Ripening pawpaw fruit exhibit respiratory and ethylene climacterics

Postharvest Biology and Technology 30 (2003) 99/103 Research Note Ripening pawpaw fruit exhibit respiratory and ethylene climacterics Douglas D. Archbold a,+, Kirk W. Pomper b www.elsevier.com/locate/postharvbio a N318 Agricultural Sciences Building North, Department of Horticulture, University of Kentucky, Lexington, KY 40546-0091, USA b 129 Atwood Research Facility, Kentucky State University, Frankfort, KY 40601, USA Received 20 December 2002; accepted 10 July 2003 Abstract The ripening behavior of the native American pawpaw (Asimina triloba (L.) Dunal.) fruit was studied immediately after harvest and after 1 month of 4 8C storage. Fruit were harvested at two different maturity stages. Fruit that were unripe (minimal softening evident) at harvest exhibited respiratory and ethylene climacterics at 3 and 5 days postharvest, respectively, at ambient temperature, and a precipitous decline in fruit firmness was evident prior to the climacteric peaks. Fruit classified as having commenced ripening (some softening evident) at harvest exhibited both respiratory and ethylene climacteric peak at 3 days at ambient storage temperature. Fruit in cold storage at 4 8C for 28 days exhibited minimal to no loss of firmness, and upon removal to ambient temperature both respiratory and ethylene climacterics occurred within 7 days for both harvest maturities. The maximum rates of respiration and ethylene production in these studies were: CO 2 production 90 mg kg 1 h 1 and C 2 H 4 production 14.4 mg kg 1 h 1, respectively. These results indicate that pawpaw fruit ripening is climacteric. # 2003 Elsevier B.V. All rights reserved. Keywords: Asimina triloba; Postharvest; Firmness 1. Introduction Pawpaw is generating growing interest as a high value, alternative fruit crop for the southeastern US (Layne, 1996). It exhibits unique quality traits for a temperate fruit that are similar to other fruit in the Annonaceae family, including cherimoya (Annona cherimola Mill.), sugar apple or sweetsop (A. squamosa L.), soursop (A. muricata L.), custard apple (A. reticulata L.), and atemoya (A. squamosa X A. cherimola), all of which are tropical. These traits include an intense, pleasant aroma and a custard-like texture. Ripe pawpaws enter local fresh markets, and the fruit have significant processing potential due to their unique aroma and flavor. To enter the fresh and processing markets in an orderly manner, the fruit must be harvested and stored to * Corresponding author. Tel.: /1-859-257-3352; fax: /1-859-224-3356. E-mail address: darchbol@uky.edu (D.D. Archbold). 0925-5214/03/$ - see front matter # 2003 Elsevier B.V. All rights reserved. doi:10.1016/s0925-5214(03)00135-2

100 D.D. Archbold, K.W. Pomper / Postharvest Biology and Technology 30 (2003) 99/103 maintain high quality. Even though the American Genetics Association (1916) noted that perishability was the greatest hindrance to developing a market for the fruit almost 90 years ago, harvest and storage techniques havenever been developed for this orphan fruit. In order to develop recommendations for harvest and storage of pawpaw, the ripening behavior of the fruit must be established. As pawpaw fruit ripen, the soluble solids content increases to /20%, the flesh softens rapidly, volatile production increases, and the fruit color exhibits a decline in the hue angle (i.e. a color change of green to yellow) (McGrath and Karahadian, 1994a,b). Ethyl and methyl esters contribute significantly to fruit aroma and flavor (McGrath and Karahadian, 1994a,b). Classifying the fruit as climacteric or nonclimacteric is essential for defining harvest and storage techniques that may extend fruit storage life. Ripening of climacteric fruit is often ethylene induced and/or coordinated, and this aspect provides an opportunity to regulate the process. Biale (1960) reported that pawpaw fruit were climacteric, citing the work of Wardlaw and Leonard (1936). A careful reading of that work clearly shows that they studied a different species, papaya (Carica papaya), not pawpaw. The confusion has arisen due to a common regional name of papaya, papaw, which has also sometimes been used as the spelling of the North American pawpaw. Biale s erroneous classification of pawpaw has subsequently been repeated by others (Rhodes, 1970; Watkins, 2002). However, the evidence is merely anecdotal that pawpaw fruit are climacteric, exhibiting an increase in respiration and ethylene production during ripening (Peterson, 1991). All of the other species in the Annonaceae that are of commercial importance are climacteric (Brown et al., 1988; Merodio and De la Plaza, 1997; Paull, 1982; Wills et al., 1984), so it is expected that the pawpaw is climacteric as well. In addition there are no reports on the response of the fruit to cold storage. The objectives of this study were to determine if (1) pawpaw fruit ripening is climacteric, and (2) 4 8C storage for 1 month delays ripening. 2. Materials and methods 2.1. Fruit harvest and ripening Fruit were harvested from the Kentucky State University pawpaw orchards in Frankfort, KY, on three dates during August /September 1998. Fruit were segregated into two groups based on firmness to touch: (1) unripe with minimal softening evident, and (2) ripening with some softening evident. The fruit were from several numbered genotypes but showed no differences in ripening patterns, thus the data were pooled within ripening category across genotypes. Fruit fresh weight (FW) was determined the day of harvest. Fruit were ripened at ambient temperature ( /22 8C) on the open laboratory bench during and between subsequent analyses described below. To coldstore fruit, individual fruit were placed in sealed Ziploc bags at 4 8C for 28 days. Then, fruit were the removed from cold storage and the Ziploc bags, and they were placed at ambient temperature on the laboratory bench. 2.2. Ethylene production, respiration, and firmness measurement On the day of harvest and at intervals during ripening and cold storage, the ethylene production and respiration rates and fruit firmness of each fruit were measured. Individual fruit were placed in a 0.9 l bottle, capped, and held for 2/3 h at their respective temperatures. Gas samples were withdrawn from the headspace to determine C 2 H 4 and CO 2 concentrations. The CO 2 levels were measured by taking a 10 ml sample from each bottle and injecting it into an Oxygen/Carbon dioxide Headspace Analyzer (Model ZR 892 HS, Illinois Instruments, McHenry, IL). The ethylene concentration was measured by taking a 1 ml sample from each bottle and injecting it into a Varian 2100 GC fitted with a 1 m alumina column and run at 100/70/100 8C for the injector/column/fid temperatures, respectively. The N 2 carrier gas flow rate was 0.50 ml s 1. Fruit volume was subtracted from bottle volume using a fresh weight, FW, versus volume regression (/volume 1:790:81

D.D. Archbold, K.W. Pomper / Postharvest Biology and Technology 30 (2003) 99/103 101 FW); generated in preliminary work, to calculate C 2 H 4 and CO 2 production rates. Using a Chatillon force gauge (Model DFM 10, John Chatillon and Sons, Inc., Greensboro, NC) mounted on a Model LTC test stand, external firmness was determined on opposite sides of each fruit surface with a 2 mm compression using the flat head. Fruit in cold storage were rapidly removed for measurement then returned to cold storage. The two measurements were averaged for each fruit and recorded. Fig. 1. Changes in firmness, respiration, and ethylene production by pawpaw fruit after harvest. Fruit were classified as unripe (minimal softening evident) or having commenced ripening (slight softness to touch); note initial firmness values. Fruit were held at ambient temperature on the lab bench (solid circles) or stored in individual sealed polyethylene bags at 4 8C (open circles) for 4 weeks, then moved to the lab bench at ambient temperature (indicated by arrow). Each data point is the mean of 10 or more replicate fruit. The overall S.E. of the room temperature and 4 8C groups is shown by the symbols with error bars.

