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Photosystem II Photochemistry in Biotic and Abiotic Stress

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A special issue of Molecules (ISSN 1420-3049). This special issue belongs to the section "Photochemistry".

Deadline for manuscript submissions: closed (31 January 2023) | Viewed by 13960

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Prof. Dr. Michael Moustakas

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Department of Botany, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
Interests: plant ecophysiology; biotic stress; abiotic stress; photosynthesis; antioxidative mechanisms; photoprotective mechanisms; mineral nutrition; ROS
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Dear Colleagues,

Photosynthesis is the process by which organisms convert absorbed solar energy into chemical energy via photosystem II (PSII) and photosystem I (PSI). In the light reactions of photosynthesis, the absorbed light as photons by the light-harvesting complexes (LHCs) is transferred to the reaction centers (RCs), where through charge separation, the electrons flow from photosystem II (PSII) through cytochrome b6f and diffusible electron carriers to photosystem I (PSI). PSII and PSI, which work coordinately for efficient electron transfer, are located in the photosynthetic membranes of chloroplasts, the thylakoids. Chloroplasts exhibit stacked and unstacked thylakoid membranes, designated as grana and stroma thylakoids, respectively. The two photosystems, PSI and PSII, are laterally and functionally separated mainly into the stroma (non-appressed) and grana (appressed) thylakoid membranes, respectively, that allow the regulation of the excitation energy distribution between the two photosystems. PSII is a multi-protein super-complex that initiates electron transport within the thylakoid membrane, catalyzing one of the most exciting reactions in nature, the light-driven oxidation of H₂O and the production of O₂. PSII eventually provides the electrons required for the conversion of inorganic molecules into the organic molecules and establishes itself as the “engine of life”. In the light reactions, the result is the generation of a proton gradient (ΔpH) for ATP synthesis and the reduction of NADP⁺ by the electrons transferred.

In light reactions of photosynthesis, reactive oxygen species (ROS), such as superoxide anion radical (O₂^•^–), hydrogen peroxide (H₂O₂), and singlet oxygen (¹O₂) are continuously produced at basal levels that are incapable of causing damage, as they are being scavenged by different antioxidant mechanisms. Under most biotic or abiotic stresses the absorbed light energy exceeds what can be used and, thus, it can damage the photosynthetic apparatus, with PSII being particularly exposed to damage. If this excess excitation energy is not quenched by the photoprotective mechanism of non-photochemical quenching (NPQ), increased production of ROS occurs that can lead to oxidative stress. Thus, under biotic or abiotic stress, the oxidative stress that results from an imbalance between ROS production and scavenging by the antioxidant mechanisms can cause cellular damage that can lead to cell death. The response of plants to this imbalance before damage to their cellular structures is critical for maintaining high rates of photosynthesis and also for their survival. Nevertheless, these ROS signals not only provide cells with tools to monitor electron transport and, thus, prevent over-reduction or over-oxidation, but also produce redox regulatory networks that facilitate plants to sense and respond to biotic and abiotic stress conditions.

We encourage original research submissions, as well as review/mini-review articles, concerning basic aspects and future research directions in the field.

Prof. Dr. Michael Moustakas
Guest Editor

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Keywords

Photosynthesis
Light reactions
Electron transport
Chlorophyll fluorescence
Excitation energy
Light-harvesting complex
Antioxidant mechanisms
Thylakoids
Reaction centers
Stacked and un-stacked membranes
Reactive oxygen species (ROS)
ROS production and scavenging
Superoxide anion radical
Hydrogen peroxide
Proton gradient (ΔpH)
Singlet oxygen
Oxidative stress
Environmental stress
Redox regulation

Published Papers (7 papers)

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Research

19 pages, 3209 KiB

Open AccessArticle

Compensatory Transcriptional Response of Fischerella thermalis to Thermal Damage of the Photosynthetic Electron Transfer Chain

by Pablo Vergara-Barros, Jaime Alcorta, Angélica Casanova-Katny, Dennis J. Nürnberg and Beatriz Díez

Molecules 2022, 27(23), 8515; https://doi.org/10.3390/molecules27238515 - 03 Dec 2022

