Abstract
The effects of high light (HL) stress on the photosynthetic proteins of green tide-forming macroalga were studied. The naturally grown Ulva prolifera was collected from an intertidal habitat and subjected to 1000 μE m−2 s−1 HL for 12 h. The thylakoid membrane proteins were subsequently extracted and qualitatively analyzed using LC/MS. Quantitative analysis of the thylakoid membrane proteins showed that both PSII reaction center proteins and PSII chlorophyll antenna proteins were decreased. Comparatively, the main PSI reaction center proteins were well preserved. The cytochrome f subunit was significantly decreased, while the other subunits of cytochrome b 6 /f complex were maintained. These results demonstrated that the HL-induced cytochrome b 559 might play a role in photoacclimation of U. prolifera by involving in cyclic photosynthetic electron transfer (PET) flow around PSII. The LhcSR and PsbS proteins were also identified in U. prolifera, and PsbS was noted to be significantly increased under HL stress. The long-term photoacclimation mechanism of U. prolifera under HL stress might not depend on cyclic PET flow around PSI.
Similar content being viewed by others
References
Alboresi A, Gerotto C, Giacometti GM, Bassi R, Morosinotto T (2010) Physcomitrella patens mutants affected on heat dissipation clarify the evolution of photoprotection mechanisms upon land colonization. Proc Natl Acad Sci U S A 107:11128–11133
Alric J (2010) Cyclic electron flow around photosystem I in unicellular green algae. Photosynth Res 106:47–56
Apel K, Hirt H (2004) Reactive oxygen species: metabolism oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta (BBA) Bioenerg 1143:113–134
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis. In Vivo Annu Rev Plant Biol 59:89–113
Barber J (1995) Molecular basis of the vulnerability of photosystem II to damage by light. Funct Plant Biol 22:201–208
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brambilla F, Resta D, Isak I, Zanotti M, Arnoldi A (2009) A label-free internal standard method for the differential analysis of bioactive lupin proteins using nano HPLC-chip coupled with Ion trap mass spectrometry. Proteomics 9:272–286
Chuartzman SG et al (2008) Thylakoid membrane remodeling during state transitions in Arabidopsis. The Plant Cell Online 20:1029–1039
de Bianchi S, Dall'Osto L, Tognon G, Morosinotto T, Bassi R (2008) Minor antenna proteins CP24 and CP26 affect the interactions between photosystem II subunits and the electron transport rate in grana membranes of Arabidopsis. Plant Cell Online 20:1012–1028
Ebenhoh O, Fucile G, Finazzi G, Rochaix JD, Goldschmidt-Clermont M (2014) Short-term acclimation of the photosynthetic electron transfer chain to changing light: a mathematical model. Philos Trans R Soc Lond B Biol Sci 369:20130223
Eberhard S, Finazzi G, Wollman FA (2008) The dynamics of photosynthesis. Annu Rev Genet 42:463–515
Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838
Gao S, Shen S, Wang G, Niu J, Lin A, Pan G (2011) PSI-driven cyclic electron flow allows intertidal macro-algae Ulva sp. (Chlorophyta) to survive in desiccated conditions. Plant Cell Physiol 52:885–893
Gerotto C, Alboresi A, Giacometti GM, Bassi R, Morosinotto T (2011) Role of PSBS and LHCSR in Physcomitrella patens acclimation to high light and low temperature. Plant, Cell Environ 34:922–932
Golding A, Johnson G (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107–114
Griffin NM et al (2010) Label-free, normalized quantification of complex mass spectrometry data for proteomic analysis. Nat Biotechnol 28:83–89
Gu W, Xie X, Gao S, Zhou W, Pan G, Wang G (2013) Comparison of different cells of Haematococcus pluvialis reveals an extensive acclimation mechanism during its aging process: From a perspective of photosynthesis. PLoS One 8
Hamilton M, Franco E, Deák Z, Schlodder E, Vass I, Nixon PJ (2014) Investigating the photoprotective role of cytochrome b-559 in photosystem II in a mutant with altered ligation of the haem. Plant Cell Physiol 55:1276–1285
Hankamer B, Morris E, Nield J, Gerle C, Barber J (2001) Three-dimensional structure of the photosystem II core dimer of higher plants determined by electron microscopy. J Struct Biol 135:262–269
Huan L et al. (2014) Positive Correlation Between PSI Response and Oxidative Pentose Phosphate Pathway Activity During Salt Stress in the Intertidal Macroalgae Plant and Cell Physiology
Ivanov AG et al (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 113:191–206
Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193
