Abstract
Moderately elevated temperatures can induce state transitions in higher plants by phosphorylation of light-harvesting complex II (LHCII). In this study, we exposed unicellular algae Chlamydomonas reinhardtii to moderately elevated temperatures (38 °C) for short period of time in the dark to understand the thylakoid membrane dynamics and state transition mechanism. Here we report that under elevated temperatures (1) LHCII gets phosphorylated similar to higher plants and (2) there is decreased absorption cross section of photosystem II (PSII), whereas (3) there is no change in absorption cross section of photosystem I (PSI) indicating that LHCII trimers are largely disconnected with both photosystems under moderately elevated temperatures and (4) on return to room temperature after elevated temperature treatment there is a formation of state transition complex comprising of PSII–LHCII–PSI. The temperature-induced state transition mechanism also depends on stt7 kinase-like in light-induced state transition. The protein content was stable at the moderately elevated temperature treatment of 40 °C; however, at 45 °C severe downregulation in photosynthetic performance and protein content was observed. In addition to the known changes to photosynthetic apparatus, elevated temperatures can destabilize the PSII–LHCII complex that can result in decreased photosynthetic efficiency in C. reinhardtii. We concluded that the membrane dynamics of light-induced state transitions differs considerably from temperature-induced state transition mechanisms in C. reinhardtii.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allakhverdiev SI, Hayashi H, Nishiyama Y, Ivanov AG, Aliev JA, Klimov VV, Murata N, Carpentier R (2003) Glycinebetaine protects the D1/D2/Cytb559 complex of photosystem II against photo-induced and heat-induced inactivation. J Plant Physiol 160(1):41–49. https://doi.org/10.1078/0176-1617-00845
Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98(1–3):541–550. https://doi.org/10.1007/s11120-008-9331-0
Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098(3):275–335. https://doi.org/10.1016/S0005-2728(09)91014-3
Allen JF, Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6(7):317–326. https://doi.org/10.1016/S1360-1385(01)02010-6
Armond PA, Bjorkman O, Staehelin LA (1980) Dissociation of supramolecular complexes in chloroplast membranes. A manifestation of heat damage to the photosynthetic apparatus. Biochim Biophys Acta 601(3):433–443. https://doi.org/10.1016/0005-2736(80)90547-7
Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31(1):491–543. https://doi.org/10.1146/annurev.pp.31.060180.002423
Boucher N, Harnois J, Carpentier R (1990) Heat-stress stimulation of electron flow in a photosystem I submembrane fraction. Biochem Cell Biol 68(7–8):999–1004. https://doi.org/10.1139/o90-147
Brestic M, Zivcak M, Kunderlikova K, Sytar O, Shao H, Kalaji HM, Allakhverdiev SI (2015) Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines. Photosynth Res 125(1–2):151–166. https://doi.org/10.1007/s11120-015-0093-1
Bukhov N, Carpentier R (2004) Alternative photosystem I-driven electron transport routes: mechanisms and functions. Photosynth Res 82(1):17–33. https://doi.org/10.1023/b:pres.0000040442.59311.72
Carratu L, Franceschelli S, Pardini CL, Kobayashi GS, Horvath I, Vigh L, Maresca B (1996) Membrane lipid perturbation modifies the set point of the temperature of heat shock response in yeast. Proc Natl Acad Sci USA 93(9):3870–3875
Chua N-H, Bennoun P (1975) Thylakoid membrane polypeptides of Chlamydomonas reinhardtii: wild-type and mutant strains deficient in photosystem II reaction center. Proc Natl Acad Sci USA 72(6):2175–2179. https://doi.org/10.1073/pnas.72.6.2175
