Abstract
Moderate heat stress and fluctuating light are typical conditions in summer in tropical and subtropical regions. This type of stress can cause photodamage to photosystems I and II (PSI and PSII). However, photosynthetic responses to the combination of heat and fluctuating light in young leaves are little known. In this study, we investigated chlorophyll fluorescence and P700 redox state under fluctuating light at 25 °C and 42 °C in young leaves of tobacco. Our results indicated that fluctuating light caused selective photodamage to PSI in the young leaves at 25 °C and 42 °C. Furthermore, the moderate heat stress significantly accelerated photoinhibition of PSI under fluctuating light. Within the first 10 s after transition from low to high light, cyclic electron flow (CEF) around PSI was highly stimulated at 25 °C but was slightly activated at 42 °C. Such depression of CEF activation at moderate heat stress were unable to maintain energy balance under high light. As a result, electron flow from PSI to NADP+ was restricted, leading to the over-reduction of PSI electron carriers. These results indicated that moderate heat stress altered the CEF performance under fluctuating light and thus accelerated PSI photoinhibition in tobacco young leaves.
Similar content being viewed by others
References
Alboresi A, Storti M, Morosinotto T (2019) Balancing protection and efficiency in the regulation of photosynthetic electron transport across plant evolution. New Phytol 221:105–109. https://doi.org/10.1111/nph.15372
Allahverdiyeva Y, Mustila H, Ermakova M et al (2013) Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light. Proc Natl Acad Sci 110:4111–4116. https://doi.org/10.1073/pnas.1221194110
Allahverdiyeva Y, Suorsa M, Tikkanen M, Aro EM (2015) Photoprotection of photosystems in fluctuating light intensities. J Exp Bot 66:2427–2436. https://doi.org/10.1093/jxb/eru463
Armbruster U, Carrillo LR, Venema K et al (2014) Ion antiport accelerates photosynthetic acclimation in fluctuating light environments. Nat Commun 5:1–8. https://doi.org/10.1038/ncomms6439
Armbruster U, Correa Galvis V, Kunz HH, Strand DD (2017) The regulation of the chloroplast proton motive force plays a key role for photosynthesis in fluctuating light. Curr Opin Plant Biol 37:56–62. https://doi.org/10.1016/j.pbi.2017.03.012
Armbruster U, Leonelli L, Galvis VC et al (2016) Regulation and levels of the thylakoid K+/H+ antiporter KEA3 shape the dynamic response of photosynthesis in fluctuating light. Plant Cell Physiol 57:1557–1567. https://doi.org/10.1093/pcp/pcw085
Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta Bioenerg 1143:113–134. https://doi.org/10.1016/0005-2728(93)90134-2
Barth C, Krause GH, Winter K (2001) Responses of photosystem I compared with photosystem II to high-light stress in tropical shade and sun leaves. Plant Cell Environ 24:163–176. https://doi.org/10.1046/j.1365-3040.2001.00673.x
Brestic M, Zivcak M, Kunderlikova K, Allakhverdiev SI (2016) High temperature specifically affects the photoprotective responses of chlorophyll b-deficient wheat mutant lines. Photosynth Res 130:251–266. https://doi.org/10.1007/s11120-016-0249-7
Chaux F, Burlacot A, Mekhalfi M et al (2017) Flavodiiron proteins promote fast and transient O2 photoreduction in Chlamydomonas. Plant Physiol 174:1825–1836. https://doi.org/10.1104/pp.17.00421
Chen Y, Xu DQ (2006) Two patterns of leaf photosynthetic response to irradiance transition from saturating to limiting one in some plant species. New Phytol 169:789–798. https://doi.org/10.1111/j.1469-8137.2005.01624.x
Chovancek E, Zivcak M, Botyanszka L et al (2019) Transient heat waves may affect the photosynthetic capacity of susceptible wheat genotypes due to insufficient photosystem I photoprotection. Plants 8:282. https://doi.org/10.3390/plants8080282
De Souza AP, Wang Y, Orr DJ et al (2020) Photosynthesis across African cassava germplasm is limited by Rubisco and mesophyll conductance at steady state, but by stomatal conductance in fluctuating light. New Phytol 225:2498–2512. https://doi.org/10.1111/nph.16142
Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta Gen Subj 990:87–92. https://doi.org/10.1016/S0304-4165(89)80016-9
