Biotecnología en Plinia sp: necesidades y perspectivas para un grupo desatendido de especies frutales

Daniele Damian dos Santos

Artículo de revisión

Biotecnología Vegetal Vol. 21, No. 1: 3-14 , enero - marzo, 2021

Instituto de Biotecnología de las Plantas. UCLV. MES

eISSN 2074-8647, RNPS: 2154

Biotechnology in Plinia spp.: needs and perspectives for a neglected group of fruit species

Biotecnología en Plinia spp.: necesidades y perspectivas para un grupo desatendido de especies frutales

Daniele Damian dos Santos1 https://orcid.org/0000-0002-3795-1796

Luana Oliveira de Oliveira1 https://orcid.org/0000-0001-7472-4149

Dalvan Carlos Beise2 https://orcid.org/0000-0001-8638-7004

Lilian de Oliveira Machado2 https://orcid.org/0000-0002-4172-2283

Valdir Marcos Stefenon1,2* https://orcid.org/0000-0003-1091-700X

1Programa de Pós-Graduação em Ciências Biológicas, Universidade Federal do Pampa. Av Antonio Trilha 1847. São Gabriel. RS. Brazil. 97300-162

2Departamento de Fitotecnia, Laboratório de Fisiologia do Desenvolvimento e Genética Vegetal, Rod Admar Gonzaga 1346. Universidade Federal de Santa Catarina. Florianópolis. SC. Brazil. 88034-000

*Corresponding author e-mail: valdir.stefenon@ufsc.br

ABSTRACT

Plinia species comprise a group of underrated fruit trees native to the South and Central American neotropics. Their fruits have high potential as a nutraceutical food and to the medicinal industry. However, among the 80 accepted species, less than a dozen are cultivated. In this review, the state-of-the-art of the genetic diversity and the techniques of vegetative propagation of Plinia spp. was updated. Therewith, it is intended to encourage further studies for genetically disentangle the taxonomic classification the species, and the development of propagation protocols towards the establishment of commercial plantations. Establishing commercial orchards of Plinia species may open new markets for this fruit crop, but the absence of breeding programs and superior quality seedlings hinder such endeavors. The main outcomes of this study are the need of using molecular approaches for solving the taxonomic uncertainties among Plinia species and micropropagation protocols to overcome the difficulties concerning to the vegetative propagation of this species.

Keywords: biotechnology, jaboticabeira, micropropagation, molecular taxonomy, morphological diversity, vegetative propagation

RESUMEN

Las especies de Plinia comprenden un grupo subestimado de árboles frutales nativos de los neotrópicos de América del Sur y Central. Sus frutos tienen un alto potencial como alimento nutracéutico y para la industria medicinal. Sin embargo, entre las 80 especies aceptadas, se cultivan menos de una docena. En esta revisión, se actualizó el estado del arte de la diversidad genética y las técnicas de propagación vegetativa Plinia spp. Con ello, se propondrá impulsar nuevos estudios para dilucidar genéticamente la clasificación taxonómica de la especie y el desarrollo de protocolos de propagación hacia el establecimiento de plantaciones comerciales. El establecimiento de plantaciones comerciales de especies Plinia puede abrir nuevos mercados para este cultivo de frutas, pero la ausencia de programas de mejoramiento genético y plántulas de calidad superior obstaculizan tales esfuerzos. Los principales resultados de este estudio son la necesidad de utilizar enfoques moleculares para resolver las incertidumbres taxonómicas entre las especies de Plinia y los protocolos de micropropagación para superar las dificultades relacionadas con la propagación vegetativa de esta especie.

Palabras clave: biotecnología, diversidad morfológica, jaboticabeira, micropropagación, propagación vegetativa, taxonomía molecular

INTRODUCTION

Jaboticabeira is the popular name of different species of the genus Plinia L. (Myrtaceae), native to the South and Central American neotropics (Figure 1 A). The main characteristic of these trees (Figure 1 B) is the development of flowers and fruits (popularly known as jaboticaba) over the wood trunk and main stems (Figure 1 C-D), a feature known as cauliflory. Reproductive buds of Plinia initiate from vascular cambium cells through cell division followed by an increase in the size of the meristematic region from the vascular cambium toward both the bark and the xylem, keeping the connection with vessel elements (Oliveira et al., 2019).

