Abstract
We investigated the role of organic osmolytes in regulating substomatal apoplast water potential (ψwa) in the leaves of pea (Pisum sativum L.) plants grown under normal or doubled CO2 concentrations exposed to a 3-day drought. The sucrose content, the leading organic osmolyte, was higher in the leaves of drought-stressed plants grown under doubled CO2 concentration than in those grown under normal CO2 concentration. However, the content of proline and reducing sugars (glucose + fructose) was higher in the leaves of plants grown under normal CO2 concentration. Interestingly, the substomatal apoplast ψwa decreased 2-fold under normal CO2 concentration while remaining unchanged under doubled CO2 concentration. Similarity in the decline of ψwa and increase of proline and reducing sugars in leaves under drought indicates their specific role as apoplast osmotic agents that help diminish the turgor of guard cells by lowering ψwa, resulting in stomatal closure and diminish leaf water loss.
Similar content being viewed by others
REFERENCES
Boretti, A. and Florentine, S., Atmospheric CO2 concentration and other limiting factors in the growth of C3 and C4 plants, Plants, 2019, vol. 8, p. 92. https://doi.org/10.3390/plants8040092
Hussain, S., Ulhassan, Z., Brestic, M., Zivcak, M., Zhou, W., Allakhverdiev, S.I., Yang, X., Safdar, M.E., Yang, W., and Liu, W., Photosynthesis research under climate change, Photosynth. Res., 2021, vol. 150, p. 5. https://doi.org/10.1007/s11120-021-00861-z
Dammour, G., Simonneau, Th., Cochard, H., and Urban, L., An overview of models of stomatal conductance at leaf level, Plant, Cell Environ., 2010, vol. 33, p. 1419. https://doi.org/10.1111/j.1365-3040.2010.02181.x
Buckley, T.N., Modelling stomatal conductance, Plant Physiol., 2017, vol. 174, p. 572. https://doi.org/10.1104/pp.16.01772
Farquhar, G.D., Feedforward responses of stomata to humidity, Aust. J. Plant Physiol., 1978, vol. 5, p. 787. https://doi.org/10.1071/PP9780787
Monteith, J.L., A reinterpretation of the stomatal response to humidity, Plant, Cell Environ., 1995, vol. 18, p. 357. https://doi.org/10.1111/j.1365-3040.1995.tb00371.x
Buckley, T.N., The control of stomata by water balance, New Phytol., 2005, vol. 168, p. 275. https://doi.org/10.1111/j.1469-8137.2005.01543.x
Shope, J.C., Peak, D., and Mott, K.A., Stomatal responses to humidity in isolated epidermes, Plant, Cell Environ., 2008, vol. 31, p. 1290. https://doi.org/10.1111/j.1365-3040.2008.01844.x
Mott, K.A., Leaf hydraulic conductivity and stomatal responses to humidity in amphistomatous leaves, Plant, Cell Environ., 2007, vol. 30, p. 1444. https://doi.org/10.1111/j.1365-3040.2007.01720.x
Mott, K.A. and Peak, D., Stomatal responses to humidity and temperature in darkness, Plant, Cell Environ., 2010, vol. 33, p. 1084. https://doi.org/10.1111/j.1365-3040.2010.02129.x
Peak, D. and Mott, K.A., A new, vapor-phase mechanism for stomatal responses to humidity and temperature, Plant, Cell Environ., 2011, vol. 34, p. 162. https://doi.org/10.1111/j.1365-3040.2010.02234.x
Voronin, P.Yu., Rakhmankulova, Z.F., Shuyskaya, E.V., Maevskaya, S.N., Nikolaeva, M.K., Maksimov, A.P., Maximov, T.Chr., Myasoedov, N.A., Balnokin, Yu.V., Rymar, V.P., Valdayskih, V.V., and Kuznetsov, V.V., New method for quantitative determination of water potential of mesophyll cell’ apoplast in substomatal cavity of the leaf, Russ. J. Plant Physiol., 2017, vol. 64, p. 452. https://doi.org/10.1134/S1021443717020133
Ashraf, M. and Harris, P.J.C., Photosynthesis under stressful environments: An overview, Photosynthetica, 2013, vol. 51, p. 163. https://doi.org/10.1007/s11099-013-0021-6