Delosme R, Olive J, Wollman F-A (1996) Changes in light energy distribution upon state transitions: an in vivo photoacoustic study of the wild type and photosynthesis mutants from Chlamydomonas reinhardtii. Biochim Biophys Acta 1273(2):150–158. https://doi.org/10.1016/0005-2728(95)00143-3
Dinc E, Tian L, Roy LM, Roth R, Goodenough U, Croce R (2016) LHCSR1 induces a fast and reversible pH-dependent fluorescence quenching in LHCII in Chlamydomonas reinhardtii cells. Proc Natl Acad Sci USA 113(27):7673–7678. https://doi.org/10.1073/pnas.1605380113
Enami I, Kitamura M, Tomo T, Isokawa Y, Ohta H, Katoh S (1994) Is the primary cause of thermal inactivation of oxygen evolution in spinach PS II membranes release of the extrinsic 33 kDa protein or of Mn? Biochim Biophys Acta 1186(1):52–58. https://doi.org/10.1016/0005-2728(94)90134-1
Galka P, Santabarbara S, Khuong TT, Degand H, Morsomme P, Jennings RC, Boekema EJ, Caffarri S (2012) Functional analyses of the plant photosystem I-light-harvesting complex II supercomplex reveal that light-harvesting complex II loosely bound to photosystem II is a very efficient antenna for photosystem I in state II. Plant Cell 24(7):2963–2978. https://doi.org/10.1105/tpc.112.100339
Gorman DS, Levine RP (1965) Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proc Natl Acad Sci USA 54(6):1665–1669. https://doi.org/10.1073/pnas.54.6.1665
Grieco M, Suorsa M, Jajoo A, Tikkanen M, Aro EM (2015) Light-harvesting II antenna trimers connect energetically the entire photosynthetic machinery - including both photosystems II and I. Biochim Biophys Acta 1847(6–7):607–619. https://doi.org/10.1016/j.bbabio.2015.03.004
Havaux M (1996) Short-term responses of Photosystem I to heat stress: Induction of a PS II-independent electron transport through PS I fed by stromal components. Photosynth Res 47(1):85–97. https://doi.org/10.1007/bf00017756
Inaba M, Suzuki I, Szalontai B, Kanesaki Y, Los DA, Hayashi H, Murata N (2003) Gene-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in synechocystis. J Biol Chem 278(14):12191–12198. https://doi.org/10.1074/jbc.M212204200
Ivanov AG, Velitchkova MY (1990) Heat-induced changes in the efficiency of P700 photo-oxidation in pea chloroplast membranes. J Photochem Photobiol B 4(3):307–320. https://doi.org/10.1016/1011-1344(90)85036-V
Ivanov AG, Rosso D, Savitch LV, Stachula P, Rosembert M, Oquist G, Hurry V, Huner NP (2012) Implications of alternative electron sinks in increased resistance of PSII and PSI photochemistry to high light stress in cold-acclimated Arabidopsis thaliana. Photosynth Res 113(1–3):191–206. https://doi.org/10.1007/s11120-012-9769-y
Ivanov AG, Velitchkova MY, Allakhverdiev SI, Huner NPA (2017) Heat stress-induced effects of photosystem I: an overview of structural and functional responses. Photosynth Res 133(1–3):17–30. https://doi.org/10.1007/s11120-017-0383-x
Iwai M, Yokono M, Inada N, Minagawa J (2010) Live-cell imaging of photosystem II antenna dissociation during state transitions. Proc Natl Acad Sci USA 107(5):2337–2342. https://doi.org/10.1073/pnas.0908808107
Klimov VV, Shafiev MA, Allakhverdiev SI (1990) Photoinactivation of the reactivation capacity of photosystem II in pea subchloroplast particles after a complete removal of manganese. Photosynth Res 23(1):59–65. https://doi.org/10.1007/BF00030063
Kouril R, Zygadlo A, Arteni AA, de Wit CD, Dekker JP, Jensen PE, Scheller HV, Boekema EJ (2005) Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 44(33):10935–10940. https://doi.org/10.1021/bi051097a
Kouřil R, Lazár D, Ilík P, Skotnica J, Krchňák P, Nauš J (2004) High-temperature induced chlorophyll fluorescence rise in plants at 40–50 °C: experimental and theoretical approach. Photosynth Res 81(1):49–66. https://doi.org/10.1023/B:PRES.0000028391.70533.eb
