Drought affects both photosystems in Arabidopsis thaliana.
Arabidopsis
Photosystem I
Photosystem II
drought
fluorescence
light reactions
photosynthesis
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
received:
23
04
2023
accepted:
14
07
2023
medline:
22
9
2023
pubmed:
2
8
2023
entrez:
2
8
2023
Statut:
ppublish
Résumé
Drought is a major abiotic stress that impairs plant growth and development. Despite this, a comprehensive understanding of drought effects on the photosynthetic apparatus is lacking. In this work, we studied the consequences of 14-d drought treatment on Arabidopsis thaliana. We used biochemical and spectroscopic methods to examine photosynthetic membrane composition and functionality. Drought led to the disassembly of PSII supercomplexes and the degradation of PSII core. The light-harvesting complexes (LHCII) instead remain in the membrane but cannot act as an antenna for active PSII, thus representing a potential source of photodamage. This effect can also be observed during nonphotochemical quenching (NPQ) induction when even short pulses of saturating light can lead to photoinhibition. At a later stage, under severe drought stress, the PSI antenna size is also reduced and the PSI-LHCI supercomplexes disassemble. Surprisingly, although we did not observe changes in the PSI core protein content, the functionality of PSI is severely affected, suggesting the accumulation of nonfunctional PSI complexes. We conclude that drought affects both photosystems, although at a different stage, and that the operative quantum efficiency of PSII (Φ
Substances chimiques
Photosystem I Protein Complex
0
Photosystem II Protein Complex
0
Light-Harvesting Protein Complexes
0
Chlorophyll
1406-65-1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
663-675Informations de copyright
© 2023 The Authors New Phytologist © 2023 New Phytologist Foundation.
Références
Bailleul B, Cardol P, Breyton C, Finazzi G. 2010. Electrochromism: a useful probe to study algal photosynthesis. Photosynthesis Research 106: 179-189.
Bielczynski LW, Schansker G, Croce R. 2016. Effect of light acclimation on the organization of Photosystem II super- and sub-complexes in Arabidopsis thaliana. Frontiers in Plant Science 7: 105.
Borisova-Mubarakshina MM, Vetoshkina DV, Naydov IA, Rudenko NN, Zhurikova EM, Balashov NV, Ignatova LK, Fedorchuk TP, Ivanov BN. 2020. Regulation of the size of Photosystem II light-harvesting antenna represents a universal mechanism of higher plant acclimation to stress conditions. Functional Plant Biology 47: 959-969.
Caffarri S, Kouril R, Kereiche S, Boekema EJ, Croce R. 2009. Functional architecture of higher plant Photosystem II supercomplexes. EMBO Journal 28: 3052-3063.
Chaves MM, Maroco JP, Pereira JS. 2003. Understanding plant responses to drought - from genes to the whole plant. Functional Plant Biology 30: 239-264.
Chen YE, Liu WJ, Su YQ, Cui JM, Zhang ZW, Yuan M, Zhang HY, Yuan S. 2016. Different response of Photosystem II to short and long-term drought stress in Arabidopsis thaliana. Physiologia Plantarum 158: 225-235.
Chen YE, Yuan S, Du JB, Xu MY, Zhang ZW, Lin HH. 2009. Phosphorylation of photosynthetic antenna protein CP29 and Photosystem II structure changes in monocotyledonous plants under environmental stresses. Biochemistry 48: 9757-9763.
Cohen I, Zandalinas SI, Huck C, Fritschi FB, Mittler R. 2021. Meta-analysis of drought and heat stress combination impact on crop yield and yield components. Physiologia Plantarum 171: 66-76.
Croce R, Canino G, Ros F, Bassi R. 2002. Chromophore organization in the higher-plant Photosystem II antenna protein CP26. Biochemistry 41: 7334-7343.
Cruz de Carvalho MH. 2008. Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signaling & Behavior 3: 156-165.
Daryanto S, Wang L, Jacinthe PA. 2016. Global synthesis of drought effects on maize and wheat production. PLoS ONE 11: e0156362.