102 D.D. Archbold, K.W. Pomper / Postharvest Biology and Technology 30 (2003) 99/103 2.3. Replication and data analysis There were five fruit for each treatment group by storage temperature (ambient and 4 8C) on each harvest date. When fruit firmness was at or below 2 N, firmness measurement caused visible tissue injury of some fruit, so they were removed from the study at that time. The mean9s:e: for each fruit trait on each measurement date during ripening and cold storage was calculated across the three harvest dates. 3. Results and discussion At harvest, fruit in the unripe group exhibited a mean firmness of 52 N (Fig. 1A). Held at room temperature, firmness declined rapidly starting the day after harvest and fruit were soft (firmness B/20 N) by 3 days postharvest. A respiratory climacteric was evident at 3 days and peaked at 86 mg kg 1 h 1 of CO 2 on day 5 (Fig. 1B). An ethylene climacteric was evident at 5 days, peaking at 2.8 mg kg 1 h 1 (Fig. 1C). Fruit exhibiting some softness at harvest had a mean firmness of 8 N (Fig. 1D). Respiratory and ethylene climacterics occurred within 3 days at room temperature with peak values at 75 mg kg 1 h 1 of CO 2 and 3.7 mg kg 1 h 1 of C 2 H 4, respectively (Fig. 1E and F). Firmness continued to decline after harvest, and fruit in this group were softer than fruits ripened after harvest at the unripe stage. Cold storage delayed the ripening process of both unripe and ripening fruit (Fig. 1). Fruit that were unripe at harvest showed respiratory and ethylene climacterics 4 days after removal from 4 8C storage with peak values at 82 mg kg 1 h 1 of CO 2 and 9.8 mg kg 1 h 1 of C 2 H 4, respectively. Fruit that were ripening at harvest showed respiratory and ethylene climacterics with peak values at 90 mg kg 1 h 1 of CO 2 4 days after removal from 4 8C storage and 14.4 mg kg 1 h 1 of C 2 H 4 7 days after removal, respectively. Peak ethylene production of these fruit exceeded that of fruit not stored, similar to that observed following several days of cold storage of cherimoya (Alique and Zamorano, 2000). Firmness of fruit from both groups declined little during cold storage but dropped rapidly upon removal to room temperature. Pawpaw fruit exhibited single respiratory and ethylene climacteric peaks like sugar apple (Brown et al., 1988), but in contrast to other Annonaceaous fruit. In cherimoya (Brown et al., 1988; Martinez et al., 1993; Merodio and De la Plaza, 1997), atemoya (Brown et al., 1988), and soursop (Bruinsma and Paull, 1984), a first respiratory peak preceded the ethylene peak by 1/3 days, and a second was coincident with or followed the ethylene climacteric. Bruinsma and Paull (1984) speculated that the first respiratory climacteric may be due to a perturbation in carbohydrate metabolism following detachment from the tree and may not be indicative of the beginning of ripening. If so, the second peak is of most interest as it relates to the pattern observed with pawpaw. The respiratory peak values of pawpaw were comparable to those for the Annona species which range from 175 to 250 mg kg 1 h 1 of CO 2 for cherimoya (Alique and Zamorano, 2000; Brown et al., 1988; Merodio and De la Plaza, 1997), 90/ 400 mg kg 1 h 1 for atemoya (Brown et al., 1988), 50/180 mg kg 1 h 1 for sugar apple (Brown et al., 1988), and 100/250 mg kg 1 h 1 for soursop (Bruinsma and Paull, 1984), but the values are high when compared to many temperate fruit such as apple at 5/10 mg kg 1 h 1 and peach at 10/20 mg kg 1 h 1 (Kader, 2002). The ethylene climacteric peak values of pawpaw were considerably less than for cherimoya, atemoya, and soursop which range from 50 to 300 mg kg 1 h 1 of C 2 H 4 (Alique and Zamorano, 2000; Brown et al., 1988; Bruinsma and Paull, 1984; Merodio and De la Plaza, 1997), but they were similar to those of sugar apple for which values of 0.6/1.8 mg kg 1 h 1 have been reported (Brown et al., 1988). The ethylene production values of pawpaw are low when considered against other temperate fruit species as well, with apple at 10/100 mg kg 1 h 1 of C 2 H 4, for example (Kader, 2002). As noted in other Annonaceous fruits, the decline in fruit firmness was rapid as fruit ripened. The decline was evident prior to or coincident with the respiratory and ethylene climacterics. Like