Viewed by 1785

Abstract

Key organisms in the environment, such as oxygenic photosynthetic primary producers (photosynthetic eukaryotes and cyanobacteria), are responsible for fixing most of the carbon globally. However, they are affected by environmental conditions, such as temperature, which in turn affect their distribution. Globally, the cyanobacterium Fischerella thermalis is one of the main primary producers in terrestrial hot springs with thermal gradients up to 60 °C, but the mechanisms by which F. thermalis maintains its photosynthetic activity at these high temperatures are not known. In this study, we used molecular approaches and bioinformatics, in addition to photophysiological analyses, to determine the genetic activity associated with the energy metabolism of F. thermalis both in situ and in high-temperature (40 °C to 65 °C) cultures. Our results show that photosynthesis of F. thermalis decays with temperature, while increased transcriptional activity of genes encoding photosystem II reaction center proteins, such as PsbA (D1), could help overcome thermal damage at up to 60 °C. We observed that F. thermalis tends to lose copies of the standard G4 D1 isoform while maintaining the recently described D1^INT isoform, suggesting a preference for photoresistant isoforms in response to the thermal gradient. The transcriptional activity and metabolic characteristics of F. thermalis, as measured by metatranscriptomics, further suggest that carbon metabolism occurs in parallel with photosynthesis, thereby assisting in energy acquisition under high temperatures at which other photosynthetic organisms cannot survive. This study reveals that, to cope with the harsh conditions of hot springs, F. thermalis has several compensatory adaptations, and provides emerging evidence for mixotrophic metabolism as being potentially relevant to the thermotolerance of this species. Ultimately, this work increases our knowledge about thermal adaptation strategies of cyanobacteria. Full article

(This article belongs to the Special Issue Photosystem II Photochemistry in Biotic and Abiotic Stress)

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16 pages, 2362 KiB

Open AccessArticle

Effects of Pre-Harvest Supplemental UV-A Light on Growth and Quality of Chinese Kale

by Youzhi Hu, Xia Li, Xinyang He, Rui He, Yamin Li, Xiaojuan Liu and Houcheng Liu

Molecules 2022, 27(22), 7763; https://doi.org/10.3390/molecules27227763 - 11 Nov 2022

Cited by 1 | Viewed by 1162

Abstract

The effects of supplemental UV-A (385 nm) period and UV-A intensity for 5 days before harvest (DBH) on growth, antioxidants, antioxidant capacity, and glucosinolates contents in Chinese kale (Brassica oleracea var. alboglabra Bailey) were studied in plant factory. In the experiment of the UV-A period, three treatments were designed with 10 W·m⁻² UV-A supplement, T1(5 DBH), T2 (10 DBH), and no supplemental UV-A as control. In the experiment of UV-A intensity, four treatments were designed with 5 DBH, control (0 W·m⁻²), 5 w (5 W·m⁻²), 10 w (10 W·m⁻²), and 15 w (15 W·m⁻²). The growth light is as follows: 250 μmol·m⁻²·s⁻¹; red light: white light = 2:3; photoperiod: 12/12. The growth and quality of Chinese kale were improved by supplemental UV-A LED. The plant height, stem diameter, and biomass of Chinese kale were the highest in the 5 W·m⁻² treatment for 5 DBH. The contents of chlorophyll a, chlorophyll b, and total chlorophyll were only highly increased by 5 W·m⁻² UV-A for 5 DBH, while there was no significant difference in the content of carotenoid among all treatments. The contents of soluble sugar and free amino acid were higher only under 10 DBH treatments than in control. The contents of total phenolic and total antioxidant capacity were the highest in 5 W·m⁻² treatment for 5 DBH. There was a significant positive correlation between total phenolic content and DPPH and FRAP value. After 5 DBH treatments, the percentages and contents of total aliphatic glucosinolates, sinigrin (SIN), gluconapin (GNA), and glucobrassicanapin (GBN) were highly increased, while the percentages and contents of glucobrassicin (GBS), 4-methoxyglucobrassicin (4-MGBS), and Progoitrin (PRO) were significantly decreased, especially under 10 W·m⁻² treatment. Our results show that UV-A LED supplements could improve the growth and quality of Chinese kale, and 5 W·m⁻² UV-A LED with 5 DBH might be feasible for Chinese kale growth, and 10 W·m⁻² UV-A LED with 5 DBH was better for aliphatic glucosinolates accumulation in Chinese kale. Full article

(This article belongs to the Special Issue Photosystem II Photochemistry in Biotic and Abiotic Stress)

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15 pages, 3267 KiB

Open AccessArticle

Investigation of Photosystem II Functional Size in Higher Plants under Physiological and Stress Conditions Using Radiation Target Analysis and Sucrose Gradient Ultracentrifugation

by Maria Teresa Giardi, Amina Antonacci, Eleftherios Touloupakis and Autar K. Mattoo

Molecules 2022, 27(17), 5708; https://doi.org/10.3390/molecules27175708 - 05 Sep 2022

