17

Passion Fruits

Geo Coppens d'Eeckenbrugge, Sergio D. Segura, Elizabeth Hodson de Jaramillo and Gustavo A. Góngora

The genus Passiflora (Passifloraceae) includes about sixty species p ro ­ducing an edible fruit. Several species are of ornam ental interest be­cause of the un ique and spectacular shape of their flowers, and other species are g row n for their sedative, antispasmodic, antibacterial and insect-resistant properties (Perry et al., 1991; V anderplank, 1991). This chapter deals w ith the m ain fruit-bearing species, w hich belong to the subgenera Passiflora and Tacsonia (Plate XVII, 1).

Of the subgenus Passiflora, the best know n species is P. edulis. It exists in tw o forms: the p u rp le maracuja, P. edulis, and the yellow maracuja, P. edulis f. flavicarpa. These maracujas, originally from Brazil, are now found in most tropical countries. Their fruits are consum ed both fresh and in the form of juice, ice cream, jams and pastries. The sweet granadilla, P. ligularis, originally from the Andes and Central America, is also interesting bu t is not as well k now n as the maracujas. It is cultivated in cooler regions and at higher altitudes, from H awaii to Australia and East Africa. Its fruit, the same size as that of the yellow maracuja bu t less acidic, is preferred fresh ra ther than as a juice or in processed form. The giant granadilla, P. quadrangularis, originally from the A ndean countries, p roduces a large fruit. The pulp , used for juice, and the m esocarp in the form of fruit mash, are relatively b land. It is widely cultivated b u t only for local markets. Similarly, the w inged-stem passiflora, P. alata, originally from the Brazilian p lateau and the eastern Amazon region is w idespread but only cultivated in sou thern Brazil for its pleasant tasting fruit.

The subgenus Tacsonia comprises 47 species, all of which originated from the A ndes. M ost have a d is t r ib u tio n re s tr ic ted to a l t i tu d es between 1800 and 4200 metres. Their fruit, called curubas in Colombia,

382 Tropical Plant Breeding

provide juices w ith delicate fragrance and colour and is used in various preparations. The m ost w idely g row n species, P. mollissima, is culti­vated at lower altitudes in Kenya, Hawaii, N ew Zealand and Australia, w here it is called the banana passion-fruit.

Statistics on passion fruit p roduc tion and trade are scant and in­complete, offering little infprmation about national m arkets and local consum ption (sometimes high), of any species other than maracujas. Brazil is the largest p roducer with approxim ate ly 300,000 tons, mainly the yellow maracuja, of which more than 50% is processed and con­sum ed domestically. Colombia comes second w ith an internal m arket of 70 to 80,000 tons, followed by Ecuador w ith about 50,000 tons, more than 70% of which is processed. Only p roduc ing countries have signifi­cant m arkets for fresh fruit. The limited in ternational trade m ainly in­volves maracuja juice, w ith exports ranging from 10,000 to 14,000 tons of concentrate at 50°Brix (about 10 tons of fruit are requ ired for 1 ton of concentrate). Europe is the m ain importer, accounting for 60 to 70% of export m arket, versus 20 to 22% for the U nited States.

Commercial cultivation of P. edulis began in developed regions— Australia, H awaii and Florida. Pioneer b reeding w ork based on hy­brid isation of yellow and purp le maracujas, w as followed by selection and clonal p ropagation or interspecific hybrid isa tion (Payan and Mar­tin, 1975; Winks et al., 1988; V anderplank, 1991; Knight, 1992). In Co­lombia, w ork on P. mollissima was directed tow ards the developm ent of new lines and interspecific hybrid isation (Escobar, 1981; Schoeniger, 1986). In the present decade, laboratories have concentra ted on biotech­nological m ethods (Hodson and Cancino, 1992; Cancino and Hodson, 1994; Dornelas and Viera, 1994; M anders et al., 1994; Otoni et al., 1995; Ovalle, 1995). Institutions in A ndean countries, belonging to a network u n d e r the aegis of IPGRI (International Plant Genetic Resources Insti­tute), have now begun to investigate the genetic resources of Andean passion-fruit.

REPRODUCTION AND DIVERSITY

Biology of R eproduction

Passion-flowers are recognised by their characteristic elements (Plate XVII, 1). The relative degrees of expansion of the floral cup and floral tube, w hich together consti tu te the h y p an th iu m , vary considerably betw een subgenera. The floral tube is rem arkably long in the subgenus Tacsortia. There m ay be three, five or eight sepals and petals. The ovary and the five s tam ens are borne on an androgynophore . The unilocular

Passion-fruit 383

ovary formed of three joined carpels w ith a parietal p lacentation is su rm ounted by three styles. The fruit is a globular or oval berry of highly variable size, depend ing on the species. The seeds are hard and su rrounded by an aril constituted by a juicy or mucilaginous pulp.

In m any species, rapid movements of the stigma are observed. When the flower opens, the styles are erect; they then bend, bringing the su r ­face of the stigm a close to the s tam ens, enabling contact w ith the pollinator; the styles then straighten before the flower closes. In some flowers, how ever, this m odus operandi is incomplete, or even non-ex- istent, precluding natural pollination (Fouque and Fouque, 1980; Escobar, 1981; Oliveira et al., 1983; Escobar, 1985; May and Spears, 1988; da Silva-Vasconcellos and Cereda, 1992). The female fertility of these flow­ers is relatively low, some exhibiting degeneration of the pistil, bu t male fertility remains unchanged. The ratio of male functional flowers varies during flowering, apparently dependen t on the resources the p lan t has already expended in fruit p roduction (May and Spears, 1988).

In passion fruits, the link between shape, aroma, flower colour and species of pollinator is very close. Species of the subgenus Passiflora attract m any insects but the only effective pollinators are those which, like Xylocopa, are s trong enough to reach the nectar by opening the operculum and large enough to reach the anthers and stigma. Species of the subgenus Tacsonia, on the other hand , are well adap ted for pollina­tion by hum m ingbirds (Escobar, 1992).

Species of the su b g en u s Tacsonia are genera lly se lf-com patib le (Escobar, 1992) while those of Passiflora have a self-incompatibility sys­tem, variable in efficiency, especially in P. edulis (Ruberte-Torres and Marin, 1974; Howell, 1976; Fouque and Fouque, 1980; Oliveira et al., 1983; May and Spears, 1988; Giron, 1992; da Silva-Vasconcellos and Cereda, 1992). U nder such conditions, the com bination of a high degree of pseudo-self-compatibility, w ith stigma and anthers close together, could facilitate self-pollination by com m on bees (Knight, 1992). N ever­theless, even in self-pollinating clones, the fruits formed by cross-polli- nation are heavier and more fertile. They yield more juice and the juice has a h igher sugar content (Hammer, 1987). M anual pollination of the floral buds helps overcome self-incompatibility (da Silva-Vasconcellos and Cereda, 1992).

Species of the subgenera Passiflora and Tacsonia have 18 small chro ­mosomes (Beal, 1973). Cytological analyses by Corriveau and Coleman (1988) indicated b iparental heredity of plastid DNA in P. edulis, which was further confirmed by Do et al. (1992) iri a s tudy on the chloroplast DNA in interspecific hybrids of purp le P. edulis used as female parent. In P. edulis f. flavicarpa, the transmission of chloroplast DNA is m aternal w hen used as female and paternal w hen used as male; an interaction b e tw een o rganelles of the tw o p aren ts , re su lt in g in the exclusive

384 Tropical Plant Breeding

maintenance of the chloroplast genome of P. edulis f. flavicarpa, could explain this phenom enon.

