Review n. 32 – Italus Hortus 24 (2), 2017: 19-24 doi: 10.26353/j.itahort/2017.2.1924

Vine cacti ( Hylocereus species): an emerging fruit crop

Noemi Tel-Zur The French Associates Institute for Agriculture and Biotechnology of Drylands, The Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Israel

Ricezione: 19 novembre 2017; Accettazione: 12 gennaio 2018

Vine cacti (specie Hylocereus ): una Hylocereus species as good candidates for dryland coltura emergente agriculture

Riassunto. I di vite del genere Hylocereus , Global warming and diminishing fresh water originari delle regioni tropicali del Nord America del resources are among the major factors impacting the Sud, dell'America centrale e del Messico, costituis - future of agricultural and food production worldwide. cono un gruppo di piante emipifitiche contenenti frutti A challenge of supreme importance for farmers and commestibili esotici. I frutti, noti come pitahaya o frut - agricultural researchers alike is, therefore, to intro - to del drago, hanno una polpa dolce e succosa con duce, domesticate and develop new crop candidates piccoli semi neri croccanti. Praticamente sconosciuto with high water-use efficiency and improved resis - tre decenni fa, oggi queste colture stanno occupando tance to adverse conditions, especially drought. Such una nicchia in crescita nei mercati di frutta esotica in newly developed crops will slot into the overall map tutto il mondo. Attualmente sono coltivati in Messico, Colombia, Ecuador, Stati Uniti, Israele, Tailandia, of food production as low-volume but high-value Australia, Cina e Vietnam, l'ultimo dei quali è il più crops for specific niches where traditional agriculture grande paese esportatore. I metodi tradizionali di is impractical or otherwise undesirable. Species of coltivazione sono cambiati considerevolmente nelle vine cactus of the genus Hylocereus (Cactaceae) nuove aree di coltivazione, poiché sono state svilup - belong to this group of perennial fruit crops in which pate tecnologie per aumentare la produttività. Le there is emerging worldwide interest. pratiche agricole di recente sviluppo, che hanno cre - Species of the cactus family, which are native to ato una "rivoluzione" nella coltivazione e nelle rese North and South America and the West Indies dei cactus, includono l'uso di supporti verticali per (Gibson and Noble, 1986), were introduced into at consentire l'arrampicata e l'ombreggiamento per the end of the 15th century and from there spread ridurre i danni causati dall'irraggiamento e dalle tem - throughout the entire world. The different species can perature estreme. Inoltre, l'impollinazione incrociata thrive in a variety of extreme habitats, from hot manuale viene spesso applicata a causa del sistema di autoincompatibilità di diverse cultivar e della man - deserts (up to 55ºC) through tropical rain forests to canza di impollinatori naturali in aree al di fuori degli cool areas with freezing temperatures. Cactaceae habitat nativi della specie. Nonostante i progressi exhibit a range of specific adaptations that make them compiuti, sono necessari ulteriori intensi studi e promising crops for introduction into arid lands, i.e., ricerche per l'addomesticamento e la produzione spines instead of leaves, succulent shoots, and the commerciale di queste colture frutticole, in particolare crassulacean acid metabolism (CAM) pathway for nelle zone aride, dove l'efficienza dell'uso di acqua CO 2 fixation. In CAM plants, transpiration and photo - alta deve ancora essere sfruttata. Questa recensione synthesis take place during the night, while during the affronta le principali scoperte sullo sviluppo agricolo day the stomata are closed-mechanisms that result in delle specie di Hylocereus come colture da frutto. high water use efficiency (Nobel, 1988; 1994). Hylocereus species, for example, require around 10% sviluppo della coltura, tolleranza Parole chiave: of the water required by C and C plants (Mizrahi et alla siccità, caratteristiche del frutto, Hylocereus , usi. 3 4 al ., 2007). An additional advantage of many cactus species as crops is their ability to thrive in poor and *

