A blue-light photoreceptor mediates the feedback regulation of photosynthesis

Abstract

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), the latter containing two photosensory light, oxygen, or voltage (LOV) domains. Photoperception spans several orders of light intensity, ranging from far below the threshold for photosynthesis to values beyond the capacity of photosynthetic CO 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. 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.

UV-B photoreceptor-mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii

“…We now demonstrate that the photoreceptor UVR8 and its partner COP1 initiate a signaling pathway under UV-B that induces nuclear gene expression of proteins that are then targeted to the chloroplast, where they are involved in the regulation of photosynthesis. Our findings, together with the recent description of a complementary role for PHOT in high-light activation of LHCSR3 expression (14), add a tier of regulation through anterograde signaling to the better-known feedback mechanisms operating within the chloroplast. In Arabidopsis, photoperception of UV-B by UVR8 is also important for the maintenance of photosynthetic competence, but the underlying mechanism in higher plants is not clear (35).…”

“…In response to high levels of visible light, LHCSR3 protein accumulation is of major importance for qE capacity in Chlamydomonas reinhardtii (11). The induction of LHCSR3 expression under high light is thought to involve retrograde signaling, from the chloroplast to nuclear gene expression (13), and recent data show that the response is also dependent on the phototropin (PHOT) blue light photoreceptor (14).…”

Bilin-Dependent Photoacclimation in Chlamydomonas reinhardtii

“…The lack of HMOX1 dependence on light-regulated accumulation of LHSCR3 ( Figure 3C) is also inconsistent with a role for PHOT1 in the bilin-dependent blue light response (Petroutsos et al, 2016). Blue-light-absorbing phytochromes and cyanobacteriochromes that use PCB as chromophores are well known (Rockwell et al, 2011(Rockwell et al, , 2014.…”

“…Among the genes associated with light sensing in Chlamydomonas, cryptochromes and phototropin appear to be obvious candidates to play roles in blue-light-dependent regulatory mechanisms (Huang et al, 2002;Zorin et al, 2009;Ahmad, 2016;Petroutsos et al, 2016;Duanmu et al, 2017Zou et al, 2017). Among the five genes encoding cryptochrome (CRY) photoreceptors (for a recent review on algal CRYs, see Duanmu et al, 2017;Kottke et al, 2017), expression levels for the gene encoding plant CRY (pCRY) are highest, peak in the dark, and are rapidly repressed upon the onset of light.…”

Shining Light on the Function of NPH3/RPT2-Like Proteins in Phototropin Signaling

“…More recently, C. reinhardtii phot was shown to be pivotal for modulating the abundance of key molecular effectors required for photoprotection of the photosynthetic machinery. As a result, the photdeficient mutants of C. reinhardtii displays reduced fitness under excessive light conditions (Petroutsos et al, 2016).…”