P ro paga tion and C ultiva tion Cycle

Most cultivated passion-fruit species are m ultip lied th rough seed taken from selected fruit or recovered after commercial pu lp extraction. In the case of the maracuja, p ropagation by cuttings or runners is easy to implement, b u t multiplication using seed guarantees m ore effective pol­lination because of the self-incompatibility, at the cost of a certain amount of heterogeneity. Seeds m ay undergo a dorm ancy period of one to three m onths (Schoeniger, 1986). Plantlets are produced in nurseries and, after two to four m onths, p lanted in the field where they are trim m ed. For P. edulis f. flavicarpa, the first flowering occurs six m onths after emergence and p roduc tion begins two m onths later. The maracuja cultivation cycle lasts two to four years and that of granadilla, curuba and P. alata lasts four to ten years.

C ultiva ted Species

M a r a c u j a s

P. edulis is a v igorous liana w ith stems reaching 20 to 50 or even 80 metres in length. Its leaves are deeply trilobate at the adu lt stage; the length of the central lobe is 5 to 18 cm and that of the lateral lobes 4 to 17 cm. The flowers are white, t inged violet, w ith a crow n of four or five rows of filaments, w hite above and violet at the base.

The purp le maracuja bears small globular to ovoid fruits, 4 to 9 cm long and 4 to 7 cm in diameter, w ith a m oderately resistant, sometimes brittle pericarp and a dark yellow, highly scented pu lp constitu ting 35 to 50% of the fruit weight. It is generally self-fertile w ith a relatively low yield, 5 to 10 t h a -1 y_1. Originally from sou thern Brazil, northern Argentina and Paraguay, it is adap ted to tropical and subtropical re­gions and can even be frost tolerant (winter hardy). That is w h y this cultivated form predom inates at higher latitudes and elevations, as in A ustralia and Kenya.

The yellow maracuja, P. edulis (.flavicarpa, is more v igorous than the purp le form. Its leaves and flowers are slightly larger, its tendrils con­tain anthocyanin and its flowers have more pigment. Its ro u n d to oval fruit w ith a sm ooth yellow surface is also more attractive than that of the purp le maracuja; the pericarp is h a rder and the size larger—6 to 12 cm long and 4 to 7 cm broad, and weighing 60 to 150 g. They are also less aromatic and slightly more tangy. The seeds are flatter and

Passion-fruit 385

elongate. Self-sterility is frequently observed (Beal, 1975). In Australia and Hawaii, the yellow maracuja flowers in the afternoon while the purple form flowers in the morning; flowering also occurs in different seasons, w hich is not the case in Brazil (Oliveira et al., 1987). The yellow maracuja needs h igh tem peratures, betw een 20 and 34° C, and develops better at lower altitudes. It gives h igh yields: 10 to 25 t ha-1 y_1 and, in some cases, 55 tons w ith 30 to 46% juice yield. It is more resistant to fusarium w ilt and nem atodes and is sometimes used as rootstock for the purple form. Some rootstock varieties are said to be resistant to the passion-fruit w oodiness virus, PWV (Vanderplank, 1991).

The origin of the yellow maracuja and its taxonomic position have yet to be clearly established. According to V anderplank (1991), the p res ­ently cultivated plant material originated from several fruits found in a London m arket whose seeds were sent to Argentina. In 1915, the p rog ­eny from these seeds passed through the USDA (United States D epart ­ment of Agriculture) into the United States, which redistributed them to Australia and N ew Zealand. Yellow maracuja breeding has m ost often involved direct m ass selection of this material w ith a narrow genetic base or its hybrid isation w ith purp le genotypes obtained from material exported to Australia and H awaii more than a h u n d re d years ago.

The purp le and yellow forms have frequently been crossed and spontaneous hybrids are encountered in Haw aii and Australia. The di­rection of crossing determ ines its success: P. edulis f. flavicarpa should be used as the male (Beal, 1975). The hybrids are in termediate , norm al and vigorous (Nakasone et al., 1967). Meiosis is norm al w ith the form a­tion of nine bivalents, bu t the chiasma frequency is lower in the hybrid than in the parents , which suggests slightly reduced chromosom al ho ­mology. In the Fj, 6 to 8% of the plants w ere found to be abnormal (Beal, 1975). These data, as well as differences in the phenology and acclimatisation of the two forms, indicate the beginning of differentia­tion, tem pered by the fact that equally im portan t divergences m ay be observed w ith in the purp le form in Brazil (Oliveira et al., 1987).

The varie ty concept is not well defined w ith respect to P. edulis. Most phytotechnical studies refer to two varieties that actually corre­spond to the two purp le and yellow forms. V anderp lank (1991) placed these tw o botanical forms at the same level as cultivars obtained by selection. Selected materials in Australian and especially H awaiian b reed ­ing p rogram m es have spread rapidly. The old H aw aiian clones and pedigrees described by Abeysinghe (1973) and by V anderp lank (1991) exhibit a very narrow genetic base. In Australia, the genetic base is hardly any w ider and the passion-fruit industry is totally d ep en d en t on hybrids of crosses between the purp le form and a yellow genotype that has now disappeared (Winks et al., 1988). The Purple Possum clone cultivated in Florida is also of hybrid origin (Knight, 1992). Purple

386 Tropical Plant Breeding

varieties Maloya and Galea were developed in R éunion— the first from an Austra lian hybrid and the second an introduction from Mauritius. They are resistant to Phytophthora ssp. and Fusarium spp. and tolerant to Alternaria alternata (Vuillaume, 1992).

The narrow ness of the genetic base in these varieties contrasts with the variability of those cultivated in South America, especially in Brazil. A s tudy of 10 Brazilian accessions revealed considerable variability with respect to all characters, in particular fruit weight, which m ay be 26 to 78 g for the purp le form and 17 to 93 g for the yellow. The juice yield ranges from 15 to 33% and the Brix from 15 to 16°, b u t som etim es reach­ing as high as 18° (Oliveira et al., 1987). Some Brazilian accessions of pu rp le maracuja are resistant to nem atodes. The variability observed in South America is associated w ith seed m ultiplication and open pollina­tion with effective pollinators, thus tapping the full na tu ra l allogamy potential of the plant, as well as very gentle mass selection in the field.

S w e e t G r a n a d i l l a

The sw eet granadilla , P. ligularis, is still g row ing wild from Mexico to Bolivia and Venezuela. It is a v igorous liana w ith sim ple cordate leaves. Its fruit is round to ovoid, 5 to 9 cm long, 4 to 7 cm broad , tapering tow ards the peduncle, w ith a thin pericarp, hard and brittle, light brown to orange, sometimes violet tinged, w ith small light spots or stripes. Its light grey pu lp is aromatic, slightly tangy and relished by consum ers in raw form. Lastly, the fruit has a good shelf life.

This species is usually cultivated at alti tudes of 1400 to 2200 metres near the Equator, w ith extremes of 800 and 3000 metres. It grows at average tem pera tu res of 14 to 22° C and a relative h u m id ity of 70%. It can tolerate short and very light frosts. It is said to be to lerant to para­sites and diseases of the root and collar, bu t is susceptible to w ithering du e to Nectria haematococca (anam orph ic Fusarium solani) in poorly d ra ined soils. A p lan ta tion is p roduc tive for four to eight years. The sw eet granadilla commences flowering in the n in th m on th and produc­tion starts 75 to 80 days later. P roduction reaches 10 to 15 t h a '1 y_1 at a density of 400 p lan ts per hectare. The juice yield is 30% (Bernal, 1992).

