Abstract
The in vitro propagation is a technique that is used for the large-scale generation of stable genotypes that are free of disease. Satisfactory propagation has been obtained using Bactris gasipaes Kunth through the direct in vitro regeneration of adventitious buds and somatic embryos, which is likely because of the pluri—and totipotency of the preprocambial cells, which reduces the probability of genetic instability. The consequences of the prolonged period of in vitro cultivation of perennial species such as the peach palm are not clear, as well as the senescence process has only been investigated in species originating from callus structures. The senescence of peach palm clones established and cultivated in vitro for 8 years through direct morphogenic methods (in vitro regeneration of adventitious buds without callus formation) was investigated in the leaves, roots and stem bases using histological, histochemical and ultrastructural analyses, in addition to the TUNEL reaction, to detect programmed cell death. These data from old cultures (8 years cultured) were compared to similar data from plants of the same species that had been established and cultivated in vitro for 1 year (young cultures). These analyses demonstrated the existence of intensive programmed cell death in the various tissues of the old cultures. The in vitro cultivation of peach palm for long periods promoted generalized senescence and probable aging of clones.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- BAP:
-
6-Benzylaminopurine
- MS:
-
Murashige and Skoog (1962)
- NAA:
-
1-Naphthaleneacetic acid
- PCD:
-
Programmed cell death
- PGR:
-
Plant growth regulator
- PPCs:
-
Preprocambial cells
- TUNEL:
-
Terminal deoxynucleotidyl transferase dUTP nick end labelling
References
Abreu-Tarazi MF, Navarrete AA, Andreote FD, Almeida CV, Tsai SM, Almeida M (2010) Endophytic bacteria in long-term in vitro cultivated ‘‘axenic’’ pineapple microplants revealed by PCR–DGGE. World J Microbiol Biotechnol 26(3):555–560. doi:10.1007/s11274-009-0191-3
Akin-Idowu PE, Ibitoye DO, Ademoyegun OT (2009) Tissue culture as a plant production technique for horticultural crops. Afr J Biotechnol 8(16):3782–3788
Almeida M, Almeida CV (2006) Somatic embryogenesis and in vitro plant regeneration from pejibaye adult plant leaf primordial. Pesq Agrop Brasileira 41:1449–1452. doi:10.1590/S0100-204X2006000900015
Almeida M, Kerbauy GB (1996) Micropropagation of Bactris gasipaes HBK (Palmae) through flowers bud culture. R Bras Fisiol Veg 8(3):215–217
Almeida CV, Andreote FD, Yara R, Tanaka F, Azevedo JL, Almeida M (2009) Bacteriosomes in axenic plants: endophytes as stable endosymbionts. World J Microbiol Biotechnol 25(10):1757–17642. doi:10.1007/s11274-009-0073-8
Almeida M, Almeida CV, Graner E, Brondani GE, Abreu-Tarazi MF (2012) Pre-procambial cells are niches for pluripotent and totipotent stem-like cells for organogenesis and somatic embryogenesis in the peach palm: a histological study. Plant Cell Rep 31(9):1449–1452. doi:10.1007/s00299-012-1264-6
Blumwald E, Aharon GS, Lam BCH (1998) Early signal transduction pathways in plant-pathogen interactions. Trends Plant Sci 3(9):342–346. doi:10.1016/S1360-1385(98)01289-8
Bordallo PN, Silva DH, Maria J, Cruz CD, Fontes EP (2004) Somaclonal variation on in vitro callus culture potato cultivars. Hortic Bras 22:300–304
Buckner B, Janick-Buckner D, Gray J, Johal GS (1998) Cell-death mechanisms in maize. Trends Plant Sci 3(6):218–223. doi:10.1016/S1360-1385(98)01254-0
