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Functional roles of the major chloroplast lipids in the violaxanthin cycle

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Abstract

Monogalactosyldiacylglyceride (MGDG) and digalactosyldiacylglyceride (DGDG) are the major membrane lipids of chloroplasts. The question of the specialized functions of these unique lipids has received limited attention. One function is to support violaxanthin de-epoxidase (VDE) activity, an enzyme of the violaxanthin cycle. To understand better the properties of this system, the effects of galactolipids and phosphatidylcholines on VDE activity were examined by two independent methods. The results show that the micelle-forming lipid (MGDG) and bilayer forming lipids (DGDG and phosphatidylcholines) support VDE activity differently. MGDG supported rapid and complete de-epoxidation starting at a threshold lipid concentration (10 μM) coincident with complete solubilization of violaxanthin. In contrast, DGDG supported slow but nevertheless complete to nearly complete de-epoxidation at a lower lipid concentration (6.7 μM) that did not completely solubilize violaxanthin. Phosphotidylcholines showed similar effects as DGDG except that de-epoxidation was incomplete. Since VDE requires solubilized violaxanthin, aggregated violaxanthin in DGDG at low concentration must become solubilized as de-epoxidation proceeds. High lipid concentrations had lower activity possibly due to formation of multilayered structures (liposomes) that restrict accessibility of violaxanthin to VDE. MGDG micelles do not present such restrictions. The results indicate VDE operates throughout the lipid phase of the single bilayer thylakoid membrane and is not limited to putative MGDG micelle domains. Additionally, the results also explain the differential partitioning of violaxanthin between the envelope and thylakoid as due to the relative solubilities of violaxanthin and zeaxanthin in MGDG, DGDG and phospholipids. The violaxanthin cycle is hypothesized to be a linked system of the thylakoid and envelope for signal transduction of light stress.

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Abbreviations

A:

Antheraxanthin

Asc:

Ascorbate

DES:

De-epoxidation state calculated as A+Z/A+Z+V

DGDG:

Digalactosyldiacylglycerol

EPC:

Egg phosphatidylcholine

HPLC:

High performance liquid chromatography

MGDG:

Monogalactosyldiacylglycerol

NPQ:

Non-photochemical quenching

PDE:

Percent de-epoxidation calculated as (½A+Z/½A+Z+V)×100

PE:

Phosphatidylethanolamine

SPC:

Soy phosphatidylcholine

V:

Violaxanthin

VDE:

Violaxanthin de-epoxidase

Z:

Zeaxanthin

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Acknowledgments

This research was supported in part by United States Department of Energy Grant DE-FG03-92ER20078. The author thanks Dr. David Hieber for helpful discussions and Dr. Osamu Kawabata for technical assistance.

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Authors and Affiliations

  1. Department of Plant Molecular Biosciences and Biosystems Engineering, University of Hawai’i at Manoa, Honolulu, HI, 96922, USA

    Harry Y. Yamamoto

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Correspondence to Harry Y. Yamamoto.

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Yamamoto, H.Y. Functional roles of the major chloroplast lipids in the violaxanthin cycle. Planta 224, 719–724 (2006). https://doi.org/10.1007/s00425-006-0257-5

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