The study of plant adaptation to oxygen deficiency in Saint Petersburg University

Tamara Chirkova; Vladislav Yemelyanov

doi:10.21638/spbu03.2018.104

Authors

Tamara Chirkova Department of Plant Physiology and Biochemistry, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0002-2315-0816
Vladislav Yemelyanov Department of Genetics and Biotechnology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0003-2323-5235

DOI:

https://doi.org/10.21638/spbu03.2018.104

Abstract

The first studies on plant anaerobiosis started at the Department of Plant Physiology at St. Petersburg University in the beginning of the XXth century, but interest in this subject became most intensive during the investigations of the ecological plant physiology group under the supervision of Prof. T. V. Chirkova. Their first step was focused on the mechanisms of transport of gases from the aerated aboveground part of the plant to the flooded root system. Further interest shifted towards clarifying the biochemistry of respiratory metabolism, pathways of reoxidation of the reduced cofactors, and protein and lipid metabolism of plants under anoxic conditions. The group’s studies have always distinguished the comparative approach, in which the changes taking place in plants differing in resistance to oxygen deficiency were analyzed. In many ways, this research was pioneering and was recognized throughout the world. For the first time the possibility of hydrogen peroxide formation in plants under total anoxia was demonstrated. The role of cell membranes in adaptation processes was revealed. Pioneering investigations distinguished the features of photosynthesis in an oxygen-free environment and the work of an antioxidant system under conditions of anoxia and post-anoxic oxidative effects. Now, the plant ecophysiology group of the Department of Plant Physiology and Biochemistry of St. Petersburg State University concentrates on the mechanisms of anaerobic signal transduction and reveals how plant hormones regulate adaptation to anoxic and post-anoxic stresses.

Keywords:

oxygen deficiency, post-anoxic stress, plant respiration, fermentation, protein and lipid metabolism, reactive oxygen species, antioxidants

Downloads

Download data is not yet available.

References

Armstrong, W., Brändle, R., and Jackson, M. B. 1994. Mechanisms of flood tolerance in plants. Acta Botanica Neerlandica 43(4):307–358. https://doi.org/10.1111/j.1438–8677.1994.tb00756.x" target="_blank">https://doi.org/10.1111/j.1438–8677.1994.tb00756.x

Bailey-Serres, J. and Voesenek, L. A. C. J. 2008. Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59:313–339. https://doi.org/10.1146/annurev.arplant.59.032607.092752" target="_blank">https://doi.org/10.1146/annurev.arplant.59.032607.092752

Banti, V., Giuntoli, B., Gonzali, S., Loreti, E., Magneschi, L., Novi, G., Paparelli, E., Parlanti, S., Pucciariello, C., Santaniello, A., and Perata, P. 2013. Low oxygen response mechanisms in green organisms. International Journal of Molecular Sciences 14(3):4734–4761. https://doi.org/10.3390/ijms14034734" target="_blank">https://doi.org/10.3390/ijms14034734

Belonogova, V. A., and Chirkova, T. V. 1994. Rol’ nitratnogo dykhaniya v adaptatsii rasteniy amaranta k usloviyam zatopleniya [The role of nitrate respiration in adaptation of amaranth plants to flooding conditions]. Biological Communications (3):99–105.

Belonogova, V. A., and Chirkova, T. V. 1995. Vliyanie zatopleniya na metabolizm nitratov v tkanyakh rasteniy pshenitsy i ovsa, razlichayushchikhsya po ustoychivosti k nedostatku kisloroda [Influence of flooding on the metabolism of nitrates in the tissues of wheat and oats, differing in resistance to lack of oxygen]. Agrokhimiya [Agricultural Chemistry] (6):38–46.

Belonogova, V. A., Chirkova, T. V., and Zabruskov, V. G. 1995. Nitratnoe dykhanie i ustoychivost’ amaranta argentinskogo k nedostatku kisloroda pri pereuvlazhnenii [Nitrate respiration and the resistance of Amaranthus edulus to oxygen deficiency under flooding]. Biological Communications (4):106–110.

