| POSTHARVEST BIOLOGY AND TECHNOLOGY
HORTSCIENCE 51(9):1127–1133. 2016. doi: 10.21273/HORTSCI10883-16 of S. muricatum. Most importantly, these authors confirmed that the center of origin Solanum and diversity of pepino is Northern Ecuador/ A Review of Pepino ( Southern Colombia, and that pepino is closely related to species of the Caripensia muricatum Aiton) Fruit: A series (Blanca et al., 2007). Pepinos have been commercially and Quality Perspective experimentally grown in several countries, including Australia (El-Zeftawi et al., 1988), Carolina Contreras, Mauricio Gonzalez-Ag uero,€ and Bruno G. Defilippi1 Chile (Bravo and Arias, 1983), Colombia Instituto de Investigaciones Agropecuarias, INIA-La Platina, Unidad de (Ruiz and Nuez, 1997), Peru, Ecuador (Bravo Postcosecha, Santa Rosa 11610, Santiago, Chile and Arias, 1983), Israel (Levy et al., 2006; Schaffer et al., 1989), New Zealand (Heyes Additional index words. Solanaceae, quality, breeding, storage potential, climacteric, flavor et al., 1994; Redgwell and Turner, 1986), Abstract Turkey (Kola et al., 2015), United States . Many attempts have been made to introduce pepinos in several countries. These (Ahumada and Cantwell, 1996), and Spain efforts have involved breeding programs designed to adapt pepino plants to the respective (Rodríguez-Burruezo et al., 2004b, 2011; climates and consumer preferences. However, low yields and the relatively small amount of Ruiz and Nuez, 1997; Ruiz et al., 1997), information on the crop have played a negative role for the expansion of the pepino. where cultivars have been developed for Information on other features of the fruit (e.g., quality, physiology, and sensory attributes) is a Mediterranean climate. also scarce. Only a few studies provide useful data on pepino handling and storage potential; For Chile, the cultivated surface is un- hence, there is not an adequate postharvest strategy to store this species. The objective of known, but the latest census data on planted this review is to provide and discuss the available literature, with an emphasis on farms reported 634 ha of pepino with the postharvest physiology aspects, and present 1) breeding for quality and how this has led specific geographic area for this crop in the to the development of the cultivars known today, 2) fruit physiology and quality, 3) handling IV Region of Coquimbo (North of Chile) and physiological disorders of pepino, and 4) highlight challenges for future research. (ODEPA, Census of Agriculture, 2007). Production is mainly destined for the do- mestic market, and no export records are The pepino (Solanum muricatum Aiton), (Rodríguez-Burruezo et al., 2011). Unfortu- kept. There are currently no registered which is also referred to as pepino dulce in nately, pepino studies in the area of origin are cultivars in Chile, although characteristic Spanish, has been described as a succulent, scarce, and some reasons may lie in the fact that types are distinguished by fruit characteris- juicy, and sweet fruit that is used mainly in pepino is classified as a secondary fruit (Lizana tics and/or by regions where pepinos are desserts, although some cultivars have been and Levano, 1977), exotic or nontraditional grown (Bravo and Arias, 1983). In general, used in salads due to their higher acidity crop, it has a low cultivated surface leading to clonal propagation by cuttings is the only content and grassy flavor notes (Rodríguez- reduced product availability in markets, and an mean of reproduction. This is also recom- Burruezo et al., 2004a, 2011). In the 1990s, insignificant economic importance relative to mended for the cultivars released by Spain pepino was proposed as a physiological other major crops. and other breeding programs, where each model of the texture or firmness changes that The aim of the present review is to cultivar must be vegetatively propagated by occur during maturation and ripening (Heyes critically summarize information of past stem cuttings to maintain the characteristics et al., 1994), and in recent years, research has and recent years on pepino breeding and (Prohens et al., 2002; Rodríguez-Burruezo focused on genetic improvement of fruit postharvest physiology. In particular, re- et al., 2004b). Although the plant is a pe- quality (Levy et al., 2006; Rodríguez- search experiences about storage potential rennial shrub, it is grown annually due to Burruezo et al., 2004b, 2011). The pepino and quality are discussed. its frost sensitivity. Additionally, the plant fruit is a diploid (2n = 24) subtropical species is moderately tolerant to salinity (Ruiz and and is also known as melon pear, melon Nuez, 1997) and grows well under poor shrub, or sweet cucumber. Native species Pepino Crop soil conditions (Bravo and Arias, 1983) from South America, more specifically from The first documented use of S. murica- (Fig. 2). However, pepino plants are sen- the Andes area of Peru and Chile, is widely tum is cited on pre-Inca ceramics displaying sitive to high temperatures, particularly distributed from Colombia to Bolivia (Daunay images of the fruit that date to at least 2000 during pollination and fruit setting (Burge, et al., 1995) (Fig. 1). The pepino fruit served as years ago (Anderson et al., 1996). These 1989). an important crop in Pre-Columbian Andean authors also found that several unique hap- One of the main problems of pepino fruit cultures, and it is a member of the Solanaceae lotypes come from Colombia, suggesting is its low organoleptic quality, which does family, which includes several important crops, that Colombia is the