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Indirect Shoot Regeneration Using 2,4-D Induces Somaclonal Variations in Cinchona Officinalis Rosa Armijos-González1 Luisa Espinosa-Delgado1 Augusta Cueva-Agila1,2

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Indirect Shoot Regeneration Using 2,4-D Induces Somaclonal Variations in Cinchona Officinalis Rosa Armijos-González1 Luisa Espinosa-Delgado1 Augusta Cueva-Agila1,2 Floresta e Ambiente 2021; 28(3): e20210017 https://doi.org/10.1590/2179-8087-FLORAM-2021-0017 ISSN 2179-8087 (online) ORIGINAL ARTICLE – Conservation of Nature Indirect Shoot Regeneration Using 2,4-D Induces Somaclonal Variations in Cinchona officinalis Rosa Armijos-González1 Luisa Espinosa-Delgado1 Augusta Cueva-Agila1,2 1Universidad Técnica Particular de Loja, Departamento de Ciencias Biológicas y Agropecuarias, Loja, Ecuador. 2Pontificia Universidad Católica del Ecuador Sede Ibarra, Escuela de Ciencias Agrícolas y Ambientales, Ibarra, Ecuador. Abstract Cinchona officinalis is an important species from the Andean cloud forest that has a low regeneration rate in natural populations. In vitro regeneration of C. officinalis has been successfully established but somaclonal variation was not evaluated. The regeneration pathway and the number of subcultures on somaclonal variation were evaluated using six ISSR primers that amplified 58 loci of Inter Simple Sequence Repeats (ISSR). A dendrogram based on Jaccard´s genetic distance between the subcultures and the donor plant was produced. The results show that indirect shoot regeneration induces somaclonal variation, in the presence 2,4-Dichlorophenoxyacetic acid (2,4-D) in combination with kinetin and 6-Benzylaminopurine (BAP). In combination with 1-Naphthaleneacetic acid (NAA) or with Indole-3-butyric acid (IBA), BAP produces genetically stable explants. The highest proliferation rate was achieved using BAP and IBA. The present research study suggests avoiding the use of 2,4-D when C. officinalis is propagated for reintroduction and restoration projects. Keywords: In vitro regeneration, subcultures, auxin, ISSR. 1. INTRODUCTION AND OBJECTIVES genetic diversity of six populations of C. officinalis was analyzed. The majority of the populations studied were composed of Cascarilla, Cinchona officinalis Linneo. (Rubiaceae) is a adult plants located in areas of difficult access in fragmented tree species from the Andean cloud forest of southern Ecuador forest and pasture areas. They suggested that the moderate and northern Peru (Brako & Zarucchi, 1993; Andersson et al., levels of genetic diversity of these populations have to be 1998). During the period between the 16th and 19th centuries, conserved, and that it is necessary to develop strategies to this species had enormous importance for the cure of malaria protect and conserve the remnant populations. (Jaramillo-Arango, 1947; Cuvi, 2009). The use of tree bark Ex situ management and conservation techniques are caused a huge decrease in natural populations (Arias, 2017). important tools to allow for the recovery and conservation of Besides this, habitat fragmentation due to urban development, threatened species. In vitro culture is a useful tool for those species agriculture, and livestock establishment resulted in small and that present difficult regeneration under natural conditions, being dispersed populations of the species (Madsen, 2002; Arias, successfully applied to many rare or threatened species (Slazak 2017; Cueva et al., 2019). et al., 2015; Upadhyay et al., 2015). The species of the Cinchona Cinchona officinalis presents a high germination rate, genus have not been the exception. This technique was used in ranging from 50 to 87% in assays performed with in vitro and the 1980s and 1990s in order to increase alkaloid productivity ex vitro controlled conditions (Caraguay–Yaguana et al., 2016; through in vitro cultivation of various tissues (Koblitz et al., 1983a; Armijos-González & Pérez-Ruiz, 2016; Romero-Saritama & Koblitz et al., 1983b; Hay et al. 1986, 1987; Hoekstra et al., 1990). Munt, 2017). Despite this fact, the species requires specific The most successful of these techniques is the culture of cells in conditions to continue its development in nature, resulting in a suspension before callus formation. Some of the cited works low regeneration rate in the remnant populations (Acosta, 1947; had been the base for the establishment of protocols of in vitro Garmendia, 2005). In a recent study (Cueva et al., 2019), the massive propagation that aim to reintroduce and reinforce the Creative Commons License. All the contents of this journal, except where otherwise noted, is licensed under a Creative Commons Attribution License. 