Abstract
The Turiaçu pineapple cultivar produces fruits of high organoleptic value but has few biotechnological studies on seedling production. However, conventional in vitro propagation can affect the photosynthetic potential of plants when transferred to the field, thus mitigating measures should be undertaken to solve this limitation, for example by decreasing carbohydrate concentration in the growth medium, adopting bioreactors of temporary immersion with forced ventilation, and using gas permeable membranes in the culture flask. The present work focused on evaluating the growth and development of plantlets from Ananas comosus [L]. Merr. cultivar Turiaçu, an important but neglected pineapple cultivar, under different sucrose concentrations and cultivation systems. For that, the impact of the photomixotrophic and photoautotrophic growth on morphophysiological responses of plants and survival during the ex vitro acclimatization was assessed. The plants were grown in four cultivation systems: permanent immersion system with sealed flasks (PIS-SF); permanent immersion system with natural ventilation (PIS-NV); single-flask temporary immersion bioreactors (TIS-PF); and twin-flasks temporary immersion bioreactors (TIS-RALM), combined with sucrose concentrations (0, 5.0, 15.0, and 30.0 g L−1). The results indicate that Turiaçu plants have photoautotrophic potential in vitro, as the photochemical efficiency of the plants increased in cultivation systems with TIS –RALM gas exchange without the addition of sucrose. Furthermore, it also improved the performance and hardening of plants in ex vitro conditions, which constitutes a crucial step towards the diffusion of this cultivar.
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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Akdemir H, Süzerer V, Onay A, Tilkat E, Ersali Y, Çiftçi YO (2014) Micropropagation of the pistachio and its rootstocks by temporary immersion system. Plant Cell Tiss Org Cult 117:65–76. https://doi.org/10.1007/s11240-013-0421-0
Aliniaeifard S, Asayesh ZM, Driver J, Vahdati K (2020) Stomatal features and desiccation responses of Persian walnut leaf as caused by in vitro stimuli aimed at stomatal closure. Trees 34:1219–1232. https://doi.org/10.1007/s00468-020-01992-x
Alves JP, Pinheiro MVM, Corrêa TR, Alves GL, Marinho TRS, Batista DS, Figueiredo FAMMA, Reis FO, Ferraz TM, Campostrini E (2023) Morphophysiology of Ananas comosus during in vitro photomixotrophic growth and ex vitro acclimatization. In Vitro Cell Dev Biol - Plant 59:106–120. https://doi.org/10.1007/s11627-022-10321-5
Aragón CE, Sánchez C, Gonzalez-Olmedo J, Escalona M, Carvalho L, Amâncio S (2014) Comparison of plantain plantlets propagated in temporary immersion bioreactors and gelled medium during in vitro growth and acclimatization. Biol Plant 58:29–38. https://doi.org/10.1007/s10535-013-0381-6
Arve LE, Terfa MT, Gislerød HR, Olsen JE, Torre S (2013) High relative air humidity and continuous light reduce stomata functionality by affecting the ABA regulation in rose leaves. Plant Cell Environ 36:382–392. https://doi.org/10.1111/j.1365-3040.2012.02580.x
Ayub RA, Santos JN, Zanlorensi Junior LA, Silva DMd, Carvalho TC, Grimaldi F (2019) Sucrose concentration and volume of liquid medium on the in vitro growth and development of blackberry cv. Tupy in temporary immersion systems. Cienc Agrotec 43:e007219. https://doi.org/10.1590/1413-7054201943007219
Batista DS, Dias LLC, Rêgo MM, Saldanha CW, Otoni WC (2017) Flask sealing on in vitro seed germination and morphogenesis of two types of ornamental pepper explants. Cienc Rural 47:e20150245. https://doi.org/10.1590/0103-8478cr20150245
Bello-Bello JJ, Cruz-Cruz CA, Pérez-Guerra JC (2019) A new temporary immersion system for commercial micropropagation of banana (Musa AAA cv. Grand Naine). In Vitro Cell Dev Biol - Plant 55:313–320. https://doi.org/10.1007/s11627-019-09973-7
