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Utilization of biotechnological tools in soursop (Annona muricata L.)
Scientia Horticulturae 245 (2019) 269–273
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Scientia Horticulturae journal homepage: www.elsevier.com/locate/scihorti
Review
Utilization of biotechnological tools in soursop (Annona muricata L.) a,b
T
b
Guillermo Berumen-Varela , Miguel Angel Hernández-Oñate , ⁎ Martín Ernesto Tiznado-Hernándezb, a
Unidad de Tecnología de Alimentos-Universidad Autónoma de Nayarit, Ciudad de la Cultura S/N., Tepic, Nayarit 63155, Mexico Coordinación de Tecnología de Alimentos de Origen Vegetal, Centro de Investigación en Alimentación y Desarrollo, A. C. Carretera a la Victoria Km 0.6, Hermosillo, Sonora 83304, Mexico b
A R T I C LE I N FO
A B S T R A C T
Keywords: Biotechnology Disease Micropropagation Postharvest treatments Soursop Transcriptomics
Global interest in soursop (Annona muricata L.) had increased considerably in recent years due to its medical properties. Nevertheless, there is a rather scarce information regarding genomic and genetic resources. Soursop fruit shows a short postharvest shelf life due to the high respiration rate, ethylene production and fungi attack which increases the postharvest fruit losses and makes difficult its commercialization at international markets. Besides, postharvest handling and processing of this fruit is deficient due to the lack of scientific information in physiology, diseases and molecular biology. In this regard, the utilization of biotechnology tools should be integrated to increase the genetic variability and help in the design of improved agronomic practices with the goal to improve yield, reduce fungi attack and prolong the postharvest shelf life of soursop in the near future. The objective of this review is to discuss the most important biotechnological aspects of Annona muricata L. including fruit physiology, postharvest technologies, disease control, micropropagation and the utilization of tools derived from the DNA recombinant technology.
1. Introduction In the last few years, one of the most studied species of the Annonaceae family is Annona muricata L. whose common name is soursop, graviola, guanábana (names in English, Portuguese and Spanish, respectively) among others. Soursop is a climacteric fruit which is usually consumed fresh due to its rather short postharvest shelf life. Because of this, several efforts have been made in order to delay deterioration by using conservation technologies and appropriate postharvest handling. However, other characteristics had reduced the commercialization such as low fruit quality, pathogen attack, irregular production and low yield. In this context, micropropagation can be a good strategy to increase soursop production and reduce costs. However, there are still many challenges to confront and the need to generate biochemical, molecular and genomic information in order to understand the pre- and postharvest physiological changes of soursop fruit to prolong shelf life. 2. Fruit composition and description The height of a soursop tree varies from 3 up to 10 m tall, possess
oval leaves with axillary buds, reaching a full size of 6 cm wide and 12 cm long (Jiménez-Zurita et al., 2017a). The soursop is a spiny aggregate fruit constituted of a berry product of multiple ovaries (Thompson, 2003). The fruits can have a length of 30 cm with a weight up to 5 kg. Phenotypically, is a dark-green shell with an oval, conical or irregular heart form, which is the product of an inadequate development of the carpels (Jiménez-Zurita et al., 2017a). The white pulp makes up more than 80% of the fruit, which is mainly constituted by water, non-reducing sugars and carbohydrates. Paull (1982) reported ºBrix values from 10 to 16 and pH values from 3.6 to 5.8 in the soursop pulp during three days of ripening. On the other hand, Jiménez-Zurita et al. (2016) characterized the postharvest physiological parameters of soursop at Nayarit, México, reporting average values of 8.3 N in firmness, 10.9 in total soluble solids, pH of 3.6 and 0.7% of titratable acidity. Proximate analysis performed in soursop fruits harvested in physiological maturity reported average values of 80.71 for moisture (g/100 g fresh weight of edible food). Further, 0.82 of protein, 0.77 of fat, 74.6 of soluble sugars and 3.32 of ash in grams per 100 g dry matter of edible portion (Moreno-Hernández et al., 2014). Besides, vitamins, carotenoids, flavonoids and lipophilic antioxidants compounds have been reported in soursop fruits (Correa-Gordillo et al., 2012). Recently,
⁎
Corresponding author. E-mail addresses: [email protected] (G. Berumen-Varela), [email protected] (M.A. Hernández-Oñate), [email protected] (M.E. Tiznado-Hernández). https://doi.org/10.1016/j.scienta.2018.10.028 Received 16 August 2018; Received in revised form 12 October 2018; Accepted 13 October 2018 0304-4238/ © 2018 Elsevier B.V. All rights reserved.
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Fig. 1. Soursop fruit development from flower to physiological maturity.
shelf life in optimal conditions for consumption (de Lima and Alves, 2011; Jiménez-Zurita et al., 2017a). A correct handling, right storage conditions and other postharvest technologies to delay fruit ripening need to be designed and utilized during soursop commercialization to avoid postharvest fruit losses and bad quality. Nowadays, several technologies have been used to prolong the shelf life of soursop, including refrigeration, waxes, emulsions, 1-methylcyclopropene (1-MCP) usage and combinations of all of these treatments. In this regard, Castillo-Ánimas et al. (2005) evaluated the harvest index (light and dark-green) in combination with different temperatures and distinct formulations of candelilla wax and growth regulators. They found that only candelilla wax delayed fruit maturity and reduced weight loss. Candelilla wax formulation reduced CO2 production in fruits with a weight range of 560–750 g and harvested at dark-green, indicating that wax formulation was able to delay the onset of the respiration climacteric peak. However, chilling injury in soursop fruits harvested at the dark-green stage and stored at temperatures between 16 to 18 and 12 to 14 °C was observed. Furthermore, the fruits harvested at light green stage showed chilling injury only at 12–14 °C. Based on all the previously mentioned, the physiological stage of the fruit at harvest time and store temperatures are two important factors that affect shelf life in soursop. In a recently published paper, Jiménez-Zurita et al. (2017b) analyzed the physiological and biochemical parameters at different temperatures (15 °C and 22 °C) during the postharvest shelf life of soursop fruits. It was found an increase in the postharvest shelf life up to 8 days with no chilling injury or alteration on the ripening phenomena in fruits stored at 15 °C and then at 22 °C. On the other hand, it was studied the effect of 1-MCP treatment and storage at 16 °C and 25 °C on the postharvest shelf life of soursop fruit. It was found that fruits treated with 200 nanoliters per liter (nLL−1) and 400 