Abstract
Lhcb1-2 and PsbS proteins of photosystem II (PSII) have important roles in photoprotective thermal energy dissipation of the absorbed excess light energy. The light responses of chlorophyll fluorescence parameters were analyzed to examine how the absence of Lhcb1-2 or PsbS proteins can modify the energy allocation patterns of absorbed light energy in PSII using an antisense construct of lhcb2 and a psbS deletion (npq4-1) mutant of Arabidopsis thaliana. Both mutants exhibit reduced Stern–Volmer non-photochemical chlorophyll fluorescence quenching (NPQ). Here, we have adopted an approach, presented by Hendrickson et al. (Photosynth Res 82:73–81, 2004), to gain a better insight into the mechanism of the NPQ in these mutants. We have found no significant differences in the quantum yields of photochemical energy conversion (ΦPSII) between the mutants and the wild type. Nevertheless, as it was expected, the fraction of the energy, which is dissipated as heat via regulated pathways in PSII (ΦNPQ) for both mutants, were reduced as compared to the wild type. In a complementary way, the extent of non-regulated non-photochemical energy loss in PSII (ΦNO) for both mutants was significantly higher than that in the wild type. This reflects, together with the lower ΦNPQ (or NPQ) values, suboptimal capacity of photoprotective reactions at higher light intensities.


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Andersson J, Walters RG, Horton P, Jansson S (2001) Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: implications for the mechanism of protective energy dissipation. Plant Cell 13:1193–1204
Andersson J, Wentworth M, Walters RG, Howard CA, Ruban AV, Horton P, Jansson S (2003) Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II—effects on photosynthesis, grana stacking and fitness. Plant J 35:350–361
Bajkán Sz, Váradi Gy, Balogh M, Domonkos Á, Kiss GyB, Kovács L, Lehoczki E (2010) Conserved structure of the chloroplast-DNA encoded D1 protein is essential for effective photoprotection via non-photochemical thermal dissipation in higher plants. Mol Genet Genom 284:55–63
Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in Hedera canariensis. Photosynth Res 25:173–185
Croce R, Canino G, Ros F, Bassi R (2002) Chromophore organisation in the higher plant photosystem II antenna protein CP26. Biochemistry 41:7334–7343
Demmig-Adams B, Adams WW, Barker DH, Logan BA, Bowling DR, Verhoeven AS (1996) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiol Plant 98:253–264
Elrad DH, Niyogi KK, Grossman AR (2002) A major light-harvesting polypeptide of photosystem II functions in thermal dissipation. Plant Cell 14:1801–1816
Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92
Goss R, Opitz C, Lepetit B, Wilhelm C (2008) The synthesis of NPQ-effective zeaxanthin depends on the presence of a transmembrane proton gradient and slightly basic stromal side of the thylakoid membrane. Planta 228:999–1009
Haldrup A, Jensen PE, Lunde C, Scheller HV (2001) Balance of power: a view of the mechanism of photosynthetic state transitions. Trends Plant Sci 6:301–305
Harrison MA, Melis A (1992) Organization and stability of polypeptides associated with the chlorophyll a-b light-harvesting complex of photosystem-II. Plant Cell Physiol 33:627–637
Härtel H, Lokstein H (1995) Relationship between quenching of maximum and dark-level chlorophyll fluorescence in vivo: dependence on photosystem II antenna size. Biochim Biophys Acta 1228:91–94
Härtel H, Lokstein H, Grimm B, Rank B (1996) Kinetic studies on the xanthophyll cycle in barley leaves. Plant Physiol 110:471–482
Havaux M, Dall’Osto L, Bassi R (2007) Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiol 145:1506–1520
Hendrickson L, Furbank RT, Chow WS (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynth Res 82:73–81
Holt NE, Fleming GR, Niyogi KK (2004) Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43:8381–8289
Holt NE, Zigmantas D, Valkunas L, Li XP, Niyogi KK, Fleming GR (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307:433–436
Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684
Horton P, Wentworth M, Ruban AV (2005) Control of the light harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching. FEBS Lett 579:4201–4206
