Sources and concentrations of silicon modulate the physiological and anatomical responses of Aechmea blanchetiana (Bromeliaceae) during in vitro culture

Abstract

The use of silicon (Si) has been shown to be a good alternative to improve the growth and content of photosynthetic pigments of plants propagated in vitro. So far, it is not well understood how the sources and concentrations of Si can affect the root and leaf anatomy as well as the functioning of the photosynthetic apparatus of these plants. The aim was to assess the physiological and anatomical responses of Aechmea blanchetiana plants in function of sources and concentrations of Si during in vitro culture. Side shoots of plants previously established in vitro were excised and transferred to a culture medium containing CaSiO3 or Na2SiO3 in four concentrations (0, 7, 14 or 21 µM). After culture for 90 days, the chlorophyll a fluorescence transient, root and leaf anatomy, contents of photosynthetic pigments and mineral nutrients as well as growth were analyzed. Plants grown in medium supplemented with Na2SiO3 presented characteristics of salt stress, such as smaller stomata, higher potassium content and lower number of active reaction centers (RC/CSM). On the other hand, plants cultured with 7 and 14 µM CaSiO3 had an increase in photosynthetic pigment content and performance of photosynthetic apparatus, verified by the performance indexes (PI(ABS) and PI(TOTAL)). The employment of concentrations equal to or higher than 21 µM Si, independent of Si source, caused toxicity symptoms in the plants. The use of CaSiO3 had a positive effect on the concentration interval between 7 and 14 µM by improving physiological and anatomical quality of A. blanchetiana plants.

Key message

Silicon source and concentration can affect the physiological responses of Aechmea blanchetiana during in vitro culture. This study highlights that CaSiO3 increases the photosynthetic pigment content and photosynthetic apparatus performance.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

References

  1. Adams WW, Zarter CR, Mueh KE, Amiard V, Demmig-Adams B (2008) Energy dissipation and photoinhibition: a continuum of photoprotection gene. Regul Environ 21:49–64. https://doi.org/10.1007/1-4020-3579-9_5

    Article  Google Scholar 

  2. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Arshi A, Ahmad A, Aref IM, Iqbal M (2010) Effect of calcium against salinity-induced inhibition in growth, ion accumulation and proline contents in Cichorium intybus L. J Environ Biol 31:939–944

    CAS  PubMed  Google Scholar 

  4. Asmar SA, Pasqual M, Rodrigues FA, Araujo AG, Pio LAS, Silva SO (2011) Fontes de silício no desenvolvimento de plântulas de bananeira ‘Maçã’ micropropagadas. Cienc Rural 41:1127–1131. https://doi.org/10.1590/S0103-84782011005000086

    Article  CAS  Google Scholar 

  5. Asmar AS, Castro EM, Pasqual M, Pereira FJ, Soares JDR (2013) Changes in leaf anatomy and photosynthesis of micropropagated banana plantlets under different silicon sources. Sci Hortic 161:328–332. https://doi.org/10.1016/j.scienta.2013.07.021

    Article  CAS  Google Scholar 

  6. Asmar AS, Soares JDR, Silva RAL, Pasqual M, Pio LAS, Castro EM (2015) Anatomical and structural changes in response to application of silicon (Si) in vitro during the acclimatization of banana cv. ‘Grand Naine’. Aust J Crop Sci 9:1236–1241

    CAS  Google Scholar 

  7. Bowsher AW, Mason CM, Goolsby EW, Donovan LA (2016) Fine root tradeoffs between nitrogen concentration and xylem vessel traits preclude unified whole-plant resource strategies in Helianthus. Ecol Evol 6:1016–1031. https://doi.org/10.1002/ece3.1947

    Article  PubMed  PubMed Central  Google Scholar 

  8. Cai W, Gao X, Hu J, Chen L, Li X, Liu Y, Wang G (2016) UV-B radiation inhibits the photosynthetic electron transport chain in Chlamydomonas reinhardtii. Pak J Bot 48:2587–2593

    CAS  Google Scholar 

  9. Chen S, Kang Y, Zhang M, Wang X, Strasser RJ, Zhou B, Qiang S (2015) Differential sensitivity to the potential bioherbicide tenuazonic acid probed by the JIP-test based on fast chlorophyll fluorescence kinetics. Environ Exp Bot 112:1–15. https://doi.org/10.1016/j.envexpbot.2014.11.009

    Article  CAS  Google Scholar 

  10. Correia CM, Pereira JMM, Coutinho JF, Björn LO, Torres-Pereira JMG (2005) Ultraviolet-B radiation and nitrogen affect the photosynthesis of maize: a Mediterranean field study. Eur J Agron 22:337–347

