Comparative Analysis of Mesophyll and Bundle Sheath Chloroplasts from Maize Plants Subjected to Salt Stress
- Авторлар: Alieva N.K.1, Alieva D.R.1, Suleymanov S.Y.1, Rzayev F.H.2, Gasimov E.K.2, Huseynova I.M.1
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Мекемелер:
- Institute of Molecular Biology & Biotechnologies
- Azerbaijan Medical University
- Шығарылым: Том 90, № 4 (2025)
- Беттер: 580-592
- Бөлім: Articles
- URL: https://kazanmedjournal.ru/0320-9725/article/view/685818
- DOI: https://doi.org/10.31857/S0320972525040076
- EDN: https://elibrary.ru/IIALEG
- ID: 685818
Дәйексөз келтіру
Аннотация
The effect of salt stress was studied in mesophyll (M) and bundle sheath (BS) chloroplasts of maize plants treated with NaCl for 5 days. Pigment content, chlorophyll fluorescence at 77 K, activity of photosystems (PS) I and II, polypeptide compositions and ultrastructure of the thylakoid membranes were determined in plants grown under different salinity conditions (0, 100, 200, and 250 mM NaCl). The salt treatment caused a decrease in fluorescence, photochemical activity of PSII and PSI, as well as the protein content of the thylakoids. At high salt concentrations, the F735/F686 nm fluorescence ratio in M chloroplasts was reduced, while it was stimulated in BS chloroplasts. The photochemical activity of PSII was reduced in both chloroplasts, while there was no statistically significant difference in the activity of PSI compared to the control. According to the analysis of the protein content of the thylakoid membranes of M and BS chloroplasts, polypeptides belonging to the core antenna of PSII (47 kDa and 43 kDa) and LHCII (28-24 kDa) were present in both types of membranes, but their intensity was weak in BS thylakoids. The synthesis of the 68 kDa apoprotein belonging to the core of PSI was inhibited in the M membranes. There was no noticeable change in the membrane system of BS thylakoids. Salt stress had a greater impact on the ultrastructure of M chloroplasts than on BS ones and caused the formation of granal stacking in BS chloroplast. These results may indicate different responses of the two chloroplast types to salt stress.
Толық мәтін

Авторлар туралы
N. Alieva
Institute of Molecular Biology & Biotechnologies
Хат алмасуға жауапты Автор.
Email: irada.huseynova@science.az
Әзірбайжан, Baku
D. Alieva
Institute of Molecular Biology & Biotechnologies
Email: irada.huseynova@science.az
Әзірбайжан, Baku
S. Suleymanov
Institute of Molecular Biology & Biotechnologies
Email: irada.huseynova@science.az
Әзірбайжан, Baku
F. Rzayev
Azerbaijan Medical University
Email: irada.huseynova@science.az
Әзірбайжан, Baku
E. Gasimov
Azerbaijan Medical University
Email: irada.huseynova@science.az
Әзірбайжан, Baku
I. Huseynova
Institute of Molecular Biology & Biotechnologies
Email: irada.huseynova@science.az
Әзірбайжан, Baku
Әдебиет тізімі
- Stefanov, M., Biswal, A. K., Misra, M., Misra, A. N., and Apostolova, E. L. (2019) Responses of photosynthetic apparatus to salt stress: Structure, function, and protection, in: Handbook of Plant and Crop Stress, 4th Edn., p. 233-250, CRC Press, https://doi.org/10.1201/9781351104609-13.
- Podolec, R., Demarsy, E., and Ulm, R. (2021) Perception and signaling of ultraviolet-B radiation in plants, Annu. Rev. Plant Biol., 72, 793-822, https://doi.org/10.1146/annurev-arplant-050718-095946.
- Aliyeva, N. K., Aliyeva, D. R., Suleymanov, S. Y., Rzayev, F. H., Gasimov, E. K., and Huseynova, I. M. (2020) Biochemical properties and ultrastructure of mesophyll and bundle sheath thylakoids from maize (Zea mays) chloroplasts, Func. Plant Biol., 47, 970-976, https://doi.org/10.1071/FP20004.
- Aliyeva, D. R., Gurbanova, U. A., Rzayev, F. H., Gasimov, E. K., and Huseynova, I. M. (2023) Biochemical and ultrastructural changes in wheat plants during drought stress, Biochemistry (Moscow), 88, 1944-1955, https://doi.org/10.1134/S0006297923110226.