center of origin, based not meet consumer standards as a result such as tomatoes (S. lycopersicum), potatoes on the presumption that diversity is associ- of poor handling and inadequate storage (S. tuberosum), and eggplants (S. melongena) ated with the genetic origin. Therefore, treatments (Huyskens-Keil et al., 2001; among others (Prohens et al., 1996). Of the Anderson et al. (1996) hypothesized that Rodríguez-Burruezo et al., 2011). Very few 1500 species described in the Solanum although the progenitor(s) is/are likely ex- studies report harvest indices. For example, genus (Weese and Bohs, 2007), pepino is tinct, the closest wild ancestors are Solanum El-Zeftawi et al. (1988) recommend that one of the few that is domesticated and caripense and Solanum tabanoense because pepinos should be golden yellow in color, cultivated for food purposes (Daunay et al., they are also found in Colombia and are both with a firmness of 2 kg·cm–2, 40% juice, and 1995). haplotype-associated with S. muricatum. 9 Brix. Today, consumers are more informed Interestingly, most pepino research has been Later, Blanca et al. (2007), by taking advan- and interested in the consumption of exotic conducted in New Zealand, Spain, and Israel tage of more sophisticated genetic tools, fruits of high nutritional value (Rodríguez- through their respective breeding programs concluded that S. muricatum is a compli- Burruezo et al., 2011). For example, pepino is cated cultigen and suggested that several described as a fruit with high water content wild species contributed to its origins and (92% fresh weight) and with excellent anti- Received for publication 22 Apr. 2016. Accepted evolution. Part of the haplotype richness of oxidant properties; therefore, pepino is rec- for publication 22 July 2016. the pepino may be attributed to hybridiza- ommended for diabetic and sugar-free diets We gratefully acknowledge the financial support of tions that occurred at several places and due to its low sugar content. Thus, pepino CONICYT-Chile (Fondecyt project 3150082). times, and to a lack of genetic and geographic has a great potential for use as a natu- 1Corresponding author. E-mail: bdefi[email protected]. barriers between cultivated and wild species ral antioxidant and beyond its nutritional
HORTSCIENCE VOL. 51(9) SEPTEMBER 2016 1127 the early 1990s (Ruiz et al., 1992). As a result, into relatively high amplified fragment length two commercial pepino cultivars for the polymorphism (AFLP)-estimated genetic dis- Mediterranean climate, ‘Sweet Long’ and tance and high heterozygosity (Rodríguez- ‘Sweet Round’, were developed as clone Burruezo et al., 2011). In other countries, such selections from seeds from northern and cen- as Israel, lesser-known cultivars have been tral Chilean accessions (Ruiz et al., 1997). developed. The breeding program in Israel Both cultivars were commercially cultivated in released the following cultivars Pepo (the most Spain, and their fruit were exported to several widely cultivated cultivar in Israel), Becky, European countries. Thereafter, through the Rosy, Hannah, Nitza, and Tally (Levy et al., same breeding program, Spain selected hy- 2006). Although this program is not as exten- brids with elevated levels of ascorbic acid, sive as the Spanish breeding program, the high firmness for increased resistance to bruis- authors confirmed an improvement in quality ing, round to ovoid fruit shapes (Prohens and traits (flavor and appearance) by breeding. Fig. 1. Pepino fruit at three different maturity Nuez, 1999), a crispy texture, and low sugar Noteworthy, the authors found no correlation stages. Green (top), white (center), and yellow content for use in salads, as in the case of cv. between high SSC and flavor acceptance. Other (bottom) ground color. Puzol (Prohens et al., 2002). pepino cultivars mentioned in the literature are Other breeding studies have indicated that listed in Table 1; unfortunately, the breeding pepino presents high genotypic variation, programs for some cultivars are unknown or confirming that the pepino is a highly vari- not mentioned. Other pepino cultivars that able species. In addition, dramatic pheno- are briefly mentioned in the literature include typic variations exist among pepino cultivars ‘Lincoln Long’, ‘Golden Litestripe’, ‘Schmidt’ and ecotypes. Contrary to tomatoes, this (Prohens et al., 1996), ‘Lima’, ‘Otavalo’, and phenotypic variation is correlated with a high ‘Quito’ (Prohens et al., 2002). variation at the molecular level, as demon- As for Chile, Munoz~ et al. (2014) recently strated by phylogeny studies (Anderson et al., reported a study based on the physiological 1996; Rodríguez-Burruezo et al., 2003). fruit traits of 14 different Chilean ecotypes Rodríguez-Burruezo et al. (2002) studied 26 and found a moderate genetic variability in different pepino clones and their quality pa- these seed-propagated selections. Most of the rameters under autumn–winter and spring– genetic variability among the ecotypes was summer conditions. The authors found that related to fruit length, shape, mass, pulp under autumn–winter conditions, the fruit firmness, and SSC. Recently, Herraiz et al. mass was genetically correlated with soluble (2015a), in the Spanish breeding program, solids concentration (SSC) and ascorbic acid evaluated 58 morphological traits, using 14 levels, and that during spring–summer condi- pepino accessions (local Andean varieties tions, yield, SSC, and titratable acidity (TA) and modern cultivars) and 8 wild relatives. were all correlated. The genotypic variation High genetic diversity