Light-independent regulation of algal photoprotection by CO2 availability

Abstract

Photosynthetic algae have evolved mechanisms to cope with suboptimal light and CO2 conditions. When light energy exceeds CO2 fixation capacity, Chlamydomonas reinhardtii activates photoprotection, mediated by LHCSR1/3 and PSBS, and the CO2 Concentrating Mechanism (CCM). How light and CO2 signals converge to regulate these processes remains unclear. Here, we show that excess light activates photoprotection- and CCM-related genes by altering intracellular CO2 concentrations and that depletion of CO2 drives these responses, even in total darkness. High CO2 levels, derived from respiration or impaired photosynthetic fixation, repress LHCSR3/CCM genes while stabilizing the LHCSR1 protein. Finally, we show that the CCM regulator CIA5 also regulates photoprotection, controlling LHCSR3 and PSBS transcript accumulation while inhibiting LHCSR1 protein accumulation. This work has allowed us to dissect the effect of CO2 and light on CCM and photoprotection, demonstrating that light often indirectly affects these processes by impacting intracellular CO2 levels.

Widening the landscape of transcriptional regulation of green algal photoprotection

“…NPQ encompasses several processes that are distinguished in terms of their timescales 2 , among which the rapidly reversible energy-quenching (qE) is, under most circumstances, the predominant NPQ component 2 , 4 . The major molecular effector of qE in the green model microalga Chlamydomonas reinhardtii (hereafter Chlamydomonas ) is the LIGHT HARVESTING COMPLEX STRESS RELATED protein LHCSR3, encoded by the LHCSR3.1 and LHCSR3.2 genes 5 that slightly differ only in their promoters; LHCSR1 can also contribute significantly to qE under conditions where LHCSR3 is not expressed 6 , 7 . PSBS, the key qE effector protein in higher plants 8 is encoded in two highly similar paralogues PSBS1 and PSBS2 in Chlamydomonas 9 .…”

“…Intracellular levels of CO 2 are modulated by the availability of its gaseous and hydrated forms 3 in the culture media and the supply of acetate, which is partly metabolized into CO 2 7 , 13 . Under low CO 2 , Chlamydomonas activates the CO 2 -concentrating mechanism (CCM) to avoid substrate-limitation of photosynthesis by raising the CO 2 concentration at the site of RuBisCO, where CO 2 is assimilated 3 .…”

“…Almost all CCM-related genes are under the control of the nucleus-localized zinc-finger type nuclear factor CIA5 (aka CCM1) 14 – 16 , including the Myb Transcription Factor LOW-CO 2 -STRESS RESPONSE 1 (LCR1) that controls the expression of genes coding for the periplasmic CAH1, the plasma membrane-localized bicarbonate transporter LOW CO 2 -INDUCED 1 (LCI1), and the low-CO 2 responsive LCI6, whose role remains to be elucidated 17 . CIA5 is also a major qE regulator activating transcription of genes encoding LHCSR3 and PSBS, while repressing accumulation of LHCSR1 protein 7 .…”

“…LHCSR3 expression relies on blue light perception by the photoreceptor phototropin (PHOT) 18 , on calcium signaling, mediated by the calcium sensor CAS 19 and on active photosynthetic electron flow 18 – 20 , likely via indirectly impacting CO 2 availability 7 . The critical importance of CO 2 in LHCSR3 expression is demonstrated by the fact that changes in CO 2 concentration can trigger LHCSR3 expression 21 – 23 even in the absence of light 7 . Accumulation of LHCSR1 and PSBS mRNA is under control of the UV-B photoreceptor UVR8 11 and PHOT 24 , 25 and is photosynthesis-independent 20 , 25 .…”

“…Accumulation of LHCSR1 and PSBS mRNA is under control of the UV-B photoreceptor UVR8 11 and PHOT 24 , 25 and is photosynthesis-independent 20 , 25 . While LHCSR1 is CO 2 /CIA5 independent at the transcript level 7 , 25 , PSBS is responsive to CO 2 abundance and is under partial control of CIA5 7 . A Cullin (CUL4) dependent E3-ligase 24 , 26 , 27 has been demonstrated to post-translationally regulate the transcription factor (TF) complex of CONSTANS (CrCO) 26 and NF-Y isomers 27 , which bind to DNA to regulate the transcription of LHCSR1 , LHCSR3 , and PSBS .…”