Das K, Roychoudhury A. 2014. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Frontiers in Environmental Science 2: 53.
Desclaux D, Roumet P. 1996. Impact of drought stress on the phenology of two soybean (Glycine max L. Merr) cultivars. Field Crops Research 46: 61-70.
Digris AV, Novikov EG, Skakun VV, Apanasovich VV. 2014. Global analysis of time-resolved fluorescence data. In: Engelborghs Y, Visser A, eds. Fluorescence spectroscopy and microscopy. Methods in molecular biology (methods and protocols). Totowa, NJ, USA: Humana Press, 257-277.
Engelmann E, Zucchelli G, Casazza AP, Brogioli D, Garlaschi FM, Jennings RC. 2006. Influence of the Photosystem I-light harvesting complex I antenna domains on fluorescence decay. Biochemistry 45: 6947-6955.
Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S et al. 2017. Crop production under drought and heat stress: plant responses and management options. Frontiers in Plant Science 8: 1147.
Farooq M, Basra SMA, Wahid A, Ahmad N, Saleem BA. 2009. Improving the drought tolerance in rice (Oryza sativa L.) by exogenous application of salicylic acid. Journal of Agronomy and Crop Science 195: 237-246.
Flexas J, Medrano H. 2002. Energy dissipation in C-3 plants under drought. Functional Plant Biology 29: 1209-1215.
Fristedt R, Hu C, Wheatley N, Roy LM, Wachter RM, Savage L, Harbinson J, Kramer DM, Merchant SS, Yeates T. 2018. RAF 2 is a RuBis CO assembly factor in Arabidopsis thaliana. The Plant Journal 94: 146-156.
Giardi M, Cona A, Geiken B, Kučera T, Masojidek J, Mattoo A. 1996. Long-term drought stress induces structural and functional reorganization of Photosystem II. Planta 199: 118-125.
Gupta R. 2020. The oxygen-evolving complex: a super catalyst for life on earth, in response to abiotic stresses. Plant Signaling & Behavior 15: 1824721.
Hao L, Liang H, Wang Z, Liu X. 1999. Effects of water stress and rewatering on turnover and gene expression of Photosystem II reaction center polypeptide D1 in Zea mays. Functional Plant Biology 26: 375-378.
Havaux M, Canaani O, Malkin S. 1986. Photosynthetic responses of leaves to water stress, expressed by photoacoustics and related methods: II. The effect of rapid drought on the electron transport and the relative activities of the two photosystems. Plant Physiology 82: 834-839.
He W, Yan K, Zhang Y, Bian L, Mei H, Han G. 2021. Contrasting photosynthesis, photoinhibition and oxidative damage in honeysuckle (Lonicera japonica Thunb.) under iso-osmotic salt and drought stresses. Environmental and Experimental Botany 182: 104313.
Hu C, Mascoli V, Elias E, Croce R. 2023. The photosynthetic apparatus of the CAM plant Tillandsia flabellate and its response to water deficit. Journal of Plant Physiology 282: 153945.
Huang B, Chen YE, Zhao YQ, Ding CB, Liao JQ, Hu C, Zhou LJ, Zhang ZW, Yuan S, Yuan M. 2019. Exogenous melatonin alleviates oxidative damages and protects Photosystem II in maize seedlings under drought stress. Frontiers in Plant Science 10: 677.
Jarvi S, Suorsa M, Paakkarinen V, Aro EM. 2011. Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes. Biochemical Journal 439: 207-214.
Khorobrykh S, Havurinne V, Mattila H, Tyystjarvi E. 2020. Oxygen and ROS in photosynthesis. Plants 9: 91.
Klughammer C, Schreiber U. 1994. An improved method, using saturating light-pulses, for the determination of photosystem-I quantum yield via P700+-absorbency changes at 830 Nm. Planta 192: 261-268.
Koochak H, Puthiyaveetil S, Mullendore DL, Li M, Kirchhoff H. 2019. The structural and functional domains of plant thylakoid membranes. The Plant Journal 97: 412-429.
