Abstract
The husk tomato (Physalis spp.) is an exceptional commercial crop for its nutritional and medicinal properties where the whole plant is used. This has led to the search for new micropropagation methods to accelerate plant production in the field. P. angulata and P. chenopodifolia were micropropagated via shoot proliferation of axillary buds and indirect organogenesis. Shoot multiplication was performed on Murashige and Skoog (MS) basal medium supplemented with 2.22, 4.43, or 6.65 μM 6-Benzylaminopurine (BAP) combined with 2.32, 4.64, or 6.96 μM Kinetin (Kin). For P. chenopodifolia, the largest number of new shoots was obtained by adding 4.64 μM Kin (10.47 ± 2.25 shoots per explant); for P. angulata, the best treatment was obtained with a combination of 4.43 μM BAP and 2.32 μM Kin (8.47 ± 2.91 shoots per explant). Indirect organogenesis was performed by placing leaf sections of both Physalis species on MS medium supplemented with 2.22, 4.43, 6.65, or 8.87 BAP combined with 1.13, 2.26, or 3.39 μM 2,4-dichlorophenoxyacetic acid (2,4-D). P. chenopodifolia showed the highest number of new indirect shoots (37.14 ± 3.54) with the addition of 1.13 μM 2,4-D and 6.65 μM BAP; P. angulata had the highest result (22.71 ± 2.5 shoots per explant) with 1.13 μM 2,4-D and 4.43 μM BAP. Stimulation of root induction was obtained in different mediums with auxins 1.07, 2.68, 5.37, or 8.05 μM 1-Naphthaleneacetic acid (NAA) and 1.41, 2.85, 5.70, or 8.55 μM Indoleacetic acid (IAA). The regenerated plantlets resulting from the rooting process were acclimatized and transferred to the greenhouse. The average of shoots per explant in the indirect organogenesis method was higher than the axillary bud culture method. These results could provide an efficient alternative for the micropropagation and conservation of these species with high commercial potential.
Similar content being viewed by others
References
Afroz F, Hassan AS, Bari LS, Sultana R, Begum N, Jahan MAA, Khatun R (2010) In vitro shoot proliferation and plant regeneration of Physalis minima L. - a perennial medicinal herb. Bangladesh J Sci Ind Res 44:453–456. https://doi.org/10.3329/bjsir.v44i4.4597
Bertoni BW, Souza AV, Biondo R, FrançaI SC, Telles MPC, Pereira MS (2010) Genetic diversity among natural populations of Mandevilla velutina. Hortic Bras 28:209–213. https://doi.org/10.1590/S0102-05362010000200012
Blakesley D, Weston GD, Elliott MC (1991) Endogenous levels of indole-3-acetic acid and abscisic acid during the rooting of Cotinus coggygria cuttings taken at different times of the year. Plant Growth Regul 10:1–12. https://doi.org/10.1007/bf00035126
Borchetia S, Das SC, Handique PJ, Sudripta D (2009) High multiplication frequency and genetic stability for commercialization of the three varieties of micropropagated tea plants (Camellia spp.). Sci Hortic 120:544–550. https://doi.org/10.1016/j.scienta.2008.12.007
Brassard N, Brissette L, Lord D, Laliberte S (1996) Elongation, rooting and acclimatization of micropropagated shoots from mature material of hybrid larch. Plant Cell Tiss Org Cult 44:37–44. https://doi.org/10.1007/BF00045911
Cheng ZJ, Wang L, Sun W, Zhang Y, Zhou C, Su YH, Li W, Sun TT, Zhao XY, Li XG, Cheng Y, Zhao Y, Xie Q, Zhang XS (2013) Pattern of auxin and cytokinin responses for shoot meristem induction results from the regulation of cytokinin biosynthesis by auxin response factor3. Plant Physiol 161:240–251. https://doi.org/10.1104/pp.112.203166
da Silva L, Villa F, Fernandes D, Costa E, Ritter G, Eberling T (2021) Micropropagation of Physalis species with economic potential. Rev Ceres 68:521–529. https://doi.org/10.1590/0034-737x202168060003
da Silva RRP, da Silva BJ, Rodrigues APD, Farias LHS, da Silva MN, Alves DTV, Bastos GNT, do Nascimento JLM, Silva EO (2015) In vitro biological action of aqueous extract from roots of Physalisangulata against Leishmania (Leishmania) amazonensis. BMC Complement Altern Med 15:249. https://doi.org/10.1186/s12906-015-0717-1
