Plant Soil Environ., 2026, 72(1):49-65 | DOI: 10.17221/564/2025-PSE
Decoupling of stomatal and mesophyll recovery drives photosynthetic resilience to water deficit in sugar beet: evidence from multiscale structural and functional traitsOriginal Paper
- 1 School of Agricultural Sciences, Zhengzhou University, Zhengzhou, Henan, P.R. China
- 2 Agricultural College, Shihezi University, Shihezi, Xinjiang, P.R. China
- 3 Institute for Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, P.R. China
Water deficit severely constrains sugar beet productivity by impairing photosynthetic capacity. However, the underlying structure-function mechanisms conferring photosynthetic resilience remain poorly characterised. This study investigates the temporal dynamics of photosynthetic limitations and structural adaptations in sugar beet during water deficit and subsequent rehydration. We found that water deficit significantly reduced the maximum net CO2 assimilation rate (ANmax) and the Rubisco carboxylation rate (Vcmax) by impairing CO2 diffusion and biochemical processes. The reduction in photosynthetic capacity is primarily and stably attributed to mesophyll limitation, while contributions from stomatal and biochemical limitations flexibly change with deficit degree and rehydration. Severe water deficit caused irreversible structural damage that hinders recovery even after rehydration, while moderate water deficit allows partial restoration of leaf and chloroplast function. Partial least squares structural equation modelling (PLS-SEM) demonstrated that CO2 diffusion was governed by the volume fraction of intercellular air space (fias, β = 0.28) and surface areas of the chloroplasts exposed to leaf intercellular air spaces (Sc/S, β = 0.35), with Sc/S indirectly influencing mesophyll conductance (gm) through fias mediation (β = 0.53). Severe water deficit caused irreversible fias reduction and chloroplast interface damage (59% cell volume loss). These findings establish that resilience to water deficit in sugar beet depends on mesophyll structural integrity, with fias and Sc/S as key modulators of gm recovery. The study advances understanding of stress recovery mechanisms in sugar beet and provides a framework for multiscale crop improvement in the context of climate change.
Keywords: sugar crop; stress condition; drought; chlorophyll; leaf thickness; chloroplast ultrastructure
Received: December 15, 2025; Revised: January 13, 2026; Accepted: January 15, 2026; Prepublished online: January 27, 2026; Published: January 29, 2026 Show citation
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References
- Aneja P., Sanyal R., Ranjan A. (2025): Leaf growth in third dimension: a perspective of leaf thickness from genetic regulation to ecophysiology. New Phytologist, 245: 989-999.
Go to original source...
Go to PubMed... - Barratt G.E., Sparkes D.L., McAusland L., Murchie E.H. (2020): Anisohydric sugar beet rapidly responds to light to optimize leaf water use efficiency utilizing numerous small stomata. AoB PLANTS, 13: plaa067.
Go to original source... - Bloch D., Hoffmann C.M., Märländer B. (2006): Impact of water supply on photosynthesis, water use and carbon isotope discrimination of sugar beet genotypes. European Journal of Agronomy, 24: 218-225.
Go to original source... - Brown K.F., Messem A., Dunham R., Biscoe P. (1987): Effect of drought on growth and water use of sugar beet. The Journal of Agricultural Science, 109: 421-435.
Go to original source... - Charuvi D., Nevo R., Aviv-Sharon E., Gal A., Kiss V., Shimoni E., Farrant J.M., Kirchhoff H., Reich Z. (2018): Chloroplast breakdown during dehydration of a homoiochlorophyllous resurrection plant proceeds via senescence-like processes. Environmental and Experimental Botany, 157: 100-111.
Go to original source... - Chaves M.M., Flexas J., Pinheiro C. (2009): Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany, 103: 551-560.
Go to original source...
Go to PubMed... - Cosgrove D.J. (2016): Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes. Jour-nal of Experimental Botany, 67: 463-476.
Go to original source...
Go to PubMed... - Cosgrove D.J. (2022): Building an extensible cell wall. Plant Physiology, 189: 1246-1277.
Go to original source...
Go to PubMed... - Dohm J.C., Minoche A.E., Holtgräwe D., Capella-Gutiérrez S., Zakrzewski F., Tafer H., Rupp O., Sörensen T.R., Stracke R., Reinhardt R. (2014): The genome of the recently domesticated crop plant sugar beet (Beta vulgaris). Nature, 505: 546-549.
Go to original source...
Go to PubMed... - Evans J.R., Caemmerer S.V., Setchell B.A., Hudson G.S. (1994): The relationship between CO2 transfer conductance and leaf anatomy in transgenic tobacco with a reduced content of Rubisco. Australian Journal of Plant Physiology, 21: 475-495.
Go to original source... - Farquhar G.D., Caemmerer S.V., Berry J.A. (1980): A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta, 149: 78-90.
Go to original source...
Go to PubMed... - Fitters T.F., Mooney S.J., Sparkes D.L. (2022): Impact of water availability on root growth of sugar beet varieties. Soil Use and Management, 38: 1033-1043.