Blokhina, O. B., Chirkova, T. V., and Fagerstedt, K. V. 2001. Anoxic stress leads to hydrogen peroxide formation in plant cells. Journal of Experimental Botany 52(359):1179–1190. https://doi.org/10.1093/jexbot/52.359.1179" target="_blank">https://doi.org/10.1093/jexbot/52.359.1179

Blokhina, O. B., Fagerstedt, K. V., and Chirkova, T. V. 1999. Relationships between lipid peroxidation and anoxia tolerance in a range of species during post-anoxic reaeration. Physiologia Plantarum 105(4):625–632. https://doi.org/10.1034/j.1399-3054.1999.105405.x" target="_blank">https://doi.org/10.1034/j.1399-3054.1999.105405.x

Blokhina, O. B., Virolainen, E., Fagerstedt, K. V., Hoikkala, A., Wähälä, K., and Chirkova, T. V. 2000. Antioxidant status of anoxia-tolerant and -intolerant plant species under anoxia and reaeration. Physiologia Plantarum 109(4):396–403. https://doi.org/10.1034/j.1399-3054.2000.100405.x" target="_blank">https://doi.org/10.1034/j.1399-3054.2000.100405.x

Blyudzin, Yu.A., Barskiy, I. E., Chirkova, T. V., and Sokolova, G. P. 1986. Zhirnye kisloty fosfolipidov mitokhondrial’noy i mikrosomal’noy fraktsiy korney prorostkov pshenitsy i risa [Phospholipid fatty acids of mitochondrial and microsomal fractions of roots of wheat and rice seedlings]. Biological Communications (2):85–89.

Blyudzin, Yu.A., Hoang, K. L., and Chirkova, T. V. 1980. Zhirnye kisloty fosfolipidov gomogenata i mitokhondriy korney prorostkov pshenitsy i risa [Phospholipid fatty acids of the homogenate and mitochondria of the roots of wheat and rice seedlings]. Biological Communications (3):92–97.

Chen, Y., Chen, X., Wang, H., Bao, Y., and Zhang, W. 2014. Examination of the leaf proteome during flooding stress and the induction of programmed cell death in maize. Proteome Science 12:33. https://doi.org/10.1186/1477-5956-12-33" target="_blank">https://doi.org/10.1186/1477-5956-12-33

Chirkova, T. V. 1964. Dykhanie korney rasteniy v usloviyakh razlichnoy aeratsii [Respiration of plant roots under different aeration]. Biological Communications (2):127–130.

Chirkova, T. V. 1968a. Puti obespecheniya kornevykh sistem kislorodom [The delivery of additional oxygen to root systems]. Sel’skokhozyaystvennaya Biologiya [Agricultural Вiology] 3(3):350–355.

Chirkova, T. V. 1968b. Osobennosti snabzheniya kislorodom korney nekotorykh drevesnykh rasteniy, pomeshchennykh v anaerobnye usloviya [Pecularities of oxygen supply to woody plant roots subjected to anaerobic conditions]. Fiziologiya Rasteniy [Soviet Plant Physiology] 15(3):565–568.

Chirkova, T. V. 1971. Rol’ nitratnogo dykhaniya korney v zhiznedeyatel’nosti nekotorykh drevesnykh rasteniy v usloviyakh vremennogo anaerobioza [The role of nitrate respiration of roots in the survival of some woody plants under conditions of temporary anaerobiosis]. Biological Communications (4):118–124.

Chirkova, T. V. 1973. Rol’ anaerobnogo dykhaniya v prisposoblenii nekotorykh drevesnykh rasteniy k vremennomu anaerobiozu [The role of anaerobic respiration in the adaptation of some woody plants to temporary anaerobiosis]. Biological Communications (1):88–95.

Chirkova, T. V. 1975. Metabolizm etanola i laktata v tkanyakh drevesnykh rasteniy, razlichayushchikhsya po ustoychivosti k nedostatku kisloroda [Metabolism of ethanol and lactate in the tissues of trees with different resistance to oxygen deficiency]. Fiziologiya Rasteniy [Soviet Plant Physiology] 22(5):952–957.

Chirkova, T. V. 1978. Some regulatory mechanisms of plant adaptation to temporal anaerobiosis; pp. 137–155 in D. D. Hook, R. M. M. Crawford (eds.), Plant life in anaerobic environments. Ann Arbor Science Publishers Inc., Ann Arbor, Michigan, USA.

Chirkova, T. V. 1983. Rol’ kletochnykh membran v ustoychivosti rasteniy k gipo- i anoksii [The role of cell membranes in plant resistance to hypo- and anoxia]. Uspekhi sovremennoy biologii 95(1):44–56.