There are no commercial varieties of the sweet granadilla . Although som e su p e r io r ty p es m ay be p ro p a g a te d by c u t t in g s or grafting, m ultip lica tion is usually by seed and the p lan t a llogam y m ain ta ins con­siderable variability in plantations.

G i a n t G r a n a d i l l a a n d W i n g e d - s t e m P a s s i f l o r a

The giant granadilla, P. quadrangularis—also know n as badea or barbadine, is cultivated in the West Indies and the n o r th e rn p ar t of South America, w here it still g row s in a w ild state. It is a very v igorous liana with

Passion-fruit 387

strong climbing stems that can reach 50 m in length. Its leaves are s im ­ple, oval or oblanceolate and 10 to 25 cm long and 8 to 18 cm broad. The flowers m ay reach 12 cm: the interior surface of the sepals and petals is white, pink, red or violet; the crown m ay reach 6 cm in length. The fruit is yellowish-green, sometimes w ith a p inkish tint, ovoid to oblong. It is 20 to 30 cm long and 10 to 18 cm broad, and weighs 2.8 kg on average (H addad and Figueroa, 1972) and m ay even reach 4 kg. It develops in 62 to 85 days. The fruit mesocarp is 2 to 3 cm thick and soft and edible but b land. The pu lp is transparent, w hite to orange, sweet and slightly tangy, the taste variable bu t always less p ungen t than that of maracuja. Manual pollination is often recom m ended. This species is tolerant to Alternaria passiflorae (McMillan and Graves, 1992) and resistant to w ith ­ering bu t highly susceptible to nematodes and Xanthomonas spp. (Oliveira and Ferreira, 1991; Vanderplank, 1991).

It w ou ld appear that the giant granadilla has not been the object of breeding. However, there are several types that differ w ith respect to fruit size, mesocarp thickness and taste. Howell (1976) has described two current forms, one of which is self-fertile, p roduc ing large num bers of small 15 to 20 cm fruits; the other, which he has called P. quadrangularis var. macrocarpa, is self-sterile w ith fruit reaching 30 cm.

The w in g ed -s tem passiflora , P. alata, also k n o w n as the sweet maracuja from Brazil, where it is the second-most economically im por­tant species, is very similar to P. quadrangularis. It is a highly po lym or­phic liana, w ith thick quadrangular w inged stems. Passiflorin , a sedative, is extracted from the leaves (oval or oblong, 10 to 15 cm long and 7 to 10 cm broad). Its highly odoriferous flowers are similar to those of P. quadrangularis b u t smaller—7 to 10 cm broad and almost 15 cm in some ornamental cultivars. The fruit is oval, ovoid or pyriform, yellow to bright orange, 8 to 15 cm long and 5 to 10 cm broad. The pu lp is slightly acidic (tangy) and tasty, which explains its success in the fresh-fruit market. According to the description prov ided for five Brazilian acces­sions, fruit w eight varies from 90 to 300 g and the pu lp content from 17 to 26%. The juice at 15 to 25° Brix, constitutes 14 to 21% of the fruit. Variability is also observed in susceptibility to withering in this passiflora (Oliveira et al., 1982), and some resistant accessions are used as root- stock for P. edulis (Oliveira et al., 1994). O n the other hand , this species is attacked by nem atodes of the genus Meloidogyne and by bacteria Xanthomonas spp. (Oliveira and Ferreira, 1991). It can hybridise w ith P. edulis, p u rp le or yellow, and w ith P. quadrangularis (Rubert-Torres and Martin, 1974; Vanderplank, 1991; Oliveira et al., 1994).

388 Tropical Plant Breeding

CURUBAS

The curubas— tacsos in Ecuador, and tumbos in Bolivia and Peru—are long narrow fruits w ith a soft skin, very com m on in A ndean countries. The m ain cultivated species, P. mollissima, is a w o o d y liana w ith deeply trilobate leaves, 5 to 10 cm long and 6 to 12 cm broad. The flower is p en d an t and the corolla variable in size, w ith pink to deep red sepals and petals, 2.5 to 4 cm long (Plate XVII, 3). The crow n is reduced to a w horl of w hite tubercles on a red background. The floral tube is 6 to 11 cm long and 1 to 1.5 cm broad. The fruit is oblong, 6 to 15 cm in length and 3 to 5 cm in breadth , w ith rounded ends; it w eighs 50 to 150 g (average 80 g). The pericarp is pale yellow, occasionally green, some­w ha t pubescent, thin and supple bu t corcaceous. The pectin-rich pericarp can be processed if in a perfect state w ithou t an thracnose spots. The pulp , which constitutes 60% of the fruit, is salm on-pink to dark orange, s lightly acidic, very p leasantly scented bu t generally astringent.

The p lan t grows at alti tudes betw een 2000 and 3000 m, sometimes up to 3600 m, at average tem peratures of 12 to 15°C and relative hu m id ­ity 70 to 80%. It cannot ad ap t to w arm er climates yet is sensitive to extended periods of frost. P roduction begins at about 18 m onths. Com­mercial cultivation began in the 1950s. Fruit yield ranges from 7 t h a '1 y_1 in rural cultivation conditions (Campos, 1992) to 45 tons u n d e r the most suitable conditions. The major phy tosanitary problem s are anthra­cnose, w hich spoils the fruit, and nem atodes of the genus Meloidogyne. Being an allogam ous species, its repetitive self-fertilisation results in a serious loss of v igour (Schoeniger, 1986).

The species nearest to P. mollissima is P. tripartita, w hich is origi­nally from Ecuador and northern Peru, w here it is cultivated in house­hold gardens at alti tudes of 1800 to 3500 m. It bears a 6 to 8 cm long curuba, tapering slightly at the side of the peduncle, is dark yellow, often w ith a redd ish tint, and has a dark orange pu lp similar to that in P. mollissima (Escobar, 1981).

P. cumbalensis var. goudotiana— curuba bogotana or rosy passion-fruit, originally from the Colombian Andes, bears an obovoid curuba with a dark red skin and a small vo lum e of sweet light o range translucent pulp. It can be cultivated at a ltitudes of 1800 to 3000 m and eaten in the same w ay as P. mollissima. It tastes som ew hat like the sw eet granadilla. It is highly variable and comprises nine botanical varieties (Holm-Nielsen et al., 1988). It is resistant to fungal diseases—vine m ildew , anthracnose and Alternaria (Sañudo and Jurado, 1990). It is a llogam ous and may m anifest depression associated w ith inbreeding (Schoeniger, 1986).

Passion-fruit 389

Chem ical C om position

The chemical composition of the pu lp in different passiflora is given in Table 17.1 (Chan, 1980). Passion-fruit pu lp has a h igh glucoside and phosphorus content. The yellow maracuja has high starch content of around 2.4%, w hich increases juice viscosity and im pedes heat trans­mission du r in g pasteurisa tion and concentration, especially w hen the gélatinisation tem perature is exceeded (Idarraga, 1992). Maracujas and curuba have h igh to very high prov itam in A contents. Maracujas, bu t especially curuba, are excellent sources of v itam in C. The riboflavin and niacin contents are also substantial.

