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The Pomegranate: A New Look at the Fruit of ParadiseEd Stover!USDAIARS, National Clonal Germplasm Repository, One Shields Avenue,University ofCalifornia, Davis, CA 95616

Eric W. MercureParamount Farming Company, Bakersfield, CAAdditional index words. antioxidant, heterostyly, Punica granatum

In this paper, a broad overview is provide

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forming a large shrub or small tree, andreaching a height of 12 to 20 ft at maturity.Trees may be trained to multiple trunks incolder areas, to reduce risk of total tree loss.Very dwarf pomegranates (such as 'Nana')are known with small plant, flower, and fruitsizes, and are widely used as ornamentals.The pomegranate plant is more or less spinyand deciduous, with small, narrow, oblongleaves with short stems (Morton, 1987).Plants aggressively sucker from the crownarea and the roots.The flower. The pomegranate flowers aremost commonly red to red-Drange and arefunnel shaped, although "double" and variegated flowers are found in some ornamentalselections, which are not grown for fruit.Pomegranate can be self-pollinated or crosspollinated by insects (Morton, 1987). Flowersare primarily borne subterminally, primarilyon short lateral branches older than 1year (EIKassas et a!., 1998), although some cultivarsflower on spurs. Flowers occur as singleblossoms or in clusters of up to five.

In the Central Valley ofCalifornia, pomegranate blooms from early May to November, with most flowering from mid May toearly June. Pollination in California is primarily affected by insects or hummingbirds.Stigma receptivity lasts 2 to 3 dand declinesquickly in unpollinated flowers (Melgarejoet a!., 2000).Pomegranate flowers are heterostylous.Long-styled perfect flowers are larger, havelarger ovaries, and set more fruit than shortstyle types, which are either intermediate orfunctionally male only. The proportion ofthese two flower types varies among cultivarsand year to year (Martinez et a!., 2000).Thefruit. The pomegranate fruit is berrylike with a leathery rind (or husk) enclosingmany seeds surrounded by the juicy arils,which comprise the edible portion of the fruit(Watson and Dallwitz, 1992). The aril juicesack is composed of many epidermal cells.According to cultivar, arils range from deepred to virtually colorless, whereas theenclosed seed varies in content of sclerenchyma tissue, which affects seed softness.The number of locules and arils (andenclosed seeds) varies, but may be as highas 1300 per fruit (Levin, 2006). The fruit hasa prominent calyx, which is maintained tomaturity and is a distinCtive feature of thepomegranate fruit. The husk is comprised oftwo parts: the pericarp, which provides acuticle layer and fibrous mat; and the mesocarp (known also as the albedo), which is thespongy tissue and inner fruit wall where thearils attach. Septal membranes are thepaperytissue that further compartmentalizes groupsof arils, but arils do not attach to this tissue(Matthew Quist, pers. comm.). There isinterest in identifying or developing cultivarsthat have more locules to fill the fruit interior,fewer septal membranes for easier eating, anda thinner mesocarp.Fruits ripen about 6 to 7 months afterflowering (Morton, 1987) and are harvestedwhen qualities are deemed most appropriatefor expected market use. In Israel, theyHORTSCIENCE VOL. 42(5) AUGUST 2007

harvest 'Wonderful' when soluble solidsreach 15% (Morton, 1987). Minimum maturity for 'Wonderful' in California is based ontitratable acidity less than 1.85% and colordarker than an established reference (Kader,2006). In a Spanish study, soluble solids ofthe cultivars examined did not vary greatlyfrom mid August through mid November,and the principal acids were malic and citric(Legua et a!., 2000).Unlike most horticultural fruits, inherentseed dispersal is not achieved through consumption of all or most of the fruit and seedswith accompanying spread. Rather, thepomegranate fruit structure has apparentlyevolved to ensure splitting of the leatheryhusk, and exposure of the tempting arils andseeds (Morton, 1987) to the many happilycooperative birds and so forth serving asdispersal agents.

POMEGRANATE PRODUCTIONCurrent global production estimates forpomegranate are unavailable. However, it iswidely grown in many countries where it iswell adapted. In India more than 100,000 ha

of pomegranate are produced. It is consideredone of the most important fruits of thetropical an,d subtropical areas because oflow maintenance cost, good yields, goodkeeping quality, and ability to thrive withlimited moisture (Indian Council of Agricultural Research, 2005). In Iran, 65,000 ha ofpomegranate produces 600,000 tons of fruitannually, with about 30% of yield exported(Mehrnews, 2006). Turkish production in1997 was 56,000 tons/year (Gozlekci andKaynak, 2000). Spain, with R:!3000 ha, isthe largest western European producer ofpomegranate, and production has been increasing as a result of high market prices(Costa and Melgarejo, 2000).In the United States, there are 5600 ha ofcommercial pomegranate, mostly in the SanJoaquin Valley. The 'Wonderful' cultivardominates almost completely, but there isinterest in earlier and later cultivars to extendthe market season (Kotkin, 2006).