Chirkova, T. V. 1988a. O putyakh prisposobleniya rasteniy k gipoksii i anoksii [On the pathways of plant adaptation to hypoxia and anoxia]. Fiziologiya Rasteniy [Soviet Plant Physiology] 35(2):393–411.

Chirkova, T. V. 1988b. Puti adaptatsii rasteniy k gipoksii i anoksii [Pathways of plant adaptation to hypoxia and anoxia]. Leningrad University Press, Leningrad.

Chirkova, T. V. 1998. Rastenie i anaerobioz [Plant and anaerobiosis]. Biological Communications (2):41–52.

Chirkova, T. V. 2002. Fiziologicheskie osnovy ustoychivosti rasteniy. [Physiological basis of plant resistance]. 244 pp. Izdatelstvo Sankt-Peterburgskogo Universiteta, Saint Petersburg

Chirkova, T. V., and Benko, G. N. 1973. Znachenie nitratov v dykhanii korney rasteniy razlichnykh ekologicheskikh grupp v usloviyakh vremennogo anaerobioza [The role of nitrates in the respiration of roots in plants of different ecological groups under the conditions of temporary anaerobiosis]. Sel’skokhozyaystvennaya Biologiya [Agricultural Вiology] 8(2):258–262.

Chirkova, T. V., and Blokhina, O. B. 1991. Vliyanie anoksii na uroven’ endogennogo perekisnogo okisleniya lipidov v kornyakh rasteniy, razlichayushchikhsya po ustoychivosti k nedostatku kisloroda [Effect of anoxia on the level of endogenous lipid peroxidation in roots of plants, differing in resistance to lack of oxygen]. Biological Communications (4):85–90.

Chirkova, T. V., and Gobedzhishvili, L. O. 1993. Perekisnoe okislenie lipidov i zashchitnaya rol’ α-tokoferolatsetata (vitamina E) v list’yakh prorostkov pshenitsy i risa v usloviyakh aeratsii i anoksii [Lipid peroxidation and protective role of α-tocopherol (vitamin E) in leaves of wheat and rice seedlings under normoxic and anoxic conditions]. Biological Communications (1):111–118.

Chirkova, T. V., and Grevnina, G. S. 1982. Vliyanie anaerobnykh usloviy na funktsionirovanie glioksilatnogo tsikla v prorostkakh pshenitsy i risa [Influence of anaerobic conditions on the glyoxylate cycle in seedlings of wheat and rice]. Biological Communications (2):73–78.

Chirkova, T. V., and Gutman, T. S. 1972. O fiziologicheskoy roli chechevichek vetvey ivy i topolya v usloviyakh kornevogo anaerobioza [Physiological role of branch lenticels of willow and poplar under conditions of root anaerobiosis]. Fiziologiya Rasteniy [Soviet Plant Physiology] 19(2):352–359.

Chirkova, T. V., and Hoang, K. L. 1981. Elektroforeticheskie spektry tsitoplazmaticheskikh i mitokhondrial’nykh belkov korney pshenitsy i risa v usloviyakh anaerobioza [Electrophoretic patterns of cytoplasmic and mitochondrial proteins in wheat and rice roots under anaerobiosis]. Fiziologiya Rasteniy [Soviet Plant Physiology] 28(1):136–143.

Chirkova, T. V., and Karpenko, L. A. 1981. Pogloshchenie ksiloroda i redoks-sostoyanie flavinovykh i piridinovykh nukleotidov korney pshenitsy i risa pod vliyaniem ingibitorov transporta elektronov v usloviyakh aeratsii i posle deystviya anaerobioza [Oxygen uptake and redox state of flavin and pyridine nucleotides in roots of wheat and rice treated with inhibitors of electron transport under conditions of aeration and after anaerobiosis]. Biological Communications (1):89–96.

Chirkova, T. V., and Khazova, I. V. 1974. Sootnoshenie putey okisleniya glyukozy pri razlichnom obespechenii rasteniy kislorodom [Ratio of glucose oxidation pathways in plants under different oxygen supply]. Biological Communications (4):111–117.

