Лаборатория молекулярных основ внутриклеточной регуляции

Институт физиологии растений им. К.А. Тимирязева РАН

127276 Москва, ул. Ботаническая 35

 

 

Victor E. Semenenko

(1932-1998 гг.)
  

Victor E. Semenenko is known in Russia and in other countries as a contributor to the studies of self-regulation of physiological functions in photosynthetic cells. He was also the founder of algal biotechnology in Russia.
His first student scientific paper "On the effect of light starvation on the chloroplasts in leaves of green plants," in which a young researcher observed the disintegration and division of chloroplasts of the alga Selagenella, was published in 19521. After graduation from the University of Kiev (Ukraine), V.E. Semenenko started his research at the Institute of Plant Physiol. (Moscow) under supervision of Professor Nichiporovich. Since that time his research activities were tightly linked with the name of this institution. Research and communication with A. Nichiporovich had a strong influence on the development of basic biological views, and the personality of Victor Semenenko. His PhD thesis was devoted to the study of photosynthetic gas exchange processes. In that work he first discovered the phenomenon light-dependent emission of CO2. The biochemical studies of this phenomenon in other laboratories had later led to the discovery of photorespiration2.
After finishing his PhD thesis in 1958, Victor Semenenko became a leader of a group associated with the Laboratory of photosynthesis. The group was focused on the problem of application of the unicellular phototrophic microorganisms in closed biological for life support systems. The organization of this group, was prompted by the successful beginning of space exploration in those years and the emergence of a new branch of knowledge - Space Biology.
Great success in space exploration in the late 50s and 60s of the XX century gave rise to the optimism, and enthusiasm in scientific community. Even before Gagarin's flight into space, the prospects for long-term space travel, construction of the habitable extraterrestrial stations and orbital complexes had been discussed. Intensively grown algae have been considered as one of the main elements of such stations responsible for the biological life support in space. At that time Victor Semenenko became the head of the Laboratory for algological studies.
First of all, the viability and the level of mutations in Chlorella cells during space flight were studied in 1958. The experiments were conducted on unpiloted satellites. The results did not demonstrate any significant changes in physiological states in populations of algae in the flight experiments3.

Another important step was to examine the compatibility of green unicellular algae and humans in their permanent contact. This problem was solved in the early 60s in the joint experiments with the Institute of Biophysics, Medical Academy of Sciences. A prolonged stay of astronauts in an isolated hermetic cabin, which was connected to the system of gas exchange ran by a photobioreactor with unicellular algae, did not affect the status of the crew and as well as the viability of microalgae4-6.

At the same time, the selection of the most promising forms of life support systems for unicellular algae was conducted that implied optimization of their growth in newly developed closed photobioreactors of various types. As a result, during a 1.5-month continuous experiment, the productivity of Chlorella reached 25-30 liters of oxygen from 1 liter of cell suspension per day. These experiments lead to construction of flat-panel photobioreactors, the reactors with air lifts, turbosorbers, the spray systems for suspension, to the design of distribution of light energy in a suspension with fiber optics7.

The principal condition that determined the possibility of the use of biological life support systems based on algae was high reliability and stability of a system at the level of algae themselves. In 1967, Victor Semenenko together with Lev Tsoglin proposed the autoselection theory for populations of microalgae, which was experimentally verified in 1969-72. This theory eliminated the possibility of deterioration in gas exchange characteristics of the unit. It demonstrated the exclusive ability to improve photosynthetic characteristics and production rates of algae in the course of their long-term continuous cultivation8,9.

Along with the regeneration of the atmosphere, the problem of biological life support system includes the nutrition for the crew - fitness of the biochemical composition of microalgae to the diet ration of human. The regulation of biochemical pathways of the photosynthetic metabolism in microalgae became the major focus of research of Victor Semenenko. Studies in this field had finally resulted in the hypothesis of endogenous regulation of photosynthesis10. These studies led to the selection of algal strains - producers of various compounds and to the development of methods of controlled biosynthesis, which allowed the maintenance of biochemical composition of microalgae under various extreme conditions11,12. The two-phase method for cultivation of algae developed in the 70's, made ​​it possible to perform continuous growth of biomass with a determined biochemical composition without reduction in the photosynthetic activity13-15.