19 Tel Zur marginal soils (Nobel, 1988). The potential of cactus edible fruits, known as pitahayas in their countries of species for high economic impact lies in their diverse origin and as dragon fruits in Asia. The fruits exhibit a uses not only as agricultural produce and processed variety of shapes and sizes, with broad foliaceous foods but also in industrial and medicinal products. scales on peels that range in color from white/yellow Thus, in view of global climate change and the scarci - to pink/red. The fruit flesh, which ranges from white ty of water in extensive regions, cactus species hold through pink to red/purple in the various species, is the promise as a significant option for sustainable dry - sweet and juicy and carries edible black small seeds land agriculture. (fig. 1C,D) (Lichtenzveig et al ., 2000). Among the cactus species, the vine cacti - Hylocereus - are a group of emerging fruit species Genetic resources with high economic potential for arid regions (Raveh et al ., 1998; Nobel and De La Barrera, 2004; Mizrahi The taxonomy of Hylocereus (Berger) Br. and R., et al ., 2007). The natural distribution area of the mem - as revised by Bauer (2003), comprises 15 species: H. bers of Hylocereus lies mainly in the forests of extensus (Salm-Dyck ex De Candolle) Bauer, H. Central America, the West Indies, and the northern setaceus (Salm-Dyck ex De Candolle) Bauer, H. tri - areas of South America (Barthlott and Hunt, 1993). cae (Hunt) Bauer, H. minutiflorus Br. and R., H. Hylocereus species are hemi-epiphyte plants that megalanthus (Schum. ex Vaupel) Bauer, H. attach themselves to trees by aerial roots. The plants stenopterus (Weber) Br. and R., H. calcaratus are characterized by elongated three-angled stems and (Weber) Br. and R., H. undatus (Haw.) Br. and R., H. hermaphrodite flowers, mostly white (rarely red), with escuintlensis (Kimn.), H. ocamponis (Salm-Dyck) Br. the ovary and tube bearing large foliaceous scales (fig. and R., H. guatemalensis (Eich.) Br. and R., H. 1A). The flowers are very large, reaching at anthesis costaricensis (Weber) Br. and R., H. monacanthus 30 cm or more in length and 40 cm in diameter (fig. (Lem.) Br. and R., H. trigonus (Haw.) Safford, and H. 1B). The flowers are nocturnal, staying open and triangularis (L.) Br. and R. Among the first species to receptive only for one night (Nerd and Mizrahi, 1997). be cultivated out of their native areas as fruit crops They are pollinated in their natural habitats by fruit were H. undatus (white flesh and red peel), bats or hawk moths (Grant and Grant, 1979; Valiente H. monacanthus (purple flesh and red peel) and H. Banuet et al ., 2007). Hylocereus species bear large megalanthus (white flesh, yellow spiny peel, and a

Fig. 1 - Hylocereus plants. A. Flower buds. B. Flower at anthesis. C. H. undatus fruit. D. H. megalanthus fruit. Fig. 1 - Piante di Hylocereus . A. Boccioli di fiori. B. Fiore ad antesi. C. frutto di H. undatus . D. frutto di H. megalanthus .

20 Vine cacti ( Hylocereus species): an emerging fruit crop superior taste) (Weiss et al ., 1994). H. undatus and species is reflected in the registration of many new H. monacanthus both bear large scaled fruits of 200- cultivars in recent years (Lobo et al., 2016). 600 g, and H. megalanthus bears medium-sized fruits (80-200 g) with large spines that can easily be Agrotechniques removed upon ripening. H. monacanthus and H. undatus are diploids (2 n = 2x = 22) and H. megalan - The first step in the cultivation of a new crop thus is a tetraploid (2 n = 4x = 44) (Lichtenzveig et al ., should be focused on the development of the agricul - 2000; Tel-Zur et al ., 2004). In Israel, H. monacanthus tural techniques needed for profitable cultivation and H. undatus bloom during the summer and pro - (Mizrahi and Nerd, 1999). The most important con - duce fruit that matures in 28 to 37 days from anthesis sideration in the cultivation of vine cacti are the dual (Tel-Zur et al ., 2011). H. megalanthus blooms either needs for support and protection from intense radia - in autumn or early winter (November and December) tion and extreme temperatures, since in the wild vine with the fruits maturing in 90 and about 180 days cacti grow on trees, which fulfil both these needs from anthesis, respectively (Tel-Zur et al ., 2011). need. Currently, the standard technique for vegetative Ripening time in H. megalanthus is genotype specific, propagation of selected cultivars is based on cuttings with considerable variability among different acces - of 30-50 cm in length. The cuttings are stored for 1-2 sions (Dag and Mizrahi, 2005). weeks in a dry place and then potted to induce root - During the past two decades, the high-value diploid ing. The rooted cuttings are then planted in net-hous - hybrids designated ‘Omer’, ‘Venus’, and ‘Nili’, with es or greenhouses, and the stems are attached to trellis improved fruit quality and a prolonged harvesting sea - structures to hold and support the growing plants. A son, were released for cultivation to Israeli farmers. variety of trellis structures has been developed in dif - These cultivars exhibit different peel and flesh colors, ferent orchards (fig. 2) (Martinez et al ., 1996; Ortiz, different fruit sizes and the absence of spines in the 2000). Under good growing conditions, the recom - peel. An additional diploid cultivar, known as mended distance between plants in the same row is ‘Golden’, has also been released to Israeli farmers; this cultivar has a yellow peel and white flesh. All these diploid cultivars ripen during the summer, and their fresh fruit production ranges between 30 and 35 tons per hectare (Y. Mizrahi personal communication). In addition, two triploid hybrids - the result of a cross between the diploid H. monacanthus and the tetraploid H. megalanthus - with excellent fruit taste and long shelf-life were released to Israeli farmers a short while ago. The ripening season of these triploid hybrids begins in late autumn and ends in mid-winter, thus enabling the farmer to extend the marketing season from the summer (for the diploids) well into the win - ter. The disadvantages of these triploid hybrids are that they lack fertile pollen and that they have a spiny peel (Mizrahi, 2014). For these reasons, a second round of crossing has been performed, and the improved hybrids are currently under observation in commercial orchards. These hybrids - as well as all the genebank resources - are described in detail in a database that can be accessed via the Internet: www.bgu.ac.il/life/Faculty/Mizrahi/index.html. In China, three red-skinned cultivars are currently cultivated, ‘Guanhuahong’ (red pulp), ‘Guanhuabai’ (white pulp) and ‘Guanhuahongfen’ (pink pulp); they were selected from ‘Conghuazhixing’ (the hybrid off - spring of H. monacanthus and H. undatus ) through Fig. 2 - Trellis systems. A. Vietnam orchard. B. Israeli orchard (planted in pots). seedling selection (Y. Qin, personal communication). Fig. 2 - Sistemi a traliccio. A. Frutteto del Vietnam. B. Frutteto In the USA, the rise interest in pitahayas as crop israeliano (piantato in vasi).