Chirkova, T. V., and Kovalenko, L. A. 1982. O vozmozhnosti funktsionirovaniya tsianidrezistentnogo dykhaniya v kornyakh pshenitsy i risa posle anaerobnogo vozdeystviya [On the possibility of functioning of cyanide-resistant respiration in the roots of wheat and rice after anaerobic exposure]. Biological Communications (1):74–81.

Chirkova, T. V., and Nastinova, G. E. 1975a. O reparatornoy sposobnosti dykhaniya korney prorostkov pshenitsy i risa posle vozdeystviya usloviy anaerobioza [On the respiratory ability of the roots of wheat and rice seedlings after exposure to anaerobiosis]. Biological Communications (1):104–107.

Chirkova, T. V., and Nastinova, G. E. 1975b. O putyakh okisleniya glyukozy v kornyakh prorostkov pshenitsy i risa v anaerobnykh usloviyakh [On ways of glucose oxidation in roots of wheat and rice seedlings under anaerobic conditions]. Fiziologiya i biokhimiya kul’turnykh rasteniy 7(3):270–274.

Chirkova, T. V., and Nastinova, G. E. 1977. Osobennosti metabolizma C¹⁴-glyukozy v kornyakh prorostkov pshenitsy i risa v razlichnykh usloviyakh aeratsii [Metabolism of C¹⁴-glucose in the roots of wheat and rice seedlings under various conditions of aeration]. Fiziologiya Rasteniy [Soviet Plant Physiology] 24(2):291–297.

Chirkova, T. V., and Petrova, V. N. 1971. Dykhanie i obmen organicheskikh kislot ivy i topolya v zavisimosti ot razlichnykh usloviy aeratsii [Respiration and organic acid metabolism of willow and poplar depending on different aeration conditions]. Biological Communications (1):98–106.

Chirkova, T. V., and Semenova, I. N. 1979. Vliyanie etanola na zhiznesposobnost’ rasteniy, razlichayushchikhsya po ustoychivosti k kislorodnomu defitsitu, i soderzhanie v ikh kornyakh belka [Effect of ethanol on viability of plants differing in resistance to oxygen deficiency and on protein content in their roots]. Fiziologiya i biokhimiya kul’turnykh rasteniy 11(1):18–23.

Chirkova, T. V., and Sokolovskaya, E. L. 1976. K voprosu o prichinakh vozrastaniya aktivnosti peroksidazy v kornyakh rasteniy v usloviyakh ogranichennoy aeratsii [To the question of the causes of increase in peroxidase activity in the roots of plants under limited aeration]. Biological Communications (4):123–129.

Chirkova, T. V., and Soldatenkov, S. V. 1965. Puti peredvizheniya kisloroda iz list’ev v korni, nakhodyashchiesya v anaerobnykh usloviyakh [Pathways of movement of oxygen from leaves to roots kept under anaerobic conditions]. Fiziologiya Rasteniy [Soviet Plant Physiology] 12(2):216–225.

Chirkova, T. V., and Voitsekovskaya, S. A. 1999a. Induced synthesis of non-histone chromatin proteins under anoxia. Russian Journal of Plant Physiology 46(4):544–550.

Chirkova, T. V., and Voitsekovskaya, S. A. 1999b. Sintez belka v rasteniyakh v usloviyakh gipo- i anoksii [Plant protein synthesis under hypoxia and anoxia]. Uspekhi Sovremennoy Biologii 119(2):178–189.

Chirkova, T. V., and Zhukova, T. M. 1987. Ob osobennostyakh i roli glikoliza v ustoychivosti rasteniy k anaerobnomu vozdeystviyu [The peculiarities and role of glycolysis in plant resistance to anaerobiosis]. Biological Communications (4):61–68.

Chirkova, T. V., Barzhinkova, Z. I., and Hoang, K. L. 1980. Vliyanie etanola na sukhoy i syroy ves i rost korney prorostkov pshenitsy i risa v zavisimost’ ot obespecheniya ikh kislorodom [Effect of ethanol on dry and fresh weight and root growth of wheat and rice seedlings in relation to their oxygen supply]. Biological Communications (1):103–108.

Chirkova, T. V., Dragunova, E. V., and Burgova, M. P. 1977. Issledovanie in vivo redoks-reaktsiy flavoproteidov i piridinnukleotidov korney rasteniy, razlichayushchikhsya po ustoychivosti k nedostatku kisloroda [Redox reactions of flavoproteins and pyridine nucleotides from roots of plants different in their resistance to oxygen deficiency studied in vivo]. Fiziologiya Rasteniy [Soviet Plant Physiology] 24(1):126–131.