was found for both the found in these traits provided further possi- cultivated and wild accessions. Fifty-five of bilities for selecting pepino materials adapted the 58 traits were found to be variable, and to a Mediterranean climate as part of the only 3 were not found to vary (fruit with breeding objectives of Spain. Autumn– stripes, 2 locules inside the fruit, and seeds winter clones were more adapted to cold with no wings). Interestingly, local varieties Fig. 2. Pepino field located in Ovalle, northern conditions giving higher yields and fruit originating from Chile are clustered closer to Chile (top). Developing pepino fruits (bottom). quality (Rodríguez-Burruezo et al., 2002). In the modern varieties developed in Spain regard to other traits (e.g., aroma), Rodríguez- (Herraiz et al., 2015a). Burruezo et al. (2004a) studied 10 different potential (Redgwell and Turner, 1986; Sudha clones (4 parents with different flavors and Postharvest Physiology of Pepino Fruit et al., 2012). 6 clone hybrids selected from segregating crossings among these parents) and con- The pepino fruit has been described as Breeding for Quality cluded that a major fraction of volatiles is a berry that develops on a cymose inflores- inheritable, thus demonstrating that aroma cence (Gould et al., 1990). The fruit presents In the 1990s, in their study on Solanum constitutes an important breeding trait. A a simple sigmoid growth curve, and its species, Daunay et al. (1995) suggested that strong relationship was found between the maximum fruit size is reached 60 d some South American fruit species such as parents and hybrids for the concentration of after anthesis, corresponding to morpho- the pepino may be worth investigating as individual volatiles. The cultivar Valencia is logical stage 8 according to the BBCH potential ‘‘new’’ species for inclusion in the one of the most prominent breeding selec- (Biologische Bundesanstalt, Bundessortenamt European market. The authors noted a need tions due to its quality characteristics such as und CHemische Industrie) numerical scale of a breeding program for the adaptation of high SSC content, vigor, high yield, intense (Herraiz et al., 2015b), at which point the organoleptic requirements and agroclimatic yellow flesh, and early ripe fruit compared maximum sugar accumulation is also reached conditions. Since then, several attempts to with other cultivars (Rodríguez-Burruezo (Schaffer et al., 1989). The fruit takes be- introduce pepinos into other markets have been et al., 2004b). Later, the cultivar Turia was tween 30 and 60 d to grow to full size, after made with modest success. Possible reasons for released as the result of an intraspecific breed- which, depending on the cv., can take between this limited use of pepinos include high sensi- ing program, and this new cultivar was de- 7 and 25 d to fully ripen (Prohens and Nuez, tivity of fruit set to environmental conditions, veloped for use in salads, unlike the Valencia 2001). Pepino fruit has been considered non- especially to high temperatures, which affects cultivar, which was developed for use in des- starchy and a sucrose accumulator (S anchez its pollen viability; poor fruit quality (ripening serts (Prohens et al., 2005). The breeding et al., 2000). Slightly more than 50% of the is highly affected by temperature); the time program conducted in Spain was mainly fo- sweetness of pepino is attributed to its sucrose required for fruit ripening; plant propagation; cused on quality (sweetness and aroma) and content, which increases dramatically during and a lack of exploration of its high degree of nutritional value (ascorbic acid content), and maturation (Kola et al., 2015; Redgwell and genetic diversity (Prohens et al., 1996). involved the use of a wide variety of genetic Turner, 1986; S anchez et al., 2000). The A first attempt to introduce the pepino resources, clonal hybrids, and the introgres- average soluble solids content values re- fruit to a new market was made by Spain in sion of genes of wild species, which translated ported by Redgwell and Turner (1986) and
1128 HORTSCIENCE VOL. 51(9) SEPTEMBER 2016 Table 1. Registered pepino cultivars documented in various research sources. Pepino cultivar Parameters studied Reference Golden Spendour Maturity indices El-Zeftawi et al. (1988) El Camino Chemical position of fruit Redgwell and Turner (1986) Textural changes Heyes et al. (1994) Bruise resistance Gould et al. (1990) Aroma profile Shiota et al. (1988) Suma Storage potential Ahumada and Cantwell (1996) Bruise resistance Gould et al. (1990) Aroma profile Shiota et al. (1988) Colossal Commercially produced in the United States Ahumada and Cantwell (1996) Miski Prolific Commercially produced in the United States Ahumada and Cantwell (1996) Toma Storage potential Ahumada and Cantwell (1996) Sweet round Spain breeding program Ruiz et al. (1997) Carbohydrate content S anchez et al. (2000) Aroma profile Ruiz-Bevi a et al. (2002) Sweet Long Spain breeding program Ruiz et al. (1997) Carbohydrate content S anchez et al. (2000) Storage potential Martínez-Romero et al. (2003) Aroma profile Ruiz-Bevi a et al. (2002) Golden Globe Storage potential under CA Huyskens-Keil et al. (2006) Kawi Aroma profile Shiota et al. (1988) Puzol Spain breeding program Prohens et al. (2002) Cultivar developed for salad Parthenocarpy Valencia Spain breeding program Rodríguez-Burruezo et al. (2004a) High SSC, good fruit quality Cultivar developed for dessert Turia Spain breeding program Prohens et al. (2005) Cultivar developed for salad Pepo Israel breeding program Levy et al. (2006) Cultivar developed for dessert Becky Israel breeding program Levy et al. (2006) Small fruits, ‘‘cherry pepinos’’ Little flavor Rosy Israel breeding program Levy et al. (2006) High yield, little flavor Hannah Israel breeding program Levy et al. (2006) Medium size fruit, high SSC, ‘‘apricot’’ flavor Nitza Israel breeding program Levy et al. (2006) Large fruit, medium SSC, ‘‘banana’’-like aroma Tally Israel breeding program Levy et al. (2006) Large fruit, apple-like texture