Go to original source... - Flexas J., Barbour M.M., Brendel O., Cabrera H.M., Carriquí M., Diaz-Espejo A., Douthe C., Dreyer E., Ferrio J., Juan P., Galle A., Galmés J., Kodama N., Medrano H., Niinemets Ü., Peguero Pina J.J., Pou A., Ribas-Carbo M., Tomas M., Tosens T., Warren C.R. (2012): Mesophyll diffusion conductance to CO2: an unappreci-ated central player in photosynthesis. Plant Science (Amsterdam, Netherlands), 193: 70-84.
Go to original source...
Go to PubMed... - Flexas J., Carriquí M. (2020): Photosynthesis and photosynthetic efficiencies along the terrestrial plant's phylogeny: lessons for improving crop photosynthesis. The Plant Journal, 101: 964-978.
Go to original source...
Go to PubMed... - Flexas J., Fernie A., Usadel B., Alonso-Forn D., Ardiles V., Ball M., Ballesteros D., Bravo L., Brodribb T., Carriquí M., Castanyer-Mallol F., Cavieres L., Chondol T., Clemente-Moreno M., Coopman R., Corcuera L., De Vries J., Diaz-Espejo A., Dolezal J., Ergo V., Fernández H., Fernández-Marín B., Galmes J., García-Plazaola J., Quintanilla L., Gulías J., Hernández A., Luo K1, Martínez-Abaigar J., Nadal M., Niinemets Ü., Núñez-Olivera M., Ostria-Gallardo E., Perera, Castro A., Pérez-López U., Ribas-Carbo M., Roig-Oliver M., Rojas R., Sáez P., Tosens T., Viveros R., Xiong D., Yan J., Zhang Y., Gago J. (2025): What can we learn from the eco-physiology of plants inhabiting extreme environment. Journal of Experimental Botany, 76: eraf236.
Go to original source...
Go to PubMed... - Flexas J., Matilde B., Josefina B., Jean-Marc D., Alexander G., Jeroni G., Miguel J., Alícia P., Miquel R.-C., Carlota S. (2009): Photosynthesis limitations during water stress acclimation and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandieri × V. rupestris). Journal of Experimental Botany, 60: 2361-2377.
Go to original source...
Go to PubMed... - Galle A., Florez-Sarasa I., Tomas M., Pou A., Medrano H., Ribas-Carbo M., Flexas J. (2009): The role of mesophyll conductance during water stress and recovery in tobacco (Nicotiana sylvestris): acclimation or limitation? Journal of Experimental Botany, 60: 2379-2390.
Go to original source...
Go to PubMed... - Ghaffari H., Tadayon M.R., Bahador M., Razmjoo J. (2021): Investigation of the proline role in controlling traits related to sugar and root yield of sugar beet under water deficit conditions. Agricultural Water Management, 243: 106448.
Go to original source... - Gowacka K., Kromdijk J., Salesse-Smith C.E., Smith C., Driever S.M., Long S.P. (2023): Is chloroplast size optimal for photosynthetic efficiency? New Phytologist, 239: 2197-2211.
Go to original source...
Go to PubMed... - Grassi G., Magnani F. (2005): Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. Plant Cell and Environment, 28: 834-849.
Go to original source... - Hair J.F., Hult G.T.M., Ringle C.M., Sarstedt M. (2022): A Primer on Partial Least Squares Structural Equation Modeling (PLS-SEM). 3rd Edition. Sage, Thousand Oaks.
Go to original source... - Harley P.C., Loreto F., Di Marco G., Sharkey T.D. (1992): Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiology, 98: 1429-1436.
Go to original source...
Go to PubMed... - Kim J.Y., Ahn J., Bong H., Wada M., Kong S.G. (2020): ACTIN2 functions in chloroplast photorelocation movement in Arabidopsis thaliana. Journal of Plant Biology, 63: 379-389.
Go to original source... - Lodeyro A.F., Krapp A.R., Néstor C. (2021): Photosynthesis and chloroplast redox signaling in the age of global warming: stress tolerance, acclimation and devel-opmental plasticity. Journal of Experimental Botany, 72: 5919-5937.
Go to original source...
Go to PubMed... - Moustakas M., Sperdouli I., Moustaka J. (2022): Early drought stress warning in plants: color pictures of photosystem II photochemistry. Climate, 10: 179.
Go to original source... - Nagy-Deri H., Péli E.R., Georgieva K., Tuba Z. (2011): Changes in chloroplast morphology of different parenchyma cells in leaves of Haberlea rhodopensis Friv. during desiccation and following rehydration. Photosynthetica, 49: 119-126.
Go to original source... - Niinemets Ü., Reichstein M. (2003): Controls on the emission of plant volatiles through stomata: a sensitivity analysis. Journal of Geophysical Research: Atmos-pheres, 108: SOS 5-1-SOS 3-11.
Go to original source... - Onoda Y., Wright I.J., Evans J.R., Hikosaka K., Kitajima K., Niinemets Ü., Poorter H., Tosens T., Westoby M. (2017): Physiological and structural tradeoffs underly-ing the leaf economics spectrum. New Phytologist, 214: 1447-1463.
Go to original source...