- Soni, A., Dhakar, S., and Kumar, N. (2017) Mechanisms and strategies for improving salinity tolerance in fruit crops, IJCMAS, 6, 1917-1924, https://doi.org/10.20546/ijcmas.2017.603.226.
- Jiang, Z., Song, G., Shan, X., Wei, Z., Liu, Y., Jiang, C., and Li, Y. (2018) Association analysis and identification of ZmHKT1;5 variation with salt-stress tolerance, Front. Plant Sci., 9, 1485, https://doi.org/10.3389/fpls. 2018.01485.
- Hameed, M. A., Ali, N. S., and Karim, H. M. (2023) Tolerance of two sorghum varieties to salinity using different nutritional practices and two leaching requirements, IOP Conference Ser. Earth Environ. Sci., 1262, 082024, https://doi.org/10.1088/1755-1315/1262/8/082024.
- Fang, L. L., Liu, Y. J., Wang, Z. H., Lu, X. Y., Li, J. H., and Yang, Ch. X. (2023) Electrical conductivity and pH are two of the main factors influencing the composition of arbuscular mycorrhizal fungal communities in the vegetation succession series of songnen saline-alkali grassland, J. Fungi, 9, 870, https://doi.org/10.3390/jof9090870.
- Amunts, A., Drory, O., and Nelson, N. (2007) The structure of a plant photosystem I supercomplex at 3.4 Å resolution, Nature, 447, 58-63, https://doi.org/10.1038/nature05687.
- Faryal, S., Ullah, R., Khan, M. N., Ali, B., Hafeez, A., Jaremko, M., and Qureshi, K. A. (2022) Thiourea-capped nanoapatites amplify osmotic stress tolerance in Zea mays L. by conserving photosynthetic pigments, osmolytes biosynthesis and antioxidant biosystems, Molecules, 27, 5744, https://doi.org/10.3390/molecules27185744.
- Hasegawa, P. M., Bressan, R. A., Zhu, J. K., and Bohnert, H. J. (2000) Plant cellular and molecular responses to high salinity, Annu. Rev. Plant Biol., 51, 463-499, https://doi.org/10.1146/annurev.arplant.51.1.463.
- Kan, X., Ren, J., Chen, T., Cui, M., Li, C., Zhou, R., and Yin, Z. (2017) Effects of salinity on photosynthesis in maize probed by prompt fluorescence, delayed fluorescence and P700 signals, Environ. Exp. Bot., 140, 56-64, https://doi.org/10.1016/j.envexpbot.2017.05.019.
- Basu, S., Kumar, A., Benazir, I., and Kumar, G. (2021) Reassessing the role of ion homeostasis for improving salinity tolerance in crop plants, Physiol. Plant., 171, 502-519, https://doi.org/10.1111/ppl.13112.
- Sharma, P., Jha, A. B., Dubey, R. S., and Pessarakli, M. (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions, J. Bot., 2012, 217037, https://doi.org/10.1155/2012/217037.
- Aliyeva, D. R., Aydinli, L. M., Zulfugarov, I. S., and Huseynova, I. M. (2020) Diurnal changes of the ascorbate-glutathione cycle components in wheat genotypes exposed to drought, Funct. Plant Biol., 47, 998-1006, https://doi.org/10.1071/FP19375.
- Maury, G. L., Méndez Rodríguez, D., Hendrix, S., Escalona Arranz, J. C., Fung Boix, Y., Pacheco, A. O., and Cuypers, A. (2020) Antioxidants in plants: a valorization potential emphasizing the need for the conservation of plant biodiversity in Cuba, Antioxidants, 9, 1048, https://doi.org/10.3390/antiox9111048.
- Shannon, M. C. (1993) Development of salt stress tolerance-screening and selection systems for genetic improvement, in: Workshop on Adaptation of Plants to Soil Stresses (Maranville, J. W., Baligar, B. V., Duncan, R. R., and Yohe, J. M., eds), pp. 117-132.
- Massange-Sánchez, J. A., Sánchez-Hernández, C. V., Hernández-Herrera, R. M., and Palmeros-Suárez, P. A. (2021) The biochemical mechanisms of salt tolerance in plants, J. Plant Stress Physiol. Perspect. Agricult., 1-24, https://doi.org/10.5772/intechopen.101048.
