Minimizing an Electron Flow to Molecular Oxygen in Photosynthetic Electron Transfer Chain: An Evolutionary View

Abstract

Recruitment of H 2 O as the final donor of electrons for light-governed reactions in photosynthesis has been an utmost breakthrough, bursting the evolution of life and leading to the accumulation of O 2 molecules in the atmosphere. O 2 molecule has a great potential to accept electrons from the components of the photosynthetic electron transfer chain (PETC) (so-called the Mehler reaction). Here we overview the Mehler reaction mechanisms, specifying the changes in the structure of the PETC of oxygenic phototrophs that probably had occurred as the result of evolutionary pressure to minimize the electron flow to O 2 . These changes are warranted by the fact that the efficient electron flow to O 2 would decrease the quantum yield of photosynthesis. Moreover, the reduction of O 2 leads to the formation of reactive oxygen species (ROS), namely, the superoxide anion radical and hydrogen peroxide, which cause oxidative stress to plant cells if they are accumulated at a significant amount. From another side, hydrogen peroxide acts as a signaling molecule. We particularly zoom in into the role of photosystem I (PSI) and the plastoquinone (PQ) pool in the Mehler reaction.

Recording true oxygen reduction capacity during photosynthetic electron transfer in Arabidopsis thylakoids and intact leaves

“…Our conclusions broadly support what is already described regarding the formation of ROS by photosynthetic processes in the chloroplast (Kozuleva, Ivanov et al 2020), including our observation of multiple distinct pathways for ROS formation associated with the thylakoid membrane. We have not ruled out that O 2 −• and possibly H 2 O 2 form upstream of PSI and can be detected by rapidly reacting dyes (Cathcart, Schwiers et al 1983), spin-traps or specific sensor proteins (Villamena, Zweier 2004).…”

“…Whilst chloroplast H 2 O 2 signaling pathways are slowly being defined (Gollan, Aro 2020, Crisp, Ganguly et al 2017, Bechtold, Richard et al 2008, Rossel, Wilson et al 2007, Dietz, Mittler et al 2016), the endogenous sources of specific ROS in the thylakoid membrane and the environmental conditions that lead to their formation are still subject to debate. For example, the current literature supports the generation of a stable H 2 O 2 pool, capable of export from the chloroplast, in multiple sites of PETC including the reduction of O 2 at PSII (Khorobrykh, Andrey 2019, Tiwari, Pospisil 2009), the PQ pool (Khorobrykh, S. A., Ivanov 2002, Mubarakshina, Ivanov 2010, Khorobrykh, Sergey A., Karonen et al 2015), PTOX (Heyno, Gross et al 2009), Cyt- b 6 f complex (Baniulis, Hasan et al 2013) and PSI (Mehler 1951, Kozuleva, Ivanov et al 2020). This broad range of candidates complicates models of ROS signaling, resulting in debates like those between Wang et al (Wang, He et al 2016) and Iwai et al (Iwai, Ogata et al 2019).…”

Intrinsic Fluctuations in Transpiration Induce Photorespiration to Oxidize P700 in Photosystem I

“…This is known as the Mehler reaction, which is the primary reaction of the water–water cycle [ 41 ]. The electron carriers localized at the acceptor side of PSI (A 0 , A 1 , F X , F A /F B , and Fd) can easily reduce O 2 to superoxide radicals [ 47 , 48 , 49 ]. However, the oxidation of P700 decreases the apparent quantum yield of PSI [ 50 ] and inhibits the accumulation of electrons on the acceptor side of PSI [ 12 ].…”

The Mehler reaction site is the Phylloquinone within Photosystem I

“…As a result, the photosynthetic apparatus appears to have evolved strong regulation of such reactions in an aerobic environment (2).…”

“…Nowadays, O2 photoreduction to O2 •− by a photosynthetic electron transfer (ET) chain is referred to as the true Mehler reaction, in order to distinguish it from a Mehler-like reaction (5,6). Although some evidence indicates that O2 •− production can take place in various locations (2,(7)(8)(9), photosystem I (PSI) seems to be the major site of this process (10,11).…”