Accumulation of geranylgeranylated chlorophylls in the pigment-protein complexes of Arabidopsis thaliana acclimated to green light: effects on the organization of light-harvesting complex II and photosystem II functions

. 2021 Aug ; 149 (1-2) : 233-252. [epub] 20210504

Jazyk angličtina Země Nizozemsko Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33948813

Grantová podpora
19-13637S Grantová Agentura České Republiky
18-12178S Grantová Agentura České Republiky
CZ.02.1.01/0.0/0.0/16_019/0000797 Ministerstvo Školství, Mládeže a Tělovýchovy
LM2018123 Ministerstvo Školství, Mládeže a Tělovýchovy
K 128679 Hungarian Scientific Research Fund

Odkazy

PubMed 33948813
PubMed Central PMC8382614
DOI 10.1007/s11120-021-00827-1
PII: 10.1007/s11120-021-00827-1
Knihovny.cz E-zdroje

Light quality significantly influences plant metabolism, growth and development. Recently, we have demonstrated that leaves of barley and other plant species grown under monochromatic green light (500-590 nm) accumulated a large pool of chlorophyll a (Chl a) intermediates with incomplete hydrogenation of their phytyl chains. In this work, we studied accumulation of these geranylgeranylated Chls a and b in pigment-protein complexes (PPCs) of Arabidopsis plants acclimated to green light and their structural-functional consequences on the photosynthetic apparatus. We found that geranylgeranylated Chls are present in all major PPCs, although their presence was more pronounced in light-harvesting complex II (LHCII) and less prominent in supercomplexes of photosystem II (PSII). Accumulation of geranylgeranylated Chls hampered the formation of PSII and PSI super- and megacomplexes in the thylakoid membranes as well as their assembly into chiral macrodomains; it also lowered the temperature stability of the PPCs, especially that of LHCII trimers, which led to their monomerization and an anomaly in the photoprotective mechanism of non-photochemical quenching. Role of geranylgeranylated Chls in adverse effects on photosynthetic apparatus of plants acclimated to green light is discussed.

Zobrazit více v PubMed

Akhtar P, Dorogi M, Pawlak K, Kovács L, Bóta A, Kiss T, Garab G, Lambrev PH. Pigment interactions in light-harvesting complex II in different molecular environments. J Biol Chem. 2015;290(8):4877–4886. doi: 10.1074/jbc.M114.607770. PubMed DOI PMC

Akhtar P, Görföl F, Garab G, Lambrev PH. Dependence of chlorophyll fluorescence quenching on the lipid-to-protein ratio in reconstituted light-harvesting complex II membranes containing lipid labels. Chem Phys. 2019;522:242–248. doi: 10.1016/j.chemphys.2019.03.012. DOI

Amunts A, Toporik H, Borovikova A, Nelson N. Structure determination and improved model of plant photosystem I. J Biol Chem. 2010;285(5):3478–3486. doi: 10.1074/jbc.M109.072645. PubMed DOI PMC

Anderson JM, Chow WS, De Las RJ. Dynamic flexibility in the structure and function of photosystem II in higher plant thylakoid membranes: the grana enigma. Photosynth Res. 2008;98(1–3):575–587. doi: 10.1007/s11120-008-9381-3. PubMed DOI

Andreeva A, Stoitchkova K, Busheva M, Apostolova E. 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. 2003;70(3):153–162. doi: 10.1016/s1011-1344(03)00075-7. PubMed DOI

Barzda V, Mustárdy L, Garab G. Size dependency of circular-dichroism in macroaggregates of photosynthetic pigment-protein complexes. Biochemistry. 1994;33(35):10837–10841. doi: 10.1021/bi00201a034. PubMed DOI

Battle MW, Vegliani F, Jones MA. Shades of green: untying the knots of green photoperception. J Exp Bot. 2020 doi: 10.1093/jxb/eraa312. PubMed DOI PMC

