ABSTRACT

Background:

Hancornia speciosa is a species known for its medicinal and nutritional properties. Despite being a plant native to several regions of Brazil, some aspects of its production system are not yet well defined. Large-scale asexual propagation stands out, making it difficult to establish commercial orchards with materials with superior characteristics. In this context, this article aimed to investigate the scientific production related to the propagation and conservation of the mangabeira, using a mixed methodology of bibliometric analysis and literature review. The Scopus and Web of Science databases were consulted and the VOSviewer software was used to map the cooperation network between authors, institutions, and keywords.

Results:

The study included 72 articles and found a significant increase in scientific production on mangabeira propagation and conservation since 2009. Most studies focused on seed technology, seedling production, in vitro propagation and conservation, and cryopreservation. Additionally, it was observed that mangabeira seeds do not tolerate a reduction in moisture content, and the combination of materials for the composition of the substrate, such as coconut fiber, manure, and sand, can provide an adequate basis for developing seedlings. It was also observed that MS culture medium, complete or with half saline concentration, or WPM medium can be used for in vitro germination and initial seedling growth.

Conclusion:

Through this review, we concluded that the mangabeira presents substantial potential for the development of innovative propagation techniques, with a special focus on methods that facilitate the clonal propagation of the species, such as grafting, rooting cuttings, and micropropagation. It is expected that future research will expand knowledge about the in vitro and ex vitro propagation of this species, contributing to the expansion of commercial plantations with a focus on adding to the processing of its fruits.

Keywords:
Apocynaceae; germination; mangaba; micropropagation; native fruit.

HIGHLIGHTS

After 2009 there was an increase in studies on mangabeira propagation/conservation. A total of 72 scientific articles were identified and included in the review. The studies involving the vegetative propagation of mangabeira in broad are still scarce. Cloning by cuttings on a large scale may be a future trend.

INTRODUCTION

The mangabeira tree (Hancornia speciosa Gomes) is a fruit-bearing and medicinal tree that is native to Brazil and belongs to the Apocynaceae family. It has a wide distribution throughout the country, occurring in the Caatinga, Amazon, Cerrado, and Atlantic Forest biomes, and it is also found in Bolivia, Peru, and Paraguay (Coradin et al., 2018CORADIN, L.; CAMILO, J.; PAREYN, F. Espécies Nativas da Flora Brasileira de Valor Econômico Atual ou Potencial: Região Nordeste. Brasília-DF, 2018. ). This species holds great economic importance as its fruit, mangaba, is consumed fresh or processed by small agro-industries to make juices, popsicles, ice creams, jams, and other products. It serves as an important source of income for traditional communities, such as mangabeira gatherers (Soares et al., 2011SOARES, F. P.; PAIVA, R.; ALVARENGA, A. A. de; et al. Taxa de multiplicação e efeito residual de diferentes fontes de citocinina no cultivo in vitro de Hancornia speciosa Gomes. Ciência e Agrotecnologia, v. 35, n. 1, p. 152-157, 2011. , Chaves- Almeida et al., 2022, Nunes et al., 2022NUNES, V. V.; SILVA-MANN, R.; SOUZA, J. L.; et al. Physiological and molecular changes in seeds of Hancornia speciosa Gomes stored in conservative solutions. Journal of Seed Science, v. 44, n. e202244018, 2022. a). Furthermore, the mangabeira tree exhibits significant pharmacological potential due to the presence of compounds like rutin and chlorogenic acid, which can be found in its leaves, barks, fruits, and latex, possessing anti-inflammatory and antioxidant properties (Leite et al., 2020LEITE, S. P.; TIAGO, B. A.; THIAGO, R. B.; et al. Ultrasonic assisted extraction of bioactive compounds from different parts of Hancornia Speciosa Gomes. Journal of Medicinal Plants Research, v. 14, n. 7, p. 300-308, 2020. ; Nassiri-Asl et al., 2017NASSIRI-ASL, M.; NIKFARJAM, B. A.; ADINEH, M.; et al. Treatment with Rutin - A Therapeutic Strategy for Neutrophil-Mediated Inflammatory and Autoimmune Diseases. Journal of Pharmacopuncture, v. 20, n. 1, p. 52-56, 2017. ; Torres-Rêgo et al., 2016TORRES-RÊGO, M.; FURTADO, A. A.; BITENCOURT, M. A. O.; et al. Anti-inflammatory activity of aqueous extract and bioactive compounds identified from the fruits of Hancornia speciosa Gomes (Apocynaceae). BMC Complementary and Alternative Medicine, v. 16, n. 1, p. 275, 2016. ). Additionally, it is worth noting that this species can be used as an ornamental plant in urban tree planting for streets, squares, and parks (Araújo e Pires, 2009ARAÚJO, R. de; PIRES, L. L. Opções de frutíferas do cerrado para paisagismo urbano em bairros da periferia de Goiânia-GO. Revista Caatinga, v. 22, n. 4, p. 235-239, 2009. ).

The natural populations of mangabeira trees have been drastically reduced due to the expansion of agricultural and livestock activities, as well as real estate speculation, especially in coastal areas, which are suppressing the native vegetation and, consequently, the natural habitats of this species (Álvares-Carvalho et al., 2022ÁLVARES-CARVALHO, S. V.; VIEIRA, T. R. S.; FREITAS, B. A. L. de; et al. Biodiversity hotspots for conservation of Hancornia speciosa Gomes. Genetic Resources and Crop Evolution, v. 69, n. 6, p. 2179-2189, 2022. ; Oliveira et al., 2014OLIVEIRA, K. S. de; OLIVEIRA, M. da S.; PEREIRA, E. C.; et al. Efeito de diferentes meios de cultura na germinação in vitro de sementes de mangabeira (Hancornia speciosa Gomes). Revista Árvore, v. 38, n. 4, p. 601-607, 2014. ). Another challenge to conserving this species is that its seeds are recalcitrant, making long-term storage unviable (Nunes et al., 2022NUNES, V. V.; SILVA-MANN, R.; SOUZA, J. L.; et al. Pharmaceutical, food potential, and molecular data of Hancornia speciosa Gomes: a systematic review. Genetic Resources and Crop Evolution, v. 69, n. 2, p. 525-543, 2022. ).

