A blue-light photoreceptor mediates the feedback regulation of photosynthesis

• Published in: Nature (London) Vol. 537; no. 7621; pp. 563 - 566
• Main Authors: Petroutsos, Dimitris, Tokutsu, Ryutaro, Maruyama, Shinichiro, Flori, Serena, Greiner, Andre, Magneschi, Leonardo, Cusant, Loic, Kottke, Tilman, Mittag, Maria, Hegemann, Peter, Finazzi, Giovanni, Minagawa, Jun
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 22.09.2016; Nature Publishing Group
• Subjects: 38; 38/1; 631/208/200; 631/449/1734/2687; 631/80/86; 82; 96; Acclimatization; Acclimatization - radiation effects; Algae; Apoptosis; Aquatic plants; Biochemistry, Molecular Biology; Carbon dioxide; Carotenoids; Cell Survival; Cell Survival - radiation effects; Chlamydomonas reinhardtii; Chlamydomonas reinhardtii - genetics; Chlamydomonas reinhardtii - metabolism; Chlamydomonas reinhardtii - radiation effects; Chloroplasts; Color; Cyanobacteria; Energy sources; Feedback, Physiological; Feedback, Physiological - radiation effects; Humanities and Social Sciences; Kinases; letter; Life Sciences; Light; Light intensity; Light Signal Transduction; Light Signal Transduction - radiation effects; Light-Harvesting Protein Complexes; Light-Harvesting Protein Complexes - biosynthesis; Light-Harvesting Protein Complexes - metabolism; multidisciplinary; Photoreception; Photoreceptors; Photosynthesis; Photosynthesis - radiation effects; Photosynthesis research; Photosystem II Protein Complex; Photosystem II Protein Complex - metabolism; Phototropins; Phototropins - chemistry; Phototropins - genetics; Phototropins - metabolism; Physiological aspects; Physiological regulation; Protein Kinases; Protein Kinases - chemistry; Protein Kinases - metabolism; Proteins; Science; Light acclimation; Photoprotection; Algae; Photoreceptor
• ISSN: 0028-0836; 1476-4687; 1476-4687
• DOI: 10.1038/nature19358

Algae rely on blue-light-sensitive phototropin to trigger induction of LHCRS3, allowing it to dissipate energy from excess light that would otherwise compromise the fitness of the organism. Phototropin mediates photosynthesis regulation Excessive light can overwhelm the photosynthetic system of plants and algae, leading to damage or even cell death. Consequently, plants have evolved systems to prevent such overload. Giovanni Finazzi and colleagues demonstrate that, in the green alga Chlamydomonas reinhardtii , the blue-light photoreceptor phototropin (PHOT) induces the expression of light-harvesting complex stress-related protein 3 (LHCSR3) when light levels are sufficiently high. This causes the dissipation of excess light from photosystem II. In the absence of PHOT activity, the fitness of the algae is severely compromised. In plants and algae, light serves both as the energy source for photosynthesis and a biological signal that triggers cellular responses via specific sensory photoreceptors. Red light is perceived by bilin-containing phytochromes and blue light by the flavin-containing cryptochromes and/or phototropins (PHOTs) 1 , the latter containing two photosensory light, oxygen, or voltage (LOV) domains 2 . Photoperception spans several orders of light intensity 3 , ranging from far below the threshold for photosynthesis to values beyond the capacity of photosynthetic CO 2 assimilation. Excess light may cause oxidative damage and cell death, processes prevented by enhanced thermal dissipation via high-energy quenching (qE), a key photoprotective response 4 . Here we show the existence of a molecular link between photoreception, photosynthesis, and photoprotection in the green alga Chlamydomonas reinhardtii. We show that PHOT controls qE by inducing the expression of the qE effector protein LHCSR3 (light-harvesting complex stress-related protein 3) in high light intensities. This control requires blue-light perception by LOV domains on PHOT, LHCSR3 induction through PHOT kinase, and light dissipation in photosystem II via LHCSR3. Mutants deficient in the PHOT gene display severely reduced fitness under excessive light conditions, indicating that the sensing, utilization, and dissipation of light is a concerted process that plays a vital role in microalgal acclimation to environments of variable light intensities.