How Do Photosynthetic Organisms Manage Light Stress?
This Special Focus Issue (Vol. 57, Issue 7) of Plant and Cell Physiology is organised and guest edited by Jun’ichi Mano, Tsuyoshi Endo and Chikahiro Miyake and reveals how light stress is managed in plants and algae. This issue is dedicated to the late Prof. Kozi Asada whose life’s work was dedicated to understanding photosynthesis photoinhibition, photosynthetic regulation through alternative electron flows, and the metabolic pathway to scavenge ROS in chloroplasts, which is more widely known as the water-water cycle.
Jun’ichi Mano, Tsuyoshi Endo and Chikahiro Miyake
This special focus issue on “How Do Photosynthetic Organisms Manage Light Stress?” is dedicated to the late Professor Kozi Asada, one of the pioneers of reactive oxygen species (ROS) and cyclic electron flow (CEF) research in plant sciences who established the water-water cycle, the ROS-scavenging metabolic pathway, and NADH dehydrogenase in chloroplasts of plants and algae. The issue is organized by Jun’ichi Mano, Tsuyoshi Endo and Chikahiro Miyake, and includes a variety of reviews and original research articles.
Gilles Curien, Serena Flori, Valeria Villanova, Leonardo Magneschi, Cécile Giustini, Giorgio Forti, Michel Matringe, Dimitris Petroutsos, Marcel Kuntz, Giovanni Finazzi
In this review we summarize current knowledge on the occurrence and regulation of the so-called water to water cycles, i.e. the reduction of molecular oxygen by light-generated photosynthetic electron flow. We focus on the different mechanisms allowing these reactions to proceed, and highlight their relevance in algae and (to a lesser extent) in plant acclimation to abiotic stress.
Luis A. del Río and Eduardo López-Huertas
*Free: Editor-in-Chief’s Choice Article*
Peroxisomes are subcellular organelles, which have an essentially oxidative type of metabolism and carry out key functions in eukaryotic cells. This review analyzes the generation of different ROS in plant peroxisomes (H2O2, O2·- and 1O2) and its regulation, the different antioxidant systems present in these organelles, and the proteomics of ROS metabolism, in the context of a function for peroxisomes as a source of ROS signaling molecules that can participate in plant cell metabolism under both physiological and stress conditions.
Takanori Maruta, Yoshihiro Sawa, Shigeru Shigeoka, and Takahiro Ishikawa
Ascorbate peroxidases (APXs) had been considered a bottleneck in the water-water cycle in chloroplasts because of their susceptibility to H2O2 damage. Biochemical, genetic, and molecular structural studies have indicated that the susceptibility of APXs has been acquired during plant evolution, which might allow for the flexible use of H2O2 as a signaling molecule in plants. How chloroplastic APXs mediate the light stress response is not so clear as they act both as oxidative stress defense and signaling regulators.
Giles N. Johnson and Piotr Stepien
The plastid terminal oxidase (PTox) is amongst the most recently discovered protein complexes in the thylakoid membrane. We still know little about its functioning in vivo, however there is evidence that in some species it can play a major role in protecting leaves from stress. This review examines our current knowledge and discusses how this function may be used to increase stress tolerance in crop species.
Marina A. Kozuleva and Boris N. Ivanov
The drain of electrons to O2 from electron transport chains of aerobic organisms, which is inevitable in the present Earth atmosphere leads to production of O2·− and H2O2. The review describes O2 reduction in the chloroplast photosynthetic electron transport chain, focusing on the main site of the process. The knowledge of its mechanisms there helps understanding of both an evolution of photosynthetic apparatus towards minimization/control of the electron leakage to O2 and ways of regulation of metabolic processes by ROS.
Masaru Kono and Ichiro Terashima
The importance of the photosynthetic alternative electron pathways in protection of PSI against fluctuating light photoinhibition has been suggested, but the protective mechanisms have not been fully clarified. Here we show that the cyclic electron flow around PSI (CEF-PSI) contributes to alleviation of the acceptor-side limitation and to acceleration of the donor-side limitation of PSI during fluctuating light exposure. These data suggest that CEF-PSI plays a key role in balancing these limitations.
Michael Liebthal, Marcel Strüve, Xin Li,Yvonne Hertle, Daniel Maynard, Thomas Hellweg, Andrea Viehhauser and Karl-Josef Dietz
The chloroplast 2-cysteine peroxiredoxin (2-CysPrx) establishes an alternative water-water cycle and interacts with cyclophilin 20-3, a regulator of chloroplast cysteine synthesis. Here we found that 2-CysPrx switches between the reduced decamer and dimer, and the catalytically inactive hyperoxidized form after about 250 turnovers, depending on the pH. The data support a model where 2-CysPrx and Cyp20-3 form a redox-sensitive regulatory module under the control of the stromal pH value, the redox state and additional stromal protein factor(s).
