fruit production.

In order to understand the influence of N on yellow passion fruit, ^{Borges et al. (2006)} applied two sources, urea and calcium nitrate, in five doses (0 to 800 kg ha^-1) and found the maximum fruit yield (34.3 t ha^-1) with the application of 457 kg ha^-1 of N in the form of urea, without influencing the characteristics of the fruit and the quality of the juice.

^{Freitas et al. (2006)} studied the deficiencies of macronutrients and boron (B) in yellow passion fruit and found that the lack of Mg, N, phosphorus (P) and sulfur (S) in the nutrient solution caused the lowest number of fruits per plant (0, 2, 3 and 4, respectively), compared to the control (10 fruits). The authors also found that TSS were lower in fruits deficient in N, P and K, and the content of ascorbic acid decreased with the lack of N, K and S in the nutrient solution.

With different levels of K in the nutrient solution, ^{Araújo et al. (2006)} found that 6 mmol L^-1 of K produced fruits of greater weight and yield/plant, while the thickness and relative water content of the pericarp as well as the concentration of vitamin C increased with the dose of K (from 0 to 8 mmol L^-1). Also, the increase in K concentration to 8 mmol L^-1 shortened the time to fruit maturity by around 25 d (Araújo et al., 2005).

Passion fruits are notable for their high content of mineral nutrients. ^{Martin and Nakasone (1970)} reported higher contents of Ca and P (measured in 100 g of fresh weight) in purple passion fruit (14 g and 41 mg, respectively), while sweet granadilla excelled in Fe (0.8 mg), but yellow passion fruit and banana passion fruit presented low Ca contents (4 g).

Water and irrigation

In yellow passion fruit cultivated in the semi-arid region of Paraíba (Brazil) and irrigated with 133% of the crop evapotranspiration (Eto), gas exchange rates were higher in the 'BRS Sol do Cerrado' genotype, in addition to fruit production with a higher market classification, compared to 'BRS Gigante Amarelo' which was more prone to develop in conditions of low water availability due to its lower stomatal conductance (^{Melo et al., 2014}). In the same semi-arid region, ^{Suassuna et al. (2011)} found in the yellow passion fruit hybrid IAC 273/277 that the irrigation level at 120% of ETo promoted a greater proportion of fruits with fresh weights higher than 150 g, an increase in juice yield and a higher percentage of skin compared to lower and higher levels of irrigation.

A symptom of severe deterioration is the cracking of the passion fruits due to possible effects such as higher water influx to organs, drastic change between night and daytime temperature and/or lack of B, Ca, K or Mg (^{Rivera et al., 2002}; ^{Fischer et al., 2009}; ^{Parra-Coronado and Miranda, 2016}), which is observed especially in sweet granadilla and banana passion fruit.

Pruning

Regarding pruning, growing yellow passion fruits with a different number of reproductive branches (40, 30, 24, 20 and 14 branches/plant) evidenced that a smaller number of tertiary branches decreased production (number of fruits/ plant) and productivity (kg ha^-1 of fruits) and juice yield, but increased the average fruit weight without modifying the internal characteristics of organs (^{Hafle et al., 2009}). According to ^{Weber et al. (2017)}, fruit weight accumulation includes competition for compounds produced by Fischer, Melgarejo, and Cutler: Pre-harvest factors that influence the quality of passion photosynthesis, and a lower fruit number increases the available assimilates for fruit filling.

Grafting

In different combinations of yellow passion fruits in Viçosa-MG (Brazil) grafted on two wild species (P. gibertti and P. mucronata),^{Salazar et al. (2016)} observed significant correlations in fruits for ascorbic acid, brightness values, chroma and angle Hue. However, the content of β-carotene in the fruit did not show significant differences, which indicates that the two rootstocks did not influence this compound; nevertheless, there was a decrease in the ascorbic acid content, compared to non-grafted plants. The results indicate the potential use of wild rootstocks due to their positive effects on grafted plants, while maintaining the commercial quality of the fruits.