The studies of Victor Semenenko in space biology have laid important foundations of modern biotechnology of microalgae and initiated its development in Russia.

The wide spectrum of scientific interests of Victor Semenenko allowed him to go beyond the practical space biology. In 1971, his group was transformed into a Laboratory of molecular bases of intracellular regulation, and then into the Department of intracellular regulation of biotechnology and photoautotrophic biosynthesis.

All these years, microalgae served to Victor Semenenko as an excellent model for investigation of the principles of self-regulation by virtue of extremely high plasticity of their metabolism16,17. Together with his wife and colleague, Maya G. Vladimirova, he founded The Collection of Microalgae (IPPAS), which became a member of the International Association of Collections. Currently, this is the most representative collection of microalgae in Russia.

The main interests of Viktor Semenenko, as he formulated them, have been focused on self-regulation of physiological processes and metabolism of photoautotrophic cells:
- Elucidation of the physiological responses of the genetic systems of plant cells.
- Investigation of molecular and cellular mechanisms of organization of endogenous regulation of photosynthesis10,18-22.
- Investigation of metabolism and cell cycle of unicellular photoautotrophic organism9,23-26.
Along this way, ​​the most significant discoveries had been made that leaved the unique and bright mark in science. Among Russian scientists of the 20th century, who made a significant contribution to the study of the primary processes of photosynthesis (V.B. Evstigneev, A.A. Krasnovskii), the structure and biosynthesis of chlorophyll (T. Godnev, A. Shlyk), photosynthetic carbon metabolism (A.T. Mokronosov, N.G. Doman, E.N. Kondratyev, A.K. Romanova), the genome of the photosynthetic apparatus (N.M. Sissakian) and photosynthetic productivity (A.A. Nichiporovich), Victor Semenenko holds a special position.

In the early 70's Victor Semenenko turned to the old problem of plant Physiol. on the influence of assimilates (or overfeeding of plants) on photosynthesis in order to uncover the molecular level of these events. To investigate the metabolic regulation of photosynthesis three main questions have been asked: 1) what is the possible nature of the regulatory metabolite or effector; 2) what is the molecular mechanism of its action in the chloroplast; and 3) what is the mechanism of coupling of photo- and metabolic regulation?

Screening among the metabolites, products of photosynthesis, the modified glucose molecules have been used possess biological function, but are limited in utilization. One of such molecules was 2-deoxy-D-glucose (2dDG), which was applied in the studies of the repression of photosynthesis and protein synthesis in the chloroplast. Further detection of light-dependent repressive action of 2dDG revealed close cooperation of metabolic regulation and light regulation in chloroplasts10,19,20,22,27-29,29-37.

In 1982, the inhibitory analysis and chronology of events in chloroplasts revealed that the regulatory effect of glucose is carried out at the level of transcription in chloroplasts22. Later, these findings were confirmed by investigation the transcription of genes for the proteins of the reaction center of photosystem II. Mutagenesis of Chlorella vulgaris led to the production of the regulatory mutants, which were characterized by overproduction of the end-products of photosynthesis32,38,39. Similar studies had been conducted with cells of the cyanobacterium Synechocystis sp. PCC 6803, from which the 2dDG-resistant mutants have been selected 40,41. These approaches (M.V. Zvereva, E.S. Kuptsova, L.A. Shitova, N.V. Lebedeva) helped to demonstrate the participation of glucose in the regulation of transcription of the chloroplast genome and in regulation the photosynthesis at the genetic level36-38,41.