Cavallaro V, Avola G, Fascella G, Pellegrino A, Ierna A (2023) Effects of Spectral Quality and Light Quantity of LEDs on In Vitro Shoot Development and Proliferation of Ananas comosus L. Merr Agron 13:1072. https://doi.org/10.3390/agronomy13041072
Chaari-Rkhis A, Maalej M, Drira N, Standardi A (2011) Micropropagation of olive tree Olea europaea L. ‘Oueslati.’ Turk J Agric for 35:403–412. https://doi.org/10.3906/tar-1002-741
Corrêa JPO, Vital CE, Pinheiro MVM, Batista DS, Azevedo JFL, Saldanha CW, da Cruz ACF, DaMatta FM, Otoni WC (2015) In vitro photoautotrophic potential and ex vitro photosynthetic competence of Pfaffia glomerata (Spreng.) Pedersen accessions. Plant Cell Tiss Org Cult 121:289–300. https://doi.org/10.1007/s11240-014-0700-4
Couto TR, Silva JR, Torres Netto A, Carvalho VS, Campostrini E (2014) Eficiência fotossintética e crescimento de genótipos de abacaxizeiro cultivados in vitro em diferentes qualidades de luz, tipos de frasco de cultivo e concentrações de sacarose. Rev Bras Frutic 36:459–466. https://doi.org/10.1590/0100-2945-167/13
Cutter EG (1986) Anatomia vegetal. Parte I - Células e tecidos, 2nd edn. Roca, São Paulo, pp 304
Damiani CR, Schuch MW (2008) Multiplicação fotoautotrófica de mirtilo através do uso de luz natural. Rev Bras Frutic 30:482–487. https://doi.org/10.1590/S0100-29452008000200037
Dias DP, Marenco RA (2007) Fotossíntese e fotoinibição em mogno e acariquara in função da luminosidade e temperatura foliar. Pesq Agropec Bras 42:305–311. https://doi.org/10.1590/S0100-204X2007000300002
Erol MH, Dönmez D, Biçen B, Şimşek Ö, Kaçar YA (2023) Modern approaches to in vitro clonal banana production: Next-generation tissue culture systems. Horticulturae 9:1154. https://doi.org/10.3390/horticulturae9101154
Escalona M, Lorenzo JC, González B, Daquinta M, González JL, Desjardins Y, Borroto CG (1999) Pineapple (Ananas comosus L. Merr) micropropagation in temporary immersion systems. Plant Cell Rep 18:743–748. https://doi.org/10.1007/s002990050653
Fanourakis D, Carvalho SM, Almeida DP, Heuvelink EJPP (2011) Avoiding high relative air humidity during critical stages of leaf ontogeny is decisive for stomatal functioning. Physiol Plant 142:274–286. https://doi.org/10.1111/j.1399-3054.2011.01475.x
Farquhar GD, Von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90. https://doi.org/10.1007/BF00386231
Ferreira DF (2011) Sisvar: a computer statistical analysis system. Cienc Agrotec 35:1039–1042. https://doi.org/10.1590/S1413-70542011000600001
Ferreira PRB, da Cruz ACF, Batista DS, Nery LA, Andrade IG, Rocha DI, Felipe SHS, Koehler AD, Nunes-Nesi A, Otoni WC (2019) CO2 enrichment and supporting material impact the primary metabolism and 20-hydroxyecdysone levels in Brazilian ginseng grown under photoautotrophy. Plant Cell Tiss Org Cult 139:77–89. https://doi.org/10.1007/s11240-019-01664-w
Fuentes G, Talavera C, Desjardins Y, Santamaía JM (2007) Low exogenous sucrose improves ex vitro growth and photosynthesis in coconut in vitro plantlets if grown in vitro under high light. Acta Hortic 748:151–155. https://doi.org/10.17660/ActaHortic.2007.748.18
Georgiev V, Schumann A, Pavlov A, Bley T (2014) Temporary immersion systems in plant biotechnology. Eng Life Sci 14:607–621. https://doi.org/10.1002/elsc.201300166
Gonçalves JFC, Silva CE, Guimarães DG, Bernardes RS (2010) Análise dos transientes da fluorescência da clorofila a de plantas jovens de Carapa guianensis e de Dipteryx odorata submetidas a dois ambientes de luz. Acta Amaz 40:89–98. https://doi.org/10.1590/S0044-59672010000100012
Hazarika BN (2006) Morpho-physiological disorders in in vitro culture of plants. Sci Horticult 108:105–120. https://doi.org/10.1016/j.scienta.2006.01.038
