Long- and short-term acclimation of the photosynthetic apparatus to salinity in Chlamydomonas reinhardtii. The role of Stt7 protein kinase

. 2023 ; 14 () : 1051711. [epub] 20230405

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37089643

Salt stress triggers an Stt7-mediated LHCII-phosphorylation signaling mechanism similar to light-induced state transitions. However, phosphorylated LHCII, after detaching from PSII, does not attach to PSI but self-aggregates instead. Salt is a major stress factor in the growth of algae and plants. Here, our study mainly focuses on the organization of the photosynthetic apparatus to the long-term responses of Chlamydomonas reinhardtii to elevated NaCl concentrations. We analyzed the physiological effects of salt treatment at a cellular, membrane, and protein level by microscopy, protein profile analyses, transcripts, circular dichroism spectroscopy, chlorophyll fluorescence transients, and steady-state and time-resolved fluorescence spectroscopy. We have ascertained that cells that were grown in high-salinity medium form palmelloids sphere-shaped colonies, where daughter cells with curtailed flagella are enclosed within the mother cell walls. Palmelloid formation depends on the presence of a cell wall, as it was not observed in a cell-wall-less mutant CC-503. Using the stt7 mutant cells, we show Stt7 kinase-dependent phosphorylation of light-harvesting complex II (LHCII) in both short- and long-term treatments of various NaCl concentrations-demonstrating NaCl-induced state transitions that are similar to light-induced state transitions. The grana thylakoids were less appressed (with higher repeat distances), and cells grown in 150 mM NaCl showed disordered structures that formed diffuse boundaries with the flanking stroma lamellae. PSII core proteins were more prone to damage than PSI. At high salt concentrations (100-150 mM), LHCII aggregates accumulated in the thylakoid membranes. Low-temperature and time-resolved fluorescence spectroscopy indicated that the stt7 mutant was more sensitive to salt stress, suggesting that LHCII phosphorylation has a role in the acclimation and protection of the photosynthetic apparatus.

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Akhtar P., Lingvay M., Kiss T., Deák R., Bóta A., Ughy B., et al. . (2016). Excitation energy transfer between light-harvesting complex II and photosystem I in reconstituted membranes. Biochim. Biophys. Acta 1857 (4), 462–472. doi: 10.1016/j.bbabio.2016.01.016 PubMed DOI

Allakhverdiev S. I., Sakamoto A., Nishiyama Y., Inaba M., Murata N. (2000). Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiol. 123 (3), 1047–1056. doi: 10.1104/pp.123.3.1047 PubMed DOI PMC

Allen J. F., Forsberg J. (2001). Molecular recognition in thylakoid structure and function. Trends Plant Sci. 6 (7), 317–326. doi: 10.1016/S1360-1385(01)02010-6 PubMed DOI

Al-Taweel K., Iwaki T., Yabuta Y., Shigeoka S., Murata N., Wadano A. (2007). A bacterial transgene for catalase protects translation of D1 protein during exposure of salt-stressed tobacco leaves to strong light. Plant Physiol. 145 (1), 258–265. doi: 10.1104/pp.107.101733 PubMed DOI PMC

Anderson J. M., Chow W. S., Park Y. I. (1995). The grand design of photosynthesis: Acclimation of the photosynthetic apparatus to environmental cues. Photosynth. Res. 46 (1-2), 129–139. doi: 10.1007/BF00020423 PubMed DOI

Andreeva A., Stoitchkova K., Busheva M., Apostolova E. (2003). Changes in the energy distribution between chlorophyll–protein complexes of thylakoid membranes from pea mutants with modified pigment content: I. changes due to the modified pigment content. J. Photochem. Photobiol. B: Biol. 70 (3), 153–162. doi: 10.1016/S1011-1344(03)00075-7 PubMed DOI

Bailey S., Walters R. G., Jansson S., Horton P. (2001). Acclimation of Arabidopsis thaliana to the light environment: The existence of separate low light and high light responses. Planta 213 (5), 794–801. doi: 10.1007/s004250100556 PubMed DOI

Bellafiore S., Barneche F., Peltier G., Rochaix J.-D. (2005). State transitions and light adaptation require chloroplast thylakoid protein kinase Stn7. Nature 433 (7028), 892–895. doi: 10.1038/nature03286 PubMed DOI