Figure 1. (A) Distribution of Plinia species in neotropical South and Central America according to the Plants of the World platform (www.plantsoftheworldonline.org). CU: Cuba, HA: Haiti, SD: San Domingo, BZ: Belize, GU: Guatemala, HO: Honduras, CR: Costa Rica, PN: Panamá, CO: Colombia, VE: Venezuela, GU: Guyana, SU: Suriname, EQ: Equador, PE: Peru, BO: Bolivia, BR: Brazil, PY: Paraguay, AR: Argentina, UR: Uruguay. (B) Adult tree of Plinia peruviana growing in an urban backyard. (C) Flowers growing along the tree stem. (D) Rip fruits along the tree stem.

Fruits are produced once or twice a year, eventually up to three times, depending on climatic conditions and the management adopted. In Plinia jaboticaba, it seems that inflorescence sprouting is stimulated by low temperatures and water deficit (Oliveira et al., 2019). The fruits have economic potential both for fresh consumption and in the food and pharmaceutical industries. They present a wide variety of classic nutrients and components capable of providing positive physiological effects on health (Teixeira et al., 2008; Rufino et al., 2011). They also have recognized antioxidant properties, protecting from damages caused by free radicals, preventing or postponing the onset of cardiovascular, chronic, and neurodegenerative diseases (Pitz et al., 2017).

In this context, this review aims at updating the state-of-the-art of the taxonomic and genetic diversity and the techniques of vegetative propagation of Plinia spp. Therewith, it is intended to encourage the development of further studies for genetically disentangle the taxonomic classification of the Plinia species, and the development of propagation protocols towards the establishment of commercial plantations, attempting the market valuation of the fruit.

Expanding genetic and genomic analyses are needed to disentangle the subtle inter-species morphological differences.

The jabuticabeiras were firstly taxonomically described into genus Myrtus Tourn ex. L. and Guapurium Juss. and were relocated within genus Myrciaria O. Berg (Berg, 1857). As some floral traits diverged from other species of genus Myrciaria, species of jabuticabeira were transferred to genus Plinia (Kausel, 1956; Sobral, 1985; Mattos, 1998). Currently, 80 species of Plinia are accepted (Govaerts et al., 2008).

Given the morphological variation observed in characteristics of fruits (Table 1, Table 2 and Table 3), the taxonomy of Plinia species is fairly a puzzle in the scientific literature. A miscellaneous of different species is suggested by diverging authors, making advances in selection, domestication, and breeding difficult.

Besides recognizing the morphological multiplicity, understanding the genetic divergence among species can be useful for the comprehension and conservation of the available genetic resources. Moreover, the morphological differences among some Plinia species are rather modest, making the species delimitation a great challenge for breeders and farmers.

Table 1. Morphological characteristics of Plinia cauliflora, P. jaboticaba and P. aureana according to Lorenzi (2000), Lorenzi et al.(2006), and Lorenzi (2011).

Table 2. Morphological characteristics of Plinia coronata, P. grandifolia and P. oblongata according to Lorenzi (2000), Lorenzi et al.(2006), and Lorenzi (2011)

Table 3. Morphological characteristics of Plinia peruviana, P. phitrantha and P. spiritosantensis according to Lorenzi (2000), Lorenzi et al. (2006), and Lorenzi (2011).

Despite these needs, only a few studies using molecular markers were published, reporting the comparative analysis among different species of Plinia . Pereira et al. (2005) used 45 polymorphic RAPD markers in a study including P. jaboticaba, P. cauliflora, P. coronata, and P. phitrantha , while Vilela et al. (2012) used 37 polymorphic RAPD markers to study the relationship among P. cauliflora, P. jaboticaba, P. coronata, and P. peruviana. In both studies, clustering analyses were unsuited for defining the taxonomic groups, since the formed clusters comprised assortments of plants from different species and did not correspond to the taxonomic classifications based on morphological traits. Moreover, RAPD markers are not confident for such an analysis, due to several technical weaknesses.