The phenomenon of metabolic regulation of photosynthesis studied in model experiments with non-metabolized glucose analogues was observed in physiological experiments with hyper-accumulation of assimilates in the chloroplast after filling the pool of storage polysaccharides. Transition of photosynthetic cells to specialized biosynthesis is determined by a complex chain of events that are genetically determined. This chain involves the processes of synthesis and induced selective proteolysis of proteins. These observations (G.L. Klyachko-Gurvich, T.S. Rudova) formed the basis for controlled biosynthesis of algal biomass with determined amounts of carbohydrates, lipids, or biologically active compounds 25,42-46,46-50.

In parallel with the study of endogenous regulation of photosynthesis under excess photosynthetic activity, Victor Semenenko developed the research in the area of self-limitation of photosynthesis under CO2 defficiency51-62. Semenenko maintained the hypothesis that low concentration of CO2 in our modern atmosphere is one of global limiting factors forphotosynthesis of algae and of C3 plants. In the early 70's, after the discovery of C4 photosynthesis, it was accepted that the ability to concentrate CO2 in the cell is a distinctive feature of C4 plants, whereas the C3 plants do not possess this ability. At that time many researchers studied the pathways of carbon in C3 plants after its interaction with RuBisCO, whereas the transport of CO2 into the cell was considered as resistance to diffusion of CO2.

However, a number of facts, such as a) discrepancy between the actual affinity of RuBisCo to CO2 and the calculated its concentrations in the stroma; b) the increase in photosynthetic affinity for CO2 during adaptation of cells to a decrease of carbon dioxide in the environment; c) the ability of algae to grow in the absence of CO2 in bicarbonate-containing media – all these facts contradicted with the hypothesis of direct diffusion of CO2 to the centers of carboxylation and showed that substrate supply for the dark reactions of photosynthesis is under genetic control33,63,64.

Already in his first article on this subject (1977) Victor Semenenko proposed and experimentally confirmed the existence of the carbonic anhydrase system in photosynthetic cells, which includes soluble and membrane-associated forms of the enzyme62.

In 1981, based on the detailed studies of the organization of carbonic anhydrase system in different taxonomic groups of algae, its physiological and biochemical properties, regulation of synthesis of different forms of carbonic anhydrase, as well as adaptive reorganizations of their activities, Victor Semenenko and his students and colleagues (N.A. Pronina, Z.M. Ramazanov) presented the original model of the CO2-concentrating mechanism (CCM) in the algae59. This has initiated the interest in this problem by many researchers.

One of the major achievements was the discovery (Semenenko & Ramazanov) of the regulatory role of the oxygenase function of RuBisCO in the induction of a CO2-dependent form of carbonic anhydrase and in regulatory interactions between photosynthesis, photorespiration and nuclear genetic apparatus of plant cells in optimization of carbon nutrition in microalgae. It was shown that glyoxylate, being a product of photorespiration, is the inducer of the synthesis of carbonic anhydrase involved in the transport of Ci into the chloroplast55,59,65,66.

The theoretical works of Victor Semenenko may be supplemented by the hypothesis on the importance of pyrenoid containing RuBisCO and carbonic anhydrase in the concentration, generation, and fixation of CO2 in the chloroplast. Semenenko & Vladimirova have been the first how showed localization of the RuBisCO in the pyrenoid67-69. Later this line of work was developed further by N.A. Pronina70-75.

The discovery in 1988 of carbonic anhydrase in the thylakoid membranes, the kinetic studies of photochemical reactions in chloroplasts in the presence of carbonic anhydrase inhibitors, and in CCM mutants, showed the direct involvement of thylakoid carbonic anhydrase in the control of the Calvin cycle. These data served as a serious argument in favor of the shunting of CCM, which essence is in the transfer of HCO3 into the lumen and in its carbonic-anhydrase-mediated transformation to CO2, which diffuses into the stroma due to the gradient of concentrations51,52,54. The presented model of the mechanism of concentration, generation and fixation of CO2 in the chloroplasts of algae, which takes into account the pH of individual cellular compartments, the selective properties of membranes, intracellular localization of the carbonic anhydrases, RuBisCO, and photosystems, had analyzed in special reviews and articles (S. Miyachi76, J.V. Moroney77, J.A. Raven78, G. Samuelsson79). This model was recognized mostly by all investigators of photosynthesis. The advantage of this model is also in the fact that it induces a range of new directions in research of photosynthesis, in particular, the integration of functions of carbonic anhydrase in photosynthesis with the role of its isozymes in the process of respiration, water photolysis and O2 evolution, that ensure the symmetry of the photosynthetic and respiratory functions of the family of carbonic anhydrases in the plant cell.