Table 17.1: C om posit ion of 100 g ram s of p u lp for the five m ost w id e sp re ad passiflora species (after Bernal, 1992; C han , 1980 and V anderp lank , 1991)

Purp lem aracu ja(P. edulis)

Yellow m aracu ja

(P. edulis f. flavicarpa)

Sweetgranadilla

(P. ligu- laris)

G iant g ranad illa (P. quad­

rangularis)

B ananapassion-

fru it(P. mollis­

sima)

W ater (g) 75-85 80-87 79-86 78-88 92Protein (g) 0.4-2.2 0.7 0.47-1.1 0.3-0.9 0.6Lipids (g) 0.1-0.7 0.2 0.1-1.5 0.2-1.2 0.1Glucosides (g) 13-21.2 13.7 12 10.1 6.3Ash (g) 0.3-0.8 0.5 0.9-1.3 0.8-0.9 0.7Calcium (mg) 3.6-13 4 7-13.7 9-10 4Phosp h o ru s (mg) 12.5-6.4 25 30-78 22-40 20Iron (mg) 0.2-1.6 0.4 0.8-1.56 0.6-3 0.4Vitamin A (IU) 700-1310 2410 0 70 1700Riboflavin (mg) 0.1-0.15 0.1 0.1-0.12 0.1 0.03Niacin (mg) 1.5-1.7 2.2 1.8-2.1 2.7-15.3 2.5Vitamin C (mg) 30 16-29 20-28 14-20 64-70Energy (kCal) 51-90 53 46-80 41 25Fibre (g) 0 0.2 0.3-5.6 0-3 .6 0.3

P o ly m o rp h ism of M olecular M arkers

Do et al. (1992), using RFLP markers, s tud ied chloroplast DNA in two P. edulis genotypes, one wild and the other cultivated, that of P. edulis {.flavicarpa as well as those of the species P. ligularis, P. alata, P. caerulea, P. coccinea, P. suberosa, P. foetida and intra- and interspecific hybrids. The size of the chloroplast genom e in maraquja has been estim ated at 110 000 base pairs. The p u rp le and yellow forms are d is t ingu ished by three restriction fragm ents as com pared to only one for the two purp le genotypes. The chloroplast genom e of P. alata differs from that of P. edulis in 41% of its sequences, while that of P. coccinea differs by only

390 Tropical Plant Breeding

29% of its sequences. The size of the chloroplast genom e of P. alata is similar to that of P. edulis: 113000 base pairs.

In studies on A ndean passifloras co-ordinated by IPGRI, several m ap p in g techniques were used: isozymes, RFLP, RAPD and AFLP. The results of p ioneering RFLP studies revealed considerable genetic poly­m orph ism for the eight species stud ied thus far. Two groups are distin­guishable: the first, w ith two subgroups, corresponds to the tw o main cultivated species in the section Tiliaefolia of the subgenus Passiflora, P. ligularis and P. maliformis; the second is com posed m ainly of accessions of the subgenus Tacsonia (I. Sanchez, pers. comm.). These results repre­sent the first step tow ards a better unders tan d in g of the organisa tion of the genus Passiflora.

R elated Species

O r i g i n o f C u l t i v a t e d F o r m s

It is quite easy to determ ine the origin of cultivated passifloras since they all still exist in a w ild state, som etim es in d irectly cultivable forms. They have often become natura lised in countries w here they w ere intro­duced for cultivation. But m any wild species are d isappearing , some w ith o u t h av in g been identified , d u e to rap id d e g rad a t io n of their habitats, notably in the A ndean valleys w here isolation has given rise to n u m ero u s endem ic species.

Even the most cultivated passifloras appear to have been domesti­cated recently. A lthough passion-fruit and flowers have been widely described, for reasons of religious symbolism, it is very difficult to ac­curately ascertain the species referred to in the ancient docum ents . The p resen t nam es are derived directly from A m erind ian nam es recorded in 1582: curubabi, badeas, chupas, etc.

W i l d a n d O r n a m e n t a l S p e c i e s

Subgenus PassifloraP. incarnata, the type species of the subgenus Passiflora and the section Incarnatae to which P. edulis belongs, orig inated in arid zones of south ­western U nited States, w here it is know n as 'm ay p o p ' . It is of interest m ain ly because of its taxonomic re la tionship to P. edulis and the resist­ance of its root to fusarium wilt and frost—at tem pera tu res as low as -16° C (V anderplank, 1991). It is also resistant to som e potyviruses to w hich P. edulis f. flavicarpa is susceptible (Winks et al., 1988; Bin, 1992). A nother floral species, P. cincinnata, whose fruit is som etim es eaten, belongs to the sam e section.

Passion-fruit 391

P. caerulea—blue passion-flower—of the section Lobatae, is one of the best-known ornam ental passion fruits in temperate regions where it was introduced in 1699. It is well know n for its cold resistance and root regrowth after extremely severe winters. Its profuse fruit is yellow to orange, the size of a hen 's egg, w ith a pu lp that is edible but bland. In South Africa, it is used as rootstock for P. edulis because of its resistance to cold, collar rot due to Phytophthora, and fusarium wilt, as well as its high tolerance against nem atodes and to saline or poorly dra ined soils (Terblanche et al., 1986). But its tendency to produce shoots at the base is problematic (Winks et al., 1988).

Species closely related to P. ligularis include the A ndean species P. tiliaefolia and two low-elevation species, P. triloba and P. palenquensis. It is difficult to d is tinguish between these species and the first three are often m istaken for one another. P. platyloba is a little know n species, found in Central America from Guatem ala to Costa Rica. The fruit is small—3 to 4 cm long and 1 to 2 cm in d iam eter—w ith a hard pericarp and a h ighly acidic pu lp (Killip, 1938). It is said to be cultivated in Florida (Howell, 1976).

Subgenus TacsoniaP. mixta, or curubito de indio, is a typical species of the subgenus Tacsonia. Highly polym orphic, it is found from Bolivia to Venezuela w here it grows at a l titudes of 1700 to 3700 m. It resembles P. mollissima and bears fruit 4 to 7 cm long and 2 to 4 cm in diameter. The pericarp varies from green to yellow and is som ew hat coriaceous; the aril is grey, yel­low or light orange. The fruit is sometimes m arketed but rarely culti ­vated. This species adapts easily to drier and w arm er climates and lower altitudes. It is resistant to anthracnose, vine-mildew, Alternaria passiflorae and probably Meloidogyne (Escobar, 1981; Schoeniger, 1986; Sañudo and Jurado, 1990).

Subgenus ManicataThe subgenus Manicata has m orphological characteristics m id w ay be­tween those of the subgenera Passiflora and Tacsonia. The species P. manicata bears a globular to oblong fruit, 3 to 6 cm long and 3 to 4 cm in d iam eter, w ith a pericarp that is coriaceous green w hen ripe. The aril is grey or orange and no t very tasty (Plate XVII, 4). It differs from species of the subgenus Tacsonia w ith respect to natura l habitat, at lower altitudes betw een 1500 and 2700 m on semi-arid A n d ean slopes from Venezuela to n o rthern Peru, and in flowering, w hich occurs in the dry season. It has adap ted to the subtropical clifnate of Florida (Howell, 1976). It is polym orphic, very h ard y and resistant to nem atodes and fungal d iseases— anthracnose, vine-m ildew and Alternaria. It can also be used as rootstock for P. mollissima (Sañudo and Jurado, 1990; Cam pos, 1992). It is self-compatible and capable of spon taneous self-pollination

392 Tropical Plant Breeding

due to tem porary contact betw een its anthers and stigma (Escobar, 1985; Giron, 1992).