Gerotto C, Alboresi A, Meneghesso A et al (2016) Flavodiiron proteins act as safety valve for electrons in Physcomitrella patens. Proc Natl Acad Sci 113:12322–12327. https://doi.org/10.1073/pnas.1606685113
Graham PJ, Nguyen B, Burdyny T, Sinton D (2017) A penalty on photosynthetic growth in fluctuating light. Sci Rep 7:1–11. https://doi.org/10.1038/s41598-017-12923-1
Grieco M, Tikkanen M, Paakkarinen V et al (2012) Steady-state phosphorylation of light-harvesting complex II proteins preserves photosystem I under fluctuating white light. Plant Physiol 160:1896–1910. https://doi.org/10.1104/pp.112.206466
Hahn A, Vonck J, Mills DJ et al (2018) Structure, mechanism, and regulation of the chloroplast ATP synthase. Science 360:e4318. https://doi.org/10.1126/science.aat4318
Huang W, Cai Y-F, Wang J-H, Zhang S-B (2018a) Chloroplastic ATP synthase plays an important role in the regulation of proton motive force in fluctuating light. J Plant Physiol 226:40–47. https://doi.org/10.1016/j.jplph.2018.03.020
Huang W, Hu H, Zhang S-B (2015) Photorespiration plays an important role in the regulation of photosynthetic electron flow under fluctuating light in tobacco plants grown under full sunlight. Front Plant Sci 6:621. https://doi.org/10.3389/fpls.2015.00621
Huang W, Suorsa M, Zhang S-B (2018b) In vivo regulation of thylakoid proton motive force in immature leaves. Photosynth Res 138:207–218. https://doi.org/10.1007/s11120-018-0565-1
Huang W, Tikkanen M, Cai Y-F et al (2018c) Chloroplastic ATP synthase optimizes the trade-off between photosynthetic CO2 assimilation and photoprotection during leaf maturation. Biochim Biophys Acta Bioenerg 1859:1067–1074. https://doi.org/10.1016/j.bbabio.2018.06.009
Huang W, Yang Y-J, Zhang S-B (2019a) The role of water-water cycle in regulating the redox state of photosystem I under fluctuating light. Biochim Biophys Acta Bioenerg 1860:383–390. https://doi.org/10.1016/j.bbabio.2019.03.007
Huang W, Yang Y-J, Zhang S-B (2017) Specific roles of cyclic electron flow around photosystem I in photosynthetic regulation in immature and mature leaves. J Plant Physiol 209:76–83. https://doi.org/10.1016/j.jplph.2016.11.013
Huang W, Yang Y-J, Zhang S-B (2019b) Photoinhibition of photosystem I under fluctuating light is linked to the insufficient ΔpH upon a sudden transition from low to high light. Environ Exp Bot 160:112–119. https://doi.org/10.1016/j.envexpbot.2019.01.012
Ilík P, Pavlovič A, Kouřil R et al (2017) Alternative electron transport mediated by flavodiiron proteins is operational in organisms from cyanobacteria up to gymnosperms. New Phytol 214:967–972. https://doi.org/10.1111/nph.14536
Jokel M, Johnson X, Peltier G et al (2018) Hunting the main player enabling Chlamydomonas reinhardtii growth under fluctuating light. Plant J 94:822–835. https://doi.org/10.1111/tpj.13897
Kono M, Noguchi K, Terashima I (2014) Roles of the cyclic electron flow around PSI (CEF-PSI) and O2-dependent alternative pathways in regulation of the photosynthetic electron flow in short-term fluctuating light in Arabidopsis thaliana. Plant Cell Physiol 55:990–1004. https://doi.org/10.1093/pcp/pcu033
Kono M, Terashima I (2016) Elucidation of photoprotective mechanisms of PSI against fluctuating light photoinhibition. Plant Cell Physiol 57:1405–1414. https://doi.org/10.1093/pcp/pcw103
Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218. https://doi.org/10.1023/B:PRES.0000015391.99477.0d
Lima-Melo Y, Gollan PJ, Tikkanen M et al (2019) Consequences of photosystem-I damage and repair on photosynthesis and carbon use in Arabidopsis thaliana. Plant J 97:1061–1072. https://doi.org/10.1111/tpj.14177
Liu J, Last RL (2017) A chloroplast thylakoid lumen protein is required for proper photosynthetic acclimation of plants under fluctuating light environments. Proc Natl Acad Sci 114:E8110–E8117. https://doi.org/10.1073/pnas.1712206114
Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends Plant Sci 4:130–135. https://doi.org/10.1016/S1360-1385(99)01387-4
Munekage Y, Hojo M, Meurer J et al (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371. https://doi.org/10.1016/S0092-8674(02)00867-X