Pollination

^{Akamine and Girolami (1959)} reported that the fruit set, the number of seeds, the weight of the fruit and the fruit yield depend on the amount of pollen deposited on the stigma. Seed development is directly correlated to the juice content (^{Knight and Winters, 1962}). The Passifloraceae species are commonly pollinated by bumblebees, especially by Xylocopa sp. (^{Miranda, 2012}) and also by Centris sp., Epicharis sp., Eulaema sp., Bombus sp. and Ptiloglossa sp. (^{Schotsmans and Fischer, 2011}). In the allogamous yellow passion fruit, artificial pollination is very common, achieving a fruit set of 80% (^{Cleves et al., 2012}). ^{Rodriguez-Amaya (2003)} reports that manual pollination will produce larger and more succulent fruits.

Phytosanitary status

Bacteria affecting quality are: Xanthomonas axonopodis pv. passiflorae causing dark brownish green spot lesions (^{Castilho and Granada, 1995}) and Pseudomonas syringae pv. passiflorae causing small green spots that develop into golden brown sticky necrotic lesions (^{Fischer and Rezende, 2008}). The following fungi are causal agents affecting quality: Fusarium oxyporum f. sp. passiflorae causes a pale beige color in fruits (Fischer and Rezende, 2008), Phyto-phtera sp. causes gray spots (^{Varón de Agudelo, 1993}), Colletotrichum gloeosporioides induces lesions on fruit skin that become corky and brown, Alternaria passiflorae causes browning, and Septoria sp. causes blotch. Of the viruses found in passion fruit, Cowpea-aphid borne mosaic virus (CaBMV) causes fruit deformation, East Asian Passiflora virus (EAPV) induces fading in fruit color, Passion fruit vein clearing virus (PVCV) reduces fruit size (^{Kitajima et al. 1986}), Passion fruit green spot virus (PGSV) causes green spots on yellow passion fruit (Kitajima et al., 2003), fruit: A review 221 and Passion fruit mottle virus (PaMV) induces fruit skin mottling (Fischer and Rezende, 2008).

Fruit ripening and quality

Ripening can be defined as the integration of external and internal changes, including the taste and texture that a fruit provides when it completes its growth (^{Agustí, 2004}). The cultivated passion fruits are climacteric (Hernández and ^{Fischer, 2009}); it means that berries growth and development take place while attached to the plant or after the harvesting process, depending on the state of fruit development.

In two sweet granadilla plantations in the municipalities of Santa María and La Argentina in the province of Huila (Colombia), ^{Espinosa et al. (2015)} grouped the fruits into four stages of maturity, recording the change in color, the increase in TSS (Brix degrees) and maturity index (TSS/ TTA), and the decrease in total titratable acidity (TTA) (Tab. 3). Since the color change of the epidermis during the maturation of the passion fruit is the most notable characteristic (^{Schotsmans and Fischer, 2011}), the change of the passion fruit from green to yellow is due to the degradation of chlorophyll and the production of new pigments, mainly carotenoids, which generate the yellow to red coloration of the tissues (^{Valero and Serrano, 2010}).

TABLE 3 Development of sweet granadilla fruit quality grouped into four stages of maturity. 

daa - days after anthesis. Photos: D.D. ^{Espinosa. Table and photos with permission from Espinosa et al. (2015)} and Universidad Nacional de Colombia, Bogotá.

Similar results were obtained by ^{Pinzón et al. (2007)} for purple passion fruit, only differing in the purple skin color and the maturity index (MI). The purple passion fruit retains a higher content of TTA at the consumption ripeness, recording a MI of 4.14 (with a TTA of 3.92), regardless of the higher concentration of TSS (16.21), compared to 13.1 of the sweet granadilla (Tab. 2). After analyzing the stages immature (I), color change (breaker) (II) and mature (III) for purple passion fruits, ^{Jiménez et al. (2011)} found an increase of the TSS from 13.5 to 17.4, a decrease in the TTA from 4.68 to 2.51 and an increase in the concentration of anthocyanin, between stage II and III, from 0.45 to 1.73 g cy-3glu equiv./kg fruit.