The advances of the sequencing platforms have enabled researchers to generate comprehensive genomic data for several plant species, including also minor-crop species. Sequences of the complete chloroplast genome (plastome) of P. cauliflora, P. aureana, and P. trunciflora are available in the GenBank database. To test the usefulness of these molecular data for understanding the taxonomic relationship among Plinia species, the plastome sequences of P. cauliflora (KX527622; Machado et al., unpublished), P. aureana (KY392759; Machado et al., unpublished), P. trunciflora (KU318111; Eguiluz et al., 2017), Acca sellowiana (KX289887; Machado et al., 2017), Campomanesia xanthocarpa (KY392760; Machado et al., 2020), and Allosyncarpia ternata (KC180806; Bayly et al., 2013) were downloaded and a phylogenomic analysis was performed. This analysis (Figure 2) enabled more accurate analysis of the correlation among these Plinia species. Although the length, genetic composition, and structure of the plastomes are conserved among these species, the phylogenomic analysis based on the whole plastomes sequences resolved these three species with high support (Figure 2).

Thus, sequencing the plastomes of more Plinia species seems to be a meaningful strategy for resolving the remaining taxonomic uncertainties in this group, aiding the planning of conservation and breeding programs for Plinia species.

Figure 2. Phylogenomic analysis based on the whole plastome sequences of Plinia cauliflora, P. aureana, P. trunciflora, Acca sellowiana, Campomanesia xanthocarpa, and Allosyncarpia ternata. The phylogenomic tree was obtained using the maximum likelihood algorithm, the GTR+G evolution model, and 1000 bootstrap replications for branch support, as implemented in the software RAxML, CIPRES Science Gateway V. 3.1 platform. Allosyncarpia ternata (Myrtaceae, Eucalypteae) was employed as an outgroup. All other species belong to the family Myrtaceae, tribe Myrteae.

Germplasm conservation and genetic improvement also need molecular genetic studies

Information about the genetic diversity of natural populations is also needed when aiming at the establishment of germplasm banks and genetic improvement of the species (Melo et al., 2015). Cruz et al.(2016) evaluated the genetic diversity of Plinia spp. in Northeastern Brazil. Thirty-five genotypes were characterized using ISSR (Inter Simple Sequence Repeats) markers. With a polymorphism of 99.65%, five groups were identified based on the genetic divergence among genotypes. Moreover, no correlation between geographical and genetic distances among genotypes was observed. This study revealed the existence of moderate genetic variability of the studied genotypes, an important insight regarding plant collection for breeding programs in the region.

The organization and distribution of population genetic variability of six populations of P. peruviana based on microsatellite markers were reported by Salla (2019). Ten microsatellite loci revealed significant genetic diversity for the six populations, with a high number of alleles and heterozygosis. The analyses of the molecular diversity partition revealed 17.6% of differentiation among populations, 2.6% within populations, and 72.2% within individuals. These results suggest that for conservation proposes, seed collections should maximize the number of seeds per matrix plant, lessening the number of individuals per population (Salla, 2019).

This scarcity of genetic studies and the small geographical amplitude of the two existing studies with Plinia spp. natural populations hinders planning reliable programs of in situ or ex situ species conservation, seed collection, genotype selection, and genetic improvement. So, efforts towards characterizing the genetic diversity and structure of Plinia spp.natural populations using molecular markers and in a wider geographical perspective is needed.

Moderate to low rooting rates is the main limitation for traditional vegetative propagation of Plinia species

A review on the propagation of Plinia spp. by Silva et al. (2018) highlighted that the main form of seedling production is still carried out mainly by seeds, due to the greater ease and speed in the production of new plants. However, despite good germination rates, seed recalcitrance (Danner et al., 2011; Hössel et al., 2013) hampers the establishment of orchards through sexual propagation and studies about the conditions of seed germination of Plinia species (Andrade and Martins, 2003; Wagner et al., 2006; Alexandre et al., 2006; Rossa et al., 2010; Sartor et al., 2010; Dias et al., 2011; Wagner et al., 2011) are puzzling and inconclusive.

