Relaxation of the non-photochemical chlorophyll fluorescence quenching in diatoms: kinetics, components and mechanisms
Jazyk angličtina Země Anglie, Velká Británie Médium electronic-print
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
24591721
PubMed Central
PMC3949399
DOI
10.1098/rstb.2013.0241
PII: rstb.2013.0241
Knihovny.cz E-zdroje
- Klíčová slova
- diatom, high light stress, photoprotection, photosynthesis, relaxation, xanthophyll cycle,
- MeSH
- časové faktory MeSH
- chlorid amonný MeSH
- chlorofyl metabolismus účinky záření MeSH
- dithiothreitol MeSH
- fluorescence MeSH
- fotosystém II - proteinový komplex metabolismus MeSH
- kadmium MeSH
- kinetika MeSH
- oniové sloučeniny MeSH
- regresní analýza MeSH
- rozsivky fyziologie MeSH
- světlo * MeSH
- tylakoidy metabolismus MeSH
- xanthofyly metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- chlorid amonný MeSH
- chlorofyl MeSH
- diphenyleneiodonium MeSH Prohlížeč
- dithiothreitol MeSH
- fotosystém II - proteinový komplex MeSH
- kadmium MeSH
- oniové sloučeniny MeSH
- xanthofyly MeSH
Diatoms are especially important microorganisms because they constitute the larger group of microalgae. To survive the constant variations of the light environment, diatoms have developed mechanisms aiming at the dissipation of excess energy, such as the xanthophyll cycle and the non-photochemical chlorophyll (Chl) fluorescence quenching. This contribution is dedicated to the relaxation of the latter process when the adverse conditions cease. An original nonlinear regression analysis of the relaxation of non-photochemical Chl fluorescence quenching, qN, in diatoms is presented. It was used to obtain experimental evidence for the existence of three time-resolved components in the diatom Phaeodactylum tricornutum: qNf, qNi and qNs. qNf (s time-scale) and qNs (h time-scale) are exponential in shape. By contrast, qNi (min time-scale) is of sigmoidal nature and is dominant among the three components. The application of metabolic inhibitors (dithiothreitol, ammonium chloride, cadmium and diphenyleneiodonium chloride) allowed the identification of the mechanisms on which each component mostly relies. qNi is linked to the relaxation of the ΔpH gradient and the reversal of the xanthophyll cycle. qNs quantifies the stage of photoinhibition caused by the high light exposure, qNf seems to reflect fast conformational changes within thylakoid membranes in the vicinity of the photosystem II complexes.
Zobrazit více v PubMed
Guiry MD. 2012. How many species of algae are there? J. Phycol. 48, 1057–1063. (10.1111/j.1529-8817.2012.01222.x) PubMed DOI
Bowler C, Vardi A, Allen AE. 2010. Oceanographic and biogeochemical insights from diatom genomes. Annu. Rev. Mar. Sci. 2, 333–363. (10.1146/annurev-marine-120308-081051) PubMed DOI
Field CB, Behrenfeld MJ, Dall'Osto L, Zito F, Bonente G, Falkowski G. 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240. (10.1126/science.281.5374.237) PubMed DOI
Masmoudi S, Nguyen-Deroche N, Caruso A, Ayadi A, Morant-Manceau A, Tremblin G, Bertrand M, Schoefs B. 2013. Cadmium, copper, sodium and zinc effects on diatoms: from heaven to hell: a review. Cryptogamie Algol. 34, 185–225. (10.7872/crya.v34.iss2.2013.185) DOI
Ewert M, Deming JW. 2013. Sea ice microorganisms: environmental constraints and extracellular responses. Biology 2, 603–628. (10.3390/biology2020603) PubMed DOI PMC
McIntyre HL, Kana TM, Geider RJ. 2000. The effect of water motion on short-term rates of photosynthesis by marine phytoplankton. Trends Plant. Sci. 5, 12–17. (10.1016/S1360-1385(99)01504-6) PubMed DOI
Moulin P, Lemoine Y, Schoefs B. 2010. Modifications of the carotenoid metabolism in plastids: a response to stress conditions. In Handbook of plant and crop stress (ed. Pessarakli M.), p. 407, 3rd edn Boca Raton, FL: CRC Press.
