Regulation of the photosynthetic apparatus under fluctuating growth light

Abstract

Safe and efficient conversion of solar energy to metabolic energy by plants is based on tightly interregulated transfer of excitation energy, electrons and protons in the photosynthetic machinery according to the availability of light energy, as well as the needs and restrictions of metabolism itself. Plants have mechanisms to enhance the capture of energy when light is limited for growth and development. Also, when energy is in excess, the photosynthetic machinery slows down the electron transfer reactions in order to prevent the production of reactive oxygen species and the consequent damage of the photosynthetic machinery. In this opinion paper, we present a partially hypothetical scheme describing how the photosynthetic machinery controls the flow of energy and electrons in order to enable the maintenance of photosynthetic activity in nature under continual fluctuations in white light intensity. We discuss the roles of light-harvesting II protein phosphorylation, thermal dissipation of excess energy and the control of electron transfer by cytochrome b 6 f, and the role of dynamically regulated turnover of photosystem II in the maintenance of the photosynthetic machinery. We present a new hypothesis suggesting that most of the regulation in the thylakoid membrane occurs in order to prevent oxidative damage of photosystem I.

Induction of Photosynthetic Carbon Fixation in Anoxia Relies on Hydrogenase Activity and Proton-Gradient Regulation-Like1-Mediated Cyclic Electron Flow in Chlamydomonas reinhardtii

“…It is generally acknowledged that the PGRL1 protein participates to PSI-CEF both in C. reinhardtii and Arabidopsis (Arabidopsis thaliana; DalCorso et al, 2008;Iwai et al, 2010;Tolleter et al, 2011;Hertle et al, 2013;Johnson et al, 2014). By generating an additional proton motive force, PSI-CEF is proposed to enhance ATP synthesis in the illuminated chloroplast (Allen, 2003) and/or to trigger photoprotection of the photosynthetic apparatus (Joliot and Johnson, 2011;Tikkanen et al, 2012). Occurrence of PSI-CEF has been a matter of debate during the last decade, mainly because most experiments have been performed in nonphysiological conditions (e.g.…”

Photosynthesis of microalgae in outdoor mass cultures and modelling its effects on biomass productivity for fuels, feeds and chemicals

“…In fact, Tikkanen et al (2012) postulated that PSII photoinhibition is a major photoprotective mechanism because detached photoinhibited PSII centres and their LHCs slow down electron transfer, consequentially protecting PSI, which lacks an efficient repair system. This theory is supported by studies that found PSI damage was completely dependent on electron flow from PSII, as blocking LEF by 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) prevented PSI damage (Sonoike andTerashima, 1994, Havaux andDavaud, 1994).…”

“…Tikkanen et al (2010) reason that the high dissipation capacity of qE under high light diminishes the need for qT. Under fluctuating light conditions, Tikkanen et al (2012) reported 'severely stunted phenotypes' in STN7-deficient mutants (stn7 and stn7stn8). The authors stated that "Coordination of excitation energy distribution between PSII and PSI from the common P-LHCII antenna is crucial in preventing the accumulation of electrons in ETC under low illumination phases of fluctuating growth light, and is therefore important for photoprotection of PSI in plant chloroplasts during the subsequent high light peak".…”

“…"mixed cultures") suggests that a rapid change in thylakoid luminal pH occurs from dark to light transitions. Studies have shown that proton gradient regulation is essential for the health of plants and algae under low and fluctuating light conditions (Tikkanen et al, 2012). This allows a rapid proton motive force across the thylakoid membrane from dark to light transitions and has been connected to increased rates of both cyclic electron flow (Alric et al, 2010, Johnson et al, 2014 and the water-water cycle (Asada, 1999).…”

“…This allows a rapid proton motive force across the thylakoid membrane from dark to light transitions and has been connected to increased rates of both cyclic electron flow (Alric et al, 2010, Johnson et al, 2014 and the water-water cycle (Asada, 1999). Apart from being necessary to initiate linear electron transport, an important benefit of a rapidly developing proton motive force under fluctuating light is to slow down the electron transfer from cytochrome b6f to protect PSI, and to induce NPQ to prevent overexcitation of PSII (Tikkanen et al, 2012). Therefore, it is likely that the rapid increase in NPQ with incident irradiance observed under fluctuating light conditions is due to increased protonation of LHCSR3 (Figure 4-5E & F), by the rapid development of a luminal pH gradient.…”