The development of methods for the asexual propagation of Plinia spp. is of great importance for obtaining seedlings. In addition to reducing the juvenile phase, vegetative propagation has some advantages such as maintenance of the genetic characteristics of the mother plant, greater productivity, and fruits of better quality (Danner et al., 2006; Hartmann et al., 2011). However, there is no established fully efficient methods of vegetative propagation of Plinia spp. that ensure the formation of commercial orchards in a short period.

In general, Plinia species are recalcitrant for the formation of adventitious roots, and layering seems to be a relatively effective method for vegetative propagation of the species. This method, mediated by indole-butyric acid (IBA) treatment provides the gathering of numerous rooting co-factors (Danner et al., 2006; Sasso et al., 2010; Cassol et al., 2015). However, for the establishment of a conclusive protocol, new studies must be carried out, considering the percentage of harvesting of the transplanted seedlings, the minimum period for the disconnection of the mother plant layering, the quality of the roots formed, the time between the planting of seedlings in the field, and the beginning of fruit production.

The few studies using cutting as a propagation method in Plinia species (Pereira et al., 2005; Fachinello et al., 2005; Sartor et al., 2010; Silva et al., 2019) revealed rooting rates lower than 50%. For commercial seedling production, the percentage of cuttings rooting obtained should be higher than 70% (Hartmann et al., 2011). The values reported for Plinia spp. are quite variable and usually lower than this threshold. The low rooting of the vegetative propagules seems to be correlated with the age of the tissue, the type and time of collection of the cuttings, the presence or absence of growth regulators, and cuttings cultivation conditions. Therefore, several adjustments are needed to increase the rooting percentage in Plinia species propagated through the cutting technique.

Grafting has supported somewhat more promissory results as a vegetative propagation strategy for Plinia species. Setting values reaching up to 90% were reported (Manica, 2000; Sasso et al., 2010; Franco et al., 2010; Malagi et al., 2012; Cassol et al., 2017), but these results revealed to be dependent on the cultivars used and the season. Despite the optimistic results obtained, long-term field monitoring of plants produced from grafting is necessary so that compatibility is verified. Besides, it is still necessary to verify the evolution of growth in the field, and the time elapsed from grafting to the beginning of the fruiting of the grafted seedling.

Protocols of in vitro propagation are promising strategies for Pliniaspp.

In vitro micropropagation is the most practical application of tissue culture and the one with the greatest impact toward allowing conditions to obtain plants that are difficult to propagate and have long life cycles. This approach allows obtaining plants in an aseptic and controlled environment, faster than compared to conventional breeding. In vitro germination (Figure 3) can be the first step to obtain aseptic plants, which can be used as a source of propagules for micropropagation. In vitro germination of Plinia species also enables easy follow of the occurrence of polyembryony, since the number of embryos can reach up to five per seed (Figure 3C).

Figure 3. In vitro germination of Plinia spp. (A) In vitro axenic germination of seeds. (B) Germination of a single plantlet from the seed. (C) Polyembryony with four plantlets germinated from a single seed.

The in vitro germination of P. jaboticaba has been performed in MS (Murashige and Skoog, 1962) culture medium (Picolotto et al., 2007; Santos et al., 2019) and agar:water medium (5-6%, w/v). However, fungal and bacterial contaminations are the most worrisome issues. Treatments of the seeds with sodium hypochlorite (Picolotto et al., 2007), and soaking for 24 hours in sterile water and antibiotics (Santos et al., 2019) have been the commonly used methods for seeds disinfection. Besides, the germination is also influenced by the temperature of culture, but not by the photoperiod (Picolotto et al., 2007), with the best germination rates at 25 °C.

