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Carotenogenic response in photosynthetic organisms: a colorful story

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Abstract

Carotenoids are a diverse group of terpenoid pigments ubiquitous in and essential for functioning of phototrophs. Most of the researchers in the field are focused on the primary carotenoids serving light harvesting, photoprotection, and supporting the structural integrity of the photosynthetic apparatus (PSA) within the thylakoid membranes. A distinct group of the pigments functionally and structurally uncoupled from the PSA and accumulating outside of the thylakoids is called secondary carotenoids. Induction of the biosynthesis and massive accumulation of the latter termed as secondary carotenogenesis and carotenogenic response (CR), respectively, is a major though insufficiently studied stress response discovered in many phototrophic organisms ranging from single-celled algae to terrestrial higher plants. The CR protects cell by means of optical shielding of cell structures vulnerable photodamage, consumption of potentially harmful dioxygen, augmenting sink capacity of photoassimilates, and exerting an antioxidant effect. The secondary carotenoids exhibit a remarkable photostability in situ. Therefore, the CR-based photoprotective mechanism, unlike, e.g., antioxidant enzyme-based protection in the chloroplast, does not require continuous investment of energy and metabolites making it highly suitable for long-term stress acclimation in phototrophs. Capability of the CR determines the strategy of acclimation of photosynthetic organisms to different stresses such as excessive irradiance, drought, extreme temperatures, and salinities. Build-up of the CR might be accompanied by gradual disengagement of ‘classical’ active (energy-dependent) photoprotective mechanisms such as non-photochemical quenching. In addition to that, the CR has great ecological significance. Illustrious examples of this are extremely stress-tolerant ‘snow’ algae and conifer species developing red coloration during winter. The CR has also considerable practical implications since the secondary carotenoids exert a plethora of beneficial effects on human and animal health. The carotenogenic microalgae are the richest biotechnological sources of natural value-added carotenoids such as astaxanthin and β-carotene. In the present review, we summarize current functional, mechanistic, and ecological insights into the CR in a broad range of organisms suggesting that it is obviously more widespread and important stress response than it is currently thought to be.

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Adapted from (Grunewald et al. 2001; Lemoine and Schoefs 2010)

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Acknowledgements

Critical reading of the manuscript by Prof. Inna Khozin-Goldberg is gratefully appreciated.

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This study was funded by Russian Scientific Foundation (Project 14-50-00029).

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Solovchenko, A., Neverov, K. Carotenogenic response in photosynthetic organisms: a colorful story. Photosynth Res 133, 31–47 (2017). https://doi.org/10.1007/s11120-017-0358-y

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