El-Zeftawi et al. (1988) range between 7.8% than late crops, and the inverse is true for pattern in the cv. Toma. Interestingly, El- and 9.6%, and even lower values were re- sugars. Organic acids are almost exclusively Zeftawi et al. (1988) applied ethephon in ported by S anchez et al. (2000), ranging represented by citric acid, which accounts for pepinos cv. Golden Spendour and concluded between 5.2% and 8.6%. Once pepinos reach 91% of the total nonvolatile organic acids that pepinos require high concentrations of near 9% on the plant (6 to 3 weeks before found in the fruit. Kola et al. (2015) reported ethylene to stimulate ripening, likely with harvest), the soluble solids content stays low in pepino cv. Miski that the citric acid content a small increase in respiration. Likewise, the constant. Coincident with the literature, our increased by 25% in ripe fruit compared with authors showed that ethylene application to data also showed a rather low content of immature fruit. In addition, pepino contains pepino triggered a change in color and fruit sugars reaching a maximum of 9% during vitamin C at higher levels (48–68.8 mg/100 g softening. Heyes et al. (1994) argue that ‘‘this different developmental stages, and for fruit fresh tissue) than normally found in most was interpreted to suggest that pepinos are stored at 20 C (data not shown). Our fruit fruits (including citrus fruits) (Redgwell and climacteric but other workers dispute this.’’ were collected between January and Mar. Turner, 1986). Their data supported the conclusion that the 2015 from a commercial orchard located in The first sign of pepino ripening is the pepino should be classified as a nonclimacteric Ovalle (30 33#22.854$S71 38#43.004$W, appearance of purple strips. Conclusions on fruit. Lizana and Levano (1977) reported north of Chile). the climacteric (an increase or not in respira- a climacteric for pepinos with respiratory Therefore, the fruit must be picked at or tion during ripening classifies fruit as climac- values ranging from 12.2 to 48.6 mg close to the desired stage of consumption teric or nonclimacteric) of the pepino are not CO2/kg/hr; however, ethylene production because of its failure to improve flavor after yet conclusive. The fruit has been described was not measured. picking (S anchez et al., 2000). Glucose and as both nonclimacteric (Ahumada and Cantwell, Ethylene and respiratory rates were mea- fructose are also present in pepino, represent- 1996; Harman et al., 1986; Heyes et al., 1994) sured in pepino fruits at different conditions: ing 28% and 18% of total sugars, respectively and climacteric (Lizana and Levano, 1977). 1) during different phenological stages of (Redgwell and Turner, 1986), but compara- Heyes et al. (1994) reported accelerated color development, from 10 d after fruit set until tively they increase less than sucrose development and fruit softening when using senescence; 2) commercial harvest maturity (Huyskens-Keil et al., 2006; Schaffer et al., propylene; however, ethylene production did fruit stored a 7 C for 14 d and then at 20 C; 1989). S anchez et al. (2000) found an inverse not increase, and a transient respiratory rate and 3) commercial harvest maturity fruit relationship between water content and was present. Ahumada and Cantwell (1996) stored at 20 C for 16 d. In all cases, fruit sugars that is highly dependent on environ- reported very low ethylene production rates showed a moderate increase in autocatalytic mental conditions. The authors found that (only >0.4 mL·kg–1·h–1 in fruit with severe ethylene after 65 d of development, and for early crops always had higher water content decay) and lack of a climacteric respiratory storage after 10 d at 7 C and after 5 d when
HORTSCIENCE VOL. 51(9) SEPTEMBER 2016 1129 stored at 20 C (Fig. 3). The CO2 rate stayed volatile compounds (Dimick and Hoskin, alcohols; however, the authors only quantified rather constant the same day of the ethylene 1982), a tomato produces close to 400 volatiles the four compounds listed above and did not autocatalytic burst, and a modest respiratory (Buttery, 1993), and a strawberry 360 vola- mention the total volatile emissions from the peak appeared when stored at 20 C. How- tiles (McFadden et al., 1965). These volatile fruit peel. Rodríguez-Burruezo et al. (2004a) ever, additionally, we studied three different chemicals fall into several categories includ- studied the odor-contributing volatiles (OCVs) stages of maturity and no respiratory peak or ing terpenes, esters, aldehydes, alcohols, and of 10 different pepino clones by GC- autocatalytic burst was detected in any fruit ketones. Esters, aldehydes, and alcohols are olfactometry-MS analyses. Of the more than (data not shown). These data coincide with considered the most important aromatic per- 50 volatile compounds found in the aroma the respiratory behavior that Kader (2002) ception for fresh fruits (Paliyath and Murr, profile, 17 were found to contribute signifi- classified pepino: a nonclimacteric fruit with 2008). The ripeness of the fruit will determine cantly to