Chirkova, T. V., Hoang, K. L., and Blyudzin, Yu. A. 1981. Vliyanie usloviy anaerobioza na zhirnokislotnyy sostav fosfoliidov korney pshenitsy i risa [Effect of anaerobic conditions on fatty acid composition of wheat and rice root phospholipids]. Fiziologiya Rasteniy [Soviet Plant Physiology] 28(2):358–366.

Chirkova, T. V., Hoang, K. L., and Sinyutina, N. F. 1980. Vozdeystvie etanola na lipidnyy obmen korney prorostkov pshenitsy i risa v razlichnykh usloviyakh gazovogo rezhima [Ethanol effect on lipid metabolism in wheat and rice seedling roots under various gas conditions]. Fiziologiya i biokhimiya kul’turnykh rasteniy 12(1):24–28.

Chirkova, T. V., Karpenko, M. E., and Chernyaeva, E. V. 1992. Vliyanie anaerobioza na pogloshchenie ionov kornyami prorostkov pshenitsy i risa [The effect of anaerobiosis on the ion uptake by the roots of wheat and rice seedlings]. Biological Communications (4):73–78.

Chirkova, T. V., Khazova, I. V., and Astafurova, T. P. 1974. K voprosu o metabolicheskoy regulyatsii prisposobleniya rasteniy k usloviyam vremennogo anaerobioza [On metabolic regulation of plant adaptation to temporal anaerobiosis]. Fiziologiya Rasteniy [Soviet Plant Physiology] 21(1):102–107.

Chirkova, T. V., Nastinova, G. E., and Semenova, I. N. 1978. Puti detoksikatsii produktov anaerobnogo obmena v kornyakh rasteniy, razlichayushchikhsya po ustoychivosti k kislorodnomu defitsitu [Pathways of the anaerobic metabolism products detoxification in roots of plants differing in resistance to oxygen deficiency]. Fiziologiya i biokhimiya kul’turnykh rasteniy 10(5):469–475.

Chirkova, T. V., Nastinova, G. E., and Zhukova, T. M. 1978. Vliyanie ingibitorov sinteza belka na soderzhanie belka i aktivnost’ alkogol’- i laktatdegidrogenaz v kornyakh pshenitsy i risa v raznykh usloviyakh aeratsii [The effect of protein synthesis inhibitors on the protein content and the activity of alcohol and lactate dehydrogenases in wheat and rice roots under different aeration conditions]. Biological Communications (2):120–126.

Chirkova, T. V., Novitskaya, L. O., and Blokhina, O. B. 1998. Lipid peroxidation and antioxidant systems under anoxia in plants differing in their tolerance to oxygen deficiency. Russian Journal of Plant Physiology 45(1):55–62.

Chirkova, T. V., Sokolovskaya, E. L., and Khazova, I. V. 1973. Aktivnost’ i izofermentnyy sostav peroksidazy korney rasteniy v zavisimosti ot usloviy vremennogo anaerobioza [Effect of temporal anaerobiosis on the activity and isoenzyme composition of peroxidase in plant roots]. Fiziologiya Rasteniy [Soviet Plant Physiology] 20(6):1236–1241.

Chirkova, T. V., Surodeeva, E. K., and Semenova, L. L. 1986. Vliyanie anaerobioza na sostav negistonovykh belkov khromatina prorostkov pshenitsy i risa [Influence of anaerobiosis on the composition of non-histone proteins in wheat and rice seedling chromatin]. Fiziologiya Rasteniy [Soviet Plant Physiology] 33(5):979–986.

Chirkova, T. V., Zhukova, T. M., and Goncharova, N. N. 1991a. Osobennosti pronitsaemosti membran korney prorostkov pshenitsy i risa v usloviyakh anaerobioza [Peculiarities of membrane permeability of wheat and rice seedling roots under anaerobic condition]. Fiziologiya i biokhimiya kul’turnykh rasteniy 23(6):541–546.

Chirkova, T. V., Zhukova, T. M., and Goncharova, N. N. 1991b. Sposob opredeleniya ustoychivosti rasteniy k nedostatku kisloroda [A method for defining plant tolerance to oxygen deficiency]. Fiziologiya Rasteniy [Soviet Plant Physiology] 38(2):359–364.