The main source for supplying the mangaba market is extractive activity, and there are only a few orchards established for rational exploitation for fruit production (Soares et al., 2020SOARES, F. S.; LUZ, P. B. da; ROCHA, V. L. P.; et al. Aspectos anatômicos de impedimentos ao enraizamento em estacas caulinares de mangabeira. Acta Iguazu, v. 9, n. 1, p. 82-89, 2020. ). According to data from IBGE (2021)IBGE - INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. Produção da Extração Vegetal e da Silvicultura. Rio de Janeiro: IBGE, 2021. Disponível em: https://sidra.ibge.gov.br/tabela/289.
https://sidra.ibge.gov.br/tabela/289... , Brazil’s national production amounted to 2,173 t, with the Northeast region being the largest producer in the country, particularly the states of Paraíba (882 t) and Sergipe (457 t). Therefore, the expansion into new markets is contingent upon the commercial production of mangaba, as the current production does not meet the consumer market’s demand (Soares et al., 2020SOARES, F. S.; LUZ, P. B. da; ROCHA, V. L. P.; et al. Aspectos anatômicos de impedimentos ao enraizamento em estacas caulinares de mangabeira. Acta Iguazu, v. 9, n. 1, p. 82-89, 2020. ).

The main method for obtaining seedlings of the species is still through seeds, which discourages its cultivation due to slow field growth and uneven fruit production among progenies, thus making it difficult to expand commercial orchards (Ganga et al., 2010GANGA, R. M. D.; FERREIRA, G. A.; CHAVES, L. J.; et al. Caracterização de frutos e árvores de populações naturais de Hancornia speciosa Gomes do cerrado. Revista Brasileira de Fruticultura, v. 32, n. 1, p. 101-113, 2010. ; Vieira et al., 2013VIEIRA, C. do M.; REGINA, E.; SOUZA, B.; et al. Desenvolvimento de mudas de mangabeira provenientes de frutos de diferentes localidades do Estado de Goiás. Revista de Ciências Agrárias, v. 36, n. 3, p. 363-371, 2013.). Strategies for seedling production through asexual techniques such as micropropagation, grafting, or rooting of cuttings are more promising for the establishment of commercial orchards. Grafting has been successfully applied to botanical varieties from the Cerrado due to the rapid growth of rootstocks (Pereira et al., 2006PEREIRA, A.; PEREIRA, E.; ARAÚJO, I.; et al. A cultura da mangaba. [s.l.] Embrapa Tabuleiros Costeiros, 2006. . ). Micropropagation protocols have been established by several authors (Oliveira et al., 2016OLIVEIRA, K. S. de; FREIRE, F. A. de M.; ALOUFA, M. A. I. Efeito de 6-benzilaminopurina e ácido naftalenoacético sobre a propagação in vitro de Hancornia speciosa Gomes. Floresta, v. 46, n. 3, p. 335-342, 2016. ; Prudente et al., 2016PRUDENTE, D. de O.; PAIVA, R.; NERY, F. C.; et al. Indirect in vitro organogenesis of Hancornia speciosa Gomes. Bioscience Journal, v. 32, n. 3, p. 721-729, 2016. ; Sá et al., 2012SÁ, A. de J.; LÉDO, A. da S.; LÉDO, C. A. da S.; et al. Sealing and explant types on the mangaba micropropagation. Ciência e Agrotecnologia, v. 36, n. 4, p. 406-414, 2012. ; Soares et al., 2011SOARES, F. P.; PAIVA, R.; ALVARENGA, A. A. de; et al. Taxa de multiplicação e efeito residual de diferentes fontes de citocinina no cultivo in vitro de Hancornia speciosa Gomes. Ciência e Agrotecnologia, v. 35, n. 1, p. 152-157, 2011. ), but there are no biofactories with large-scale production of seedlings and no protocols for cutting propagation.

A bibliometric review is a statistical approach used to quantify the impact of research by analyzing performance and productivity measures (Romanelli et al., 2021ROMANELLI, J. P.; GONÇALVES, M. C. P.; PESTANA, L. F. de A.; et al. Four challenges when conducting bibliometric reviews and how to deal with them. Environmental Science and Pollution Research, v. 28, n. 43, p. 60448-60458, 2021. ). Additionally, bibliometrics provides insights into the current state of a knowledge area, assisting in the development of future research lines (Chaves Almeida et al., 2022CHAVES ALMEIDA, F. L.; OLIVEIRA, E. N. A. de; ALMEIDA, E. C.; ET AL. Hancornia speciosa: An overview focused on phytochemical properties, recent achievements, applications, and future perspectives. International Journal of Gastronomy and Food Science, v. 29, p. 100561, 2022. ). Thus, this technique can be applied to the topic of propagation and conservation of the mangabeira tree to support future research actions.

Therefore, this review aims to explore the main studies on the propagation and conservation of the H. speciosa tree, including articles related to in vitro and ex vitro propagation, in vitro conservation, and cryopreservation. A mixed methodology of bibliometric analysis and literature review was adopted to present the state of the art and prospects for expanding large-scale sexual and asexual propagation techniques of this native fruit tree.

METHODS

The present study was based on bibliometric analysis, followed by a systematic literature review (Araújo et al., 2020ARAÚJO, A. G.; CARNEIRO, A. M. P.; PALHA, R. P. Sustainable construction management: A systematic review of the literature with meta-analysis. Journal of Cleaner Production, v. 256, p. 120350, 2020. ), following the guidelines of the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) methodological tool (Moher et al., 2009MOHER, D.; LIBERATI, A.; TETZLAFF, J.; et al. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Medicine, v. 6, n. 7, p. e1000097, 2009. ; Page et al., 2021PAGE, M. J.; MCKENZIE, J. E.; BOSSUYT, P. M.; et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ, v. 372, p. n. 71, 2021. ). A bibliographic search was conducted in the following scientific databases: SCOPUS (http://www.scopus.com) and Web of Science (http://www.webofknowledge.com). The literature search was conducted in March 2023 using the following keyword: “Hancornia speciosa.” No time interval was specified to gather as much information as possible. Articles published in English, Spanish, and Portuguese were included.