Calvete EO, Azevedo M, Bordignon MH, Suzin M (2002) Anatomic analyses and biomass of strawberry plants cultivated in vitro and ex vitro. Hortic Bras 20:649–653. doi:10.1590/S0102-05362002000400028
Ceita GO, Macêdo JNA, Santos TB, Alemanno L, Gesteira AS, Micheli F, Mariano AC, Gramacho KP, Silva DC, Meinhardt J, Mazzafera P, Pereira GAG, Cascardo JCM (2007) Involvement of calcium oxalate degradation during programmed cell death in Theobroma cacao tissues triggered by the hemibiotrophic fungus Crinipellis perniciosa. Plant Sci 173(2):106–117. doi:10.1016/j.plantsci.2007.04.006
Chaturvedi HC, Mitra GC (1975) A shift in morphogenic pattern in citrus callus tissue during prolonged culture. Ann Bot 39(4):683–687
Danon A, Delorme V, Mailhac N, Gallois P (2000) Plant programmed cell death: a common way to die. Plant Physiol Biochem 38(9):647–655. doi:10.1093/jxb/erm189
Dettmer J, Elo A, Helariutta Y (2009) Hormone interactions during vascular development. Plant Mol Biol 69(4):347–360. doi:10.1007/s11103-008-9374-9
Dhindsa RS, Matawe W (1981) Drought tolerance in two mosses: correlated with difference against lipid peroxidation. J Exp Bot 32(1):19–21. doi:10.1093/jxb/32.1.79
Domínguez F, Moreno J, Cejudo FJ (2004) A gibberellin-induced nuclease is localized in the nucleus of wheat aleurone cells undergoing programmed cell death. J Biol Chem 279(12):11530–11536. doi:10.1074/jbc.M308082200
Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35(4):495–516. doi:10.1080/01926230701320337
Filonova LH, von Arnold S, Daniel G, Bozhkov PV (2002) Programmed cell death eliminates all but one embryo in a polyembryonic plant seed. Cell Death Differ 9(10):1057–1062. doi:10.1038/sj.cdd.4401068
Fuzinatto VA, Pagliarini MS, Valle CB (2007) Evidence of programmed cell death during microsporogenesis in a interespecific Brachiaria (Poaceae: Panicoideae: Paniceae). Genet Mol Res 6(2):308–315
Gaspar TH, Kevers C, Faivre-Rampant O, Crèvecoeur M, Pennel CL, Greppin H, Dommes J (2003) Changing concepts in plant hormone action. In Vitro Cell Dev Biol Plant 39(2):85–106. doi:10.1079/IVP2002393
Giles KL, Morgan WM (1987) Industrial scale plant micropropagation. Trends Biotechnol 5(2):35–39. doi:10.1016/0167-7799(87)90035-7
Graner EM, Oberschelp GPJ, Brondani GE, Batagin-Piotto KD, Almeida CV, Almeida M (2013) TDZ pulsing evaluation on the in vitro morphogenesis of peach palm. Physiol Mol Biol Plants 19:283–288. doi:10.1007/s12298-012-0160-4
Grout BWW (1988) Photosynthesis of regenerated plantlets in vitro, and stress of transplanting. Acta Hort 230:129–135
Hartmann HT, Kester DE, Davies FT, Geneve RL (2011) Principles and practices of clonal selection. In: Hartmann HT, Kester DE, Davies FT, Geneve RL (eds) Hartmann and Kester’s plant propagation: principles and practices. Prentice Hall, New Jersey, pp 594–641
Häsler J, Wüest J, Gaspar T, Crèvecoeur M (2003) Long term in vitro-cultured plant cells show typical neoplastic features at the cytological level. Biol Cell 95(6):357–364. doi:10.1016/S0248-4900(03)00077-7
Held MA, Boulaflous A, Brandizzi F (2008) Advances in fluorescent protein-based imaging for the analysis of plant endomembranes. Plant Physiol 147(4):1469–1481. doi:10.1104/pp.108.120147
Johansen DA (1940) Plant microtechnique. Mc Graw Hill Book, New York
Jones AM (2001) Programmed cell death in development and defense. Plant Physiol 125(1):94–97. doi:10.1104/pp.125.1.94
Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43(2–3):179–188
Karnovsky MJ (1965) A formaldehyde–glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27(2):137–138