nLL−1 of 1-MCP and stored at 16 °C, showed a 7 days delay to reach the mature stage without chilling injury (Espinosa et al., 2013). Taken together, it is possible the utilization of low-temperature technology to prolong the soursop shelf life without adversely affect the fruit quality. Besides, several studies using 1-MCP in combination with waxes and emulsions have been carried out to increase the soursop postharvest shelf life, described next. Lima et al. (2004) studied the effect of 200 nLL−1 of 1-MCP and polyethylene wax during storage at 15.4 ± 1.1 °C during 0, 4, 8, 11, 13 and 15 days on soursop fruits. The change in total soluble solids was delayed by all the treatments whereas no change in titratable acidity, pH, total soluble sugars and reducing sugars was recorded. Tovar-Gómez et al. (2011) evaluated the utilization of carnauba wax type III, carnauba wax with silicone oils, candelilla wax and 1-MCP one by one or in different combinations on the physiological parameters of soursop during postharvest. It was found that 1000 nLL−1 for 12 h of 1-MCP in combination with the emulsions delayed fruit ripening between six and seven days as
great interest has been focused on pharmacological compounds in A. muricata L. Coria-Téllez et al. (2016) mentioned that 212 bioactive compounds have been reported in soursop, from which acetogenins, alkaloids and phenols are the most prevalent. Moreover, 37 volatile compounds have been found in soursop pulp, mainly aromatic and aliphatic esters (Cheong et al., 2011). The importance of these compounds is currently being studied to obtain more information about the therapeutic potential of soursop. 3. Fruit growth and ripening Soursop needs a warm and tropical climate for its development. The pollination in soursop is complex, causing low fruit set and in consequence low yield. Climate conditions of 25 °C temperature and 80% of relative humidity (low temperature, high humidity) can improve the pollination process (Janick and Paull, 2008). The soursop is a climacteric fruit and the time of harvesting is established based on the skin color of the fruit. According to Worrell et al. (1994), after the soursop flowers are pollinated, they have a quiescent stage (period of eco dormancy after fertilization of the blossom) of around 6–15 weeks (Fig. 1). After this, the fruit reaches half of its final size. The soursop fruits have a life cycle of around 105–150 days (15–21 weeks) from post-anthesis quiescent stage to physiological maturity (Fig. 1). It is frequently manually harvested at physiological maturity, and usually the fruit reaches the peak of ethylene production at 5 or 6 days after harvesting (Paull, 1982). Being a climacteric fruit, it shows a high respiration rate and ethylene production during ripening. In this regard, Bruinsma and Paull (1984) have shown that ethylene production is detectable from two to three days after harvesting. Worrell et al. (1994) found that mature fruit shows a biphasic respiratory climacteric, with a start of CO2 production of 100 mL kg−1 h−1 (day zero) and increasing to 350 mL kg−1 h−1 (day four) at 25–30 °C. The peak of ethylene production was reported between the fourth and sixth day after harvesting, with values ranging from 250 to 350 mL kg−1 h−1 (Márquez Cardozo et al., 2012; Worrell et al., 1994). In agreement with the data mentioned above, the average shelf life of the Annonaceae family is around 4–9 days with a storage temperature of 15–20 °C (Pareek et al., 2011). 4. Postharvest handling and technology The soursop is a very perishable fruit, and that is why it requires a careful handling from harvest to consumption (de Lima and Alves, 2011). Probably, the most important factor that affects the quality of the soursop is the precise time in which the fruit is physiologically mature. For instance, a fruit harvested immature will show an irregular maturation and a bad taste in the pulp as a consequence. Furthermore, when the fruits are harvested ripe, they show a reduced postharvest 270
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and efficient propagation of soursop. The cherimoya (Annona cherimola) is the most studied specie of the family Annonaceae, although it shows low morphogenic response and low rooting percentage which makes difficult to induce the complete organogenesis from an explant (LópezEncina et al., 2014). One of the first reports regarding in vitro micropropagation of soursop was carried out by Bejoy and Hariharan (1992). In this work, hypocotyls were used as an explant. They recorded the induction of 4.8 shoots in average per explant after 35 days of culture by using 1X of MS including 2 mg L−1 of benzylaminopurine (BAP) and 0.1 mg L−1 of naphthalene acetic acid (NAA). Moreover, 1X MS medium containing 30 g L−1 sucrose, 8 g L−1 agar and 9.8 μM of Indole3-butyric acid (IBA) was used for root induction, obtaining 2–6 roots in a range of 30–35 days. Lemos and Blake (1996) established the conditions for micropropagation of soursop, using hypocotyls and nodal cuttings as explants. On hypocotyls, woody plant medium (WPM), developed by McCown and Lloyd (1981) supplemented with 2 mg L−1 of BAP and 0.5 mg L−1 of NAA induced shoots elongation after six weeks of culture. On nodal explants, same BAP concentration in combination with 0.1 mg L−1 NAA induced shoots formation. Moreover, it was also found that activated charcoal before rooting and the addition of galactose (as a source of sugar) to the root medium improved the root induction. Furthermore, Abubacker and Deepalakshmi (2017) established a micropropagation protocol for soursop using leaf base segments. MS medium with BAP 1.5 mg L−1 and 2,4-D 2.0 mg L−1 induced callus tissue growth. This is the first report in which the induction of callus was recorded. Shoot elongation was accomplished with 1X MS medium supplemented with BAP 1.0 mg L−1, Kinetin 0.5 mg L−1 and IBA 1.5 mg L−1. The rooting medium was composed by 1X MS medium with IBA 2.0 mg L−1, NAA 0.5 mg L−1 and BAP 1.0 mg L−1. In both articles previously mentioned, the plantlets were transferred successfully to the greenhouse. Micrografting technique is carried out by collocating a meristem or other type of explant over a decapitated rootstock to stimulate the in vitro development of the tissue (Hartmann et al., 1997). This technique is frequently utilized for the in vitro micropropagation of recalcitrant species. Acosta Rangel et al. (2011) utilized the monophasic micrografting approach to stimulate the growth of Annona muricata L. However, rooting of Annona muricata L. was not possible. As it has been discussed, BAP and NAA concentrations appear to be very important hormones for the induction of shoots and roots on the Annona muricata specie. However, it is necessary to improve the rooting protocol, because most methods have shown problems to obtain a high percentage of rooting. Because the genotype, type of explant and hormone concentration of the medium affect the plant regeneration system, the development of an efficient tissue culture protocol for the in vitro micropropagation of A. muricata is still needed to establish an orchard with individuals of the same genotype.