Kono M, Terashima I (2014) Long-term and short-term responses of the photosynthetic electron transport to fluctuating light. J Photochem Photobiol B: Biol 137:89–99
Lemoine Y, Schoefs B (2010) Secondary ketocarotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress. Photosynth Res 106:155–177
Li X-P, Müller-Moulé P, Gilmore AM, Niyogi KK (2002) PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc Natl Acad Sci U S A 99:15222–15227
Li X-P, Gilmore AM, Caffarri S, Bassi R, Golan T, Kramer D, Niyogi KK (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS. Protein J Biol Chem 279:22866–22874
Lin A, Shen S, Wang G, Yi Q, Qiao H, Niu J, Pan G (2011) Comparison of chlorophyll and photosynthesis parameters of floating and attached Ulva prolifera. J Integr Plant Biol 53:25–34
Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–1044
Long SP (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:633–662
Mou S et al (2013) Photoprotection in the green tidal alga Ulva prolifera: role of LHCSR and PsbS proteins in response to high light stress. Plant Biol (Stuttg) 15:1033–1039
Munekage Y, Hashimoto M, Miyake C, Tomizawa K-I, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582
Nelson N, Yocum CF (2006) Structure and function of photosystem I and II. Annu Rev Plant Biol 57:521–565
Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359
Pascal AA et al (2005) Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 436:134–137
Peers G et al (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462:518–521
Pospíšil P (2009) Production of reactive oxygen species by photosystem II. Biochim Biophys Acta (BBA) - Bioenerg 1787:1151–1160
Pospíšil P (2011) Enzymatic function of cytochrome b 559 in photosystem II. J Photochem Photobiol B: Biol 104:341–347
Pospíšil P (2012) Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochim Biophys Acta (BBA) - Bioenerg 1817:218–231
Rochaix J-D (2007) Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett 581:2768–2775
Rochaix J-D (2011) Regulation of photosynthetic electron transport. Biochim Biophys Acta (BBA) - Bioenerg 1807:375–383
Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ 30:1041–1051
Shinopoulos KE, Brudvig GW (2012) Cytochrome b 559 and cyclic electron transfer within photosystem II. Biochim Biophys Acta (BBA) - Bioenerg 1817:66–75
Sun S et al. (2008) Emerging challenges: Massive green algae blooms in the Yellow Sea Nature Precedings:hdl:10101/npre.12008.12266.10101
Tan S, Cunningham FX, Youmans M, Grabowski B, Sun Z, Gantt E (1995) Cytochrome f loss in astaxanthin-accumulating red cells of Haematococcus pluvialis (chlorophyceae): comparasion of photosynthetic activity, photosynthetic enzymes, and thylakoid membrane polyppeptides in red and green cells. J Phycol 31:897–905
Tikhonov AN (2014) The cytochrome b6f complex at the crossroad of photosynthetic electron transport pathways. Plant Physiol Biochem 81:163–183
Tiwari A, Pospíšil P (2009) Superoxide oxidase and reductase activity of cytochrome b559 in photosystem II. Biochim Biophys Acta (BBA) - Bioenerg 1787:985–994
Van Gorkom H, Schelvis J (1993) Kok's oxygen clock: what makes it tick? The structure of P680 and consequences of its oxidizing power. Photosynth Res 38:297–301
Vass I (2012) Molecular mechanisms of photodamage in the photosystem II complex. Biochim Biophys Acta (BBA) - Bioenerg 1817:209–217
Wada M (2013) Chloroplast movement. Plant Sci 210:177–182
Wada M, Kagawa T, Sato Y (2003) Chloroplast movement. Annu Rev Plant Biol 54:455–468
Xie X, Gao S, Gu W, Pan G, Wang G (2013) Desiccation induces accumulations of antheraxanthin and zeaxanthin in intertidal macro-alga Ulva pertusa (Chlorophyta). PLoS One 8, e72929
Acknowledgments
This work was supported by the National Science & Technology Program (2012BAC07B03), the National Natural Science Foundation of China (41176134; 41176137), Science and Technology Strategic Pilot of the Chinese Academy of Sciences (XDA05030401) and Public Science and Technology Research Funds Projects of the Ocean (201205010).
Conflicts of Interest
The authors declare no conflicts of interest.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(TIFF 5825 kb)
Rights and permissions
About this article
Cite this article
Gu, W., Huan, L., Yu, R. et al. Enhancement of Cytochrome b 559 Indicates Its Possible Involvement in Long-Term High Light Stress Tolerance in Intertidal Macroalgae. Plant Mol Biol Rep 33, 1918–1927 (2015). https://doi.org/10.1007/s11105-015-0885-7
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-015-0885-7