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. 1998 Jul;10(7):1121–1134. doi: 10.1105/tpc.10.7.1121

Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion.

K K Niyogi 1, A R Grossman 1, O Björkman 1
PMCID: PMC144052  PMID: 9668132

Abstract

A conserved regulatory mechanism protects plants against the potentially damaging effects of excessive light. Nearly all photosynthetic eukaryotes are able to dissipate excess absorbed light energy in a process that involves xanthophyll pigments. To dissect the role of xanthophylls in photoprotective energy dissipation in vivo, we isolated Arabidopsis xanthophyll cycle mutants by screening for altered nonphotochemical quenching of chlorophyll fluorescence. The npq1 mutants are unable to convert violaxanthin to zeaxanthin in excessive light, whereas the npq2 mutants accumulate zeaxanthin constitutively. The npq2 mutants are new alleles of aba1, the zeaxanthin epoxidase gene. The high levels of zeaxanthin in npq2 affected the kinetics of induction and relaxation but not the extent of nonphotochemical quenching. Genetic mapping, DNA sequencing, and complementation of npq1 demonstrated that this mutation affects the structural gene encoding violaxanthin deepoxidase. The npq1 mutant exhibited greatly reduced nonphotochemical quenching, demonstrating that violaxanthin deepoxidation is required for the bulk of rapidly reversible nonphotochemical quenching in Arabidopsis. Altered regulation of photosynthetic energy conversion in npq1 was associated with increased sensitivity to photoinhibition. These results, in conjunction with the analysis of npq mutants of Chlamydomonas, suggest that the role of the xanthophyll cycle in nonphotochemical quenching has been conserved, although different photosynthetic eukaryotes rely on the xanthophyll cycle to different extents for the dissipation of excess absorbed light energy.