Interspecific Crosses

In the subgenus Passiflora, in spite of high interspecific incompatibility, n um erous crosses have helped obtain new floral forms. The species P. caerulea, for example, has been crossed with several species, including P. alata, P. quadrangularis, P. incarnata and P. amethystina (Vanderplank, 1991). Ruberte-Torres and Martin (1974) and Payan and Martin (1975) have obtained 12 different hybrids from 42 crosses involving 7 species.

To im prove P. edulis, it is often crossed with P. incarnata. Fertile hybrids have been obtained by some researchers (Beal, 1972; Anderson, 1976; Winks et al., 1988) and sterile hybrids by others (Knight, 1991), w ho resorted to chrom osom al doubling to partially restore fertility. The two forms of P. edulis have also been crossed w ith P. cincinnata. Accord­ing to Howell (1976), the hybrid resembles the P. edulis p a ren t bu t does not flower. The hybrids obtained by Ruberte-Torres and M artin (1974) are in term edia te and flower normally. Their fruit is edible. These au­thors consider this fertile cross to be of considerable interest.

The interspecific barriers are m uch w eaker in the subgenus Tacsonia. Spontaneous interspecific hybrids are often observed betw een wild and cu l t iv a ted form s, n o tab ly b e tw e en P. mollissima, P. tripartita, P. cumbalensis, P. mixta and P. pinnatistipula (Killip, 1938; Escobar, 1981). Experimental crosses w ith P. mollissima as the female p aren t and the Fj hybrids are fertile. However, fertility declines considerabley in subse­q uen t generations, F2and backcrosses (Rt ) due to reduced flowering or fruiting, exacerbated by poor seed germ ina tion and h igh mortality (Schoeniger, 1986).

The species P. manicata can be hybridised w ith P. mollissima regard­less of the direction of crossing, and also with P. edulis if this species is used as the male parent. The p rogeny of these crosses are adequately fertile (Escobar, 1985).

VARIETAL IMPROVEMENT

Types of Varieties

Several levels of passion fruit selection are observed in rela tion to the coexistence of all dom estication stages. Most of the species, which are rarely cultivated bu t s im ply harvested , have never und erg o n e selection. C u ltiva tion of species g row n in hom e ga rd en s has resu lted in the

Passion-fruit 393

creation of some unique types, such as the large-fruited giant granadilla P. quadrangularis var. macrocarpa, which bears exceptionally large fruit. In commercialised species, such as the maracuja, sweet granadilla and curubas, breeders carry out phenotypic or mass selection w hen repeat­ing seed sowing: seeds are collected from a small num ber of good qual­ity fruits plucked from one or two high perform ing plants. Given the size of the plots, the total population is small and the selection intensity is low, especially since the p lan tation renewal cycle is long. This prac­tice and exchanges of material m aintain considerable variability in the populations.

In regions w here maracuja plantations are extensive and intensive, such as Minas Gerais in Brazil, private companies have developed syn­thetic popu la tions th rough selection of ten or even several tens of p a ­rental clones m ain ta ined vegetatively to form seed banks.

In developing countries, w here m ainly maracuja is cultivated in suboptimal climatic conditions for commercial purposes, short- and long­term program m es are im plem ented to produce hybrid clones from the purple and yellow forms; the self-fertility of these hybrids will likely ensure fruiting in m onoclonal cultivation. H owever, this w ork is being carried ou t w ith genetic bases that are m uch too narrow to result in truly new varie ties . Long-term p ro g ram m es based on in terspecific hybridisations and introgressions in the subgenus Passiflora could over­come this d raw back by w iden ing the variability bu t the inadequacy of germplasm collections handicaps efforts to identify significant charac­ters an d d o n o r genotypes. Frost resistance, c learly identif ied in P. incarnata and P. caerulea, and resistance to fusarium wilt observed in P. alata are the focus of interesting hybrid isa tion and backcrossing p ro ­grammes, with the most advanced being a rootstock selection program m e in A ustra lia (Winks et al., 1988).

Breeding Objectives

The m ain b reed ing objectives are sum m arised in Table 17.2. W hen graft­ing is carried out, they can be separated into two groups: objectives related to the rootstock— resistance to parasites and root and collar diseases— and those related to the canopy.

Genetic Im p ro v e m e n t T echniques

M e t h o d s B a s e d o n S e x u a l R e p r o d u c t i o n

An initial economic so lu tion for passion fruit selection m ay be to ra tion ­alise pheno typ ic selection by the grow er and tap the variability that

Table 17.2: B reeding objectives

394 Tropical Plant Breeding

Objective Selection criteria

P roduc tiv i ty Vigour, early m atu ri ty , p ro d u c tiv i ty (flowering, budding)Self-fertility (clonal varieties)

Fru it qua li ty A d eq u a te an d un iform size

Yield of p u lp a n d / o r juice

S u g a r /ac id i ty ratio (fresh or processed) and p u lp aroma

C olour of p u lp attractive, d a rk yellow for m aracujas, or­ange to sa lm on for cu rubas an d g ian t g ranad illa

Small seeds

Pericarp coloured , tu rgescen t (sm ooth), du rab le and re­sis tan t d u r in g transporta t ion

Resistance to fungal diseases Alternaria alternata, A. passiflorae a n d o th e r species form aracujas and curubas

Fusarium oxysporum an d F. solani for the p u rp le maracuja a n d sw eet g ranad illa

Phytophthora nicotianae and P. cinnamoni for m aracujas

Septoria passiflorae for the p u rp le m aracuja

Oidium sp. for cu rubas

Colletotrichum gloeosporioides (anthracnose) a n d Cladospo- rium herborum, especially for cu rubas

Xanthomonas passiflorae and X. campestris pv. passiflorae for m aracujas, P. alata an d g ian t g ranad illa

Po ty v iru se s for m aracu jas (PMV an d SMV) a n d sweet g ranad illa (ringspot)

Tym ovirus and c los terovirus for m aracujas

Meloidogyne incognita and M. javanica for m aracu jas , giant g ranad illa , P. alata and curubas

Rotylenchulus reniformis for the p u rp le m aracuja

Resistance to bacterial diseases

Resistance to v iral d iseases

R esistance to n em atodes

Acclim atisa tion Cold resistance for yellow a n d p u rp le m aracu jas an d frost resistance for cu rubas

exists in cultivated populations. The value of genotypes retained in various orchards is confirmed in trials carried ou t u n d e r controlled con­ditions w here they are m ultiplied through cuttings and cultivated to­gether. A s tudy of genetic variability of 110 clones selected in 9 orchards thus revealed high levels of heritability for yield and early maturity. The genetic gain anticipated by selection and direct utilisation of 24 of these clones was 29% for yield and 89% for earliness (Maluf et al., 1989). This first phase can be followed by selection based on an assessm ent of breeding value.

In the second phase, a test is conducted on lineage of half- or full- sib progeny, using six ind iv iduals per descent. Cloning, followed by

Passion-fruit 395

intercrossing of the best parents, can result in the developm ent of syn ­thetic populations. Seeds from the best individuals obtained from the best families are used in the second selection cycle (Oliveira and Ferreira, 1991). Such w ork on intra- and interfamily selection is being carried out in Brazil.

These m ethods are fully in line w ith regional developm ent objec­tives: they enable progressive quality im provem ent and increased p ro ­ductivity as the present level is generally far below the yield potential of various species. How ever, they are not suitable in terms of breeding for disease resistance.