The review consisted of three steps: (i) identification of articles in the Web of Science and Scopus databases that contained specific descriptors, as well as papers from other sources that were not detected by the descriptors but were relevant to this review; (ii) screening (omitting duplicates, reviews, as well as unavailable papers and those outside the scope of the present study); and (iii) inclusion of eligible, full-text articles that were available online and provided information related to mangabeira propagation and conservation.

The search for the keyword “Hancornia speciosa” identified 543 documents, of which 309 were on the Scopus platform and 233 were on the Web of Science platform. All these documents had their titles and abstracts read to exclude documents that were not related to the propagation and conservation of mangabeira, of which 51 articles were selected from Scopus and 41 from Web of Science. After that, the duplicates existing in the two platforms were excluded, and another 14 articles considered important for the review and not identified in these platforms were also inserted, forming a total of 71 articles (Figure 1). The quantitative analyses of the bibliometric indexes were compiled in a Microsoft Office Excel® 365 spreadsheet. Finally, VOSviewer (Eck e Waltman, 2010ECK, N. J. VAN; WALTMAN, L. Software survey: VOSviewer, a computer program for bibliometric mapping. Scientometrics, v. 84, n. 2, p. 523-538, 2010. ) was used to set up cooperation networks among authors, keywords, and organizations.

Figure 1
PRISMA 2020 flow diagram in this systematic review.

RESULTS AND DISCUSSION

Years of publication

Bibliographic research on the propagation and conservation of mangabeira revealed that the first work on this species was published in 1992 and dealt with the effect of different levels of humidity on the germination of its seeds (Oliveira e Valio, 1992OLIVEIRA, L. M. Q.; VALIO, I. F. M. Effects of moisture content on germination of seeds of Hancornia speciosa Gomes (Apocynaceae). Annals of Botany, v. 69, n. 1, p. 1-5, 1992. ). Since then, studies have been published almost every subsequent year, until the year 2022. It is important to note that between 2009 and 2022, 57 papers were published, corresponding to approximately 79.1% of the total number of papers published during the entire period evaluated, with an average of about 4 papers published per year (Figure 2).

Figure 2
Number of articles by year of publication on mangabeira propagation and conservation.

Most relevant authors

Below is a figure where we can observe the most relevant authors in the field of propagation and conservation of the mangaba tree, who have published works related to this theme (Figure 3). We can highlight that there are four main clusters, in which the main authors are distributed. The red cluster is formed by the research group of Dr. Renato Paiva of the Universidade Federal de Lavras, with nine papers, which together with other researchers has developed work focused mainly on the cryopreservation of mangabeira (Prudente et al., 2017PRUDENTE, D. O.; PAIVA, R.; NERY, F. C.; et al. Encapsulation of lateral buds of Hancornia speciosa. Acta Horticulturae, v. 1155, n. 1155, p. 59-64, 2017. ; Prudente et al., 2017PRUDENTE, D. de O.; PAIVA, R.; NERY, F. C.; et al. Compatible solutes improve regrowth, ameliorate enzymatic antioxidant systems, and reduce lipid peroxidation of cryopreserved Hancornia speciosa Gomes lateral buds. In Vitro Cellular and Developmental Biology - Plant, v. 53, n. 4, p. 352-362, 2017. ; Santos et al., 2015SANTOS, P. A. A.; PAIVA, R.; SILVA, L. C.; et al. Effect of load solution and growth media on cryopreservation by droplet vitrification of Hancornia speciose shoot tips. Acta Horticulturae, n. 1083, p. 507-512, 2015. ; Santos et al., 2015SANTOS, P. A. A.; PAIVA, R.; SILVA, L. C.; et al. Cryopreservation of the mangaba tree (Hancornia speciosa Gomes): A protocol for long-term storage. Acta Scientiarum - Agronomy, v. 37, n. 3, p. 289-296, 2015. ). The dark blue cluster is composed of the research group of Dr. Ana da Silva Lédo from Embrapa Tabuleiros Costeiros, with 8 articles, whose work is mainly focused on the propagation and in vitro conservation of this species (Lédo et al., 2007LÉDO, A. da.; SECA, G. S. V.; BARBOZA, S. B. S. C.; et al. Crescimento inicial de mangabeira (Hancornia speciosa Gomes) em diferentes meios de germinação in vitro. Ciência e Agrotecnologia, v. 31, n. 4, p. 989-993, 2007. , Sá et al., 2011SÁ, A. de J.; LÉDO, A. da S.; LÉDO, C. A. da S. Conservação in vitro de mangabeira da região nordeste do Brasil. Ciência Rural, v. 41, n. 1, p. 57-62, 2011. , Sá et al., 2012SÁ, A. de J.; LÉDO, A. da S.; LÉDO, C. A. da S.; et al. Sealing and explant types on the mangaba micropropagation. Ciência e Agrotecnologia, v. 36, n. 4, p. 406-414, 2012. ).

Figure 3
Most relevant authors (based on several published papers) on the propagation and conservation of mangabeira.

The light blue cluster is formed by researchers from the research group of Dr. Fabiano Guimarães Silva from the Instituto Federal Goiano, Campus Rio Verde, with five papers, whose research is mainly focused on micropropagation and seedling production, with emphasis on the deficiency of macronutrients and micronutrients (Bessa et al., 2012BESSA, L. A.; SILVA, F. G.; MOREIRA, M. A.; et al. Characterization of the effects of macronutrient deficiencies in mangabeira seedlings. Revista Brasileira de Fruticultura, v. 34, n. 4, p. 1235-1244, 2012. , 2013BESSA, L. A.; SILVA, F. G.; MOREIRA, M. A.; TEODORO, J. P. R.; SOARES, F. A. L.. Characterization of nutrient deficiency in Hancornia speciosa Gomes seedlings by omitting micronutrients from the nutrient solution. Revista Brasileira de Fruticultura, v. 35, n. 2, p. 616-624, 2013. ). Finally, the purple cluster is composed of the research group of Dr. Adaucto Bellarmino de Pereira Netto from the Universidade Federal do Paraná, with 5 published papers, which stands out for having started research with the in vitro propagation of mangabeira, with the first paper published in 1996 (Pereira-Netto, 1996PEREIRA-NETTO, A. B. In vitro propagation of Hancornia speciosa, a tropical fruit tree. In Vitro Cellular & Developmental Biology - Plant, v. 32, n. 4, p. 253-256, 1996. ).