D'Arcy W (1991) The Solanaceae since 1976, with a review of its biogeography. In: Hawkes JG, Lester RL, Nee M, Estrada N (eds) Solanaceae III: Taxonomy, chemistry, evolution, Royal Botanic Gardens, Richmond, Kew, pp 75–137
de Klerk GJ, Ter Brugge J, Marinova S (1997) Effectiveness of indoleacetic acid, indolebutyric acid and naphthaleneacetic acid during adventitious root formation in vitro in Malus ‘Jork 9.’ Plant Cell Tiss Org Cult 49:39–44. https://doi.org/10.1023/a:1005850222973
de Oliveira JAR, Golle DP, Schoffel A, Camera JN, Koefender J (2019) Physalis angulata L. propagation in vitro. Rev Ceres 66:486–492. https://doi.org/10.1590/0034-737X201966060010
de Oliveira LM, Silva CS, Pereira DMS, Lucchese AM, Santana JRF (2013) In vitro establishment and initial growth of Physalisangulata (Solanaceae). Sitientibus Ser Cien Biol 13:1–5. https://doi.org/10.13102/scb323
Delgado-Aceves L, González-Arnao MT, Santacruz-Ruvalcaba F, Folgado R, Portillo L (2021) Indirect somatic embryogenesis and cryopreservation of Agave tequilana Weber Cultivar ‘Chato.’ Plants 10:249. https://doi.org/10.3390/plants10020249
Duclercq J, Sangwan-Norreel B, Catterou M, Sangwan RS (2011) De novo shoot organogenesis: From art to science. Trends Plant Sci 16:597–606. https://doi.org/10.1016/j.tplants.2011.08.004
Escobar-Guzmán RE, Hernández-Godínez F, Martínez O, Ochoa-Alejo N (2009) In vitro embryo formation and plant regeneration from anther culture of different cultivars of Mexican husk tomato (Physalis ixocarpa Brot.). Plant Cell Tiss Org Cult 96:181–189. https://doi.org/10.1007/s11240-008-9474-x
García-Pérez P, Lozano-Milo E, Landín M, Gallego PP (2020) Machine learning technology reveals the concealed interactions of phytohormones on medicinal plant in vitro organogenesis. Biomolecules 10:746. https://doi.org/10.3390/biom10050746
Greb T, Lohmann JU (2016) Plant stem cells. Current Biol 26:816–821. https://doi.org/10.1016/j.cub.2016.07.070
Gupta P, Durzan D (1987) Biotechnology of somatic polyembryogenesis and plantlet regeneration in loblolly pine. Bio/Technol 5:147–151. https://doi.org/10.1038/nbt0287-147
Gupta SC, Chandra (1987) Control of organogenesis in cultures of different vegetative explants of Mexican tomato (Physalis ixocarpa Brot.). Indian J Plant Physiol 30:114–118
Handique PJ, Bhattacharjee S (2000) In vitro propagation of wood apple (Feronia elephantum Correa.). Adv Plant Sci 13:241–243
Harish MC, Rajeevkumar S, Sathishkumar R (2010) Efficient in vitro callus induction and regeneration of different tomato cultivars of India. Asian J Biotechnol 2:178–184. https://doi.org/10.3923/ajbkr.2010.178.184
Hernández-Villalobos K, Chico-Ruíz J (2020) Inducción de brotes y raíces en hipocotilos y cotiledones de Physalis peruviana L. utilizando 6-bencilaminopurina y 2,4-diclorofenoxiacético. Rev Investig Altoandin 22:86–94. https://doi.org/10.18271/ria.2020.539
Hnatuszko-Konka K, Gerszberg A, Weremczuk-Jeżyna I, Grzegorczyk-Karolak I (2021) Cytokinin signaling and de novo shoot organogenesis. Genes 12:265. https://doi.org/10.3390/genes12020265
Huetteman CA, Preece JE (1993) Thidiazuron: a potent cytokinin for woody plant tissue culture. Plant Cell Tiss Org Cult 33:105–119. https://doi.org/10.1007/BF01983223
Jafari N, Othman RY, Khalid N (2011) Effect of benzylaminopurine (BA) pulsing on in vitro shoot multiplication of Musa acuminata (banana) cv. Berangan. Afr J Biotechnol 10:2446–2450. https://doi.org/10.5897/AJB
Kazemiani S, Motallebi-Azar A, Panahandeh J, Mokhtarzadeh S, Ozdemir FA (2018) Shoot proliferation from potato (Solanum tuberosum cv. Agria) under different concentration of MS include vitamins and BAP medium. Prog Nutr 20:160–166. https://doi.org/10.23751/pn.v20i1-S.6686
Kumar AO, Ramesh S, Tata SS (2015) Establishment of a rapid plant regeneration system in Physalisangulata L. through axillary meristems. Not Sci Biol 7:471–474. https://doi.org/10.15835/nsb749707
Kumar AO, Ramesh S, Tata SS (2016) In vitro micropropagation of the medicinal plant Physalisangulata L. Not Sci Biol 8:161–163. https://doi.org/10.15835/nsb829817