To achieve more perceptible im provem ent and especially to intro­duce new characters such as diseases resistance, all available variability has to be assessed and sources of resistance identified. To date, work has m ainly focused on the possibilities offered at the interspecific level and rarely on intraspecific variability,despite the considerable potential. Passiflora genetic resources have only recently been collected, sampled and evaluated. It is difficult to assemble field collections due to the following constraints: considerable vegetative developm ent of lianas— each plan t requires 10 to 25 square metres to grow; difficulty in their individualisation, which complicates data collection; dura tion of the evaluation—several years of harvesting m ay be necessary to estimate the produc tion potential of a genotype.

Intraspecific crossing schemes are relatively easy to im plem ent. Crosses are easy to carry out since the m orphology and physiology of the flowers render them perfectly suitable for m anipu la tions—em ascu ­lation, pollination, labelling. Nevertheless, situations of incompatibility, as well as the low percentage of b u d d in g associated with the p ro d u c ­tion of partia lly or totally female-sterile flowers,, m ust be taken into account. Evaluation of families and individuals is subject to the same space, time and cost constraints as the base material evaluation.

For interspecific crosses, it is necessary to d istinguish betw een the subgenera Passiflora and Tacsonia. All authors agree that it is easy to obtain Ft hybrids in Tacsonia and that they have a high potential— trans­fer of resistance to fungal diseases, but the sterility and anomalies en ­countered by Schoeniger (1986) in F2 show that im provem ent at the interspecific level is a long d raw n-ou t process. Interspecific crosses in the subgenus Passiflora often require special techniques such as the use of horm ones, w hich re tard floral abscission, or intra- and interspecific double pollination (Payan and Martin, 1975). The fertility of the crosses and hybrids obtained is much lower.

396 Tropical Plant Breeding

B i o t e c h n o l o g i c a l M e t h o d s

In vitro MultiplicationThe m ain objective in tissue culture is to reduce problem s associated w ith conventional vegetative propagation, especially the ineffectiveness of using rooted cuttings in the 'subgenus Tacsonia. It is also in tended to provide a rem edy against viral diseases of maracuja.

This m icropropagation technique was first applied successfully on juven ile m ater ia l w ith frequen t fo rm a tion of calli an d the risk of somaclonal variations. On the other hand, adult material w as found to be recalcitrant and satisfactory techniques for the p ropagation of adult plants, evaluated and selected in the field, have only recently been ef­fectively developed. Cancino and H odson (1994) induced bu d multipli­cation and g row th in P. edulis (.flavicarpa from nodes and bu d s cultured in M urashige and Skoog (MS) m edium , w ith an antibiotic, cefotaxime, in the absence of g row th regulators. They subsequently ob tained root­ing on basal MS m edium .

Tissue culture m ay also provide an answ er to the problem of genetic resource conservation. Protocols have been d raw n up for in vitro collec­tions u n d er conditions of m inimal grow th conditions for several spe­cies: P. edulis (. flavicarpa, P. ligularis, P. maliformis, P. quadrangularis, P. mollissima, P. caerulea, P. erythrophylla and P. cuspidifolia. The genetic stability of the material preserved or propagated in vitro is verified by m olecular techniques using isozymes, chloroplast DNA, PCR and RFLP (Gongora et al., 1994).

C urren t efficient regeneration techniques have opened the w ay for genom e m anipulation by genetic transform ation or somatic hybrid isa ­tion. Plants have thus been regenerated by direct organogenesis from explants of leaves, cotyledons and hypocotyls of P. edulis (.flavicarpa, P. amethystina, P. giberi, P. maliformis and P. mollissima (Cancino and Hodson, 1994; D óm elas and Vieira, 1994; Ovalle, 1995). Regeneration was also obtained from m esophyll protoplasts for P. edulis (. flavicarpa (d'Utra- Vaz et al., 1993) and from co ty ledons for P. edulis (. flavicarpa, P. amethystima and P. cincinnata, w ith 40% polyploid plants regenerated in the latter case (Dornelas and Vieira, 1993). A technique for the isolation and culture of pollen pro toplasts of P. mollissima has recently been de­scribed (Espindola, 1995).

Genome Manipulation TechniquesSomatic hybrid isation betw een P. edulis (.flavicarpa and P. incarnata was achieved by pro toplast electrofusion. Analysis of m orphological m ark ­ers, leaves and flowers, and m olecular m arkers, isozym es and RAPD, confirm ed the hybrid na tu re of the regenerated p lan ts (Otoni et al., 1995). Their pollen viability is very low: about 15% versus 81 to 86% for

Passion-fruit 397

the parents. The backcross obtained w ith P. edulis f. flavicarpa is fertile, unlike the reciprocal cross, and most of the seeds p roduced do not abort.

Explants of leaves and stems of P. edulis {.flavicarpa have been trans­formed using an Agrobacterium tumefaciens strain bearing the nptll gene. Three transgenic plants were regenerated, after which they were rooted and acclim atised (M anders et al., 1994). The p lan t b iology un it of Javeriana U n iv ers ity in Colombia , in co llabora tion w ith the P lant Genetic M anipulation G roup at the University of N ottingham (UK) and the Plant Pathology D epartm ent at the University of Florida (USA), trans­ferred two genes of potyvirus proteins to P. edulis f. flavicarpa, one from PWV and the other from SMV (soybean mosaic virus). The genetic trans­formation was obtained by infection of leaf discs w ith A. tumefaciens strains bearing either of these genes as well as the nptll m arker gene. The presence of viral genes—which should confer potyvirus-resistance to regenerated p lan ts—and their expression in the p lan t are now being tested by m olecular techniques.

GENETIC PROGRESS AND DISSEMINATION OF VARIETIES

There is very little published inform ation on the deve lopm ent of the first clonal selections of maracuja in Hawaii and Australia. Some of these varieties were obtained by cloning elite individuals that were some­times spontaneous hybrids spotted in commercial fields, which implies minimal self-fertility or cultivation of a m ixture of clones.

H ybrids w ere subsequen tly deve loped be tw een the p u rp le and yellow forms, and further intercrossed (Abeysinghe, 1973). Australian production is based essentially on hybrids betw een purp le maracujas and a single clone of the yellow form obtained tow ards the end of the 1950s. They have the advantage of being productive , bu t they are sus­ceptible to Alternaria alternata and PWV. Their p ropagation by rooted cuttings transmits the virus. Grafting young P. edulis seedlings on young P. edulis {.flavicarpa seedlings has proven the only way to obtain healthy m ater ia l . At the in traspecific level, n e i th e r se lf-po ll ina t ion no r backcrossing to P. edulis has helped to obtain competitive material. The program m e on graft selection is presently restricted to intercrosses among high-yielding hybrids or their crosses w ith the resistant Tom 's Special variety.

Interspecific hybrid isation between P. edulis and P. incarnata has given rise to plants w ith cold resistance and a h igh level of virus toler­ance. These hybrids are fertile and selection of this m aterial is about to result in commercial types w ith cold resistance and virus tolerance.

398 Tropical Plant Breeding

Rootstock p roduc tion is based on the use of selections of P. edulis f. flavicarpa seedlings resistant to fusarium wilt, Phytophthora and nem a­todes, b u t sensitive to cold and susceptible to PWV. A new program m e, also based on interspecific hybrids w ith P. incarnata, has been imple­mented. At the p resen t stage, the best selection is the 3-19 derived from the F , which has v igorous grow th and is more early m a tu ring on P. edulis f. flavicarpa rootstocks bu t still possesses considerable variability. Its susceptibility to fusarium wilt is m idw ay betw eem that of P. edulis and that of P. edulis f. flavicarpa. O ther accessions of P. incarnata and of P. caerulea have been tested for hybridisation with P. edulis f. flavicarpa (Winks et al., 1988).