compared with the control. Further, these fruits reached the mature stage after 15 days of storage in comparison with the control that reached the mature stage in a range of 8–9 days. In another study, Montalvo-González et al. (2014) did not record chilling injury in the pulp of fruits treated with 1500 nLL−1 for 12 h of 1-MCP in combination with candelilla wax or beeswax diluted with water and stored at 16 °C. Besides, Moreno-Hernández et al. (2014) evaluated the proximate analysis (moisture, protein, fat and ash content), soluble sugars, total dietary fiber, vitamin C, polyphenols, and antioxidant capacity of soursop fruits treated with 1-MCP and wax emulsions. It was recorded that the combination of 1-MCP and flava wax prolonged the shelf life without affecting the nutritional parameters. Based on all of the studies just mentioned, it seems that a combination of low-temperature storage, waxes and 1-MCP is required to increase the soursop postharvest shelf life in order to allow the fruit commercialization in optimal quality conditions and preserve the nutritional values. Nevertheless, further studies need to be done with the aim to design an optimal treatment to increase the soursop postharvest shelf life with good organoleptic characteristics and nutritional quality. 5. Soursop postharvest diseases Soursop fruits are infected by numerous fungi species, which have been isolated, identified and characterized. Cyriacus and Kingsley (2010) identified several fungi on the exocarp and mesocarp of mature green soursop fruits from Nigeria, namely: Aspergillus flavus, Aspergillus niger, Botryodiplodia theobromae, Colletotrichum sp., Fusarium solani, Mucor sp., Penicillium chrysogenium, Penicillium sp., Rhizopus stolonifer among others. Moreover, Nweke and Ibiam (2012) found that soft-rot disease of the soursop fruit was due to the attack of the fungi Colletotrichum gloeosporoides, Rhizopus stolonifer and Aspergillus niger. On the other hand, flowers and fruits of soursop are susceptible to a disease called anthracnose caused by the fungi Colletotrichum gloeosporoides. In this context, a study was carried out to identify the presence of Colletotrichum species from different tissues of soursop by PCR amplification using the sequences of the ITS region. Also, anthracnose severity was evaluated. The Colletotrichum species identified were: C. theobromicola, C. tropicale, C. siamense, C. gloeosporioides among others. Among these, C. theobromicola was the most pathogenic specie inducing almost 76% of anthracnose severity on soursop trees (Álvarez et al., 2014). From above, it is clear that. the most important fungi disease of soursop fruit is caused by Colletotrichum species, so more studies are needed to develop strategies to control the disease caused by these fungi. In this regard, Ramos-Guerrero et al. (2018) evaluated the in vitro effect of resistance inductors such as chitosan, salicylic acid and methyl jasmonate (alone or in combination) on the infection by Colletotrichum gloeosporioides and Rhizopus stolonifer isolated from soursop fruits. The authors showed that all treatments inhibited the conidial germination more than 75% in C. gloeosporioides and 100% in R. stolonifer. Moreover, in both fungi, a range of 81–96% in vitro growth inhibition was observed with a treatment of 1.0% chitosan alone or in combination with salicylic acid or methyl jasmonate. These results clearly showed the in vitro effect of these treatments over the fungi inducing soursop anthracnose. Further, in vivo studies are required to know whether these treatments are equally effective on the fungi infecting the soursop fruit.
7. Genetic diversity The molecular diversity of the specie Annona muricata soursop is still largely unknown. The evaluation of genetic variation of crop species is fundamental for the design of a successful plant breeding program because it helps to choose parental lines for the genetic crosses with the goal to induce a much larger variation in the progeny (Boora and Dhillon, 2010). Nowadays, there is a lack of information about the genetic characteristics of soursop commercial varieties partially due to the very low knowledge of the species genome. However, DNA analysis has been carried out on soursop germplasm collection in order to identify and characterize the genetic diversity of cultivars or accessions, using random amplified polymorphic DNA (RAPD). This technique had been shown to be a quick, low cost and easy method for the detection of DNA polymorphism and categorization of different genotypes. Suratman et al. (2015) analyzed the genetic variation of seven soursop populations from Indonesia. As a result, the different populations were classified into three clusters, in which one of the clusters was shown to
6. Micropropagation Soursop propagation is usually carried out by seed (Paull and Duarte, 2011). In Mexico, the large existing genotype variability of soursop fruits had been generated by seed propagation (EvangelistaLozano et al., 2003). The multiplication of Annona muricata L. by seed is preferred because propagation through traditional methods such as layering, budding, grafting, shoots and root cuttings are very slow and expensive (Zobayed et al., 2002). For this reason, the micropropagation techniques by tissue culture can be an alternative method for the rapid 271
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multidisciplinary international consortium generated the transcriptomic data of 1000 plants species, including species from the clade Viridiplantae, which includes green algae and flowering plants, and represents nearly one billion years of evolution (Matasci et al., 2014). Within this project, the A. muricata leaves transcriptome was sequenced. The de novo transcriptome assembly revealed 92,924 transcripts with a total assembly length of 51.12 Mbp. The transcripts show a length range from 100 to 17,040 bp (mean length of 498.6 bp), an N50 value of 1558 bp and GC percentage of 42.8%. Moreover, only 17.6% (16,353) transcripts have an open-reading frame analysis (Matasci et al., 2014). Although this work represents the first transcripts sequences generated in the soursop crop, sequence annotation was not carried out. Nevertheless, this effort represents an important advance in the research of this crop, that together with the transcriptomes of A. squamosa (Gupta et al., 2015; Liu et al., 2016, 2017) represent the unique available transcriptomics data in species of the gender Annona, giving information that promises a better understanding of the biology of these crops, which will be invaluable for both academic research and biotechnology industry.
be genetically more distant than the others. Furthermore, it was found a low genetic diversity within the population of each cluster. Similar results were found by Hasan et al. (2017) in which Annona muricata from 9 accessions of West Java and Indonesia, were classified in two main clusters based on the dendrogram from the similarity matrices. Furthermore, Brown et al. (2003) estimated the genetic variability of nine soursop accessions, seven from Venezuela and two from Brazil. It was recorded that some of the Venezuelan accessions were found to be genetically distant from the Brazilian accessions. Furthermore, the nine accessions were grouped into two different clusters. The first cluster was grouped with five Venezuelan accession and two Brazilian accessions. The remaining two Venezuelan accessions (The Palmarito 4 and Amado) were clustered with other Venezuelan germplasm. Moreover, Brazilian accession showed no significant variability among them. In a recent study, five species of Annonaceae: A. cherimola, A. reticulata, A. muricata, A. atemoya and A. squamosa, collected from different locations of India, were analyzed for molecular diversity analysis using RAPD and simple sequence repeats markers. The molecular data revealed seven clusters showing a large genetic diversity among all Annonaceae genotypes evaluated (Anuragi et al., 2016). As it has been observed, exists a large molecular variability among the species of the Annonaceae family. Moreover, it seems that cultivar, accession, as well as the place of the genetic population, are related to genetic diversity. However, the few studies carried out in A. muricata suggests a low genetic variation, although the creation of a germplasm collection and further studies need to be performed in order to obtain more information regarding the molecular diversity of A. muricata.
9. Future perspectives Even when during the last years, studies of the Annona muricata L. had increased, major efforts are required to uncover the transcriptomic and genomic sequences of the specie. The improvement of DNA sequencing technologies and the advances in genomics and transcriptomics will make possible to obtain a better understanding of the Annona muricata L. genes expression patterns, which will provide a large amount of valuable biological information that can be used in several ways. For instance, it will allow the design of strategies directed towards the improvement of important agronomical traits of the crop such as resistance to pathogen attack, uniform flowering, reduction in fruit drop percentage, higher fruit postharvest shelf life, among others. In this sense, in our research group, we are carrying out the creation and analysis of a soursop exocarp’s transcriptome in three stages of development: physiological maturity, ripening and senescence. This main goal of the project is to identify genes playing a role in the biosynthesis of cuticle components. We believe that this soursop transcriptome will establish the molecular and genetic basis to begin a soursop breeding program in order to create a soursop variety, with a better and longer postharvest shelf life, in such a way that it will be possible to increase the production for national consumption and for fruit exportation to international markets.