Kumar OA, Rupavati T, Tata SS (2011) Multiple shoot induction and plant regeneration from nodal explants of chili peppers (Capsicum annuum L.). Asian J Exp Biol Sci 2:517–520
Lardon R, Geelen D (2020) Natural variation in plant pluripotency and regeneration. Plants 9:1261. https://doi.org/10.3390/plants9101261
Lima LGB, Montenegro J, Abreu JP, Santos MCB, Nascimento TP, Santos MS, Ferreira AG, Cameron LC, Ferreira MSL, Teodoro AJ (2020) Metabolite profiling by UPLC-MSE, NMR, and antioxidant properties of Amazonian fruits: Mamey Apple (Mammeaamericana), Camapu (Physalisangulata), and Uxi (Endopleura uchi). Molecules 25:1–18. https://doi.org/10.3390/molecules25020342
Martinez M (1998) Revisión de Physalis Sección Epetiorhiza (Solanaceae). Anales Inst Biol Univ Nac Autón México Bot 69:71–117
Mascarenhas LMS, Santana JRFD, Brito AL (2019) Micropropagation of Physalis peruviana L. Pesquisa Agropecuária Tropical 49:1–8
Mills D, Wenkart S, Benzioni A (1997) Micropropagation of Simmondsia chinensis (Jojoba). In: Bajaj YPS (ed) Biotechnology in agriculture and forestry, Vol 40. High-Tech and Micropropagation VI. Springer, Berlin, Heidelberg, pp 370–393. https://doi.org/10.1007/978-3-662-03354-8_27
Mungole AJ, Doifode VD, Kamble RB, Chaturvedi A, Zanwar P (2011) In vitro callus induction and shoot regeneration in Physalis minima L. Ann Biol Res 2:79–85
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.13993054.1962.tb08052.x
Otroshy M, Mokhtari A, Mohammad S, Khodaee M, Bazrafshan AH (2013) Direct regeneration from leaves and nodes explants of Physalis peruviana L. Intl J Farm Alli Sci 2:214–218
Ozel CA, Khawar KM, Mirici S, Arslan O, Ozcan S (2006) Induction of ex vitro adventitious roots on soft wood cuttings of Centaurea tchihatcheffii tchihatcheffii Fisch et. Mey using Indole 3-butyric acid and α-naphthaleneacetic acid. Int J Agri Biol 8:6669
Phillips GC, Collins GB (1979) In vitro tissue culture of selected legumes and plant regeneration from callus cultures of red clover. Crop Sci 19:59–64. https://doi.org/10.2135/cropsci1979.0011183x0019000100
Phillips GC, Garda M (2019) Plant tissue culture media and practices: an overview. In Vitro Cell Dev Biol - Plant 55:242–257. https://doi.org/10.1007/s11627-019-09983-5
Puente LA, Pinto-Muñoz CA, Castro ES, Cortés M (2011) Physalis peruviana Linnaeus, the multiple properties of a highly functional fruit: A review. Food Res Int 44:1733–1740. https://doi.org/10.1016/j.foodres.2010.09.034
Ramar K, Arulprakash T, Ayyadurai V (2014) In vitro flower induction and multiple shoot regeneration studies in Solanum americanum L. (Solanaceae). Ann Plant Sci 3:582–587
Ramírez-Malagón R, Ochoa-Alejo N (1991) Adventitious shoot formation and plant regeneration from tissues of tomatillo (Physalis ixocarpa Brot.). Plant Cell Tiss Org Cult 25:185–188. https://doi.org/10.1007/BF00036209
Reyes-Reyes EM, Jin Z, Vaisberg AJ, Hammond GB, Bates PJ (2012) Physangulidine A, a withanolide from Physalis angulata, perturbs the cell cycle and induces cell death by apoptosis in prostate cancer cells. J Nat Prod 76:2–7. https://doi.org/10.1021/np300457g
Rezanejad F, Hosseini A (2019) The effect of growth factors on direct micropropagation of Physalis alkekengi L. (Solanaceae) through buds and stems explants to transfer to the greenhouse and flowering phase. Modares J Biotechnol 10:441–446
Rodrígues FA, Penoni E, Soares JR, Pasqual M (2013) Diferentes concentrações de sais do meio MS e BAP na multiplicação in vitro de Physalis peruviana. Bioscience J 29:77–82. https://doi.org/10.1590/0034-737X201663030009
Romo-Paz FJ, Folgado R, Delgado-Aceves L, Zamora-Natera JF, Portillo L (2021) Tissue culture of Physalis angulata L. (Solanaceae): techniques for micropropagation and germplasm long-term preservation. Plant Cell Tiss Org Cult 144:73–78. https://doi.org/10.1007/s11240-020-01970-8