Concerning the sweet granadilla and giant granadilla , no breeding w ork has been described in the literature. For curuba, Schoeniger (1986) has p rov ided a detailed descrip tion of the results of crosses betw een P. mollissima, P. mixta and P. cumbalensis aim ed at incorporating genes for resistance to vine-m ildew and anthracnose. The resistant F hybrids are remarkable for their vigour, large sized leaves, stipules, bracts and flow­ers, as well as their pollen viability, which is equal to or better than that of the p aren ta l species (Escobar, 1981). H ow ever , m u ch decline in fertility in the F2 and Rt generations is due to the lack of flowering or fruiting, aggravated by poor germ ination and high mortality. Consider­able variability is obtained for different aspects including fruit charac­teristics—production, size, shape, succulence and aroma of the aril—with m any cases of transgression in the segregations and the appearance of abnorm al leaf or flower forms. Self-pollination of the best plants from the F2 and Rj generation in P. mollissima and P. cumbalensis has resulted in a third generation, which is also characterised by abnorm al germ ina­tion, lack of vigour, high mortality and increased variability, a long with the appearance of new characters unk n o w n in the parental species. Fi­nally, the results p rov ided by Schoeniger (1986) indicate nu m ero u s di­vergences betw een P. mollissima and the other two species, and show tha t— in sp ite of their resem blance and com patib il i ty—b reed in g by interspecific in trogression is a long d raw n-ou t and difficult process.

Acknowledgement: The au thors thank Catherine M athuriau for assist­ing in the m anuscr ip t preparation .

R EFERE NCES

Abeysinghe , A. 1973. C om m erc ia l p a ss io n fru it cu ltivation , p rocess ing and m arketing . J.Nat. Agrie. Soc. Ceylon, 9: 88-111.

A n d e rso n , E.R. 1976. A com parison of two species of Passiflora. D isser ta tion Abstracts In terna tiona l, 36: 4267B.

Passion-fruit 399

Beal, P.R. 1972. Two new interspecific hybrids in the genus Passiflora. SABRAO N e w s ­letter, 4: 113-115.

Beal, P.R. 1973. C yto logy of the na tive A ustra lian and several exotic Passiflora species. 2. C hrom osom e m orphology . Q u een slan d J. Agrie. A nim al Sciences, 30: 17-18.

Beal, P.R. 1975. H y b rid iza t io n of Passiflora edulis Sims an d P. edulis Sims f. flavicarpa Degener. Q u een slan d J. Agrie. A nim al Sciences, 32: 101-111.

Bernal, J.A. 1992. El cultivo de la g ranadilla , Passiflora ligularis. In: P rim er sim posio in te rnacional de passifloras. U n iversidad nacional de C olombia, Palm ira , C olom ­bia, pp . 153-161.

Bin, Y. 1992. D iseases of go ld en pass ion fruit, Passiflora edulis var. flavicarpa in Malaysia. In: P rim er s im posio in ternacional de passifloras. U n ivers idad Nacional de C olom ­bia, Palm ira , C olombia, pp. 145-146.

Campos, T.C. 1992. El culitvo de la cu ruba , Passiflora mollissima (H.B.K.) Bailey, en Colombia. Acta H orticu ltu rae , 310: 215-229.

Cancino, O. a n d H odson , E. 1994. Cultivo de tejidos y m ic rop ropagac ión en m aracuyá Passiflora edulis var. flavicarpa Degener. Tablero, Revista de l C onvenio A n d rés Bello, 18: 81-83.

Chan, H.T. 1980. P ass io n fru i t . In: T rop ica l an d S u b to rp ica l Fru its : C o m p o s i t io n , Properties a n d Uses. S. N ag y and P. Shaw (eds.). AVI Publish ing, W estport, USA, pp. 36-47.

Corriveau, J.L. a n d C olem an, A.W. 1988. R apid screening m eth o d to de tec t poten tia l b iparen ta l inheritance of p lastid DNA and results for over 200 an g io sp erm species. Amer. J. Bot., 75: 1443-1458.

Do, Y.Y., Shii, C.T. an d H u a n g , P.L. 1992. R estr ic tion p a t te rn s an d in h er i tan ce of ch lo rop last D N A in Passiflora edulis Sims and its re la ted species: the im pac t of biological research on agricu ltu ra l p roductiv ity . In: SABRAO Internat. Symp. Taipei, Taiw an , pp. 10-13.

Dóm elas, M.C. a n d Vieira, M.L. 1993. Plant regeneration from p ro to p la s t cu ltu res of Passiflora edulis var. flavicarpa Deg., P. amesthystina M ikan a n d P. cincinnata Mast. Plan t Cell Reports, 113: 23-27.

Dóm elas, M.C. a n d Vieira, M.L. 1994. Tissue cu ltu re s tud ies on species of Passiflora. Plan t Cell, T issue a n d O rgan C ultu re , 36: 211-217.

Escobar, L.A. 1981. E xperim entos p re lim inares en la h ibridac ión de especies comestibles de Passiflora. A c tualidades Biológicas, 10: 103-111.

Escobar, L.A. 1985. Biología rep roductiva de Passiflora manicata e h ib ridac ión con la curuba, Passiflora mollissima. A c tualidades Biológicas, 14: 111-121.

Escobar, L.A. 1992. La sistem ática y evolución de las passifloras. In: P rim er sim posio in te rnacional de passifloras. U n ivers idad Nacional de C olom bia , Palm ira , C o lom ­bia, pp . 51-54.

Espindola, C. 1995. Aislam iento y cultivo de p ro top lastos de po len de Passiflora mollissima (H.B.K.) Bailey. Thèse de Maestria , U nv ie rs idad Javeriana, Bogatá, Colom bia , 70 pp.

Fouque, A. an d Fouque , R. 1980. Q ue lques notes su r la grenad ille jaune, Passiflora edulis Sims. var. flavicarpa. Fruits, 35: 309-312.

Giron, M. 1992. Biología floral d e dos especies de passifloras . In: P r im er s im posio in ternacional de passifloras. U n ivers idad Nacional d e Colom bia , Palm ira , C o lom ­bia, pp . 89-93.

Gongora, G.A., H o d so n de Jaramillo, E. and C onstan tino , S. 1994. C onservación genética in vitro de passifloras s ilvestres y cultivadas. In: P rim er congreso nacional sobre b iod iversidad . U n ivers idad N acional de Colombia, Cali, C olom bia , pp. 309-314.

Haddad , G.O. an d Figueroa, R.M. 1972. A s tu d y of flowering a n d fru iting of passion fru it (Passiflora quadrangularis). A gronom ía Tropical, 22: 483-496.

Hammer, L.H. 1987. The pollina tors of the yellow passion-fru it, do they limit the suc ­cess of Passiflora edulis f. flavicarpa as a tropical crop? Proc. F lorida State Hortic. Soc., 100: 283-287.

400 Tropical Plant Breeding

H odson , J.E. a n d Cancino, E.G. 1992. M icropropagación de la cu ruba , Passiflora mollissima (H.B.K.) Bailey (Passifloraceae). U n iv e rs id ad Javeriana, C u ad ern o s de Divulgación, Bogota, C olombia, 15 pp.