Mus F, Toussaint JP, Cooksey KE, Fields MW, Gerlach R, Peyton BM, Carlson MP. 2013. Physiological and molecular analysis of carbon source supplementation and pH stress-induced lipid accumulation in the marine diatom Phaeodactylum tricornutum. Appl. Microbiol. Biotechnol. 97, 3625–3642. (10.1007/s00253-013-4747-7) PubMed DOI
Sun GD, Mu M. 2013. Understanding variations and seasonal characteristics of net primary production under two types of climate change scenarios in China using the LPJ model. Clim. Change 120, 755–769. (10.1007/s10584–013–0833–1) DOI
Thomas MK, Kremer CT, Klausmeier CA, Litchman E. 2012. A global pattern of thermal adaptation in marine phytoplankton. Science 338, 1085–1088. (10.1126/science.1224836) PubMed DOI
Canion A, Mac Intyre HL, Phipps S. 2013. Short term to seasonal variability in factors driving primary productivity in a shallow estuary: implications for modelling production. Estuar. Coast. Shelf Sci. 131, 224–234. (10.1016/j.ecss.2013.07.009) DOI
Szymanska R, Latowski D, Strzalka K. 2012. Chloroplasts: the powerful photoprotective machinery. Curr. Chem. Biol. 6, 254–264.
Goss R, Jakob T. 2010. Regulation and function of xanthophyll cycle-dependent photoprotection in algae. Photosynth. Res. 106, 103–122. (10.1007/s11120-010-9536-x) PubMed DOI
Bertrand M. 2010. Carotenoid biosynthesis in diatoms. Photosynth. Res. 106, 89–102. (10.1007/s11120-010-9589-x) PubMed DOI
Lavaud J. 2007. Fast regulation of photosynthesis in diatoms: mechanism, evolution and ecophysiology. Funct. Plant Sci. Biotechnol. 1, 267–287.
Jahns P, Latowski D, Strzalka K. 2009. Mechanisms and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim. Biophys. Acta 1787, 3–14. (10.1016/j.bbabio.2008.09.013) PubMed DOI
Roháček K, Soukupová J, Barták M. 2008. Chlorophyll fluorescence: a wonderful tool to study plant physiology and plant stress. In Plant cell compartments: selected topics (ed. Schoefs B.), p. 41 Kerala, India: Research Signpost.
Baker NR. 2009. Chlorophyll fluorescence of photosynthesis in vivo. Annu. Rev. Plant Biol. 59, 89–113. (10.1146/annurev.arplant.59.032607.092759) PubMed DOI
Bailleul B, et al. 2010. An atypical membre of the light harvesting complex stress-related protein family modulates diatom response to light. Proc. Natl Acad. Sci. USA 107, 18 214–18 219. (10.1073/pnas.1007703107) PubMed DOI PMC
Grouneva I, Jakob T, Wilhelm C, Goss R. 2008. A new multicomponent mechanism in the diatom Cyclotella meneghiniana. Plant Cell Physiol. 49, 1217–1225. (10.1093/pcp/pcn097) PubMed DOI
Serôdio J, Lavaud J. 2011. A model describing the light response of the nonphotochemical quenching of chlorophyll fluorescence. Photosynth. Res. 108, 61–76. (10.1007/s11120-011-9654-0) PubMed DOI
Roháček K. 2010. Method for resolution and quantification of components of the nonphotochemical quenching (qN). Photosynth. Res. 105, 101–113. (10.1007/s11120-010-9564-6) PubMed DOI
Lemoine Y, Schoefs B. 2010. Secondary ketocarotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress. Photosynth. Res. 106, 155–177. (10.1007/s11120-010-9583-3) PubMed DOI
Mimouni V, Ulmann L, Pasquiet V, Mathieu M, Picot L, Bougaran G, Cadoret JP, Morant-Manceau A, Schoefs B. 2012. The potential of microalgae for the production of bioactive molecules of pharmaceutical interest. Curr. Pharm. Biotechnol. 13, 2733–2750. (10.2174/138920112804724828) PubMed DOI
Heydarizadeh P, Poirier I, Loizeau D, Ulmann L, Mimouni V, Schoefs B, Bertrand M. 2013. Plastids of marine phytoplankton produce bioactive pigments and lipids. Mar. Drugs 11, 3425–3471. (10.3390/md11093425) PubMed DOI PMC
Harrison PJ, Water RE, Taylor FJR. 1980. A broad spectrum artificial sea water medium for coastal and open ocean phytoplankton. J. Phycol. 16, 28–35.
