‘Regulation of photosynthesis’ session of the Russian Photobiology Society 9th Congress (Shepsi, September 12–19, 2021)

Abstract

The ‘Regulation of Photosynthesis’ session was one of the largest events of the Congress, with 17 talks and 9 poster presentations. It covered many topics on the cutting edge of modern photosynthesis research: from the electron transport within the cytochrome b₆f-complex to the novel role of carbonic anhydrase in the regulation of pH within the thylakoid lumen, the expanding role of retrograde signaling in all aspects of plant life including the regulation of cell-to-cell traffic via plasmodesmata, and the development of new non-invasive techniques to measure photosynthetic response. Here, a short survey of the presented reports is given.

Photosynthesis fuel plants with the energy of sunlight; moreover, being sensitive to fluctuations of many external factors, it provides the plant with the information about the environment. Thus, it is not surprising that photosynthesis as a central process for plant life is subject to finely tuned regulation. The session “Regulation of Photosynthesis” included four plenary lectures. Two of them were devoted to the retrograde signaling. Olga Voitsekhovskaja (Komarov Botanical Institute RAS, Saint Petersburg) provided an overview of the emerging role of the levels of antenna chlorophyll b as the source of signals regulating plant development, including transitions between ontogenetic stages, and presented evidence for impaired retrograde control of gene expression in barley mutants and Arabidopsis transgenic lines with changed levels of chlorophyll b. She proposed a hypothesis that one of the underlying mechanisms might be related to the changed size of PSII antenna supercomplexes (which depends on the levels of chlorophyll b) that affects the rate of their diffusion within the thylakoid membrane leading to disturbances in reduction and oxidation events within photosynthetic electron transport chain. Maria Borisova-Mubarakshina (Institute of Basic Biological Problems RAS, Pushchino) presented an update on pathways of hydrogen peroxide production in chloroplasts, the mechanisms of H₂O₂ diffusion from the chloroplast to the cytoplasm, and the key signaling role of H₂O₂ in the downregulation of PSII antenna size in response to prolonged high light. She put forward a hypothesis that H₂O₂ molecules produced in the reaction between reduced plastoquinone and superoxide anion radical generated in photosynthetic electron transport chain are the signal agents. Just, they but not the redox-state of plastoquinone pool, the signaling role of which was frequently suggested, inform the adaptive cell systems about the chain redox-state, which depends on the environment state. The plenary lecture by Galina Riznichenko (Moscow State University, Department of Biophysics) presented mathematical and computational models of several steps of photosynthetic electron transport: electron transfer within the reaction centers of photosystems and the cytochrome b₆f-complex, models of linear and cyclic electron flow, build-up of electrochemical potentials at the thylakoid membrane with special attention to the role of buffering groups of lipids, non-photochemical quenching (NPQ), and the coupling of photosynthetic light reactions with the Calvin cycle. The details of these models were further highlighted in several talks and posters.

A search for advanced non-invasive methods for monitoring photosynthetic responses to various stresses is becoming a hotspot of modern photosynthesis research. In his plenary talk, Vladimir Sukhov (Lobachevsky State University of Nizhny Novgorod) elegantly demonstrated that stress-induced long-distance electric signals can cause systemic changes in the functions of the photosynthetic machinery aimed at the adjustment of photosynthesis to stress factors. It is noteworthy that the authors were able to show the effects of electric signals on the narrow-band photochemical reflectance index (PRI) of leaves and related the observed changes to photosynthesis parameters. This provides a new basis for the development of non-invasive monitoring tools.

Some aspects touched on in the plenary lectures were further developed in detail in talks of early career researchers. Valeriya Dmitrieva (Komarov Botanical Institute RAS, Saint Petersburg) presented an evidence for cross-talk between photosynthesis and plasmodesmata in the leaves of several Arabidopsis mutants, showing for the first time that photoassimilates exported from the leaves via plasmodesmata is limited by an increase in chloroplast ATP and/or NADPH levels; this may represent an evolutionary defense mechanism to prevent depletion of the pool of Calvin cycle intermediates. Data on the decrease in the size of PSII antenna as the key mechanism of adaptation to a wide range of abiotic and biotic stresses has been presented by Daria Vetoshkina (Institute of Basic Biological Problems RAS, Pushchino). Ekaterina Sukhova (Lobachevsky State University of Nizhny Novgorod) characterized the usefulness of various spectral ranges of reflected light for evaluation and prediction of changes in photosynthesis in response to abiotic stress.

Many talks were devoted to the responses of photosynthesis to changes in the environment. In her study of barley grown at different wavelengths, Olga Avercheva (Moscow State University) showed that blue light causes changes in the induction of non-photochemical fluorescence quenching (NPQ) compared to white light; however, the reason was not related to changes in the proton gradient at the thylakoid membrane but rather to some non-identified energy-related components of quenching. Oxana Ptushenko (Moscow State University) analyzed light-dependent changes in the optical transparency of the leaves of several Tradescantia species in response to high light stress, due to the anatomical features of the leaf. Lyudmila Kabashnikova and Tatiana Viks (Institute of Biophysics and Cell Bioengineering NAN, Minsk, Republic of Belarus) reported on photosynthesis in barley after infection by pathogenic fungus Bipolaris sorokiniana and showed that the function and structure of chloroplasts can be indicators of the level of plant immunity, and thus can be used in plant selection during plant breeding and in the development of new technologies for plant protection.

