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1. Introduction 1.1. Botany and history

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The pantropical family Annonaceae that is included in the order Magnoliales is the largest family within the early-divergent Magnoliid clade with around 2400 species in 208 genera of trees, shrubs and lianas (Chatrou et al., 2004, 2012) distributed in the tropical and subtropical areas of Africa, America, Asia, Australia and Europe (Watson and Dallwitz, 1992 onwards). This abundance and diversity are positively correlated with rainfall and temperature (Punyasena et al., 2007), and their evolution has been suggested as parallel to the development of the tropical rainforest (Couvreur et al., 2011). There are several large genera in the family, i.e. Annona (150 spp.), Guatteria (265 spp.), Duguetia (100 spp.), Uvaria (100 spp.) and Polyalthia (100 spp.). From an African ancestral area before the separation of western and eastern Gondwana (Su and Saunders, 2009) and during the lower Cretaceous, Annonaceae seems to have appeared at least 110–102 Ma and started to diversify by 89 Ma (Couvreur et al., 2011). The genus Annona diversified during the late early Miocene (25.6–21.8 Ma ± 3.8) (Richardson et al., 2004; Pirie and Doyle, 2012; Li et al., 2017). Most species in the Annonaceae are medium-sized, low-branched trees, although the family also includes small shrubs, tall canopy trees and lianas. The flowers are hermaphroditic and appear singly or in small clusters and exhibit protogynous dichogamy. In addition to their importance for the production of edible fruits, interest in different species of the Annonaceae has increased in recent years due to the presence in different tissues of polyketide secondary metabolites, acetogenins, which are exclusive to this family and have shown promising cytotoxic, antitumour, antimalarial and pesticidal properties (Alaly et al., 1999; Liaw et al., 2010). Despite the great diversity of the Annonaceae, only a few Annona (the genus Rollinia has been included in the genus Annona (Rainer, 2007)) and Asimina species produce edible fruits. These include Annona cherimola Mill. (cherimoya), A. squamosa L. (sugar apple), A. muricata L. (soursop), the hybrid between A. cherimola and A. squamosa (atemoya), A. reticulata L. (custard apple), A. macroprophyllata Donn. Sm. (ilama), A. glabra L. (pond apple) and A. purpurea Moc. & Sessé ex Dunal (soncoya). The North American pawpaw (Asimina triloba (L.) Dunal) is the only genus in this family with species adapted to cold climates. Other species, such as the ylang-ylang (Cananga odorata (Lam.) Hook.f. & Thomson), are cultivated for the production of essential oils. Probably cherimoya is the most popular of those fruits and it has been considered as ‘the pearl of the Andes’ and declared as ‘deliciousness itself’ by Mark Twain (National Research Council, 1989) and even praised by a young Charles Darwin during the last stopover of the Beagle on the South American continent in Lima (Peru) in 1835 before heading for the Galapagos islands (Darwin, 1835). ‘There are two things in Lima which all travelers have discussed; the ladies “tapadas”, or concealed in the saya and manta, and a fruit called chilimoya. To my mind the former is as beautiful as the latter is delicious […]’. Cherimoya cultivation dates back to the pre-Columbian times of the Maya (south-eastern Mexico and northern Central America), Olmec (Guatemala and Mexico) or/and Izapa (Guatemala) civilizations in the Mesoamerican region (Central America). Indeed, Ruz Lhuillier (1997) suggested that the cherimoya and related species in the genus could be an important fruit in Mayan culture. Archaeological evidence such as Chimu/Inca and Moche ceramics as well as seeds have also revealed the presence of cherimoya and/or soursop in ancient Peru (Bonavia et al., 2004), although those two species are difficult to distinguish using only archaeological records (Pozorski and Pozorski, 1997) and seed anatomy can hardly be considered a discriminating test within Annona (Koek-Noorman, 1987). Based on these reports and the phenotypic diversity of cherimoya in the inter-Andean valleys of southern Ecuador and northern Peru, that region has been considered as the area of origin of the cherimoya (Popenoe, 1921; National Research Council, 1989; Van Damme and Scheldeman, 2000; Bonavia et al., 2004). However, if that were the case, cherimoya would then be the only representative of the Atta section of Annona growing naturally in South America since the remaining species of this clade only occur naturally in Central America and the Caribbean Region. In fact, recent studies on molecular genetic diversity show higher diversity in Mesoamerican cherimoya accessions compared to the diversity found in South America, strongly supporting the Mesoamerican origin of cherimoya and a pre-Columbian movement of plant material (probably seeds) to South America that resulted in a secondary centre of diversity in the Andean region (Larranaga et al., 2017).