Bertrand M, Schoefs B, Siffel P, Roháček K, Molnar I. 2001. Cadmium inhibits epoxidation of diatoxanthin to diadinoxanthin in the xanthophyll cycle of the marine diatom Phaeodactylum tricornutum. FEBS Lett. 508, 153–156. (10.1016/S0014-5793(01)03050-2) PubMed DOI
Nguyen-Deroche TLN, Caruso A, Le TT, Bui TV, Schoefs B, Tremblin G, Morant-Manceau A. 2012. Zinc affects differently growth, photosynthesis, antioxidant enzyme activities and phytochelatin synthase expression of four marine diatoms. Scientific World Journal 2012, 982957 (10.1100/2012/982957) PubMed DOI PMC
Lavaud J, Kroth P. 2006. In diatoms, the transthylakoid proton gradient regulates the photoprotective non-photochemical fluorescence quenching beyond its control on the xanthophyll cycle. Plant Cell Physiol. 47, 1010–1016. (10.1093/pcp/pcj058) PubMed DOI
Ting CS, Owens TG. 1993. Photochemical and nonphotochemical quenching processes in the diatom Phaeodactylum tricornutum. Plant Physiol. 101, 1323–1330. PubMed PMC
Darko E, Schoefs B, Lemoine Y. 2000. An improved LC method for the analysis of photosynthetic pigments of higher plants. J. Chromatogr. 876A, 111–116. (10.1016/S0021-9673(00)00141-2) PubMed DOI
Juneau P, Harrison PJ. 2005. Comparison by PAM fluorometry of photosynthetic activity of nine marine phytoplankton grown under identical conditions. Photochem. Photobiol. 81, 649–653. (10.1562/2005-01-13-RA-414.1) PubMed DOI
Domingues N, Matos AR, Marques de la Silva J, Cartaxana P. 2012. Response of the diatom Phaeodactylum tricornutum to photoxidative stress resulting from high light exposure. PLoS ONE 7, e38162 (10.1371/journal.pone.0038162) PubMed DOI PMC
Jakob T, Schreiber U, Kirchesch V, Langner U, Wilhelm C. 2005. Estimation of chlorophjyll content and daily primary production of the major algal group by means of multiwavelength-excitation PAM chlorophyll fluorometry: performance and methodological limits. Photosynth. Res. 83, 343–361. (10.1007/s11120-005-1329-2) PubMed DOI
Lavaud J, Rousseau R, van Gorkom HJ, Etienne AL. 2002. Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum. Plant Physiol. 129, 1398–1406. (10.1104/pp.002014) PubMed DOI PMC
Ruban AV, Lavaud J, Rousseau B, Guglielmi G, Horton P, Etienne AL. 2004. The super-excess energy dissipation in diatom algae: comparative analysis with higher plants. Photosynth. Res. 82, 165–175. (10.1007/s11120-004-1456-1) PubMed DOI
Eisenstadt D, Ohad I, Keren N, Kaplan A. 2008. Changes in the photosynthetic reaction centre II in the diatom Phaeodactylum tricornutum result in non-photochemical fluorescence quenching. Environ. Microbiol. 10, 1997–2007. (10.1111/j.1462-2920.2008.01616.x) PubMed DOI
Grouneva I, Jakob T, Wilhelm C, Goss R. 2009. The regulation of xanthophyll cycle and non-photochemical fluorescence quenching by two alternative electron flows in the diatom Phaeodactylum tricornutum and Cyclotella meneghiniana. Biochem. Biophys. Acta 1087, 929–938. (10.1016/j.bbabio.2009.02.004) PubMed DOI
Grouneva I, Jakob T, Wilhelm C, Goss R. 2006. Influence of ascorbate and pH on the activity of the diatom xanthophyll cycle-enzyme diadinoxanthin de-epoxidase. Physiol. Plant. 126, 205–211. (10.1111/j.1399-3054.2006.00613.x) DOI
Lavaud J, Rouseau B, Etienne A-L. 2002. In diatoms, a transthylakoid proton gradient alone is not sufficient to induce a non-photochemical fluorescence quenching. FEBS Lett. 523, 163–166. (10.1016/S0014-5793(02)02979-4) PubMed DOI
Opanacenko VK, Vasyukhina LA, Naydov IA. 2010. Two types of ammonium uncoupling in pea chloroplasts. Biochemistry 75, 784–791. (10.1134/S0006297910060143) PubMed DOI
Tsuno M, Suzuki H, Kondo T, Mino H, Noguchi T. 2011. Interaction and inhibitory effect of ammonium cation in the oxygen evolving center of photosystem II. Biochemistry 50, 2506–2514. (10.1021/bi101952g) PubMed DOI