Callogenesis was obtained in P. cauliflora leaf explants using MS medium with different combinations of plant growth regulators: 2,4-dichlorophenoxyacetic acid (2,4-D) at 0.0, 1.0, 2.0, 4.0 mg l-1 + 6-benzylaminopurine (BAP) at 0.0, 0.1, 0.2 mg l-1 and naphthaleneacetic acid (NAA) at 0.0, 1.0, 2.0, 4.0 mg l-1 + BAP (0.0, 1.0, 2.0 mg l-1. All treatments presented callus formation, also in absence of plant growth regulators, not differing statistically (Cardoso, 2016).

Somatic embryos at the cotyledonary stage were obtained from seed explants of P. peruviana by Oliveira (2018). Pro-embryogenic masses were induced in 82.5% of explants using the two cotyledons detached and cultivated in the MS medium with 300 μM of 2,4-D and 1 g l-1 of activated charcoal. During phase I of maturation, the most suitable medium for the conversion of somatic embryos at the torpedo stage was MS with 30 g l-1 of polyethyleneglycol 4000 (77.5% of the formation of embryos in the torpedo stage). There was no conversion of somatic embryos into seedlings and the formation of embryos was possible up to the cotyledonary stage (3.05%), forming abnormal embryos. Anatomical studies showed the development of asynchronous somatic embryos.

Silveira et al. (2020) established a somatic embryogenesis protocol for P. peruviana using mature seeds (two separate cotyledons) as explant, inoculated in MS medium with the addition of 1000 mg l-1 of glutamine, and 10 μM of 2,4-D. Larger embryos and in more advanced stages of development were obtained in a medium containing 60 g l-1 of polyethyleneglycol 6000. There was no conversion of somatic embryos into seedlings and anatomical sections of the embryos revealed deleterious effects of the prolonged period of exposure to 2,4-D.

Although failing to convert somatic embryos into seedlings, the studies of Oliveira (2018) and Silveira et al. (2020) were pioneers in the development of a somatic embryogenesis protocol for Plinia spp. Thus, further studies are needed to determine the optimum exposure period to 2,4-D for the formation of somatic embryos with normal morphology, which drives conversion to seedlings.

How may biotechnology help to boost jaboticaba into the market?

The fruits of Plinia species have a high market value, good organoleptic characteristics, high nutritive content, and beneficial properties to health. Thus, there is a forecast of growth in demand for fresh consumption and use by industries. As the cultivation of Plinia spp. is practically restricted to domestic orchards and the establishment of commercial plantations demands a large amount of vigorous and uniform selected seedlings, it is necessary to develop protocols of vegetative propagation. Micropropagation seems to be the most promising technique providing seedlings on a large scale with high phytosanitary quality, regardless of the time of year.

Plastome based phylogenomic studies may be an important strategy towards understanding the taxonomic relationships among Plinia species, as well as to verify the validity of all proposed species. Also, genetic studies using molecular markers should be performed to characterize the genetic diversity of natural populations towards germplasm conservation and genetic improvement of the species. This biotechnological tool can also be used to evaluate the somaclonal variation of micropropagated seedlings since in clonal propagation the main purpose is the maintenance of the genetic characteristics of selected plants. Besides, to circumvent situations in which the multiplication from natural seeds is problematic, the encapsulation of vegetative structures into sodium alginate droplets and protocols for cryopreservation of embryos and cell cultures are also needed for the species.

CONCLUSIONS

Aiming at seeking the market valuation of the fruits of Plinia spp., studies involving molecular approaches are necessary to resolve the taxonomic uncertainties between species. In addition, the establishment of micropropagation protocols for jaboticabeira is needed to overcome the difficulties related to the vegetative propagation of these species.

ACKNOWLEDGMENTS

The authors would like to thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/Brazil) for the financial support and grant awarded to V.M.S. (Process 302501/2017-7) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES/Brazil) for the scholarship to D.D.S. (Finance code 001). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflict of interest

The authors declare that there is no conflict of interest regarding the publication of this article.

Author contributions

Conceptualization, Investigation, and Writing - original draft DDS, LOO, DCB; Resources DDS; Writing-review and editing VMS; Methodology and Formal analysis DDS, LOM; Supervision VMS.

