Role of cyclic and pseudo‐cyclic electron transport in response to dynamic light changes in Physcomitrella patens

Abstract

Photosynthetic organisms support cell metabolism by harvesting sunlight and driving the electron transport chain at the level of thylakoid membranes. Excitation energy and electron flow in the photosynthetic apparatus is continuously modulated in response to dynamic environmental conditions. Alternative electron flow around photosystem I plays a seminal role in this regulation contributing to photoprotection by mitigating overreduction of the electron carriers. Different pathways of alternative electron flow coexist in the moss Physcomitrella patens, including cyclic electron flow mediated by the PGRL1/PGR5 complex and pseudo-cyclic electron flow mediated by the flavodiiron proteins FLV. In this work, we generated P. patens plants carrying both pgrl1 and flva knock-out mutations. A comparative analysis of the WT, pgrl1, flva, and pgrl1 flva lines suggests that cyclic and pseudo-cyclic processes have a synergic role in the regulation of photosynthetic electron transport. However, although both contribute to photosystem I protection from overreduction by modulating electron flow following changes in environmental conditions, FLV activity is particularly relevant in the first seconds after a light change whereas PGRL1 has a major role upon sustained strong illumination.

PGRL1 overexpression in Phaeodactylum tricornutum inhibits growth and reduces apparent PSII activity

“…In C. reinhardtii (Jokel et al, 2018), PGRL1 plays an important role in the response to FL, although it takes some time to activate. Moreover, in Physcomitrella patens, PGRL1 is mostly active under continuous light (Storti et al, 2019). By contrast, in P. tricornutum, a chlorophyll c-containing organism, we found that PGRL1 plays an important role in responding to fluctuating light.…”

“…Studies have shown that an absence of PGRL1 in A. thaliana, which are sensitive to AA, causes a decrease of CET. Recently, studies have indicated that PGRL1 acts synergistically with FLV under fluctuating light conditions (Storti et al, 2019). In C. reinhardtii (Jokel et al, 2018), PGRL1 plays an important role in the response to FL, although it takes some time to activate.…”

“…However, in Chlamydomonas reinhardtii, a super-complex containing PSI, light harvesting complex 1 (LHCI), LHCII, Fd-NADPH oxidoreductase, cytochrome b(6)f complex and PGRL1 without PGR5 performs the FQR function in which PGRL1 appears to maintain a structure with resistance to AA (Iwai et al, 2010). Although the function of PGR5 under fluctuating light has been investigated thoroughly (Suorsa et al, 2012;Yamori et al, 2016;Kawashima et al, 2017;Jokel et al, 2018;Wada et al, 2018), there is little information available on the function of PGRL1 under fluctuating light conditions (Jokel et al, 2018;Storti et al, 2019). Previously, researchers have focused mainly on the lack of PGRL1 when studying the activity of PSI.…”

Regulation of electron transport is essential for photosystem I stability and plant growth

“…Plant material and growth P. patens (Gransden ecotype) wild-type (WT) and flva, pgrl1 and ndhm knockout (KO) lines (Kukuczka et al, 2014;Gerotto et al, 2016;Storti et al, 2019Storti et al, , 2020 were maintained in the protonemal stage by vegetative propagation on PpNH 4 medium (Ashton et al, 1979) and grown under controlled conditions: 24°C, 16 h : 8 h, light : dark photoperiod with 50 µmol photons m À2 s À1 (control light, CL) unless otherwise specified. Physiological and biochemical experiments were performed on 10-d-old plants grown in PpNO 3 medium (Ashton et al, 1979).…”

“…For triple mutant isolation, the pgrl1 construct was used to remove pgrl1 from the flva-ndhm background. Similarly, the ndhm KO construct (Storti et al, 2020) was used to remove the gene from the flva-pgrl1 KO background (Storti et al, 2019), obtaining triple flva-pgrl1-ndhm KO mutant plants in both cases (Fig. S2).…”