- Borisova-Mubarakshina, M. M., Vetoshkina, D. V., Naydov, I. A., Rudenko, N. N., Zhurikova, E. M., Balashov, N. V., and Ivanov, B. N. (2020) Regulation of the size of photosystem II light harvesting antenna represents a universal mechanism of higher plant acclimation to stress conditions, Funct. Plant Biol., 47, 959-969, https://doi.org/10.1071/FP19362.
- Sozharajan, R., and Natarajan, S. (2016) Influence of NaCl salinity on plant growth and nutrient assimilation of Zea mays L., J. Adv. Acad. Res., 1, 54-61, https://doi.org/10.21839/jaar.2016.v1i1.16.
- Belous, O., Klemeshova, K., and Malyarovskaya, V. (2018) Photosynthetic pigments of subtropical plants, in: Photosynthesis – From Its Evolution to Future Improvements in Photosynthetic Efficiency Using Nanomaterials, Intech Open Limited, London, UK, pp. 31-52, https://doi.org/10.5772/intechopen.75193.
- Sharma, A., Kumar, V., Shahzad, B., Ramakrishnan, M., Singh Sidhu, G. P., Bali, A. S., and Zheng, B. (2020) Photosynthetic response of plants under different abiotic stresses: a review, J. Plant Growth Regul., 39, 509-531, https://doi.org/10.1007/s00344-019-10018-x.
- Misra, A. N., Latowski, D., and Strzalka, K. (2006) The xanthophyll cycle activity in kidney bean and cabbage leaves under salinity stress, Russ. J. Plant Physiol., 53, 102-109, https://doi.org/10.1134/S1021443706010134.
- Jusovic, M., Velitchkova, M. Y., Misheva, S. P., Börner, A., Apostolova, E. L., and Dobrikova, A. G. (2018) Photosynthetic responses of a wheat mutant (Rht-B1c) with altered DELLA proteins to salt stress, J. Plant Growth Regul., 37, 645-656, https://doi.org/10.1007/s00344-017-9764-9.
- Srivastava, S., and Sharma, P. K. (2021) Effect of NaCl on chlorophyll fluorescence and thylakoid membrane proteins in leaves of salt sensitive and tolerant rice (Oryza sativa L) varieties, J. Stress Physiol. Biochem., 17, 35-44.
- Wang, X., Chen, Z., and Sui, N. (2024) Sensitivity and responses of chloroplasts to salt stress in plants, Front. Plant Sci., 15, 1374086, https://doi.org/10.3389/fpls.2024.1374086.
- Murata, N., Mohanty, P. S., Hayashi, H., and Papageorgiou, G. C. (1992) Glycinebetaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen-evolving complex, FEBS Lett., 296, 187-189, https://doi.org/10.1016/0014-5793(92)80376-R.
- Hatch, M. D. (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure, Biochim. Biophys. Acta, 895, 81-106, https://doi.org/10.1016/S0304-4173(87)80009-5.
- Hibberd, J. M., Sheehy, J. E., and Langdale, J. A. (2008) Using C4 photosynthesis to increase the yield of rice-rationale and feasibility, Curr. Opin. Plant Biol., 11, 228-231, https://doi.org/10.1016/j.pbi.2007.11.002.
- Kirchhoff, H., Sharpe, R. M., Herbstova, M., Yarbrough, R., and Edwards, G. E. (2013) Differential mobility of pigment-protein complexes in granal and agranal thylakoid membranes of C3 and C4 plants, Plant Physiol., 161, 497-507, https://doi.org/10.1104/pp.112.207548.
- Farooq, M., Hussain, M., Wakeel, A., and Siddique, K. H. (2015) Salt stress in maize: effects, resistance mechanisms, and management. A review, Agron. Sustain. Dev., 35, 461-481, https://doi.org/10.1007/s13593-015-0287-0.
- Raza, A., Ashraf, F., Zou, X., Zhang, X., and Tosif, H. (2020) Plant adaptation and tolerance to environmental stresses: mechanisms and perspectives, in Plant Ecophysiology and Adaptation under Climate Change: Mechanisms and Perspectives I: General Consequences and Plant Responses, pp. 117-145, https://doi.org/10.1007/978-981-15-2156-0_5.