REFERENCES

Alexandre RS, Wagner A, Negreiros JRS, Bruckner CH (2006) Estádio de maturação dos frutos e substratos na germinação de sementes e desenvolvimento inicial de plântulas de jabuticabeira. R Bras Agrociência 12(2): 227-230

Andrade RA, Martins ABG (2003) Influência da temperatura na germinação de sementes de jabuticabeira. Rev Bras Frutic 25: 197-198; doi:10.1590/S0100-29452003000100056

Bayly MJ, Rigault P, Spokevicius A, Ladiges PY, Ades PK, Anderson C, Bossinger G, Merchant A, Udovicic F, Woodrow IE, Tibbits J (2013) Chloroplast genome analysis of Australian eucalypts--Eucalyptus, Corymbia, Angophora, Allosyncarpia and Stockwellia (Myrtaceae). Mol Phylogenet Evol 69(3): 704-716; doi:10.1016/j.ympev.2013.07.006

Berg OC (1857) Myrtaceae. In: Martius CPF, Eichler A and Urban I (Eds). Flora Brasiliensis 14, pp. 1-528. R Oldenbourg Verlag, Múnich

Cardoso BP (2016) Reguladores de crescimento na emergência e indução de calos de Plinia cauliflora (Mart.) Kausel. MSc Thesis, Universidade Federal de Goiás, Goiânia, Brazil

Cassol DA, Wagner JA, Pirola K, Dotto M, Citadin I (2015) Embalagem, época e ácido indolbutírico na propagação de jabuticabeira por alporquia. Rev Bras Frutic 37(1): 267-272; doi:10.1590/0100-2945-011/14

Cassol DA, Pirola K, Dotto M, Citadin I, Mazaro SM, Wagner JA (2017) Grafting technique and rootstock species for the propagation of Plinia cauliflora. Ciência Rural 47(2): e20140452; doi:10.1590/0103-8478cr20140452

Cruz ES, Dantas ACVL, Carmo CD, Bastos LP (2016) Molecular characterization of jaboticaba tree genotypes located in the municipalities of Recôncavo of Bahia. Rev Bras Frutic 38(3): e-510; doi:10.1590/0100-29452016510

Danner MA, Citadin I, Fernandes Júnior AA, Assmann AP, Mazaro SM, Donazzolo J, Sasso SAZ (2006) Enraizamento de jabuticabeira (Plinia trunciflora) por mergulhia aérea. Rev Bras Frutic 28(3): 530-532; doi:10.1590/S0100-29452006000300043

Danner MA, Citadin I, Sasso SAZ, Ambrosio R, Wagner JA (2011) Armazenamento a vácuo prolonga a viabilidade de sementes de jabuticabeira. Rev Bras Frutic 33(1): 246-252; doi:10.1590/S0100-29452011005000037

Dias MA, Lopes JC, Souza Neto JD, Heberle H (2011) Influência da temperatura e substrato na germinação de sementes de jabuticabeira (Myrciaria cauliflora Berg.). Idesia 29(1): 23-27; doi:10.4067/S0718-34292011000100004

Eguiluz M, Yuyama PM, Guzman F, Rodrigues NF, Margis R (2017) Complete sequence and comparative analysis of the chloroplast genome of Plinia trunciflora. Genetics and Molecular Biology 40(4): 871-876; doi:10.1590/1678-4685-gmb-2017-0096

Fachinello JC, Hoffmann A, Nachtigal JC (2005) Propagação de plantas frutíferas. Embrapa Informação Tecnológica, Brasília; ISBN: 8573833009

Franco LRL, Silva JF, Maia VM, Lopes PS, Amorim IJF, Mizobutsi EH (2010) Pegamento e crescimento inicial de mudas de jabuticabeiras ‘açu’ e ‘sabará’ submetidas a dois tipos de enxertia. Rev Ceres 57(4): 535-538; doi:10.1590/S0034-737X2010000400016

Govaerts R, Sobral N, Ashton P, Barrie F, Holst BK, Landrum LL, Matsumoto K, Fernanda Mazine F, Nic Lughadha E, Proença C (2008) World Checklist of Myrtaceae. Royal Botanic Gardens, Kew; ISBN: 1842463918