Sharma, A., Kumar, V., Shahzad, B., Ramakrishnan, M., Singh Sidhu, G.P., Bali, A.S., Handa, N., Kapoor, D., Yadav, P., Khanna, K., Bakshi, P., Rehman, A., Kohli, S.K., Khan, E.A., Parihar, R.D., et al., Photosynthetic response of plants under different abiotic stresses: a review, J. Plant Growth Reg., 2020, vol. 39, p. 509. https://doi.org/10.1007/s00344-019-10018-x
Pelleschi, S., Rocher, J.-P., and Prioul, J.-L., Effect of water restriction on carbohydrate metabolism and photosynthesis in mature maize leaves, J. Cell Environ., 1997, vol. 20, p. 493. https://doi.org/10.1046/j.1365-3040.1997.d01-89.x
Nikolaeva, M.K., Maevskaya, S.N., and Voronin, P.Yu., Photosynthetic CO2/H2O gas exchange and dynamics of carbohydrates content in maize leaves under drought, Russ. J. Plant Physiol., 2017, vol. 64, p. 536. https://doi.org/10.1134/S1021443717030116
Malinovsky, A.V., Akanov, E.N., and Voronin, P.Yu., A vegetation climatic unit for studying the impact on higher plants of an increased CO2 concentration in comparison with the atmospheric CO2 concentration, Russ. J. Plant Physiol., 2020, vol. 67, p. 194. https://doi.org/10.1134/S1021443720010112
Bates, L.S., Waldren, R., and Teare, I.D., Rapid determination of free proline for water stress studies, Plant Soil, 1973, vol. 39, p. 205. https://doi.org/10.1007/BF00018060
Heath, R.L. and Packer, L., Photoperoxidation in isolated chloroplasts, Arch. Biochem. Biophys., 1968, vol. 125, p. 180. https://doi.org/10.1016/0003-9861(68)90654-1
Lichtenthaler, H.K., Chlorophyll and carotenoids: pigments of photosynthetic biomembranes, Method. Enzymol., 1987, vol. 148, p. 350. https://doi.org/10.1016/0076-6879(87)48036-1
Turkina, M.B. and Sokolova, S.V., Methods for monosaccharide and oligosaccharide determination, in: Biokhim. Met. v Fiz. Rast., Pavlinova O.A., Ed., Moscow: Nauka, 1971, p. 7.
Voronin, P.Yu., Experimental installation for measurements of chlorophyll fluorescence, CO2 exchange, and transpiration in a detached leaf, Russ. J. Plant Physiol., 2014, vol. 61, p. 269. https://doi.org/10.1134/S1021443714020174
Demmig-Adams, B., Polutchko, S.K., Zenir, M.C., Fourounjian, P., Stewart, J.J., López-Pozo, M., and Adams III, W.W., Intersections: photosynthesis, abiotic stress, and the plant microbiome, Photosynthetica, 2022, vol. 60, p. 59. https://doi.org/10.32615/ps.2021.065
Salazar-Parra, C., Aguirreolea, J., Sánchez-Díaz, M., Irigoyen, J.J., and Morales, F., Photosynthetic response of Tempranillo grapevine to climate change scenarios, Ann. Applied Biology, 2012, vol. 161, p. 277. https://doi.org/10.1111/j.1744-7348.2012.00572.x
Ghosh, U.K., Islam, M.N., Siddiqui, M.N., Cao, X., and Khan, M.A.R., Proline, a multifaceted signalling molecule in plant responses to abiotic stress: understanding the physiological mechanisms, Plant Biol. (Stuttg), 2022, vol. 24, p. 227. https://doi.org/10.1111/plb.13363
Szabados, L. and Savoure, A., Proline: A multifunctional amino acid, Trends Plant Sci., 2010, vol. 15, p. 89. https://doi.org/10.1016/j.tplants.2009.11.009
Sharma, S., Villamor, J.G., and Verslues, P.E., Essential role of tissue-specific proline synthesis and catabolism in growth and redox balance at low water potential, Plant Physiol., 2011, p. 157, p. 292. https://doi.org/10.1104/pp.111.183210
Borawska-Jarmułowicz, B., Mastalerczuk, G., Dąbrowski, P., Kalaji, H.M., and Wytrążek, K., Improving tolerance in seedlings of some Polish varieties of Dactylis glomerata to water deficit by application of simulated drought during seed germination, Photosynthetica, 202, vol. 58, p. 540. https://doi.org/10.32615/ps.2020.007