The maturity index (TSS/TTA), which is the balance between sugars and acids giving the characteristic flavor to the fruit (^{Flórez et al., 2012}), is a parameter stated to identify the maturity of passion fruit. For example, in the case of purple passion fruit, the consumption quality improves mainly due to the decrease in acidity (^{Shiomi et al., 1996a}). In several sensory tests, it has been found that acidity masks the sensation of sweetness and as the acidity decreases due to the reduction of TTA during post-harvest, the sweetness is evident (^{Schotsmans and Fischer, 2011}).

In relation to ascorbic acid, ^{Patel et al. (2014)} recorded the maturity of the purple and yellow passion fruits to contain the highest content (48.75 mg 100 mL^-1) of this antioxidant, produced in purple passion fruit (var. Megha Purple) at the end of maturation (90 d), while in yellow passion fruit (var. Kerala Yellow) the highest ascorbic acid concentration (28.4 mg 100 mL^-1) is produced until 83 d and then decreases. The reduction of ascorbic acid in the final stage of fruit ripening was attributed by these authors to the oxidation of L-ascorbic acid to dehydro-ascorbic acid during the metabolic process.

^{Pongener et al. (2014)} reported for purple passion fruit that the quality attributes of these fruits were better when they were harvested after the breaker state in which the fruits had developed 50% of their purple coloration (Tab. 4). The ethylene evolution rate increased almost 8.15 times the value with maximum levels of 505.35 μL kg^-1 h^-1 of C₂H₄ in fruits harvested in the color change (breaker) state. The changes in the color values L*, a* and b* indicated an optimal color development only in harvested fruits after 50% of its coloring. These authors concluded that the purple passion fruit should be harvested only after 50% of coloring on its fruit surface, for an optimal storage, appropriate ripening and development of flavor and quality.

TABLE 4 Recommended harvest indices for different passion fruit crops. 

In contrast, ^{Shiomi et al. (1996b)}, in an experimental orchard of purple passion fruit in Kenya, observed that harvested fruits at 70 d after flowering (daf; "ripe" green stage), showed characteristics almost similar to the more developed fruits (80 and 90 daf). If the color can develop normally after the application of exogenous ethylene in post-harvest, it should be possible to harvest the purple passion fruit in a stage of "ripe" green or in the change from green to purple (breaker). This is much earlier than the usual maturity of the harvest and would give the product a good export quality, with a longer shelf life when marketed and transported abroad. Shiomi et al. (1996a) reported that the application of ethylene in post-harvest of the purple passion fruit should be at least 1 d after harvesting, given that the ethylene biosynthesis regulated mainly by the activity of the ACC synthase could change its sensitivity after the harvest when the fruit is ripening.

^{Flórez et al. (2012)} harvested purple passion fruits in different ripening stages, from physiological (100% green) to mature (100% purple), registering in all of these a peak of ethylene production on day 18 of post-harvest. The fruits harvested in the states 70% (30% green, 70% purple) and 100% purple presented the highest ethylene production rate. In addition, these authors found that the climacteric peak (of respiration) preceded the ethylene production, which confirms the hypothesis that this hormone is not responsible for the respiratory increase in the purple passion fruits, which, in the 100% state, obtained the maximum CO₂ production.

^{Vianna-Silva et al. (2010)} found a different behavior in yellow passion fruit, as fruits ripen differently depending on whether they are attached to the plant or have already been removed from it. Fruits delayed their coloration and decreased the thickness of the epidermis, compared with fruits of the same age already stored. The same authors stated that the optimum harvest time is 63 d after anthesis (daa), while when harvested at 54 daa fruits had 21% less juice yield.