Research Institutions

The most relevant research institutions are illustrated below, where it can be observed that five institutions concentrate the majority of published works related to the propagation and conservation of the mangabeira tree. The Federal University of Lavras (UFLA), the Federal University of Paraíba (UFPB), the Federal University of Sergipe (UFS), the Brazilian Agricultural Research Corporation (EMBRAPA), and the Federal Institute of Goiano (IFGOIANO) stand out (Figure 4).

Figure 4
Most relevant research institutions (based on several published papers) on the propagation and conservation of mangabeira. *UFLA = Universidade Federal de Lavras; UFPB = Universidade Federal da Paraíba; UFS = Universidade Federal de Sergipe; EMBRAPA = Empresa Brasileira de Pesquisa Agropecuária; IFGOIANO = Instituto Federal Goiano; UFRN = Universidade Federal do Rio Grande do Norte; UFPE = Universidade Federal de Pernambuco; UFPR = Universidade Federal do Paraná; UEMS = Universidade Estadual do Mato Grosso do Sul; UNESP = Universidade Estadual Paulista; UEFS = Universidade Estadual de Feira de Santana; UFSJ = Universidade Federal de São João del-Rei; UFGD = Universidade Federal da Grande Dourados; UFPA = Universidade Federal do Pará; UNICAMP = Universidade Estadual de Campinas; UNIFESP = Universidade Federal de São Paulo; UNB = Universidade de Brasília.

Analysis of keyword trends

In addition to the analyses presented above, a trend study was conducted based on the keywords used by authors in the field of mangabeira tree propagation (Figure 5). It is evident that, alongside keywords emphasizing the scientific name, fruit, and the species’ natural range, studies have predominantly centered around plant tissue culture, with a specific emphasis on micropropagation (Oliveira et al., 2016OLIVEIRA, K. S. de; FREIRE, F. A. de M.; ALOUFA, M. A. I. Efeito de 6-benzilaminopurina e ácido naftalenoacético sobre a propagação in vitro de Hancornia speciosa Gomes. Floresta, v. 46, n. 3, p. 335-342, 2016. ; Prudente et al., 2016PRUDENTE, D. de O.; PAIVA, R.; NERY, F. C.; et al. Indirect in vitro organogenesis of Hancornia speciosa Gomes. Bioscience Journal, v. 32, n. 3, p. 721-729, 2016. ). Moreover, other significant terms highlight aspects related to the species’ recalcitrant seeds, germination, and research focused on the mineral nutrition of seedlings (Bessa et al., 2013BESSA, L. A.; SILVA, F. G.; MOREIRA, M. A.; TEODORO, J. P. R.; SOARES, F. A. L.. Characterization of nutrient deficiency in Hancornia speciosa Gomes seedlings by omitting micronutrients from the nutrient solution. Revista Brasileira de Fruticultura, v. 35, n. 2, p. 616-624, 2013. ; Santos et al., 2021SANTOS, G. R. dos; FERREIRA, W. de M.; COIMBRA, R. R. Seed germination in natural populations of Hancornia speciosa. Diversitas Journal, v. 6, n. 1, p. 376-395, 2021. ).

Figure 5
Trends in mangabeira based on authors’ keywords on mangabeira propagation and conservation.

Seed technology

Considering the information presented in the table below, it is emphasized that a wide range of factors affects the germination of mangabeira seeds, including storage, processing, drying, seed morphology, and biometrics (Table 1). Biometric analyses of fruits and seeds have revealed significant phenotypic variability among different mangabeira accessions (Soares et al., 2019SOARES, A. N. R.; SILVA, A. V. C. da; MUNIZ, E. N.; et al. Biometry, Emergence and Initial Growth of Accessions and Mangaba Progenies. Journal of Agricultural Science, v. 11, n. 4, p. 436-448, 2019. ). Regarding processing, manual extraction proves more effective in obtaining seeds of higher physiological quality compared to mechanical methods (Barros et al., 2006BARROS, D. I.; BRUNO, R. de L. A.; NUNES, H. V.; et al. Métodos de extração de sementes de mangaba visando à qualidade fisiológica. Revista Brasileira de Fruticultura, v. 28, n. 1, p. 25-27, 2006. ; Nunes et al., 2021NUNES, V. V.; SILVA-MANN, R.; VASCONCELOS, M. C.; et al. Physical and physiological quality of mangaba seeds obtained by different processing methods. Revista Brasileira de Engenharia Agrícola e Ambiental, v. 25, n. 6, p. 429-435, 2021. ).

The ideal temperature for germination of H. speciosa seeds has been determined to be between 20-30°C (Oliveira e Valio, 1992OLIVEIRA, L. M. Q.; VALIO, I. F. M. Effects of moisture content on germination of seeds of Hancornia speciosa Gomes (Apocynaceae). Annals of Botany, v. 69, n. 1, p. 1-5, 1992. ). In the guidelines for seed analysis of forest species, it is recommended that germination tests occur at 25°C on a paper roll substrate, with eight replications of 50 seeds (Brazil, 2013BRASIL. Ministério da Agricultura, Pecuária e Abastecimento. Instruções para análise de sementes de espécies florestais Ministério da Agricultura, Pecuária e Abastecimento. Secretaria de Defesa Agropecuária. Brasília: MAPA/ACS , 2013. 98 p.). Natural drying of H. speciosa seeds in a laboratory environment can impair emergence and initial seedling growth after 48 hours (Santos et al., 2010SANTOS, P. C. G. dos; ALVES, E. U.; GUEDES, R. S.; et al. Qualidade de sementes de Hancornia speciosa Gomes em função do tempo de secagem. Semina: Ciências Agrárias, v. 31, n. 2, p. 343, 2010. ). In addition, reducing the water content between 20% and 5% reduces the physiological potential of the seeds (Masetto e Scalon, 2014MASETTO, T. E.; SCALON, S. de P. Q. Drying and Osmotic Conditioning in Hancornia speciosa Gomes Seeds. Floresta e Ambiente, v. 21, n. 1, p. 62-68, 2014. ). Mangabeira seeds are also influenced by the depth of sowing and the type of substrate and should be planted one centimeter deep in Cerrado soil with up to 15% washed sand (Oliveira et al., 2018OLIVEIRA, K. S. de; ALOUFA, M. A. I. Slow growth in vitro culture for conservation of Hancornia speciosa Gomes. FLORESTA, v. 52, n. 1, p. 007, 2022. ).