Kudoh H, Sonoike K. 2002. Irreversible damage to Photosystem I by chilling in the light: cause of the degradation of chlorophyll after returning to normal growth temperature. Planta 215: 541-548.
Laemmli U. 1970. SDS-page Laemmli method. Nature 227: 680-685.
Lazar D, Pospisil P. 1999. Mathematical simulation of chlorophyll a fluorescence rise measured with 3-(3′,4′-dichlorophenyl)-1,1-dimethylurea-treated barley leaves at room and high temperatures. European Biophysics Journal 28: 468-477.
Liu J, Guo YY, Bai YW, Li HJ, Xue JQ, Zhang RH. 2019. Response of photosynthesis in maize to drought and re-watering. Russian Journal of Plant Physiology 66: 424-432.
Lu C, Zhang J. 1999. Effects of water stress on Photosystem II photochemistry and its thermostability in wheat plants. Journal of Experimental Botany 50: 1199-1206.
Masojidek J, Trivedi S, Halshaw L, Alexiou A, Hall DO. 1991. The synergistic effect of drought and light stresses in Sorghum and pearl-millet. Plant Physiology 96: 198-207.
Medrano H, Escalona JM, Bota J, Gulias J, Flexas J. 2002. Regulation of photosynthesis of C-3 plants in response to progressive drought: stomatal conductance as a reference parameter. Annals of Botany 89: 895-905.
Meng LL, Song JF, Wen J, Zhang J, Wei JH. 2016. Effects of drought stress on fluorescence characteristics of photosystem II in leaves of Plectranthus scutellarioides. Photosynthetica 54: 414-421.
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. 2010. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell & Environment 33: 453-467.
Nawrocki WJ, Bailleul B, Picot D, Cardol P, Rappaport F, Wollman FA, Joliot P. 2019. The mechanism of cyclic electron flow. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1860: 433-438.
Nicol L, Nawrocki WJ, Croce R. 2019. Disentangling the sites of non-photochemical quenching in vascular plants. Nature Plants 5: 1177-1183.
Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer CH. 2002. Drought and oxidative load in the leaves of C-3 plants: a predominant role for photorespiration? Annals of Botany 89: 841-850.
van Oort B, Alberts M, de Bianchi S, Dall'Osto L, Bassi R, Trinkunas G, Croce R, van Amerongen H. 2010. Effect of antenna-depletion in Photosystem II on excitation energy transfer in Arabidopsis thaliana. Biophysical Journal 98: 922-931.
van Oort B, Amunts A, Borst JW, van Hoek A, Nelson N, van Amerongen H, Croce R. 2008. Picosecond fluorescence of intact and dissolved PSI-LHCI crystals. Biophysical Journal 95: 5851-5861.
Oquist G, Chow WS, Anderson JM. 1992. Photoinhibition of photosynthesis represents a mechanism for the long-term regulation of photosystem-Ii. Planta 186: 450-460.
Pandey J, Devadasu E, Saini D, Dhokne K, Marriboina S, Raghavendra AS, Subramanyam R. 2023. Reversible changes in structure and function of photosynthetic apparatus of pea (Pisum sativum) leaves under drought stress. The Plant Journal 113: 60-74.
Porra R, Thompson W, Kriedemann P. 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. Biochimica et Biophysica Acta (BBA) - Bioenergetics 975: 384-394.
Rantala M, Tikkanen M, Aro EM. 2017. Proteomic characterization of hierarchical megacomplex formation in Arabidopsis thylakoid membrane. The Plant Journal 92: 951-962.
Reddy AR, Chaitanya KV, Vivekanandan M. 2004. Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. Journal of Plant Physiology 161: 1189-1202.
Sairam R, Tyagi A. 2004. Physiology and molecular biology of salinity stress tolerance in plants. Current Science 1: 407-421.
Sapeta H, Yokono M, Takabayashi A, Ueno Y, Cordeiro AM, Hara T, Tanaka A, Akimoto S, Oliveira MM, Tanaka R. 2023. Reversible down-regulation of photosystems I and II leads to fast photosynthesis recovery after long-term drought in Jatropha curcas. Journal of Experimental Botany 74: 336-351.