- Meierhoff, K., and Westhoff, P. (1993) Differential biogenesis of photosystem II in mesophyll and bundle-sheath cells of monocotyledonous NADP-malic enzyme-type C4 plants: the non-stoichiometric abundance of the subunits of photosystem II in the bundle-sheath chloroplasts and the translational activity of the plastome-encoded genes, Planta, 191, 23-33, https://doi.org/10.1007/BF00240892.
- Malkin, R., and Niyogi, K. (2000) Photosynthesis, in: Biochemistry and Molecular Biology of Plants (Buchanan, B. B., Gruissem, W., and Jones, R. L., eds.), pp. 568-628, ASPP, Rockville, MD.
- Gardeström, P., and Edwards, G. E. (1983) Isolation of mitochondria from leaf tissue of Panicum miliaceum, a NAD-malic enzyme type C4 plant, Plant Physiol., 71, 24-29, https://doi.org/10.1104/pp.71.1.24.
- Scheibe, R., and Stitt, M. (1988) Comparison of NADP-malate dehydrogenase activation, QA reduction and O2 evolution in spinach leaves, Plant Physiol. Biochem., 26, 473-481.
- Du, Y.-C., Nose, A., Kawamitsu, Y., Murayama, S., Wasano, K., and Uchida, Y. (1996) An improved spectrophotometric determination of the activity of ribulose 1,5-bishosphate carboxylase, Japan. J. Crop Sci., 65, 714-721, https://doi.org/10.1626/jcs.65.714.
- Rogowski, P., Wasilewska-Dębowska, W., Krupnik, T., Drożak, A., Zienkiewicz, M., Krysiak, M., and Romanowska, E. (2019) Photosynthesis and organization of maize mesophyll and bundle sheath thylakoids of plants grown in various light intensities, Environ. Exp. Bot., 162, 72-86, https://doi.org/10.1016/j.envexpbot.2019.02.006.
- Porra, R. J., Thompson, W. A., and Kriedemann, P. E. (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 Bioenerg., 975, 384-394, https://doi.org/10.1016/S0005-2728(89)80347-0.
- Laemmli, V. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 227, 680-685, https://doi.org/10.1038/227680a0.
- Huseynova, I. M., Suleymanov, S. Y., Rustamova, S. M., and Aliyev, J. A. (2009) Drought-induced changes in photosynthetic membranes of two wheat (Triticum aestivum L.) cultivars, Biochemistry (Moscow), 74, 903-909, https://doi.org/ 10.1134/S0006297909080124.
- Strasser, R. J., Tsimilli-Michael, M., Srivastava, A. (2004) Analysis of the chlorophyll a fluorescence transient, In: Chlorophyll a Fluorescence: A Signature of Photosynthesis, pp. 321-362, Dordrecht, Springer, Netherlands, https://doi.org/10.1007/978-1-4020-3218-9_12.
- Shevela, D., Do, H. N., Fantuzzi, A., Rutherford, A. W., and Messinger, J. (2020) Bicarbonate-mediated CO2 formation on both sides of photosystem II, Biochemistry, 59, 2442-2449, https://doi.org/10.1021/acs.biochem.0c00208.
- Kuo, J. (2014) Electron Microscopy: Methods and Protocols, Totowa, Humana Press, 799 p., https://doi.org/10.1007/ 978-1-62703-776-1.
- Hernández, J. A., and Almansa, M. S. (2002) Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves, Physiol. Plant., 115, 251-257, https://doi.org/10.1034/j.1399-3054.2002.1150211.x.
- Omoto, E., Kawasaki, M., Taniguchi, M., and Miyake, H. (2009) Salinity induces granal development in bundle sheath chloroplasts of NADP-malic enzyme type C4 plants, Plant Prod. Sci., 12, 199-207, https://doi.org/10.1626/pps.12.199.
- Romanowska, E., Kargul, J., Powikrowska, M., Finazzi, G., Nield, J., Drozak, A., and Pokorska, B. (2008) Structural organization of photosynthetic apparatus in agranal chloroplasts of maize, J. Biol. Chem., 283, 26037-26046, https://doi.org/10.1074/jbc.M803711200.
- Romanowska, E., Buczyńska, A., Wasilewska, W., Krupnik, T., Drożak, A., Rogowski, P., and Zienkiewicz, M. (2017) Differences in photosynthetic responses of NADP-ME type C4 species to high light, Planta, 245, 641-657, https://doi.org/10.1007/s00425-016-2632-1.
