Effects of lincomycin on PSII efficiency, non-photochemical quenching, D1 protein and xanthophyll cycle during photoinhibition and recovery
Kristine Mueh Bachmann A D , Volker Ebbert A , William W. Adams III A , Amy S. Verhoeven B , Barry A. Logan C and Barbara Demmig-Adams AA Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80 309-0034, USA.
B Biology Department, University of Saint Thomas, 2115 Summit Ave, (OWS390), St. Paul, MN 55 105, USA.
C Biology Department, Bowdoin College, 6500 College Station, Brunswick, ME 04 011, USA.
D Corresponding author; email: kristine.bachmann@colorado.edu
Functional Plant Biology 31(8) 803-813 https://doi.org/10.1071/FP04022
Submitted: 27 January 2004 Accepted: 10 May 2004 Published: 23 August 2004
Abstract
Leaves of Parthenocissus quinquefolia (L.) Planch. (Virginia creeper) were treated with lincomycin (an inhibitor of chloroplast-encoded protein synthesis), subjected to a high-light treatment and allowed to recover in low light. While lincomycin-treated leaves had similar characteristics as controls after a 1 h exposure to high light, total D1 levels in lincomycin-treated leaves were half those in controls at the end of the recovery period. In addition, lincomycin delayed recovery of maximal PSII efficiency of open centers (ratio of variable to maximal chlorophyll fluorescence, F v / F m) and of estimated PSII photochemistry rate upon return to low light subsequent to the high-light treatment. Furthermore, lincomycin treatment slowed the removal of zeaxanthin (Z) and antheraxanthin (A) during recovery in low light, and the level of thermal energy dissipation (non-photochemical fluorescence quenching, NPQ) remained elevated. In lincomycin-treated leaves infiltrated with the uncoupler nigericin immediately after high-light exposure, thermal energy dissipation, sustained with lincomycin alone, declined quickly to control levels. In summary, lincomycin treatment affected not only D1 protein turnover but also xanthophyll-cycle operation and thermal-energy dissipation. The latter effect was apparently a result of the maintenance of a high trans-thylakoid proton gradient. Similar effects were also seen subsequent to short-term exposures to high light in lincomycin-treated Spinacia oleracea L. (spinach) leaves. In contrast, lincomycin treatments under low-light levels did not induce Z formation or NPQ. These results suggest that lincomycin has the potential to lower PSII efficiency (F v / F m) through inhibition of NPQ relaxation and Z + A removal subsequent to high-light exposures.
Keywords: Cucurbita pepo, energy dissipation, light stress, nigericin, Parthenocissus quinquefolia, photoinhibition, photoprotection, zeaxanthin.
Acknowledgments
We thank our colleague, Dr Autar K. Mattoo, for donation of an antibody against the D1 protein. This work was supported by a grant from the USA Department of Agriculture (Award Number 00–35100–9564) and a Fellowship from the David and Lucile Packard Foundation to BD-A.
Adams WW, Demmig-Adams B
(1992) Operation of the xanthophyll cycle in higher plants in response to diurnal changes in incident sunlight. Planta 186, 390–398.
Adams WW,
Demmig-Adams B,
Rosenstiel TN, Ebbert V
(2001a) Dependence of photosynthesis and energy dissipation activity upon growth form and light environment during the winter. Photosynthesis Research 67, 51–62.
| Crossref | GoogleScholarGoogle Scholar |
Anderson JM, Aro E-M
(1994) Grana stacking and protection of photosystem II in thylakoid membranes of higher plant leaves under sustained high irradiance: an hypothesis. Photosynthesis Research 41, 315–326.