The experimental data and the conclusions allowed Victor Semenenko and co-workers to formulate the concept of the functional role of CCM as a complete integrated system, in which the crucial role is played by the compartmentalization, the selective properties of membranes, the proton gradient, location and topology of the carbonic anhydrase and the transmembrane transport of Ci. This concept significantly extends the concept of photosynthetic metabolism.

Cited articles:

  1. Semenenko VE (1952) The effect of starvation onthe light condition of the chloroplasts in leaves of green plants. Proceedings of the Fomin Botanical Garden of Kiev State University. pp. 99-102. (Kiev State University,1952). in Russian.
  2. Semenenko VE (1962) Mechanism of the processes of transition states in photosynthesis. p. 1- 30. in Russian.
  3. Semenenko VE (1958) Apparatus for studying the kinetics of induction period of photosynthesis, carbon dioxide gas analyzer with a differential for thermistors. Sov. Plant Physiol. 5(6): 561-568.
  4. Semenenko VE, Vladimirova MG (1961) Effect of space flight on board the satellite to maintain viability of the culture of Chlorella. Sov. Plant Physiol. 8(6): 743-749.
  5. Semenenko VE, Vladimirova MG (1962) Problems of space biology. Sisakyan NM (ed.), pp. 190-203 ( USSR Academy of Sciences, Moscow). in Russian.
  6. Semenenko VE, Vladimirova MG (1962) Satellites. pp. 56-62 ( USSR Academy of Sciences, Moscow). in Russian.
  7. Ivanov et al. (1967) The biological reactor. (Inventor's Certificate N 201 137, 15.06.1967). BI 17: 171-172, 1967. in Russian.
  8. Tsoglin LN, Semenenko VE Polyakov AK (1967) The theoretical basis of the principle of auto-competitive selection of productive forms of unicellular algae based on mathematical modeling of the dynamics of population growth in multicomponent flow culture. Biophysics 12 (4): 704- 714. in Russian.
  9. Tsoglin LN, Vladimirova MG, Semenenko VE (1970) Mathematical and experimental simulation of autoselection of microalgae in a flow-through culture. Sov. Plant Physiol. 17(6): 1129-1139.
  10. Semenenko VE (1975) Photoregulation of plant metabolism and morphogenesis. pp. 135-157 (Nauka, Moscow). in Russian
  11. Semenenko VE, Vladimirova MG, Orleanskaya OB (1967) The physiological characteristics of Chlorella sp. K at high temperature extremes. I. Uncoupling effect of extreme temperatures on cellular functions of chlorella. Sov. Plant Physiol. 14(4): 612-625.
  12. Semenenko VE Vladimirova MG, Orleanskaya OB, Raikov NI, Kovanova YS (1969) The physiological characteristics of Chlorella sp. K at high temperature extremes. II. Change biosynthesis, ultrastructure and activity of the photosynthetic apparatus of Chlorella in dividing cell function extreme temperatures. Sov. Plant Physiol. 16(2): 210-220.
  13. Bochacher FM, Neimark VM, Semenenko VE, Tsoglin LN (1973) Apparatus for the cultivation of algae. AC 377 030, 1973. Not to be published in open press. Inventor's Certificate. Application N1617441 27.01.1971.
  14. Bochacher FM, Borisenko ON, Otchenashenko IM, Semenenko VE, Tsoglin LN (1971) Setting turbidistatic cultivation of microorganisms. Inventor's Certificate N 326 874 10/22/1971.
  15. Tsoglin LN, Avramova S, Gebov A, Dilov Ch, Semenenko VE (1980) Study of O2 gas exchange and optimization mode cultivation of algae in open settings such as "Šetlík." Sov. Plant Physiol. 27(3): 644-652.
