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http://dx.doi.org/10.5772/62261

#### **Abstract**

Plants and algae are subjected to changes in light quality and quantity and in nutrient availability in their natural habitat. To adapt to these changing environmental condi‐ tions, these organisms have developed efficient means to adjust their photosynthetic apparatus so as to preserve photosynthetic efficiency and appropriate photoprotection. Under limiting light, this system optimizes light capture and photosynthetic yield through a reorganization of its light-harvesting system. In contrast, under high light, when the absorption capacity of the system is exceeded, the excess absorbed light energy is dissipated as heat to prevent oxidative damage. One of the key photosynthetic complexes, photosystem II, is prone to photodamage but is efficiently repaired. The photosynthetic machinery is also able to adjust when specific micronutrients such as copper, iron or sulfur become limiting by remodeling some of the photosynthetic complexes and metabolic pathways. While some of these responses occur in the short term, others occur in the long term and involve an intricate signaling system within chloroplasts and between the chloroplast and the nucleus accompanied with changes in gene expression. These signals involve the tetrapyrrole pathway, plastid protein synthesis, the redox state of the photosynthetic electron transport chain, reactive oxygen species and several metabolites.

**Keywords:** photosynthesis, thylakoid membrane, acclimation, retrograde signaling, *Chlamydomonas*

#### **1. Introduction**

Photosynthetic organisms are constantly subjected to changes in light quality and quantity and have to adapt to this changing environment. On the one hand they need light energy and have to collect it efficiently especially when light is limiting; on the other hand, they have to be able to dissipate the excess absorbed light energy when the capacity of the photosynthetic appara‐ tus is exceeded. The primary events of photosynthesis occur in the thylakoids, a complex network

© 2016 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

of membranes localized within chloroplasts. These primary reactions are mediated by three major protein–pigment complexes, photosystem II (PSII), the cytochrome *b*6*f* complex (Cyt*b*6*f*) and photosystem I (PSI) embedded in the thylakoid membrane and which act in series. Both PSII and PSI are associated with their light-harvesting complex systems, LHCII and LHCI, respectively, which collect and transfer the light excitation energy to the reaction centers of the two photosystems. In both cases, a chlorophyll dimer is oxidized and a charge transfer occurs across the thylakoid membrane. PSII creates thereby a strong oxidant capable of splitting water on its donor side with concomitant evolution of molecular oxygen and the release of protons in the lumensidewhile electrons are transferredalong thephotosynthetic electrontransport chain throughPSIItotheplastoquinonepoolandCyt*b*6*f.*Thiscomplexpumpsprotonsfromthestromal to the lumen side of the thylakoid membrane while transferring electrons to plastocyanin and PSI. Ultimately the electrons are transferred to ferredoxin and NADP(H), the final acceptor. A fourth complex, the ATP synthase, is functionally linked to the other three by using the proton gradient generated by the photosynthetic electron flow across the thylakoid membrane to produce ATP (**Figure 1**). Both ATP and NADPH fuel the Calvin–Benson cycle (CBC) for CO2 assimilation. Besides linear electron flow (LEF), cyclic electron flow (CEF) occurs in which electrons are transferred from the PSI acceptor ferredoxin to the plastoquinone pool through eitheratypeI/IIthylakoid-boundNADHdehydrogenase[1]ortheantimycin-sensitivepathway involving Pgr5 and Pgrl1 [2,3]. Analysis of a *pgr5* mutant of *Chlamydomonas* revealed that the loss of Pgr5 leads to a reduced proton gradient across the thylakoid membrane and to dimin‐ ished CEF activity [4]. Pgrl1 has been proposed to act as a ferredoxin–plastoquinone reduc‐ tase [3]. In contrast to linear electron flow, which generates both reducing power and ATP, CEF produces exclusively ATP. The NADPH/ATP ratio can thus be modulated through regulation of CEF versus LEF.

**Figure 1.** Scheme of the photosynthetic electron transport chain with PSII, Cyt*b*6*f*, PSI and ATP synthase.

Linear electron flow (LEF) and cyclic electron flow (CEF) are shown in red and blue, respec‐ tively, with arrows indicating the direction of electron flow. The LEF pathway is driven by the two photochemical reactions of PSII and PSI: electrons are extracted by PSII from water and transferred subsequently to the PQ pool, Cyt*b*6*f*, plastocyanin (Pc), PSI and ferredoxin (Fd). Ferredoxin–NADPH reductase (Fnr) catalyzes the formation of NADPH at the expense of reduced Fd. The CEF pathway is driven by PSI in the stroma lamellae. In *C. reinhardtii*, PSI forms a supercomplex with Cyt*b*6*f*, Fnr, Pgrl1, Pgr5 and additional factors. Upon reduction of Fd, electrons are returned to the PQ pool either through the NADH complex (Ndh) or via Pgrl1 which acts as a Fd-PQ oxidoreductase. Both LEF and CEF are associated with proton pumping into the lumen. The resulting proton gradient is used by ATP synthase to produce ATP which together with NADPH drives CO2 assimilation by the Calvin–Benson cycle (CBC). G, grana; SL, stroma lamellae. Reproduced from Ref. 5 with permission.

