Effects of selenate and red Se-nanoparticles on the photosynthetic apparatus of Nicotiana tabacum
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Selenium (Se) is a natural trace element, which shifts its action in a relatively narrow concentration range from nutritional role to toxicity. Although it has been well established that in plants chloroplasts are among the primary targets, the mechanism of toxicity on photosynthesis is not well understood. Here, we compared selenate and red-allotrope elemental selenium nanoparticles (red nanoSe) in in vitro tobacco cultures to investigate their effects on the structure and functions of the photosynthetic machinery. Selenate at 10 mg/L concentration retarded plant growth; it also led to a decreased chlorophyll content, accompanied with an increase in the carotenoid-to-chlorophyll ratio. Structural examinations of the photosynthetic machinery, using electron microscopy, small-angle neutron scattering and circular dichroism spectroscopy, revealed significant perturbation in the macro-organization of the pigment-protein complexes and sizeable shrinkage in the repeat distance of granum thylakoid membranes. As shown by chlorophyll a fluorescence transient measurements, these changes in the ultrastructure were associated with a significantly diminished photosystem II activity and a reduced performance of the photosynthetic electron transport, and an enhanced capability of non-photochemical quenching. These changes in the structure and function of the photosynthetic apparatus explain, at least in part, the retarded growth of plantlets in the presence of 10 mg/L selenate. In contrast, red nanoSe, even at 100 mg/L and selenate at 1 mg/L, exerted no negative effect on the growth of plantlets and affected only marginally the thylakoid membrane ultrastructure and the photosynthetic functions.
KeywordsChlorophyll fluorescence transients Chloroplast thylakoid membranes Circular dichroism Electron microscopy Nicotiana tabacum Selenate and Se-nanoparticles Small-angle neutron scattering
This research was supported by the “ÚNKP-17-4 New National Excellence Program of the Ministry of Human Capacities” and by grants from the National Research Development and Innovation Office of Hungary (OTKA KH 124985 to GG and GINOP-2.2.1-15-2017-00051 to MF and OTKA NN 114524 to SZT). Zs L-SZ was supported by the European Union and the State of Hungary, co-financed by the European Regional Development Fund in the project of GINOP-2.3.2.-15-2016-00009 ‘ICER’.
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Conflict of interest
The authors declare that there is no kind of conflicts of interest.
- Ayres M, Ayres M Jr, Ayres DL, Santos AS (1998) BioEstat. Versão 1.0, Sociedade Civil Mamirauá, MCT – CNPq. Belém, ParáGoogle Scholar
- De Man JC, Rogosa M, Sharpe ME (1960) A medium for the cultivation of lactobacilli. J Appl Bacteriol 23:30–35Google Scholar
- Demmig-Adams B, Garab G, Adams III WW, Govindjee (2014) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Advances in photosynthesis and respiration, vol 40. Springer, DordrechtGoogle Scholar
- Dobrikova AG, Domonkos I, Sozer O, Laczko-Dobos H, Kis M, Parducz A, Gombos Z, Apostolova EL (2013) Effect of partial or complete elimination of light-harvesting complexes on the surface electric properties and the functions of cyanobacterial photosynthetic membranes. Physiol Plant 147:248–260CrossRefGoogle Scholar
- El-Ramady H, Abdalla N, Alshaal T, El-Henawy A, Faizy SE-DA, Shams SM, Shalaby T, Bayoumi Y, Elhawat N, Shehata S, Sztrik A, Prokisch J, Fári M, Pilon-Smits EAH, Domokos-Szabolcsy E (2015) Selenium and its role in higher plants. In: Lichtfouse E et al (eds) Pollutants in buildings, water and living organisms, environmental chemistry for a sustainable world, vol 7. Springer, Cham, pp 235–296. https://doi.org/10.1007/978-3-319-19276-5_6 CrossRefGoogle Scholar
- Eszenyi P, Sztrik A, Babka B, Prokisch J (2011) Elemental, nano-sized (100–500 nm) selenium production by probiotic lactic acid bacteria. Int J Biosci Biochem Bioinform 1:148–152Google Scholar
- Hurd-Karrer AM (1935) Factors affecting the absorption of selenium from soils by plants. J Agr Res 50:413–427Google Scholar
- Nagy G, Ünnep R, Zsiros O, Tokutsu R, Takizawa K, Porcar L, Moyet L, Petroutsos D, Garab G, Finazzi G, Minagawa J (2014) Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo. Proc Natl Acad Sci USA 111:5042–5047CrossRefGoogle Scholar
- Palomo-Siguero M, Lopez-Heras MI, Camara C, Madrid Y (2015) Accumulation and biotransformation of chitosan-modified selenium nanoparticles in exposed Radish (Raphanus stivus). J Anal At Spectrsc 30:137–1244Google Scholar
- Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394CrossRefGoogle Scholar
- Posselt D, Nagy G, Kirkensgaard JJK, Holm JK, Aagaard TH, Timmins P, Retfalvi E, Rosta L, Kovacs L, Garab G (2012) Small-angle neutron scattering study of the ultrastructure of chloroplast thylakoid membranes—periodicity and structural flexibility of stroma lamellae. Biochim Biophys Acta 1817:1220–1228CrossRefGoogle Scholar
- Ünnep R, Zsiros O, Solymosi K, Kovács L, Lambrev PH, Tóth T, Schweins R, Posselt D, Székely NK, Rosta L, Nagy G, Garab G (2014b) The ultrastructure and flexibility of thylakoid membranes in leaves and isolated chloroplasts as revealed by small-angle neutron scattering. Biochim Biophys Acta 1837:1572–1580CrossRefGoogle Scholar
- Valdez Barillas JR, Quinn CF, Freeman JL, Lindblom SD, Fakra SC, Marcus MA, Gilligan TM, Alford ÉR, Wangeline AL, Pilon-Smits EAH (2012) Selenium distribution and speciation in the hyperaccumulator Astragalus bisulcatus and associated ecological partners. Plant Physiol 159:1834–1844CrossRefGoogle Scholar
- van Hoewyk D, Takahashi H, Inoue E, Hess A, Tamaoki M, Pilon-Smits EAH (2008) Transcriptome analyses give insights into selenium-stress responses and selenium tolerance mechanisms in Arabidopsis. Physiol Plant 132:236–253Google Scholar
- White PJ (2016) Selenium accumulation by plants. Ann Bot 117(2):217–235Google Scholar