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1.5 meters, and that between rows is 3 meters (Y. To obtain good yields, manual pollination may be Moyal, personal communication). Higher plant densi - necessary due to the self-incompatibility system of ties would require intensive pruning of the plants and several cultivars and the lack of natural pollinators in complicate the field work. areas beyond the species’ native habitats. Under the As indicated above, vine cacti are sensitive to both growing conditions in Israel, H. undatus is self-com - extremely low and extremely high radiation and tem - patible, especially at the beginning and end of the peratures, with a marked variation in sensitivity flowering season, but the fruits are smaller than those between the different species and genotypes. In tropi - obtained with cross-pollination (Weiss et al ., 1994; cal areas, vine cacti species were initially planted in Lichtenzveig et al ., 2000). The tetraploid H. megalan - the open (Barbeau, 1990), where high solar radiation thus is also self-compatible (Dag and Mizrahi, 2005). resulted in the bleaching of the green tissues, inhibi - Nonetheless, due to the absence of efficient pollina - tion of growth and, eventually, death. Consequently, tors (bees are not considered to be efficient pollina - outside their natural environment, today orchards are tors) and the low yields obtained after self-pollination frequently planted in net-houses or greenhouses to pre - in the self-compatible cultivars, hand-cross pollina - vent photo-inhibition damage (Mizrahi and Nerd, tion is routinely carried out to guarantee good yields 1999; Raveh et al . 1998). The shade net density used (Weiss et al ., 1994; Nerd and Mizrahi, 1997). This depends on the intensity and range of the local radia - procedure involves collecting pollen from flowers at tion and may range from 20% to 60% (expressed as a anthesis and then brushing the stigma of a flower of percent of full solar irradiation) (Mizrahi and Nerd, another cultivar with the fresh pollen. 1999). Under conditions of very low sunlight, the number of flowers and hence the yields will be Nutritional value and additional uses reduced, and therefore the minimum shade net density is used to maximize yields and prevent bleaching. A Increased worldwide interest in these cactus reduced number of flowers and very low crop yields species has emerged due to their economic potential have also been observed in regions with very high as exotic fruit crops (Mizrahi and Nerd, 1999; summer temperatures (a monthly average of 38°C) Hammer, 2001). In terms of nutritional value, H. (Mizrahi and Nerd, 1999; Nerd et al ., 2002). The dam - undatus and H. monacanthus fruits have high levels age from very high temperatures varies from yellow - of sodium, potassium, and vitamin A (Martinez et al ., ing (bleaching) of the green tissues to a total “liquefac - 1996; Nerd et al ., 1999). Their soluble sugar content tion” of large stem areas of the whole plant. Among ranges from 5.4 to 6.8%, and total solids, from 12.5 to the Hylocereus species that have been studied, H. 16.6% (Martinez et al ., 1996; Nerd et al ., 1999). A undatus showed the greatest sensitivity to high tem - study of the metabolite profiles of the fruit pulp and perature, with stems turning brown and liquefying at seeds of the diploid H. monacanthus , the allotriploid 45°C, whereas other species showed better tolerance S-75 (a cross between H. monacanthus and H. mega - under similar conditions (Mizrahi and Nerd, 1999). lanthus ) and their autotetraploid and autohexaploid