POMEGRANATE CULTIVARSMore than 500 cultivars of pomegranatehave been named (IPGRI, 2001), but such

ancient and widespread fruits often haveconsiderable synonymy, in which the samebasic genotype is known by different namesin different regions. Synonymy is likelyfurther encouraged by the fact that husk andaril color can vary markedly when grown indifferent regions. A numberof characteristicsvarybetween pomegranate genotypes and arekey to identification, consumer preference,preferred use, and potentially niche marketing. The most important traits are fruit size,husk color (ranging from yellow to purple,with pink and red most common), aril color(ranging from white to red), hardness of theseed, maturity, juice content, acidity, sweetness, and astringency.

The 'Wonderful' cultivar was discoveredin Florida and brought to California in 1896(California Rare Fruit Growers, 1997). Thisis the primary cultivar of commerce in theUnited States. I t is also grown in westernEurope, Israel, and Chile (Sepulveda et a!.,2000). 'Wonderful' is among themost deeplycolored of pomegranates in both husk andjuice, with a rich flavor, goodjuice yield, andboth sprightly acidity and slight thirstquenching astringency similar to that ofgrapefruit juice and cranberries. Many pomegranate lovers consider it to be among thebest-tasting cultivars (Karp, 2006). 'Wonderful' is nearly ideal for juicing, with excellentjuice percentage as well as quality. It also hasuseful resistance to fruit cracking after rainfall onmature fruit (Karp, 2006). Other commercial U.S. cultivars include 'Granada' (a'Wonderful' sport), 'Early Wonderful' (alsoa 'Wonderful' sport), and 'Early Foothill' .The cultivars 'Mollarde Elche' and 'Valenciana ', in Spain, are among the most widelymarketed pomegranate cultivars in westernEurope (Costa and Melgarejo, 2000). The'Valenciana' cultivar is harvested early(August), with very little sun damage and lowerrisk from pest attack or bad weather, but alsohas low yield, average to poor internal fruitquality, and small fruit size. The 'Mollar 'cultivar is harvested much later (end ofSeptember until mid November) and displaysmore sun and split damage, but has higheryield, excellent internal fruit quality, largersize, longer harvest period, and greater consumer acceptance (Costa andMelgarejo, 2000)Because of differences in quality andproductivity observed in commercial plantings, Spanish researchers have selected distinct clones of their most important cultivars.Selections were made in 1986, in the provinces of Alicante and Murcia. Numberedclones were propagated and are undergoingreplicated trials to identify the best materials(Amoros et a!., 2000).The countries of pomegranate origin growinnumerable cultivars, with many regionalfavorites. Local pomegranate germplasmcollections have been established in severalMediterranean countries, including Spain,Morocco, Tunisia, Greece, Turkey, andEgypt (Mars, 2000). India has three collections containing at least 30 accessions each(Gulick and VariSloten, 1984). Azerbaijan,the Ukraine, Uzbekistan, and Tajikistan havecollections of 200 to 300 accessions, andthe collection of the Turkmenistan Experimental Station of Plant Genetic Resources isthe largest in the world, containing more than1000 accessions (Levin, 1995). The U.S.National Clonal Germplasm Repository, inDavis, CA, has almost 200 pomegranateaccessions, including many obtained fromthe Turkmenistan collection. Included inthis collection are several types with verysoft seeds, a trait sometimes optimisticallycalled "seedless." Interestingly, in a preliminary molecular marker study, genetic variability was found to be quite low amongthe diverse cultivars in the U.S. collection(M. Aradhya, pers. comm.).

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Little detailed information is availableon pomegranates grown outside of westernEurope and the United States, althoughefforts have been made to assemble cultivarsummary information for this paper (Table1). Cultivars mentioned as important in theliterature, but with no descriptions, include'Ahrnar ', 'Aswad' , and 'Halwa' from Iraq;'Mangulati' from Saudi Arabia; and 'RedLoufani ' and 'Ras el Baghl' from Israel andPalestine (Morton, 1987).Pomegranate cuttings root with greatease, facilitating spread o f desirable clones.Efforts to graft pomegranate are reported notto be successful, but air-layering and rootsucker transplantation can be used for vegetative propagation (Morton, 1987).

