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Ultra- and Mesostructural Response to Salinization in Two Populations of С3–С4 Intermediate Species Sedobassia sedoides

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Abstract

The plants from two populations (P1 and P2) of xero-halophyte Sedobassia sedoides (Pall.) Freitag & G. Kadereit (Chenopodiaceae) with С3–С4 intermediate type of photosynthesis were examined. Morphophysiological parameters were determined: dry biomass of the above-ground organs, maximum quantum yield of photosystem II (PSII), ultra- and mesostructure of the leaf, carbon isotope discrimination (δ13С) in plants grown under normal conditions and exposed to moderate salinization (0 and 200 mM NaCl). By the values of δ13С and efficiency of PSII, we did not detect significant differences between the populations. Under control conditions, the chloroplasts and mitochondria were located in Kranz-like cells of the bundle sheath of both populations in the region adjacent to vascular bundle, which is characteristic of С2 type of photosynthesis (with photorespiratory СО2 concentrating mechanism). P2 plants were notable for a greater volume of Kranz-like cells of the bundle sheath and more numerous, larger chloroplasts and mitochondria than in P1 plants. By structural leaf parameters, P1 plants may be attributed to a proto-Kranz type of photosynthesis (intermediate between С3 and С2 types) and P2 plants to С2 photosynthesis. Under salinization, the accumulation of dry biomass was reduced in both populations but more considerably in P1. The ultrastructure of organelles in both populations showed different responses to salinization, which was especially pronounced in Kranz-like cells of the bundle sheath. In P1 plants, the area of chloroplasts and mitochondria rose, whereas the area and number of chloroplasts under stress did not change in P2 plants but the area and number of mitochondria decreased. In the cells of plants from both populations, signs of degradation were observed (more pronounced in P1 plants); they were shown in chloroplasts twisting and a disturbance of their granal stacking. In P2 plants, Kranz-like cells of the bundle sheath preserved safer organelles but there occurred the cells with complete degradation of a vacuolar type. Thus, intraspecific ultra- and mesostructural differences were detected in plants from two populations of С3–С4 intermediate species S. sedoides, which reflect different stages of development of photorespiratory СО2 concentrating mechanism. Under salinization, the plants from two different populations showed unlike strategies of adaptation on the level of leaf ultra- and mesostructure.

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REFERENCES

  1. Sage, R.F., Sage, T.L., and Kocacinar, F., Photorespiration and the evolution of C4 photosynthesis, Annu. Rev. Plant Biol., 2012, vol. 63, p. 19. https://doi.org/10.1146/annurev-arplant-042811-105511

    Article  PubMed  CAS  Google Scholar 

  2. Rakhmankulova, Z.F., Photorespiration: its role in the productive process and evolution of C4 plants, Russ. J. Plant Physiol., 2018, vol. 65, p. 303.

    Article  CAS  Google Scholar 

  3. Rakhmankulova, Z.F., Shuiskaya, E.V., Voronin, P.Yu., Velivetskaya, T.A., Ignat’ev, A.V., and Usmanov, I.Yu., Comparative study on resistance of C3 and C4 xerohalophytes of the genus Atriplex to water deficit and salinity, Russ. J. Plant Physiol., 2018, vol. 65, p. 250.

    Google Scholar 

  4. Voznesenskaya, E.V., Koteyeva, N.K., Akhani, H., Roalson, E.H., and Edwards, G.E., Structural and physiological analyses in Salsoleae (Chenopodiaceae) indicate multiple transitions among C3, intermediate, and C4 photosynthesis, J. Exp. Bot., 2013, vol. 64, p. 3583. https://doi.org/10.1093/jxb/ert191

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Sage, R.F., Khoshravesh, R., and Sage, T.L., From proto-Kranz to C4 Kranz: building the bridge to C4 photosynthesis, J. Exp. Bot., 2014, vol. 65, p. 3341. https://doi.org/10.1093/jxb/eru180

    Article  PubMed  Google Scholar 

  6. Bauwe, H., Photorespiration: the bridge to C4 photosynthesis, in C4photosynthesis and related CO2 concentrating mechanisms, Advances in Photosynthesis, Raghavendra, A.S. and Sage, R.F., Eds., Heidelberg-Berlin: Springer Verlag, 2011, vol. 32, p. 81.