Belgio E, Johnson MP, Juric S, Ruban AV. Higher plant photosystem II light-harvesting antenna, not the reaction center, determines the excited-state lifetime-both the maximum and the nonphotochemically quenched. Biophys J. 2012;102(12):2761–2771. doi: 10.1016/j.bpj.2012.05.004. PubMed DOI PMC

Bollivar DW. Recent advances in chlorophyll biosynthesis. Photosynth Res. 2006;90(2):173–194. doi: 10.1007/s11120-006-9076-6. PubMed DOI

Bollivar DW, Wang SJ, Allen JP, Bauer CE. Molecular-genetic analysis of terminal steps in bacteriochlorophyll a biosynthesis—characterization of a rhodobacter-capsulatus strain that synthesizes geranylgeraniol-esterified bacteriochlorophyll A. Biochemistry. 1994;33(43):12763–12768. doi: 10.1021/bi00209a006. PubMed DOI

Bourget CM. An introduction to light-emitting diodes. HortScience. 2008;43(7):1944–1946. doi: 10.21273/Hortsci.43.7.1944. DOI

Brodersen CR, Vogelmann TC. Do changes in light direction affect absorption profiles in leaves? Funct Plant Biol. 2010;37(5):403–412. doi: 10.1071/Fp09262. DOI

Buschmann C. Variation of the quenching of chlorophyll fluorescence under different intensities of the actinic light in wildtype plants of tobacco and in an aurea mutant deficient of light-harvesting-complex. J Plant Physiol. 1995;145(3):245–252. doi: 10.1016/S0176-1617(11)81884-5. DOI

Buschmann C. Variability and application of the chlorophyll fluorescence emission ratio red/far-red of leaves. Photosynth Res. 2007;92(2):261–271. doi: 10.1007/s11120-007-9187-8. PubMed DOI

Caffarri S, Tibiletti T, Jennings RC, Santabarbara S. A comparison between plant photosystem I and photosystem II architecture and functioning. Curr Protein Pept Sc. 2014;15(4):296–331. doi: 10.2174/1389203715666140327102218. PubMed DOI PMC

Chen K, Rios JJ, Perez-Galvez A, Roca M. Development of an accurate and high-throughput methodology for structural comprehension of chlorophylls derivatives. (I) Phytylated derivatives. J Chromatogr A. 2015;1406:99–108. doi: 10.1016/j.chroma.2015.05.072. PubMed DOI

Chmeliov J, Gelzinis A, Songaila E, Augulis R, Duffy CDP, Ruban AV, Valkunas L. The nature of self-regulation in photosynthetic light-harvesting antenna. Nat Plants. 2016 doi: 10.1038/Nplants.2016.45. PubMed DOI

Chmeliov J, Gelzinis A, Franckevicius M, Tutkus M, Saccon F, Ruban AV, Valkunas L. Aggregation-related nonphotochemical quenching in the photosynthetic membrane. J Phys Chem Lett. 2019;10(23):7340–7346. doi: 10.1021/acs.jpclett.9b03100. PubMed DOI

Chow WS, Kim EH, Horton P, Anderson JM. Granal stacking of thylakoid membranes in higher plant chloroplasts: the physicochemical forces at work and the functional consequences that ensue. Photochem Photobiol Sci. 2005;4(12):1081–1090. doi: 10.1039/b507310n. PubMed DOI

Crepin A, Santabarbara S, Caffarri S. Biochemical and spectroscopic characterization of highly stable photosystem II supercomplexes from Arabidopsis. J Biol Chem. 2016;291(36):19157–19171. doi: 10.1074/jbc.M116.738054. PubMed DOI PMC

Cseh Z, Rajagopal S, Tsonev T, Busheva M, Papp E, Garab G. Thermooptic effect in chloroplast thylakoid membranes. Thermal and light stability of pigment arrays with different levels of structural complexity. Biochemistry. 2000;39(49):15250–15257. doi: 10.1021/bi001600d. PubMed DOI