Salcedo-Pérez E, Arvizu ML, Vargas-Radillo JJ, Vargas-Ponce O, Bernabe-Antonio A, Barrientos-Ramírez L (2015) Contenido mineral y tamizaje fitoquímico en Physalischenopodifolia Lam. In: condiciones de desarrollo. Rev Mex cienc forestales 6:58–73
Sandhya H, Rao S (2016) Effect of growth regulators on regeneration through leaf and stem derived callus in Physalis minima Linn. Curr Trends Biotechnol Pharm 10:280–285
Santos GC, Cardoso FP, Martins AD, Pasqual M, Ossani PC, Queiroz JM, Dória J (2020) Effect of light and sucrose on photoautotrophic and photomixotrophic micropropagation of Physalis angulata. Biosci J 36(4):1353–1357. https://doi.org/10.14393/BJ-v36n4a2020-47738
Shin J, Bae S, Seo PJ (2020) De novo shoot organogenesis during plant regeneration. J Exp Bot 71:63–72. https://doi.org/10.1093/jxb/erz395
Silva D, Pio R, Doria J, Nogueira P, Peche P, Villa F (2016) The production of Physalis spp. seedlings grown under different-colored shade nets. Acta Sci Agron 38:2. https://doi.org/10.4025/actasciagron.v38i2.27893
Singh A, Reddy MP, Patolia JS (2008) An improved protocol for micropropagation of elite genotypes of Simmondsia chinensis (Link) Schneider. Biol Plant 52:401–412. https://doi.org/10.1007/s10535-008-0105-5
Soares ELC, Vendruscolo GS, Vignoli-Silva M, Thode VA, Silva JG, Mentz LA (2009) O gênero Physalis L. (Solanaceae) no Rio Grande do Sul, Brasil. Pesquisas Bot 60:323–340
Stehmann JR, Mentz LA, Agra MF, Vignoli-Silva M, Giacomin L, Rodrigues IMC (2015) Solanaceae. In: Lista de Espécies da Flora do Brasil, Jardim Botanico do Rio de Janeiro.. Accessed 8 Jan 2022
Su YH, Zhang XS (2014) The hormonal control of regeneration in plants. Curr Top Dev Biol 108:35–69. https://doi.org/10.1016/B978-0-12-391498-9.00010-3
Sugiyama M (2014) Molecular genetic analysis of organogenesis in vitro with temperature-sensitive mutants. Plant Biotechnol Rep 8:29–35. https://doi.org/10.1007/s11816-013-0292-1
Swartwood K, Van-Eck J (2019) Development of plant regeneration and Agrobacterium tumefaciens-mediated transformation methodology for Physalis pruinosa. Plant Cell Tiss Org Cult 137:465–472. https://doi.org/10.1007/s11240-019-01582-x
Trillos O, Cotes JM, Medina CI, Lobo M, Navas A (2008) Caracterización morfológica de cuarenta y seis accesiones de Uchuva (Physalis peruviana L.), en Antioquia (Colombia). Rev Bras Frutic 30:708–715. https://doi.org/10.1590/s0100-29452008000300025
Valdivia-Mares MLE, Rodríguez FA, Sánchez-González JJ, Vargas-Ponce O (2016) Phenology, agronomic and nutritional potential of three wild husk tomato species (Physalis, Solanaceae) from Mexico. Sci Hort 200:83–94. https://doi.org/10.1016/j.scienta.2016.01.005
Vargas-Ponce O, Pérez-Álvarez LF, Zamora-Tavares P, Rodríguez A (2011) Assessing genetic diversity in Mexican husk tomato species. Plant Mol Biol Rep 29:733–738. https://doi.org/10.1007/s11105-010-0258-1
Vargas-Ponce O, Sánchez MJ, Zamora TMP, Valdivia-Mares LE (2016) Traditional management and small-scale crop of Physalis angulata in Western Mexico. Genet Resour Crop Evol 63:1383–1395. https://doi.org/10.1007/s10722-015-0326
Acknowledgements
We thank Rebeca Mendez-Hernandez for assistance with the English Language.
Funding
This work was financially supported by Consejo Nacional de Ciencia y Tecnología (scholarship 709220).
Author information
Authors and Affiliations
Contributions
FJ-RP wrote the manuscript. FJ-RP, JD-OF, and L-DA carried out in vitro propagation experiments. FJ-RP and JD-OF designed and performed organogenesis experiments. FJ-RP and L-DA took and processed the photos. O-VP: seed collection and manuscript reviewing. LP, JF-ZN, E-SP, and L-DA conceived the review. All authors reviewed and approved the final manuscript.
Corresponding author
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Romo-Paz, F., Orozco-Flores, J.D., Delgado-Aceves, L. et al. Micropropagation of Physalis angulata L. and P. chenopodifolia Lam. (Solanaceae) via indirect organogenesis. In Vitro Cell.Dev.Biol.-Plant 59, 497–506 (2023). https://doi.org/10.1007/s11627-023-10363-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11627-023-10363-3