Bassi R, Caffarri S
(2000) Lhc proteins and the regulation of photosynthetic light harvesting function by xanthophylls. Photosynthesis Research 64, 243–256.
| Crossref | GoogleScholarGoogle Scholar |
Booij-James IS,
Swegle WN,
Edelman M, Mattoo AK
(2002) Phosphorylation of the D1 photosystem II reaction center protein is controlled by an endogenous circadian rhythm. Plant Physiology 130, 2069–2075.
| Crossref |
PubMed |
Demmig-Adams B, Adams WW
(1992) Carotenoid composition in sun and shade leaves of plants with different life forms. Plant, Cell and Environment 15, 411–419.
Demmig-Adams B, Adams WW
(1993) Xanthophyll cycle, protein turnover, and the high-light tolerance of sun-acclimated leaves. Plant Physiology 103, 1413–1420.
| PubMed |
Demmig-Adams B, Adams WW
(1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science 1, 21–26.
| Crossref | GoogleScholarGoogle Scholar |
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. Physiologia Plantarum 98, 253–264.
| Crossref | GoogleScholarGoogle Scholar |
Demmig-Adams B,
Moeller DL,
Logan BA, Adams WW
(1998) Positive correlation between levels of retained zeaxanthin + antheraxanthin and degree of photoinhibition in shade leaves of Schefflera arboricola (Hayata) Merrill. Planta 205, 367–374.
| Crossref | GoogleScholarGoogle Scholar |
Dominici P,
Caffarri S,
Armenante F,
Ceoldo S,
Crimi M, Bassi R
(2002) Biochemical properties of the PsbS subunit of photosystem II either purified from chloroplast or recombinant. Journal of Biological Chemistry 277, 22 750–22 758.
| Crossref | GoogleScholarGoogle Scholar |
Ebbert V,
Demmig-Adams B,
Adams WW,
Mueh KE, Staehelin LA
(2001) Association between persistent forms of zeaxanthin-dependent energy dissipation and thylakoid protein phosphorylation. Photosynthesis Research 67, 63–78.
| Crossref | GoogleScholarGoogle Scholar |
Ettinger WF,
Clear AM,
Fanning KJ, Peck ML
(1999) Identification of a Ca2+
Plant Physiology 119, 1379–1385.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fiekers JF,
Marshall IG, Parsons RL
(1979) Clindamycin and lincomycin alter miniature endplate current decay. Nature 281, 680–682.
| PubMed |
Genty B,
Briantais J-M, Baker N
(1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
Gilmore AM
(1997) Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiologia Plantarum 99, 197–209.
| Crossref | GoogleScholarGoogle Scholar |
Gilmore AM, Yamamoto HY
(1991) resolution of lutein and zeaxanthin using a non-endcapped, lightly carbon-loaded C-18 high-performance liquid chromatographic column. Journal of Chromatography 543, 137–145.
| Crossref | GoogleScholarGoogle Scholar |
Greer DH,
Berry JA, Björkman O
(1986) Photoinhibition of photosynthesis in intact bean leaves: role of light and temperature, and requirement for chloroplast-protein synthesis during recovery. Planta 168, 253–260.
Jahns P, Miehe B
(1996) Kinetic correlation of recovery from photoinhibition and zeaxanthin epoxidation. Planta 198, 202–210.
Jegerschöld C,
Rutherford AW,
Mattioli TA,
Crimi M, Bassi R
(2000) Calcium binding to the photosystem II subunit CP29. Journal of Biological Chemistry 275, 12 781–12 788.
| Crossref | GoogleScholarGoogle Scholar |
Jin ES,
Polle JEW, Melis A
(2001) Involvement of zeaxanthin and of the Cbr protein in the repair of photosystem II from photoinhibition in the green alga Dunaliella salina.