Chirkova, T. V., Zhukova, T. M., and Ivanova, E. A. 1984. Aktivnost’ adenilatkinazy v kornyakh prorostkov pshenitsy i risa v usloviyakh aeratsii i posle anaerobnogo vozdeystviya [Activity of adenylate kinase in roots of wheat and rice seedlings under conditions of aeration and after anaerobic action]. Fiziologiya i biokhimiya kul’turnykh rasteniy 16(4):329–335.

Chirkova, T. V., Barkova, I. G., Barzhinkova, Z. I., and Magomedov, I. M. 1985. Dikarbonovye organicheskie kisloty korney pshenitsy i risa v usloviyakh aeratsii i anaerobioza [Dicarboxylic organic acids in the roots of wheat and rice under aeration and anaerobiosis]. Biological Communications (4):48–56.

Chirkova, T. V., Barzhinkova, Z. I., Barkova, I. G., and Magomedov, I. M. 1984. Malatdegidrogenaza korney pshenitsy i risa v usloviyakh aeratsii i posle anaerobnogo vozdeystviya [Malate dehydrogenase in the roots of wheat and rice under aeration and after anaerobic action]. Biological Communications (4):59–68.

Chirkova, T. V., Gobedzhishvili, L. O., Hakala, K.-L., and Sinyutina, N. F. 1991a. Vliyanie anaerobioza na metabolizm fosfolipidov khloroplastov prorostkov pshenitsy i risa [Influence of anaerobiosis on the metabolism of phospholipids in chloroplasts of wheat and rice seedlings]. Biological Communications (2):77–82.

Chirkova, T. V., Gobedzhishvili, L. O., Hakala, K.-L., and Sinyutina, N. F. 1991b. Vliyanie anaerobioza i temnoty na metabolizm galaktolipidov khloroplastov prorostkov pshenitsy i risa [Effect of anaerobiosis and darkness on the metabolism of galactolipid in chloroplasts of wheat and rice seedlings]. Biological Communications (3):88–96.

Chirkova, T. V., Novitskaya, L. O., Walter, G., and Leffer, S. 1995. Vliyanie anaerobioza i dlitel’noy temnoty na soderzhanie belka v list’yakh prorostkov pshenitsy i risa [The influence of anaerobiosis and long darkening upon the protein content in the leaves of wheat and rice seedlings]. Biological Communications (3):96–103.

Chirkova, T. V., Saakov, V. S., Semenova, A. V., and Avdeeva, A. V. 1993. The effect of anoxia on the structural and biochemical properties of mitochondrial proteins in the roots of wheat and rice seedlings. Russian Journal of Plant Physiology 40(4):563–567.

Chirkova, T. V., Sinyutina, N. F., Smetannikova, S. V., and Krynkina, E. N. 1989. Vliyanie anoksii na vklyuchenie 1-¹⁴C-atsetata v fosfolipidy mitokhondriy i mikrosom korney pshenitsy i risa [Effect of anoxia on the incorporation of 1-¹⁴C-acetate into phospholipids of mitochondria and microsomes in roots of wheat and rice]. Biological Communications (3):76–82.

Chirkova, T. V., Verzilin, N. N., Barzhinkova, Z. I., and Petryaevskaya, T. G. 1981. Vliyanie usloviy anaerobioza na sdvigi pH v kornyakh pshenitsy i risa [Effect of anaerobic conditions on pH shifts in wheat and rice roots]. Fiziologiya i biokhimiya kul’turnykh rasteniy 13(6):587–593.

Chirkova, T. V., Walter, G., Leffer, S., and Novitskaya, L. O. 1995. Chloroplasts and mitochondria in the leaves of wheat and rice seedlings exposed to anoxia and longterm darkness: some characteristics of organelle state. Russian Journal of Plant Physiology 42(3):321–329.

Chirkova, T. V., Zhukova, T. M., Goncharova, N. N., and Belonogova, V. A. 1991. Opredelenie stepeni pronitsaemosti membran kak sposob diagnostiki rasteniy na ustoychivost’ k nedostatku kisloroda [Determination of the membrane permeability level as the method of plant diagnostic for resistance to oxygen dificiency]. Fiziologiya i biokhimiya kul’turnykh rasteniy 23(1):68–75.