Darko E, Heydarizadeh P, Schoefs B, Sabzalian MR. Photosynthesis under artificial light: the shift in primary and secondary metabolism. Philos Trans Royal Soc B Biol Sci. 2014 doi: 10.1098/rstb.2013.0243. PubMed DOI PMC

DeLucia EH, Nelson K, Vogelmann TC, Smith WK. Contribution of intercellular reflectance to photosynthesis in shade leaves. Plant Cell Environ. 1996;19(2):159–170. doi: 10.1111/j.1365-3040.1996.tb00237.x. DOI

Dobrikova AG, Várkonyi Z, Krumova SB, Kovács L, Kostov GK, Todinova SJ, Busheva MC, Taneva SG, Garab G. Structural rearrangements in chloroplast thylakoid membranes revealed by differential scanning calorimetry and circular dichroism spectroscopy. Thermo-optic effect. Biochemistry. 2003;42(38):11272–11280. doi: 10.1021/bi034899j. PubMed DOI

Färber A, Jahns P. The xanthophyll cycle of higher plants: influence of antenna size and membrane organization. Biochim Biophys Acta Bioenerg. 1998;1363(1):47–58. doi: 10.1016/S0005-2728(97)00093-5. PubMed DOI

Garab G. Hierarchical organization and structural flexibility of thylakoid membranes. Biochim Biophys Acta Bioenerg. 2014;1837(4):481–494. doi: 10.1016/j.bbabio.2013.12.003. PubMed DOI

Garab G. Self-assembly and structural-functional flexibility of oxygenic photosynthetic machineries: personal perspectives. Photosynth Res. 2016;127(1):131–150. doi: 10.1007/s11120-015-0192-z. PubMed DOI

Garab G, van Amerongen H. Linear dichroism and circular dichroism in photosynthesis research. Photosynth Res. 2009;101(2–3):135–146. doi: 10.1007/s11120-009-9424-4. PubMed DOI PMC

Garab G, Kieleczawa J, Sutherland JC, Bustamante C, Hind G. Organization of pigment protein complexes into macrodomains in the thylakoid membranes of wild-type and chlorophyll-B-less mutant of barley as revealed by circular-dichroism. Photochem Photobiol. 1991;54(2):273–281. doi: 10.1111/j.1751-1097.1991.tb02016.x. DOI

Garab G, Cseh Z, Kovács L, Rajagopal S, Várkonyi Z, Wentworth M, Mustárdy L, Der A, Ruban AV, Papp E, Holzenburg A, Horton P. Light-induced trimer to monomer transition in the main light-harvesting antenna complex of plants: thermo-optic mechanism. Biochemistry. 2002;41(51):15121–15129. doi: 10.1021/bi026157g. PubMed DOI

Gáspár L, Sárvári E, Morales F, Szigeti Z. Presence of ‘PSI free’ LHCI and monomeric LHCII and subsequent effects on fluorescence characteristics in lincomycin treated maize. Planta. 2006;223(5):1047–1057. doi: 10.1007/s00425-005-0149-0. PubMed DOI

Georgakopoulou S, van der Zwan G, Bassi R, van Grondelle R, van Amerongen H, Croce R. Understanding the changes in the circular dichroism of light harvesting complex II upon varying its pigment composition and organization. Biochemistry. 2007;46(16):4745–4754. doi: 10.1021/bi062031y. PubMed DOI

Giannino D, Condello E, Bruno L, Testone G, Tartarini A, Cozza R, Innocenti AM, Bitonti MB, Mariotti D. The gene geranylgeranyl reductase of peach (Prunus persica [L.] Batsch) is regulated during leaf development and responds differentially to distinct stress factors. J Exp Bot. 2004;55(405):2063–2073. doi: 10.1093/jxb/erh217. PubMed DOI

Gilmore AM, Yamamoto HY. Zeaxanthin formation and energy-dependent fluorescence Quenching in pea-chloroplasts under artificially mediated linear and cyclic electron-transport. Plant Physiol. 1991;96(2):635–643. doi: 10.1104/pp.96.2.635. PubMed DOI PMC