pepino aroma (OCVs). The authors a moderate production of CO2 (10–20 mg the level and type of the defined aroma classified these into three groups: fruity/fresh CO2/kg/h) and low C2H4 production (0.1–10 compounds emitted by the fruit. (acetates and prenol), green (C6 and C9 mLC2H4/kg/h). The aroma of a pepino fruit has been aldehydes), and exotic (lactones, mesifuran, Perhaps, physiological behavior varies described as green, fresh, and reminiscent of and b-damascenone). Rodríguez-Burruezo with the cultivar, that is, some pepino cultivars melon and mango fruit (Shiota et al., 1988). A et al. (2004b) quantified aroma compounds in are climacteric and others nonclimacteric. This ripe pepino has a scent reminiscent of a canta- cv. Valencia and found fruity notes from the 3- variable ripening behavior has been exten- loupe melon, but when it is not fully ripe, it has methyl-3-buten-yl acetate and 3-methyl-2- sively documented in other species, such as a cucumber-like scent (S anchez et al., 2000). buen-yl acetate esters to be the most abundant. Asian pear, pepper, and tomato- rin and nor The main volatile components identified in The authors also found grassy notes of C6 mutants (Grierson, 2013; Obando-Ulloa et al., pepino were 3-methyl-2-buten-1-ol (a.k.a. pre- compounds to be mainly derived from trans-2- 2008; Watkins, 2002). nol), 3-methyl-3-buten-1-ol, and their respec- hexenal, and C9 compounds from 2,6-non- tive acetates, butyl acetate and (Z)-6-non-1-ol adienal and (E)-2-nonenal. Rodríguez-Burruezo Fruit Quality (Shiota et al., 1988). Interestingly, C9 com- et al. (2011) also identified 17 OCVs and pounds that have only been described in reported 3-methylbut-2-en-1-yl acetate and Aroma. Aroma is defined as the odor of cucurbit species (Matsui et al., 2006) have 3-methylbut-3-en-1-yl acetate as the main a food product (Meilgaard et al., 2007). The also been found in pepino, and include non- compounds of fruity pepino selections, along odor of a product is detected when volatiles anol, (Z)-6-nonenol, (Z)-6-nonenal, 2-nonanone, with ‘‘exotic’’ notes such as b-damascenone, enter the nasal passage (voluntarily or in- nonyl acetate, and (Z)-6-nonen-1-yl acetate. lactones, and mesifuran. For the green/vegetable voluntarily) and are perceived by the olfac- These C9 compounds undoubtedly account aromas found for the other selections, pre- tory system, whereas ‘‘aromatics are the for the melon and cucumber-like fruit notes dominant volatiles included aldehydes, such volatiles perceived by the olfactory system of pepino (Shiota et al., 1988). These authors as hexanal and trans-2-hexenal, and several from a substance in the mouth’’ (Meilgaard detected at least 35 different volatiles in the C9 compounds or nonenals. et al., 2007). Aroma is a critical component of flesh of ‘El Camino’, ‘Suma’, and ‘Kawi’, Among the few studies conducted on the perceived quality (Kader, 2002; Paliyath and where the cv. Suma showed the greater sensory field, Ruiz and Nuez (1997) per- Murr, 2008; Wills et al., 2007). The quality of amount of saturated and unsaturated C9 formed an organoleptic test on different a fruit is defined as the set of internal and compounds, ‘Kawi’ the lowest level of total pepino clones after nutrition (focused on K+ external features inherent to the fruit, thus volatiles, and ‘El Camino’ showed the most among other nutrients) and salinity treat- determining consumer acceptability (Paliyath pleasant aroma as it was found to include ments. The sensory test showed that such and Murr, 2008). These characteristics, which more unsaturated esters (Shiota et al., 1988). treatments did not significantly affect aroma are also known as ‘‘quality criteria’’ for the Other authors have reported changes in vola- and that flavor was significantly improved as consumer include appearance (internal and/or tiles associated with different ripening stages. a result of an increased concentration of external defects, size, color, and shape), tex- For example, a change during ripening from soluble solids. ture, nutritional value, safety (Kader, 2002), 3-methyl-2-buten-1-ol and 3-methyl-3-buten- Color. Often mentioned as the main qual- and taste (Wills et al., 2007). 1-ol to their respective acetates has been found, ity criterion of the ripening stage, this char- Aroma is a complex attribute to study due to increasing the aroma in the ripe fruits (S anchez acter has been reported as an excellent the use of sensations that are translated into et al., 2000). Ruiz-Bevi a et al. (2002) also harvest index for pepino (El-Zeftawi et al., standard vocabulary, and the existence of a wide showed that 3-methyl-2-buten-1-ol was the 1988; Lizana and Levano, 1977). Although variety of volatiles. About 17,000 different main volatile compound in pulp tissue, fol- both ground and cover color (stripes) are used types of odors are known, of which a trained lowed by 3-methyl-3-buten-1-ol, and their re- for harvesting purposes, ground color serves person can detect 150–200 (Meilgaard et al., spective acetates. Interestingly, fruit peel as a more robust index due to the strong 2007). For example, an apple produces 270 samples showed low amounts of acetate and pigmentation that the purple stripes undergo
Fig. 3. Ethylene and respiratory patterns for pepino fruit during (A) developmental stages up to 65 d after fruit set, (B) storage at 7 C for 14 d and at 20 C for 10 d, and (C) storage at 20 C for 16 d. For (B) and (C), each point represents the mean of 10 fruits of stage of maturity green ground color. Fruit were measured every 2 d under a static system.