Iarema L, da Cruz ACF, Saldanha CW, Dias LLC, Vieira RF, de Oliveira EJ, Otoni WC (2012) Photoautotrophic propagation of Brazilian ginseng [Pfaffia glomerata (Spreng.) Pedersen]. Plant Cell Tiss Org Cult 110:227–238. https://doi.org/10.1007/s11240-012-0145-6
Kessel-Domini A, Pérez-Brito D, Guzmán-Antonio A, Barredo-Pool FA, Mijangos-Cortés JO, Iglesias-Andreu LG, Cortés-Velázquez A, Canto-Flick A, Avilés-Viñas SA, Rodríguez-Llanes Y, Santana-Buzzy N (2022) Indirect somatic embryogenesis: an efficient and genetically reliable clonal propagation system for Ananas comosus L. Merr. hybrid “MD2”. Agriculture 12:713. https://doi.org/10.3390/agriculture12050713
Kozai T (1991) Micropropagation under photoautotrophic conditions. In: Debergh PC, Zimmerman RH (eds) Micropropagation: Technology and Application. Springer, Netherlands, Dordrecht, pp 447–469. https://doi.org/10.1007/978-94-009-2075-0_26
Kozai T (2010) Photoautotrophic micropropagation-environmental control for promoting photosynthesis. Propag Ornam Plants 10:188–204
Kozai T, Kubota C (2001) Development a photoautotrophic micropropagation system for woody plants. J Plant Res 114:525–537. https://doi.org/10.1007/PL00014020
Kozai T, Kubota C, RyoungJeong B (1997) Environmental control for the large-scale production of plants through in vitro techniques. Plant Cell Tiss Org Cult 51:49–56. https://doi.org/10.1023/A:1005809518371
Le KC, Dedicova B, Johansson S, Lelu-Walter MA, Egertsdotter U (2021) Temporary immersion bioreactor system for propagation by somatic embryogenesis of hybrid larch (Larix × eurolepis Henry). Biotechnol Rep 32:e00684. https://doi.org/10.1016/j.btre.2021.e00684
Lima GPP, Campos RAS, Willadino GL, Câmara TJR, Vianello F (2012) Polyamines, gelling agents in tissue culture, micropropagation of medicinal plants and bioreactors. In: Annarita L, Laura MRR (eds) Recent advances in plant in vitro culture. Rijeka, pp 165–182. https://doi.org/10.5772/51028
Majada JP, Fal MA, Sánchez-Tamés R (1997) The effect of ventilation rate on proliferation and hyperhydricity of Dianthus caryophyllus L. In Vitro Cell Dev Biol - Plant 33:62–69. https://doi.org/10.1007/s11627-997-0042-6
Martins JPR, de Almeida Rodrigues LC, Santos ER, Gontijo ABPL, Falqueto AR (2020) Impacts of photoautotrophic, photomixotrophic, and heterotrophic conditions on the anatomy and photosystem II of in vitro-propagated Aechmea blanchetiana (Baker) L.B. Sm. (Bromeliaceae). In Vitro Cell Dev Biol - Plant 56:350–361. https://doi.org/10.1007/s11627-019-10034-2
McCarthy A, Chung M, Ivanov AG, Krol M, Inman M, Maxwell DP, Hüner NPA (2016) An established Arabidopsis thaliana var. Landsberg erecta cell suspension culture accumulates chlorophyll and exhibits a stay-green phenotype in response to high external sucrose concentrations. J Plant Physiol 199:40–51. https://doi.org/10.1016/j.jplph.2016.05.008
Mohamed MAH, Alsadon AA (2010) Influence of ventilation and sucrose on growth and leaf anatomy of micropropagated potato plantlets. Sci Horticult 123:295–300. https://doi.org/10.1016/j.scienta.2009.09.014
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Nasri A, Baklouti E, Ben Romdhane A, Maalej M, Schumacher HM, Drira N, Fki L (2019) Large-scale propagation of Myrobolan (Prunus cerasifera) in RITA® bioreactors and ISSR-based assessment of genetic conformity. Sci Horticult 245:144–153. https://doi.org/10.1016/j.scienta.2018.10.016
Oliveira-Cauduro Yd, Lopes VR, Bona CMD, Alcantara GBd, Biasi LA (2016) Micropropagação de abacaxizeiro com enraizamento in vitro e ex vitro. Plant Cell Cult Micropropag 12:53–60
Pinheiro MVM, Ríos-Ríos AM, da Cruz ACF, Rocha DI, Orbes MY, Saldanha CW, Batista DS, de Carvalho ACPP, Otoni WC (2021) CO2 enrichment alters morphophysiology and improves growth and acclimatization in Etlingera Elatior (Jack) R.M. Smith Micropropagated Plants Braz J Bot 44:799–809. https://doi.org/10.1007/s40415-021-00741-9
