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Involvement of a Second Xanthophyll Cycle in Non-Photochemical Quenching of Chlorophyll Fluorescence: The Lutein Epoxide Story

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Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 40))

Summary

The lutein epoxide (Lx) cycle (Lx-L cycle), initially described in tomato fruits, remained unexplored during the following 25 years until it was re-discovered in the stems of the parasitic plant Cuscuta reflexa. Since then, 15 years of continuous research have revealed that the Lx-L cycle is present in a wide diversity of species, allowing us to make significant progress in our understanding of this carotenoid cycle. However, due to its absence in some traditional model plant species, much of its functional significance remains to be clarified. We have therefore provided an overview of the current knowledge of this cycle as well as an ecological perspective of the possible benefits derived from the possession of two xanthophyll cycles (all plants possess a xanthophyll cycle involving violaxanthin, antheraxanthin, and zeaxanthin, i.e., the VAZ cycle, whereas only some species possess the Lx-L cycle). In the Lx-L cycle, Lx is de-epoxidized upon illumination, by the action of violaxanthin de-epoxidase (VDE), and transformed into lutein (L). Correlative evidence supports a role for this newly formed L (ΔL) in the regulation of thermal energy dissipation as assessed from the non-photochemical quenching of chlorophyll fluorescence (NPQ). The reversibility of this reaction in darkness differentiates two modes of operation, one “completed” in which the initial Lx pool is restored and one “truncated” in which ΔL remains for a longer period. The first, described in sun and shade leaves of a few unrelated species, apparently provides fine-tuning for the adjustment of photoprotective energy dissipation complementary to that exerted by the VAZ cycle. On the other hand, the “truncated” cycle is widespread amongst woody plants, but is restricted to shaded environments where it may act as a rapid switch for the photosynthetic apparatus from a photosynthetically highly efficient state to a photoprotected one. The latter may be necessary for chloroplast acclimation after transition to high light, such as that which occurs following gap formation in forests or budbreak and subsequent leaf greening in trees.

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Abbreviations

A  –  :

Antheraxanthin;

A-Lx  –  :

Accumulative Lx pool;

Chl –:

Chlorophyll;

C-Lx –:

Constitutive Lx pool;

D-Lx –:

Dynamic Lx pool;

DPS –:

De-epoxidation state of the xanthophyll cycle involving the carotenoids violaxanthin, antheraxanthin and zeaxanthin;

Fm –:

Maximal chlorophyll fluorescence emission in the dark-adapted state;

Fv –:

variable chlorophyll fluorescence emission in the dark-adapted state;

Fv/Fm –:

Intrinsic efficiency (or quantum yield) of photosystem II in the dark-adapted state;

L1 –:

Intra-protein site L1;

L2 –:

Intra-protein site L2;

LHC –:

Light-harvesting complex;

Lhcb5 –:

Chlorophyll a-b binding protein;

LHCII –:

Major light-harvesting complex of photosystem II;

Lx –:

Lutein epoxide;

Lx-L cycle –:

Lutein epoxide cycle involving the carotenoids lutein epoxide and lutein;

NPQ –:

Non-photochemical quenching of chlorophyll fluorescence;

PFDi –:

Incident photon flux density;

PS II –:

Photosystem II;

qE –:

ΔpH-dependent component of NPQ;

V –:

Violaxanthin;

V1 –:

Peripheral V1 site;

VAZ cycle –:

The xanthophyll cycle involving the carotenoids violaxanthin, antheraxanthin and zeaxanthin;

VDE –:

Violaxanthin de-epoxidase;

Z  –  :

Zeaxanthin;

ZEP  –  :

Zeaxanthin epoxidase;

α-C –:

α-carotene;

β-C –:

β-carotene;

ΔL –:

Newly formed L from Lx de-epoxidation

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Acknowledgments

The authors acknowledge the support of research grants BFU 2010-15021, UPV/EHU-GV IT-299-07, and a Fellowship from the Basque Government, the doctor specialization grant from the UPV/EHU, and the JAE-Doc fellow from the Spanish National Research Council (CSIC) received by RE. We also thank Brian Webster for language editing. We are greatly indebted to all the researchers involved in the Lx-L cycle for advancing knowledge in this field, and especially to our friends and colleagues Barry Osmond and Shizue Matsubara for their helpful comments and continuous advice in the endeavor to understand what is behind the Lx-L cycle. We also thank Marisol Jimenez, Domingo Morales, Patricia Brito, Eduardo Jimenez and Beatriz Fernandez-Marín for their constant help and support during field studies in Tenerife. Finally, we thank the useful comments of the reviewers and the editor.

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Authors and Affiliations

  1. Department of Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Bilbao, 48080, Spain

    Raquel Esteban & José I. García-Plazaola

  2. Agrobiotechnology Institute, IdAB-CSIC-UPNA-Government of Navarre, Pamplona, E-31192, Spain

    Raquel Esteban

Authors
  1. Raquel Esteban
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  2. José I. García-Plazaola
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Correspondence to Raquel Esteban .

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Editors and Affiliations

  1. Ecology and Evolutionary Biology, University of Colorado, Boulder, Boulder, Colorado, USA

    Barbara Demmig-Adams

  2. Laboratory of Photosynthetic Membranes Biological Research Center, Institute of Plant Biology Hungarian Academy of Sciences, Szeged, Hungary

    Gyozo Garab

  3. Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, USA

    William Adams III

  4. Department of Plant Biology 265 Morrill Hall, MC-116, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA

    Govindjee

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Esteban, R., García-Plazaola, J.I. (2014). Involvement of a Second Xanthophyll Cycle in Non-Photochemical Quenching of Chlorophyll Fluorescence: The Lutein Epoxide Story. In: Demmig-Adams, B., Garab, G., Adams III, W., Govindjee, . (eds) Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Advances in Photosynthesis and Respiration, vol 40. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9032-1_12

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