    Article  CAS  Google Scholar 

  11. Costa BNS, Costa IJS, Dias GMG, Assis FA, Pio LAS, Soares JDR, Pasqual M (2018) Morpho-anatomical and physiological alterations of passion fruit fertilized with silicon. Pesq Agropec Bras 53:163–171. https://doi.org/10.1590/s0100-204x2018000200004

    Article  Google Scholar 

  12. Dias GMG, Soares JDR, Pasqual M, Alves RL, Rodrigues LCA, Pereira FJ, Castro EM (2014) Photosynthesis and leaf anatomy of Anthurium cv. Rubi plantlets cultured in vitro under different silicon (Si) concentrations. Aust J Crop Sci 8:1160–1167

    CAS  Google Scholar 

  13. Dias GMG, Soares JDR, Ribeiro SF, Martins AD, Paqual M, Alves E (2017) Morphological and physiological characteristics in vitro anthurium plantlets exposed to silicon. Crop Breed Appl Biot 17:18–24. https://doi.org/10.1590/s0100-204x2018000100004

    Article  Google Scholar 

  14. Fajinmi OO, Amoo SO, Finnie JF, Van Staden J (2014) Optimization of in vitro propagation of Coleonema album, a highly utilized medicinal and ornamental plant. S Afr J Bot 94:9–13. https://doi.org/10.1016/j.sajb.2014.05.006

    Article  CAS  Google Scholar 

  15. Ghassemi-Golezani K, Lotfi R (2015) The Impact of salicylic acid and silicon on chlorophyll a fluorescence in mung bean under salt stress. Russ J Plant Physiol 62:611–616. https://doi.org/10.1134/S1021443715040081

    Article  CAS  Google Scholar 

  16. Goltsev VN, Kalaji HM, Paunov M, Bąba W, Horaczek T, Mojski J, Kociel H, Allakhverdiev SI (2016) Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. Russ J Plant Physiol 63:869–893. https://doi.org/10.1134/S1021443716050058

    Article  CAS  Google Scholar 

  17. Johansen DA (1940) Plant microtechnique. Mc Graw-Hill (2ª Ed.), New York, pp 523

  18. Jordan GJ, Carpenter RJ, Koutoulis A, Price A, Brodribb TJ (2015) Environmental adaptation in stomatal size independent of the effects of genome size. New Phytologist Trust 205:608–617. https://doi.org/10.1111/nph.13076

    Article  Google Scholar 

  19. Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Cetner MD, Łukasik I, Goltsev V, Ladle RJ (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 4:1–11. https://doi.org/10.1007/s11738-016-2113-y

    CAS  Article  Google Scholar 

  20. Kaya C, Higgs D (2003) Supplementary potassium nitrate improves salt tolerance in bell pepper plants. J Plant Nutr 26:1367–1382. https://doi.org/10.1081/PLN-120021048

    Article  CAS  Google Scholar 

  21. Kwano BH, Moreira A, Moraes LAC, Nogueira MA (2017) Magnesium-manganese interaction in soybean cultivars with different nutritional requirements. J Plant Nutr 40:372–381. https://doi.org/10.1080/01904167.2016.1240198

    Article  CAS  Google Scholar 

  22. Lembrechts R, Ceusters N, De Proft M, Ceusters J (2017) Sugar and starch dynamics in the medium-root-leaf system indicate possibilities to optimize plant tissue culture. Sci Hortic 224:226–231. https://doi.org/10.1016/j.scienta.2017.06.015

    Article  CAS  Google Scholar 

  23. Malavolta E, Vitti GC, Oliveira AS (1997) Avaliação do estado nutricional das plantas: princípios e aplicações, 2.ed. POTAFOS, Piracicaba, 319 p

    Google Scholar 

  24. Malvi UR (2011) Interaction of micronutrients with major nutrients with special reference to potassium. Karnataka J Agric Sci 24:106–109

    Google Scholar 

  25. Manivannan A, Soundararajan P, Cho YS, Park JE, Jeong BR (2018) Sources of silicon influence photosystem and redox homeostasis-related proteins during the axillary shoot multiplication of Dianthus caryophyllus. Plant Biosyst 152:704–710. https://doi.org/10.1080/11263504.2017.1320312