Voronin, P.Yu., Maevskaya, S.N., and Nikolaeva, M.K., Physiological and molecular responses (Zea mays L.) plants to drought and rehydration, Photosynthetica, 2019, vol. 57, p. 850. https://doi.org/10.32615/ps.2019.101
Scharwies, J.D. and Dinneny, J.R., Water transport, perception, and response in plants, J. Plant Res., 2019, vol. 132, p. 311. https://doi.org/10.1007/s10265-019-01089-8
Sánchez, F.J., Manzanares, M., de Andres, E.F., Tenorio, J.L., and Ayerbe, L., Turgor maintenance, osmotic adjustment and soluble sugar and proline accumulation in 49 pea cultivars in response to water stress, Field Crops Res., 1998, vol. 59, p. 225. https://doi.org/10.1016/S0378-4290(98)00125-7
Takahashi, F., Kuromori, T., Urano, K., Yamaguchi-Shinozaki, K., and Shinozaki, K., Drought stress responses and resistance in plants: From cellular responses to long-distance intercellular communication, Front. Plant Sci., 2020, vol. 11, p. 556972. https://doi.org/10.3389/fpls.2020.556972
Sehgal, A., Sita, K., Siddique, K.H., Kumar, R., Bhogireddy, S., Varshney, R.K., HanumanthaRao, B., Nair, R.M., Prasad, P.V.V., and Nayyar, H., Drought or/and heat-stress effects on seed filling in food crops: impacts on functional biochemistry, seed yields, and nutritional quality, Front. Plant Sci., 2018, vol. 9, p. 1705. https://doi.org/10.3389/fpls.2018.01705
Muhammadkhani, N. and Heidari, R., Drought-induced accumulation of soluble sugars and proline in two maize varieties, World Appl. Sci. J., 2008, vol. 3, p. 448.
Morales, F., Ancín, M., Fakhet, D., González-Torralba, J., Gámez, A.L., Seminario, A., Soba, D., Ben Mariem, S., Garriga, M., and Aranjuelo, I., Photosynthetic metabolism under stressful growth conditions as a bases for crop breeding and yield improvement, Plants, 2020, vol. 9, p. 88. https://doi.org/10.3390/plants9010088
Du, Y., Zhao, Q., Chen, L., Yao, X., Zhang, W., Zhang, B., and Xie, F., Effect of drought stress on sugar metabolism in leaves and roots of soybean seedlings, Plant Physiol. Biochem., 2020, vol. 146, p. 1. https://doi.org/10.1016/j.plaphy.2019.11.003
Sicher, R.C. and Barnaby, J.Y., Impact of carbon dioxide enrichment on the responses maize leaf transcripts and metabolites to water stress, Physiol. Plant., 2012, vol. 144, p. 238. https://doi.org/10.1111/j.1399-3054.2011.01555.x
ACKNOWLEDGMENTS
The authors are grateful to Dr. Nikolaeva M.K. for her help in conducting the biochemical analysis.
Funding
The research was conducted within the state assignment of the Ministry of Science and Higher Education of the Russian Federation (Theme no. 122042700044-6).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants as objects of research.
Additional information
Abbreviations: Car—carotenoids; Chl—chlorophyll; DS—drought-stress; E—transpiration rate; FC—field capacity; FM—fresh mass; Fru—fructose; Glu—glucose; gs—stomatal conductance; LPO—lipid peroxidation; MDA—malondialdehyde; PN—net photosynthetic rate; RH—relative humidity; ROS—reactive oxygen species; Suc—sucrose; ψwa—water potential of mesophyll cells’ apoplast in substomatal cavity.
Rights and permissions
About this article
Cite this article
Voronin, P.Y., Maevskaya, S.N., Malinovsky, A.V. et al. Organic Osmolytes Regulate Substomatal Apoplast Water Potential in Pea (Pisum sativum L.) Leaves during Mild Drought. Russ J Plant Physiol 70, 123 (2023). https://doi.org/10.1134/S1021443723601167
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1134/S1021443723601167