Sacksteder CA, Kanazawa A, Jacoby ME, Kramer DM (2000) The proton to electron stoichiometry of steady-state photosynthesis in living plants: a proton-pumping Q cycle is continuously engaged. Proc Natl Acad Sci 97:14283–14288. https://doi.org/10.1073/pnas.97.26.14283
Schneider T, Bolger A, Zeier J et al (2019) Fluctuating light interacts with time of day and leaf development stage to reprogram gene expression. Plant Physiol 179:1632–1657. https://doi.org/10.1104/pp.18.01443
Schreiber U, Klughammer C (2008) Saturation pulse method for assessment of energy conversion in PSI. PAM Appl Notes. https://doi.org/10.1007/s00415-017-8571-3
Sejima T, Takagi D, Fukayama H et al (2014) Repetitive short-pulse light mainly inactivates photosystem I in sunflower leaves. Plant Cell Physiol 55:1184–1193. https://doi.org/10.1093/pcp/pcu061
Shikanai T, Yamamoto H (2017) Contribution of cyclic and pseudo-cyclic electron transport to the formation of proton motive force in chloroplasts. Mol Plant 10:20–29. https://doi.org/10.1016/j.molp.2016.08.004
Shimakawa G, Ishizaki K, Tsukamoto S et al (2017) The liverwort, Marchantia, drives alternative electron flow using a flavodiiron protein to protect PSI. Plant Physiol 173:1636–1647. https://doi.org/10.1104/pp.16.01038
Slattery RA, Walker BJ, Weber APM, Ort DR (2018) The impacts of fluctuating light on crop performance. Plant Physiol 176:990–1003. https://doi.org/10.1104/pp.17.01234
Sonoike K (1996) Photoinhibition of photosystem I: its physiological significance in the chilling sensitivity of plants. Plant Cell Physiol 37:239–247. https://doi.org/10.1093/oxfordjournals.pcp.a028938
Storti M, Alboresi A, Gerotto C et al (2019) Role of cyclic and pseudo-cyclic electron transport in response to dynamic light changes in Physcomitrella patens. Plant Cell Environ 42:1590–1602. https://doi.org/10.1111/pce.13493
Sun H, Zhang S-B, Liu T, Huang W (2020) Decreased photosystem II activity facilitates acclimation to fluctuating light in the understory plant Paris polyphylla. Biochim Biophys Acta Bioenerg 1861:148135. https://doi.org/10.1016/j.bbabio.2019.148135
Suorsa M, Jarvi S, Grieco M et al (2012) PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell 24:2934–2948. https://doi.org/10.1105/tpc.112.097162
Suorsa M, Rossi F, Tadini L et al (2016) PGR5-PGRL1-dependent cyclic electron transport modulates linear electron transport rate in Arabidopsis thaliana. Mol Plant 9:271–288. https://doi.org/10.1016/j.molp.2015.12.001
Takagi D, Amako K, Hashiguchi M et al (2017a) Chloroplastic ATP synthase builds up a proton motive force preventing production of reactive oxygen species in photosystem I. Plant J 91:306–324. https://doi.org/10.1111/tpj.13566
Takagi D, Ishizaki K, Hanawa H et al (2017b) Diversity of strategies for escaping reactive oxygen species production within photosystem I among land plants: P700 oxidation system is prerequisite for alleviating photoinhibition in photosystem I. Physiol Plant 161:56–74. https://doi.org/10.1111/ppl.12562
Takagi D, Takumi S, Hashiguchi M et al (2016) Superoxide and singlet oxygen produced within the thylakoid membranes both cause photosystem I photoinhibition. Plant Physiol 171:1626–1634. https://doi.org/10.1104/pp.16.00246
Tan S-L, Yang Y-J, Liu T et al (2020) Responses of photosystem I compared with photosystem II to combination of heat stress and fluctuating light in tobacco leaves. Plant Sci 292:110371. https://doi.org/10.1016/j.plantsci.2019.110371
Tikkanen M, Aro EM (2012) Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. Biochim Biophys Acta Bioenerg 1817:232–238. https://doi.org/10.1016/j.bbabio.2011.05.005
Tikkanen M, Grieco M, Kangasjarvi S, Aro E-M (2010) Thylakoid Protein Phosphorylation in Higher Plant Chloroplasts Optimizes Electron Transfer under Fluctuating Light. Plant Physiol 152:723–735. https://doi.org/10.1104/pp.109.150250
Tikkanen M, Grieco M, Nurmi M et al (2012) Regulation of the photosynthetic apparatus under fluctuating growth light. Philos Trans R Soc B Biol Sci 367:3486–3493. https://doi.org/10.1098/rstb.2012.0067
Tikkanen M, Mekala NR, Aro E-M (2014) Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage. Biochim Biophys Acta Bioenerg 1837:210–215. https://doi.org/10.1016/j.bbabio.2013.10.001