- Retta, M. A., Yin, X., Ho, Q. T., Watté, R., Berghuijs, H. N. C., Verboven, P., Saeys, W., Cano, F. J., Ghannoum, O., Struik, P. C., and Nicolaï, B. M. (2023) The role of chloroplast movement in C4 photosynthesis: a theoretical analysis using a three-dimensional reaction–diffusion model for maize, J. Exp. Bot., 74, 4125-4142, https://doi.org/10.1093/jxb/erad138.
- Perveen, S., Shahbaz, M., and Ashraf, M. (2010) Regulation in gas exchange and quantum yield of photosystem II (PSII) in salt-stressed and non-stressed wheat plants raised from seed treated with triacontanol, Pak. J. Bot., 42, 3073-3081.
- Manai, J., Kalai, T., Gouia, H., and Corpas, F. J. (2014) Exogenous nitric oxide (NO) ameliorates salinity-induced oxidative stress in tomato (Solanum lycopersicum) plants, J. Soil Sci. Plant Nutr., 14, 433-446, https://doi.org/10.4067/S0718-95162014005000034.
- Subramanyam, R., Jolley, C., Thangaraj, B., Nellaepalli, S., Webber, A. N., and Fromme, P. (2010) Structural and functional changes of PSI-LHCI supercomplexes of Chlamydomonas reinhardtii cells grown under high salt conditions, Planta, 231, 913-922, https://doi.org/10.1007/s00425-009-1097-x.
- Shu, S., Guo, S. R., Sun, J., Yuan, L.Y. (2012) Effects of salt stress on the structure and function of the photosynthetic apparatus in Cucumis sativus and its protection by exogenous putrescine, Physiol. Plant., 146, 285-296, https://doi.org/10.1111/j.1399-3054.2012.01623.x.
- Stefanov, M. A., Rashkov, G. D., Yotsova, E. K., Borisova, P. B., Dobrikova, A. G., and Apostolova, E. L. (2023) Protective effects of sodium nitroprusside on photosynthetic performance of Sorghum bicolor L. under salt stress, Plants, 12, 832, https://doi.org/10.3390/plants12040832.
- Pan, T., Liu, M., Kreslavski, V. D., Zharmukhamedov, S. K., Nie, C., Yu, M., and Shabala, S. (2021) Non-stomatal limitation of photosynthesis by soil salinity, Crit. Rev. Environ. Sci. Techno., 51, 791-825, https://doi.org/10.1080/10643389.2020.1735231.
- Aro, E. M., McCaffery, S., and Anderson, J. M. (1993) Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances, Plant Physiol., 103, 835-843, https://doi.org/10.1104/pp.103.3.835.
- Allakhverdiev, S. I., and Murata, N. (2008) Salt stress inhibits photosystems II and I in cyanobacteria, Photosynth. Res., 98, 529-539, https://doi.org/10.1007/s11120-008-9334-x.
- Hasan, R., Kawasaki, M., Taniguchi, M., and Miyake, H. (2006) Salinity stress induces granal development in bundle sheath chloroplasts of maize, an NADP-malic enzyme-type C4 plant, Plant Prod. Sci., 9, 256-265, https://doi.org/10.1626/pps.9.256.
- Omoto, E., Taniguchi, M., Miyake, H. (2010) Effects of salinity stress on the structure of bundle sheath and mesophyll chloroplasts in NAD-malic enzyme and PCK type C4 plants, Plant Prod. Sci., 13, 169-176, https://doi.org/10.1626/pps.13.169.
- Zahra, N., Al Hinai, M. S., Hafeez, M. B., Rehman, A., Wahid, A., Siddique, K. H. M., et al. (2022) Regulation of photosynthesis under salt stress and associated tolerance mechanisms, Plant Physiol. Biochem., 178, 55-69, https://doi.org/10.1016/j.plaphy.2022.03.003.
- Rozak, P. R., Seiser, R. M., Wacholtz, W. F., and Wise, R. R. (2002) Rapid, reversible alterations in spinach thylakoid appression upon changes in light intensity, Plant Cell Environ., 25, 421-429, https://doi.org/10.1046/ j.0016-8025.2001.00823.x.
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