  16. Tsoglin LN, Yevstratov AV, Semenenko VE (1979) The use of microalgae for the biosynthesis of C-compounds. Sov. Plant Physiol. 26 (1): 215-218.
  17. Vladimirova MG, Semenenko VE (1977) The life of plants. pp. 367-376. (Education, Moscow). in Russian.
  18. Semenenko VE, Afanasyev VP (1972) to study the mechanisms of autoregulation of photosynthesis. Reversible 2-deoxy-D-glucose repression effect of the photosynthetic apparatus of the cell. Sov. Plant Physiol. 9(5): 1074-1081.
  19. Semenenko VE (1978) Molecular biology of the endogenous regulation of photosynthesis. Sov. Plant Physiol. 25(5): 903-921.
  20. Kuptsova ES, Semenenko VE (1981) Light-dependent repressive action of glucose analogs in the chloroplast. Sov. Plant Physiol. 28(4): 743-748.
  21. Semenenko VE (1981) Metabolite regulation of chloroplast genome expression and the activity of photosynthetic apparatus. Proceeding of the fifth international congress on photosynthesis. G. Akoyunoglou (ed.) pp. 767-776. (BIS Services, Philadelphia).
  22. Semenenko VE (1982) Physiol. of photosynthesis. (Ed. Nichiporovich AA). pp. 164-187. (Nauka, Moscow). in Russian.
  23. Tsoglin LN, Semenenko VE (1979) Increased productivity and efficiency of photosynthesis by algae control population age structure. Proceedings of Xth All-Union Conference, Kanev, 1979. pp. 294-303. (Naukova Dumka, Kiev). in Russian.
  24. Tsoglin LN, Vladimirova MG, Semenenko VE (1976) Autoselection of microalgal strains in a flowing culture. Proceedings of the XIth Research Symposium, Scientific Coordination Meeting on I-184 of the CMEA. pp. 22-36. (Published by Leningrad State University). in Russian.
  25. Semenenko VE, Vladimirova MG, Tsoglin LN, Tauts MI, Filippovskiy JN, Klyachko-Gurvich GL, Kuznetsov ED, Kovanova ES, Raikov NI (1966) Continuous cultivation of algae: controlled flow, physiological and biochemical characteristics. I) Productivity and efficiency of utilization of radiant energy during prolonged intensive cultivation of Chlorella. In: "Controlled biosynthesis." pp. 75-86. (Nauka, Moscow). in Russian.
  26. Tsoglin LN, Semenenko VE, Bochacher FM, Filippovskiy JN (1966) Device for the controlled flow cultivation of algae with automatic measurement, registration and regulation of the density of the suspension. In: "Controlled biosynthesis." pp. 324-330. (Nauka, Moscow). in Russian.
  27. Klimova LA, Roshchin VV, Zvereva MG, Semenenko VE (1983) Reversible violations of photosynthesis electron transport chain in intact Chlorella cells under the action of the stereochemical analog of glucose. XI All-Union Workshop on the cycle of substances in closed systems. pp. 50-56. (Naukova Dumka, Kiev). in Russian.
  28. Zvereva MG, Klimova LA, Semenenko VE (1980) Repression of rRNA synthesis and activity of the breach of the chloroplast photochemical systems under the action of 2-deoxy-D-glucose and hyper-accumulation of assimilates in Chlorella cells. Sov. Plant Physiol. 27(6): 1218- 1228. in Russian.
  29. Semenenko VE Kuptsova ES, Kasatkina T, Pronina NA, Vladimirova MG, Zvereva MG, Kuznetsova LG (1979) Kinetic characteristics of the reversible repression of protein synthesis and functional activity of the chloroplast stereochemical analogues of glucose. pp. 313-320. In: “The Role of the lower organisms in the circulation of substances in closed ecological systems” (Proceedings of X All-Union Conference, Kanev, 1979, Naukova Dumka, Kiev). in Russian.