8. Genomic sequencing Since the first plant genome sequence was published (ArabidopsisGenome-Initiative, 2000), the number of plant genomes sequenced has increased continuously. This has been possible thanks to the improvement in the sequencing technologies in terms of cost and speed; the storage capacity and the bioinformatics tools for sequence analysis. All of this gave rise to the plant genomics era, which has brought great advances in agronomic sciences (Bolger et al., 2014). Currently, there are few genomic studies in Annona muricata L. Indeed, a search in the NCBI database (https://www.ncbi.nlm.nih.gov/Taxonomy/Browser/ wwwtax.cgi?id=13337) shows information available only for 46 and 26 nucleotide and protein sequences respectively; as well as two datasets of sequence reads archives generated by using high-throughput DNA and RNA sequence technology. The genome sequencing of crops provides powerful tools that have an important impact on the research and crop agronomic improvement in a relatively short time (Bolger et al., 2014; Varshney et al., 2014). So far, there is no information about the genome sequence of A. muricata L., however, based on a DNA Cvalues analysis of six Annona sp., it is estimated a genome size of 665–1320 Mbp and a chromosome number of 14–28 for Annona muricata (Bennett and Leitch, 2012). Furthermore, in order to evaluate the evolution rate in the Annonaceae family, the chloroplast genome of A. muricata L., and at least nine other species of the Annonaceae subfamily Annonoideae and 10 of the Annonaceae subfamily Malmeoideae were sequenced and assembled using Next Generation Sequencing technologies. The A. muricata L. chloroplast genome sequence assembly resulted in three contigs with a total assembly length of 137,441 bp, a coverage of 593 and an N50 of 69,457 bp. The molecular analysis of the chloroplast genome sequences showed a greater genetic variability for the Annonoideae subfamily compared to the Malmeoideae subfamily (Hoekstra et al., 2017) which is consistent with the observed phylogenetic relationships within the Annonaceae family (Chaowasku et al., 2014; Guo et al., 2017). On the other hand, expression patterns analysis of the plant gene set (plant transcriptomics) has contributed to the knowledge in key areas such as fruit development and ripening, as well as in the response to different stress types of plants with agronomic interest (Rai and Shekhawat, 2015; Simsek et al., 2017). Interestingly, a
10. Conclusions As can be stated in the present review paper, a better understanding of several aspects such as fruit physiology, postharvest pathology, postharvest technology, biochemistry and molecular biology will enable the development of a more precise strategy to increase the number of soursop varieties, understand the positive effects on human health and improve soursop fruit shelf life and commercialization. Conflict of interest The authors declare that they have no conflict of interest. Acknowledgments The authors thanks CONACYT (Consejo Nacional de Ciencia y Tecnología), México for the financial support by the grant Fronteras de la Ciencia 2015-1-579: “Elucidación del mecanismo molecular de biosíntesis de cutícula utilizando como modelo frutos tropicales” and PRODEP (Programa para el Desarrollo Profesional Docente. Program for the Professional Development of Teachers) for the postdoctoral fellowship granted to Guillermo Berumen Varela, PhD. 272
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Ramos-Guerrero, A., González-Estrada, R.R., Hanako-Rosas, G., Bautista-Baños, S., Acevedo-Hernández, G., Tiznado-Hernández, M.E., Gutiérrez-Martínez, P., 2018. Use of inductors in the control of Colletotrichum gloeosporioides and Rhizopus stolonifer isolated from soursop fruits: in vitro tests. Food Sci. Biotechnol. 1–9. Simsek, O., Donmez, D., Kacar, Y.A., 2017. RNA–Seq analysis in fruit science: a review. Am. J. Plant Biol. 2, 1–7. Suratman, S., Pitoyo, A., Mulyani, S., Suranto, S., 2015. Assessment of genetic diversity among soursop (Annona muricata) populations from Java, Indonesia using RAPD markers. Biodiver. J. Biol. Div. 16, 247–253. Postharvest technology of fruit and vegetables. In: 2nd ed. In: Thompson, A.K. (Ed.), Fruit and Vegetables: Harvesting, Handling and Storage, vol. 634.046/T468. Blackwell Publishing, Oxford, pp. 115–369 Chapter 12. Tovar-Gómez, B., Mata-Montes de Oca, M., García-Galindo, H.S., Montalvo-González, E., 2011. Efecto de emulsiones de cera y 1-metilciclopropeno en la conservación poscosecha de guanabana. Rev. Chapingo Ser. Hortic. 17, 53–61. Varshney, R.K., Terauchi, R., McCouch, S.R., 2014. Harvesting the promising fruits of genomics: applying genome sequencing technologies to crop breeding. PLoS Biol. 12 (6), e1001883. Worrell, D.B., Sean, C., Huber, D.J., 1994. Growth, maturation and ripening of soursop (Annona muricata L.) fruit. Sci. Hortic. 57, 7–15. Zobayed, S., Armstrong, J., Armstrong, W., 2002. Multiple shoot induction and leaf and flower bud abscission of Annonacultures as affected by types of ventilation. Plant Cell Tissue Org Cult. 69, 155–165.