Importantly, the germination of H. speciosa seeds starts from day 12 and extends until day 41, with an average emergence of 55.4% and average days to emergence of 22.64 (Vieira et al., 2015VIEIRA, C. do M.; NAVES, R. V.; SOUZA, R. B. de S. E.; et al. Emergência de plântulas de mangabeira provenientes de frutos coletados em diferentes localidades do Estado de Goiás. Comunicata Scientiae , v. 6, n. 1, p. 33-44, 2015. ). Mangabeira seeds are classified as recalcitrant, meaning that they do not tolerate drying and storage (Nunes et al., 2022NUNES, V. V.; SILVA-MANN, R.; SOUZA, J. L.; et al. Physiological and molecular changes in seeds of Hancornia speciosa Gomes stored in conservative solutions. Journal of Seed Science, v. 44, n. e202244018, 2022. ). Some studies have sought to develop protocols for the conservation of mangabeira seeds for long periods. An example is the work done by Nunes et al. (2022)NUNES, V. V.; SILVA-MANN, R.; SOUZA, J. L.; et al. Physiological and molecular changes in seeds of Hancornia speciosa Gomes stored in conservative solutions. Journal of Seed Science, v. 44, n. e202244018, 2022. , who observed that mangabeira seeds can be stored for up to 50 days in preservative solutions.

In general, this information is valuable for improving the seedling production of this species, as it provides important information about the factors that affect seed quality and can be used to improve conservation practices and large-scale seedling production of this species.

Production of seedlings

Studies show that the combination of various materials for substrate composition, such as topsoil, coconut fiber, and sand, can provide a suitable foundation for developing mangabeira seedlings (Dias et al., 2007DIAS, T. J.; PEREIRA, W. E.; SOUSA, G. G. de. Fertilidade de substratos para mudas de mangabeira, contendo fibra de coco e adubados com fósforo. Acta Scientiarum. Agronomy, v. 29, n. 5, p. 649-658, 2007. ; Nogueira et al., 2003NOGUEIRA, R. J. M. C.; ALBUQUERQUE, M. B. de; SILVA JUNIOR, J. F. Efeito do substrato na emergência, crescimento e comportamento estomático em plântulas de mangabeira. Revista Brasileira de Fruticultura, v. 25, n. 1, p. 15-18, 2003. ). The use of bovine manure has also been indicated as an important component for substrate fertilization in the production of seedlings of this species (Arrua et al., 2016ARRUA, L. L. C. de; COSTA, E.; BARDIVIESSO, E. M.; et al. Protected environments and substrates for mangabeira seedlings (Hancornia speciosa Gomes) production. Engenharia Agricola, v. 36, n. 6, p. 984-995, 2016. ; Dias et al., 2009DIAS, T. J.; PEREIRA, W. E.; CAVALCANTE, L. F.; et al. Desenvolvimento e qualidade nutricional de mudas de mangabeiras cultivadas em substratos contendo fibra de coco e adubação fosfatada. Revista Brasileira de Fruticultura, v. 31, n. 2, p. 512-523, 2009. ; Oliveira Lima et al., 2020LIMA, I. M. de O.; SALLES, J. S.; COSTA, E.; et al. Quality and growth of mangaba (Hancornia speciosa) seedlings according to the substrate and shading. Australian Journal of Crop Science, v. 14, n. 3, p. 531-536, 2020. ; Silva et al., 2009SILVA, E. A. da; MARUYAMA, W. I.; OLIVEIRA, A. C. de; et al. Efeito de diferentes substratos na produção de mudas de mangabeira (Hancornia speciosa). Revista Brasileira de Fruticultura, v. 31, n. 3, p. 925-929, 2009. ). It is interesting to note that different combinations of these materials have been used in various studies, suggesting that the choice of substrate may depend on several factors, such as the type of substrate, botanical variety, and production objectives. This choice stands out as one of the main factors influencing seedling production (Table 2).

Furthermore, there is evidence that inoculation of mycorrhizal fungi can be beneficial for the growth of mangabeira seedlings (Abreu et al., 2022ABREU, G. M.; PAIVA, H. N. DE; KASUYA, M. C. M.; et al. Soil of the parent plant and AMF mix improve Cerrado’s seedlings growth in forest nurseries. IForest, v. 15, p. 197-205, 2022. ; Cardoso Filho et al., 2008CARDOSO FILHO, J. A.; LEMOS, E. E. P. de; SANTOS, T. M. C. dos; et al. Mycorrhizal dependency of mangaba tree under increasing phosphorus levels. Pesquisa Agropecuária Brasileira, v. 43, n. 7, p. 887-892, 2008. ; Costa et al., 2003COSTA, C. M. C.; CAVALCANTE, U. M. T.; LIMA JUNIOR, M. de L.; et al. Inoculum density of arbuscular mycorrhizal fungi needed to promote growth of Hancornia speciosa Gomes seedlings. Fruits, v. 58, n. 5, p. 247-254, 2003. , 2005COSTA, C. M. C.; CAVALCANTE, U. M. T.; GOTO, B. T.; et al. Fungos micorrízicos arbusculares e adubação fosfatada em mudas de mangabeira. Pesquisa Agropecuária Brasileira, v. 40, n. 3, p. 225-232, 2005. ). These fungi can form a symbiotic relationship with plant roots, increasing their ability to absorb nutrients from the soil. The choice of the type of mycorrhizal fungus used may depend on soil conditions and nutrient availability (Smith, Read, 2008SMITH, S. E.; READ, D. The symbionts forming arbuscular mycorrhizas. In: SMITH, S. E.; READ, D. (Eds.). Mycorrhizal Symbiosis. Third Edition ed. London: Academic Press, p. 13-41, 2008. ).

