Dynamic in vivo monitoring of granum structural changes of Ctenanthe setosa (Roscoe) Eichler during drought stress and subsequent recovery

Hembrom, Richard; Ünnep, Renáta; Sárvári, Éva; Nagy, Gergely; Solymosi, Katalin

doi:10.1111/ppl.14621

Title: Dynamic in vivo monitoring of granum structural changes of Ctenanthe setosa (Roscoe) Eichler during drought stress and subsequent recovery

Journal Article · 21 January 2025 · Physiologia Plantarum

DOI: https://doi.org/10.1111/ppl.14621 · OSTI ID:2538233

Hembrom, Richard ^[1]; Ünnep, Renáta ^[2]; Sárvári, Éva ^[1];

^[3]; Solymosi, Katalin ^[1]

Eotvos Lorand University, Budapest (Hungary)
HUN-REN Centre for Energy Research, Budapest (Hungary)
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Investigating the effects of drought stress and subsequent recovery on the structure and function of chloroplasts is essential to understanding how plants adapt to environmental stressors. We investigated Ctenanthe setosa (Roscoe) Eichler, an ornamental plant that can tolerate prolonged drought periods (40 and 49 days of water withdrawal). Conventional biochemical, biophysical, physiological and (ultra)structural methods combined for the first time in a higher plant with in vivo small-angle neutron scattering (SANS) were used to characterize the alterations induced by drought stress and subsequent recovery. Upon drought stress, no significant changes occurred in the chloroplast ultrastructure, chlorophyll content, 77K fluorescence emission spectra and maximal quantum efficiency of PSII (Qy dark), but the actual quantum efficiency of PSII (Qy light) decreased, the amounts of PSI-LHCII complexes and PSII monomers declined, and that of PSII supercomplexes increased. Thickness of the leaf and of the adaxial hypodermis, chloroplast length and granum repeat distance (RD) values decreased upon drought stress, as shown by light microscopy and SANS, respectively. Because of the very slight (nm-range) changes in RD values, the large biological variability (significant differences in RD values among the leaves and studied leaf regions) and the invasive sampling required for this method, transmission electron microscopy (TEM) hardly showed significant differences. On the other side, in situ SANS analyses provided a unique insight in vivo into the fast structural recovery of the granum structure of drought-stressed leaves, which happened already 18 h after re-watering, while functional and biochemical recovery took place on a longer time scale.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 2538233

Journal Information:: Physiologia Plantarum, Journal Name: Physiologia Plantarum Journal Issue: 1 Vol. 177; ISSN 0031-9317

Publisher:: Wiley - Scandinavian Plant Physiology SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (60)