Müller P, Li XP, Niyogi KK. 2001. Non-photochemical quenching. A response to excess light energy. Plant Physiol. 125, 1558–1566. (10.1104/pp.125.4.1558) PubMed DOI PMC
Büch K, Stransky H, Hager A. 1995. FAD is a further cofactor of NAD(P)H and O2-dependent zeaxanthin-epoxidases. FEBS Lett. 376, 45–48. (10.1016/0014-5793(95)01243-9) PubMed DOI
Price NM, Morel FMN. 1990. Cadmium and cobalt substitution for zinc in a marine diatom. Nature 344, 658–660. (10.1038/344658a0) DOI
Brembu T, Jorstad M, Winge P, Valle KC, Bones AM. 2011. Genome-wide profiling of responses to cadmium in the diatom Phaeodactylum tricornutum . Environ. Sci. Technol. 45, 7640–7647. (10.1021/es2002259) PubMed DOI
Torres E, Cid A, Herrero C, Abalde J. 1998. Removal of cadmium ions by the marine diatom Phaeodactylum tricornutum Bohlin accumulation and long-term kinetics of uptake. Bioresour. Technol. 63, 213–220. (10.1016/S0960-8524(97)00143-0) DOI
Groppa MD, Ianuzzo MP, Rosales EP, Vazquez SC, Benavides MP. 2012. Cadmium modulates NADPH oxidase activity and expression in sunflower leaves. Biol. Plant. 56, 167–171. (10.1007/s10535-012-0036-z) DOI
Fagioni M, D'Amiel GM, Timperio AM, Zolla L. 2009. Proteomic analysis of multiprotein complexes in the thylakoid membrane upon cadmium treatment. J. Proteome Res. 8, 310–326. (10.1021/pr800507x) PubMed DOI
Goss R, Pinto EA, Wilhelm C, Richter M. 2006. The importance of a highly active and ΔpH regulated diatoxanthin epoxidase for the regulation of the PS II antenna function in diadinoxanthin cycle containing algae. J. Plant Physiol. 163, 1008–1021. (10.1016/j.jplph.2005.09.008) PubMed DOI
McCarty RE, Rachter E. 1967. The inhibition and stimulation of photophosphorylation by N,N′-dicyclohexylcarbodiimide. J. Biol. Chem. 242, 3435–3439.
Shoshan V, Selman BR. 1967. The interaction of N,N′-dicyclohexylcarbodiimide with chloroplast coupling factor 1. J. Biol. Chem. 255, 384–389. PubMed
Mou S, Zhang X, Ye N, Miao J, Cao S, Xu D, Fan X, An M. 2013. Analysis of ΔpH and the xanthophyll cycle in NPQ of the Antartic sea ice alga Chlamydomonas sp. ICE-L. Extremophiles 17, 477–484. (10.1007/s00792-013-0532-x) PubMed DOI
Horton P, Ruban AV, Rees D, Pascal AA, Noctor G, Young AJ. 1991. Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll-protein complex. FEBS Lett. 292, 1–4. (10.1016/0014-5793(91)80819-O) PubMed DOI
Goss R, Garab G. 2001. Non-photochemical chlorophyll fluorescence quenching and structural rearrangements induced by low pH in intact cells of Chlorella fusca (Chlorophyceae) and Mantoniella squamata (Prasinophyceae). Photosynth. Res. 67, 185–197. (10.1023/A:1010681511105) PubMed DOI
Walters RG, Ruban AV, Horton P. 1994. Higher plant light harvesting complexes LHCIIa and LHCIIc are bound by dicyclohexylcarbodiimide during inhibition of energy dissipation. Eur. J. Biochem. 226, 1063–1069. (10.1111/j.1432-1033.1994.01063.x) PubMed DOI
Lepetit B, Goss R, Jakob T, Wilhelm C. 2011. Molecular dynamics of the diatom thylakoid membrane under different light conditions. Photosynth. Res. 111, 245–257. (10.1007/s11120-011-9633-5) PubMed DOI
Miloslavina Y, Grouneva I, Lambrev PH, Lepetit B, Goss R, Wilhelm C, Holzwarth AR. 2009. Ultrafast fluorescence study on the location and mechanism of non-photochemical quenching in diatoms. Biochim. Biophys. Acta 1787, 1189–1197. (10.1016/j.bbabio.2009.05.012) PubMed DOI
Květoň J, Durchan M, Roháček K, Šantrůček J, Vácha F, Šesták Z. 2005. PAVEL ŠIFFEL (1954–2003) or life full of chlorophyll. Photosynthetica 43, 323–328. (10.1007/s11099-005-0055-5) DOI
A two-component nonphotochemical fluorescence quenching in eustigmatophyte algae