Hartmann HT, Kester DE, Davies Júnior FT, Geneve RL (2011) Propagation: principles and practices. Prentice Hall, New Jersey; ISBN: 0135014492

Hössel C, Oliveira JSMA, Fabiane KC, Wagner JA, Citadin I (2013) Conservação e teste de tetrazólio em sementes de jabuticabeira. Rev Bras Frutic 35(1): 255-261; doi:10.1590/S0100-29452013000100029

Kausel VE (1956) Beitrag zur Systematik der Myrtaceen. In: Kausel VE (Ed). Arkiv för Botanik, pp. 491-516. Almqvist and Wikssels Boktryckeri Ab, Estocolmo

Lorenzi H (2000) Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. Instituto Plantarum, Nova Odessa; ISBN: 8586714119

Lorenzi H (2011) Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. Instituto Plantarum, Nova Odessa; ISBN: 85-86714337

Lorenzi H, Bacher L, Lacerda M, Sartori S (2006) Frutas brasileiras e exóticas cultivadas: de consumo in natura. Instituto Plantarum, Nova Odessa; ISBN: 9788586714238

Machado LO, Vieira LN, Stefenon VM, Pedrosa FO, Souza EM, Guerra MP, Nodari RO (2017) Phylogenomic relationship of feijoa (Acca (O. Berg) Burret) with other Myrtaceae based on complete chloroplast genome sequences. Genetica 145(2): 163-174; doi:10.1007/s10709-017-9954-1

Machado LO, Vieira LN, Stefenon VM, Faoro H, Pedrosa FO, Guerra MP, Nodari RO (2020) Molecular relationships of Campomanesia xanthocarpa within Myrtaceae based on the complete plastome sequence and on the plastid ycf2 gene. Genetics and Molecular Biology 43(2): e20180377; doi:10.1590/1678-4685-GMB-2018-0377

Malagi G, Citadin I, Scariotto S, Wagner JA, Sachet MR (2012) Enxertia interespecífica de jabuticabeira: influência do tipo de garfo. Ciênc Rural 42(2): 221-224; doi:10.1590/S0103-84782012005000006

Manica I (2000) Frutas nativas, silvestres e exóticas 1: técnicas de produção e mercado: abiu, amora-preta, araçá, bacuri, biriba, carambola, cereja-do-rio-grande, jabuticaba. Cinco Continentes, Porto Alegre; ISBN: 8586466123

Mattos JR (1998) Novidades Taxonômicas em Myrtaceae. Loefgrenia: Comunicações Avulsas de Botânica 112: 5

Melo ATO, Coelho ASG, Pereira MF, Blanco AJV, Franceschinelli EV (2015) Genética da conservação de Cabralea canjerana (vell.) Mart. (Meliaceae) em fragmentos florestais de mata atlântica na APA Fernão Dias. Rev Árvore 39(2): 365-374; doi:10.1590/0100-67622015000200016

Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15: 473-497

Oliveira FLR (2018) Embriogênese somática em jabuticabeira (Plinia cauliflora (Mart.) Kausel). MSc Thesis, Universidade Federal do Paraná, Curitiba, Brazil

Oliveira GP, Angelotti-Mendonça J, Tanaka FAO, Silva SR, Scarpare Filho JA (2019) Origin and development of reproductive buds in jabuticaba cv. Sabará (Plinia jaboticaba Vell). Scientia Horticulturae 249: 432-438; doi:10.1016/j.scienta.2019.02.020

Pereira M, Oliveira AL, Pereira REA, Sena JAD, Costa JRV, Almeida M, Gonçalves AN (2005) Morphologic and molecular characterization of Myrciaria spp species. Rev Bras Frutic 27(3): 507-510; doi:10.1590/S0100-29452005000300040

Picolotto L, Schuch MW, Souza JA, Silva LC, Ferri J, Fachinello JC (2007) Efeito do hipoclorito de sódio, fotoperíodo e temperatura no estabelecimento in vitro de jabuticabeira. Sci Agrar 8(1): 19-23; doi:10.5380/rsa.v8i1.8337

