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Article Dans Une Revue Trends in Plant Science Année : 2020

Changing Color for Photoprotection: The Orange Carotenoid Protein

Résumé

Under high irradiance, light becomes dangerous for photosynthetic organisms and they must protect themselves. Cyanobacteria have developed a simple mechanism, involving a photoactive soluble carotenoid protein, the orange carotenoid protein (OCP), which increases thermal dissi-pation of excess energy by interacting with the cyanobacterial antenna, the phycobilisome. Here, we summarize our knowledge of the OCP-related photoprotective mechanism, including the remarkable progress that has been achieved in recent years on OCP photoactivation and interaction with phycobilisomes, as well as with the fluorescence recovery protein, which is necessary to end photoprotection. A recently discovered unique mechanism of carotenoid transfer between soluble proteins related to OCP is also described. The Orange Carotenoid Protein (OCP) and Photoprotection Living organisms need to constantly sense environmental changes and adapt to them for survival. For photosynthetic organisms, it is crucial to sense changes in the light intensity and rapidly respond to them. These organisms are able to modify their photosynthetic apparatus to efficiently harvest light under fluctuating light conditions, which rapidly change from subsaturating to oversaturating light intensities. At the same time, photosynthetic organisms must avoid photodamage, generated by an excess of energy reaching photochemical reactions centers. Indeed, light becomes dangerous when the entire photosynthetic electron transport chain becomes over-reduced and reactive oxygen species are formed, leading to severe cell damage. Thus, the survival and growth of photosynthetic organisms strongly depend on the balance between an efficient collection of light energy to sustain photosynthesis and protection against its photo-oxidizing effects. Plants, algae, and cyanobacteria have developed a photoprotective mechanism through which a normally highly efficient light-harvesting antenna is reversibly switched into a photoprotective, 'dark' state. In this state, potentially harmful absorbed energy is dissipated as heat, decreasing the energy reaching photochemical reaction centers. This increase in thermal energy dissipation is accompanied by a significant non-photo-chemical quenching (NPQ) of chlorophyll (phycobiliproteins) fluorescence. This mechanism differs in cyanobacteria from those existing in plants and algae, owing to the special cyanobacterial antenna, the phycobilisome (PBS; Figure 1). In cyanobacteria, a water-soluble photoactive carotenoid protein, the orange carotenoid protein (OCP), senses light intensity and induces thermal dissipation of excess excitation energy by interacting with PBS (see previous reviews [1-4]). The existence of the cyanobac-terial OCP was reported in 1981 [5], but its function in cyanobacterial photoprotective thermal energy dissipation was only elucidated in 2006 [6]. Moreover, although it was first isolated in the late 1990s [7] and its tridimensional structure was described in 2003 [8], the photoactivity of OCP was only discovered in 2008 [9]. OCP has a second role in photoprotection as a very good quencher of singlet oxygen [8,10]. Large progress in the understanding of the OCP photocycle and interactions with its partners has been made in the past 5 years. OCP-coding genes are present in a large number of PBS-containing cyanobacteria; however, one-third of sequenced strains have no ocp genes [11-14]. For example, Synechococcus elongatus and Thermosynechococcus elongatus, which are largely used as model organisms, lack ocp-like genes. OCP is completely absent in PBS-lacking cyanobacteria (alpha clade, including Prochlorococcus mar-inus strains) and in red algae, which are eukaryotic PBS-containing algae. There exist at least three paralog families of OCP, namely, OCP1, OCP2, and OCPX [11,12,15]. Most OCPs (approximately 65% of available sequences) belong to the OCP1 family, to which the well-characterized Synechocys-tis PCC 6803, Arthrospira maxima, and Anabaena PCC 7120 OCPs belong [11,12,15]. Only one OCP2 (Tolypothrix sp. PCC 7601) and one OCPX (Scytonema hofmanni PCC 7110) have been characterized
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hal-02569937 , version 1 (10-11-2020)

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Fernando Muzzopappa, Diana Kirilovsky. Changing Color for Photoprotection: The Orange Carotenoid Protein. Trends in Plant Science, 2020, 25 (1), pp.92-104. ⟨10.1016/j.tplants.2019.09.013⟩. ⟨hal-02569937⟩
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