Cited by 1 | Viewed by 1324

Abstract

The photosystem II (PSII) reaction centre is the critical supramolecular pigment–protein complex in the chloroplast which catalyses the light-induced transfer of electrons from water to plastoquinone. Structural studies have demonstrated the existence of an oligomeric PSII. We carried out radiation inactivation target analysis (RTA), together with sucrose gradient ultracentrifugation (SGU) of PSII, to study the functional size of PSII in diverse plant species under physiological and stress conditions. Two PSII populations, made of dimeric and monomeric core particles, were revealed in Pisum sativum, Spinacea oleracea, Phaseulus vulgaris, Medicago sativa, Zea mais and Triticum durum. However, this core pattern was not ubiquitous in the higher plants since we found one monomeric core population in Vicia faba and a dimeric core in the Triticum durum yellow-green strain, respectively. The PSII functional sizes measured in the plant seedlings in vivo, as a decay of the maximum quantum yield of PSII for primary photochemistry, were in the range of 75–101 ± 18 kDa, 2 to 3 times lower than those determined in vitro. Two abiotic stresses, heat and drought, imposed individually on Pisum sativum, increased the content of the dimeric core in SGU and the minimum functional size determined by RTA in vivo. These data suggest that PSII can also function as a monomer in vivo, while under heat and drought stress conditions, the dimeric PSII structure is predominant. Full article

(This article belongs to the Special Issue Photosystem II Photochemistry in Biotic and Abiotic Stress)

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16 pages, 3372 KiB

Open AccessArticle

Root-Associated Entomopathogenic Fungi Modulate Their Host Plant’s Photosystem II Photochemistry and Response to Herbivorous Insects

by Julietta Moustaka, Nicolai Vitt Meyling and Thure Pavlo Hauser

Molecules 2022, 27(1), 207; https://doi.org/10.3390/molecules27010207 - 29 Dec 2021

Cited by 9 | Viewed by 1898

Abstract

The escalating food demand and loss to herbivores has led to increasing interest in using resistance-inducing microbes for pest control. Here, we evaluated whether root-inoculation with fungi that are otherwise known as entomopathogens improves tomato (Solanum lycopersicum) leaflets’ reaction to herbivory by Spodoptera exigua (beet armyworm) larvae using chlorophyll fluorescence imaging. Plants were inoculated with Metarhizium brunneum or Beauveria bassiana, and photosystem II reactions were evaluated before and after larval feeding. Before herbivory, the fraction of absorbed light energy used for photochemistry (Φ_PSII) was lower in M. brunneum-inoculated than in control plants, but not in B. bassiana-inoculated plants. After herbivory, however, Φ_PSII increased in the fungal-inoculated plants compared with that before herbivory, similar to the reaction of control plants. At the same time, the fraction of energy dissipated as heat (Φ_NPQ) decreased in the inoculated plants, resulting in an increased fraction of nonregulated energy loss (Φ_NO) in M. brunneum. This indicates an increased singlet oxygen (¹O₂) formation not detected in B. bassiana-inoculated plants, showing that the two entomopathogenic fungi differentially modulate the leaflets’ response to herbivory. Overall, our results show that M. brunneum inoculation had a negative effect on the photosynthetic efficiency before herbivory, while B. bassiana inoculation had no significant effect. However, S. exigua leaf biting activated the same compensatory PSII response mechanism in tomato plants of both fungal-inoculated treatments as in control plants. Full article

(This article belongs to the Special Issue Photosystem II Photochemistry in Biotic and Abiotic Stress)

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13 pages, 2349 KiB

Open AccessArticle

Polymer-Modified Single-Walled Carbon Nanotubes Affect Photosystem II Photochemistry, Intersystem Electron Transport Carriers and Photosystem I End Acceptors in Pea Plants

by Nia Petrova, Momchil Paunov, Petar Petrov, Violeta Velikova, Vasilij Goltsev and Sashka Krumova

Molecules 2021, 26(19), 5958; https://doi.org/10.3390/molecules26195958 - 01 Oct 2021

Cited by 6 | Viewed by 1536

Abstract

Single-walled carbon nanotubes (SWCNT) have recently been attracting the attention of plant biologists as a prospective tool for modulation of photosynthesis in higher plants. However, the exact mode of action of SWCNT on the photosynthetic electron transport chain remains unknown. In this work, we examined the effect of foliar application of polymer-grafted SWCNT on the donor side of photosystem II, the intersystem electron transfer chain and the acceptor side of photosystem I. Analysis of the induction curves of chlorophyll fluorescence via JIP test and construction of differential curves revealed that SWCNT concentrations up to 100 mg/L did not affect the photosynthetic electron transport chain. SWCNT concentration of 300 mg/L had no effect on the photosystem II donor side but provoked inactivation of photosystem II reaction centres and slowed down the reduction of the plastoquinone pool and the photosystem I end acceptors. Changes in the modulated reflection at 820 nm, too, indicated slower re-reduction of photosystem I reaction centres in SWCNT-treated leaves. We conclude that SWCNT are likely to be able to divert electrons from the photosynthetic electron transport chain at the level of photosystem I end acceptors and plastoquinone pool in vivo. Further research is needed to unequivocally prove if the observed effects are due to specific interaction between SWCNT and the photosynthetic apparatus. Full article