Konan KE, Gasselin TD, Kouadio YJ, Flori A, Rival A, Duval Y, Pannetier C (2010) In vitro conservation of oil palm somatic embryos for 20 years on a hormone-free culture medium: characteristics of the embryogenic cultures, derived plantlets and adult palms. Plant Cell Rep 29(1):1–13. doi:10.1007/s00299-009-0787-y
Kumar A, Altabella T, Taylor MA, Tiburcio AF (1997) Recent advances in polyamine research. Trends Plant Sci 2(4):124–130. doi:10.1016/S1360-1385(97)01013-3
Kuznetsov S, Lyanguzowa M, Bosh TCG (2001) Role of epithelial cells and programmed cell death in Hydra spermatogenesis. Zoology 104(1):25–31. doi:10.1078/0944-2006-00005
Li W, Ahn IP, Ning Y, Park CH, Zeng L, Whitehill J, Lu H, Zhao Q, Ding B, Xie Q, Zhou JM, Daí L, Wang GL (2012) The U-box/ARM E3 ligase PUB13 regulates cell death, defense and flowering time in Arabidopsis. Plant Physiol 159(1):239–250. doi:10.1104/pp.111.192617
Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58(1):115–136. doi:10.1146/annurev.arplant.57.032905.105316
Liu Y, Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Physiol 63:215–237. doi:10.1146/annurev-arplant-042811-105441
Lynch P, Souch G, Trigwell S, Keller J, Harding K (2011) Plant cryopreservation: from laboratory to genebank. Asia Pac J Mol Biol Biotechnol 18(1):239–242
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51(345):659–668. doi:10.1093/jexbot/51.345.659
McCabe PF, Leaver CJ (2000) Programmed cell death in cell cultures. In: Lam E, Fukuda H, Greenberg J (eds) Programmed cell death in higher plants. Kluwer, Dordrecht, pp 115–124
Medawar PB (1957) The uniqueness of the individual. Basic Books, New York
Meins F (1989) Habituation: hereditable variation in the requirement of cultured plant cells for hormones. Annu Rev Gen 23:395–408
Monaco LC, Söndahl MR, Carvalho A, Crocomo OJ, Sharp WR (1977) Aplications of tissue culture in the improvement of coffe. In: Reinert J, Bajaj YPS (eds) Applied and fundamental aspects of plant cell, tissue and organ culture. Springer, Berlin, pp 109–129
Munné-Bosch S (2007) Aging in perennials. Crit Rev Plant Sci 26(3):123–138. doi:10.1080/07352680701402487
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15(2):473–497
Obara K, Kuriyama H, Fukuda H (2001) Direct evidence of active and rapid nuclear degradation triggered by vacuole rupture during programmed cell death in Zinnia. Plant Physiol 125(2):615–626. doi:10.1104/pp.125.2.615
Overmyer K, Brosche M, Pellinen R, Kuittinen T, Tuominen H, Ahlfors R, Keinaenen M, Saarma M, Scheel D, Kangasjaervi J (2005) Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death 1 mutant. Plant Physiol 137(3):1092–1104. doi:10.1104/pp.104.055681
Pastori GM, Del Rio LA (1997) Natural senescence of pea leaves. Plant Physiol 113(2):411–418. doi:10.1104/pp.113.2.411
Reape TJ, Molony EM, McCabe PF (2008) Programmed cell death in plants: distinguishing between different modes. J Exp Bot 59(3):435–444. doi:10.1093/jxb/erm258
Riha K, Mcknight TD, Griffing LR, Shippen DE (2001) Living with genome instability: plant responses to telomere dysfunction. Science 291(5509):1797–1800. doi:10.1126/science.1057110
Sakai WS (1973) Simple method for differential staining of paraffin embedded plant material using toluidine blue O. Stain Tech 48:247–249. doi:10.3109/10520297309116632
Sgonc R, Boeck G, Dietrich, Gruber J, Wick G (1994) Simultaneous determination of cell surface antigens and apoptosis. Trends Genet 10(2):41–42. doi:10.1016/0168-9525(94)90140-6
Sharma T, Modgil M, Thakur M (2007) Factors affeting induction and development of in vitro rooting in apple rootstocks. Indian J Exp Biol 45(9):824–829
