Evolution of an atypical de-epoxidase for photoprotection in the green lineage

Nature Plants

Volumn 2, Issue 10, 2016, Pages

  Li, Zhirong ^a,b   Peers, Graham ^c   Dent, Rachel M ^a   Bai, Yong ^a   Yang, Scarlett Y ^a,d   Apel, Wiebke ^a,e   Leonelli, Lauriebeth ^a   Niyogi, Krishna K ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c Department of Environmental and Radiological Health Sciences   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; OXIDOREDUCTASE; VIOLAXANTHIN DE-EPOXIDASE;

CHLAMYDOMONAS REINHARDTII; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PHOTOSYNTHESIS; PHYLOGENY; PHYSIOLOGY; THYLAKOID;

BACTERIAL PROTEINS; CHLAMYDOMONAS REINHARDTII; EVOLUTION, MOLECULAR; OXIDOREDUCTASES; PHOTOSYNTHESIS; PHYLOGENY; THYLAKOIDS;

EID: 84990206869     PISSN: None     EISSN: 20550278     Source Type: Journal    
DOI: 10.1038/nplants.2016.140     Document Type: Article

References (34)

1. Demmig-Adams, B. Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim. Biophys. Acta 1020, 1-24 (1990).
2. Jahns, P., Latowski, D. and Strzalka, K. Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim. Biophys. Acta 1787, 3-14 (2009).
3. Maresca, J. A., Graham, J. E., Wu, M., Eisen, J. A. and Bryant, D. A. Identification of a fourth family of lycopene cyclases in photosynthetic bacteria. Proc. Natl Acad. Sci. USA 104, 11784-11789 (2007).
4. Niyogi, K. K. Photoprotection revisited: genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 333-359 (1999).
5. Muller, P., Li, X.-P. and Niyogi, K. K. Non-photochemical quenching. A response to excess light energy. Plant Physiol. 125, 1558-1566 (2001).
6. Ruban, A. V., Johnson, M. P. and Duffy, C. D. P. The photoprotective molecular switch in the photosystem II antenna. Biochim. Biophys. Acta 1817, 167-181 (2012).
7. Niyogi, K. K. and Truong, T. B. Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr. Opin. Plant Biol. 16, 307-314 (2013).
8. Briantais, J. M., Vernotte, C., Picaud, M. and Krause, G. H. A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochim. Biophys. Acta 548, 128-138 (1979).
9. Casper-Lindley, C. and Bjorkman, O. Fluorescence quenching in four unicellular algae with different light-harvesting and xanthophyll-cycle pigments. Photosynth. Res. 56, 277-289 (1998).
10. Lunch, C. K. et al. The xanthophyll cycle and NPQ in diverse desert and aquatic green algae. Photosynth. Res. 115, 139-151 (2013).
11. Quaas, T. et al. Non-photochemical quenching and xanthophyll cycle activities in six green algal species suggest mechanistic differences in the process of excess energy dissipation. J. Plant Physiol. 172, 92-103 (2015).
12. Baroli, I., Do, A. D., Yamane, T. and Niyogi, K. K. Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects Chlamydomonas reinhardtii from photooxidative stress. Plant Cell 15, 992-1008 (2003).
13. Baroli, I. and Niyogi, K. K. Molecular genetics of xanthophyll-dependent photoprotection in green algae and plants. Phil. Trans. R. Soc. Lond. B 355, 1385-1394 (2000).
14. Havaux, M. and Niyogi, K. K. The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc. Natl Acad. Sci. USA 96, 8762-8767 (1999).
15. Niyogi, K. K., Bjorkman, O. and Grossman, A. R. Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell 9, 1369-1380 (1997).
16. Niyogi, K. K., Grossman, A. R. and Bjorkman, O. Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10, 1121-1134 (1998).
17. Anwaruzzaman, M. et al. Genomic analysis of mutants affecting xanthophyll biosynthesis and regulation of photosynthetic light harvesting in Chlamydomonas reinhardtii. Photosynth Res. 82, 265-276 (2004).
18. Yamamoto, H. Y. in Photoprotection, Photoinhibition, Gene Regulation, and Environment Vol. 21 (eds Demmig-Adams, B., Adams, W. W. III and Mattoo, A. K.) Ch. 1, 1-10 (Advances in Photosynthesis and Respiration Series, Springer Netherlands, 2006).
19. Macko, S., Wehner, A. and Jahns, P. Comparison of violaxanthin de-epoxidation from the stroma and lumen sides of isolated thylakoid membranes from Arabidopsis: implications for the mechanism of de-epoxidation. Planta 216, 309-314 (2002).
20. Britton, G. Later reactions of carotenoid biosynthesis. Pure Appl. Chem. 47, 223-236 (1976).
21. Bradbury, L. M. T. et al. Lycopene cyclase paralog CruP protects against reactive oxygen species in oxygenic photosynthetic organisms. Proc. Natl Acad. Sci. USA 109, E1888-E1897 (2012).
22. Leliaert, F. et al. Phylogeny and molecular evolution of the green algae. Crit. Rev. Plant Sci. 31, 1-46 (2012).
23. Kathir, P. et al. Molecular map of the Chlamydomonas reinhardtii nuclear genome. Eukaryotic Cell 2, 362-379 (2003).
24. Dent, R. M. et al. Large-scale insertional mutagenesis of Chlamydomonas supports phylogenomic functional prediction of photosynthetic genes and analysis of classical acetate-requiring mutants. Plant J. 82, 337-351 (2015).
25. Dent, R. M., Haglund, C. M., Chin, B. L., Kobayashi, M. C. and Niyogi, K. K. Functional genomics of eukaryotic photosynthesis using insertional mutagenesis of Chlamydomonas reinhardtii. Plant Physiol. 137, 545-556 (2005).
26. Muller-Moule, P., Conklin, P. L. and Niyogi, K. K. Ascorbate deficiency can limit violaxanthin de-epoxidase activity in vivo. Plant Physiol. 128, 970-977 (2002).
27. Horton, R. M., Cai, Z. L., Ho, S. N. and Pease, L. R. Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8, 528-535 (1990).
28. Earley, K. W. et al. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616-629 (2006).
29. Zhang, X., Henriques, R., Lin, S.-S., Niu, Q.-W. and Chua, N.-H. Agrobacteriummediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 1, 641-646 (2006).
30. Leonelli, L., Erickson, E., Lyska, D. and Niyogi, K. K. Transient expression in Nicotiana benthamiana for rapid functional analysis of genes involved in non-photochemical quenching and carotenoid biosynthesis. Plant J. http://dx.doi.org/10.1111/tpj.13268 (2016).
31. Brooks, M. and Niyogi, K. in Chloroplast Research in Arabidopsis Vol. 775 (ed. Paul Jarvis, R.) Ch. 16, 299-310 (Methods in Molecular Biology Series, Humana Press, 2011).
32. Harris, E. H. The Chlamydomonas Sourcebook (Academic Press, 1989).
33. Chua, N. H. and Bennoun, P. Thylakoid membrane polypeptides of Chlamydomonas reinhardtii: wild-type and mutant strains deficient in photosystem II reaction center. Proc. Natl Acad. Sci. USA 72, 2175-2179 (1975).
34. Brooks, M. D., Sylak-Glassman, E. J., Fleming, G. R. and Niyogi, K. K. A thioredoxin-like/β-propeller protein maintains the efficiency of light harvesting in Arabidopsis. Proc. Natl Acad. Sci. USA 110, E2733-E2740 (2013).