  30. Zvereva MG, Shubin LM, Klimova LA, Semenenko VE (1979) Reversible changes in the spectra of low-temperature fluorescence of intact Chlorella cells caused by repression of the photosynthetic apparatus by 2-deoxy-D-glucose. Proc. Acad. Sci. USSR 244: 1244-1247. in Russian.
  31. Semenenko VE, Zvereva, MG (1972) Comparative study of restructuring in the direction of the photobiosynthesis in two strains of Chlorella functions under uncoupling action of extreme temperatures. Sov. Plant Physiol. 19(2): 229- 237. in Russian.
  32. Semenenko VE, Shitova LA, LA Shitova, Rudova TS, Pronina NA (1992) Regulatory 2-deoxy-D-glucose-resistant mutants of Chlorella vulgaris with impaired metabolic system of negative regulation of expression of the chloroplast genome of the end products of photosynthesis. Sov. Plant Physiol. 39(6): 1135-1145.
  33. Semenenko VE, Kasatkina TI, Rudova TS (1976) Reversible inhibition of protein synthesis in fraction I under the influence 2-deoxy-D-glucose. Sov. Plant Physiol. 23(6): 1225-1231.
  34. Kuptsova ES, Semenenko VE (1986) The dependence of the repressive action of glucose analogs in the chloroplast of the spectral composition of light. Sov. Plant Physiol. 33(4): 699-708.
  35. Kuptsova ES, Semenenko VE (1983) The relationship between the structure of glucose analogues and their repressive action in the chloroplast. Sov. Plant Physiol. 30(5): 1006-1014.
  36. Semenenko VE (1988) Photosynthesis and production process. pp. 69-81 (Nauka, Moscow). in Russian.
  37. Semenenko V.E. (1996) Physiological and genetic potentials of microalgae and molecular biology aspects of photoautotrophic biosyntheses biotechnology. TIT Symposium Microalgal Biotechnology: Basics and Applications. pp. 1-8. ( Osaka, Japan).
  38. Shitova LA, Meshcheryakov AB, Semenenko VE (1994) Regulatory mutants of Chlorella c impaired transport system of exogenous glucose into the cell. Sov. Plant Physiol. 41 (2): 223-226.
  39. Semenenko VE, Shitova LA (1991) A method for the selection of regulatory mutants of photosynthetic algae and algae strain Chlorella sp. K – the producer of carbohydrates. Inventor's certificate N1654337. 02/08/1991.
  40. Lebedeva NV, Semenenko VE (2000) Regulation of photosynthesis by glucose and its stereochemical analogue in the cyanobacterium Synechocystis sp. PCC 6803. Russ. J. Plant Physiol. 47(5): 662-667.
  41. Lebedeva NV, Semenenko VE (1992) The 2-deoxy-D-glucose effect on the mRNA levels of psbA, psbD and desA genes in Synechocystis PCC6803. Research in Photosynthesis. Murata N. (ed.), pp. 457-460 (Kluwer Academic Publishers, Dordrecht, The Netherlands).
  42. Yurieva MI, Klyachko-Gurvich GL, Semenenko VE, Temnykh AA (1990) A method of biomass production of the unicellular alga Porphyridium enriched with eicosapentaenoic and arachidonic acid. Inventor's certificate N1609827, 1.08.1990.
  43. Ramazanov ZM, Klyachko-Gurvich GL, Ksenofontov AL, Semenenko VE (1988) Effect of suboptimal temperature on the content of b-carotene and lipids in halophilic alga Dunaliella salina. Sov. Plant Physiol. 35(5): 864-872.
  44. Klyachko-Gurvich GL, Tauts MI, Semenenko VE (1985) Microorganisms in artificial ecosystems. pp. 53-61. (Nauka, Novosibirsk). in Russian.