Measuring the dynamic response of the thylakoid architecture in plant leaves by electron microscopy Li, Meng; Mukhopadhyay, Roma; Svoboda, Václav Plant Direct, Vol. 4, Issue 11 https://doi.org/10.1002/pld3.280	journal	November 2020
Plant Drought Stress: Effects, Mechanisms and Management Farooq, M.; Wahid, A.; Kobayashi, N. Sustainable Agriculture https://doi.org/10.1007/978-90-481-2666-8_12	book	January 2009
Long-term drought stress induces structural and functional reorganization of photosystem II Giardi, M. T.; Cona, A.; Geiken, B. Planta, Vol. 199, Issue 1 https://doi.org/10.1007/BF00196888	journal	May 1996
High biological variability of plastids, photosynthetic pigments and pigment forms of leaf primordia in buds Solymosi, Katalin; Morandi, Dominique; Bóka, Károly Planta, Vol. 235, Issue 5 https://doi.org/10.1007/s00425-011-1559-9	journal	December 2011
Ionic, not the osmotic component, is responsible for the salinity-induced inhibition of greening in etiolated wheat (Triticum aestivum L. cv. Mv Béres) leaves: a comparative study Sóti, Adél; Ounoki, Roumaissa; Kósa, Annamária Planta, Vol. 258, Issue 5 https://doi.org/10.1007/s00425-023-04255-4	journal	October 2023
Leaf rolling and photosystem II efficiency in Ctenanthe setosa exposed to drought stress Nar, H.; Saglam, A.; Terzi, R. Photosynthetica, Vol. 47, Issue 3 https://doi.org/10.1007/s11099-009-0066-8	journal	September 2009
Effect of drought stress on the photosynthesis of Acacia tortilis subsp. raddiana at the young seedling stage Kebbas, S.; Lutts, S.; Aid, F. Photosynthetica, Vol. 53, Issue 2 https://doi.org/10.1007/s11099-015-0113-6	journal	June 2015
Changes in chloroplast ultrastructure in leaves of drought-stressed maize inbred lines Shao, R. X.; Xin, L. F.; Zheng, H. F. Photosynthetica, Vol. 54, Issue 1 https://doi.org/10.1007/s11099-015-0158-6	journal	March 2016
Frequently asked questions about chlorophyll fluorescence, the sequel Kalaji, Hazem M.; Schansker, Gert; Brestic, Marian Photosynthesis Research, Vol. 132, Issue 1 https://doi.org/10.1007/s11120-016-0318-y	journal	November 2016
Neutron scattering in photosynthesis research: recent advances and perspectives for testing crop plants Nagy, Gergely; Garab, Győző Photosynthesis Research https://doi.org/10.1007/s11120-020-00763-6	journal	June 2020
Spectral diversity of photosystem I from flowering plants Bos, Peter R.; Schiphorst, Christo; Kercher, Ian Photosynthesis Research, Vol. 155, Issue 1 https://doi.org/10.1007/s11120-022-00971-2	journal	October 2022
Leaf rolling effects on lipid and fatty acid composition in Ctenanthe setosa (Marantaceae) subjected to water-deficit stress Ayaz, F. Ahmet; Kadioglu, Asım; Dogru, Ali Acta Physiologiae Plantarum, Vol. 23, Issue 1 https://doi.org/10.1007/s11738-001-0021-1	journal	March 2001
Comparison of ultrastructural and physiological changes of potato (Solanum tuberosum L.) plantlets subjected to salt and modeling drought stresses Bai, Jiang-Ping; Gao, Hui-Juan; Yang, Hong-Yu Acta Physiologiae Plantarum, Vol. 38, Issue 7 https://doi.org/10.1007/s11738-016-2202-y	journal	June 2016
Light sensitivity of Haberlea rhodopensis shade adapted phenotype under drought stress Georgieva, Katya; Solti, Ádam; Mészáros, Ilona Acta Physiologiae Plantarum, Vol. 39, Issue 8 https://doi.org/10.1007/s11738-017-2457-y	journal	July 2017
Effect of Drought Stress on Anatomical Structure and Chloroplast Ultrastructure in Leaves of Sugarcane Zhang, Feng-Juan; Zhang, Kun-Kun; Du, Cheng-Zhong Sugar Tech, Vol. 17, Issue 1 https://doi.org/10.1007/s12355-014-0337-y	journal	October 2014