CU LTNATIONPomegranate is especiallywell adaptedtoMediterranean envirouments with cool winters and hot summers, butcan be grown inthehumid tropics or subtropics, andthe plant willsurvive as far north asWashington, DC, but is

injured by temperatures less than - 1 1 C(Morton, 1987). Commercial production isconcentrated in dry summer climates, andpomegranate is extremely drought tolerantonce established, but crops much betterwith more generous moisture. Pomegranatethrives on a wide variety of soils and has ahigh resistance to salinity (Melgarejo, 2003).In all regions, newly planted trees requireadequate moisture for establishment. Forexample, in California, plantings are established in late winter to spring when soilmoisture is abundant from winter rain. Similarly plantings are made in India during themonsoon season (L.S. Dinkar, pers. comm.).Pomegranate cuttings root so easily thatunrooted cuttings are sometimes placeddirectly into the orchard (Blumenfeld et aI.,2000). Plants are trained to one to five trunksand should receive light annual pruning tomaintain the production of short spurs, whichbearmost fruit, and such pruningalso reducesthe potential for wind scarring on longwhippy shoots.Pomegranates will set a few fruit in thesecond or third year after propagation, butgenerally reach good commercial productionat 5 to 6 years. Mature yields of33 tha-1 areexpected in California commercial orchards(Karp, 2006). When possible, providing adequate moisture is recommended throughoutthe growing season (with soil moisturessimilar to those used in citrus production),which contributes to growth, production, anda reduction in splitting (LaRue, 1980). It isespecially'important to avoid drought stressduring initial fruit set (Still, 2006). Pomegranate orchards benefit from 0.2 to 0.5 kgN/tree peryear, appliedonce in fall or winter,or a split application in latewinterand in spring.High or late N application may compromisefruit maturity and color. Zinc is the only othernutrient recommended for application topomegranate in California. When Zn deficiency is evident, sprays should be applied tofoliage in spring and early summer (LaRue,1090

1980). In Israeli conditions, K20 is applied atrates similar to N (Blumenfeld et aI., 2000).Serious disease does not routinely affectpomegranate trees in California, but Alter-naria heart rot, may sometimes affect fruit(LaRue, 1980). There are two widespreadarthropodpests on commercial pomegranatesin California: 1) the flat mite Brevipalpuslewisi and 2) the leafroller Platynola stul-tana. Both these pests cause russeting andchecking on fruit. However, a number ofspecies have caused localized damage insome years. In some other regions, Viracholaspecies of moths are a severe threat andrequire multiple sprays each year (Blumenfeld et aI., 2000; S. Dinkar, pers. comm.).This moth bores into the fruit, causing widespread fungal infections in the arils andbruising on the fruit surface.Premium prices for fresh fruit areobtained only for large blemish-free pomegranates. In India, developing fruit are sometimes protected from birds and other threatsby bagging them on the tree (Morton, 1987).Another practice in India is the "MirgBahar" practice of inducing drought stressfrom December through May so that the peakof production is in October and November(L.S. Dinkar, pers. comm.). Hand thinningis practiced in Israel to produce larger andmore uniform fruit (Blumenfeld et aI., 2000),and is also practiced in Spain.Storage life o f the pomegranate is quitelong and equals the apple, and the fruits shipvery well (Morton, 1987), although bruisingcan be an issue. The pomegranate fruit is notclimacteric (Kader et aI., 1984). Harvest andstorage factors affecting postharvest qualityo f pomegranate have been summarized in arecent review (Kader, 2006).

MEDICINAL PROPERTIESAccording to Eber's papyrus (ca. 1550

BCE), the ancient Egyptians used tannin-richpomegranate root extracts for the riddance oftapeworms (Wren, 1988). Hippocrates (400BCE) usedpomegranate extractions for a widevariety of ailments, such as a plasterto reduceskin and eye inflammation, and as an aid todigestion (Adams, 1849). No discussion ofancient medical applications of plants iscomplete without mention of Dioscorides(40-90 CE), who indicates: "All sorts ofpommegranats are of a pleasant taste andgood for ye stomach" and further suggeststhe juice for" . . . ulcers, and for ye paines ofye eares, and for the griefs in ye nosthrills"(Gunter, 1934). Other traditional uses o fpomegranate products have included treatments for contraception, snakebite, diabetes,and leprosy (reviewedin Lanskyet aI., 2000).Extracts o f tannins (bark, leaves, immaturefruit) have been used to halt diarrhea andhemorrhage, whereas dried, crushed flowerbuds are made into a tea as remedy forbronchitis. In Mexico, extracts of the flowersare used as a gargle to relieve mouth andthroat inflammation (Morton, 1987). Interestingly, many of these uses are at leastsomewhat supported by recent scientific