Grasses T, Grimm B, Koroleva O, Jahns P. Loss of alpha-tocopherol in tobacco plants with decreased geranylgeranyl reductase activity does not modify photosynthesis in optimal growth conditions but increases sensitivity to high-light stress. Planta. 2001;213(4):620–628. doi: 10.1007/s004250100532. PubMed DOI

Gruszecki WI, Grudzinski W, Gospodarek M, Patyra M, Maksymiec W. Xanthophyll-induced aggregation of LHCII as a switch between light-harvesting and energy dissipation systems. Biochim Biophys Acta Bioenerg. 2006;1757(11):1504–1511. doi: 10.1016/j.bbabio.2006.08.002. PubMed DOI

Hamdani S, Khan N, Perveen S, Qu MN, Jiang JJ, Govindjee X, Zhu XG. Changes in the photosynthesis properties and photoprotection capacity in rice (Oryza sativa) grown under red, blue, or white light. Photosynth Res. 2019;139(1–3):107–121. doi: 10.1007/s11120-018-0589-6. PubMed DOI

Hasan MM, Bashir T, Ghosh R, Lee SK, Bae H. An overview of LEDs’ effects on the production of bioactive compounds and crop quality. Molecules. 2017 doi: 10.3390/molecules22091420. PubMed DOI PMC

Havaux M, Lutz C, Grimm B. Chloroplast membrane photostability in chlP transgenic tobacco plants deficient in tocopherols. Plant Physiol. 2003;132(1):300–310. doi: 10.1104/pp.102.017178. PubMed DOI PMC

He J, Qin L, Chow WS. Impacts of LED spectral quality on leafy vegetables: Productivity closely linked to photosynthetic performance or associated with leaf traits? Int J Agric Biol Eng. 2019;12(6):16–25. doi: 10.25165/j.ijabe.20191206.5178. DOI

Hey D, Rothbart M, Herbst J, Wang P, Muller J, Wittmann D, Gruhl K, Grimm B. LIL3, a light-harvesting complex protein, links terpenoid and tetrapyrrole biosynthesis in Arabidopsis thaliana. Plant Physiol. 2017;174(2):1037–1050. doi: 10.1104/pp.17.00505. PubMed DOI PMC

Horton P, Ruban AV, Rees D, Pascal AA, Noctor G, Young AJ. Control of the light-harvesting function of chloroplast membranes by aggregation of the Lhcii chlorophyll protein complex. FEBS Lett. 1991;292(1–2):1–4. doi: 10.1016/0014-5793(91)80819-O. PubMed DOI

Ilík P, Krchňák P, Tomek P, Nauš J. 2-D gel densitometer for high-contrast and selective imaging of chlorophyll-containing protein complexes separated by non-denaturing polyacrylamide gel electrophoresis. J Biochem Biophys Methods. 2002;51(3):273–281. doi: 10.1016/S0165-022x(02)00029-5. PubMed DOI

Iñigo S, Barber MR, Sánchez-Lamas M, Iglesias FM, Cerdán PD. The photomorphogenic signal: an essential component of photoautotrophic life. In: Najafpour M, editor. Advances in photosynthesis—fundamental aspects. London: IntechOpen; 2012.

Järvi S, Suorsa M, Paakkarinen V, Aro EM. Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes. Biochem J. 2011;439:207–214. doi: 10.1042/bj20102155. PubMed DOI

Karlický V, Podolinská J, Nadkanská L, Štroch M, Čajánek M, Špunda V. Pigment composition and functional state of the thylakoid membranes during preparation of samples for pigment-protein complexes separation by nondenaturing gel electrophoresis. Photosynthetica. 2010;48(3):475–480. doi: 10.1007/s11099-010-0063-y. DOI

