**2.3.2 D1 repair cycle**

162 Artificial Photosynthesis

secondary metabolism in plants. Thus, the LTR appears to contribute also to the adaptation

All evidence gathered to data indicates that short- and long-term photosynthetic acclimation responses are triggered by changes in the redox state of the PQ pool and require the modulated activity of the kinase STN7. Due to its dual regulatory role, STN7 initiates a phosphorylation cascade that induces state transitions by phosphorylating LHCII and promotes the LTR process via the phosphorylation of as yet unknown chloroplast proteins. Beyond this point, the LTR signaling pathway is divided into two main branches: one is responsible for transcriptional regulation of chloroplast gene expression, while the other controls the expression of nuclear photosynthesis-related genes at transcriptional and post-

State transitions and LTR are acclimation responses that typically occur under low-light conditions and are controlled via redox signals. Under conditions resulting in high or excess excitation pressure other acclimation responses are activated, such as non-photochemical dependent antenna quenching, the D1 repair cycle or various other stress-response programs. These responses are also controlled via redox signals originating from the photosynthetic process (i.e. the PQ redox state and signals from the PSI acceptor side), but may also involve the participation of ROS such as hydrogen peroxide (H2O2) or singlet

Non-photochemical quenching (NPQ) is a rapid de-excitation photo-protective quenching mechanism (qE) that involves dissipation of excess energy occurring upon short-term high light exposure. In addition, NPQ is considered to act as a ''light intensity counter,'' providing the photosynthetic membrane with a ''memory'' of the light-exposure history of the leaf (Horton et al., 2008; Foyer & Noctor, 2009). qE is induced by a low thylakoid lumen pH (i.e. a high ΔpH) generated by photosynthetic electron transport in excess light and involves the harmless thermal dissipation of excess energy in the chlorophyll (Chl) singlet excited states (1Chl\*) in photosystem II (PSII) of green plants and algae. qE is designed to minimize alternative reaction pathways that generate toxic photo-oxidative intermediates. It functions by activating a lumen-localized violaxanthin de-epoxidase enzyme that catalyses the conversion of violaxanthin to zeaxanthin via the intermediate antheraxanthin, in what is known as the xanthophyll cycle (which is completed by the conversion of zeaxanthin back to violaxanthin by means of a zeaxanthin epoxidase activated under limiting light conditions). The process also requires the protonation of PsbS, a PSII subunit that plays a role in the regulation of photosynthetic light harvesting and is also necessary for qE *in vivo*  (possibly by establishing a binding site for zeaxanthin that facilitates the de-excitation of singlet excited chlorophyll via energy or electron transfer). Experimental evidence has shown that energy transfer from chlorophyll molecules to a chlorophyll-zeaxanthin heterodimer that undergoes charge separation is the main mechanism for excess energy dissipation during feedback de-excitation (Horton et al., 1999; Külheim et al., 2002; Niyogi et al., 2005; Holt et al., 2004, 2005). However, quenching of excess energy can also occur independently of zeaxanthin via a reversible inactivation of a fraction of photosystem II

of plant primary productivity to environmental conditions (Pesaresi et al., 2010).

transcriptional levels (see Figure 1) (Pesaresi et al., 2010).

oxygen (Pfannschmidt et al., 2009).

**2.3.1 Non-photochemical quenching** 

**2.3 Acclimation responses under high or excess excitation pressure**

In addition to the D1 and D2 proteins that conform its core reaction center, PSII contains *α* and *β* subunits of cytochrome *b*559, the *psb*I gene product and a few low molecular weight polypeptides. The D1-D2 heterodimer within PSII binds all the electron carriers and cofactors necessary for electron transport (Nanba & Satoh, 1987; Mattoo et al., 1989). The reaction center protein D1 of PSII is also the primary target of photo-inhibition (Mattoo et al., 1984; Prasil et al., 1992). Due to its intrinsic vulnerability, the short-lived D1 protein must be constantly replaced by new copies via a complicated and evolutionary conserved process known as the PSII or D1 repair cycle, whose significance remains elusive (Mattoo et al., 1989; Andersson & Aro, 2001; Baena-Gonzales & Aro, 2002; Yokthongwattana & Melis, 2006; Edelman & Mattoo, 2008). Nevertheless, the process has an undoubted physiological importance considering that an accumulation of photo-inactivated PSII centers, leading to a decreased photochemical efficiency and the consequent photo-damage, occurs whenever its repair capacity is surpassed (Melis, 1999; Andersson & Aro, 2001).

D1 is a target of at least five post-translational modifications during its life cycle, including N-acetylation, palmitoylation and phosphorylation (Edelman & Mattoo, 2008). One or more of these post-translational modifications could potentially alter protein degradation kinetics, although the use of nitric oxide donors to inhibit *in vivo* phosphorylation of the D1 protein suggested that redox-dependent phosphorylation and D1 degradation in plants are not linked events (Booij-James et al., 2009). The DegP and FtsH proteases have been shown to be involved in D1 degradation *in vitro* (Haussuhl et al., 2001; Kanervo et al., 2003; Lindahl et al., 2000). The physiological significance of these specific proteases was demonstrated in the Arabidopsis *var2* (for *yellow variegated2*) or *var1* mutants, lacking the FtsH2 or FtsH5 membrane-bound metalloproteases, respectively, and the *fu-gaeri1* (*fug1*) mutant that suppresses interfering leaf variegation in *var1* and *var2*, all of which led to an inefficient degradation of the D1 protein and a concomitant increase in ROS levels that was connected to an enhanced susceptibility to photoinhibition (Bailey et al., 2002; Kato et al., 2009). Similar results were reported in cyanobacteria, where impaired D1 protein turnover was detected in an FtsH inactivation mutant (Silva et al., 2003). Moreover, experiments in which an increased transcription of two FtsH-coding genes and of FtsH protease activity was found to be induced upon transfer of cyanobacteria to high light, demonstrated that FtsH proteolysis is a light regulated process (Hihara et al., 2001; Singh et al., 2005).