Hydrogen peroxide extends postharvest life of Ctenanthe setosa leaf cuts under osmotic stress by reducing leaf rolling Saglam, Aykut; Kalaycioglu, Ebru; Guven, Funda Gul Horticulture, Environment, and Biotechnology, Vol. 55, Issue 4 https://doi.org/10.1007/s13580-014-0138-y	journal	August 2014
[34] Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes Lichtenthaler, Hartmut K. Methods in Enzymology https://doi.org/10.1016/0076-6879(87)48036-1	book	January 1987
Fluorescence of chlorophyll in photosynthetic systems III. Emission and action spectra of fluorescence—Three emission bands of chlorophyll a and the energy transfer between two pigment systems Murata, Norio; Nishimura, Mitsuo; Takamiya, Atusi Biochimica et Biophysica Acta (BBA) - Biophysics including Photosynthesis, Vol. 126, Issue 2 https://doi.org/10.1016/0926-6585(66)90059-8	journal	October 1966
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 Porra, R. J.; Thompson, W. A.; Kriedemann, P. E. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 975, Issue 3 https://doi.org/10.1016/S0005-2728(89)80347-0	journal	August 1989
Metabolic engineering of plants for osmotic stress resistance Nuccio, Michael L.; Rhodest, David; McNeil, Scott D. Current Opinion in Plant Biology, Vol. 2, Issue 2 https://doi.org/10.1016/S1369-5266(99)80026-0	journal	April 1999
The ultrastructure and flexibility of thylakoid membranes in leaves and isolated chloroplasts as revealed by small-angle neutron scattering Ünnep, R.; Zsiros, O.; Solymosi, K. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 9 https://doi.org/10.1016/j.bbabio.2014.01.017	journal	September 2014
The relevance of dynamic thylakoid organisation to photosynthetic regulation Johnson, Matthew P.; Wientjes, Emilie Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 4 https://doi.org/10.1016/j.bbabio.2019.06.011	journal	April 2020
Succulent plants Griffiths, Howard; Males, Jamie Current Biology, Vol. 27, Issue 17 https://doi.org/10.1016/j.cub.2017.03.021	journal	September 2017
Drought stress response in Jatropha curcas: Growth and physiology Sapeta, Helena; Costa, J. Miguel; Lourenço, Tiago Environmental and Experimental Botany, Vol. 85 https://doi.org/10.1016/j.envexpbot.2012.08.012	journal	January 2013
Galactolipid remodeling is involved in drought-induced leaf senescence in maize Chen, Daoqian; Wang, Shiwen; Qi, Lingyun Environmental and Experimental Botany, Vol. 150 https://doi.org/10.1016/j.envexpbot.2018.02.017	journal	June 2018
Progress and perspective on drought and salt stress tolerance in cotton Abdelraheem, Abdelraheem; Esmaeili, Nardana; O’Connell, Mary Industrial Crops and Products, Vol. 130 https://doi.org/10.1016/j.indcrop.2018.12.070	journal	April 2019
Comparison of thylakoid structure and organization in sun and shade Haberlea rhodopensis populations under desiccation and rehydration Sárvári, Éva; Mihailova, Gergana; Solti, Ádám Journal of Plant Physiology, Vol. 171, Issue 17 https://doi.org/10.1016/j.jplph.2014.07.015	journal	November 2014
Mantid—Data analysis and visualization package for neutron scattering and μ SR experiments Arnold, O.; Bilheux, J. C.; Borreguero, J. M. Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment, Vol. 764 https://doi.org/10.1016/j.nima.2014.07.029	journal	November 2014
Vegetative desiccation tolerance: Is it a goldmine for bioengineering crops? Toldi, Ottó; Tuba, Zoltán; Scott, Peter Plant Science, Vol. 176, Issue 2 https://doi.org/10.1016/j.plantsci.2008.10.002	journal	February 2009
Monitoring thylakoid ultrastructural changes in vivo using small-angle neutron scattering Ünnep, Renáta; Nagy, Gergely; Markó, Márton Plant Physiology and Biochemistry, Vol. 81 https://doi.org/10.1016/j.plaphy.2014.02.005	journal	August 2014