    Article  Google Scholar 

  26. Marschner P (2012) Mineral nutrition of higher plants. Academic Press, London

    Google Scholar 

  27. Martins JPR, Schimildt ER, Alexandre RS, Falqueto AR, Otoni WC (2015a) Chlorophyll a fluorescence and growth of Neoregelia concentrica (Bromeliaceae) during acclimatization in response to light levels. In Vitro Cell Dev 51:471–481. https://doi.org/10.1007/s11627-015-9711-z

    Article  CAS  Google Scholar 

  28. Martins JPR, Verdoodt V, Pasqual M, De Proft M (2015b) Impacts of photoautotrophic and photomixotrophic conditions on in vitro propagated Billbergia zebrina (Bromeliaceae). Plant Cell Tissue Organ Cult 123(1):121–132. https://doi.org/10.1007/s11240-015-0820-5

    Article  CAS  Google Scholar 

  29. Martins JPR, Verdoodt V, Pasqual M, De Proft M (2016) Physiological responses by Billbergia zebrina (Bromeliaceae) when grown under controlled microenvironmental conditions. Afr J Biotechnol 15:1952–1961. https://doi.org/10.5897/AJB2016.15584

    Article  CAS  Google Scholar 

  30. Martins AD, Martins JPR, Batista LA, DIAS GMG, Almeida MO, Pasqual M, Santos HO (2018a) Morpho-physiological changes in Billbergia zebrina due to the use of silicates in vitro. An Acad Bras Ciênc 90:3449–3462. https://doi.org/10.1590/0001-3765201820170518

    Article  PubMed  Google Scholar 

  31. Martins JPR, Rodrigues LCA, Santos ER, Batista BG, Gontijo ABPL, Falqueto AR (2018b) Anatomy and photosystem II activity of in vitro grown Aechmea blanchetiana as affected by 1-naphthaleneacetic acid. Biol Plantarum 62:211–221. https://doi.org/10.1007/s10535-018-0781-8

    Article  CAS  Google Scholar 

  32. Martins JPR, Santos ER, Rodrigues LCA, Gontijo ABPL, Falqueto AR (2018c) Effects of 6-benzylaminopurine on photosystem II functionality and leaf anatomy of in vitro cultivated Aechmea blanchetiana. Biol Plantarum 62:793–800. https://doi.org/10.1007/s10535-018-0822-3

    Article  CAS  Google Scholar 

  33. Matysiak B, Gabryszewska E (2016) The effect of in vitro culture conditions on the pattern of maximum photochemical efficiency of photosystem II during acclimatisation of Helleborus niger plantlets to ex vitro conditions. Plant Cell Tissue Organ Cult 125:585–593. https://doi.org/10.1007/s11240-016-0972-y

    Article  CAS  Google Scholar 

  34. Meng LL, Song JF, Wen J, Zhang J, Wei JH (2016) Effects of drought stress on fluorescence characteristics of photosystem II in leaves of Plectranthus scutellarioides. Photosynthetica 54:414–421. https://doi.org/10.1007/s11099-016-0191-0

    Article  CAS  Google Scholar 

  35. Monda K, Araki H, Kuhara S, Ishigaki G, Akashi R, Negi R, Kojima M, Sakakibara H, Takahashi S, Hashimoto-Sugimoto M, Goto N, Iba K (2016) Enhanced stomatal conductance by a spontaneous arabidopsis tetraploid, Me-0, results from increased stomatal size and greater stomatal aperture. Plant Physiol 01450.2015; https://doi.org/10.1104/pp.15.01450

  36. 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.1399-3054.1962.tb08052.x

    Article  CAS  Google Scholar 

  37. Patil AA, Durgude AG, Pharande Al (2018) Effect of silicon application along with chemical fertilizers on nutrient uptake and nutrient availability for rice plants. Int J Chem Stud 6:260–266

    CAS  Google Scholar 

  38. Pitman JK (2005) Manganese molecular mechanism of manganese transport and homeostasis. New Phytol 167:733–742. https://doi.org/10.1111/j.1469-8137.2005.01453.x

    Article  CAS  Google Scholar 

  39. Poschenrieder C, Barcelo´ J (1999) Water relations in heavy metal stressed plants. In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants. Springer, Berlin, pp 207–229. https://doi.org/10.1007/978-3-662-07745-0_10

    Google Scholar 

  40. Rab A, Sajid M, Ahmad N, Nawab K, Ali SG (2017) Foliar calcium application ameliorates salinity-induced changes of tomato crop grown in saline conditions. Sarhad J Agric 33:540–548. https://doi.org/10.17582/journal.sja/2017/33.4.540.548