Krumova SB, Várkonyi Z, Lambrev PH, Kovács L, Todinova SJ, Busheva MC, Taneva SG, Garab G (2014) Heat- and light-induced detachment of the light-harvesting antenna complexes of photosystem I in isolated stroma thylakoid membranes. J Photochem Photobiol B 137(Supplement C):4–12. https://doi.org/10.1016/j.jphotobiol.2014.04.029
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685. https://doi.org/10.1038/227680a0
Law RD, Crafts-Brandner SJ (1999) Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant physiol 120(1):173–182. https://doi.org/10.1104/pp.120.1.173
Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666(1–2):142–157. https://doi.org/10.1016/j.bbamem.2004.08.002
McDonald AE, Ivanov AG, Bode R, Maxwell DP, Rodermel SR, Huner NP (2011) Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX). Biochim Biophys Acta 1807(8):954–967. https://doi.org/10.1016/j.bbabio.2010.10.024
Minagawa J (2011) State transitions—the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochim Biophys Acta 1807(8):897–905. https://doi.org/10.1016/j.bbabio.2010.11.005
Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37(3):118–125. https://doi.org/10.1016/j.tibs.2011.11.007
Mohanty P, Vani B, Prakash JS (2002) Elevated temperature treatment induced alteration in thylakoid membrane organization and energy distribution between the two photosystems in Pisum sativum. Z Naturforsch C 57(9–10):836–842. https://doi.org/10.1515/znc-2002-9-1014
Mohanty P, Allakhverdiev SI, Murata N (2007) Application of low temperatures during photoinhibition allows characterization of individual steps in photodamage and the repair of photosystem II. Photosynth Res 94(2):217–224. https://doi.org/10.1007/s11120-007-9184-y
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767(6):414–421. https://doi.org/10.1016/j.bbabio.2006.11.019
Nash D, Miyao M, Murata N (1985) Heat inactivation of oxygen evolution in Photosystem II particles and its acceleration by chloride depletion and exogenous manganese. Biochim Biophys Acta 807(2):127–133. https://doi.org/10.1016/0005-2728(85)90115-X
Nellaepalli S, Mekala NR, Zsiros O, Mohanty P, Subramanyam R (2011) Moderate heat stress induces state transitions in Arabidopsis thaliana. Biochim Biophys Acta 1807(9):1177–1184. https://doi.org/10.1016/j.bbabio.2011.05.016
Nellaepalli S, Kodru S, Subramanyam R (2012a) Effect of cold temperature on regulation of state transitions in Arabidopsis thaliana. J Photochem Photobiol B 112:23–30. https://doi.org/10.1016/j.jphotobiol.2012.04.003
Nellaepalli S, Kodru S, Tirupathi M, Subramanyam R (2012b) Anaerobiosis induced state transition: a non photochemical reduction of PQ pool mediated by NDH in Arabidopsis thaliana. PLoS ONE 7(11):e49839. https://doi.org/10.1371/journal.pone.0049839
Nellaepalli S, Zsiros O, Tóth T, Yadavalli V, Garab G, Subramanyam R, Kovács L (2014) Heat- and light-induced detachment of the light harvesting complex from isolated photosystem I supercomplexes. J Photochem Photobiol B 137(Supplement C):13–20. https://doi.org/10.1016/j.jphotobiol.2014.04.026
Nellaepalli S, Kodru S, Raghavendra AS, Subramanyam R (2015) Antimycin A sensitive pathway independent from PGR5 cyclic electron transfer triggers non-photochemical reduction of PQ pool and state transitions in Arabidopsis thaliana. J Photochem Photobiol B 146:24–33. https://doi.org/10.1016/j.jphotobiol.2015.02.013
Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A, Murata N (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 20(20):5587–5594. https://doi.org/10.1093/emboj/20.20.5587
Osmond CB (1981) Photorespiration and photoinhibition: some implications for the energetics of photosynthesis. Biochim Biophys Acta 639(2):77–98. https://doi.org/10.1016/0304-4173(81)90006-9