Abubacker, N., Deepalakshmi, T., 2017. In vitro direct regeneration of Annona muricata L. from Nodal Explant. Biosci. Biotechnol. Res. Asia 14, 123–128. Acosta Rangel, A.M., Peña Salamanca, E.J., Castro Restrepo, D., 2011. Evaluación de medios de cultivo para la producción in vitro de Annona muricata mediante la técnica de microinjertación seriada. Acta Agron. 60, 140–146. Álvarez, E., Gañán, L., Rojas-Triviño, A., Mejía, J.F., Llano, G.A., González, A., 2014. Diversity and pathogenicity of Colletotrichum species isolated from soursop in Colombia. Eur. J. Plant Pathol. 139, 325–338. Anuragi, H., Dhaduk, H.L., Kumar, S., Dhruve, J.J., Parekh, M.J., Sakure, A.A., 2016. Molecular diversity of Annona species and proximate fruit composition of selected genotypes. 3 Biotech 6, 204. Arabidopsis-Genome-Initiative, 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796. Bejoy, M., Hariharan, M., 1992. In vitro plantlet differentiation in Annona muricata. Plant Cell Tissue Org. Cult. 31, 245–247. Bennett, M., Leitch, I., 2012. Plant DNA C-Values Database (Release 6.0, Dec. 2012). [www Document]. URL. (Accessed 14 October 2014). http://data.kew.org/ cvalues/. Bolger, M.E., Weisshaar, B., Scholz, U., Stein, N., Usadel, B., Mayer, K.F., 2014. Plant genome sequencing-applications for crop improvement. Curr. Opin. Biotechnol. 26, 31–37. Boora, K., Dhillon, R., 2010. Evaluation of genetic diversity in Jatropha curcas L. using RAPD markers. Indian J. Biotechnol. 9, 50–57. Brown, J., Laurentín, H., Dávila, M., 2003. Genetic relationships between nine Annona muricata L. accessions using RAPD markers. Fruits 58, 255–259. Bruinsma, J., Paull, R.E., 1984. Respiration during postharvest development of soursop fruit, Annona muricata L. Plant Physiol. 76, 131–138. Castillo-Ánimas, D., Varela-Hernández, G., Pérez-Salvador, B., Pelayo-Zaldívar, C., 2005. Daños por frío en guanábana. Índice de corte y tratamientos postcosecha. Rev. Chapingo Ser. Hortic. 11, 51–57. Chaowasku, T., Thomas, D.C., Ham, R.W., Smets, E.F., Mols, J.B., Chatrou, L.W., 2014. A plastid DNA phylogeny of tribe Miliuseae: insights into relationships and character evolution in one of the most recalcitrant major clades of Annonaceae. Am. J. Bot. 101, 691–709. Cheong, K.W., Tan, C.P., Mirhosseini, H., Chin, S.T., Man, Y.B.C., Hamid, N.S.A., Osman, A., Basri, M., 2011. Optimization of equilibrium headspace analysis of volatile flavor compounds of Malaysian soursop (Annona muricata): comprehensive two-dimensional gas chromatography time-of-flight mass spectrometry (GC× GC-TOFMS). Food Chem. 125, 1481–1489. Coria-Téllez, A.V., Montalvo-Gónzalez, E., Yahia, E.M., Obledo-Vázquez, E.N., 2016. Annona muricata: a comprehensive review on its traditional medicinal uses, phytochemicals, pharmacological activities, mechanisms of action and toxicity. Arab. J. Chem. 11, 662–691. Correa-Gordillo, J., Ortiz, D., Larrahondo, J.E., Sánchez-Mejía, M., Pachon, H., 2012. Actividad antioxidante en guanábana (Annona muricata L.): una revisión bibliográfica. Bol. latinoam. Caribe plantas med. aromát. 11, 111–126. Cyriacus, I., Kingsley, N., 2010. Fungi associated with deterioration of soursop (Annona muricata Linn.) fruits in Abia State, Nigeria. Afr. J. Microbiol. Res. 4, 143–146. de Lima, M.C., Alves, R., 2011. Soursop (Annona muricata L.). Postharvest Biology and Technology of Tropical and Subtropical Fruits: Mangosteen to White Sapote. Elsevier, pp. 363–392. Espinosa, I., Ortiz, R., Tovar, B., Mata, M., Montalvo, E., 2013. Physiological and physicochemical behavior of soursop fruits refrigerated with 1‐methylcyclopropene. J. Food Qual. 36, 10–20. Evangelista-Lozano, S., Cruz-Castillo, J., Pérez-González, S., Mercado-Silva, E., DávilaOrtiz, G., 2003. Producción y calidad frutícola de guanábanos (Annona muricata L.) provenientes de semilla de Jiutepec, Morelos, México. Rev. Chapingo Ser. Hortic. 9, 69–79. Guo, X., Hoekstra, P.H., Tang, C.C., Thomas, D.C., Wieringa, J.J., Chatrou, L.W., Saunders, R.M., 2017. Cutting up the climbers: evidence for extensive polyphyly in Friesodielsia (Annonaceae) necessitates generic realignment across the tribe Uvarieae. Taxon 66, 3–19. Gupta, Y., Pathak, A.K., Singh, K., Mantri, S.S., Singh, S.P., Tuli, R., 2015. De novo assembly and characterization of transcriptomes of early-stage fruit from two genotypes of Annona squamosa L. with contrast in seed number. BMC Genomics 16 (86). Hartmann, H.T., Kester, D.E., Davies, F.T., Geneve, R.L., 1997. Plant Propagation: Principles and Practices, vol. Ed. 6 Prentice-Hall Inc. Hasan, A.E.Z., Bermawie, N., Julistiono, H., Riyanti, E.I., Hasim Artika, I.M., Khana, P., 2017. Genetic diversity analysis of soursop (Annona muricata L.) in west Java region of Indonesia using RAPD markers. Annu. Res. Rev. Biol. 14, 1–7. Hoekstra, P.H., Wieringa, J.J., Smets, E., Brandão, R.D., de Carvalho Lopes, J., Erkens, R.H., Chatrou, L.W., 2017. Correlated evolutionary rates across genomic compartments in Annonaceae. Mol. Phylogenet. Evol. 114, 63–72. Janick, J., Paull, R.E., 2008. Annonaceae. The Encyclopedia of Fruit and Nuts. CABI Publishing, Oxfordshire, UK, pp. 954.
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Scientia Horticulturae journal homepage: www.elsevier.com/locate/scihorti
Review
Utilization of biotechnological tools in soursop (Annona muricata L.) a,b
T
b
Guillermo Berumen-Varela , Miguel Angel Hernández-Oñate , ⁎ Martín Ernesto Tiznado-Hernándezb, a
Unidad de Tecnología de Alimentos-Universidad Autónoma de Nayarit, Ciudad de la Cultura S/N., Tepic, Nayarit 63155, Mexico Coordinación de Tecnología de Alimentos de Origen Vegetal, Centro de Investigación en Alimentación y Desarrollo, A. C. Carretera a la Victoria Km 0.6, Hermosillo, Sonora 83304, Mexico b
A R T I C LE I N FO
A B S T R A C T
Keywords: Biotechnology Disease Micropropagation Postharvest treatments Soursop Transcriptomics
Global interest in soursop (Annona muricata L.) had increased considerably in recent years due to its medical properties. Nevertheless, there is a rather scarce information regarding genomic and genetic resources. Soursop fruit shows a short postharvest shelf life due to the high respiration rate, ethylene production and fungi attack which increases the postharvest fruit losses and makes difficult its commercialization at international markets. Besides, postharvest handling and processing of this fruit is deficient due to the lack of scientific information in physiology, diseases and molecular biology. In this regard, the utilization of biotechnology tools should be integrated to increase the genetic variability and help in the design of improved agronomic practices with the goal to improve yield, reduce fungi attack and prolong the postharvest shelf life of soursop in the near future. The objective of this review is to discuss the most important biotechnological aspects of Annona muricata L. including fruit physiology, postharvest technologies, disease control, micropropagation and the utilization of tools derived from the DNA recombinant technology.