studies (Seeram et aI., 2006). However, itmust be noted that there is no report of trialsusing pomegranate to treat snakebite.Presumably because of its association asthe " frui t of love" rather than empiricalobservation, the pomegranate has been considered a love potion in some cultures. Theprophet Mohammed advised, "Eat the pomegranate, for it purges the system of envy andhatred" (Encyclopedia Britannica, 2006c).Seemingly these properties represent amedicine we would all like to see widelyprescribed! 'Today, pomegranate juice has beenshown to contain polyphenol antioxidants(primarily ellagic acid and punicalagin) thatmay lower risk of heart disease (Aviramet aI., 2004) and may slow cancer progress(Adams et aI., 2006). The antioxidant contentof pomegranate juice is among the highest ofany foods (Guo et aI., 2003). An analysis ofdiverse pomegranate cultivars shows considerable diversity of antioxidant content, with'Wonderful ' among those displaying thehighest levels (unpublished data).

Largely because of the interest in healthbenefits of pomegranate, 40 journal publications were produced on this fruit in 2005versus 30 total from 1945 to 2000 (Schulman,2006). Many of these papers, primarilyfocusing on medical implications of pomegranate and its products, are reviewed in abook edited by Seeram et ai. (2006).OTHER USES FOR POMEGRANATESThere are a number of other useful applications for the product of the pomegranatetree. Pomegranate barkproduces tannins thathelp create Moroccan leather. Extracts of the

flowers and fruit husks have been used asdyes for textiles. Extracts of pomegranaterinds provided a major source of medievalink in Europe (Carvalho, 1999), and specialtycraft inks are still created from pomegranate.Clearly, the most widespread "nonfood"use of pomegranate is for visual aesthetics.Several ornamental plant forms have beentouched on already, and these arewidespreadin the nursery industry where pomegranate isadapted. The distinctive appearance and longlife of the mature.harvested pomegranatefruit results in theirwidespread use in tablearrangements. In the United States, this isespecially common during the Thanksgivingthrough Christmas season. The longstandingnature of this use is apparent from pomegranate's frequent inclusion in paintings andas graphic elements in architecture, for example. This visual aesthetic use is sowidespreadthat most of the pomegranates purchased asfresh fruit in the United States are likelynever actually consumed (California RareFruit Growers, 1997)!

TH E FUTUREIncreased interest in phytonutrientsappears likely to sustain and increase interestin pomegranate within the United States.

'Wonderful' juice is widely available in theHaRTSCIENCE VOL. 42(5) AUGUST 2007

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Table I. Summary of primary characteristics for pomegranate cultivars that are indicated as "important" in the literature and. for which there are reported data.Cultivar Fruit size (g) Traits Origin Reference

Amoros et aL, 2000

LaRue, 1980

Morton, 1987

Morton, 1987

Morton, 1987Gozlekci & Kaynak, 1997

Gozlekci and Kaynak, 1997Gozlekci and Kaynak, 1997

California Rare Fruit Growers, 1997

Dave Wilson Nursery, 2005;Karp, 2006

Amoros et aL, 2000

Gozlekci and Kaynak, 1997L.S. Dinkar, pers. comm.

Karp, 2006

Gozlekci and Kaynak, 1997

California Rare Fruit Growers, 1997

Costa and Melgarejo, 2000Morton, 1987

Morton, 1987

Amoros et aL, 2000Amoros et aL, 2000

Gozlekci and Kaynak, 1997

TurkeyIndia

India

SpainIndia

USA, 2-4 weeksearlier than'Wonderful'USA, 2 weeksearlier than'Wonderful'TurkeyTurkey

USA

Turkey

Spain

USA, redder, 1month earliersport of 'Wonderful'Turkey

India

USA

India

SpainSpain

Turkey

SpainUSA

505

370

272

517

405414

"Very large"

Agridulce de Oj6s 4 524 Red arils with hard seeds, Spain Amoros et aL, 2000bitter/sweet, medium acidDeep-pink arils and veryhard seeds, sweet/sourLarge fruit, red arils,sweet/sour, soft seedsMedium-large, brownish

white rind, pink-whiteariIs, seeds soft, sweetDeep-red arilswith hardseeds, bitter, high acidLarge, yellow-red rind,white arils and hardseeds, sweet