Jahns P, Krause GH (1994) Xanthophyll cycle and energy-dependent fluorescence quenching in leaves from pea plants grown under intermittent light. Planta 192:176–182
Jansson S (1999) A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci 4:236–240
Jung HS, Niyogi KK (2009) Quantitative genetic analysis of thermal dissipation in Arabidopsis. Plant Physiol 150:977–986
Klughammer C, Schreiber U (2008) Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method. PAM Appl Notes 1:27–35
Kovács L, Damkjær J, Kereïche S, Ilioaia C, Ruban AV, Boekema EJ, Jansson S, Horton P (2006) Lack of the light-harvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts. Plant Cell 18:3106–3120
Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218
Külheim C, Jansson S (2005) What leads to reduced fitness in non-photochemical quenching mutants? Physiol Plant 125:202–211
Külheim C, Ågren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297:91–93
Lambrev PH, Nilkens M, Miloslavina Y, Jahns P, Holzwarth AR (2010) Kinetic and spectral resolution of multiple nonphotochemical quenching components in Arabidopsis leaves. Plant Physiol 152:1611–1624
Li XP, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light-harvesting. Nature 403:391–395
Li XP, Müller-Moulé P, Gilmore AM, Niyogi KK (2002a) PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc Natl Acad Sci 99:15222–15227
Li XP, Phippard A, Pasari J, Niyogi KK (2002b) Structure–function analysis of photosystem II subunit S (PsbS) in vivo. Funct Plant Biol 29:1131–1139
Lichtenthaler HK (1987) Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. In: Packer L, Douce R (eds.) Methods in enzymology. Academic Press, New York, 148:350–382
Lokstein H, Härtel H, Hoffmann P (1993) Comparison of chlorophyll fluorescence quenching in leaves of wild-type with a chlorophyll-b-less mutant of barley (Hordeum vulgare L.). J Photochem Photobiol B: Biol 19:217–225
Lokstein H, Härtel H, Hoffmann P, Woitke P, Renger G (1994) The role of light-harvesting complex II in excess excitation energy dissipation: an in vivo fluorescence study on the origin of high-energy quenching. J Photochem Photobiol B: Biol 26:175–184
Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359
Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10:1121–1134
Peter GF, Thornber JP (1991) Biochemical composition and organization of higher plant photosystem II light-harvesting pigment-proteins. J Biol Chem 266:16745–16754
Peterson RB, Havir EA (2000) A nonphotochemical-quenching-deficient mutant of Arabidopsis thaliana possessing normal pigment composition and xanthophyll-cycle activity. Planta 210:205–214
Peterson RB, Havir EA (2001) Photosynthetic properties of an Arabidopsis thaliana mutant possessing a defective PsbS gene. Planta 214:142–152
Pfündel E, Renganathan M, Gilmore AM, Yamamoto HY, Dilley RA (1994) Intrathylakoid pH in isolated pea chloroplasts as probed by violaxanthin de-epoxidation. Plant Physiol 106:1647–1658
Ruban AV, Wentworth M, Yakushevska AE, Andersson J, Lee PJ, Keegstra W, Dekker JP, Boekema EJ, Jansson S, Horton P (2003) Plants lacking the main light-harvesting complex retain photosystem II macro-organization. Nature 421:648–653
Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62
Van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150
Váradi Gy, Polyánka H, Darkó É, Lehoczki E (2003) Atrazine resistance entails a limited xanthophyll cycle activity, a lower PSII efficiency and an altered pattern of excess excitation dissipation. Physiol Plant 118:47–56
Acknowledgments
This work was supported by the Hungarian Research Fund (OTKA) (Grant Number T-035252). Our special thanks are due to P. Horton for providing the A. thaliana mutant plants for this study and to L. Kovács, G. Laskay and T. Jávorfi for their critical comments on the manuscript.
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Communicated by K. Strzalka.
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Bajkán, S., Várkonyi, Z. & Lehoczki, E. Comparative study on energy partitioning in photosystem II of two Arabidopsis thaliana mutants with reduced non-photochemical quenching capacity. Acta Physiol Plant 34, 1027–1034 (2012). https://doi.org/10.1007/s11738-011-0899-1
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DOI: https://doi.org/10.1007/s11738-011-0899-1