Karlický V, Kurasová I, Ptáčková B, Večeřová K, Urban O, Špunda V. Enhanced thermal stability of the thylakoid membranes from spruce. A comparison with selected angiosperms. Photosynth Res. 2016;130(1–3):357–371. doi: 10.1007/s11120-016-0269-3. PubMed DOI

Keller Y, Bouvier F, D’Harlingue A, Camara B. Metabolic compartmentation of plastid prenyllipid biosynthesis—evidence for the involvement of a multifunctional geranylgeranyl reductase. Eur J Biochem. 1998;251(1–2):413–417. doi: 10.1046/j.1432-1327.1998.2510413.x. PubMed DOI

Kotakis C, Akhtar P, Zsiros O, Garab G, Lambrev P. Increased thermal stability of photosystem II and the macro-organization of thylakoid membranes, induced by co-solutes, associated with changes in the lipid-phase behaviour of thylakoid membranes. Photosynthetica. 2018 doi: 10.1007/s11099-018-0782-z. DOI

Kovács L, Damkjaer J, Kereiche S, Ilioaia C, Ruban AV, Boekema EJ, Jansson S, Horton P. Lack of the light-harvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts. Plant Cell. 2006;18(11):3106–3120. doi: 10.1105/tpc.106.045641. PubMed DOI PMC

Krumova SB, Laptenok SP, Kovács L, Tóth T, van Hoek A, Garab G, van Amerongen H. Digalactosyl-diacylglycerol-deficiency lowers the thermal stability of thylakoid membranes. Photosynth Res. 2010;105(3):229–242. doi: 10.1007/s11120-010-9581-5. PubMed DOI PMC

Lambrev PH, Akhtar P. Macroorganisation and flexibility of thylakoid membranes. Biochem J. 2019;476:2981–3018. doi: 10.1042/Bcj20190080. PubMed DOI

Lambrev PH, Várkonyi Z, Krumova S, Kovács L, Miloslavina Y, Holzwarth AR, Garab G. International Conference on photosynthesis in the post genomic era—structure and function of photosystems, Pushchino, RUSSIA, Aug 20–26 2007. Amsterdam: Elsevier Science Bv; 2007. Importance of trimer-trimer interactions for the native state of the plant light-harvesting complex II; pp. 847–853. PubMed

Landi M, Zivcak M, Sytar O, Brestic M, Allakhverdiev SI. Plasticity of photosynthetic processes and the accumulation of secondary metabolites in plants in response to monochromatic light environments: a review. Biochim Biophys Acta Bioenerg. 2020;1861(2):148131. doi: 10.1016/j.bbabio.2019.148131. PubMed DOI

Li CM, Liu X, Pan JH, Guo J, Wang Q, Chen CP, Li N, Zhang K, Yang B, Sun CH, Deng XJ, Wang PR. A lil3 chlp double mutant with exclusive accumulation of geranylgeranyl chlorophyll displays a lethal phenotype in rice. BMC Plant Biol. 2019 doi: 10.1186/s12870-019-2028-z. PubMed DOI PMC

Lohscheider JN, Rojas-Stutz MC, Rothbart M, Andersson U, Funck D, Mendgen K, Grimm B, Adamska I. Altered levels of LIL3 isoforms in Arabidopsis lead to disturbed pigment-protein assembly and chlorophyll synthesis, chlorotic phenotype and impaired photosynthetic performance. Plant Cell Environ. 2015;38(10):2115–2127. doi: 10.1111/pce.12540. PubMed DOI

Loll B, Kern J, Saenger W, Zouni A, Biesiadka J. Lipids in photosystem II: Interactions with protein and cofactors. Biochim Biophys Acta Bioenerg. 2007;1767(6):509–519. doi: 10.1016/j.bbabio.2006.12.009. PubMed DOI

Materová Z, Sobotka R, Zdvihalová B, Oravec M, Nezval J, Karlický V, Vrábl D, Štroch M, Špunda V. Monochromatic green light induces an aberrant accumulation of geranylgeranyled chlorophylls in plants. Plant Physiol Biochem. 2017;116:48–56. doi: 10.1016/j.plaphy.2017.05.002. PubMed DOI