An essential part of the session was devoted to the studies of the multiple roles of carbonic anhydrases in the regulation of photosynthesis in land plants and algae. Natalia Rudenko (Institute of Basic Biological Problems RAS, Pushchino) presented a fundamental study performed by a group of authors on the novel functions of several carbonic anhydrases (CA) found in the chloroplasts of land plants. Two alpha-carbonic anhydrases, α-CA4 and α-CA2, were shown to occur in the thylakoid membrane and to regulate NPQ. Another thylakoid CA, α-CA 5, is involved in the discovered many years ago the effect of photophosphorylation rate increase in the thylakoids under an increase in bicarbonate concentration. Based on their data, the authors proposed that it is the stromal α-CA1 that is involved in the supply of Rubisco with CO2, while the other stromal CA, β-CA1, whose role in this process is frequently assumed to be involved in the regulation of stromal pH. The functions of alpha-CA2 were characterized in more detail in the talk given by Elena Nadeeva-Zhurikova (Institute of Basic Biological Problems RAS, Pushchino). The authors proposed that this CA is involved in the regulation of pH in thylakoid lumen.

Vasiliy Terent’ev and Anna Shukshina (Institute of Basic Biological Problems RAS, Pushchino) explored the role of the carbonic anhydrase named CAH3 occurring in the thylakoid lumen of the green alga Chlamydomonas reinhardtii. They demonstrated that CAH3 has an important function in the stabilization of the oxygen-evolving complex of PSII. Furthermore, the authors demonstrated for the first time the unusual changes of chloroplast morphology in a mutant lacking CAH3; these changes were proposed to represent a mechanism of PSII protection from photoinhibition because the mutant was unable to develop normal NPQ.

Several speakers presented in-depth studies of the functioning of photosynthetic complexes, PSII, b₆f, and PSI. Daria Vilianen (Institute of Basic Biological Problems RAS, Pushchino) talked about the mechanisms of plastohydroquinone oxidation in the cytochrome b₆f-complex. She presented evidence for the role of long-lived protonated amino acid residues of the quinol-oxidizing site, in particular the Glu78 of subunit IV, which is directly involved in the deprotonation of plastohydroquinone. The report of Margarita Rodionova (Institute of Plant Physiology RAS, Moscow) focused on the characterization of a number of synthetic Cu²⁺ complexes that inhibit the function of the PSI reaction center, but do not cause structural changes in polypeptide chains. These complexes also do not act as quenchers of the excited states of chlorophyll. In her poster presentation, Marina Kozuleva (Institute of Basic Biological Problems RAS, Pushchino) presented an overview of the key components of the photosynthetic electron transport chain performing electron transfer to oxygen and, thus, producing a superoxide radical, and provided a critical assessment of the evolutionary role of the oxygen reduction process in chloroplasts. Alexander Bogachev (Moscow State University) reported on the occurrence of Na⁺-translocating ferredoxin:NAD⁺-oxidoreductase in a number of marine green sulfur bacteria. Here, this enzyme is considered to assist an increase in the efficiency of light energy conversion.

A highly interesting study of an ecological and anatomical aspect of the regulation of photosynthesis was presented by Tatiana Savchenko (Institute of Basic Biological Problems RAS, Pushchino) who focused on the structure and performance of chloroplasts in the chlorenchyma of wine (Vitis vinifera). She showed that characteristics of the chloroplasts and the dynamics of NPQ development in the cortical tissues of the vine are relevant for the formation of frost resistance in perennial wine plants.

In general, the reports presented at the session showed significant progress in understanding the regulation of photosynthesis. The major regulatory mechanisms in plants discussed at the session included changes in PSII antenna size; variation in the optical transparency of leaves; feedback regulation by photoassimilate export via plasmodesmata; and changes in oxygen reduction in the photosynthetic electron transport chain. The evolutionary significance of the latter changes was noted. In green sulfur bacteria, a novel regulatory mechanism was suggested based on the occurrence of Na⁺-translocating ferredoxin:NAD⁺-oxidoreductase. The importance of the PSII antenna size as a regulatory checkpoint of the photosynthesis could be traced back to the levels of chlorophyll b influencing the lateral mobility within the thylakoid membrane. The critical role in the downregulation of PSII antenna size in response to prolonged high light and many other stresses was assigned to the formation of H₂O₂ signal molecules in the reaction between reduced plastoquinone and superoxide anion radicals. Long-distance electric signals emerged as a novel regulatory mechanism of photosynthesis able to exert systemic regulation. An astonishing diversity of the roles of various isoforms of carbonic anhydrase was revealed including their regulation of ATP synthesis, NPQ (i.e., dissipation of excess light energy into heat), supply of Rubisco with CO₂, and stabilization of the oxygen-evolving complex of PSII. The computational models of several steps of photosynthetic electron transport presented in the session offered a new tool for a search of yet-to-be discovered regulatory mechanisms. Undoubtedly, discussions during the session provided a powerful impetus to this search.