Bennoun P. (1982). Evidence for a respiratory chain in the chloroplast. Proc. Natl. Acad. Sci. 79 (14), 4352–4356. doi: 10.1073/pnas.79.14.4352 PubMed DOI PMC

Ben-Shem A., Frolow F., Nelson N. (2003). Crystal structure of plant photosystem I. Nature 426 (6967), 630–635. doi: 10.1038/nature02200 PubMed DOI

Boekema E. J., van Breemen J. F., van Roon H., Dekker J. P. (2000). Arrangement of photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. J. Mol. Biol. 301 (5), 1123–1133. doi: 10.1006/jmbi.2000.4037 PubMed DOI

Borisova-Mubarakshina M. M., Ivanov B. N., Vetoshkina D. V., Lubimov V. Y., Fedorchuk T. P., Naydov I. A., et al. . (2015). Long-term acclimatory response to excess excitation energy: Evidence for a role of hydrogen peroxide in the regulation of photosystem II antenna size. Journal of Experimental Botany 66 (22):7151–64. doi: 10.1093/jxb/erv410 PubMed DOI

Bukhov N., Carpentier R. (2004). Alternative photosystem I-driven electron transport routes: Mechanisms and functions. Photosynth. Res. 82 (1), 17–33. doi: 10.1023/B:PRES.0000040442.59311.72 PubMed DOI

Cariti F., Chazaux M., Lefebvre-Legendre L., Longoni P., Ghysels B., Johnson X., et al. . (2020). Regulation of light harvesting in Chlamydomonas reinhardtii two protein phosphatases are involved in state transitions. Plant Physiol. 183 (4), 1749–1764. doi: 10.1104/pp.20.00384 PubMed DOI PMC

Chuartzman S. G., Nevo R., Shimoni E., Charuvi D., Kiss V., Ohad I., et al. . (2008). Thylakoid membrane remodeling during state transitions in Arabidopsis . Plant Cell 20 (4), 1029–1039. doi: 10.1105/tpc.107.055830 PubMed DOI PMC

Cournac L., Redding K., Ravenel J., Rumeau D., Josse E.-M., Kuntz M., et al. . (2000). Electron flow between photosystem II and oxygen in chloroplasts of photosystem I-deficient algae is mediated by a quinol oxidase involved in chlororespiration. J. Biol. Chem. 275 (23), 17256–17262. doi: 10.1074/jbc.M908732199 PubMed DOI

Cruz J. A., Salbilla B. A., Kanazawa A., Kramer D. M. (2001). Inhibition of plastocyanin to P700+ electron transfer in Chlamydomonas reinhardtii by hyperosmotic stress. Plant Physiol. 127 (3), 1167–1179. doi: 10.1104/pp.010328 PubMed DOI PMC

Darnovsky M. J. (1965). A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron-microscopy. Journal of Cell Biology 27: 137–138A.

Depège N., Bellafiore S., Rochaix J.-D. (2003). Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas . Science 299 (5612), 1572–1575. doi: 10.1126/science.1081397 PubMed DOI

Devadasu E., Pandey J., Dhokne K., Subramanyam R. (2021). Restoration of photosynthetic activity and supercomplexes from severe iron starvation in Chlamydomonas reinhardtii . Biochim. Biophys. Acta (BBA) Bioenergetics 1862 (1), 148331. doi: 10.1016/j.bbabio.2020.148331 PubMed DOI

Drop B., Webber-Birungi M., Yadav S. K., Filipowicz-Szymanska A., Fusetti F., Boekema E. J., et al. . (2014). Light-harvesting complex II (LHCII) and its supramolecular organization in Chlamydomonas reinhardtii . Biochim. Biophys. Acta (BBA) Bioenergetics 1837 (1), 63–72. doi: 10.1016/j.bbabio.2013.07.012 PubMed DOI

Finazzi G., Rappaport F., Furia A., Fleischmann M., Rochaix J.-D., Zito F., et al. . (2002). Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii . EMBO Rep. 3 (3), 280–285. doi: 10.1093/embo-reports/kvf047 PubMed DOI PMC

Fischer N., Sétif P., Rochaix J.-D. (1997). Targeted mutations in the psac gene of Chlamydomonas reinhardtii: Preferential reduction of FB at low temperature is not accompanied by altered electron flow from photosystem I to ferredoxin. Biochemistry 36 (1), 93–102. doi: 10.1021/bi962244v PubMed DOI