Another important factor in the production of mangabeira seedlings is the adequate nutrition of the plants. The omission of important nutrients, such as N, P, K, Ca, Mg, and S, can result in significant changes in plant growth and the appearance of deficiency symptoms (Bessa et al., 2012BESSA, L. A.; SILVA, F. G.; MOREIRA, M. A.; et al. Characterization of the effects of macronutrient deficiencies in mangabeira seedlings. Revista Brasileira de Fruticultura, v. 34, n. 4, p. 1235-1244, 2012. , 2013BESSA, L. A.; SILVA, F. G.; MOREIRA, M. A.; TEODORO, J. P. R.; SOARES, F. A. L.. Characterization of nutrient deficiency in Hancornia speciosa Gomes seedlings by omitting micronutrients from the nutrient solution. Revista Brasileira de Fruticultura, v. 35, n. 2, p. 616-624, 2013. ). Therefore, it is critical to ensure that seedlings obtain balanced nutrition, either through substrate or fertilizer application. It is interesting to note that mangabeira can be grown in consortium with other crops, such as cassava. This can bring benefits to both seedling production and final crop production (Martinotto et al., 2012MARTINOTTO, F.; MARTINOTTO, C.; COELHO, M. de F. B.; et al. Sobrevivência e crescimento inicial de espécies arbóreas nativas do Cerrado em consórcio com mandioca. Pesquisa Agropecuária Brasileira, v. 47, n. 1, p. 22-29, 2012. ). In addition, the seedlings seem to be able to tolerate water deficits, adapting to stress by increasing root depth and reducing the emission of sprouts (Scalon et al., 2015SCALON, S. de P. Q.; KODAMA, F. M.; DRESCH, D. M.; et al. Gas exchange and photosynthetic activity in Hancornia speciosa Gomes seedlings under water deficit conditions and during rehydration. Bioscience Journal, v. 31, n. 4, p. 1124-1132, 2015. ; Silva et al., 2016SILVA, E. C. da; PRADO, T. B.; ALCÂNTARA, R. N. de; et al. Different levels of water deficit induces changes in growth pattern but not in chlorophyll fluorescence and water relations of Hancornia speciosa Gomes seedlings. Scientia Plena, v. 12, n. 2, 2016. ).

The production of mangabeira seedlings by vegetative propagation, whether by staking, budding, or grafting, is still little explored, especially for the northeastern botanical variety H. speciosa var. speciosa Gomes, which hinders its cloning on a large scale and, consequently, the establishment of commercial orchards. Regarding staking, the study by Soares et al. (2020SOARES, F. S.; LUZ, P. B. da; ROCHA, V. L. P.; et al. Aspectos anatômicos de impedimentos ao enraizamento em estacas caulinares de mangabeira. Acta Iguazu, v. 9, n. 1, p. 82-89, 2020. ) revealed total mortality of the cuttings, but no anatomical impediments were found for the rooting of the cuttings. Vieira et al. (2020VIEIRA, M. do C.; SOUZA, J. L. da C.; SILVA, G. D. da; ET al. 2.4-Dichlorophenoxyacetic acid and sucrose in rhizogenesis maintenance and induction in cuttings of cagaita and mangabeira from cerrado. Revista Ibero-Americana de Ciências Ambientais, v. 11, n. 2, p. 118-127, 2020.) observed a 100% survival of the cuttings, but only with the emission of root primordia. No scientific articles on the propagation of mangabeira by air layering were found in the review. However, in a master’s thesis conducted by (Reis, 2011REIS, L. L. dos. Propagação de Hancornia speciosa gomes - Apocynaceae, por alporquia e micropropagação. São Paulo-SP: Faculdade de Engenharia - UNESP, 2011.), it was observed that 25% of simple layerings took root, irrespective of the substrate or the concentration of indole butyric acid used. Similarly, (Tiago, 2020TIAGO, B. dos S. Propagação vegetativa por alporquia e otimização de protocolo de estabelecimento in vitro de mangabeira (Hancornia speciosa Gomes). Goiânia-GO: Universidade Federal de Goiás, Programa de pós-graduação em genética e melhoramento de plantas, 2020.) achieved success in layering different varieties of mangabeira. Additionally, no articles were found reporting the propagation of mangabeira by grafting. Nevertheless, this technique is detailed in books and technical communications concerning Cerrado varieties and can be executed through lateral or top grafting and budding. Success rates range from 60% to 90% on 12-month-old rootstocks (Lédo et al., 2015LÉDO, A. S.; VIEIRA NETO, R. D.; SILVA JÚNIOR, J. F.; et al. A cultura da mangaba. Brasília-DF: Embrapa (Coleção Plantar, 73), 2015. ; Pereira et al., 2006PEREIRA, A.; PEREIRA, E.; ARAÚJO, I.; et al. A cultura da mangaba. [s.l.] Embrapa Tabuleiros Costeiros, 2006. . ).

In summary, the production of mangabeira seedlings involves several important factors, such as the choice of substrate, inoculation of mycorrhizal fungi, adequate nutrition, and adaptation to environmental conditions should be considered. Large-scale vegetative propagation is still not widespread, making it difficult to establish plantations. The knowledge of these factors can contribute to the production of healthy seedlings of high genetic quality, capable of surviving the adverse conditions of the field.

In vitro propagation

Plant tissue culture presents several techniques that can assist in large-scale propagation and ex-situ conservation of native fruit species such as H. speciosa. Among these techniques, we can highlight in vitro germination, micropropagation, in vitro conservation, and cryopreservation. Micropropagation is the technique that has presented the most significant impacts and concrete results within the culture of plant tissue (Abdalla et al., 2022ABDALLA, N.; EL-RAMADY, H.; SELIEM, M. K.; et al. An academic and technical overview on plant micropropagation challenges. Horticulturae, v. 8, n. 8, p. 677, 2022. ). This technique encompasses several stages, ranging from in vitro establishment and germination, through multiplication and rooting to acclimatization (George et al., 2007GEORGE, E. F.; HALL, M. A.; KLERK, G.-J. de. Plant Propagation by Tissue Culture. Dordrecht: Springer Netherlands, 2007. ).

