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

Li, Zhirong; Peers, Graham; Dent, Rachel M.; Bai, Yong; Yang, Scarlett Y.; Apel, Wiebke; Leonelli, Lauriebeth; Niyogi, Krishna K.

doi:10.1038/nplants.2016.140

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

Journal Article · Mon Sep 12 00:00:00 EDT 2016 · Nature Plants (Online)

DOI:https://doi.org/10.1038/nplants.2016.140· OSTI ID:1420103

Li, Zhirong ^[1]; ^[2]; Dent, Rachel M. ^[3]; Bai, Yong ^[3]; Yang, Scarlett Y. ^[3]; Apel, Wiebke ^[3]; Leonelli, Lauriebeth ^[3]; Niyogi, Krishna K. ^[1]

Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst., Department of Plant and Microbial Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division
Colorado State Univ., Fort Collins, CO (United States). Dept. of Biology
Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst., Department of Plant and Microbial Biology

Plants, algae and cyanobacteria need to regulate photosynthetic light harvesting in response to the constantly changing light environment. Rapid adjustments are required to maintain fitness because of a trade-off between efficient solar energy conversion and photoprotection. The xanthophyll cycle, in which the carotenoid pigment violaxanthin is reversibly converted into zeaxanthin, is ubiquitous among green algae and plants and is necessary for the regulation of light harvesting, protection from oxidative stress and adaptation to different light conditions. Violaxanthin de-epoxidase (VDE) is the key enzyme responsible for zeaxanthin synthesis from violaxanthin under excess light. Here in this paper, we show that the Chlorophycean VDE (CVDE) gene from the model green alga Chlamydomonas reinhardtii encodes an atypical VDE. This protein is not homologous to the VDE found in plants and is instead related to a lycopene cyclase from photosynthetic bacteria. Unlike the plant-type VDE that is located in the thylakoid lumen, the Chlamydomonas CVDE protein is located on the stromal side of the thylakoid membrane. Phylogenetic analysis suggests that CVDE evolved from an ancient de-epoxidase that was present in the common ancestor of green algae and plants, providing evidence of unexpected diversity in photoprotection in the green lineage.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1420103

Journal Information:: Nature Plants (Online), Journal Name: Nature Plants (Online) Journal Issue: 10 Vol. 2; ISSN 2055-0278

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (33)