Chihiro K. Watanabe, Wataru Yamori, Shunichi Takahashi, Ichiro Terashima, Ko Noguchi
The respiratory alternative pathway (AP), which is catalyzed by the alternative oxidase (AOX), may alleviate photosystem II (PSII) photoinhibition. In this study, we showed that, when the cytochrome pathway was partially inhibited by antimycin A, PSII photoinhibition was accelerated in Arabidopsis aox1a mutants only under photorespiratory conditions. Our results suggest that the AP alleviates photoinhibition under high light conditions, by maintaining a functional photorespiratory pathway.
Md. Sanaullah Biswas and Jun’ichi Mano
Reactive carbonyl species (RCS), produced downstream of reactive oxygen species, can cause programmed cell death (PCD) in plants. In this study, it was found that RCS directly activated caspase-3-like protease (C3LP), and thereby initiated PCD in tobacco cultured cells. The results provide a specific biochemical explanation for plant oxidative injury, the importance of which is widely accepted while the process remains to be clearly resolved.
Keiichiro Shaku, Ginga Shimakawa, Masaki Hashiguchi, Chikahiro Miyake
Over-reduction of photosystem I (PSI) accelerates the production of reactive oxygen species (ROS) and in turn ROS inactivates PSI. We found that the reduction of cytochrome (Cyt) b6/f induced the suppression of electron flow from Cyt f to PSI and oxidized PSI. We propose that this suppression of electron flow is induced by the decrease in Q-cycle activity and plays an important role in disrupting the production of ROS with oxidizing PSI.
Ulrich Schreiber and Christof Klughammer
Until recently in vivo information about the state of photosystem I donor and acceptor sides has been restricted to mixed signals of P700, plastocyanin and ferredoxin NIR transmittance changes. We present measurements with a new type of spectrophotometer that allows online deconvolution of these electron carriers. The new technique has opened the way for a deeper understanding of various pathways of linear and cyclic electron transfer at photosystem I.
Henna Mustila, Pasi Paananen, Natalia Battchikova, Anita Santana-Sánchez, Dorota Muth-Pawlak, Martin Hagemann, Eva-Mari Aro and Yagut Allahverdiyeva
In cyanobacteria, the flavodiiron proteins Flv1 and Flv3 function in photoreduction of O2 to H2O, without the concomitant formation of reactive oxygen species. This reaction is dependent on both Flv proteins. Global transcript profiles of the Δflv1/Δflv3 mutant revealed a down-regulation of transcripts for carbon concentrating mechanism and nitrogen metabolism under constant and fluctuating light compared to wild-type. In strains overproducing solely Flv1 or Flv3, the homo-oligomer forms of these proteins also functioned in cell acclimation to fluctuating light by catalyzing reactions with other as yet unidentified components.
Masahiro Ikeuchi, Fumihiko Sato and Tsuyoshi Endo
Although the analysis of energy allocation at PSII has been gaining significant attention in chlorophyll fluorescence studies, understanding of regulated and non-regulated heat dissipations represented by ΦNPQ and Φf,D, respectively, remain ambiguous. We analyzed the drastic changes in these two parameters at dark-light transition based on the equation NPQ = ΦNPQ/Φf,D. We discuss the usefulness and limitation of the allocation model for measurement studies under natural light.
Milena Kulaseka, Maciej Jerzy Bernacki, Kamil Ciszakb, Damian Witoń, Stanisław Karpiński
The photon sensor protein PsbS was considered to be critical for non-photochemical quenching (NPQ) of light absorbed by PSII antennas and heat dissipation from whole leaves, however the latter had never been verified. Here we investigated foliar temperature dynamics under different light intensities using high-resolution thermal camera and a powerful adjustable LED light source. We show that light dependent foliar temperature dynamics is correlated with leaf chlorophyll content in various plant species. Further, by using PsbS null mutants, overexpressing transgenic lines and specific photosynthetic electron transport inhibitor (DCMU) we found that PsbS and measurable by modulated chlorophyll fluorescence changes in NPQ value are not directly involved in or correlated with regulation of foliar temperature dynamics during excessive light energy episodes.
The Relationship Between Photochemical Quenching and Non- Photochemical Quenching in Six Species of Cyanobacteria Reveals Species Difference in Redox State and Species Commonality in Energy Dissipation
Masahiro Misumi, Hiroshi Katoh, Tatsuya Tomo and Kintake Sonoike
Cyanobacterial electron transfers of photosynthesis and respiration interact with each other at the plastoquinone (PQ) pool, a crossing of the two pathways. Here we show that in the dark, the PQ pool is reduced in some cyanobacterial species while oxidized in others. Thus, the degree of metabolic interaction is species dependent. The development of energy dissipation under high light, however, is common in all the cyanobacterial species tested.
Ritsuko Fujii, Nami Yamano, Hideki Hashimoto, Norihiko Misawa and Kentaro Ifuku
Chloroplast genome-modified (CGM) lettuces dominantly accumulate astaxanthin and can grow normally with almost no accumulation of naturally occurring photosynthetic carotenoids. Here we reveal that functional defects of photosystem II in CGM lettuce are compensated by the anti-oxidative effect of heterologous carbonyl carotenoids. These data reveal the exquisite balance between photoinhibition and photoprotection to manage light stress.