The in vitro germination of mangabeira seeds is a fundamental process for the efficient in vitro propagation of this species. Several studies have been conducted to identify the factors that influence in vitro germination and, consequently, optimize this technique. One of the aspects investigated was the culture medium used. It has been verified that the MS medium, with half of the saline concentration or the WPM medium, supplemented with 2.0 g L^-1 of activated carbon or with 15.0 g L^-1 of sucrose and 0.2 mg L^-1 of GA₃ respectively, promoted high percentages of germination and good development of the aerial part and root system of mangabeira seedlings (Lédo et al., 2007LÉDO, A. da.; SECA, G. S. V.; BARBOZA, S. B. S. C.; et al. Crescimento inicial de mangabeira (Hancornia speciosa Gomes) em diferentes meios de germinação in vitro. Ciência e Agrotecnologia, v. 31, n. 4, p. 989-993, 2007. , Soares et al., 2009SOARES, F. P.; PAIVA, R.; STEIN, V. C.; et al. Efeito de meios de cultura, concentrações de GA3 e pH sobre a germinação in vitro de mangabeira (Hancornia speciosa Gomes). Ciência e Agrotecnologia, v. 33, n. spe, p. 1847-1852, 2009. ). Different support agents were also tested, verifying that the presence of vermiculite, either alone or combined with sand, exerted a positive influence on the in vitro germination of mangabeira seeds (Oliveira et al., 2014OLIVEIRA, K. S. de; OLIVEIRA, M. da S.; PEREIRA, E. C.; et al. Efeito de diferentes meios de cultura na germinação in vitro de sementes de mangabeira (Hancornia speciosa Gomes). Revista Árvore, v. 38, n. 4, p. 601-607, 2014. ).

Regarding micropropagation, there are several options for culture medium and growth factors that have been tested, as can be seen in Tab. 3. The multiplication of stem apices and nodal segments in an MS medium supplemented with 4 uM of BA (benzyladenine) and 2.5 µM of AIB showed to be an efficient technique for the in vitro propagation of mangabeira (Pereira-Netto, 1996PEREIRA-NETTO, A. B. In vitro propagation of Hancornia speciosa, a tropical fruit tree. In Vitro Cellular & Developmental Biology - Plant, v. 32, n. 4, p. 253-256, 1996. ). The addition of 1.0 mg L^-1 or 2.0 mg L^-1 in the WPM medium allows well-developed buds to be obtained (Soares et al., 2007SOARES, F. P.; PAIVA, R.; ALVARENGA, A. A. de; et al. Organogênese direta em explantes caulinares de mangabeira (Hancornia speciosa Gomes). Ciência e Agrotecnologia, v. 31, n. 4, p. 1048-1053, 2007. , 2011SOARES, F. P.; PAIVA, R.; ALVARENGA, A. A. de; et al. Taxa de multiplicação e efeito residual de diferentes fontes de citocinina no cultivo in vitro de Hancornia speciosa Gomes. Ciência e Agrotecnologia, v. 35, n. 1, p. 152-157, 2011. ). Moreover, in vitro, rooting of H. speciosa can be achieved in a WPM medium supplemented with the combination of 4.92 µM ANA and 4.92 µM AIB (Prudente et al., 2016PRUDENTE, D. de O.; PAIVA, R.; NERY, F. C.; et al. Indirect in vitro organogenesis of Hancornia speciosa Gomes. Bioscience Journal, v. 32, n. 3, p. 721-729, 2016. ).

These results indicate that mangabeira plants multiplied in flasks sealed with para-film® and PVC film have a higher number of sprouts in both the first and second subcultivation after 65 days (Sá et al., 2012SÁ, A. de J.; LÉDO, A. da S.; LÉDO, C. A. da S.; et al. Sealing and explant types on the mangaba micropropagation. Ciência e Agrotecnologia, v. 36, n. 4, p. 406-414, 2012. ). The use of sealing lids that allow the exchange of gases between the container and the external environment provides an increase in CO₂ concentration in the container and consequently a reduction in ethylene concentration (Fortini et al., 2021FORTINI, E. A.; BATISTA, D. S.; MAMEDES-RODRIGUES, T. C.; et al. Gas exchange rates and sucrose concentrations affect plant growth and production of flavonoids in Vernonia condensate grown in vitro. Plant Cell, Tissue and Organ Culture, v. 144, n. 3, p. 593-605, 2021. ). The accumulation of ethylene in the container negatively influences the development of the plant and may cause leaf abscission and apical necrosis, which has been a limiting factor in the in vitro propagation of mangabeira (Teixeira da Silva et al., 2020SILVA, J. A. T. da; NEZAMI-ALANAGH, E.; BARREAL, M. E.; KHER, M. M.; WICAKSONO, A.; GULYÁS, A., DOBRÁNSZKI, J. Shoot tip necrosis of in vitro plant cultures: a reappraisal of possible causes and solutions. Planta, v. 252, n. 3, p. 47, 2020. ). Other studies have shown that inoculation of bacterial isolates during mangabeira micropropagation influenced the number of buds and expanded leaves (Cabral et al., 2018CABRAL, J.; PEREIRA, F. D.; SILVA, F. G. In vitro inoculation of phosphate-solubilizing microorganisms in seedlings of Mangaba (Hancornia speciosa Gomes). Ecology Environment and Conservation, v. 24, n. 3, p. 1442-1450, 2018.). The occurrence of somaclonal variation during micropropagation of H. speciosa was also not observed (Costa et al., 2022COSTA, G. F. da; CABRAL, P. D. S.; SILVA, F. G.; et al. Clonal fidelity and genetic diversity of micropropagated Hancornia speciosa Gomes (Apocynaceae) as Evaluated by Molecular Markers. Forests, v. 13, n. 10, p. 1645, 2022. ).

Overall, the table below shows a wide variety of techniques and factors that have been tested for in vitro propagation and cultivation of mangabeira (Table 3). The findings suggest that the success of micropropagation, growth, and in vitro germination of mangabeira depends on several factors, including culture media, plant growth regulators, temperature, and culture conditions. These results may be useful for future studies on the in vitro propagation and cultivation of mangabeira and other plant species.