1. Introduction In the last few years, one of the most studied species of the Annonaceae family is Annona muricata L. whose common name is soursop, graviola, guanábana (names in English, Portuguese and Spanish, respectively) among others. Soursop is a climacteric fruit which is usually consumed fresh due to its rather short postharvest shelf life. Because of this, several efforts have been made in order to delay deterioration by using conservation technologies and appropriate postharvest handling. However, other characteristics had reduced the commercialization such as low fruit quality, pathogen attack, irregular production and low yield. In this context, micropropagation can be a good strategy to increase soursop production and reduce costs. However, there are still many challenges to confront and the need to generate biochemical, molecular and genomic information in order to understand the pre- and postharvest physiological changes of soursop fruit to prolong shelf life. 2. Fruit composition and description The height of a soursop tree varies from 3 up to 10 m tall, possess
oval leaves with axillary buds, reaching a full size of 6 cm wide and 12 cm long (Jiménez-Zurita et al., 2017a). The soursop is a spiny aggregate fruit constituted of a berry product of multiple ovaries (Thompson, 2003). The fruits can have a length of 30 cm with a weight up to 5 kg. Phenotypically, is a dark-green shell with an oval, conical or irregular heart form, which is the product of an inadequate development of the carpels (Jiménez-Zurita et al., 2017a). The white pulp makes up more than 80% of the fruit, which is mainly constituted by water, non-reducing sugars and carbohydrates. Paull (1982) reported ºBrix values from 10 to 16 and pH values from 3.6 to 5.8 in the soursop pulp during three days of ripening. On the other hand, Jiménez-Zurita et al. (2016) characterized the postharvest physiological parameters of soursop at Nayarit, México, reporting average values of 8.3 N in firmness, 10.9 in total soluble solids, pH of 3.6 and 0.7% of titratable acidity. Proximate analysis performed in soursop fruits harvested in physiological maturity reported average values of 80.71 for moisture (g/100 g fresh weight of edible food). Further, 0.82 of protein, 0.77 of fat, 74.6 of soluble sugars and 3.32 of ash in grams per 100 g dry matter of edible portion (Moreno-Hernández et al., 2014). Besides, vitamins, carotenoids, flavonoids and lipophilic antioxidants compounds have been reported in soursop fruits (Correa-Gordillo et al., 2012). Recently,
⁎
Corresponding author. E-mail addresses: [email protected] (G. Berumen-Varela), [email protected] (M.A. Hernández-Oñate), [email protected] (M.E. Tiznado-Hernández). https://doi.org/10.1016/j.scienta.2018.10.028 Received 16 August 2018; Received in revised form 12 October 2018; Accepted 13 October 2018 0304-4238/ © 2018 Elsevier B.V. All rights reserved.
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Fig. 1. Soursop fruit development from flower to physiological maturity.
shelf life in optimal conditions for consumption (de Lima and Alves, 2011; Jiménez-Zurita et al., 2017a). A correct handling, right storage conditions and other postharvest technologies to delay fruit ripening need to be designed and utilized during soursop commercialization to avoid postharvest fruit losses and bad quality. Nowadays, several technologies have been used to prolong the shelf life of soursop, including refrigeration, waxes, emulsions, 1-methylcyclopropene (1-MCP) usage and combinations of all of these treatments. In this regard, Castillo-Ánimas et al. (2005) evaluated the harvest index (light and dark-green) in combination with different temperatures and distinct formulations of candelilla wax and growth regulators. They found that only candelilla wax delayed fruit maturity and reduced weight loss. Candelilla wax formulation reduced CO2 production in fruits with a weight range of 560–750 g and harvested at dark-green, indicating that wax formulation was able to delay the onset of the respiration climacteric peak. However, chilling injury in soursop fruits harvested at the dark-green stage and stored at temperatures between 16 to 18 and 12 to 14 °C was observed. Furthermore, the fruits harvested at light green stage showed chilling injury only at 12–14 °C. Based on all the previously mentioned, the physiological stage of the fruit at harvest time and store temperatures are two important factors that affect shelf life in soursop. In a recently published paper, Jiménez-Zurita et al. (2017b) analyzed the physiological and biochemical parameters at different temperatures (15 °C and 22 °C) during the postharvest shelf life of soursop fruits. It was found an increase in the postharvest shelf life up to 8 days with no chilling injury or alteration on the ripening phenomena in fruits stored at 15 °C and then at 22 °C. On the other hand, it was studied the effect of 1-MCP treatment and storage at 16 °C and 25 °C on the postharvest shelf life of soursop fruit. It was found that fruits treated with 200 nanoliters per liter (nLL−1) and 400 nLL−1 of 1-MCP and stored at 16 °C, showed a 7 days delay to reach the mature stage without chilling injury (Espinosa et al., 2013). Taken together, it is possible the utilization of low-temperature technology to prolong the soursop shelf life without adversely affect the fruit quality. Besides, several studies using 1-MCP in combination with waxes and emulsions have been carried out to increase the soursop postharvest shelf life, described next. Lima et al. (2004) studied the effect of 200 nLL−1 of 1-MCP and polyethylene wax during storage at 15.4 ± 1.1 °C during 0, 4, 8, 11, 13 and 15 days on soursop fruits. The change in total soluble solids was delayed by all the treatments whereas no change in titratable acidity, pH, total soluble sugars and reducing sugars was recorded. Tovar-Gómez et al. (2011) evaluated the utilization of carnauba wax type III, carnauba wax with silicone oils, candelilla wax and 1-MCP one by one or in different combinations on the physiological parameters of soursop during postharvest. It was found that 1000 nLL−1 for 12 h of 1-MCP in combination with the emulsions delayed fruit ripening between six and seven days as
great interest has been focused on pharmacological compounds in A. muricata L. Coria-Téllez et al. (2016) mentioned that 212 bioactive compounds have been reported in soursop, from which acetogenins, alkaloids and phenols are the most prevalent. Moreover, 37 volatile compounds have been found in soursop pulp, mainly aromatic and aliphatic esters (Cheong et al., 2011). The importance of these compounds is currently being studied to obtain more information about the therapeutic potential of soursop. 3. Fruit growth and ripening Soursop needs a warm and tropical climate for its development. The pollination in soursop is complex, causing low fruit set and in consequence low yield. Climate conditions of 25 °C temperature and 80% of relative humidity (low temperature, high humidity) can improve the pollination process (Janick and Paull, 2008). The soursop is a climacteric fruit and the time of harvesting is established based on the skin color of the fruit. According to Worrell et al. (1994), after the soursop flowers are pollinated, they have a quiescent stage (period of eco dormancy after fertilization of the blossom) of around 6–15 weeks (Fig. 1). After this, the fruit reaches half of its final size. The soursop fruits have a life cycle of around 105–150 days (15–21 weeks) from post-anthesis quiescent stage to physiological maturity (Fig. 1). It is frequently manually harvested at physiological maturity, and usually the fruit reaches the peak of ethylene production at 5 or 6 days after harvesting (Paull, 1982). Being a climacteric fruit, it shows a high respiration rate and ethylene production during ripening. In this regard, Bruinsma and Paull (1984) have shown that ethylene production is detectable from two to three days after harvesting. Worrell et al. (1994) found that mature fruit shows a biphasic respiratory climacteric, with a start of CO2 production of 100 mL kg−1 h−1 (day zero) and increasing to 350 mL kg−1 h−1 (day four) at 25–30 °C. The peak of ethylene production was reported between the fourth and sixth day after harvesting, with values ranging from 250 to 350 mL kg−1 h−1 (Márquez Cardozo et al., 2012; Worrell et al., 1994). In agreement with the data mentioned above, the average shelf life of the Annonaceae family is around 4–9 days with a storage temperature of 15–20 °C (Pareek et al., 2011). 4. Postharvest handling and technology The soursop is a very perishable fruit, and that is why it requires a careful handling from harvest to consumption (de Lima and Alves, 2011). Probably, the most important factor that affects the quality of the soursop is the precise time in which the fruit is physiologically mature. For instance, a fruit harvested immature will show an irregular maturation and a bad taste in the pulp as a consequence. Furthermore, when the fruits are harvested ripe, they show a reduced postharvest 270