Tikkanen M, Rantala S, Aro E-M (2015) Electron flow from PSII to PSI under high light is controlled by PGR5 but not by PSBS. Front Plant Sci 6:521. https://doi.org/10.3389/fpls.2015.00521
Wada S, Yamamoto H, Suzuki Y et al (2018) Flavodiiron protein substitutes for cyclic electron flow without competing CO2 assimilation in rice. Plant Physiol 176:1509–1518. https://doi.org/10.1104/pp.17.01335
Walker BJ, Strand DD, Kramer DM, Cousins AB (2014) The response of cyclic electron flow around photosystem I to changes in photorespiration and nitrate assimilation. Plant Physiol 165:453–462. https://doi.org/10.1104/pp.114.238238
Yamamoto H, Shikanai T (2019) PGR5-dependent cyclic electron flow protects photosystem I under fluctuating light at donor and acceptor sides. Plant Physiol 179:588–600. https://doi.org/10.1104/pp.18.01343
Yamamoto H, Takahashi S, Badger MR, Shikanai T (2016) Artificial remodelling of alternative electron flow by flavodiiron proteins in Arabidopsis. Nat Plants 2:16012. https://doi.org/10.1038/nplants.2016.12
Yamauchi Y, Kimura Y, Akimoto S et al (2011) Plants switch photosystem at high temperature to protect photosystem II. Nat Preced 6:1. https://doi.org/10.1038/npre.2011.6168.1
Yamori W (2016) Photosynthetic response to fluctuating environments and photoprotective strategies under abiotic stress. J Plant Res 129:379–395. https://doi.org/10.1007/s10265-016-0816-1
Yamori W, Makino A, Shikanai T (2016) A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice. Sci Rep 6:20147. https://doi.org/10.1038/srep20147
Yan K, Chen P, Shao H et al (2013) Dissection of photosynthetic electron transport process in sweet sorghum under heat stress. PLoS ONE 8:e62100. https://doi.org/10.1371/journal.pone.0062100
Yang Y-J, Ding X-X, Huang W (2019a) Stimulation of cyclic electron flow around photosystem I upon a sudden transition from low to high light in two angiosperms Arabidopsis thaliana and Bletilla striata. Plant Sci 287:110166. https://doi.org/10.1016/j.plantsci.2019.110166
Yang Y-J, Zhang S-B, Huang W (2019b) Photosynthetic regulation under fluctuating light in young and mature leaves of the CAM plant Bryophyllum pinnatum. Biochim Biophys Acta Bioenerg 1860:469–477. https://doi.org/10.1016/j.bbabio.2019.04.006
Yang Y-J, Zhang S-B, Wang J-H, Huang W (2019c) Photosynthetic regulation under fluctuating light in field-grown Cerasus cerasoides: a comparison of young and mature leaves. Biochim Biophys Acta Bioenerg 1860:148073. https://doi.org/10.1016/j.bbabio.2019.148073
Zhang R, Cruz JA, Kramer DM et al (2009) Moderate heat stress reduces the pH component of the transthylakoid proton motive force in light-adapted, intact tobacco leaves. Plant Cell Environ 32:1538–1547. https://doi.org/10.1111/j.1365-3040.2009.02018.x
Zhang R, Sharkey TD (2009) Photosynthetic electron transport and proton flux under moderate heat stress. Photosynth Res 100:29–43. https://doi.org/10.1007/s11120-009-9420-8
Zhang S, Scheller HV (2004) Photoinhibition of photosystem I at chilling temperature and subsequent recovery in Arabidopsis thaliana. Plant Cell Physiol 45:1595–1602. https://doi.org/10.1093/pcp/pch180
Zhu XG, Ort DR, Whitmarsh J, Long SP (2004) The slow reversibility of photosystem II thermal energy dissipation on transfer from high to low light may cause large losses in carbon gain by crop canopies: a theoretical analysis. J Exp Bot 55:1167–1175. https://doi.org/10.1093/jxb/erh141
Zivcak M, Brestic M, Kunderlikova K et al (2015) Repetitive light pulse-induced photoinhibition of photosystem I severely affects CO2 assimilation and photoprotection in wheat leaves. Photosynth Res 126:449–463. https://doi.org/10.1007/s11120-015-0121-1
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Grant 31971412) and the Youth Innovation Promotion Association of the Chinese Academy of Sciences (Grant 2016347).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest to declare.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Tan, SL., Yang, YJ. & Huang, W. Moderate heat stress accelerates photoinhibition of photosystem I under fluctuating light in tobacco young leaves. Photosynth Res 144, 373–382 (2020). https://doi.org/10.1007/s11120-020-00754-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-020-00754-7