  45. Klyachko-Gurvich GL, Semenov AN, Semenenko VE (1980) Lipid metabolism in the chloroplasts of Chlorella cells to adapt to lower light conditions. Sov. Plant Physiol. 27(2): 370-379.
  46. Klyachko-Gurvich GL, Rudova TS, Kovanova ES, Semenenko VE (1973) Effect of imidazole on the exchange of fatty acids in the restoration of Chlorella cells after nitrogen starvation. Sov. Plant Physiol. 20(3): 326-331.
  47. Klyachko-Gurvich GL, Semenenko VE (1966) Biology of autotrophic organisms. pp. 154-159. (Moscow State University, Moscow, 1966). In Russian.
  48. Klyachko-Gurvich GL, Semenenko VE (1965) Some physiological and biochemical aspects aimed to provide valuable metabolites and substances under conditions of intensive culture of algae. (The study of intensive algal culture). pp. 143-151. Prague. Proceedings of the IIId coordination meeting of the CMEA. In Russian.
  49. Semenenko VE, Ramazanov ZM, Rudova TS, Abdullaev AA (1987) A method for cultivation of microalgae Dunaliella salina. Inventor's certificate N1513911. 08.06.1989. In Russian.
  50. Semenenko VE, Rudova TS (1975) Effect of cycloheximide on the biosynthesis process of restructuring the cells of Chlorella caused by nitrogen starvation. Sov. Plant Physiol. 22(5): 958-965.
  51. Furnadzhieva S, Pronina NA, Andreeva R, Petkov G, Semenenko VE (2001) Involvement of carbonic anhydrase in the bicarbonate ion assimilation by cells of Chlorella and Scenedesmus. Russ. J. Plant Physiol. 37(1): 22-30.
  52. Pronina NA, Zhila NM, Semenenko VE (1999) Two forms of carbonic anhydrase in the cells of Dunaliella salina; isolation and properties. Sov. Plant Physiol. 46(1): 62-68.
  53. Pronina NA, Semenenko VE (1991) Molecular and cellular organization of CO2 concentrating mechanisms in photoautotrophic cells of algae. Algologia 1(2): 80-92.
  54. Pronina NA, Semenenko VE (1988) Localization of carbonic anhydrase bound to membranes of cells of Chlorella. Sov. Plant Physiol. 35(1): 51-61.
  55. Ramazanov ZM, N. Pronina NA, Semenenko VE (1984) On the oxygen dependence of the induction of synthesis of CO2-dependent soluble form of carbonic anhydrase in Chlorella cells. Sov. Plant Physiol. 31(3): 448-455.
  56. Kasatkina TI, Pronina NA, Semenenko VE (1984) Quantitative isolation, fractionation and characterization of ribulose-1,5-bisphosphatcarboxylase from Chlorella cells. Sov. Plant Physiol. 31(1): 130-140.
  57. Abramova S, Pronina NA, Semenenko V, Georgiev D, Peshev IS (1984) Carbonic anhysdase activity and assimilation of bicarbonate ion cells Chlorella and Scenedesmus. Hydrobiologija 20: 8-15.
  58. Pronina NA, Semenenko VE (1984) Localization of membrane-bound and soluble forms of carbonic anhydrase in Chlorella cells. Sov. Plant Physiol. 31(2): 241-251.
  59. Pronina NA, Ramazanov ZM, Semenenko VE (1981) The dependence of the activity of the carbonic anhydrase activity of Chlorella cells on the concentration of CO2. Sov. Plant Physiol. 28(3): 494-502.
  60. Pronina NA, Abramova S, Georgiev D, Semenenko VE (1981) Dynamics of carbonic anhydrase activity of Chlorella and Scenedesmus during adaptation of cells to high light intensity and low concentrations of CO2. Sov. Plant Physiol. 28(1): 43-52.
  61. Semenenko VE, Abramova S, Georgiev D, Pronina NA (1979) On the light dependence of carbonic anhydrase activity of Chlorella and Scenedesmus cells. Sov. Plant Physiol. 26(5): 1069-1075.