H o lm -N ie lse n , L., Jo rgensen , P.M. a n d L aw esson , J.E. 1988. Flora d e E cuador. 31. Passifloraceae. U n iversity of C openhagen , C o penhagen , D enm ark , 130 pp.

How ell, C.W. 1976. Edible fru ited Passiflora a d ap te d to South Florida g ro w in g condi­tions. Proc. Florida State Hortic. Soc., 89: 236-238.

Ida rraga , H. 1992. Parám etros de ren d im ien to y ca lidad del m aracuyá com o materia p r im a in d u str ia l . In: P r im er s im posio in te rnac ional de passif lo ras . U niversidad Nacional d e C olombia, Palmira, Colom bia , pp . 207-218.

Killip, E.P. 1938. The A m erican species of Passifloraceae. Field M u seu m of Natural H istory , Chicago, USA, 613 pp.

Knight, R.J. 1991. D evelopm ent of tetrap lo id hyb rid passion fru it clones w ith potential for the n o r th tem perate zone. Hortscience, 26: 1541-1543.

Knight, R.J. 1992. C harac ters n eed ed for com m ercially successful pass ion fruit. Proc. F lorida State Hortic. Soc., 105: 280-282.

M aluf, W.R., Silva, J.R., G ra ttapag lia , D., Toma-Braghini, M., Corte , R.D., Machado, M.A. a n d C aldas, L.S. 1989. Genetic ga ins via c lonal se lection in passion-fruit. Passiflora edulis Sims. Revista Brasileira de Genética, 12: 833-841.

M anders , G., Otoni, W.C., d 'U tra-V az , F.B., Blackhall, N.W., Pow er, J.B. and Davey, M.R. 1994. T ransfo rm ation of p assion -fru it (Passiflora edulis f. flavicarpa Degener) using Agrobacterium tumefaciens. P lan t Cell Reports, 13: 697-702.

M ay, P.G. a n d Spears, E.E. 1988. A n drom onoecy a d n va r ia t io n in p h en o ty p ic gender of Passiflora incarnata (Passifloraceae). Amer. J. Bot. 75: 1830-1841.

M cMillan, R.T. an d Graves, W.R. 1992. Susceptib il ity of Passiflora spp . to Alternaria passiflorae. In: P rim er sim posio in ternacional de passifloras . U n iv e rs id ad Nacional de Colom bia , Palm ira , C olombia, pp . 123-124.

N akasone, H.Y., H irano, R. and Ito, P. 1967. Prelim inary obsrva tions on the inheritance of several factors in the pass io n -fru i t (Passiflora edulis L. a n d fo rm a flavicarpa). R eport H aw aii Agricultura l E xperim ental Station, 161: 1-11.

Oliveira , J.C. and Ferreira, F.R. 1991. M elhoram ento genético do m aracujàzeiro . In: A cu ltu ra do m aracujá no Brasil, A.R. Sao José et al. (eds.). FUNEP, Jaboticabal, Brazil, pp. 211-239.

O liv e ira , J.C., R u g g ie ro , C.K., N a k a m u ra , C.K. an d Fe rre ira , F.R. 1982. Variações obse rvadas em fru tos de Passiflora alata Ait. Proc. Torpical R egion Amer. Soc. Hortic. Sei., 25: 343-345.

O liveira , J.C., Pavani, M., Ruggiero, C. a n d Castro, R.R. 1983. Carac terização morfológica e fisico-química de Passiflora maliformis L. (m aracujá-maçã) na região de Jaboticabal (Sp). Científica, 11: 205-209.

O liveira , J.C., Ferreira, F.R., Ruggiero , C. a n d N ak am u ra , K. 1987. Caracterização e aveliação de germ oplasm a de Passiflora edulis. In: Congresso barsileiro de fruticultura. U n iv e rs id ad e E stadua l de C am pinas, C am pinas, Brazil, pp . 591-596.

O liveira , J.C., N ak am u ra , K., C en turion , M.A., Ruggiero, C., Ferriera, F.R. a n d Mauro, A.O. 1994. H ib ridação entre Passiflora alata Ait vs P. edulis Sims f. flavicarpa Deg. In: C ongresso brasileiro de fruiticultura. U niversidade Estadual de C am pinas, Campinas, Brazil, pp . 825-826.

O toni, V.C., Blackhall, N.W., d 'U tra-V az , F.B., Casali, V.W., Pow er, J.B. a n d Davey, M.R. 1995. Somatic hybrid iza tio n of the Passiflora species, P. edulis var. flavicarpa Degener and P. incarnata L. J. Experim. Bot. 46: 777-785.

Ovalle, R. 1995. O rganogénesis in vitro de Passiflora mollissima (H.B.K.) y P. ligularis Juss. a partir de discos foliares. Thèse de M aestría , U n v ie rs id ad Javeriana, Bogota, Colombia.

Payan, F.R. an d M artin , F.W. 1975. Barriers to the hyb rid iza tio n of Passiflora species. E uphytica, 24: 709-716.

Passion-fruit 401

Perry, N.B., Albertson, G.D., Blunt, J.W., Cole, A.L., Munro, M.H. and Walker, J.R. 1991.

4-hydroxy-2-cyclopentenone: an u n t i -P se u d o m o n a s and cytotoxic component from Pa ssiflora te tra n d a . Planta Medica, 57: 129-131.

Ruberte-Torres, R. and Martin, F.W. 1974. First generation hybrids of edible passion fruit species. Euphytica, 23: 61-70.

Sañudo, S.B. and Jurado, D.J. 1990. Búsqueda de fuentes de resistencia a emfermedades fungosas de la curuba en Nariño. ASCOLFI Informa, 16: 3.

Schoeniger, G. 1986. La curuba: técnicas para el majoramiento de su cultivo. Editora Guadalupe, Bogota, Colombia, 255 pp.

Silva-Vasconcellos da, A. and Cereda, E. 1992. Observaciones sobre imcompatibilidad floral y de botones en fase de pre-antésis en el maracuyá dulce, P lass iflo ra alata Dryand. In: Primer simposio internacional de passifloras. Universidad Nacional de Colombia, Palmira, Colombia, pp. 95-97.

Terblanche, J.H., Greco, N., Frean, R., Crabbe, F. and Joubert. A. 1986. Goeie nuus vir

granadillabedryf. Citrus and Subtropical Fruit Research Institute, Information Bul­letin, 164: 1-2; 4-5.

Utra-Vaz d ', F.B., dos Santos, A.V.P., Manders, G., Cocking, E.C., Davey, M.R. and Power J.B. 1993. Plant regeneration from leaf mesophyll protoplasts of the tropical woody plant, passion-fruit (Pa ssiflora e d u l is f. f la v ic a r p a Degener): the importance of the antibiotic cefotaxime in the culture medium. Plant Cell Reports, 12: 220-225.

Vanderplank, J. 1991. Passion flowers and passion fruit. Cassel, London, UK, 176 pp.Vuillaume, C. 1992. Principales resultados obtenidos y programa de investigación

sobre las passifloras en la red internacional del IRFA-CIRAD. In: Primer simposio

internacional de passifloras. Universidad Nacional de Colombia, Palmira, Colombia, pp. 73-81.

Winks, C.W., Menzel, C.M. and Simpson, D.R. 1988. Passion-fruit in Queensland. 2. Botany and cultivars. Queensland Agrie. J. 114: 217-224.