Mizoguchi T, Isaji M, Yamano N, Harada J, Fujii R, Tamiaki H. Molecular structures and functions of chlorophylls-a esterified with geranylgeranyl, dihydrogeranylgeranyl, and tetrahydrogeranylgeranyl groups at the 17-propionate residue in a diatom, Chaetoceros calcitrans. Biochemistry. 2017;56(28):3682–3688. doi: 10.1021/acs.biochem.7b00381. PubMed DOI

Mizuno T, Amaki W, Watanabe H. Effects of monochromatic light irradiation by LED on the growth and anthocyanin contents in leaves of cabbage seedlings. Vi Int Symp Light Hortic. 2011;907:179–184.

Mork-Jansson A, Bue AK, Gargano D, Furnes C, Reisinger V, Arnold J, Kmiec K, Eichacker LA. Lil3 assembles with proteins regulating chlorophyll synthesis in barley. PLoS ONE. 2015 doi: 10.1371/journal.pone.0133145. PubMed DOI PMC

Muneer S, Kim EJ, Park JS, Lee JH. Influence of green, red and blue light emitting diodes on multiprotein complex proteins and photosynthetic activity under different light intensities in lettuce leaves (Lactuca sativa L.) Int J Mol Sci. 2014;15(3):4657–4670. doi: 10.3390/ijms15034657. PubMed DOI PMC

Navrátil M, Špunda V, Marková I, Janouš D. Spectral composition of photosynthetically active radiation penetrating into a Norway spruce canopy: the opposite dynamics of the blue/red spectral ratio during clear and overcast days. Trees-Struct Funct. 2007;21(3):311–320. doi: 10.1007/s00468-007-0124-4. DOI

Nellaepalli S, Zsiros O, Tóth T, Yadavalli V, Garab G, Subramanyam R, Kovács L. Heat- and light-induced detachment of the light harvesting complex from isolated photosystem I supercomplexes. J Photochem Photobiol B-Biol. 2014;137:13–20. doi: 10.1016/j.jphotobiol.2014.04.026. PubMed DOI

Opálková M, Navrátil M, Špunda V, Blanc P, Wald L. A database of 10 min average measurements of solar radiation and meteorological variables in Ostrava, Czech Republic. Earth Syst Sci Data. 2018;10(2):837–846. doi: 10.5194/essd-10-837-2018. DOI

Ouzounis T, Rosenqvist E, Ottosen CO. Spectral effects of artificial light on plant physiology and secondary metabolism: a review. HortScience. 2015;50(8):1128–1135. doi: 10.21273/Hortsci.50.8.1128. DOI

Park MR, Cho EA, Rehman S, Yun SJ. Expression of a sesame geranylgeranyl reductase cDNA is induced by light but repressed by abscisic acid and ethylene. Pak J Bot. 2010;42(3):1815–1826.

Petrova N, Todinova S, Paunov M, Kovács L, Taneva S, Krumova S. Thylakoid membrane unstacking increases LHCII thermal stability and lipid phase fluidity. J Bioenerg Biomembr. 2018;50(6):425–435. doi: 10.1007/s10863-018-9783-7. PubMed DOI

Qin XC, Suga M, Kuang TY, Shen JR. Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex. Science. 2015;348(6238):989–995. doi: 10.1126/science.aab0214. PubMed DOI

Reinbothe C, El Bakkouri M, Buhr F, Muraki N, Nomata J, Kurisu G, Fujita Y, Reinbothe S. Chlorophyll biosynthesis: spotlight on protochlorophyllide reduction. Trends Plant Sci. 2010;15(11):614–624. doi: 10.1016/j.tplants.2010.07.002. PubMed DOI

Schoefs B. The light-dependent and light-independent reduction of protochlorophyllide a to chlorophyllide a. Photosynthetica. 1999;36(4):481–496. doi: 10.1023/A:1007002101856. DOI