Pires HP, Felipe SHS, Pinheiro MVM, Alves JP, Alves GL, Catunda PHA, Figueiredo FAMMAF, Reis FO, Ferraz TM, Corrêa TR (2023) Natural ventilation and sucrose concentrations in the in vitro culture system affect the acclimatization of “Perola” pineapple plants under different substrates. Aust J Crop Sci 17:90–98. https://doi.org/10.21475/ajcs.23.17.01.p3812
Rahmat E, Okello D, Kim H, Lee J, Chung Y, Komakech R, Kang Y (2021) Scale-up production of Rehmannia glutinosa adventitious root biomass in bioreactors and improvement of its acteoside content by elicitation. Ind Crops Prod 172:114059. https://doi.org/10.1016/j.indcrop.2021.114059
Reis COD, Silva ABD, Landgraf PRC, Batista JA, Jacome GAR (2018) Bioreactor in the micropropagation of ornamental pineapple. Ornam Hortic 24:182–187. https://doi.org/10.14295/oh.v24i2.1181
Reis FO, Araujo JRG, Braun H, Junior ACVN, Pereira APA (2019) Fruit quality of a traditional pineapple cultivar (Turiaçu) compared to the most popular cultivar (Pérola) in Brazil. Aust J Crop Sci 13:546–551. https://doi.org/10.21475/ajcs.19.13.04.p1452
Ripley BS, Redfern SP, Dames J (2004) Quantification of the photosynthetic performance of phosphorus-deficient Sorghum by means of chlorophyll-a fluorescence kinetics. S Afr J Sci 100:615–618
Rocha TT, Araújo DX, da Silva AM, de Oliveira JPV, de Carvalho AA, Gavilanes ML, Bertolucci SKV, Pinto JEBP (2022) Morphoanatomy and changes in antioxidant defense associated with the natural ventilation system of micropropagated Lippia dulcis plantlets. Plant Cell Tiss Org Cult 151:467–481. https://doi.org/10.1007/s11240-022-02364-8
Rodrigues MM, Melo MD, Aloufa MAI (2006) Propagação vegetativa in vitro e análise estrutural de macieira. Pesq Agropec Bras 41:171–173. https://doi.org/10.1590/S0100-204X2006000100024
Saldanha CW, Otoni CG, de Azevedo JLF, Dias LLC, do Rêgo MM, Otoni WC (2012) A low-cost alternative membrane system that promotes growth in nodal cultures of Brazilian ginseng [Pfaffia glomerata (Spreng.) Pedersen]. Plant Cell Tiss Org Cult 110:413–422. https://doi.org/10.1007/s11240-012-0162-5
Saldanha CW, Otoni CG, Notini MM, Kuki KN, da Cruz ACF, Neto AR, Dias LLC, Otoni WC (2013) A CO2-enriched atmosphere improves in vitro growth of Brazilian ginseng [Pfaffia glomerata (Spreng.) Pedersen]. In Vitro Cell Dev Biol - Plant 49:433–444. https://doi.org/10.1007/s11627-013-9529-5
San José MC, Blázquez N, Cernadas MJ, Janeiro LV, Cuenca B, Sánchez C, Vidal N (2020) Temporary immersion systems to improve alder micropropagation. Plant Cell Tiss Org Cult 143:265–275. https://doi.org/10.1007/s11240-020-01937-9
Santos GC, Cardoso FP, Martins AD, Pasqual M, Ossani PC, Queiroz JM, Rezende RALS, Dória J (2020) Effect of light and sucrose on photoautotrophic and photomixotrophic micropropagation of Physalis angulata. Biosci J 36:1353–1367. https://doi.org/10.14393/BJ-v36n4a2020-47738
Santos RP, Cruz ACF, Iarema L, Kuki KN, Otoni WC (2008) Protocolo para extração de pigmentos foliares em porta-enxertos de videira micropropagados. Rev Ceres 55:356–364
Scherer RF, Garcia AC, de FreitasFraga HP, Dal Vesco LL, Steinmacher DA, Guerra MP (2013) Nodule cluster cultures and temporary immersion bioreactors as a high performance micropropagation strategy in pineapple (Ananas comosus var. comosus). Scie Hortic 151:38–45. https://doi.org/10.1016/j.scienta.2012.11.027
Scherer RF, Holderbaum DF, Garcia AC, Silva DA, Steinmacher DA, Guerra MP (2015) Effects of immersion system and gibberellic acid on the growth and acclimatization of micropropagated pineapple. Crop Breed Appl Biotechnol 15:66–71. https://doi.org/10.1590/1984-70332015v15n2a13
Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing Photosynthesis: Mechanisms, Regulation and Adaptation. Taylor & Francis, London, pp 445–483