Garab G., van Amerongen H. (2009). Linear dichroism and circular dichroism in photosynthesis research. Photosynth. Res. 101 (2), 135–146. doi: 10.1007/s11120-009-9424-4 PubMed DOI PMC

Ghysels B., Godaux D., Matagne R. F., Cardol P., Franck F. (2013). Function of the chloroplast hydrogenase in the microalga Chlamydomonas: The role of hydrogenase and state transitions during photosynthetic activation in anaerobiosis. PloS One 8 (5), e64161. doi: 10.1371/journal.pone.0064161 PubMed DOI PMC

Havaux M. (1996). Short-term responses of photosystem I to heat stress: Induction of a PSII-independent electron transport through PSI fed by stromal components. Photosynth. Res. 47 (1), 85–97. doi: 10.1007/BF00017756 PubMed DOI

Hayat M. (1970). "Principles and techniques of electron microscopy. biological applications, vol. 1. New York, Cincinnati (Toronto-London, Melbourne: Van Nostrand Reinhold Co; ).

Huang Z., Shen L., Wang W., Mao Z., Yi X., Kuang T., et al. . (2021). Structure of photosystem I-LHCI-LHCII from the green alga Chlamydomonas reinhardtii in state 2. Nat. Commun. 12 (1), 1–14. doi: 10.1038/s41467-021-21362-6 PubMed DOI PMC

Jensen P. E., Rosgaard L., Knoetzel J. R., Scheller H. V. (2002). Photosystem I activity is increased in the absence of the PSI-G subunit. J. Biol. Chem. 277 (4), 2798–2803. doi: 10.1074/jbc.M110448200 PubMed DOI

Kirchhoff H., Hinz H.-J., Rösgen J. (2003). Aggregation and fluorescence quenching of chlorophyll a of the light-harvesting complex II from spinach in vitro. Biochim. Biophys. Acta (BBA) Bioenergetics 1606 (1-3), 105–116. doi: 10.1016/S0005-2728(03)00105-1 PubMed DOI

Lelong C., Boekema E. J., Kruip J., Bottin H., Rögner M., Sétif P. (1996). Characterization of a redox active cross-linked complex between cyanobacterial photosystem I and soluble ferredoxin. EMBO J. 15 (9), 2160–2168. doi: 10.1002/j.1460-2075.1996.tb00569.x PubMed DOI PMC

Lockwood D. (2019). Lakes and rivers are getting saltier. ACS Central Science 5 (3), 376–379. doi: 10.1021/acscentsci.9b00191 PubMed DOI PMC

Lu C., Vonshak A. (2002). Effects of salinity stress on photosystem II function in cyanobacterial Spirulina platensis cells. Physiologia Plantarum 114 (3), 405–413. doi: 10.1034/j.1399-3054.2002.1140310.x PubMed DOI

Lunde C., Jensen P. E., Haldrup A., Knoetzel J., Scheller H. V. (2000). The PSI-h subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature 408 (6812), 613–615. doi: 10.1038/35046121 PubMed DOI

Lurling M., Beekman W. (2006). "Palmelloids formation in Chlamydomonas reinhardtii: Defence against rotifer predators?", in: Annales de limnologie-international journal of limnology. EDP Sci., 65–72. doi: 10.1051/limn/2006010 DOI

Madireddi S. K., Nama S., Devadasu E., Subramanyam R. (2019). Thylakoid membrane dynamics and state transitions in Chlamydomonas reinhardtii under elevated temperature. Photosynth. Res. 139 (1), 215–226. doi: 10.1007/s11120-018-0562-4 PubMed DOI

Mastrobuoni G., Irgang S., Pietzke M., Assmus H. E., Wenzel M., Schulze W. X., et al. . (2012). Proteome dynamics and early salt stress response of the photosynthetic organism Chlamydomonas reinhardtii . BMC Genomics 13, 215. doi: 10.1186/1471-2164-13-215 PubMed DOI PMC

Measho S., Li F., Pellikka P., Tian C., Hirwa H., Xu N., et al. . (2022). Soil salinity variations and associated implications for agriculture and land resources development using remote sensing datasets in central Asia. Remote Sens. 14 (10), 2501. doi: 10.3390/rs14102501 DOI