2 - 8 Armijos-González R, Espinosa-Delgado L, Cueva-Agila A populations of C. officinalis in the natural habitat (Armijos- containing different combinations of cytokinins (BAP, KIN) González & Pérez-Ruiz, 2016). and auxins (NAA, IBA, 2,4-D) that resulted in direct shoot or In vitro culture generates specimens that can be genetically callus formation depending on the type and concentration of identical to the mother plant; however, in the process, there the hormone used (Armijos-González & Pérez-Ruiz, 2016). is a risk of inducing the appearance of variation between the A Gamborg B5 medium was used as control. parental cell line and its regenerants (Larkin & Scowcroft, 1981; Sarmast, 2016). The occurrence of these variations is known as 2.3. Effect of subculture on shoot multiplication somaclonal variation. This is spontaneous and uncontrolled, limiting the usefulness of the mass propagation system because The effect of subculture cycles on shoot formation was of its unpredictable nature (Singh et al., 2011). Somaclonal evaluated. New nodal segments derived from the plants of the variation or genetic fidelity can be analyzed at different levels: first culture in the PGR-containing medium were subcultured morphological, cytological, cytochemical, biochemical, and every three months for 12 months (a total of 4 stages). molecular (Chandrika et al., 2008; Ruffoni & Savona, 2013). Beginning with the second subculture, a B5 medium without At the molecular level, the most efficient are molecular markers PGR was used. Both explants and subcultures were exposed based on DNA (Tiwari et al., 2013). Among the molecular to a photoperiod of 12 hours of light and 12 hours with a markers, one of the most used is the Inter Simple Sequence photon flux density of 57 lmol m-2s-1 provided by cool white Repeat (ISSR) analysis which allows detecting the variation fluorescent lamps, at an average temperature of 23 ± 2°C and that occurs in microsatellite regions scattered in the genome an ambient humidity of 65 ± 7%. The multiplication index (Sharma et al., 2014; Akdemir et al., 2016; Martinez- Estrada was calculated as the number of newly formed shoots per et al., 2017; Babu et al., 2018; Rohela et al., 2020). each initial shoot and recorded in each subculture stage. Even though there are many studies on in vitro culture in the Cinchona genus, as far as know this is the first work 2.4. Analysis of somaclonal variations to evaluate somaclonal variation in a Cinchona species. In this study, we determine the influence of two factors on Fifty milligrams were taken from each sample, as leaf the somaclonal variation of C. officinalis: the regeneration fragments, and in those where the tissue was not differentiated, or propagation pathway using different Plant Growth callus fragments were taken. The samples were preserved at -80 °C Regulator (PGR) combinations and the number of subcultures. until DNA extraction. DNA extraction was carried out with a DNeasy Plant Mini kit (Qiagen) following the manufacturer’s 2. MATERIALS AND METHODS instructions. The amount and purity of the DNA were quantified in a NanoDrop 2000 spectrophotometer (Thermo Fisher Scientific, 2.1. Plant material USA). DNA integrity was verified by gel electrophoresis in 1% w/v agarose gel staining with Gel Red and visualized in an The laboratory work was developed in the Plant Physiology Enduro TM Gel Documentation System Touch. Laboratory of the Department of Biological Sciences (3°59’14.2 “S 79°11’52.5 “W) of the Universidad Técnica Particular de 2.5. ISSR-PCR analysis Loja, Loja, Ecuador. Mature seeds of C. officinalis were procured from the To examine the polymorphism of the genomic DNA in Aguarango sector in Vilcabamba (Loja-Ecuador). After C. officinalis, 13 ISSR primers (University of British Columbia collection, the seeds were surface-sterilized as described in Biotechnology Laboratory, Vancouver, Canada) were evaluated. Armijos-González & Pérez-Ruiz (2016) and germinated on a Based on the reproducibility of band pattern and resolution, half strength Gamborg B5 medium. Seeds were incubated at a total of 6 primers were selected (Table 1). 22.0 °C with 12 h light/12 h dark with a photon flux density PCR reactions were performed in a final volume of of 57 lmol m-2s-1 provided by cool white fluorescent lamps. 20 µL, containing 20 ng of DNA template, 4 µL of 5X buffer Seedlings 4 months old and 6-8 cm in height were used to begin containing MgCl2, 0.5 µM of primer, 0.2 mM of dNTPs and cultivation. Each seedling was considered as a donor plant. 1 U of Taq DNA polymerase (Promega). The PCR product was amplified under the following conditions: one cycle of 2.2. In vitro culture establishment 4 min at 94 °C, followed by 40 cycles with 30s at 94 °C, 45s at diverse annealing temperatures depending on each specific Nodal segments, with 2 or 3 buds each and 1.0 - 1.5 cm in marker (Table 1) and 2 min at 72 °C, and a final extension size, were cultivated on a half strength Gamborg B5 medium of 10 min at 72 °C. 2 Floresta e Ambiente 2021; 28(3): e20210017 Indirect Shoot Regeneration... 3 - 8 The PCR was carried out in the Applied Biosystems shoot formation (Figure 2c). In C. robusta with the use of Thermocycler. The visualization of products was carried out Kin and 2,4-D (Giroud et al., 1989) and in C. ledgeriana in an agarose gel at 2%. The gels were dyed with Gel Red, run with the use of BAP and 2,4-D (Hoekstra et al., 1990), the at 80 volts/cm and visualized under UV light in an Enduro formation of the same globular structures was reported. TM Gel Documentation System Touch. Amplified PCR The combination of NAA and BAP produced direct shoot products that were not clear were repeated and only clear formation.
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