The English name cherimoya derives from the Spanish ‘chirimoya’ that probably is a quechua (the main language of the Incan empire) word with a meaning of ‘cold fruit or seed’ (Pozorski and Pozorski, 1997; Bonavia et al., 2004). The cherimoya and related species are known in Central America as anona. In fact, Linnaeus used this word to name the genus Annona but claimed that he was referring to the Latin word ‘annona’, which means ‘the harvest of a year’ (Linnaeus, 1737).

From its area of origin, cherimoya cultivation has expanded into areas with frost-free Mediterranean climates where it is grown under irrigation. From America, the cherimoya was introduced to continental Spain between the 16th and 18th centuries with a first record in 1757. From there, the crop was probably distributed to Italy, Madeira (Portugal), the Canary Islands, Algeria and Egypt. In Italy, the first cherimoya plantation was in the region of Reggio Calabria in 1797 and from Italy it was introduced to Libya, Eritrea and Somalia (Morton, 1987).

Cherimoya is an evergreen tree (Fig. 3.1.1a) briefly deciduous in Mediterranean climates. The tree sheds the leaves for a couple of months around the beginning of spring and just before flowering. The trees can be up to 7–8 m. The leaves are single and alternate, with the axillary buds hidden beneath the short leaf petioles. The flower buds develop in the leaf axis after leaf unfolding. The basal nodes are differentiated almost 1 year prior to flowering and the distal buds differentiate in synchronization with the shoot (Higuchi and Utsunomiya, 1999). The flowers are fragrant and solitary or in groups of two or three and appear mainly with new growth flushes but also on old wood. The flowers show three fleshy, greenish outer petals and three smaller inner petals. The cherimoya flower is hermaphroditic with a central pyramidal gynoecium composed of up to 300 fused carpels and a basal helical androecium with stamens surrounded by two whorls of three petals. Cherimoya flowers show protogynous dichogamy (Wester, 1910; Schroeder, 1971), a common feature in the Annonaceae (Gottsberger, 1999), and often present in basal/early-divergent angiosperms (Endress, 2001), with hermaphrodite flowers in which female and male organs do not mature simultaneously generally preventing self-fertilization in the same flower. The cycle of the flower is completed in 2 days; in the first day the flower is in preanthesis (Fig. 3.1.1b) with the petals tightly closed and it passes to the female stage about midday (Fig. 3.1.1c). This phase lasts for c.30 h and on the second day the flower switches from the female to the male stage (Fig. 3.1.1d), when the anthers dehisce, around 4–5 pm under Mediterranean conditions. Cherimoya flowers of the same genotype usually open synchronously, and transfer of pollen between different flowers of the same genotype is difficult (Lora et al., 2011a). This synchronization is broken by average temperatures >22°C. The length of stigmatic receptivity can also be affected by temperature and relative humidity increasing with increasing humidity and decreasing at higher temperatures (Lora et al., 2011a). Phenological developmental stages have been described for A. cherimola (Cautín and Agustí, 2005) and A. squamosa (Liu et al., 2015). The other cultivated Annona spp. are similar to cherimoya in tree height and flowering behaviour.


Fig. 3.1.1. (a) Adult tree of Annona cherimola. (b) Flower during the earliest hours of the first day of the flowering cycle in a prefemale/preanthesis stage. (c) Flower during the first and second day of the flowering cycle in a female stage. (d) Flower in a male stage of the cycle just after anther dehiscence that occurred at 5–7 pm on the second day of the cycle.

The final pollen development period in cherimoya is also highly influenced by environmental conditions. Pollen shows an unusual mixture of bi- and tricellular pollen at anther dehiscence (Fig. 3.1.2), and this ratio of both types of pollen can be modified by temperature. Therefore the percentage of tricellular pollen increases with temperature and decreases at lower temperatures (Lora et al., 2009a, 2012). The tricellular pollen has a short viability and is highly sensitive to desiccation, a common characteristic in other species with tricellular pollen and is difficult to store (Lora et al., 2006). Environmental effects on pollen development have also been reported in A. squamosa (Rodrigues et al., 2018).