    Google Scholar 

  7. Alonso-Cantabrana, H. and von Caemmerer, S., Carbon isotope discrimination as a diagnostic tool for C4 photosynthesis in C3–C4 intermediate species, J. Exp. Bot., 2016, vol. 67, p. 3109. https://doi.org/10.1093/jxb/erv555

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Nakamura, N., Iwano, M., Havaux, M., Yokota, A., and Munekage, Y.N., Promotion of cyclic electron transport around photosystem I during the evolution of NADP-malic enzyme-type C photosynthesis in the genus Flaveria, New Phytol., 2013, vol. 199, p. 832. https://doi.org/10.1111/nph.12296

    Article  PubMed  CAS  Google Scholar 

  9. Freitag, H. and Kadereit, G., C3 and C4 leaf anatomy types in Camphorosmeae (Camphorosmoideae, Chenopodiaceae), Plant Syst. Evol., 2014, vol. 300, p. 665. https://doi.org/10.1007/s00606-013-0912-9

    Article  Google Scholar 

  10. Mokronosov, A.T., Ontogeneticheskii aspekt fotosinteza (The Ontogenetic Aspect of Photosynthesis), Moscow: Nauka, 1981.

    Google Scholar 

  11. Lundgren, M.R., Besnard, G., Ripley, B.S., Lehmann, C.E.R., Chatelet, D.S., Kynast, R.G., Namaganda, M., Vorontsova, M.S., Hall, R.C., Elia, J., Osborne, C.P., and Christin, P.A., Photosynthetic innovation broadens the niche within a single species, Ecol. Lett., 2015, vol. 18, p. 1021. https://doi.org/10.1111/ele.12484

    Article  PubMed  Google Scholar 

  12. Shuyskaya, E., Rakhmankulova, Z., Voronin, P., Kuznetsova, N., Biktimerova, G., and Usmanov, I., Salt and osmotic stress tolerance of the C3–C4 xero-halophyte Bassia sedoides from two populations differ in productivity and genetic polymorphism, Acta Physiol. Plant., 2015, vol. 37, p. 236. https://doi.org/10.1007/s11738-015-1981-x

    Article  CAS  Google Scholar 

  13. Rakhmankulova, Z.F., Shuiskaya, E.V., Suyundukov, Ya.T., Usmanov, I.Yu., and Voronin, P.Yu., Different responses of two ecotypes of C3–C4 xero-halophyte Bassiasedoides to osmotic and ionic factors of salt stress, Russ. J. Plant Physiol., 2016, vol. 63, p. 349.

    Article  Google Scholar 

  14. Gupta, B. and Huang, B., Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization, Int. J. Genomics, 2014, vol. 2014, p. 701596. https://doi.org/10.1155/2014/701596

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Kirchhoff, H., Chloroplast ultrastructure in plants, New Phytol., 2019, vol. 223, p. 565. https://doi.org/10.1111/nph.15730

    Article  PubMed  Google Scholar 

  16. Kondadi, A.K., Anand, R., and Reichert, A.S., Functional interplay between cristae biogenesis, mitochondrial dynamics and mitochondrial DNA integrity, Int. J. Mol. Sci., 2019, vol. 20, p. 4311. https://doi.org/10.3390/ijms20174311

    Article  PubMed Central  CAS  Google Scholar 

  17. Bose, J., Munns, R., Shabala, S., Gilliham, M., Pogson, B., and Tyerman, S.D., Chloroplast function and ion regulation in plants growing on saline soils: lessons from halophytes, J. Exp. Bot., 2017, vol. 68, p. 3129. https://doi.org/10.1093/jxb/erx142

    Article  PubMed  CAS  Google Scholar 

  18. Hasan, R., Ohnuki, Y., Kawasaki, M., Taniguchi, M., and Miyake, H., Differential sensitivity of chloroplasts in mesophyll and bundle sheath cells in maize, an NADP-malic enzyme-type C4 plant, to salinity stress, Plant Prod. Sci., 2005, vol. 8, p. 567. https://doi.org/10.1626/pps.8.567

    Article  CAS  Google Scholar 

  19. Mitsuya, S., Kawasaki, M., Taniguchi, M., and Miyake, H., Light dependency of salinity-induced chloroplast degradation, Plant Prod. Sci., 2003, vol. 6, p. 219. https://doi.org/10.1626/pps.6.219