Net CO 2 uptake by H. undatus was found to be zero lines showed that the autoployploid lines exhibited when the day/night temperature reached 42/32ºC, indi - reduced sugar contents but increased contents of cating that this species is not tolerant to high tempera - amino acids, tricarboxylic acid cycle intermediates, tures (Nobel and De La Barrera, 2004). In addition, organic acids and flavonoids (Cohen et al ., 2013). under extreme summer temperatures, i.e., at 45°C, Betacyanins, the major fruit pigments in the diploid annual flower production was very low and flowering H. monacanthus , decreased in the autotetraploid line time was postponed (Mizrahi and Nerd, 1999). For (Cohen et al ., 2013). expanding cultivation into dryland regions, it is thus Another important source of phytochemicals are necessary to select elite cultivars that are tolerant to the pigments - betalains - found in the fruits. A class high temperatures. At the other end of the temperature of betalains that has been identified in the fruits of H. scale, it was found that frost caused damage to the monacanthus and of some hybrids comprises beta - plants, resulting in dark spots on the stems and fruits, cyanin pigments and their isoforms (Wybraniec et al ., and temperatures between 2 and 4°C were reported to 2001; Wybraniec and Mizrahi 2002; Wybraniec et al ., cause plant mortality (Thomson, 2002). Another 2006). These pigments have attracted attention as potential problem in expanding cultivation to marginal thermo-stable food colorants (Herbach et al ., 2004). areas is the sensitivity of the plants to salinity: irriga - The anti-oxidative properties and anti-cancer activity tion with saline water; above 2.2 dS/m, was shown to of betalain pigments are currently being evaluated. damage the plants (Y. Mizrahi, pers. comm.). We are confident that our investigations and those of

22 Vine cacti ( Hylocereus species): an emerging fruit crop other groups will lead to the development of down - advances that have been made, further intensive stream products that will enhance the profitability of research and development are required for the domes - Hylocereus as crop species. tication and commercial production of these fruit crops, particularly in arid zones, where their high Future development and commercialization water use efficiency is yet to be exploited. This review addresses the key findings on the agricultural Today, vine cacti are grown as crops in Mexico, development of Hylocereus species as fruit crops. Colombia, Ecuador, the United States, Israel, Thailand, Australia, China and Vietnam, the last of Key words: crop development, drought tolerance, which is the largest exporting country. Nonetheless, fruit traits, Hylocereus , uses. Hylocereus species still remain a group of underuti - lized fruit crops, and realizing the potential of References Hylocereus species as a ‘mainstream’ commercial niche crop poses a scientific and technological chal - BARBEAU G., 1990. La pitahaya rouge, un nouveau fruit exotique . Fruits, 45:141-147. lenge. Nonetheless, the important advances that have BARTHLOTT W., H UNT D.R., 1993. Cactaceae . In “The families been made in developing agrotechniques and in and the genera of vascular plants”. Kubitzki, K. (ed) vol 2. understanding their reproductive biology can now be Springer-Verlag, Berlin, Germany: 161-196. exploited to develop breeding programs and addition - BAUER R., 2003. A synopsis of the tribe . F. Buxb . Cactaceae System Initiatives, 17: 3-63. al uses for the fruits and flowers in the form of health- COHEN H., F AIT A., T EL -Z UR N., 2013. Morphological, cytologi - promoting and nutritional phytochemicals (nutraceuti - cal and metabolic consequences of autopolyploidization in cals) for the food industry and for ornamental uses. In Hylocereus ( Cactaceae) species. BMC Plant Biol, 13: 173 DAG A., M IZRAHI Y. 2005., Effect of pollination method on fruit summary, integrating the above-described scientific set and fruit characteristics in the vine cactus and technological results, the promise of Hylocereus megalanthus (“yellow ”). J. Hort. Sci. Biotechnol., 80: species as an innovative crop with a high impact on 618-622. GIBSON CG., N OBLE PS., 1986. The cactus primer . Harvard Univ. growers, industry and consumers will surely be ful - Press, Cambridge, MA. filled. GRANT V., G RANT KA., 1979. The pollination spectrum in the southwestern American cactus flora . Plant Sys. Evo., 133: 29- Abstract 37. HAMMER K., 2001. Cactaceae . 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