Fig. 3.1.2. Fluorescence micrographs of DAPI (4 ‘,6-diamidino-2-fenilindol)-stained pollen tube of in vitro pollen germination of Annona cherimola. Pollen tubes 30 min after sowing in germination medium in vitro with (a) two and (b) three nuclei. The generative nucleus is shown with a red arrow, and the vegetative nucleus with a white arrow. Bar = 40 μm.

The short cycle of the flower is also found among other members of the Annonaceae family having protogynous dichogamy (Vithanage, 1984; Murray and Johnson, 1987; Decraene and Smets, 1990; Kiill and Costa, 2003; Pang, 2014) with the most common pattern of 2 days (Endress, 2010). However, the flower of pawpaw, which also shows protogynous dichogamy, is characterized by a very unusual prolonged flowering cycle with an anthesis duration of 12–15 days in which the stigma is receptive for a short period (Losada et al., 2017). Other Asimina species show a similar long protogynous dichogamy period (Norman and Clayton, 1986; Norman et al., 1992). While protogynous dichogamy is a mechanism to prevent self-pollination, pawpaw also shows self-incompatibility (Willson and Schemske, 1980) although several cultivars are reportedly self-compatible (Pomper and Layne, 2010).

The knowledge of flowering and flower development and their environmental dependency is crucial for an optimal management of these crops. In fact, inadequate pollination is one of the most important factors limiting commercial production of Annona species in most growing areas. Thus, hand pollination with pollen and stamens together was first proved successful by Schroeder (1943) and currently is common for commercial production in most countries (Schroeder, 1971). Natural pollination often produces asymmetric fruits in which not all the carpels are pollinated. Cherimoya pollen has a low longevity, although pollen can be stored at low temperatures for several months (Lora et al., 2006). Studies on the final pollen development stages (Lora et al., 2009b, 2012) and on stigmatic receptivity (Lora et al., 2011a) indicate that flowers should be collected at the female stage in the morning of the first day of the cycle and kept at room temperature until the following day, when pollen can be used to pollinate flowers at the female stage early in the morning.

Species in the Annonaceae are generally entomophilous. Most of the pollinators in Annonaceae are beetles (Gottsberger, 1999) and their size is determined by the size of the flower. Thus, small flowers can be pollinated by small beetles such as Nitidulidae, Curculionidae or Chrysomelida, whereas larger flowers are visited by big beetles such as Dynastinae (Gottsberger, 1999). In the case of Annona (Morton, 1987; Kiill and Costa, 2003) the flowers are generally pollinated by Nitidulidae that breed and feed on decaying fruits or sap flows (Peña et al., 2002). Some of them, such as A. muricata (soursop), are pollinated by Dynastinae. Other beetles, such as scarab beetles (Scarabaeidae), weevils (Curculionidae), cucujids (Cucujidae), rove beetles (Staphylinidae) or anthicids (Anthicidae), can also participate in pollination of fruit crops in this genus (Peña et al., 2002). The pollinators are generally attracted to the strong scent that is produced by endogenous heat production during flowering. The odour has been described as ‘fruity’, ‘aromatic’, ‘sweet’ and ‘mushroom-like’, but some Asimina species, such as pawpaw, have a ‘yeasty’ odour (Goodrich and Raguso, 2009; Goodrich, 2012). In the case of pawpaw, flies are the main pollinators, but pawpaw flowers are also visited by beetles and wasps (Willson and Schemske, 1980).

Fruit crops within Annona are fleshy and aggregated with several seeds formed mainly by reticulate endosperm and a tiny embryo. Cherimoya fruits are compound conical or heart-shaped with a sweet and juicy white flesh. The skin may be smooth with fingerprint-like markings or covered with conical or rounded protuberances. Those differences result in different exocarp types described in cherimoya (Schroeder, 1943; Bioversity International and CHERLA, 2008): laevis (smooth), impressa (slight depressions), umbonata (small protrusions), tuberculata (medium protrusions) and mamillata (large protrusions). Laevis and impressa fruits are preferred by consumers. Each segment of the flesh surrounds a single hard black seed (Morton, 1987). Soursop (A. muricata) produces the largest fruits in the genus, that can reach up to 1.5 kg (Worrell et al., 1994). Pawpaw trees can reach up to 10 m with a pyramidal growth habit in sunny locations. The fruits are botanical berries, sweet, with a unique exotic taste that resembles a combination of banana, mango and pineapple.

Biotechnology of Fruit and Nut Crops

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