Minagawa J. (2011). State transitions–the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochim. Biophys. Acta (BBA) Bioenergetics 1807 (8), 897–905. doi: 10.1016/j.bbabio.2010.11.005 PubMed DOI

Minagawa J. (2013). Dynamic reorganization of photosynthetic supercomplexes during environmental acclimation of photosynthesis. Front. Plant Sci. 4, 513. doi: 10.3389/fpls.2013.00513 PubMed DOI PMC

Montané M.-H., Tardy F., Kloppstech K., Havaux M. (1998). Differential control of xanthophylls and light-induced stress proteins, as opposed to light-harvesting chlorophyll a/b proteins, during photosynthetic acclimation of barley leaves to light irradiance. Plant Physiol. 118 (1), 227–235. doi: 10.1104/pp.118.1.227 PubMed DOI PMC

Moulton T., Bell G. (2013). Selecting for multicellularity in the unicellular alga Chlamydomonas reinhardtii . McGill Sci. Undergraduate Res. J. 8 (1), 30–38. doi: 10.26443/msurj.v8i1.108 DOI

Murata N., Miyao M. (1985). Extrinsic membrane proteins in the photosynthetic oxygen-evolving complex. Trends Biochem. Sci. 10 (3), 122–124. doi: 10.1016/0968-0004(85)90272-5 DOI

Murata N., Nishimura M., Takamiya A. (1966). Fluorescence of chlorophyll in photosynthetic systems III. emission and action spectra of "uorescence–three emission bands of chlorophyll a and the energy transfer between two pigment systems. Biochim. Biophys. Acta (BBA) Biophys. including Photosynth. 126 (2), 234–243. doi: 10.1016/0926-6585(66)90059-8 PubMed DOI

Nagy G., Ünnep R., Zsiros O., Tokutsu R., Takizawa K., Porcar L., et al. . (2014). Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo . Proc. Natl. Acad. Sci. 111 (13), 5042–5047. doi: 10.1073/pnas.1322494111 PubMed DOI PMC

Naumann B., Stauber E. J., Busch A., Sommer F., Hippler M. (2005). N-terminal processing of Lhca3 is a key step in remodeling of the photosystem I-Light-Harvesting complex under iron deficiency in Chlamydomonas reinhardtii . J. Biol. Chem. 280 (21), 20431–20441. doi: 10.1074/jbc.M414486200 PubMed DOI

Neelam S., Subramanyam R. (2013). Alteration of photochemistry and protein degradation of photosystem II from Chlamydomonas reinhardtii under high salt grown cells. J. Photochem. Photobiol. B: Biol. 124, 63–70. doi: 10.1016/j.jphotobiol.2013.04.007 PubMed DOI

Nellaepalli S., Kodru S., Raghavendra A. S., 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: Biol. 146, 24–33. doi: 10.1016/j.jphotobiol.2015.02.013 PubMed DOI

Nellaepalli S., Kodru S., Tirupathi M., Subramanyam R. (2012). Anaerobiosis induced state transition: A non photochemical reduction of PQ pool mediated by NDH in Arabidopsis thaliana . PloS One 7 (11), e49839. doi: 10.1371/journal.pone.0049839 PubMed DOI PMC

Nellaepalli S., Mekala N. R., Zsiros O., Mohanty P., Subramanyam R. (2011). Moderate heat stress induces state transitions in Arabidopsis thaliana . Biochim. Biophys. Acta (BBA) Bioenergetics 1807 (9), 1177–1184. doi: 10.1016/j.bbabio.2011.05.016 PubMed DOI

Nikolova D., Weber D., Scholz M., Bald T., Scharsack J. P., Hippler M. (2017). Temperature-induced remodeling of the photosynthetic machinery tunes photosynthesis in the thermophilic alga Cyanidioschyzon merolae . Plant Physiol. 174 (1), 35–46. doi: 10.1104/pp.17.00110 PubMed DOI PMC

Ossenbühl F., Goühre V., Meurer J. R., Krieger-Liszkay A., Rochaix J.-D., Eichacker L. A. (2004). Efficient assembly of photosystem II in Chlamydomonas reinhardtii requires Alb3. 1p, a homolog of arabidopsis Albino3. Plant Cell 16 (7), 1790–1800. doi: 10.1105/tpc.023226 PubMed DOI PMC