1130 HORTSCIENCE VOL. 51(9) SEPTEMBER 2016 under direct or indirect sunlight (Lizana and Lizana and Levano (1977) reported a dra- inedible soft fruit. Temperatures of 1 and Levano, 1977). Fruit harvest is carried out matic loss in firmness after 30 d of storage, 3 C favored superficial injury (similar to when ground color is green or white (Fig. 1). finding values of 3 lb after 60 d of storage at superficial scald on apple and pears) with However, measuring pepino color has proven 5, 8, and 10 C. Three maturity stages were brown sunken spots that were usually iso- challenging as reported by Heyes et al. evaluated yellow (M1), green yellow (M2), lated, and 0.1 to 0.3 mm in depth. They found (1994). Variable ripening rates and the diffi- and green white (M3). All pepinos stored at 5, 8, and 10 C to be optimal temperatures for culty of a fully ‘‘objective’’ assessment of 20, 10, and 1 C showed a significant de- pepino storage. Another physiological disor- pepino maturity (areas free from purple crease during storage, especially during the der reported by Lizana and Levano (1977) stripes must be chosen), make subjective first 2 weeks (Martínez-Romero et al., 2003). was internal breakdown, characterized by the evaluation system of the whole fruit surface However, these authors found that for fruits browning of ripened fruit after prolonged by the naked eye more reliable than instru- stored at 10 C, the loss of firmness was lower cold storage. Ahumada and Cantwell (1996) mental measurements. than for those stored at 1 and 20 C at any studied pepino cv. Toma at different temper- Under storage conditions, significant dif- ripening stages, and the greatest firmness atures and maturity stages for four weeks, ferences in fruit color development have been losses were found at 1 C, likely as a conse- where the most successful temperature treat- found. When stored in air at 5, 8, and 10 C, quence of the CI. The beneficial effects of ment for all fruit maturities was 7.5–10 C. minor flesh color change was noted, but high CO2 concentrations in reducing fruit Less ripe fruits stored at <5 C were severely considerable variation was found for ground softening for mature pepinos are presumably damaged with external discoloration. Physi- color (Lizana and Levano, 1977). Similar due to the inhibition of cell wall–degrading ological disorders reported by Ahumada and findings were reported in pepino by Martínez- enzyme activities, e.g., PME and PG, as Cantwell (1996) included CI that caused Romero et al. (2003) after storage treatments. reported by Heyes et al. (1994). CA studies internal and external discoloration, and decay These authors studied the cv. Sweet Long showed that mature pepino fruits exhibited symptoms due to a dark brown rot starting at at three different maturity stages (green, light significantly higher firmness than ripe fruits the stem and eventually developing within green, and yellow green) stored at 1, 10, or under all tested CA storage conditions until the fruit pulp. Huyskens-Keil et al. (2000) 20 C. Martínez-Romero et al. (2003) found 14 d of storage (Huyskens-Keil et al., 2006). studied physiological changes in pepino at significant differences in the yellow green Plant nutrition levels have also been exam- 5 C and 18 C for three different maturity stage stored at 1 C, but no significant color ined as a factor that contributes to fruit stages, and concluded that changes in exter- differences were found in the green and light firmness. Ruiz and Nuez (1997) determined nal and internal quality only occurred up to green stages at different temperatures. They that nutrition treatments (focused on K+ 14 d of storage, thereafter pepino quality also reported changes in color due to external among other nutrients) did not significantly remained almost constant. Martínez- chilling injury (CI), where more than 9% of affect pepino fruit texture. Romero et al. (2003) studied pepino cv. the fruit turned brown in color after 28 d of Another parameter closely related to firm- Sweet Long to evaluate physiological storage. In contrast, for controlled atmo- ness is bruising. The propensity of pepino to changes under chilling and nonchilling tem- sphere (CA) storage conditions, Huyskens- show bruising after handling and transport peratures (1, 10, and 20 C) at three different Keil et al. (2006) reported that CO2 gas also has become a limiting factor in its maturities for 28 d. The fruit storage potential concentrations (5% O2 and 5, 15, or 20% commercial development (Gould et al., for the riper stage was 1–2 weeks, whereas CO2 at 5 and 10 C) inhibited undesired color 1990). Gould et al. (1990) documented that for the other fruit stored at 10 or 20 C, it was changes in mature and ripe pepinos for 21 and pepinos show a dark ‘‘waterlogged’’ or 4 and 3 weeks, respectively. Martínez- 14 d, respectively, i.e., the fruits maintained ‘‘soggy’’ area after compressive force. These Romero et al. (2003) also reported internal color, regardless of the atmospheric compo- authors studied two cultivars (Suma and El CI expressed as flesh translucency associated sition. This observation is consistent with Camino) and 16 selections of pepino, de- with internal browning. External CI was findings for various other commodities termining that softer fruit are more likely to observed as brown spots on the skin where (Kader, 2002), where high CO2 concentra- show bruise injury than a firmer fruit. Thus, the most susceptible fruit were the riper stage tions led to the retention of color intensity bruising increases as a fruit ripens. The Suma stored at 1 C. (Huyskens-Keil et al., 2006). cultivar was identified as the most susceptible Other studies that have involved storage Ambiguous results have been reported in to bruising, whereas El Camino fruit pre- technologies, such as film packaging, CA, reference to external treatments involving sented a moderate susceptibility. Bruising is and modified atmosphere (MA), have found ethylene. For instance, Ahumada and Cantwell associated with the size and compactness of that changes in gas concentrations improve (1996) found ethylene to accelerate external