Biochimica et Biophysica Acta 1506, 244–259.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kitajima M, Butler WL
(1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochimica et Biophysica Acta 376, 105–115.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lee H-Y,
Hong Y-N, Chow WS
(2002) Putative effects of pH in intro-thylakoid compartments on photoprotection of functional photosystem II complexes by photoinactivated neighbours and on recovery from photoinactivation in Capsicum annuum leaves. Functional Plant Biology 29, 607–619.
| Crossref | GoogleScholarGoogle Scholar |
Li X-P,
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Li X-P,
Phippard A,
Pasari J, Niyogi KK
(2002) Structure–function analysis of photosystem II subunit S (PsbS) in vivo. Functional Plant Biology 29, 1131–1139.
| Crossref | GoogleScholarGoogle Scholar |
Mattoo AK, Edelman B
(1987) Intramembrane translocation and posttranslational palmitoylation of the chloroplast 32 kDa herbicide-binding protein. Proceedings of the National Academy of Sciences USA 84, 1497–1501.
Melis A
(1999) Photosystem II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends in Plant Science 4, 130–135.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mohanty N, Yamamoto HY
(1995) Mechanisms of non-photochemical chlorophyll fluorescence quenching. I. The role of de-epoxidized xanthophylls and sequestered thylakoid membrane protons as probed by dibucaine. Australian Journal of Plant Physiology 22, 231–238.
Niyogi KK
(1999) Photoprotection revisited: genetic and molecular responses. Annual Review of Plant Physiology and Plant Molecular Biology 50, 333–359.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ottander C,
Campbell D, Öquist G
(1995) Seasonal changes in photosystem II organization and pigment composition in Pinus sylvestris.
Planta 197, 176–183.
Pan RS, Dilley RA
(2000) Influence of Ca2+ on the thylakoid lumen violaxanthin de-epoxidase activity through Ca2+ gating of H+ flux at the CFo H+ channel. Photosynthesis Research 65, 141–154.
| Crossref | GoogleScholarGoogle Scholar |
Powles SB
(1984) Photoinhibition of photosynthesis induced by visible light. Annual Review of Plant Physiology 35, 15–44.
| Crossref | GoogleScholarGoogle Scholar |
Prior C,
Fiekers JF,
Henderson F,
Dempster J,
Marshall IG, Parsons RL
(1990) End-plate ion channel block produced by lincosamide antibiotics and their chemical analogs. Journal of Pharmacology and Experimental Therapeutics 255, 1170–1176.
| PubMed |
Salter AH,
Virgin I,
Hagman A, Andersson B
(1992) On the molecular mechanism of light-induced D1 protein degradation in photosystem II core particles. Biochemistry 31, 3990–3998.
| PubMed |
Schreiber U, Bilger W, Neubauer C
(1994) Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of in vivo photosynthesis. ‘Ecophysiology of photosynthesis’. (Eds E-D Schulze, MM Caldwell)
pp. 49–70. (Springer-Verlag: Berlin, Germany)
Shavit N,
Dilley RA, San Pietro A
(1968) Ion translocation in isolated chloroplasts. Uncoupling of photophosphorylation and translocation of K+ and H+ ions induced by nigericin. Biochemistry 7, 2356–2363.
| PubMed |
Swiatek M,
Kuras R,
Sokolenko A,
Higgs D, Olive J ,
et al
.
(2001) The chloroplasts gene ycf9 encodes a photosystem II (PSII) core subunit, PsbZ, that participates in PSII supramolecular architecture. The Plant Cell 13, 1347–1367.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Trissl HW, Lavergne J
(1995) Fluorescence induction from photosystem-II — analytical equations for the yields of photochemistry and fluorescence derived from analysis of a model including exciton-radical pair equilibrium and restricted energy-transfer between photosynthetic units. Australian Journal of Plant Physiology 22, 183–193.
Tyystjärvi E, Aro E-M
(1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proceedings of the National Academy of Sciences USA 93, 2213–2218.
| Crossref | GoogleScholarGoogle Scholar |
Tyystjärvi E,
Ali-Yrkkö K,
Kettunen R, Aro E-M
(1992) Slow degradation of the D1 protein is related to the susceptibility of low-light grown pumpkin plants to photoinhibition. Plant Physiology 100, 1310–1317.