drtsans: The data reduction toolkit for small-angle neutron scattering at Oak Ridge National Laboratory Heller, William T.; Hetrick, John; Bilheux, Jean SoftwareX, Vol. 19 https://doi.org/10.1016/j.softx.2022.101101	journal	July 2022
Increased economic drought impacts in Europe with anthropogenic warming Naumann, Gustavo; Cammalleri, Carmelo; Mentaschi, Lorenzo Nature Climate Change, Vol. 11, Issue 6 https://doi.org/10.1038/s41558-021-01044-3	journal	May 2021
Composition, phosphorylation and dynamic organization of photosynthetic protein complexes in plant thylakoid membrane Rantala, Marjaana; Rantala, Sanna; Aro, Eva-Mari Photochemical & Photobiological Sciences, Vol. 19, Issue 5 https://doi.org/10.1039/d0pp00025f	journal	January 2020
Dynamic control of protein diffusion within the granal thylakoid lumen Kirchhoff, H.; Hall, C.; Wood, M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 50 https://doi.org/10.1073/pnas.1104141109	journal	November 2011
Changes in aggregation states of light-harvesting complexes as a mechanism for modulating energy transfer in desert crust cyanobacteria Bar Eyal, Leeat; Ranjbar Choubeh, Reza; Cohen, Eyal Proceedings of the National Academy of Sciences, Vol. 114, Issue 35 https://doi.org/10.1073/pnas.1708206114	journal	August 2017
New foundations for the physical mechanism of variable chlorophyll a fluorescence. Quantum efficiency versus the light-adapted state of photosystem II Garab, Győző; Magyar, Melinda; Sipka, Gábor Journal of Experimental Botany, Vol. 74, Issue 18 https://doi.org/10.1093/jxb/erad252	journal	July 2023
The PSI–PSII Megacomplex in Green Plants Yokono, Makio; Takabayashi, Atsushi; Kishimoto, Junko Plant and Cell Physiology, Vol. 60, Issue 5 https://doi.org/10.1093/pcp/pcz026	journal	February 2019
Light-adapted charge-separated state of photosystem II: structural and functional dynamics of the closed reaction center Sipka, G�bor; Magyar, Melinda; Mezzetti, Alberto The Plant Cell, Vol. 33, Issue 4 https://doi.org/10.1093/plcell/koab008	journal	January 2021
Thylakoid membrane reorganizations revealed by small-angle neutron scattering of Monstera deliciosa leaves associated with non-photochemical quenching Ünnep, Renáta; Paul, Suman; Zsiros, Ottó Open Biology, Vol. 10, Issue 9 https://doi.org/10.1098/rsob.200144	journal	September 2020
Photoprotection Conferred by Changes in Photosynthetic Protein Levels and Organization during Dehydration of a Homoiochlorophyllous Resurrection Plant Charuvi, Dana; Nevo, Reinat; Shimoni, Eyal Plant Physiology, Vol. 167, Issue 4 https://doi.org/10.1104/pp.114.255794	journal	February 2015
The suite of small-angle neutron scattering instruments at Oak Ridge National Laboratory Heller, William T.; Cuneo, Matthew; Debeer-Schmitt, Lisa Journal of Applied Crystallography, Vol. 51, Issue 2 https://doi.org/10.1107/S1600576718001231	journal	February 2018
Chloroplast ultrastructure in plants Kirchhoff, Helmut New Phytologist, Vol. 223, Issue 2 https://doi.org/10.1111/nph.15730	journal	March 2019
Granal thylakoid structure and function: explaining an enduring mystery of higher plants Gu, Lianhong; Grodzinski, Bernard; Han, Jimei New Phytologist, Vol. 236, Issue 2 https://doi.org/10.1111/nph.18371	journal	August 2022
Drought affects both photosystems in Arabidopsis thaliana Hu, Chen; Elias, Eduard; Nawrocki, Wojciech J. New Phytologist, Vol. 240, Issue 2 https://doi.org/10.1111/nph.19171	journal	August 2023
Drought stress adaptation: metabolic adjustment and regulation of gene expression Bhargava, Sujata; Sawant, Kshitija Plant Breeding, Vol. 132, Issue 1 https://doi.org/10.1111/pbr.12004	journal	October 2012
Different response of photosystem II to short and long-term drought stress in Arabidopsis thaliana Chen, Yang-Er; Liu, Wen-Juan; Su, Yan-Qiu Physiologia Plantarum, Vol. 158, Issue 2 https://doi.org/10.1111/ppl.12438	journal	April 2016