Chirkova, T. V., Sinyutina, N. F., Blyudzin, Yu.A., Barsky, I. E., and Smetannikova, S. V. 1989. Zhirnye kisloty fosfolipidov mitokhondriy i mikrosom korney prorostkov pshenitsy i risa pri aeratsii i anaerobioze [Phospholipid fatty acids of root mitochondria and microsomes from rice and wheat seedlings exposed to aeration or anaerobiosis]. Fiziologiya Rasteniy [Soviet Plant Physiology] 36(1):126–134.

Crawford, R. M. M. 1978. Metabolic adaptation to anoxia; pp. 119–136 in D. D. Hook, R. M. M. Crawford (eds.), Plant life in anaerobic environments. Ann Arbor Science Publishers Inc., Ann Arbor, Michigan, USA.

Crawford, R. M. M. 1989. Studies in plant survival. Ecological case histories of plant adaptation to adversity; 296p. in D. J. Anderson, P. Greic-Smith, F. A. Pitelka (eds.), Studies in ecology. Vol. 11. Blackwell Scientific Publications, Oxford — London — Edinburgh — Boston — Palo Alto — Melbourne.

Crawford, R. M. M., and Braendle, R. 1996. Oxygen deprivation stress in a changing environment. Journal of Experimental Botany 47(295):145–159. https://doi.org/10.1093/jxb/47.2.145" target="_blank">https://doi.org/10.1093/jxb/47.2.145

Dennis, E. S., Dolferus, R., Ellis, M., Rahman, M., Wu, Y., Hoeren, F. U., Grover, A., Ismond, K. P., Good, A. G., and Peacock, W. J. 2000. Molecular strategies for improving waterlogging tolerance in plants. Journal of Experimental Botany 51(342):89–97. https://doi.org/10.1093/jexbot/51.342.89" target="_blank">https://doi.org/10.1093/jexbot/51.342.89

Drew, M. C. 1997. Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annual Review of Plant Physiology and Plant Molecular Biology 48:223–250. https://doi.org/10.1146/annurev.arplant.48.1.223" target="_blank">https://doi.org/10.1146/annurev.arplant.48.1.223

Emel’yanov, V. V., Kirchikhina, N. A., Lastochkin, V. V., and Chirkova, T. V. 2003. Hormonal status in wheat and rice seedlings under anoxia. Russian Journal of Plant Physiology 50(6):827–834. https://doi.org/10.1023/B:RUPP.0000003282.26789.6b" target="_blank">https://doi.org/10.1023/B:RUPP.0000003282.26789.6b

Fukao, T., and Bailey-Serres, J. 2008. Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. Proceedings of the National Academy of Sciences of USA 105(43):16814–16819. https://doi.org/10.1073/pnas.0807821105" target="_blank">https://doi.org/10.1073/pnas.0807821105

Fukao, T., Xu, K., Ronald, P. C., and Bailey-Serres, J. 2006. A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18(8):2021–2034. https://doi.org/10.1105/tpc.106.043000" target="_blank">https://doi.org/10.1105/tpc.106.043000

Hoang, K. L., Sinyutina, N. F., and Chirkova, T. V. 1979. Vliyanie usloviy anaerobioza na lipidnyy i belkovyy obmen korney pshenitsy i risa [Influence of anaerobiosis on the lipid and protein metabolism in wheat and rice roots]. Fiziologiya Rasteniy [Soviet Plant Physiology] 26(3):606–612.

Hu, Z., Qi, X., Zhang, M., Chen, X., and Nakazono, M. 2016. Roles of phytohormones in morphological and anatomical responses of plants to flooding stress. pp. 117–132. in G. J. Ahammed, J.-Q. Yu (eds.), Plant Hormones under Challenging Environmental Factors. Springer Science+Business Media, Dordrecht. https://doi.org/10.1007/978-94-017-7758-2_5" target="_blank">https://doi.org/10.1007/978-94-017-7758-2_5

Igamberdiev, A. U., and Hill, R. D. 2009. Plant mitochondrial function during anaerobiosis. Annals of Botany 103(2):259–268. https://doi.org/10.1093/aob/mcn100" target="_blank">https://doi.org/10.1093/aob/mcn100

Kende, H., van der Knaap, E., and Cho, H.-T. 1998. Deepwater rice: A model plant to study stem elongation. Plant Physiology 118(4):1105–1110. https://doi.org/10.1104/pp.118.4.1105" target="_blank">https://doi.org/10.1104/pp.118.4.1105

Kostychev, S. P. 1907. Issledovanija nad anajerobnym dyhaniem rastenij [Studies on anaerobic respiration of plants]. Botanicheskie zapiski pri Botanicheskom sade Sankt-Peterburgskogo Universiteta [Botanical Notes at the Botanical Garden of St. Petersburg University] (25):1–162.