Parida A., Das A., Mittra B. (2003). Effects of NaCl stress on the structure, pigment complex composition, and photosynthetic activity of mangrove Bruguiera parviflora chloroplasts. Photosynthetica 41 (2), 191. doi: 10.1023/B:PHOT.0000011951.37231.69 DOI

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. Biochim. Biophys. Acta (BBA) Bioenergetics 975 (3), 384–394. doi: 10.1016/S0005-2728(89)80347-0 DOI

Pribil M., Pesaresi P., Hertle A., Barbato R., Leister D. (2010). Role of plastid protein phosphatase Tap38 in LHCII dephosphorylation and thylakoid electron flow. PloS Biol. 8 (1), e1000288. doi: 10.1371/journal.pbio.1000288 PubMed DOI PMC

Reynolds E. S. (1963). The use of lead citrate at high ph as an electron-opaque stain in electron microscopy. J. Cell Biol. 17 (1), 208. doi: 10.1083/jcb.17.1.208 PubMed DOI PMC

Schägger H., von Jagow G. (1991). Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199 (2), 223–231. doi: 10.1016/0003-2697(91)90094-A PubMed DOI

Shapiguzov A., Ingelsson B., Samol I., Andres C., Kessler F., Rochaix J.-D., et al. . (2010). The Pph1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis . Proc. Natl. Acad. Sci. 107 (10), 4782–4787. doi: 10.1073/pnas.0913810107 PubMed DOI PMC

Subramanyam R., Jolley C., Brune D. C., Fromme P., Webber A. N. (2006). Characterization of a novel photosystem I–LHCI supercomplex isolated from Chlamydomonas reinhardtii under anaerobic (State II) conditions. FEBS Lett. 580 (1), 233–238. doi: 10.1016/j.febslet.2005.12.003 PubMed DOI

Subramanyam R., Jolley C., Thangaraj B., Nellaepalli S., Webber A. N., 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. doi: 10.1007/s00425-009-1097-x PubMed DOI

Sudhir P.-R., Pogoryelov D., Kovács L., Garab G., Murthy S. D. (2005). The effects of salt stress on photosynthetic electron transport and thylakoid membrane proteins in the cyanobacterium Spirulina platensis . BMB Rep. 38 (4), 481–485. doi: 10.5483/BMBRep.2005.38.4.481 PubMed DOI

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. doi: 10.1073/pnas.0509952103 PubMed DOI PMC

Tiwari B., Bose A., Ghosh B. (1998). Photosynthesis in rice under a salt stress. Photosynthetica 34 (2), 303–306. doi: 10.1023/A:1006857027398 DOI

Towbin H., Staehelin T., Gordon J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl. Acad. Sci. 76 (9), 4350–4354. doi: 10.1073/pnas.76.9.4350 PubMed DOI PMC

Unlu 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. 111 (9), 3460–3465. doi: 10.1073/pnas.1319164111 PubMed DOI PMC

Varotto C., Pesaresi P., Jahns P., Leßnick A., Tizzano M., Schiavon F., et al. . (2002). Single and double knockouts of the genes for photosystem I subunits G, K, and h of Arabidopsis. effects on photosystem I composition, photosynthetic electron flow, and state transitions. Plant Physiol. 129 (2), 616–624. doi: 10.1104/pp.002089 PubMed DOI PMC

Verma K., Mohanty P. (2000). Changes of the photosynthetic apparatus in Spirulina cyanobacterium by sodium stress. Z. fuer Naturforschung. Section C 55 (1-2), 16–22. doi: 10.1515/znc-2000-1-205 PubMed DOI

Yadavalli V., Jolley C. C., Malleda C., Thangaraj B., Fromme P., Subramanyam R. (2012). Alteration of proteins and pigments influence the function of photosystem I under iron deficiency from Chlamydomonas reinhardtii . PloS One 7 (4), e35084. doi: 10.1371/journal.pone.0035084 PubMed DOI PMC

Yamamoto Y. (2001). Quality control of photosystem II. Plant Cell Physiol. 42 (2), 121–128. doi: 10.1093/pcp/pce022 PubMed DOI

Yamamoto Y., Aminaka R., Yoshioka M., Khatoon M., Komayama K., Takenaka D., et al. . (2008). Quality control of photosystem II: Impact of light and heat stresses. Photosynth. Res. 98 (1), 589–608. doi: 10.1007/s11120-008-9372-4 PubMed DOI

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In appreciation of an ingenious scientist and a great friend: Győző Garab

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