exocarp cells. For example, the ‘Suma’ fruit pepino fruit storability and quality as in the color development in low maturity fruit, possesses larger air pockets, providing little case of other fruits (Kader, 2002). Huyskens- whereas El-Zeftawi et al. (1988), using post- resistance to an applied load, whereas for Keil et al. (2001) studied the performance of harvest ethephon dipping, found little effect on resistant selections, air spaces are smaller, edible coating (sucrose ester) and film pack- fruit color. and the stress is dispersed over a larger aging (plastic food container) on pepino Texture. Firmness is considered one of the surface area, thus decreasing the average fruits stored at 5 and 20 C. Although both main quality attributes of fruits in terms of loading transmitted onto mesocarp cells postharvest treatments were successful, the consumer acceptability. In pepino, a loss of (Gould et al., 1990). For shipping purposes, film treatment had better effects on mass loss, firmness has been determined to result from pepinos are harvested at an early ripening prevented undesirable color changes and a progressive disassembling of the cell wall stage, because they are highly sensitive to softening. Huyskens-Keil et al. (2006) in- and a loss of cellular adhesion; in turn, pulp bruising (Huyskens-Keil et al., 2006). vestigated the postharvest quality of pepino density decreases during ripening, and cell- ‘Golden Globe’ under CA combinations of to-cell contact areas likely decline, whereas Postharvest Handling and Physiological 5% O2 and 5, 15, or 20% CO2 for 21 d at 5 and intercellular spaces increase during ripening Disorders 10 C. The authors concluded that posthar- (Heyes et al., 1994). Likewise, polygalactur- vest quality was strongly dependent on the onase (PG) and pectinmethylesterase (PME) One of the first reports on pepino storage ripening stage, that is, mature pepino showed enzymes, which have been widely studied in potential was conducted by Lizana and higher retention of texture and color, and many other fruit species, exhibit the same Levano (1977). These authors studied the better storability, whereas the ripe stage was behavior in pepino, with increasing enzy- postharvest behavior of pepino fruit at three recommended for ready-to-eat fresh market matic activity during ripening (Heyes et al., maturity stages at –5, 0, 3, 5, 12, and 18 C, fruit. In reference to Chile, Galletti et al. 1994; Schaffer et al., 1989). As expected, and also determined the maximum potential (2006) studied the storage potential of pepino higher temperatures and more advanced storage period by studying pepinos up to 75 d fruit in MA (3% to 5% CO2 and 9% to 14% stages of ripening result in higher rates of of storage. The lowest temperatures (–5 and O2) for 21 and 35 d at 8 C. Two maturation softening in pepino fruit. 0 C) induced intense browning, producing stages ‘‘green’’ and ‘‘yellow green’’ were
HORTSCIENCE VOL. 51(9) SEPTEMBER 2016 1131 stored under MA, and the main effects resulted years to establish a storage protocol due to the Gould, K., K. Hammett, and S. Steinhagen. 1990. in color delay, firmness retention, and reduced validation of fruits harvested in different Mechanism of bruise resistance in pepino water loss. As Huyskens-Keil et al. (2006) years, from different plants (yearly crops), (Solanum muricatum) fruit. Ann. Bot. (Lond.) found, storage benefits of MA also depended or from different inflorescence trusses, a suit- 66:155–161. on the fruit ripening stage. In this case, Galletti able postharvest protocol must be developed. Grierson, D. 2013. Ethylene and the control of fruit ripening, p. 43–73. In: G. Seymour, M. Poole, J. et al. (2006) reported better results in matura- Giovanonni, and G. Tucker (eds.). The molec- tion stage ‘‘green,’’ suggesting that mature Conclusion ular biology and biochemistry of fruit ripening. green fruits have more storage potential. De- Chapman and Hall press, London, UK. spite quality-related benefits associated with Pepino, a Solanaceae fruit with a unique Harman, J., M. Hogg, and F. Horne. 1986. Maturity MA, Galletti et al. (2006) did not recommend sweet taste, has received modest attention and quality indices for pepino fruit. Hort- the use of MA, which reached up to 5% CO2, from the scientific community over the years. Science 21:129 (abstr.). due to the presence of ‘‘off-flavors’’ after The commercial production of this species Herraiz, F., S. Vilanova, I. Andujar, D. Torrent, M. storage. Neither CA nor MA studies reported has also been neglected, mainly due to a lack Plazas, P. Gramazio, and J. Prohens. 2015a. on the presence of postharvest physiological of information on storage and handling, Morphological and molecular characterization disorders. which has resulted in poor quality outcomes of local varieties, modern cultivars and wild relatives of an emerging vegetable crop, the for consumers. Nonetheless, pepinos present pepino (Solanum muricatum), provides insight New Perspectives and Challenges great potential as a horticultural crop due to into its diversity, relationships and breeding their plasticity in adapting to different agro- history. Euphytica 206:301–318. One of the main challenges related to the climatic conditions and for their quality Herraiz, F., S. Vilanova, M. Plazas, P. Gramazio, I. use of this crop is the identification of wild characteristics, especially in terms of flavor. Andujar, A. Rodríguez-Burruezo, A. Fita, G. genotypes that are still present in South Fruit maturity is also important for fruit Anderson, and J. Prohens. 2015b. Phenological America and the subsequent development quality at the consumer level since it is affect- growth stages of pepino (Solanum muricatum) of new cultivars. Herraiz et al. (2015a) re- ing several quality attributes, such as appear- according to the BBCH scale. Sci. Hort. 183:1–7. cently reported that the genetic diversity ance, texture, and flavor. Depending on the Heyes, J., F. Blaikie, C. Downs, and D. Sealey. levels are still very high in Ecuador, southern maturation stage, the storage conditions have 1994. Textural and physiological changes dur- ing pepino (Solanum muricatum Ait.) ripening. Colombia, and northern Peru, thus forming a strong impact in the shelf life of pepino fruit, Sci. Hort. 58:1–15. a major reservoir of genetic material. This being the loss of firmness the main limiting Huyskens-Keil, S., H. Prono-Widayat, P. Ludders,€ feature renders the Andean region a rich factor for riper stages. Further research on this and M. Schreiner. 