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and efficient propagation of soursop. The cherimoya (Annona cherimola) is the most studied specie of the family Annonaceae, although it shows low morphogenic response and low rooting percentage which makes difficult to induce the complete organogenesis from an explant (LópezEncina et al., 2014). One of the first reports regarding in vitro micropropagation of soursop was carried out by Bejoy and Hariharan (1992). In this work, hypocotyls were used as an explant. They recorded the induction of 4.8 shoots in average per explant after 35 days of culture by using 1X of MS including 2 mg L−1 of benzylaminopurine (BAP) and 0.1 mg L−1 of naphthalene acetic acid (NAA). Moreover, 1X MS medium containing 30 g L−1 sucrose, 8 g L−1 agar and 9.8 μM of Indole3-butyric acid (IBA) was used for root induction, obtaining 2–6 roots in a range of 30–35 days. Lemos and Blake (1996) established the conditions for micropropagation of soursop, using hypocotyls and nodal cuttings as explants. On hypocotyls, woody plant medium (WPM), developed by McCown and Lloyd (1981) supplemented with 2 mg L−1 of BAP and 0.5 mg L−1 of NAA induced shoots elongation after six weeks of culture. On nodal explants, same BAP concentration in combination with 0.1 mg L−1 NAA induced shoots formation. Moreover, it was also found that activated charcoal before rooting and the addition of galactose (as a source of sugar) to the root medium improved the root induction. Furthermore, Abubacker and Deepalakshmi (2017) established a micropropagation protocol for soursop using leaf base segments. MS medium with BAP 1.5 mg L−1 and 2,4-D 2.0 mg L−1 induced callus tissue growth. This is the first report in which the induction of callus was recorded. Shoot elongation was accomplished with 1X MS medium supplemented with BAP 1.0 mg L−1, Kinetin 0.5 mg L−1 and IBA 1.5 mg L−1. The rooting medium was composed by 1X MS medium with IBA 2.0 mg L−1, NAA 0.5 mg L−1 and BAP 1.0 mg L−1. In both articles previously mentioned, the plantlets were transferred successfully to the greenhouse. Micrografting technique is carried out by collocating a meristem or other type of explant over a decapitated rootstock to stimulate the in vitro development of the tissue (Hartmann et al., 1997). This technique is frequently utilized for the in vitro micropropagation of recalcitrant species. Acosta Rangel et al. (2011) utilized the monophasic micrografting approach to stimulate the growth of Annona muricata L. However, rooting of Annona muricata L. was not possible. As it has been discussed, BAP and NAA concentrations appear to be very important hormones for the induction of shoots and roots on the Annona muricata specie. However, it is necessary to improve the rooting protocol, because most methods have shown problems to obtain a high percentage of rooting. Because the genotype, type of explant and hormone concentration of the medium affect the plant regeneration system, the development of an efficient tissue culture protocol for the in vitro micropropagation of A. muricata is still needed to establish an orchard with individuals of the same genotype.
compared with the control. Further, these fruits reached the mature stage after 15 days of storage in comparison with the control that reached the mature stage in a range of 8–9 days. In another study, Montalvo-González et al. (2014) did not record chilling injury in the pulp of fruits treated with 1500 nLL−1 for 12 h of 1-MCP in combination with candelilla wax or beeswax diluted with water and stored at 16 °C. Besides, Moreno-Hernández et al. (2014) evaluated the proximate analysis (moisture, protein, fat and ash content), soluble sugars, total dietary fiber, vitamin C, polyphenols, and antioxidant capacity of soursop fruits treated with 1-MCP and wax emulsions. It was recorded that the combination of 1-MCP and flava wax prolonged the shelf life without affecting the nutritional parameters. Based on all of the studies just mentioned, it seems that a combination of low-temperature storage, waxes and 1-MCP is required to increase the soursop postharvest shelf life in order to allow the fruit commercialization in optimal quality conditions and preserve the nutritional values. Nevertheless, further studies need to be done with the aim to design an optimal treatment to increase the soursop postharvest shelf life with good organoleptic characteristics and nutritional quality. 5. Soursop postharvest diseases Soursop fruits are infected by numerous fungi species, which have been isolated, identified and characterized. Cyriacus and Kingsley (2010) identified several fungi on the exocarp and mesocarp of mature green soursop fruits from Nigeria, namely: Aspergillus flavus, Aspergillus niger, Botryodiplodia theobromae, Colletotrichum sp., Fusarium solani, Mucor sp., Penicillium chrysogenium, Penicillium sp., Rhizopus stolonifer among others. Moreover, Nweke and Ibiam (2012) found that soft-rot disease of the soursop fruit was due to the attack of the fungi Colletotrichum gloeosporoides, Rhizopus stolonifer and Aspergillus niger. On the other hand, flowers and fruits of soursop are susceptible to a disease called anthracnose caused by the fungi Colletotrichum gloeosporoides. In this context, a study was carried out to identify the presence of Colletotrichum species from different tissues of soursop by PCR amplification using the sequences of the ITS region. Also, anthracnose severity was evaluated. The Colletotrichum species identified were: C. theobromicola, C. tropicale, C. siamense, C. gloeosporioides among others. Among these, C. theobromicola was the most pathogenic specie inducing almost 76% of anthracnose severity on soursop trees (Álvarez et al., 2014). From above, it is clear that. the most important fungi disease of soursop fruit is caused by Colletotrichum species, so more studies are needed to develop strategies to control the disease caused by these fungi. In this regard, Ramos-Guerrero et al. (2018) evaluated the in vitro effect of resistance inductors such as chitosan, salicylic acid and methyl jasmonate (alone or in combination) on the infection by Colletotrichum gloeosporioides and Rhizopus stolonifer isolated from soursop fruits. The authors showed that all treatments inhibited the conidial germination more than 75% in C. gloeosporioides and 100% in R. stolonifer. Moreover, in both fungi, a range of 81–96% in vitro growth inhibition was observed with a treatment of 1.0% chitosan alone or in combination with salicylic acid or methyl jasmonate. These results clearly showed the in vitro effect of these treatments over the fungi inducing soursop anthracnose. Further, in vivo studies are required to know whether these treatments are equally effective on the fungi infecting the soursop fruit.
