Differential effects of severe water stress on linear and cyclic electron fluxes through Photosystem I in spinach leaf discs in CO2-enriched air

Abstract

Linear and cyclic electron fluxes through Photosystem I in 1% CO(2) were quantified in spinach leaf tissue under severe water stress. Using actinic light with a peak at 697 nm for preferential light absorption by Photosystem I while also stimulating Photosystem II to improve redox poising, the cyclic electron flux after 60 s of illumination was a substantial proportion (33-44%) of the total electron flux through PSI at irradiances up to ~1,070 micromol photons m(-2) s(-1). At the maximum irradiance, the cyclic electron flux changed little with the progressive water loss from leaf tissue up to ~60%; by contrast, the linear electron flux was approximately halved. A reason for this differential effect of water stress on the capacity for cyclic and linear electron flow could be the increased crowding of soluble proteins in the stroma due to chloroplast shrinkage. Indeed the confinement of soluble proteins to a smaller chloroplast volume was indicated by cryo-scanning electron microscopy. It is known that the diffusion coefficient of large proteins is decreased when the background concentration of small proteins is raised; by contrast, the diffusion coefficient of small proteins is not affected by increasing the concentration of a large protein (Muramatsu and Minton in Proc Natl Acad Sci USA 85:2984-2988, 1988). Therefore, we suggest that linear electron flow, being coupled to the Calvin-Benson cycle, is limited by the diffusion of large macromolecules, especially the ribulose 1, 5-bisphosphate carboxylase/oxygenase complex. By contrast, cyclic electron flow, involving relatively small macromolecules such as ferredoxin, is less susceptible to inhibition by crowding in the stroma.

An Arabidopsis Mutant with High Cyclic Electron Flow around Photosystem I (hcef) Involving the NADPH Dehydrogenase Complex

“…By contrast, introducing the crr2-2 mutation into hcef1 (hcef1 crr2-2, Figure 6B) resulted in severely hindered photosynthesis, suggesting that hcef1 imposes a requirement for additional ATP that is fulfilled via CEF1 that involves NDH. Similar increases in CEF1, presumably reflecting increased chloroplast ATP demand, have been reported upon imposing environmental stresses, such as drought (Jia et al, 2008;Kohzuma et al, 2008). At least in the case of hcef1, alternative ATP/NADPH balancing mechanisms (e.g., water-water cycle [Asada, 2000] and the malate shunt [Scheibe, 2004]) were apparently unable to compensate for the loss of CEF1 upon mutation of NDH.…”

“…Some groups have reported substantial increases in CEF1 under environmental stress, such as drought (Jia et al, 2008;Kohzuma et al, 2008) or high light (Baker and Ort, 1992), or during the induction of photosynthesis from prolonged dark acclimation (Joë t et al, 2002;Joliot and Joliot, 2002). Others have found only small contributions of CEF1 to the photosynthetic energy budget, especially under steady state conditions Harbinson et al, 1989;Avenson et al, 2005a).…”

How Does Cyclic Electron Flow Alleviate Photoinhibition in Arabidopsis?

“…Under such conditions, the decreased amount of NADP + causes the activation of pgr5-dependent CEF (Okegawa et al, 2008). CEF has also been demonstrated to be accelerated in stress conditions, such as strong light (Clarke and Johnson, 2001;Miyake et al, 2004;DalCorso et al, 2008), low CO 2 (Munekage et al, 2002), and drought (Golding and Johnson, 2003;Golding et al, 2004), although not in drought when the air is enriched in CO 2 and the redox posing for CEF is near optimal (Jia et al, 2008). Our results demonstrated that CEF generates an acidic lumen and a DpH and helps avoid photoinhibition by preventing photodamage to PSII in a qE-independent manner and minimizing inhibition of the repair of photodamaged PSII in a qE-dependent manner.…”

Induction kinetics of photosystem I-activated P700 oxidation in plant leaves and their dependence on pre-energization

“…The decomposition of the kinetic curve of P700 + dark reduction into sev eral exponential terms provides the means to compare the rates of electron fluxes to P700 + along the cyclic route and from alternative sources [13][14][15]. Another approach to CET quantification makes use of the leaf exposure to white light (WL) under control conditions and in the presence of methyl viologen (MV), an agent that effectively consumes all electrons available on the acceptor side of PSI, thus excluding CET [15,16].…”