Paredes M, Quiles MJ (2013) Stimulation of chlororespiration by drought under heat and high illumination in Rosa meillandina. J Plant Physiol 170(2):165–171. https://doi.org/10.1016/j.jplph.2012.09.010
Porra RJ, Thompson WA, Kriedemann PE (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. Biochim Biophys Acta 975(3):384–394. https://doi.org/10.1016/S0005-2728(89)80347-0
Rochaix J-D (2013) Redox regulation of thylakoid protein kinases and photosynthetic gene expression. Antioxid Redox Signal 18(16):2184–2201. https://doi.org/10.1089/ars.2012.5110
Salvucci ME, Crafts-Brandner SJ (2004) Relationship between the heat tolerance of photosynthesis and the thermal stability of rubisco activase in plants from contrasting thermal environments. Plant physiol 134(4):1460–1470. https://doi.org/10.1104/pp.103.038323
Schwenkert S, Umate P, Bosco CD, Volz S, Mlçochová L, Zoryan M, Eichacker LA, Ohad I, Herrmann RG, Meurer J (2006) PsbI affects the stability, function, and phosphorylation patterns of photosystem II assemblies in tobacco. J Biol Chem 281(45):34227–34238. https://doi.org/10.1074/jbc.M604888200
Subramanyam R, Jolley C, Thangaraj B, Nellaepalli S, Webber AN, Fromme P (2010) Structural and functional changes of PSI-LHCI supercomplexes of Chlamydomonas reinhardtii cells grown under high salt conditions. Planta 231(4):913–922. https://doi.org/10.1007/s00425-009-1097-x
Takahashi H, Iwai M, Takahashi Y, Minagawa J (2006) Identification of the mobile light-harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 103(2):477–482. https://doi.org/10.1073/pnas.0509952103
Tang Y, Wen X, Lu Q, Yang Z, Cheng Z, Lu C (2007) Heat stress induces an aggregation of the light-harvesting complex of photosystem II in spinach plants. Plant physiol 143(2):629
Ünlü C, Drop B, Croce R, van Amerongen H (2014) State transitions in Chlamydomonas reinhardtii strongly modulate the functional size of photosystem II but not of photosystem I. Proc Natl Acad Sci USA 111(9):3460–3465. https://doi.org/10.1073/pnas.1319164111
van Oort B, van Hoek A, Ruban AV, van Amerongen H (2007) Aggregation of light-harvesting complex II leads to formation of efficient excitation energy traps in monomeric and trimeric complexes. FEBS Lett 581(18):3528–3532. https://doi.org/10.1016/j.febslet.2007.06.070
Wen X, Gong H, Lu C (2005) Heat stress induces a reversible inhibition of electron transport at the acceptor side of photosystem II in a cyanobacterium Spirulina platensis. Plant Sci 168(6):1471–1476. https://doi.org/10.1016/j.plantsci.2005.01.015
Yadavalli V, Malleda C, Subramanyam R (2011) Protein-protein interactions by molecular modeling and biochemical characterization of PSI-LHCI supercomplexes from Chlamydomonas reinhardtii. Mol Biosyst 7(11):3143–3151. https://doi.org/10.1039/c1mb05218g
Yokono M, Takabayashi A, Akimoto S, Tanaka A (2015) A megacomplex composed of both photosystem reaction centres in higher plants. Nat Commun 6:6675. https://doi.org/10.1038/ncomms7675
Acknowledgements
R.S was financially supported by the Department of Biotechnology (BT-BRB-TF-1-2012; BT/PR14964/BPA/118/137/2015), Council of Scientific and Industrial Research [No. 38(1279)/11/EMR-II and No. 38 (1381)/14/EMR-II and DST-FIST], Govt. of India. We thank Michael Christopher, Buckingham, UK for English corrections. SM acknowledged UGC for fellowship (JRF/SRF).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Madireddi, S.K., Nama, S., Devadasu, E. et al. Thylakoid membrane dynamics and state transitions in Chlamydomonas reinhardtii under elevated temperature. Photosynth Res 139, 215–226 (2019). https://doi.org/10.1007/s11120-018-0562-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-018-0562-4