Deep-red arils,medium-hardseeds, sweet/sourDeep-red arils,medium-hard seeds,sweet/sourSour (5% TA), red ari lsDark-red skin, red arils,

sweet with low TAPink to red fruit withpink arils, soft, seeds,sweet even whenimmatureLarge pink arils, sweetwith low TA, soft seedsYellow-pink rind andpink-red arils, very softseeds, sweet/sourGolden green fruit withpink blush, pink to redarils, soft, smallseeds, sweet

Deep-red arils,medium-hard seeds,sweet/sourDark-red skin, red arils,sweet/sourLarge fruit, deep-red rind,

with deep-pink toblood-red ariIs,hard seeds, sweet/sourLarge fruit, large redarils, sweet/sourDeep-red ariIs with softseeds, sweet, low acid

Red-pink arils with softseeds, sweet, low acidRed-pink arils with soft

seeds, sweet, low acidSmall, early, but not top qualityDeep-red arils, medium-hardseeds (we would call

medium-soft), sweet/sour

Borde de Albatera

Alandi (or Vadki)AsinarBedana

Early Wonderful

Dholka

Early Foothill

Eversweet

EksilikEmar

Hicaznar

Fellahyemez

Golden Globe

Ganesh

Mollar de Elche 15

Granada

Kandhari (alsocalled Arakta)

Katirbasi

ValencianaWonderful

Mollar de OrihuelaPin6n Tierno de Oj6s 9

TA, titratable acidity.

refrigerated produce section of supermarketsand has displayed considerable sales growth.Numerous techniques are being explored toenhance postharvest life and quality of freshpomegranate (Artes and Tomas-Barbenin,2000). Consumer reluctance to open and eatintact fruits, which somesuggest is best "bestperformednaked, outdoors or in the bathtub"(Karp, 2006), has encouraged developmentof methods to blowout arils and packagethese beautiful jewels as a minimally processed fresh product (Sepulveda et al., 2000).These will soon find their way to market andwill likely be eaten as snacks and used asgarnishes in salads and savory dishes. The

preference of some consumers for cultivarswith less acid or softer seeds is also compelling consideration of more diverse cultivars,which should broaden consumer interest.When these "wonderful" properties are combined with a Food and Drug Administrationlabel as a " love pot ion" and the prophet' sprescription for curing "hatred and envy," itmay be impossible to keep up with thedemand for this amazing fruit.Literature Cited

Adams, F. 1849. Genuine works of Hippocrates.William Wood and Co., New York.

Adams , L.S. , N.P. Seeram, B.B. Aggarwa l, Y.Takada, D. Sand, and D. Heber . 2006. Pomegranate juice, total pomegranate ellagitannins,and punicalagin suppress inflammatory cellsignaling in colon cancer cel ls . J. Agr. FoodChern. 54:980-985.Amoros, A., P. Melgarejo, J.J. Martinez, F.Hernandez, and M. Martinez. 2000. Characterization of the f ruit of five pomegranate(Punica granatum L.) c lones cul tiva ted inhomogeneous soils . Opt ions Mediter raneennes Ser. A 42:129-135.

Anarinco. 2006. Pomegranat e history. I Sept.2006. .

Artes, F. and FA Tomas-Barberan. 2000. Postharvest technological treatments of pomegranate

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Bist, B.S., R. Srivastava, and G. Sharma. 1994.Variation in some promising selections ofwildpomegranate (Punica granatum L.). Hort. J.7:67-70.Blumenfeld, A, F. Shaya, and R. Hillel. 2000.Cultivation of pomegranate. Options Mediterraneennes Ser. A 42:143-147.California Rare Fruit Growers. 1997. Pomegranate. 1 Sept. 2006. .Carvalho, D.N. 1999. Forty centuries of ink. TheWorldWide School, Seattle,WA. 1Sept. 2006..Costa, Y. and P. Melgarejo. 2000. A study of theproduction costs of two pomegranate varietiesgrown in poor quality soils. Options Mediterraneennes Ser. A 42:49-53.Dave Wilson Nursery. 2005. Pomegranate1 Sept.2006. .El-Kassas, S.E., A.M. EI-Sese, A.M. EI-Salhy, andA.A. Abadia. 1998. Bearing habits in somepomegranate cultivars. Assiut 1. Agr. Sci.29:147-162.Encyclopedia Britannica. 2006a. Aphrodite. 1Sept. 2006. .Encyclopedia Britannica. 2006b. Grenade. 1 Sept.2006. .Encyclopedia Britannica. 2006c. Pomegranate. 1Sept. 2006. .

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