Comparison of violaxanthin de-epoxidation from the stroma and lumen sides of isolated thylakoid membranes from Arabidopsis : implications for the mechanism of de-epoxidation Macko, Susanne; Wehner, Antje; Jahns, Peter Planta, Vol. 216, Issue 2 https://doi.org/10.1007/s00425-002-0848-8	journal	December 2002
The xanthophyll cycle and NPQ in diverse desert and aquatic green algae Lunch, Claire K.; LaFountain, Amy M.; Thomas, Suzanne Photosynthesis Research, Vol. 115, Issue 2-3 https://doi.org/10.1007/s11120-013-9846-x	journal	June 2013
A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts Briantais, J. -M.; Vernotte, C.; Picaud, M. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 548, Issue 1 https://doi.org/10.1016/0005-2728(79)90193-2	journal	October 1979
Non-photochemical quenching and xanthophyll cycle activities in six green algal species suggest mechanistic differences in the process of excess energy dissipation Quaas, Theresa; Berteotti, Silvia; Ballottari, Matteo Journal of Plant Physiology, Vol. 172 https://doi.org/10.1016/j.jplph.2014.07.023	journal	January 2015
Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method Zhang, Xiuren; Henriques, Rossana; Lin, Shih-Shun Nature Protocols, Vol. 1, Issue 2 https://doi.org/10.1038/nprot.2006.97	journal	June 2006
Identification of a fourth family of lycopene cyclases in photosynthetic bacteria Maresca, J. A.; Graham, J. E.; Wu, M. Proceedings of the National Academy of Sciences, Vol. 104, Issue 28 https://doi.org/10.1073/pnas.0702984104	journal	July 2007
A thioredoxin-like/ -propeller protein maintains the efficiency of light harvesting in Arabidopsis Brooks, M. D.; Sylak-Glassman, E. J.; Fleming, G. R. Proceedings of the National Academy of Sciences, Vol. 110, Issue 29 https://doi.org/10.1073/pnas.1305443110	journal	July 2013
The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism Havaux, M.; Niyogi, K. K. Proceedings of the National Academy of Sciences, Vol. 96, Issue 15 https://doi.org/10.1073/pnas.96.15.8762	journal	July 1999
Molecular genetics of xanthophyll–dependent photoprotection in green algae and plants Baroli, Irene; Niyogi, Krishna K. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 355, Issue 1402 https://doi.org/10.1098/rstb.2000.0700	journal	October 2000
Non-Photochemical Quenching. A Response to Excess Light Energy Müller, Patricia; Li, Xiao-Ping; Niyogi, Krishna K. Plant Physiology, Vol. 125, Issue 4 https://doi.org/10.1104/pp.125.4.1558	journal	April 2001
Zeaxanthin Accumulation in the Absence of a Functional Xanthophyll Cycle Protects Chlamydomonas reinhardtii from Photooxidative Stress Baroli, Irene; Do, An D.; Yamane, Tomoko The Plant Cell, Vol. 15, Issue 4 https://doi.org/10.1105/tpc.010405	journal	March 2003
Arabidopsis Mutants Define a Central Role for the Xanthophyll Cycle in the Regulation of Photosynthetic Energy Conversion Niyogi, Krishna K.; Grossman, Arthur R.; Björkman, Olle The Plant Cell, Vol. 10, Issue 7 https://doi.org/10.1105/tpc.10.7.1121	journal	July 1998
Chlamydomonas Xanthophyll Cycle Mutants Identified by Video Imaging of Chlorophyll Fluorescence Quenching. Niyogi, K. K.; Bjorkman, O.; Grossman, A. R. The Plant Cell https://doi.org/10.1105/tpc.9.8.1369	journal	August 1997
Large-scale insertional mutagenesis of Chlamydomonas supports phylogenomic functional prediction of photosynthetic genes and analysis of classical acetate-requiring mutants Dent, Rachel M.; Sharifi, Marina N.; Malnoë, Alizée The Plant Journal, Vol. 82, Issue 2 https://doi.org/10.1111/tpj.12806	journal	April 2015
Molecular Map of the Chlamydomonas reinhardtii Nuclear Genome Kathir, Pushpa; LaVoie, Matthew; Brazelton, William J. Eukaryotic Cell, Vol. 2, Issue 2 https://doi.org/10.1128/ec.2.2.362-379.2003	journal	April 2003
PHOTOPROTECTION REVISITED: Genetic and Molecular Approaches Niyogi, Krishna K. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev.arplant.50.1.333	journal	June 1999
Later Reactions of Carotenoid Biosynthesis Britton, George Pure and Applied Chemistry, Vol. 47, Issue 2-3 https://doi.org/10.1351/pac197647020223	journal	January 1976
A Random Walk To and Through the Xanthophyll Cycle Yamamoto, Harry Y. Photoprotection, Photoinhibition, Gene Regulation, and Environment https://doi.org/10.1007/1-4020-3579-9_1	book	January 2008
Use of a Pulse-Amplitude Modulated Chlorophyll Fluorometer to Study the Efficiency of Photosynthesis in Arabidopsis Plants Brooks, Matthew D.; Niyogi, Krishna K. Chloroplast Research in Arabidopsis https://doi.org/10.1007/978-1-61779-237-3_16	book	January 2011
Genomic analysis of mutants affecting xanthophyll biosynthesis and regulation of photosynthetic light harvesting in Chlamydomonas reinhardtii Anwaruzzaman, M.; Chin, Brian L.; Li, Xiao-Ping Photosynthesis Research, Vol. 82, Issue 3 https://doi.org/10.1007/s11120-004-2439-y	journal	December 2004
Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin Demmig-Adams, Barbara Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1020, Issue 1 https://doi.org/10.1016/0005-2728(90)90088-L	journal	October 1990
Mechanism and regulation of the violaxanthin cycle: The role of antenna proteins and membrane lipids Jahns, Peter; Latowski, Dariusz; Strzalka, Kazimierz Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1787, Issue 1 https://doi.org/10.1016/j.bbabio.2008.09.013	journal	January 2009
The photoprotective molecular switch in the photosystem II antenna Ruban, Alexander V.; Johnson, Matthew P.; Duffy, Christopher D. P. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 1 https://doi.org/10.1016/j.bbabio.2011.04.007	journal	January 2012
Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis Niyogi, Krishna K.; Truong, Thuy B. Current Opinion in Plant Biology, Vol. 16, Issue 3 https://doi.org/10.1016/j.pbi.2013.03.011	journal	June 2013
Fluorescence quenching in four unicellular algae with different light-harvesting and xanthophyll-cycle pigments Casper-Lindley, Catharina; Björkman, Olle Photosynthesis Research, Vol. 56, Issue 3, p. 277-289 https://doi.org/10.1023/A:1006037516479	journal	January 1998
Lycopene cyclase paralog CruP protects against reactive oxygen species in oxygenic photosynthetic organisms Bradbury, L. M. T.; Shumskaya, M.; Tzfadia, O. Proceedings of the National Academy of Sciences, Vol. 109, Issue 27 https://doi.org/10.1073/pnas.1206002109	journal	June 2012
Thylakoid membrane polypeptides of Chlamydomonas reinhardtii: wild-type and mutant strains deficient in photosystem II reaction center. Chua, N. H.; Bennoun, P. Proceedings of the National Academy of Sciences, Vol. 72, Issue 6 https://doi.org/10.1073/pnas.72.6.2175	journal	June 1975
Phylogeny and Molecular Evolution of the Green Algae Leliaert, Frederik; Smith, David R.; Moreau, Hervé Critical Reviews in Plant Sciences, Vol. 31, Issue 1 https://doi.org/10.1080/07352689.2011.615705	journal	January 2012
Ascorbate Deficiency Can Limit Violaxanthin De-Epoxidase Activity in Vivo Müller-Moulé, Patricia; Conklin, Patricia L.; Niyogi, Krishna K. Plant Physiology, Vol. 128, Issue 3 https://doi.org/10.1104/pp.010924	journal	March 2002
Functional Genomics of Eukaryotic Photosynthesis Using Insertional Mutagenesis of Chlamydomonas reinhardtii Dent, Rachel M.; Haglund, Cat M.; Chin, Brian L. Plant Physiology, Vol. 137, Issue 2 https://doi.org/10.1104/pp.104.055244	journal	January 2005
Gateway-compatible vectors for plant functional genomics and proteomics Earley, Keith W.; Haag, Jeremy R.; Pontes, Olga The Plant Journal, Vol. 45, Issue 4 https://doi.org/10.1111/j.1365-313X.2005.02617.x	journal	February 2006
Transient expression in Nicotiana benthamiana for rapid functional analysis of genes involved in non-photochemical quenching and carotenoid biosynthesis Leonelli, Lauriebeth; Erickson, Erika; Lyska, Dagmar The Plant Journal, Vol. 88, Issue 3 https://doi.org/10.1111/tpj.13268	journal	September 2016
Molecular Map of the Chlamydomonas reinhardtii Nuclear Genome Kathir, Pushpa; LaVoie, Matthew; Brazelton, William J. Eukaryotic Cell, Vol. 2, Issue 2 https://doi.org/10.1128/EC.2.2.362-379.2003	journal	April 2003

