DOI: 10.1126/science.1105833. Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting

Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting

10.1126/science.1105833

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

Photosynthetic light harvesting in excess light is regulated by a process known as feedback deexcitation. Femtosecond transient absorption measurements on thylakoid membranes show selective formation of a carotenoid radical cation upon excitation of chlorophyll under conditions of maximum, steady-state feedback deexcitation. Studies on transgenic Arabidopsis thaliana plants confirmed that this carotenoid radical cation formation is correlated with feedback deexcitation and requires the presence of zeaxanthin, the specific carotenoid synthesized during high light exposure. These results indicate that energy transfer from chlorophyll molecules to a chlorophyllzeaxanthin heterodimer, which then undergoes charge separation, is the mechanism for excess energy dissipation during feedback deexcitation.

Bibliography

Holt, N. E., Zigmantas, D., Valkunas, L., Li, X.-P., Niyogi, K. K., & Fleming, G. R. (2005). Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting. Science, 307(5708), 433â436.

Authors 6

Nancy E. Holt (first)
Donatas Zigmantas (additional)
Leonas Valkunas (additional)
Xiao-Ping Li (additional)
Krishna K. Niyogi (additional)
Graham R. Fleming (additional)

References 28 Referenced 696

B. Demmig-Adams, Biochim. Biophys. Acta1020, 1 (1990). (10.1016/0005-2728(90)90088-L) / Biochim. Biophys. Acta (1990)
X.-P. Li, P. Müller-Moulé, A. M. Gilmore, K. K. Niyogi, Proc. Natl. Acad. Sci. U.S.A.99, 15222 (2002). (10.1073/pnas.232447699) / Proc. Natl. Acad. Sci. U.S.A. (2002)
10.1126/science.1072359
10.1016/0968-0004(92)90503-2
10.1146/annurev.arplant.50.1.333
M. Havaux, K. K. Niyogi, Proc. Natl. Acad. Sci. U.S.A.96, 8762 (1999). (10.1073/pnas.96.15.8762) / Proc. Natl. Acad. Sci. U.S.A. (1999)
P. Horton, A. V. Ruban, R. G. Walters, Annu. Rev. Plant Physiol.47, 655 (1996). (10.1146/annurev.arplant.47.1.655) / Annu. Rev. Plant Physiol. (1996)
P. Müller, X.-P. Li, K. K. Niyogi, Plant Physiol.125, 1558 (2001). (10.1104/pp.125.4.1558) / Plant Physiol. (2001)
B. Demmig-Adams, W. W. Adams III, Trends Plant Sci.1, 21 (1996). (10.1016/S1360-1385(96)80019-7) / Trends Plant Sci. (1996)
X.-P. Li, A. Phippard, J. Pasari, K. K. Niyogi, Funct. Plant Biol.29, 1131 (2002). (10.1071/FP02065) / Funct. Plant Biol. (2002)
X.-P. Li et al., J. Biol. Chem.279, 22866 (2004). (10.1074/jbc.M402461200) / J. Biol. Chem. (2004)
10.1038/35000131
Y.-Z. Ma, N. E. Holt, X.-P. Li, K. K. Niyogi, G. R. Fleming, Proc. Natl. Acad. Sci. U.S.A.100, 4377 (2003). (10.1073/pnas.0736959100) / Proc. Natl. Acad. Sci. U.S.A. (2003)
See supporting data on Science Online.
T. Polívka et al., J. Phys. Chem. B106, 11016 (2002). (10.1021/jp025752p) / J. Phys. Chem. B (2002)
10.1021/bi0345844
T. Polívka, T. Pullerits, H. A. Frank, R. J. Cogdell, V. Sundström, J. Phys. Chem. B108, 15398 (2004). (10.1021/jp0483019) / J. Phys. Chem. B (2004)
B. J. Pogson, K. K. Niyogi, O. Björkman, D. DellaPenna, Proc. Natl. Acad. Sci. U.S.A.95, 13324 (1998). (10.1073/pnas.95.22.13324) / Proc. Natl. Acad. Sci. U.S.A. (1998)
K. K. Niyogi, A. R. Grossman, O. Björkman, Plant Cell10, 1121 (1998). (10.1105/tpc.10.7.1121) / Plant Cell (1998)
N. E. Holt et al . data not shown.
J. A. Jeevarajan, C. C. Wei, A. S. Jeevarajan, L. D. Kispert, J. Phys. Chem.100, 5637 (1996). (10.1021/jp9530663) / J. Phys. Chem. (1996)
D. Zigmantas, R. G. Hiller, V. Sundström, T. Polívka, Proc. Natl. Acad. Sci. U.S.A.99, 16760 (2002). (10.1073/pnas.262537599) / Proc. Natl. Acad. Sci. U.S.A. (2002)
G. Kodis et al., J. Phys. Chem. B108, 414 (2004). (10.1021/jp036139o) / J. Phys. Chem. B (2004)
J. Pan, Y. Xu, L. Sun, V. Sundström, T. Polívka, J. Am. Chem. Soc.126, 3066 (2004). (10.1021/ja031775l) / J. Am. Chem. Soc. (2004)
A. Dreuw, G. R. Fleming, M. Head-Gordon, Phys. Chem. Chem. Phys.5, 3247 (2003). (10.1039/b304944b) / Phys. Chem. Chem. Phys. (2003)
J. Nield, C. Funk, J. Barber, Philos. Trans. R. Soc. London Ser. B355, 1337 (2000). (10.1098/rstb.2000.0695) / Philos. Trans. R. Soc. London Ser. B (2000)
Z. Liu et al., Nature428, 287 (2004). (10.1038/nature02373) / Nature (2004)
We thank M. Kobayashi and S. McCarthy for assistance with thylakoid preparations and G. Brudwig for the β-carotene radical cation absorption spectrum. Supported by the Fulbright Program (L.V.) and by the Office of Basic Energy Sciences Chemical Sciences Division U.S. Department of Energy (contract DE-AC03-76SF00098).

Dates

Type	When
Created	20 years, 7 months ago (Jan. 20, 2005, 4:11 p.m.)
Deposited	1 year, 7 months ago (Jan. 9, 2024, 11:45 p.m.)
Indexed	1 week, 2 days ago (Aug. 27, 2025, 12:38 p.m.)
Issued	20 years, 7 months ago (Jan. 21, 2005)
Published	20 years, 7 months ago (Jan. 21, 2005)
Published Print	20 years, 7 months ago (Jan. 21, 2005)

Funders 0

None

BibTeX

@article{Holt_2005, title={Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting}, volume={307}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.1105833}, DOI={10.1126/science.1105833}, number={5708}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Holt, Nancy E. and Zigmantas, Donatas and Valkunas, Leonas and Li, Xiao-Ping and Niyogi, Krishna K. and Fleming, Graham R.}, year={2005}, month=jan, pages={433–436} }

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