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Review
. 2016 Aug 2:7:1136.
doi: 10.3389/fpls.2016.01136. eCollection 2016.

Quality Control of Photosystem II: The Mechanisms for Avoidance and Tolerance of Light and Heat Stresses are Closely Linked to Membrane Fluidity of the Thylakoids

Yasusi Yamamoto  1
Affiliations
Review

Quality Control of Photosystem II: The Mechanisms for Avoidance and Tolerance of Light and Heat Stresses are Closely Linked to Membrane Fluidity of the Thylakoids

Yasusi Yamamoto. Front Plant Sci. .

Abstract

When oxygenic photosynthetic organisms are exposed to excessive light and/or heat, Photosystem II is damaged and electron transport is blocked. In these events, reactive oxygen species, endogenous radicals and lipid peroxidation products generated by photochemical reaction and/or heat cause the damage. Regarding light stress, plants first dissipate excessive light energy captured by light-harvesting chlorophyll protein complexes as heat to avoid the hazards, but once light stress is unavoidable, they tolerate the stress by concentrating damage in a particular protein in photosystem II, i.e., the reaction-center binding D1 protein of Photosystem II. The damaged D1 is removed by specific proteases and replaced with a new copy produced through de novo synthesis (reversible photoinhibition). When light intensity becomes extremely high, irreversible aggregation of D1 occurs and thereby D1 turnover is prevented. Once the aggregated products accumulate in Photosystem II complexes, removal of them by proteases is difficult, and irreversible inhibition of Photosystem II takes place (irreversible photoinhibition). Important is that various aspects of both the reversible and irreversible photoinhibition are highly dependent on the membrane fluidity of the thylakoids. Heat stress-induced inactivation of photosystem II is an irreversible process, which may be also affected by the fluidity of the thylakoid membranes. Here I describe why the membrane fluidity is a key to regulate the avoidance and tolerance of Photosystem II on environmental stresses.

Keywords: D1 protein; heat stress; light stress; lipid peroxidation; membrane fluidity; photosystem II; protein aggregation; thylakoid.

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Figures

FIGURE 1
FIGURE 1
Light response curve for PSII activity and the events that occur in the thylakoids when the thylakoids avoid and tolerate light stress. Under low light, PSII activity increases with increasing light intensity. Under high light conditions, chloroplasts first try to avoid the light stress by dissipating the excessive light energy as heat (qE of NPQ). However, when the light intensity increases, photoinhibition of PSII becomes apparent. Irreversible aggregation of PSII proteins occurs under severe light stress conditions, which induces irreversible photoinhibition of PSII.
FIGURE 2
FIGURE 2
A schematic representation of the major photoinhibition mechanisms of PSII. (A) A normal electron transport pathway from water to plastoquinone in PSII. (B) The acceptor-side photoinhibition mechanism of PSII. (C) The donor-side photoinhibition mechanism of PSII. For details, see the text.
FIGURE 3
FIGURE 3
Shematic models showing reversible and irreversible photoinhibition of PSII. Reversible photoinhibition (A) occurs when thylakoids are irradiated with moderate high light, while irreversible photoinhibition (B) occurs when the illumination is extremely strong. In (A), PSII/LHCII complexes are redistributed on the membrane under high light and the photodamaged D1 is removed by FtsH protease and other proteases. Free spaces with high membrane fluidity may be produced at the grana regions to assist the movement of the protein complexes and proteases to remove the damaged D1. PSII activity recovers after the repair of PSII in the dark. By contrast, in (B) excessive production of ROS such as 1O2 through photochemistry of PSII and lipid peroxidation oxidatively damage various proteins and lipids and cause irreversible cross-linking of proteins and lipids. The overall membrane fluidity may decrease and movement of protein components may be hindered significantly. Under these conditions, PSII function and turnover are inhibited completely, and eventually cell death will be brought about.
FIGURE 4
FIGURE 4
Photo-and heat-induced damage to PSII and removal of the damaged D1 by FtsH proteases. To simplify the model, only the PSII complexes and FtsH proteases are shown. For details, see the text.
FIGURE 5
FIGURE 5
A schematic diagram of light- or heat-induced unstacking of the thylakoids and swelling of thylakoid lumen. Light green particles in the grana represent PSII/LHCII complexes. Dark blue particles represent FtsH proteases, which recognize the damaged PSII complexes at the grana margins, stroma thylakoids and grana end membranes, and carry out degradation of the damaged D1. Purple, light green and light blue particles represent ATP synthase, PSI complex, and cytochrome b6/f complex, respectively. Because the exact protein packing densities in each membrane compartment such as stroma thylakoids, grana, and grana margins are not known yet, the diagram shows only a simplified image in regard to the distribution of protein complexes.
FIGURE 6
FIGURE 6
A flow chart showing the photoinhibition of PSII under high light and heat-inactivation of PSII under high temperature. Under the light stress and heat stress, ROS are produced at PSII or in the thylakoid membranes, which cause oxidative damage to PSII directly or through lipid peroxidation. Severe damages may be manifested as protein–protein, protein-lipid, and lipid–lipid cross-linking and they affect the total and local membrane fluidity of the thylakoids. Hindrance of efficient movement of the proteins in the thylakoids may results in dysfunction of the chloroplasts and finally cell death.
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