Go to PubMed... - Rachana O., Takao O., Daisuke S., Mitsutaka T. (2024): Structural changes of mesophyll cells in the rice leaf tissue in response to salinity stress based on the three-dimensional analysis. AoB PLANTS, 16: plae016.
Go to original source... - Ruehr N.K., Rüdiger G., Stefan M., Almut A. (2019): Beyond the extreme: recovery of carbon and water relations in woody plants following heat and drought stress. Tree Physiology, 39: 1285-1299.
Go to original source...
Go to PubMed... - Sagardoy R., Vázquez S., Florez-Sarasa I., Albacete A., Ribas-Carbó M., Flexas J., Abadía J., Morales F. (2010): Stomatal and mesophyll conductances to CO2 are the main limitations to photosynthesis in sugar beet (Beta vulgaris) plants grown with excess zinc. New Phytologist, 187: 145-158.
Go to original source...
Go to PubMed... - Sahin U., Ors S., Kiziloglu F.M., Kuslu Y. (2014): Evaluation of water use and yield responses of drip-irrigated sugar beet with different irrigation techniques. Chile-an Journal of Agricultural Research, 74: 302-310.
Go to original source... - Shaaban A., Abdou N.M., Elmageed T.A.A., Semida W.M., Tawwab A.R.A.E., Mohamed G.F., Mohamed M.S., Elsaadony M.T., El-Tarabily K.A., Abuqamar S.F. (2025): Foliar fertilization with potassium silicate enhances water productivity and drought resilience in sugar beet. Field Crops Research, 326: 109840.
Go to original source... - Shang B., Zang Y., Zhao X., Zhu J., Zhang X. (2018): Functional characterization of GhPHOT2 in chloroplast avoidance of Gossypium hirsutum. Plant Physiology and Biochemistry, 135: 51-60.
Go to original source...
Go to PubMed... - Sharkey T.D. (2016): What gas exchange data can tell us about photosynthesis. Plant Cell and Environment, 39: 1161-1163.
Go to original source...
Go to PubMed... - Syvertsen J.P., Lloyd J., McConchie C., Kriedemann P.E., Farquhar G.D. (1995): On the relationship between leaf anatomy and CO2 diffusion through the meso-phyll of hypostomatous leaves. Plant, Cell and Environment, 18: 149-157.
Go to original source... - Terashima I., Hanba Y.T., Tholen D., Niinemets Ü. (2011): Leaf functional anatomy in relation to photosynthesis. Plant Physiology, 155: 108-116.
Go to original source...
Go to PubMed... - Thain J.F. (1983): Curvature correction factors in the measurement of cell surface areas in plant tissues1. Journal of Experimantal Botany, 34: 87-94.
Go to original source... - Tomás M., Jaume F., Lucian C., Jeroni G., Lea H., Hipólito M., Miquel R.-C., Tiina T., Vivian V., Ülo N. (2013): Importance of leaf anatomy in determining meso-phyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models. Journal of Experimental Botany, 64: 2269-2281.
Go to original source...
Go to PubMed... - Tosens T., Nishida K., Gago J., Coopman R.E., Cabrera H.M., Carriquí M., Laanisto L., Morales L., Nadal M., Rojas R., Talts E., Tomas M., Hanba Y., Niinemets Ü., Flexas J. (2016): The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait. New Phytologist, 209: 1576-1590.
Go to original source...
Go to PubMed... - Tsai M.Y., Kuan C., Guo Z.L., Yang H.A., Chung K.F., Ho C.K. (2022): Stomatal clustering in Begonia improves water use efficiency by modulating stomatal movement and leaf structure. Plant-Environment Interactions, 3: 141-154.
Go to original source...
Go to PubMed... - Velikova V., Tsonev T., Tattini M., Arena C., Krumova S., Koleva D., Peeva V., Stojchev S., Todinova S., Izzo L.G., Brunetti C., Stefanova M., Taneva S., Loreto F. (2018): Physiological and structural adjustments of two ecotypes of Platanus orientalis L. from different habitats in response to drought and re-watering. Con-servation Physiology, 6: coy073.
Go to original source... - Von Caemmerer S. (2000): Biochemical models of leaf photosynthesis. Collingwood, Csiro Publishing.
- Xue S., Zang Y., Chen J., Shang S., Tang X. (2022): Effects of enhanced UV-B radiation on photosynthetic performance and non-photochemical quenching process of intertidal red macroalgae Neoporphyra haitanensis. Environmental and Experimental Botany, 199: 104888.
Go to original source... - Yamori W., Suzuki K., Noguchi K.O., Nakai M., Terashima I. (2006): Effects of Rubisco kinetics and Rubisco activation state on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. Plant, Cell and Environment, 29: 1659-1670.
Go to original source...
Go to PubMed... - Zou J., Hu W., Li Y., Zhu H., He J., Wang Y., Meng Y., Chen B., Zhao W., Wang S. (2022): Leaf anatomical alterations reduce cotton's mesophyll conductance under dynamic drought stress conditions. The Plant Journal, 111: 391-405.
Go to original source...
Go to PubMed...
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