Vahdati K, Asayesh ZM, Aliniaeifard S, Leslie C (2017) Improvement of ex vitro desiccation through elevation of CO2 concentration in the atmosphere of culture vessels during in vitro growth. HortScience 52:1006–1012. https://doi.org/10.21273/HORTSCI11922-17
Vahdati K, Hassankhah A (2014) Developing a photomixotrophic system for micropropagation of persian walnut. Acta Hortic 1050:181–187. https://doi.org/10.17660/ActaHortic.2014.1050.23
Valdés García A, Domingo Martínez MI, Ponce Landete M, Prats Moya MS, Beltrán Sanahuja A (2021) Potential of industrial pineapple (Ananas comosus (L.) Merrill) by-products as aromatic and antioxidant sources. Antioxidants 10:1767. https://doi.org/10.3390/antiox10111767
Vidal N, Sanchez C (2019) Use of bioreactor systems in the propagation of forest trees. Eng Life Sci 19:896–915. https://doi.org/10.1002/elsc.201900041
Welander M, Persson J, Asp H, Zhu LH (2014) Evaluation of a new vessel system based on temporary immersion system for micropropagation. Scie Hortic 179:227–232. https://doi.org/10.1016/j.scienta.2014.09.035
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313. https://doi.org/10.1016/S0176-1617(11)81192-2
Wolf S, Kalman-Rotem N, Yakir D, Zrv M (1998) Autotrophic and heterotrophic carbon assimilation of in vitro grown potato (Solanum tuberosum L) plants. J Plant Physiol 153:574–580. https://doi.org/10.1016/S0176-1617(98)80206-X
Xiao Y, Kozai T (2004) Commercial application of a photoautotrophic micropropagation system using large vessels with forced ventilation: Plantlet growth and production cost. HortSci 39:1387–1391. https://doi.org/10.21273/HORTSCI.39.6.1387
Xiao Y, Niu G, Kozai T (2011) Development and application of photoautotrophic micropropagation plant system. Plant Cell Tiss Org Cult 105:149–158. https://doi.org/10.1007/s11240-010-9863-9
Yang F, Moss LG, Phillips GN Jr (1996) The molecular structure of green fluorescent protein. Nat Biotechnol 14:1246–1251. https://doi.org/10.1038/nbt1096-1246
Zhang M, Zhao D, Ma Z, Li X, Xiao Y (2009) Growth and photosynthetic capability of Momordica grosvenori plantlets grown photoautotrophically in response to light intensity. HortScience 44:757–763. https://doi.org/10.21273/HORTSCI.44.3.757
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The authors acknowledge FAPEMA (Fundação de Amparo à Pesquisa e ao Desenvolvimento Científico e Tecnológicodo Maranhão).
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This study was partly funded by the Fundação de Amparo à Pesquisa e ao Desenvolvimento Científico e Tecnológico do Maranhão – FAPEMA – Brazil (IECT-05458/18), Graduate Program in Agroecology State University of Maranhão.
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GLA: Investigation, Conceptualization, Methodology, Data curation, Formal analysis, Writing-Original draft preparation; MVMP: Supervision, Writing – review & editing, Investigation, Formal analysis; TRMD: Methodology, Investigation, Data curation; KSV: Methodology, Investigation; FAMMAF: Resources, Methodology, Investigation; TMF: Resources, Investigation; EC: Methodology, Visualization Writing—Original Draft; JCR: Writing – review & editing; TRC: Supervision, Resources Conceptualization, Writing – review & editing; FOR: Supervision, Conceptualization, Writing – review & editing Funding acquisition, Project administration. All authors have read and approved the final manuscript.
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Alves, G.L., Pinheiro, M.V.M., Marinho-Dutra, T.R. et al. Photoautotrophic potential and photosynthetic competence in Ananas comosus [L]. Merr. cultivar Turiaçu in in vitro culture systems. In Vitro Cell.Dev.Biol.-Plant 60, 131–146 (2024). https://doi.org/10.1007/s11627-023-10410-z
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DOI: https://doi.org/10.1007/s11627-023-10410-z