D.D. Archbold, K.W. Pomper / Postharvest Biology and Technology 30 (2003) 99/103 103 cherimoya, the peak ethylene levels may not be initiators of the ripening process (Merodio and De la Plaza, 1997). The initiation of ripening may be due to other endogenous factors or may have a low threshold for ethylene sensitivity such that initial ethylene production could start the ripening process. Ethylene may be coordinating subsequent ripening events however. Cold storage has the capability of delaying the start of ripening in pawpaw fruit. Although the ripening traits studied were held in check until the fruit were moved to room temperature, other important fruit quality traits were not evaluated. It remains to be determined if fruit taken from cold storage will ripen with the same high quality as those ripening upon harvest. 4. Conclusion In conclusion, pawpaw is a climacteric fruit. Fortunately, Biale s erroneous classification (1960) was correct nonetheless. Harvest, handling, and postharvest storage techniques used with common climacteric fruit such as apple and banana may have potential for delaying the start of and/or slowing down the rate of pawpaw ripening. As more is learned about how pawpaw fruit respond to such standard practices, recommendations for extending pawpaw shelf life for commercial handling can be developed. References Alique, R., Zamorano, J.P., 2000. Influence of harvest date within the season and cold storage on cherimoya fruit ripening. J. Agric. Food Chem. 48, 4209/4216. American Genetics Association, 1916. Where are the best pawpaws? J. Hered. 7, 291/296. Biale, J.B., 1960. Respiration of fruits. In: W. Ruhland (Ed.), Encyclopedia of Plant Physiology, vol. 12. Springer, Berlin, pp. 536/592. Brown, B.I., Wong, L.S., George, A.P., Nissen, R.J., 1988. Comparative studies on the postharvest physiology of fruit from different species of Annona (custard apple). J. Hort. Sci. 63, 521/528. Bruinsma, J., Paull, R.E., 1984. Respiration during postharvest development of soursop fruit, Annona muricata L. Plant Physiol. 76, 131/138. Kader, A.A., 2002. Postharvest biology and technology: an overview. In: Kader, A.A. (Ed.), Postharvest Technology of Horticultural Crops. Univ. Calif. Agric. Nat. Res. Pub. 3311, 39/47. Layne, D.R., 1996. The pawpaw (Asimina triloba (L.) Dunal): a new fruit crop for Kentucky and the United States. HortScience 31, 777/784. Martinez, G., Serrano, M., Pretel, M.T., Riquelme, F., Romojaro, F., 1993. Ethylene biosynthesis and physicochemical changes during fruit ripening of cherimoya (Annona cherimola Mill.). J. Hort. Sci. 68, 477/483. McGrath, M.J., Karahadian, C., 1994a. Evaluation of physical, chemical, and sensory properties of pawpaw fruit (Asimina triloba) as indicators of ripeness. J. Agric. Food Chem. 42, 968/974. McGrath, M.J., Karahadian, C., 1994b. Evaluation of headspace volatiles and sensory characteristics of ripe pawpaws (Asimina triloba) from selected cultivars. Food Chem. 51, 255/262. Merodio, C., De la Plaza, J.L., 1997. Cherimoya. In: Mitra, S. (Ed.), Postharvest Physiology and Storage of Tropical and Subtropical Fruits. CAB International, New York, pp. 269/293. Paull, R.E., 1982. Postharvest variation in composition of soursop (Annona muricata L.) fruit in relation to respiration and ethylene production. J. Amer. Soc. Hort. Sci. 107, 582/ 585. Peterson, R.N., 1991. Pawpaw (Asimina). Acta Horticult. 290, 567/600. Rhodes, M.J.C., 1970. The climacteric and ripening of fruits. In: Hulme, A.C. (Ed.), The Biochemistry of Fruits and Their Products. Academic Press, London, pp. 521/533. Wardlaw, C.W., Leonard, E.R., 1936. Studies in tropical fruits. I. Preliminary observations on some aspects of development, ripening and senescence with special reference to respiration. Ann. Bot. 3, 27/42. Watkins, C.B., 2002. Ethylene synthesis, mode of action, consequences and control. In: Knee, M. (Ed.), Fruit Quality and Its Biological Basis. CRC Press LLC, Boca Raton, pp. 180/224. Wills, R.B.H., Poi, A., Greenfield, H., Rigney, C.J., 1984. Postharvest changes in fruit composition of Annona atemoya during ripening and effects of storage temperature and ripening. HortScience 19, 96/97.