Structural changes of the thylakoid membrane network induced by high light stress in plant chloroplasts

Abstract

Land plants live in a challenging environment dominated by unpredictable changes. A particular problem is fluctuation in sunlight intensity that can cause irreversible damage of components of the photosynthetic apparatus in thylakoid membranes under high light conditions. Although a battery of photoprotective mechanisms minimize damage, photoinhibition of the photosystem II (PSII) complex occurs. Plants have evolved a multi-step PSII repair cycle that allows efficient recovery from photooxidative PSII damage. An important feature of the repair cycle is its subcompartmentalization to stacked grana thylakoids and unstacked thylakoid regions. Thus, understanding the crosstalk between stacked and unstacked thylakoid membranes is essential to understand the PSII repair cycle. This review summarizes recent progress in our understanding of high-light-induced structural changes of the thylakoid membrane system and correlates these changes to the efficiency of the PSII repair cycle. The role of reversible protein phosphorylation for structural alterations is discussed. It turns out that dynamic changes in thylakoid membrane architecture triggered by high light exposure are central for efficient repair of PSII.

Keywords: PSII core phosphatase; STN8; photoinhibition; photosynthesis; photosystem II repair; thylakoid membrane.

Figure 1.

PSII repair cycle. The repair cycle is subcompartmentalized to stacked and unstacked thylakoid regions. After high light induces photodamage mainly to the D1 subunit of PSII (1), the holocomplex is phosphorylated by STN8 kinase (2). The phosphorylation triggers monomerization and detachment of LHCII from the PSII core (3) followed by lateral migration from stacked thylakoids to unstacked regions (4). Before the damaged D1 subunit is degraded by FtsH and Deg proteases (6), the PSII core is dephosphorylated by PBCP phosphatase (5). However, it is under debate whether dephosphorylation is required for D1 degradation. A new synthesized D1 copy is inserted in the PSII core (7). Before D1 is inserted, the precursor D1 protein (pD1) is processed by CtpA (7). Finally, the PSII holocomplex reassembles and migrates back to stacked grana (8). (Online version in colour.)

Figure 2.

Structural model of the thylakoid membrane and components involved in PSII repair. The model represents the structural relationship between thylakoid membrane features and the sizes of proteins. The sizes and contours of the Deg and FtsH proteases were adapted from [50,51]. For PBCP, STN8 and CtpA, the sizes were calculated from their relative molecular mass (RMM). The RMM of a protein is proportional to its volume. Assuming a spherical protein contour, the relative change in diameter for protein 1 (d_protein1) to protein 2 (d_protein2) can be derived from RMM by solving the following equation for d_protein1: d_protein1/d_protein2 = (RMM_protein1)^1/3/(RMM_protein2)^1/3. The absolute diameter for protein 1 can be calculated if the relationship between d and RMM is known for a reference protein (protein 2). PC was selected as a reference protein. Its RMM is 10.5 kDa and its dimensions are 3 × 3 × 4 nm [52]. For the calculations, a mean diameter of 3.5 nm was used. Based on this number, the diameters of PBCP, STN8 and CtpA were calculated: PBCP: 32 kDa [40] ≥ approximately 5.1 nm; STN8 kinase; 56 kDa, extrinsic part 40.5 kDa ≥ approximately 5.5 nm; CtpA, 43 kDa [44] ≥ approximately 5.6 nm. (Online version in colour.)