Pitz HS, Pereira A, Voytena APL, Trevisan ACD, Affonso RCL, Ribeiro-do-Valle RM, Maraschin M (2017) Cytoprotective Effects of Jaboticaba (Plinia peruviana, Poir. Govaerts) Fruit Peel Extracts against H2O2-Induced Oxidative Stress. Reactive Oxygen Species 4(11): 362‒371; doi:10.20455/ros.2017.859

Rossa ÜB, Triches GP, Grossi, Nogueira AC, Reissmann CB, Ramos MR (2010) Germinação de sementes e qualidade de mudas de Plinia trunciflora (jabuticabeira) em função de diferentes tratamentos pré germinativos. Floresta 40(2): 371-378; doi:10.5380/rf.v40i2.17832

Rufino MSM, Alves RE, Fernandes FAN, Brito ES (2011) Free radical scavenging behavior of ten exotic tropical fruits extracts. Food Res Int 44(7): 2072–2075; doi:10.1016/j.foodres.2010.07.002

Salla VP (2019) Diversidade e estrutura genética populacional em jaboticabais nativos no sudoeste do Paraná. PhD thesis, Universidade Tecnológica Federal do Paraná, Pato Branco, Brazil

Santos SK, Luna NP, Costa JO, Dias M, Gomes D, Fonseca K (2019) Germination in vitro of Jabuticabeira Myrciaria jaboticaba (Vell.) Berg. J Exp Agric Int 35(6): 1-8; doi:10.9734/jeai/2019/v35i630221

Sartor FR, Müller NTG, Moraes AM (2010) Efeito do ácido indolbutírico e de substratos na propagação de estacas e sementes de jabuticabeira. Tecnol and Ciên Agropec 4(3): 11-15

Sasso SAZ, Citadin I, Danner MA (2010) Propagação de jabuticabeira por enxertia e alporquia. Rev Bras Frutic 32(2): 571-576; doi:10.1590/S0100-29452010005000055

Silva CP, Lacerda EG, Sanches LFJ, Queiroz JO, Marchiotti RCB (2019) Enraizamento de estacas de Jabuticabeira tratadas com ácido indolbutírico (AIB) e ácido naftaleno acético (ANA). Rev Agr Acad 2(3): 122-132; doi:10.32406/v2n32019/122-132/agrariacad

Silva JAA, Teixeira GHA, Martins ABG, Citadin I, Wagner JA, Danner MA (2018) Advances in the propagation of Jabuticaba tree. Rev Bras Frutic 41(3): e-024; doi:10.1590/0100-29452019024

Silveira SS, Santos BFS, Degenhardt-Goldbach J, Quoirin M (2020) Somatic embryogenesis from mature split seeds of jaboticaba (Plinia peruviana (Poir) Govaerts). Acta sci 42(1): e43798; doi:10.4025/actasciagron.v42i1.43798

Sobral M (1985) Alterações nomenclaturais em Plinia (Myrtaceae). Boletim do Museu Botânico de Curitiba 63: 1-4

Teixeira LN, Stringheta PC, Oliveira FA (2008) Comparação de métodos para quantificação de antocianinas. Ceres 55(4): 297-304

Vilela RCF, Assis JGA, Filho LN, Viana BF (2012) Sistema reprodutivo e diversidade genética de quatro espécies de Myrciaria (Myrtaceae, jabuticabeiras). Acta Bot Bras 26(4): 727-734; doi:10.1590/S0102-33062012000400002

Wagner JA, Silva JOC, Pimentel LD, Negreiros JRS, Alexandre RS, Morgado MAD, Álvares VS, Bruckner CH (2006) Germinação e emergência de três espécies de jabuticabeira em quatro substratos. Revista Ceres 53(307): 322-327

Wagner JA, Silva JOC, Pimentel LD, Santos CEM, Bruckner CH (2011) Germinação e desenvolvimento inicial de duas espécies de jabuticabeira em função do tamanho de sementes. Acta Sci 33(1): 105-109; doi:10.4025/actasciagron.v33i1.4881

Recibido: 28-12-2020

Aceptado: 02-02-2021

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