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Selected References

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  1. Aro E. M., Virgin I., Andersson B. Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta. 1993 Jul 5;1143(2):113–134. doi: 10.1016/0005-2728(93)90134-2. [DOI] [PubMed] [Google Scholar]
  2. Bell C. J., Ecker J. R. Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics. 1994 Jan 1;19(1):137–144. doi: 10.1006/geno.1994.1023. [DOI] [PubMed] [Google Scholar]
  3. Bilger W., Björkman O., Thayer S. S. Light-induced spectral absorbance changes in relation to photosynthesis and the epoxidation state of xanthophyll cycle components in cotton leaves. Plant Physiol. 1989 Oct;91(2):542–551. doi: 10.1104/pp.91.2.542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bugos R. C., Yamamoto H. Y. Molecular cloning of violaxanthin de-epoxidase from romaine lettuce and expression in Escherichia coli. Proc Natl Acad Sci U S A. 1996 Jun 25;93(13):6320–6325. doi: 10.1073/pnas.93.13.6320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cogdell R. J., Frank H. A. How carotenoids function in photosynthetic bacteria. Biochim Biophys Acta. 1987;895(2):63–79. doi: 10.1016/s0304-4173(87)80008-3. [DOI] [PubMed] [Google Scholar]
  6. Crofts A. R., Yerkes C. T. A molecular mechanism for qE-quenching. FEBS Lett. 1994 Oct 3;352(3):265–270. doi: 10.1016/0014-5793(94)00976-7. [DOI] [PubMed] [Google Scholar]
  7. Demmig-Adams B., Adams W. W., Heber U., Neimanis S., Winter K., Krüger A., Czygan F. C., Bilger W., Björkman O. Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts. Plant Physiol. 1990 Feb;92(2):293–301. doi: 10.1104/pp.92.2.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Demmig-Adams B., Gilmore A. M., Adams W. W., 3rd Carotenoids 3: in vivo function of carotenoids in higher plants. FASEB J. 1996 Mar;10(4):403–412. doi: 10.1096/fasebj.10.4.8647339. [DOI] [PubMed] [Google Scholar]
  9. Gilmore A. M., Hazlett T. L., Govindjee Xanthophyll cycle-dependent quenching of photosystem II chlorophyll a fluorescence: formation of a quenching complex with a short fluorescence lifetime. Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2273–2277. doi: 10.1073/pnas.92.6.2273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Green B. R., Durnford D. G. THE CHLOROPHYLL-CAROTENOID PROTEINS OF OXYGENIC PHOTOSYNTHESIS. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):685–714. doi: 10.1146/annurev.arplant.47.1.685. [DOI] [PubMed] [Google Scholar]
  11. Grossman A. R., Bhaya D., Apt K. E., Kehoe D. M. Light-harvesting complexes in oxygenic photosynthesis: diversity, control, and evolution. Annu Rev Genet. 1995;29:231–288. doi: 10.1146/annurev.ge.29.120195.001311. [DOI] [PubMed] [Google Scholar]
  12. Horton P., Ruban A. V., Walters R. G. REGULATION OF LIGHT HARVESTING IN GREEN PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):655–684. doi: 10.1146/annurev.arplant.47.1.655. [DOI] [PubMed] [Google Scholar]
  13. Horton P., Ruban A. V., Walters R. G. Regulation of Light Harvesting in Green Plants (Indication by Nonphotochemical Quenching of Chlorophyll Fluorescence). Plant Physiol. 1994 Oct;106(2):415–420. doi: 10.1104/pp.106.2.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hurry V., Anderson J. M., Chow W. S., Osmond C. B. Accumulation of Zeaxanthin in Abscisic Acid-Deficient Mutants of Arabidopsis Does Not Affect Chlorophyll Fluorescence Quenching or Sensitivity to Photoinhibition in Vivo. Plant Physiol. 1997 Feb;113(2):639–648. doi: 10.1104/pp.113.2.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jahns P., Junge W. Dicyclohexylcarbodiimide-binding proteins related to the short circuit of the proton-pumping activity of photosystem II. Identified as light-harvesting chlorophyll-a/b-binding proteins. Eur J Biochem. 1990 Nov 13;193(3):731–736. doi: 10.1111/j.1432-1033.1990.tb19393.x. [DOI] [PubMed] [Google Scholar]
  16. Lukowitz W., Mayer U., Jürgens G. Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell. 1996 Jan 12;84(1):61–71. doi: 10.1016/s0092-8674(00)80993-9. [DOI] [PubMed] [Google Scholar]
  17. Marin E., Nussaume L., Quesada A., Gonneau M., Sotta B., Hugueney P., Frey A., Marion-Poll A. Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. EMBO J. 1996 May 15;15(10):2331–2342. [PMC free article] [PubMed] [Google Scholar]
  18. Niyogi K. K., Bjorkman O., Grossman A. R. Chlamydomonas Xanthophyll Cycle Mutants Identified by Video Imaging of Chlorophyll Fluorescence Quenching. Plant Cell. 1997 Aug;9(8):1369–1380. doi: 10.1105/tpc.9.8.1369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Niyogi K. K., Björkman O., Grossman A. R. The roles of specific xanthophylls in photoprotection. Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):14162–14167. doi: 10.1073/pnas.94.25.14162. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pesaresi P., Sandonà D., Giuffra E., Bassi R. A single point mutation (E166Q) prevents dicyclohexylcarbodiimide binding to the photosystem II subunit CP29. FEBS Lett. 1997 Feb 3;402(2-3):151–156. doi: 10.1016/s0014-5793(96)01518-9. [DOI] [PubMed] [Google Scholar]
  21. Plumley F. G., Schmidt G. W. Reconstitution of chlorophyll a/b light-harvesting complexes: Xanthophyll-dependent assembly and energy transfer. Proc Natl Acad Sci U S A. 1987 Jan;84(1):146–150. doi: 10.1073/pnas.84.1.146. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pogson B., McDonald K. A., Truong M., Britton G., DellaPenna D. Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants. Plant Cell. 1996 Sep;8(9):1627–1639. doi: 10.1105/tpc.8.9.1627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rock C. D., Zeevaart J. A. The aba mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7496–7499. doi: 10.1073/pnas.88.17.7496. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ruban A. V., Young A. J., Horton P. Induction of Nonphotochemical Energy Dissipation and Absorbance Changes in Leaves (Evidence for Changes in the State of the Light-Harvesting System of Photosystem II in Vivo). Plant Physiol. 1993 Jul;102(3):741–750. doi: 10.1104/pp.102.3.741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tardy F., Havaux M. Photosynthesis, chlorophyll fluorescence, light-harvesting system and photoinhibition resistance of a zeaxanthin-accumulating mutant of Arabidopsis thaliana. J Photochem Photobiol B. 1996 Jun;34(1):87–94. doi: 10.1016/1011-1344(95)07272-1. [DOI] [PubMed] [Google Scholar]
  26. Walters R. G., Ruban A. V., Horton P. Higher plant light-harvesting complexes LHCIIa and LHCIIc are bound by dicyclohexylcarbodiimide during inhibition of energy dissipation. Eur J Biochem. 1994 Dec 15;226(3):1063–1069. doi: 10.1111/j.1432-1033.1994.01063.x. [DOI] [PubMed] [Google Scholar]
  27. Walters R. G., Ruban A. V., Horton P. Identification of proton-active residues in a higher plant light-harvesting complex. Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):14204–14209. doi: 10.1073/pnas.93.24.14204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Yamamoto H. Y., Kamite L. The effects of dithiothreitol on violaxanthin de-epoxidation and absorbance changes in the 500-nm region. Biochim Biophys Acta. 1972 Jun 23;267(3):538–543. doi: 10.1016/0005-2728(72)90182-x. [DOI] [PubMed] [Google Scholar]
  29. Young A. J., Frank H. A. Energy transfer reactions involving carotenoids: quenching of chlorophyll fluorescence. J Photochem Photobiol B. 1996 Oct;36(1):3–15. doi: 10.1016/S1011-1344(96)07397-6. [DOI] [PubMed] [Google Scholar]

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