7. Genetic diversity The molecular diversity of the specie Annona muricata soursop is still largely unknown. The evaluation of genetic variation of crop species is fundamental for the design of a successful plant breeding program because it helps to choose parental lines for the genetic crosses with the goal to induce a much larger variation in the progeny (Boora and Dhillon, 2010). Nowadays, there is a lack of information about the genetic characteristics of soursop commercial varieties partially due to the very low knowledge of the species genome. However, DNA analysis has been carried out on soursop germplasm collection in order to identify and characterize the genetic diversity of cultivars or accessions, using random amplified polymorphic DNA (RAPD). This technique had been shown to be a quick, low cost and easy method for the detection of DNA polymorphism and categorization of different genotypes. Suratman et al. (2015) analyzed the genetic variation of seven soursop populations from Indonesia. As a result, the different populations were classified into three clusters, in which one of the clusters was shown to
6. Micropropagation Soursop propagation is usually carried out by seed (Paull and Duarte, 2011). In Mexico, the large existing genotype variability of soursop fruits had been generated by seed propagation (EvangelistaLozano et al., 2003). The multiplication of Annona muricata L. by seed is preferred because propagation through traditional methods such as layering, budding, grafting, shoots and root cuttings are very slow and expensive (Zobayed et al., 2002). For this reason, the micropropagation techniques by tissue culture can be an alternative method for the rapid 271
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multidisciplinary international consortium generated the transcriptomic data of 1000 plants species, including species from the clade Viridiplantae, which includes green algae and flowering plants, and represents nearly one billion years of evolution (Matasci et al., 2014). Within this project, the A. muricata leaves transcriptome was sequenced. The de novo transcriptome assembly revealed 92,924 transcripts with a total assembly length of 51.12 Mbp. The transcripts show a length range from 100 to 17,040 bp (mean length of 498.6 bp), an N50 value of 1558 bp and GC percentage of 42.8%. Moreover, only 17.6% (16,353) transcripts have an open-reading frame analysis (Matasci et al., 2014). Although this work represents the first transcripts sequences generated in the soursop crop, sequence annotation was not carried out. Nevertheless, this effort represents an important advance in the research of this crop, that together with the transcriptomes of A. squamosa (Gupta et al., 2015; Liu et al., 2016, 2017) represent the unique available transcriptomics data in species of the gender Annona, giving information that promises a better understanding of the biology of these crops, which will be invaluable for both academic research and biotechnology industry.
be genetically more distant than the others. Furthermore, it was found a low genetic diversity within the population of each cluster. Similar results were found by Hasan et al. (2017) in which Annona muricata from 9 accessions of West Java and Indonesia, were classified in two main clusters based on the dendrogram from the similarity matrices. Furthermore, Brown et al. (2003) estimated the genetic variability of nine soursop accessions, seven from Venezuela and two from Brazil. It was recorded that some of the Venezuelan accessions were found to be genetically distant from the Brazilian accessions. Furthermore, the nine accessions were grouped into two different clusters. The first cluster was grouped with five Venezuelan accession and two Brazilian accessions. The remaining two Venezuelan accessions (The Palmarito 4 and Amado) were clustered with other Venezuelan germplasm. Moreover, Brazilian accession showed no significant variability among them. In a recent study, five species of Annonaceae: A. cherimola, A. reticulata, A. muricata, A. atemoya and A. squamosa, collected from different locations of India, were analyzed for molecular diversity analysis using RAPD and simple sequence repeats markers. The molecular data revealed seven clusters showing a large genetic diversity among all Annonaceae genotypes evaluated (Anuragi et al., 2016). As it has been observed, exists a large molecular variability among the species of the Annonaceae family. Moreover, it seems that cultivar, accession, as well as the place of the genetic population, are related to genetic diversity. However, the few studies carried out in A. muricata suggests a low genetic variation, although the creation of a germplasm collection and further studies need to be performed in order to obtain more information regarding the molecular diversity of A. muricata.
9. Future perspectives Even when during the last years, studies of the Annona muricata L. had increased, major efforts are required to uncover the transcriptomic and genomic sequences of the specie. The improvement of DNA sequencing technologies and the advances in genomics and transcriptomics will make possible to obtain a better understanding of the Annona muricata L. genes expression patterns, which will provide a large amount of valuable biological information that can be used in several ways. For instance, it will allow the design of strategies directed towards the improvement of important agronomical traits of the crop such as resistance to pathogen attack, uniform flowering, reduction in fruit drop percentage, higher fruit postharvest shelf life, among others. In this sense, in our research group, we are carrying out the creation and analysis of a soursop exocarp’s transcriptome in three stages of development: physiological maturity, ripening and senescence. This main goal of the project is to identify genes playing a role in the biosynthesis of cuticle components. We believe that this soursop transcriptome will establish the molecular and genetic basis to begin a soursop breeding program in order to create a soursop variety, with a better and longer postharvest shelf life, in such a way that it will be possible to increase the production for national consumption and for fruit exportation to international markets.
8. Genomic sequencing Since the first plant genome sequence was published (ArabidopsisGenome-Initiative, 2000), the number of plant genomes sequenced has increased continuously. This has been possible thanks to the improvement in the sequencing technologies in terms of cost and speed; the storage capacity and the bioinformatics tools for sequence analysis. All of this gave rise to the plant genomics era, which has brought great advances in agronomic sciences (Bolger et al., 2014). Currently, there are few genomic studies in Annona muricata L. Indeed, a search in the NCBI database (https://www.ncbi.nlm.nih.gov/Taxonomy/Browser/ wwwtax.cgi?id=13337) shows information available only for 46 and 26 nucleotide and protein sequences respectively; as well as two datasets of sequence reads archives generated by using high-throughput DNA and RNA sequence technology. The genome sequencing of crops provides powerful tools that have an important impact on the research and crop agronomic improvement in a relatively short time (Bolger et al., 2014; Varshney et al., 2014). So far, there is no information about the genome sequence of A. muricata L., however, based on a DNA Cvalues analysis of six Annona sp., it is estimated a genome size of 665–1320 Mbp and a chromosome number of 14–28 for Annona muricata (Bennett and Leitch, 2012). Furthermore, in order to evaluate the evolution rate in the Annonaceae family, the chloroplast genome of A. muricata L., and at least nine other species of the Annonaceae subfamily Annonoideae and 10 of the Annonaceae subfamily Malmeoideae were sequenced and assembled using Next Generation Sequencing technologies. The A. muricata L. chloroplast genome sequence assembly resulted in three contigs with a total assembly length of 137,441 bp, a coverage of 593 and an N50 of 69,457 bp. The molecular analysis of the chloroplast genome sequences showed a greater genetic variability for the Annonoideae subfamily compared to the Malmeoideae subfamily (Hoekstra et al., 2017) which is consistent with the observed phylogenetic relationships within the Annonaceae family (Chaowasku et al., 2014; Guo et al., 2017). On the other hand, expression patterns analysis of the plant gene set (plant transcriptomics) has contributed to the knowledge in key areas such as fruit development and ripening, as well as in the response to different stress types of plants with agronomic interest (Rai and Shekhawat, 2015; Simsek et al., 2017). Interestingly, a
10. Conclusions As can be stated in the present review paper, a better understanding of several aspects such as fruit physiology, postharvest pathology, postharvest technology, biochemistry and molecular biology will enable the development of a more precise strategy to increase the number of soursop varieties, understand the positive effects on human health and improve soursop fruit shelf life and commercialization. Conflict of interest The authors declare that they have no conflict of interest. Acknowledgments The authors thanks CONACYT (Consejo Nacional de Ciencia y Tecnología), México for the financial support by the grant Fronteras de la Ciencia 2015-1-579: “Elucidación del mecanismo molecular de biosíntesis de cutícula utilizando como modelo frutos tropicales” and PRODEP (Programa para el Desarrollo Profesional Docente. Program for the Professional Development of Teachers) for the postdoctoral fellowship granted to Guillermo Berumen Varela, PhD. 272
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