Seiwert D, Witt H, Janshoff A, Paulsen H. The non-bilayer lipid MGDG stabilizes the major light-harvesting complex (LHCII) against unfolding. Sci Rep. 2017 doi: 10.1038/s41598-017-05328-7. PubMed DOI PMC

Sellaro R, Crepy M, Trupkin SA, Karayekov E, Buchovsky AS, Rossi C, Casal JJ. Cryptochrome as a sensor of the blue/green ratio of natural radiation in Arabidopsis. Plant Physiol. 2010;154(1):401–409. doi: 10.1104/pp.110.160820. PubMed DOI PMC

Shibata M, Mikota T, Yoshimura A, Iwata N, Tsuyama M, Kobayashi Y. Chlorophyll formation and photosynthetic activity in rice mutants with alterations in hydrogenation of the chlorophyll alcohol side chain. Plant Sci. 2004;166(3):593–600. doi: 10.1016/j.plantsci.2003.10.014. DOI

Shibata M, Tsuyama M, Takami T, Shimizu H, Kobayashi Y. Accumulation of menaquinones with incompletely reduced side chains and loss of alpha-tocopherol in rice mutants with alternations in the chlorophyll moiety. J Exp Bot. 2004;55(405):1989–1996. doi: 10.1093/jxb/erh218. PubMed DOI

Shpilyov AV, Zinchenko VV, Shestakov SV, Grimm B, Lokstein H. Inactivation of the geranylgeranyl reductase (ChlP) gene in the cyanobacterium Synechocystis sp PCC 6803. Biochim Biophys Acta Bioenerg. 2005;1706(3):195–203. doi: 10.1016/j.bbabio.2004.11.001. PubMed DOI

Shpilyov AV, Zinchenko VV, Grimm B, Lokstein H. Chlorophyll a phytylation is required for the stability of photosystems I and II in the cyanobacterium Synechocystis sp PCC 6803. Plant J. 2013;73(2):336–346. doi: 10.1111/tpj.12044. PubMed DOI

Su NN, Wu Q, Shen ZG, Xia K, Cui J. Effects of light quality on the chloroplastic ultrastructure and photosynthetic characteristics of cucumber seedlings. Plant Growth Regul. 2014;73(3):227–235. doi: 10.1007/s10725-013-9883-7. DOI

Suga M, Qin XC, Kuang TY, Shen JR. Structure and energy transfer pathways of the plant photosystem I-LHCI supercomplex. Curr Opin Struct Biol. 2016;39:46–53. doi: 10.1016/j.sbi.2016.04.004. PubMed DOI

Takahashi K, Takabayashi A, Tanaka A, Tanaka R. Functional analysis of light-harvesting-like protein 3 (LIL3) and its light-harvesting chlorophyll-binding motif in Arabidopsis. J Biol Chem. 2014;289(2):987–999. doi: 10.1074/jbc.M113.525428. PubMed DOI PMC

Tanaka R, Oster U, Kruse E, Rudiger W, Grimm B. Reduced activity of geranylgeranyl reductase leads to loss of chlorophyll and tocopherol and to partially geranylgeranylated chlorophyll in transgenic tobacco plants expressing antisense RNA for geranylgeranyl reductase. Plant Physiol. 1999;120(3):695–704. doi: 10.1104/pp.120.3.695. PubMed DOI PMC

Tanaka R, Rothbart M, Oka S, Takabayashi A, Takahashi K, Shibata M, Myouga F, Motohashi R, Shinozaki K, Grimm B, Tanaka A. LIL3, a light-harvesting-like protein, plays an essential role in chlorophyll and tocopherol biosynthesis. Proc Natl Acad Sci U S A. 2010;107(38):16721–16725. doi: 10.1073/pnas.1004699107. PubMed DOI PMC

