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

Abstract

Life on earth is dependent on the photosynthetic conversion of light energy into chemical energy. However, absorption of excess sunlight can damage the photosynthetic machinery and limit photosynthetic activity, thereby affecting growth and productivity. Photosynthetic light harvesting can be down-regulated by nonphotochemical quenching (NPQ). A major component of NPQ is qE (energy-dependent nonphotochemical quenching), which allows dissipation of light energy as heat. Photodamage peaks in the UV-B part of the spectrum, but whether and how UV-B induces qE are unknown. Plants are responsive to UV-B via the UVR8 photoreceptor. Here, we report in the green alga Chlamydomonas reinhardtii that UVR8 induces accumulation of specific members of the light-harvesting complex (LHC) superfamily that contribute to qE, in particular LHC Stress-Related 1 (LHCSR1) and Photosystem II Subunit S (PSBS). The capacity for qE is strongly induced by UV-B, although the patterns of qE-related proteins accumulating in response to UV-B or to high light are clearly different. The competence for qE induced by acclimation to UV-B markedly contributes to photoprotection upon subsequent exposure to high light. Our study reveals an anterograde link between photoreceptor-mediated signaling in the nucleocytosolic compartment and the photoprotective regulation of photosynthetic activity in the chloroplast.L ight is essential for photosynthesis, but absorption of excess light energy is detrimental. To avoid photodamage, photosynthetic light harvesting is regulated by nonphotochemical quenching (NPQ), which allows dissipation of harmful excess energy as heat through its qE (energy-dependent nonphotochemical quenching) component (1-6). Specialized members of the light harvesting complex (LHC) protein family, such as Photosystem II Subunit S (PSBS) in higher plants or members of the LHC Stress-Related (LHCSR) family in mosses and algae, are central to qE (7-11). Protonation of key residues in these proteins triggers qE in response to the acidification of the thylakoid lumen, which is coupled to photosynthetic electron transport (7, 9). Furthermore, the deepoxidation of violaxanthin to zeaxanthin, which is also activated by the acidification of the thylakoid lumen, enhances qE (12). 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).UV-B radiation is intrinsic to sunlight reaching the earth surface and is potentially damaging to living tissues. UV-B stress tolerance is induced through the specific activation of acclimation responses (15)(16)(17)(18)(19)(20). Plants sense UV-B radiation via the homodimeric UV-B photoreceptor UV Resistance Locus 8 (UVR8) (21-23) that is mainly localized in the cytosol ...

Bilin-Dependent Photoacclimation in Chlamydomonas reinhardtii

“…Phototropin (PHOT1) is slightly induced upon transition to the light, but no significant difference in expression of PHOT1 was seen in hmox1. Other candidate photoreceptors include UVR8 (Tilbrook et al, 2016;Allorent et al, 2016), channel rhodopsins, histidine kinase rhodopsins (HKRs), and GAF (cGMP-specific phosphodiesterases, adenylyl cyclases, and FhlA) domain-containing proteins. Although most of these genes show light-dependent changes of transcript levels, especially in the first 30 min after transition from the dark into the light, none of them appears to be affected by the absence of HMOX1.…”

UVR8‐mediated induction of flavonoid biosynthesis for UVB tolerance is conserved between the liverwort Marchantia polymorpha and flowering plants

“…The UVR8 protein sequence is strongly conserved in the plant lineage (Rizzini et al ., ; Fernández et al ., ; Soriano et al ., ), and UVR8 of the Chlorophyceae green alga Chlamydomonas reinhardtii shows conservation of action with Arabidopsis UVR8 (Allorent et al ., ; Tilbrook et al ., ). Recently, Soriano et al .…”

Light‐dependent N‐terminal phosphorylation of LHCSR3 and LHCB4 are interlinked in Chlamydomonas reinhardtii

“…However, its exact role in the qE mechanism of the alga remains elusive. Interestingly, expression of PSBS and LHCSR1 is controlled through UV‐B perception via UVR8 (Allorent et al ., ; Tilbrook et al ., ). LHCSR3 expression, conversely, is controlled through blue‐light perception via phototropin (Petroutsos et al ., ), calcium, the chloroplast CAS protein and photosynthetic electron transfer (Petroutsos et al ., ; Maruyama et al ., ).…”