The Arabidopsis thylakoid transporter PHT4;1 influences phosphate availability for ATP synthesis and plant growth Karlsson, Patrik M.; Herdean, Andrei; Adolfsson, Lisa The Plant Journal, Vol. 84, Issue 1 https://doi.org/10.1111/tpj.12962	journal	September 2015
Reversible changes in structure and function of photosynthetic apparatus of pea (Pisum sativum) leaves under drought stress Pandey, Jayendra; Devadasu, Elsinraju; Saini, Deepak The Plant Journal, Vol. 113, Issue 1 https://doi.org/10.1111/tpj.16034	journal	December 2022
Physiological changes in them in post-stress emerging Ctenanthe setosa plants under drought conditions Saglam, A.; Kadioglu, A.; Terzi, R. Russian Journal of Plant Physiology, Vol. 55, Issue 1 https://doi.org/10.1134/S1021443708010056	journal	January 2008
New Measurement Control Software on the Yellow Submarine SANS Instrument at the Budapest Neutron Centre Almásy, L. Journal of Surface Investigation: X-ray, Synchrotron and Neutron Techniques, Vol. 15, Issue 3 https://doi.org/10.1134/S1027451021030046	journal	May 2021
Qualitative and quantitative evaluation of thylakoid complexes separated by Blue Native PAGE Sárvári, Éva; Gellén, Gabriella; Sági-Kazár, Máté Plant Methods, Vol. 18, Issue 1 https://doi.org/10.1186/s13007-022-00858-2	journal	March 2022
Plant adaptation to drought stress Basu, Supratim; Ramegowda, Venkategowda; Kumar, Anuj F1000Research, Vol. 5 https://doi.org/10.12688/f1000research.7678.1	journal	January 2016
Mycorrhiza Symbiosis Increases the Surface for Sunlight Capture in Medicago truncatula for Better Photosynthetic Production Adolfsson, Lisa; Solymosi, Katalin; Andersson, Mats X. PLOS ONE, Vol. 10, Issue 1 https://doi.org/10.1371/journal.pone.0115314	journal	January 2015
Scavenging of reactive oxygen species in apoplastic and symplastic areas of rolled leaves inCtenanthe setosaunder drought stress Saruhan, Neslihan; Terzi, Rabiye; Sağlam, Aykut Acta Biologica Hungarica, Vol. 61, Issue 3 https://doi.org/10.1556/ABiol.61.2010.3.5	journal	September 2010
Analyses of OJIP transients in leaves of two epiphytic orchids under drought stress Zampirollo, Jadson Bonini; Pinheiro, Clodoaldo Leites; Santos, Vinícius Fonseca dos Ornamental Horticulture, Vol. 27, Issue 4 https://doi.org/10.1590/2447-536x.v27i4.2334	journal	December 2021
Jupyter Notebooks – a publishing format for reproducible computational workflows Kluyver, Thomas; Ragan-Kelley, Benjamin; Perez, Fernando Positioning and Power in Academic Publishing: Players, Agents and Agendas https://doi.org/10.3233/978-1-61499-649-1-87	book	January 2021
Response of plants to water stress Osakabe, Yuriko; Osakabe, Keishi; Shinozaki, Kazuo Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00086	journal	March 2014
How to Measure Grana – Ultrastructural Features of Thylakoid Membranes of Plant Chloroplasts Mazur, Radosław; Mostowska, Agnieszka; Kowalewska, Łucja Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.756009	journal	October 2021
Reactivation of the Photosynthetic Apparatus of Resurrection Plant Haberlea rhodopensis during the Early Phase of Recovery from Drought- and Freezing-Induced Desiccation Mihailova, Gergana; Christov, Nikolai K.; Sárvári, Éva Plants, Vol. 11, Issue 17 https://doi.org/10.3390/plants11172185	journal	August 2022
Lignification response for rolled leaves of Ctenanthe setosa under long-term drought stress Terzİ, Rabiye; Saruhan GÜLer, Neslihan; Kutlu ÇAliŞKan, Nihal TURKISH JOURNAL OF BIOLOGY, Vol. 37 https://doi.org/10.3906/biy-1210-27	journal	January 2013

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