of membranes localized within chloroplasts. These primary reactions are mediated by three major protein–pigment complexes, photosystem II (PSII), the cytochrome *b*6*f* complex (Cyt*b*6*f*) and photosystem I (PSI) embedded in the thylakoid membrane and which act in series. Both PSII and PSI are associated with their light-harvesting complex systems, LHCII and LHCI, respectively, which collect and transfer the light excitation energy to the reaction centers of the two photosystems. In both cases, a chlorophyll dimer is oxidized and a charge transfer occurs across the thylakoid membrane. PSII creates thereby a strong oxidant capable of splitting water on its donor side with concomitant evolution of molecular oxygen and the release of protons in the lumensidewhile electrons are transferredalong thephotosynthetic electrontransport chain throughPSIItotheplastoquinonepoolandCyt*b*6*f.*Thiscomplexpumpsprotonsfromthestromal to the lumen side of the thylakoid membrane while transferring electrons to plastocyanin and PSI. Ultimately the electrons are transferred to ferredoxin and NADP(H), the final acceptor. A fourth complex, the ATP synthase, is functionally linked to the other three by using the proton gradient generated by the photosynthetic electron flow across the thylakoid membrane to produce ATP (**Figure 1**). Both ATP and NADPH fuel the Calvin–Benson cycle (CBC) for CO2 assimilation. Besides linear electron flow (LEF), cyclic electron flow (CEF) occurs in which electrons are transferred from the PSI acceptor ferredoxin to the plastoquinone pool through eitheratypeI/IIthylakoid-boundNADHdehydrogenase[1]ortheantimycin-sensitivepathway involving Pgr5 and Pgrl1 [2,3]. Analysis of a *pgr5* mutant of *Chlamydomonas* revealed that the loss of Pgr5 leads to a reduced proton gradient across the thylakoid membrane and to dimin‐ ished CEF activity [4]. Pgrl1 has been proposed to act as a ferredoxin–plastoquinone reduc‐ tase [3]. In contrast to linear electron flow, which generates both reducing power and ATP, CEF produces exclusively ATP. The NADPH/ATP ratio can thus be modulated through regulation

**Figure 1.** Scheme of the photosynthetic electron transport chain with PSII, Cyt*b*6*f*, PSI and ATP synthase.

Linear electron flow (LEF) and cyclic electron flow (CEF) are shown in red and blue, respec‐ tively, with arrows indicating the direction of electron flow. The LEF pathway is driven by the

of CEF versus LEF.

24 Applied Photosynthesis - New Progress

A striking feature of the thylakoid membrane is its lateral heterogeneity with two distinct domains consisting of appressed membranes, called grana, and stromal lamellae, which connect the grana regions with each other [6,7]. Whereas PSII is mainly localized in the grana regions, PSI and the ATP synthase are found in the stromal lamellae and in the margins of the grana [8]. This is because these two complexes have large domains protruding in the stromal phase which do not fit into the narrow membrane space between the grana lamellae. The organization of thylakoid membranes in the grana and stromal regions is determined to a large extent by the resident photosystem complexes. As an example, mutants deficient in PSI contain mostly grana with few stromal lamellae [9,10]. In contrast to the photosystems, the Cyt*b*6*f* complex is equally distributed between the grana and stromal thylakoid regions. Grana formation appears to be mediated by van der Waals attractive forces and electrostatic inter‐ actions in which LHCII plays an important role [11].

The LHCII and LHCI genes form a large family with each member encoding a protein with three transmembrane domains and up to eight chlorophyll *a*, six chlorophyll *b* and four xanthophyll molecules. In *Chlamydomonas*, there are nine major and three minor LHCII and nine LHCI genes [12]. The LHCII antenna comprises LHCII trimers connected to the PSII core through the CP26 and CP29 LHCII monomers. The LHCII trimers bind PSII at three sites named S (strong), M (medium) and L (loose). In vivo, PSII assembles as dimers associated with two S and M LHCII trimers to form the C2S2M2 PSII-LHCII supercomplex in land plants [8]. Supercomplexes with one to three LHCII trimers per monomeric PSII core have also been detected in *Chlamydomonas* [13–15]. In eukaryotic algae the PSI complex is monomeric with a core consisting of the PsaA/PsaB heterodimer and additional subunits as well as up to 9 LHCI proteins in *Chlamydomonas.* It is noticeable that in contrast to the conserved core photosynthetic complexes, the antenna systems are considerably more diverse with hydrophobic membraneembedded LHCs in plants, green and red algae and extrinsic hydrophilic phycobilisomes in red algae and cyanobacteria. Moreover, in most green algae, thylakoid membranes are not differentiated in the grana and stroma regions [16].

The aim of this chapter is to provide a description of the remarkable dynamics and flexibility of the photosynthetic apparatus of algae in response to changes in environmental conditions and to compare these responses with those of land plants. They include changes in light quality and quantity and in nutrient availability. These responses involve a reorganization of some of the photosynthetic complexes often mediated by posttranslational modifications of their subunits through an extensive signaling network in chloroplasts and between chloroplasts and nucleus which modulates nuclear and plastid gene expression.