(This article belongs to the Special Issue Photosystem II Photochemistry in Biotic and Abiotic Stress)

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13 pages, 1700 KiB

Open AccessArticle

Changes in Light Energy Utilization in Photosystem II and Reactive Oxygen Species Generation in Potato Leaves by the Pinworm Tuta absoluta

by Ilektra Sperdouli, Stefanos Andreadis, Julietta Moustaka, Emmanuel Panteris, Aphrodite Tsaballa and Michael Moustakas

Molecules 2021, 26(10), 2984; https://doi.org/10.3390/molecules26102984 - 18 May 2021

Cited by 25 | Viewed by 2695

Abstract

We evaluated photosystem II (PSII) functionality in potato plants (Solanum tuberosum L.) before and after a 15 min feeding by the leaf miner Tuta absoluta using chlorophyll a fluorescence imaging analysis combined with reactive oxygen species (ROS) detection. Fifteen minutes after feeding, we observed at the feeding zone and at the whole leaf a decrease in the effective quantum yield of photosystem II (PSII) photochemistry (Φ_PSII). While at the feeding zone the quantum yield of regulated non-photochemical energy loss in PSII (Φ_NPQ) did not change, at the whole leaf level there was a significant increase. As a result, at the feeding zone a significant increase in the quantum yield of non-regulated energy loss in PSII (Φ_NO) occurred, but there was no change at the whole leaf level compared to that before feeding, indicating no change in singlet oxygen (¹O₂) formation. The decreased Φ_PSII after feeding was due to a decreased fraction of open reaction centers (q_p), since the efficiency of open PSII reaction centers to utilize the light energy (Fv′/Fm′) did not differ before and after feeding. The decreased fraction of open reaction centers resulted in increased excess excitation energy (EXC) at the feeding zone and at the whole leaf level, while hydrogen peroxide (H₂O₂) production was detected only at the feeding zone. Although the whole leaf PSII efficiency decreased compared to that before feeding, the maximum efficiency of PSII photochemistry (Fv/Fm), and the efficiency of the water-splitting complex on the donor side of PSII (Fv/Fo), did not differ to that before feeding, thus they cannot be considered as sensitive parameters to monitor biotic stress effects. Chlorophyll fluorescence imaging analysis proved to be a good indicator to monitor even short-term impacts of insect herbivory on photosynthetic function, and among the studied parameters, the reduction status of the plastoquinone pool (q_p) was the most sensitive and suitable indicator to probe photosynthetic function under biotic stress. Full article

(This article belongs to the Special Issue Photosystem II Photochemistry in Biotic and Abiotic Stress)

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13 pages, 3586 KiB

Open AccessArticle

A Computational Study of the S₂ State in the Oxygen-Evolving Complex of Photosystem II by Electron Paramagnetic Resonance Spectroscopy

by Bernard Baituti and Sebusi Odisitse

Molecules 2021, 26(9), 2699; https://doi.org/10.3390/molecules26092699 - 04 May 2021

Viewed by 2058

Abstract

The S₂ state produces two basic electron paramagnetic resonance signal types due to the manganese cluster in oxygen-evolving complex, which are influenced by the solvents, and cryoprotectant added to the photosystem II samples. It is presumed that a single manganese center oxidation [...] Read more.

g 4.1

electron paramagnetic resonance signals and hence it has been the most studied of all the Kok cycle intermediates due to the ease of experimental preparation and stability. The S₂ state was studied using electron paramagnetic resonance spectroscopy at X-band frequencies. The aim of this study was to determine the spin states of the

g 4.1

signal. The multiline signal was observed to arise from a ground state spin ½ centre while the

g

4.1 signal generated at ≈140 K NIR illumination was proposed to arise from a spin

\frac{5}{2}

center with rhombic distortion. The ‘ground’ state

g

4.1 signal was generated solely or by conversion from the multiline. The data analysis methods used involved numerical simulations of the experimental spectra on relevant models of the oxygen-evolving complex cluster. A strong focus in this paper was on the ‘ground’ state

g

4.1 signal, whether it is a rhombic

\frac{5}{2}

spin state signal or an axial

\frac{3}{2}

spin state signal. The data supported an X-band CW-EPR-generated

g

4.1 signal as originating from a near rhombic spin 5/2 of the S₂ state of the PSII manganese cluster. Full article

(This article belongs to the Special Issue Photosystem II Photochemistry in Biotic and Abiotic Stress)

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