Terashima I, Fujita T, Inoue T, Chow WS, Oguchi R. Green light drives leaf photosynthesis more efficiently than red light in strong white light: revisiting the enigmatic question of why leaves are green. Plant Cell Physiol. 2009;50(4):684–697. doi: 10.1093/pcp/pcp034. PubMed DOI

Tóth TN, Rai N, Solymosi K, Zsiros O, Schröder WP, Garab G, van Amerongen H, Horton P, Kovács L. Fingerprinting the macro-organisation of pigment-protein complexes in plant thylakoid membranes in vivo by circular-dichroism spectroscopy. Biochim Biophys Acta. 2016;1857(9):1479–1489. doi: 10.1016/j.bbabio.2016.04.287. PubMed DOI

Urban O, Janouš D, Acosta M, Czerny R, Marková I, Navrátil M, Pavelka M, Pokorný R, Šprtová M, Zhang R, Špunda V, Grace J, Marek MV. Ecophysiological controls over the net ecosystem exchange of mountain spruce stand. Comparison of the response in direct vs. diffuse solar radiation. Global Change Biol. 2007;13(1):157–168. doi: 10.1111/j.1365-2486.2006.01265.x. DOI

Van Grondelle R, Dekker JP, Gillbro T, Sundstrom V. Energy-transfer and trapping in photosynthesis. Biochim Biophys Acta Bioenerg. 1994;1187(1):1–65. doi: 10.1016/0005-2728(94)90166-X. DOI

Várkonyi Z, Nagy G, Lambrev P, Kiss AZ, Székely N, Rosta L, Garab G. Effect of phosphorylation on the thermal and light stability of the thylakoid membranes. Photosynth Res. 2009;99(3):161–171. doi: 10.1007/s11120-008-9386-y. PubMed DOI

Wang P, Li C, Wang Y, Huang R, Sun C, Xu Z, Zhu J, Gao X, Deng X, Wang P. Identification of a Geranylgeranyl reductase gene for chlorophyll synthesis in rice. Springerplus. 2014;3:201. doi: 10.1186/2193-1801-3-201. PubMed DOI PMC

Ware MA, Belgio E, Ruban AV. Photoprotective capacity of non-photochemical quenching in plants acclimated to different light intensities. Photosynth Res. 2015;126(2–3):261–274. doi: 10.1007/s11120-015-0102-4. PubMed DOI

Wei J, Li HL, Barrow MP, O’Connor PB. Structural characterization of chlorophyll-a by high resolution tandem mass spectrometry. J Am Soc Mass Spectr. 2013;24(5):753–760. doi: 10.1007/s13361-013-0577-1. PubMed DOI

Yang CH, Boggasch S, Haase W, Paulsen H. Thermal stability of trimeric light-harvesting chlorophyll a/b complex (LHCIIb) in liposomes of thylakoid lipids. Biochim Biophys Acta Bioenerg. 2006;1757(12):1642–1648. doi: 10.1016/j.bbabio.2006.08.010. PubMed DOI

Zhang TT, Maruhnich SA, Folta KM. Green light induces shade avoidance symptoms. Plant Physiol. 2011;157(3):1528–1536. doi: 10.1104/pp.111.180661. PubMed DOI PMC

Zhou Y, Gong ZY, Yang ZF, Yuan Y, Zhu JY, Wang M, Yuan FH, Wu SJ, Wang ZQ, Yi CD, Xu TH, Ryom M, Gu MH, Liang GH. Mutation of the light-induced yellow leaf 1 gene, which encodes a geranylgeranyl reductase, affects chlorophyll biosynthesis and light sensitivity in rice. PLoS ONE. 2013 doi: 10.1371/journal.pone.0075299. PubMed DOI PMC

Zsiros O, Ünnep R, Nagy G, Almásy L, Patai R, Székely NK, Kohlbrecher J, Garab G, Dér A, Kovács L. Role of protein-water interface in the stacking interactions of granum thylakoid membranes-as revealed by the effects of hofmeister salts. Front Plant Sci. 2020;11:1257. doi: 10.3389/fpls.2020.01257. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...