    Article  Google Scholar 

  41. Rapacz M, Kościelniak J, Jurczyk B, Adamska A, Wójcik M (2010) Different patterns of physiological and molecular response to drought in seedlings of malt- and feed-type barleys (Hordeum vulgare). J Agron Crop Sci 196:9–19. https://doi.org/10.1111/j.1439-037X.2009.00389.x

    Article  CAS  Google Scholar 

  42. Rezende RALS, Rodrigues FA, Soares JDR, Silveira HRO, Pasqual M, Dias GMG (2018) Salt stress and exogenous silicon influence physiological and anatomical features of in vitro-grown cape gooseberry. Cien Rural 48:e20170176. https://doi.org/10.1590/0103-8478cr20170176

    Article  Google Scholar 

  43. Ribera-Fonseca A, Rumpel C, Mora ML, Nikolic M, Cartes P (2018) Sodium silicate and calcium silicate differentially affect silicon and aluminium uptake, antioxidant performance and phenolics metabolism of ryegrass in an acid Andisol. Crop Pasture Sci 69:205–215. https://doi.org/10.1071/CP17202

    Article  CAS  Google Scholar 

  44. Rodrigues FA, Rezende RALS, Soares JDR, Rodrigues VA, Pasqual M, Silva SO (2017) Application of silicon sources in yam (Dioscorea spp.) micropropagation. Aust J Crop Sci 11:1469–1473. https://doi.org/10.21475/ajcs.17.11.11.pne685

    Article  CAS  Google Scholar 

  45. Rosa WS, Martins JPR, Santos ER, Rodrigues LCA, Gontijo ABPL, Falqueto AR (2018) Photosynthetic apparatus performance in function of the cytokinins used during the in vitro multiplication of Aechmea blanchetiana (Bromeliaceae). Plant Cell Tissue Organ Cul 133:339–350. https://doi.org/10.1007/s11240-018-1385-x

    Article  CAS  Google Scholar 

  46. Rouphael Y, Micco V, Arena C, Raimondi G, Colla G, Pascale S (2017) Effect of Ecklonia maxima seaweed extract on yield, mineral composition, gas exchange, and leaf anatomy of zucchini squash grown under saline conditions. J App Phycol 29:459–470. https://doi.org/10.1007/s10811-016-0937-x

    Article  CAS  Google Scholar 

  47. Sáez PL, Bravo LA, Sáez KL, Sánchez-Olate M, Latsague MI, Ríos DG (2012) Photosynthetic and leaf anatomical characteristics of Castanea sativa: a comparison between in vitro and nursery plants. Biol Pant 56:15–24. https://doi.org/10.1007/s10535-012-0010-9

    CAS  Article  Google Scholar 

  48. Sáez PL, Bravo LA, Sánchez-Olate M, Bravo PB, Ríos DG (2016) Effect of photon flux density and exogenous sucrose on the photosynthetic performance during in vitro culture of Castanea sativa. Am J Plant Sci 7:2087–2105

    Article  CAS  Google Scholar 

  49. Scholz AK, Klepsch M, Karimi Z, Jansen S (2013) How to quantify conduits in wood? Front Plant Sci 4:1–11

    Article  Google Scholar 

  50. Ševčíková H, Lhotáková Z, Hamet J, Lipavská H (2018) Mixotrophic in vitro cultivations: the way to go astray in plant physiology. Physiol Plant. https://doi.org/10.1111/ppl.12893

    Article  PubMed  Google Scholar 

  51. Sivanesan I, Park SW (2014) The role of silicon in plant tissue culture. Front Plant Sci 5:1–4. https://doi.org/10.3389/fpls.2014.00571

    Article  Google Scholar 

  52. Solmaz I, Sari N, Dasgan Y, Aktas H, Yetisir H, Unlu H (2011) The effect of salinity on stomata and leaf characteristis of dihaploid melon lines and their hybrids. J Food Agri Environ 9:172–176

    CAS  Google Scholar 

  53. Soundararajan P, Sivanesan I, Jo EH, Jeong BR (2013) Silicon promotes shoot proliferation and shoot growth of Salvia splendens under salt stress in vitro. Hort Environ Biotechnol 54:311–318. https://doi.org/10.1007/s13580-013-0118-7 2013.