  62. Semenenko VE, Abramova S, Georgiev D, Pronina NA (1977) Comparative study of carbonic anhydrase activity and localization in cells of Chlorella and Scenedesmus. Sov. Plant Physiol. 24(5): 1055-1059.
  63. Kasatkina TI, Vedeneyev AN, Semenenko VE (1985) Regulation of the synthesis of ribulose-1,5-bisphosphate carboxylase and its subunits in the cells. In: "Microorganisms in artificial ecosystems." p. 97-102. (Nauka, Novosibirsk). In Russian.
  64. Kasatkina TI, Tikhonov NG, Vladimirova MG, Volodarsky AD, Semenenko VE (1974) Study of the antigenic structure of two strains of Chlorella, with a variety of physiological and biochemical properties. Sov. Plant Physiol. 21(4): 752-755.
  65. Ramazanov ZM, Semenenko VE (1988) The dependence of the CO2-dependent form of carbonic anhydrase on the light intensity and photosynthesis. Sov. Plant Physiol. 35(3): 438-443.
  66. Ramazanov ZM, Semenenko VE (1986) The participation of products of photorespiration in CO2-dependent induction of a form of carbonic anhydrase. Sov. Plant Physiol. 33(5): 864-872.
  67. Markelova AG, Vladimirova MG, Semenenko VE (1990) Ultrastructural localization of RuBisCO in algae cells. Sov. Plant Physiol. 37(5): 907-911.
  68. Markelova AG, Shapiguzov YM, Vladimirova MG, Semenenko VE (1985) Quantitative estimation of immunofluorescence of pyrenoid as a giant carboxysome-containing compartment. In: "Microorganisms in artificial ecosystems." pp. 35-41. (Nauka, Novosibirsk). In Russian.
  69. Vladimirova MG, Markelova AG, Semenenko VE (1982) Identification of the localization of RuBisCO in the pyrenoid of a unicellular algae by immunocytochemical method. Sov. Plant Physiol. 29(5): 941-950.
  70. Dudoladova MV, Kupriyanova EV, Markelova AG, Sinetova MP, Allakhverdiev SI, Pronina NA (2007) The thylakoid carbonic anhydrase associated with photosystem II is the component of inorganic carbon accumulating system in cells of halo-and alkaliphilic cyanobacterium Rhabdoderma lineare. Biochim. Biophys. Acta 1767: 616-623.
  71. Kupriyanova E, Villarejo A, Markelova A, Gerasimenko L, Zavarzin G, Samuelsson G, Los DA, Pronina NA (2007) Extracellular carbonic anhydrases of the stromatolite-forming cyanobacterium Microcoleus chthonoplastes. Microbiology SGM 153: 1149-1156.
  72. Markelova AG, Sinetova MA, Kupriyanova EV, Pronina NA (2009) Distribution and functional role of carbonic anhydrase Cah3 associated with thylakoid membranes in the chloroplast and pyrenoid of Chlamydomonas reinhardtii. Russ. J. Plant Physiol. 56 (6): 761-798.
  73. Kupriyanova EV, Pronina NA (2011) Carbonic anhydrase: Enzyme that has transformed the biosphere. Russ. J. Plant Physiol. 58 (2): 197-209.
  74. Kupriyanova EV, Sinetova MA, Markelova AG, Allakhverdiev SI, Los DA, Pronina NA (2011) Extracellular β-class carbonic anhydrase of the alkaliphilic cyanobacterium Microcoleus chthonoplastes. J. Photochem. Photobiol. B: Biol. 103: 78-86.
  75. Sinetova MA, Kupriyanova EV, Markelova AG, Allakhverdiev SI, Pronina NA (2012) Identification and functional role of the carbonic anhydrase Cah3 in thylakoid membranes of pyrenoid of Chlamydomonas reinhardtii. Biochim. Biophys. Acta - in press.
  76. Miyachi S, Iwasaki I, Shiraiwa Y (2003) Historical perspective on microalgal and cyanobacterial acclimation to low-and extremely high-CO2 conditions. Photosynthesis Research 77: 139-153.
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