Shao RX, Xin LF, Zheng HF, Li LL, Ran WL, Mao J, Yang QH. 2016. Changes in chloroplast ultrastructure in leaves of drought-stressed maize inbred lines. Photosynthetica 54: 74-80.
Snellenburg J, Laptenok S, Seger R, Mullen K, van Stokkum IHM. 2012. Glotaran: a Java-based graphical user interface for the R package TIMP. Journal of Statistical Software 49: 1-22.
Sofo A, Tuzio AC, Dichio B, Xiloyannis C. 2005. Influence of water deficit and rewatering on the components of the ascorbate-glutathione cycle in four interspecific Prunus hybrids. Plant Science 169: 403-412.
Sonoike K. 2011. Photoinhibition of Photosystem I. Physiologia Plantarum 142: 56-64.
Sperdouli I, Moustakas M. 2012. Differential response of Photosystem II photochemistry in young and mature leaves of Arabidopsis thaliana to the onset of drought stress. Acta Physiologiae Plantarum 34: 1267-1276.
Stirbet A. 2013. Excitonic connectivity between Photosystem II units: what is it, and how to measure it? Photosynthesis Research 116: 189-214.
Suorsa M, Rantala M, Mamedov F, Lespinasse M, Trotta A, Grieco M, Vuorio E, Tikkanen M, Jarvi S, Aro EM. 2015. Light acclimation involves dynamic re-organization of the pigment-protein megacomplexes in non-appressed thylakoid domains. The Plant Journal 84: 360-373.
Tian LJ, Nawrocki WJ, Liu X, Polukhina I, van Stokkum IHM, Croce R. 2019. pH dependence, kinetics and light-harvesting regulation of nonphotochemical quenching in Chlamydomonas. Proceedings of the National Academy of Sciences, USA 116: 8320-8325.
Tjus SE, Moller BL, Scheller HV. 1999. Photoinhibition of Photosystem I damages both reaction centre proteins PSI-A and PSI-B and acceptor-side located small Photosystem I polypeptides. Photosynthesis Research 60: 75.
Wang YX, Suo B, Zhao TF, Qu XF, Yuan LG, Zhao XJ, Zhao HJ. 2011. Effect of nitric oxide treatment on antioxidant responses and psbA gene expression in two wheat cultivars during grain filling stage under drought stress and rewatering. Acta Physiologiae Plantarum 33: 1923-1932.
Weatherley PE. 1980. Citation classic - studies in the water relations of the cotton plant. 1. The field measurement of water deficits in leaves. Current Contents/Agriculture Biology & Environmental Sciences 49: 10.
Wientjes E, van Stokkum IH, van Amerongen H, Croce R. 2011. The role of the individual Lhcas in Photosystem I excitation energy trapping. Biophysical Journal 101: 745-754.
Woo NS, Badger MR, Pogson BJ. 2008. A rapid, non-invasive procedure for quantitative assessment of drought survival using chlorophyll fluorescence. Plant Methods 4: 1-14.
Xu PQ, Tian LJ, Kloz M, Croce R. 2015. Molecular insights into Zeaxanthin-dependent quenching in higher plants. Scientific Reports 5: 1-10.
Yao J, Sun D, Cen H, Xu H, Weng H, Yuan F, He Y. 2018. Phenotyping of Arabidopsis drought stress response using kinetic chlorophyll fluorescence and multicolor fluorescence imaging. Frontiers in Plant Science 9: 603.
Zhang SP, Scheller HV. 2004. Photoinhibition of Photosystem I at chilling temperature and subsequent recovery in Arabidopsis thaliana. Plant and Cell Physiology 45: 1595-1602.
Zivcak M, Brestic M, Balatova Z, Drevenakova P, Olsovska K, Kalaji HM, Yang X, Allakhverdiev SI. 2013. Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynthesis Research 117: 529-546.