    Article  CAS  Google Scholar 

  54. Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B 104:236–257. https://doi.org/10.1016/j.jphotobiol.2010.12.010

    Article  CAS  PubMed  Google Scholar 

  55. Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterise and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisms, regulation and adaptation. Taylor and Francis, London, pp 445–483

    Google Scholar 

  56. Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis. Kluwer Academic Publishers Press, Dordrecht, pp 321–362. https://doi.org/10.1007/978-1-4020-3218-9_12

    Google Scholar 

  57. Tomar RS, Sharma A, Jajoo A (2015) Assessment of phytotoxicity of anthracene in soybean (Glycine max) with a quick method of chlorophyll fluorescence. Plant Biol 17:870–876. https://doi.org/10.1111/plb.12302

    Article  CAS  PubMed  Google Scholar 

  58. Tombesi S, Johnson RS, Day KR, DeJong TM (2010) Relationships between xylem vessel characteristics, calculated axial hydraulic conductance and size-controlling capacity of peach rootstocks. Ann Bot 105:327–331. https://doi.org/10.1093/aob/mcp281

    Article  PubMed  Google Scholar 

  59. Tuna AL, Kaya C, Ashraf M, Altunlu H, Yokas I, Yagmur B (2007) The effects of calcium sulphate on growth, membrane stability and nutrient uptake of tomato plants grown under salt stress. Environ Exp Bot 59:173–178. https://doi.org/10.1016/j.envexpbot.2005.12.007

    Article  CAS  Google Scholar 

  60. Viehmannova I, Cepkova PH, Vitamvas J, Streblova P, Kisilova J (2016) Micropropagation of a giant ornamental bromeliad Puya berteroniana through adventitious shoots and assessment of their genetic stability through ISSR primers and flow cytometry. Plant Cell Tissue Organ Cul 125:293–302. https://doi.org/10.1007/s11240-016-0949-x

    Article  CAS  Google Scholar 

  61. Wang M, Zheng Q, Shen Q, Guo S (2013) The critical role of potassium in plant stress response. Int J Mol Sci 14:7370–7390. https://doi.org/10.3390/ijms14047370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. 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

    Article  CAS  Google Scholar 

  63. Yamaji N, Ma JF (2014) The node, a hub for mineral nutrient distribution in graminaceous plants. Trends Plant Sci 19:556–563. https://doi.org/10.1016/j.tplants.2014.05.007

    Article  CAS  PubMed  Google Scholar 

  64. Yarsi G, Sivaci A, Dasgan Hy, Altuntas O, Binzet R, Akhoundnejad Y (2017) Effects of salinity stress on chlorophyll and carotenoid contents and stomata size of grafted and ungrafted galia c8 melon cultivar. Pak J Bot 49:421–426

    CAS  Google Scholar 

  65. Yusuf MM, Kumar D, Rajwanshi R, Strasser RJ, Tsimilli-Michael M, Govindjee Sarin NB (2010) Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll fluorescence measurements. Biochim Biophys Acta 1797:1428–1438. https://doi.org/10.1016/j.bbabio.2010.02.002

    Article  CAS  PubMed  Google Scholar 

  66. Zhang JH, Guo SJ, Guo PY, Wang X (2014) The interacting effect of urea and fenoxaprop-P-ethyl on photosynthesis and chlorophyll fluorescence in Perilla frutescens. Photosynthetica 52:456–463. https://doi.org/10.1007/s11099-014-0050-9

    Article  CAS  Google Scholar 

  67. Zhang A, Wang H, Shao Q, Xu M, Zhang W, Li M (2015) Large scale in vitro propagation of Anoectochilus roxburghii for commercial application: pharmaceutically important and ornamental plant. Ind Crop Prod 70:158–162. https://doi.org/10.1016/j.indcrop.2015.03.032

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the scholarship awarded by CAPES (Coordination for the Improvement of Higher Education Personnel), CNPq (Brazilian National Council for Scientific and Technological Development) and the FAPES (Espírito Santo State Research Foundation).

Author information

Affiliations

Authors

Contributions

JPRM, LCAR, TSS and ERS conducted experiments. JPRM and LCAR wrote the manuscript and carried out the statistical analysis. ARF and ABPLG provided the structure and conditions to develop the experiments and contributed to the discussion of results. All the authors read and approved the final version of the paper.

Corresponding author

Correspondence to João Paulo Rodrigues Martins.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by Nokwanda Pearl Makunga.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Martins, J.P.R., Rodrigues, L.C.d., Silva, T.d. et al. Sources and concentrations of silicon modulate the physiological and anatomical responses of Aechmea blanchetiana (Bromeliaceae) during in vitro culture. Plant Cell Tiss Organ Cult 137, 397–410 (2019). https://doi.org/10.1007/s11240-019-01579-6

Download citation

Keywords

  • Bromeliad
  • Chlorophyll a fluorescence
  • Plant anatomy
  • Plant physiology
  • Plant tissue culture