    Article  Google Scholar 

  20. Yamane, K., Oi, T., Enomoto, S., Nakao, T., Arai, S., Miyake, H., and Taniguchi, M., Three-dimensional ultrastructure of chloroplast pockets formed under salinity stress, Plant Cell Environ., 2018, vol. 41, p. 563. https://doi.org/10.1111/pce.13115

    Article  PubMed  CAS  Google Scholar 

  21. Goncharenko, G.G., Padutov, V.E., and Potenko, V.V., Rukovodstvo po issledovaniyu khvoinykh vidov metodom elektroforeticheskogo analiza izofermentov (Manual for the Study of Coniferous Species by Electrophoretic Analysis of Isoferments), Gomel’: Polespechat’, 1989.

  22. Yeh, F.C., Yang, R.C., and Boyle, T., POPGEN, version 1.32. Microsoft Windows-Based Freeware for Population Genetic Analysis, Edmonton: Univ. Alberta/CIFOR, 1999.

    Google Scholar 

  23. Balnokin, Yu.V., Kurkova, E.B., Khalilova, L.A., Myasoedov, N.A., and Yusufov, A.G., Pinocytosis in the root cells of a salt-accumulating halophyte Suaedaa-ltissima and its possible involvement in chloride transport, Russ. J. Plant Physiol., 2007, vol. 54, p. 797.

    Article  Google Scholar 

  24. Mokronosov, A.T., Mesostructure and functional activity of the photosynthetic apparatus, in Mezostruktura i funktsional’naya aktivnost' fotosinteticheskogo apparata (Mesostructure and Functional Activity of the Photosynthetic Apparatus), Sverdlovsk: Ural. Gos. Univ., 1978, p. 5.

    Google Scholar 

  25. Griffiths, H., Weller, G., Toy, L.F., and Dennis, R.J., You’re sove in: bundle sheath physiology, phylogeny and evolution in C3 and C4 plants, Plant Cell Environ., 2013, vol. 36, p. 249.

    Article  CAS  Google Scholar 

  26. Wang, P., Khoshravesh, R., Karki, S., Tapia, R., Balahadia, C., Bandyopadhyay, A., Quick, W.L., Furbank, R., Sage, T.L., and Langdale, J., Re-creation of a key step in the evolutionary switch from C3 to C4 leaf anatomy, Curr. Biol., 2017, vol. 27, p. 3278. https://doi.org/10.1016/j.cub.2017.09.040

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Osborne, C.P. and Sack, L., Evolution of C4 plants: a new hypothesis for an interaction of CO2 and water relations mediated by plant hydraulics, Philos. Trans. R. Soc. Lond. B., 2012, vol. 367, p. 583.

    Article  CAS  Google Scholar 

  28. Gowik, U. and Westhoff, P., The path from C3 to C4 photosynthesis, Plant Physiol., 2011, vol. 155, p. 56. https://doi.org/10.1104/pp.110.165308

    Article  PubMed  CAS  Google Scholar 

  29. Muhaidat, R., Sage, T.L., Frohlich, M.W., Dangler, N.G., and Sage, R.F., Characterization of C3–C4 intermediate species in the genus Heliotropium L. (Boraginaceae): anatomy, ultrastructure and enzyme activity, Plant Cell Environ., 2011, vol. 34, p. 1723.

    Article  CAS  Google Scholar 

  30. Manaa, A., Goussi, R., Derbali, W., Cantamessa, S., Abdelly, C., and Barbato, R., Salinity tolerance of quinoa (Chenopodium quinoa Willd) as assessed by chloroplast ultrastructure and photosynthetic performance, Environ. Exp. Bot., 2019, vol. 162, p. 103. https://doi.org/10.1016/j.envexpbot.2019.02.012

    Article  CAS  Google Scholar 

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Correspondence to Z. F. Rakhmankulova or E. V. Shuyskaya.

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Translated by N. Balakshina

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Rakhmankulova, Z.F., Shuyskaya, E.V., Khalilova, L.A. et al. Ultra- and Mesostructural Response to Salinization in Two Populations of С3–С4 Intermediate Species Sedobassia sedoides. Russ J Plant Physiol 67, 835–844 (2020). https://doi.org/10.1134/S1021443720040135

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