Shishkova S, Dubrovsky JG (2005) Developmental programmed cell death in primary roots of sonoran desert cactaceae. Am J Bot 29(9):1590–1594. doi:10.3732/ajb.92.9.1590
Smetana O, Široký J, Houlné G, Opatrný Z, Chabouté ME (2012) Non-apoptotic programmed cell death with paraptotic-like features in bleomycin-treated plant cells is suppressed by inhibition of ATM/ATR pathways or NtE2F overexpression. J Exp Bot 63(7):2631–2644. doi:10.1093/jxb/err439
Valledor L, Hasbún R, Meijón M, Rodríguez JL, Santamaría E, Viejo M, Berdasco M, Feito I, Fraga MF, Cañal MJ, Rodríguez R (2007) Involvement of DNA methylation in tree development and micropropagation. Plant Cell Tiss Organ Cult 91:75–86. doi:10.1007/s11240-007-9262-z
van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141(2):384–390. doi:10.1104/pp.106.078295
van Doorn WG (2011) Classes of programmed cell death in plants, compared to those in animals. J Exp Bot 62(14):4749–4761. doi:10.1093/jxb/err196
van Doorn WG, Woltering EJ (2004) Senescence and programmed cell death: substance or semantics? J Exp Bot 55(406):2147–2153. doi:10.1093/jxb/erh264
Vidi PA, Kanwischer M, Baginsky S, Austin JR, Csucs G, Dörmann P, Kessler F, Bréhélin C (2006) Tocopherol cyclase (VTE1) localization and vitamin E accumulation in chloroplast plastoglobule lipoprotein particles. J Biol Chem 281(16):11225–11234. doi:10.1074/jbc.M511939200
Wang J, Bayles K (2012) Programmed cell death in plants: lessons from bacteria? Trends Plant Sci 18(3):133–139. doi:10.1016/j.tplants.2012.09.004
Wang H, Li J, Bostock RM, Gilchrist DG (1996) Apoptosis: a functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 8(3):375–391. doi:10.1105/tpc.8.3.375
Watson JM, Riha K (2011) Telomeres, aging, and plants: from weeds to Methuselah—a mini-review. Gerontology 57(2):129–136. doi:10.1159/000310174
Wright H, van Doorn WG, Gunawardena AH (2009) In vivo study of developmental programmed cell death using the lace plant (Aponogeton madagascariensis; Aponogetonaceae) leaf model system. Am J Bot 96(5):865–876. doi:10.3732/ajb.0800343
Zavaleta-Mancera HA, Thomas BJ, Thomas H, Scott IM (1999) Regreening of senescent Nicotiana leaves. II. redifferentiation of plastids. J Exp Bot 50(340):1683–1689. doi:10.1093/jxb/50.340.1683
Zhuravlev YN, Omelko AM (2008) Plant morphogenesis in vitro. Russ J Plant Physiol 55(5):579–596. doi:10.1134/S1021443708050014
Acknowledgments
This work was supported by FAPESP (São Paulo Research Foundation, Brazil), FINEP (Financier of Studies and Projects), Inaceres Agrícola, InVitroPalm (Consulting, Study and Biological Development Ltd.) and CAPES (Coordination for the Improvement of Higher Level, Brazil) supported this study. We thank PhD Edgard Graner, PhD Michelle Agostini, PhD Ricardo Della Coletta, and the Faculty of Dentistry of Piracicaba (State University of Campinas), Piracicaba, São Paulo, Brazil for assistance with the TUNEL reactions. We thank PhD Elliot Watanabe Kitajima, PhD Francisco André Ossamu Tanaka and Renato Barbosa Salaroli of Research Support Centre/Electron Microscopy Applied to Agriculture, “Luiz de Queiroz” College of Agriculture, University of São Paulo (NAP/MEPA/ESALQ/USP), Piracicaba, São Paulo, Brazil for their assistance with the ultrastructural analyses.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Graner, E.M., Brondani, G.E., de Almeida, C.V. et al. Study of senescence in old cultures of the Bactris gasipaes Kunth in vitro. Plant Cell Tiss Organ Cult 120, 1169–1189 (2015). https://doi.org/10.1007/s11240-014-0672-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-014-0672-4