2006. Postharvest quality of source of genetic material for future breeding species is needed, particularly at the molecular pepino (Solanum muricatum Ait.) fruit in con- programs. In regard to phenotypic diversity, level, and should take advantage of the fact trolled atmosphere storage. J. Food Eng. some studies have focused on the character- that the genomes of its closest relatives (e.g., 77:628–634. ization of ecotypes, and major efforts have tomato and potato) have been already se- Huyskens-Keil, S., H. Prono-Widayat, P. Ludders,€ focused on the phenotypic characterization of quenced. Thus, future efforts should focus on M. Schreiner, and P. Peters. 2000. Physiolog- specific traits of agronomic interest (Munoz~ quality and storability aspects. ical changes of pepino (Solanum muricatum et al., 2014). The availability of standardized Ait.) during maturation and ripening. Acta Hort. 531:251–256. morphological characterization data is essen- Literature Cited Huyskens-Keil, S., H. Prono-Widayat, M. tial for the development of breeding pro- Ahumada, M. and M. Cantwell. 1996. Postharvest Schreiner, and P. Peters. 2001. Effect of surface grams on this crop. coating and film packaging on the keeping Breeding for higher yields and fruit quality studies in pepino dulce (Solanum muricatum Ait.): Maturity at harvest and storage behavior. quality of solanaceous crops (Solanum muri- adapted to markets have resulted in the devel- Postharvest Biol. Technol. 7:129–136. catum Ait., Solanum quitoense Lam.). Acta opment of modern varieties with larger and Anderson, G., R. Jansen, and Y. Kim. 1996. The Hort. 553:621–625. elongated fruits (Herraiz et al., 2015a). These origin and relationships of the pepino, Solanum Kader, A. 2002. Quality and safety factors: Defini- fruits are more suitable for shipping, because muricatum (Solanaceae): DNA restriction frag- tion and evaluation for fresh horticultural crops, they pack better in boxes resulting in fewer ment evidence. Econ. Bot. 50:369–380. p. 279–285. In: A. Kader (ed.). Postharvest bruises than the round fruit. However, the Blanca, J., J. Prohens, G. Anderson, E. Zuriaga, J. technology of horticultural crops. Oakland, CA. Kola, O., M. Simsek, H. Duran, and H. Bozkir. 2015. need to develop sweeter fruit cultivars is high, Canizares,~ and F. Nuez. 2007. AFLP and DNA sequence variation in Andean domesticate, HPLC determination of carotenoid, organic particularly for European market demands, acid, and sugar content in pepino (Solanum where sugar contents of 8% are considered pepino (Solanum muricatum, Solanaceae): Im- plications for evolution and domestication. muricatum) fruit during the ripening period. to be too low by consumers (Kola et al., 2015). Amer. J. Bot. 94:1219–1229. Chem. Nat. Compd. 51:132–136. Other challenges facing the continued Bravo, A. and E. Arias. 1983. Cultivo del pepino Levy, D., N. Kedar, and N. Levy. 2006. Pepino improvement of pepino storage performance dulce. El Campesino 114:15–33. (Solanum muricatum Aiton): Breeding in Israel have taken on a greater significance: the Burge, G.K. 1989. Fruit set in the pepino (Solanum for better taste and aroma. Isr. J. Plant Sci. development of cultivars suitable for han- muricatum Ait.). Sci. Hort. 41:63–68. 54:205–213. dling, transport, and long-term storage. The Buttery, R.G. 1993. Quantitative and sensory Lizana, L. and B. Levano. 1977. Caracterizacion y study and use of storage technologies such as aspects of flavor of tomato and other vegetables comportamiento de post-cosecha del pepino CA, MA, and film packaging has been carried and fruits, p. 259–286. In: T.E. Acree and R. dulce Solanum muricatum. Ait. Proc. Trop. Reg. Am. Soc. Hort. Sci. 21:11–15. out in recent years. Unfortunately, long-term Teranishi (eds.). Flavor science: Sensible prin- ciples and techniques. Amer. Chem. Soc., Martínez-Romero, D., M. Serrano, and D. Valero. storage seems to be a challenge for pepino Washington, DC. 2003. Physiological changes in pepino (Sola- fruit, which has proven to be very sensitive to Daunay, M., F. Rousselle-Bourgeois, R. Lester, num muricatum Ait.) fruit stored at chilling and temperatures lower than 5 C (Lizana and and J. Peron. 1995. Known and less known non-chilling temperatures. Post. Biol. Technol. Levano, 1977) and can be damaged under CA Solanum species for fresh market. Acta Hort. 30:177–186. conditions (data not shown). Better strategies 412:293–305. Matsui, K., A. Minami, E. Hornung, H. Shibata, K. and/or recommendations to store pepino are Dimick, P. and J. Hoskin. 1982. Review of apple Kishimoto, V. Ahnert, H. Kindl, T. Kajiwara, and still needed. It is currently known that pepi- flavor-state of the art. Crit. Rev. Food Sci. Nutr. I. Feussner. 2006. Biosynthesis of fatty acid nos store well at 7 C for 40 d under regular 18:387–409. derived aldehydes is induced upon mechanical atmosphere (21% O 0% CO ) (data not El-Zeftawi, B., L. Brohier, L. Dooley, F. Goubran, wounding and its products show fungicidal activ- 2, 2 R. Holmes, and B. Scott. 1988. Some maturity ities in cucumber. Phytochemistry 67:649–657. shown). Given the formation of CA injury, indices for tamarillo and pepino fruits. J. Hort. McFadden, W., R. Teranishi, J. Corse, D. Black, current studies on several CA combinations Sci. 63:163–169. and T. Monday. 1965. Volatiles from straw- are being conducted by the authors of this Galletti, L., H. Berger, D. Drouilly, and A. Lizana. berries. II. Combined mass spectrometry and review for the development of an adequate 2006. Atmosfera modificada en fruto de pepino gas chromatography on complex mixtures. J. storage protocol. Although it can take several dulce. IDESIA (Chile) 24:35–40. Chromatography 18:10–19.
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