In vitro conservation and cryopreservation

The studies presented in the table below present significant advances in the area of in vitro conservation and cryopreservation of mangabeira (Table 4). In vitro conservation techniques of nodal segments and mangabeira micro shoots have been studied under different conditions, including the presence or absence of sucrose and sorbitol, as well as the use of abscisic acid in flasks sealed with aluminum foil (Lédo et al., 2011LÉDO, A. S.; SÁ, A. J.; SILVA JUNIOR, J. F.; et al. Acta Horticulturae, n. 918, p. 177-182, 2011. ; Sá et al., 2011SÁ, A. de J.; LÉDO, A. da S.; LÉDO, C. A. da S. Conservação in vitro de mangabeira da região nordeste do Brasil. Ciência Rural, v. 41, n. 1, p. 57-62, 2011. ; Santos et al., 2011SANTOS, M. da C.; LÉDO, A. da S.; LÉDO, C. A. da S.; et al. Efeito da sacarose e do sorbitol na conservação in vitro de segmentos nodais de mangabeira. Revista Ciência Agronômica, v. 42, n. 3, p. 735-741, 2011. ). The results indicate that the technique of in vitro conservation by slow growth in a half-strength culture medium or supplemented with sucrose and sorbitol is viable for a period of 90 to 120 days and that the use of abscisic acid at a concentration of 0.5 mg L^-1 is efficient for the in vitro conservation of mangabeira micro shoots (Lédo et al., 2011LÉDO, A. S.; SÁ, A. J.; SILVA JUNIOR, J. F.; et al. Acta Horticulturae, n. 918, p. 177-182, 2011. , Pires et al., 2019PIRES, D. C. M.; TRENTO, S. de M.; PAULA, M. S. P. de; et al. In vitro conservation of mangaba native to Brazilian Cerrado. Plant Cell Culture & Micropropagation, v. 15, n. 2, p. 33-39, 2020. , Oliveira e Aloufa, 2022OLIVEIRA, K. S. de; ALOUFA, M. A. I. Slow growth in vitro culture for conservation of Hancornia speciosa Gomes. FLORESTA, v. 52, n. 1, p. 007, 2022. , Pires et al., 2022PIRES, D. C. M.; ASMAR, S. A.; LUZ, J. M. Q.; et al. In vitro conservation of mangaba (Hancornia speciosa Gomes): An important fruit tree of Brazilian Cerrado. Australian Journal of Crop Science, v. 16, n. 9, p. 1084-1093, 2022. ). Osmoregulators such as sucrose and sorbitol, depending on the concentration used, perform the function of removing excess intracellular water through an osmotic gradient. This results in slower growth of the culture, which allows its conservation (El-Bahr et al., 2016EL-BAHR, M. K.; ABD EL-HAMID, A.; MATTER, M. A.; et al. In vitro, conservation of embryogenic cultures of date palm using osmotic mediated growth agents. Journal of Genetic Engineering and Biotechnology, v. 14, n. 2, p. 363-370, 2016. ; Flores et al., 2013FLORES, R.; ULIANA, S. C.; PIMENTEL, N.; et al. Sacarose e sorbitol na conservação in vitro de Pfaffia tuberosa (Spreng.) Hicken (Amaranthaceae). Journal of Biotechnology and Biodiversity, v. 4, n. 3, p. 192-199, 2013. ).

Regarding cryopreservation, the drop vitrification and encapsulation-vitrification techniques were successfully tested for mangabeira (Prudente et al., 2017PRUDENTE, D. O.; PAIVA, R.; NERY, F. C.; et al. Encapsulation of lateral buds of Hancornia speciosa. Acta Horticulturae, v. 1155, n. 1155, p. 59-64, 2017. ; Santos et al., 2015SANTOS, P. A. A.; PAIVA, R.; SILVA, L. C.; et al. Effect of load solution and growth media on cryopreservation by droplet vitrification of Hancornia speciose shoot tips. Acta Horticulturae, n. 1083, p. 507-512, 2015. ). In addition, the combination of BA×ANA was used to promote greater regeneration of H. speciosa stem apices after cryopreservation (Santos et al., 2015SANTOS, P. A. A.; PAIVA, R.; SILVA, L. C.; et al. Cryopreservation of the mangaba tree (Hancornia speciosa Gomes): A protocol for long-term storage. Acta Scientiarum - Agronomy, v. 37, n. 3, p. 289-296, 2015. ). Other studies explored encapsulation in sodium alginate capsules with BAP and precultivation of lateral buds in medium with proline for 24 hours, which resulted in higher regeneration rates of H. speciosa lateral buds (Prudente et al., 2014PRUDENTE, D. D. O.; PAIVA, R.; NERY, F. C.; et al. Criopreservação de gemas laterais de mangabeira: o papel da prolina. Revista Saúde e Ciência, v. 3, n. 3, p. 86-93, 2014.; Prudente et al., 2017PRUDENTE, D. de O.; PAIVA, R.; NERY, F. C.; et al. Behavior of lateral buds of Hancornia speciosa after cryopreservation by encapsulation-vitrification. Acta Scientiarum - Biological Sciences, v. 39, n. 1, p. 87-93, 2017. ; Prudente et al., 2017PRUDENTE, D. O.; PAIVA, R.; NERY, F. C.; et al. Encapsulation of lateral buds of Hancornia speciosa. Acta Horticulturae, v. 1155, n. 1155, p. 59-64, 2017. ). However, limitations in the cryopreservation technique were also found, such as the lack of survival and regeneration of mangabeira zygotic embryos after cryopreservation by the desiccation technique (Santana et al., 2018SANTANA, F. V.; OLIVEIRA, A. C. A. de; OLIVEIRA, L. A. R. de; et al. Effect of desiccation time on seed moisture and regeneration of mangaba (Hancornia speciosa) embryos. Journal of Experimental Agriculture International, v. 28, n. 1, p. 1-10, 2018. ). In summary, the studies present important advances in the area of in vitro conservation and cryopreservation of mangabeira, demonstrating the feasibility of different techniques for the long-term conservation of this species.

CONCLUSIONS

From the information presented above, it is possible to notice an increase in the studies related to the propagation and conservation of mangabeira in the last ten years, showing its relevance. Moreover, it is noticeable the advance of scientific knowledge about this species in several areas of study, especially about seed technology, seedling production, cryopreservation, propagation, and in vitro conservation. Linked to the points above, it is possible to consider that the asexual propagation of mangabeira via cutting, or another form of cloning, may become an important subject of study in the coming years since currently there are no well-established protocols for clonal propagation ex vitro of this species, which limits the implementation of commercial plantations and highlights the need for research in this area. Furthermore, improving techniques for cryopreservation and storage of mangabeira seeds, and the development of protocols for somatic embryogenesis, maybe a future trend to support research for this species.

ACKNOWLEDGMENTS

The authors would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for granting the scholarship to the first author.

REFERENCES

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