Cited By (8)

A penalty on photosynthetic growth in fluctuating light Graham, Percival J.; Nguyen, Brian; Burdyny, Thomas Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-12923-1	journal	October 2017
CCS2, an Octatricopeptide-Repeat Protein, Is Required for Plastid Cytochrome c Assembly in the Green Alga Chlamydomonas reinhardtii Cline, Sara G.; Laughbaum, Isaac A.; Hamel, Patrice P. Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01306	journal	August 2017
The Dynamics of Energy Dissipation and Xanthophyll Conversion in Arabidopsis Indicate an Indirect Photoprotective Role of Zeaxanthin in Slowly Inducible and Relaxing Components of Non-photochemical Quenching of Excitation Energy Kress, Eugen; Jahns, Peter Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.02094	journal	December 2017
DArTseq Molecular Markers Associated with the Spiny-Tip Leaf Margin in Pineapple (Ananas comosus L.) Sanewski, Garth M. Tropical Plant Biology, Vol. 13, Issue 1 https://doi.org/10.1007/s12042-019-09245-z	journal	January 2020
Ascorbate deficiency does not limit non-photochemical quenching in Chlamydomonas reinhardtii Vidal-Meireles, André; Tóth, Dávid; Kovács, László bioRxiv https://doi.org/10.1101/813766	posted_content	October 2019
Transcriptomic responses associated with carbon and energy flows under high salinity stress suggest the overflow of acetyl-CoA from glycolysis and NADPH co-factor induces high lipid accumulation and halotolerance in Chlorella sp. HS2 Yun, Jin-Ho; Pierrelée, Michaël; Cho, Dae-Hyun https://doi.org/10.1101/817551	posted_content	October 2019
Slow zeaxanthin accumulation and the enhancement of CP 26 collectively contribute to an atypical non‐photochemical quenching in macroalga Ulva prolifera under high light Gao, Shan; Zheng, Zhenbing; Wang, Jing Journal of Phycology, Vol. 56, Issue 2 https://doi.org/10.1111/jpy.12958	journal	January 2020
Photoprotection in a monophyletic branch of chlorophyte algae is independent of energy-dependent quenching (qE) Christa, Gregor; Cruz, Sónia; Jahns, Peter New Phytologist, Vol. 214, Issue 3 https://doi.org/10.1111/nph.14435	journal	February 2017

Similar Records

Final Report - The Xanthophyll Cycle

Technical Report · Thu Apr 21 00:00:00 EDT 2005 · OSTI ID:842478

Green diatom mutants reveal an intricate biosynthetic pathway of fucoxanthin

Journal Article · Sun Sep 11 20:00:00 EDT 2022 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1886753

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Chloroplasts
Light stress
Non-photochemical quenching

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

Citation Formats

References (33)

Cited By (8)

Similar Records

Related Subjects