Kulichikhin, K. Y., Chirkova, T. V., and Fagerstedt, K. V. 2009. Activity of biochemical pH-stat enzymes in cereal root tips under oxygen deficiency. Russian Journal of Plant Physiology 56(3)377–388. https://doi.org/10.1134/S102144370903011X" target="_blank">https://doi.org/10.1134/S102144370903011X

Kulichikhin, K. Yu., Kurchakova, E. V., and Chirkova, T. V. 2000. Aktivnost’ malatdegidrogenazy i soderzhanie endogennogo malata v kornyakh zlakov v usloviyakh anoksii [The activity of malate dehydrogenases and endogenous malate content in roots of cereals under anoxic conditions]. Biological Communications (3):70–76.

Kulichikhin, K. Y., Aitio, O., Chirkova, T. V., and Fagerstedt, K. V. 2007. Effect of oxygen concentration on intracellular pH, glucose-6-phosphate and NTP content in rice (Oryza sativa) and wheat (Triticum aestivum) root tips: In vivo ³¹P-NMR study. Physiologia Plantarum 129(3):507–518. https://doi.org/10.1111/j.1399-3054.2006.00819.x" target="_blank">https://doi.org/10.1111/j.1399-3054.2006.00819.x

Lastochkin, V. V., Yemelyanov, V. V., and Chirkova, T. V. 2000. Aktivnost’ peroksidazy v prorostkakh pshenitsy i risa v svyazi s vozdeystviem anoksii [Peroxidase activity in wheat and rice seedlings under anoxia]. Biological Communications (3):59–64.

Licausi, F. and Perata, P. 2009. Low oxygen signaling and tolerance in plants. Advances in Botanical Research 50:139–198. https://doi.org/10.1016/S0065-2296(08)00804-5" target="_blank">https://doi.org/10.1016/S0065-2296(08)00804-5

Licausi, F., Weits, D. A., Pant, B. D., Scheible, W.-R., Geigenberger, P., and van Dongen, J. T. 2011. Hypoxia responsive gene expression is mediated by various subsets of transcription factors and miRNAs that are determined by the actual oxygen availability. New Phytologist 190(2):442–456. https://doi.org/10.1111/j.1469-8137.2010.03451.x" target="_blank">https://doi.org/10.1111/j.1469-8137.2010.03451.x

Nabokikh, A. I. 1905. Vremennyj anajerobioz vysshih rastenij: Eksperimental’noe issledovanie. Chast’ 1. Nabljudenija nad processami rosta v beskislorodnoj srede. [Temporary anaerobiosis of higher plants: Experimental study. Part 1. Observations on growth processes in an oxygenfree environment.] St. Petersburg: Publishing house of I. N. Skorokhodov.

Nastinova, G. E., and Chirkova, T. V. 1978. O vozmozhnosti sinteza alkogol’- i laktatdegidrogenaz pri nedostatke kisloroda [On the possibility of synthesis of alcohol and lactate dehydrogenases in conditions of oxygen deficiency]. Fiziologiya Rasteniy [Soviet Plant Physiology] 25(1):55–63.

Nishiuchi, S., Yamauchi, T., Takahashi, H., Kotula, L., and Nakazono, M. 2012. Mechanisms for coping with submergence and waterlogging in rice. Rice 5(1):2 https://doi.org/10.1186/1939-8433-5-2" target="_blank">https://doi.org/10.1186/1939-8433-5-2

Pedersen, O., Colmer, T. D., and Sand-Jensen, K. 2013. Underwater photosynthesis of submerged plants ― recent advances and methods. Frontiers in Plant Science 4:140. https://doi.org/10.3389/fpls.2013.00140" target="_blank">https://doi.org/10.3389/fpls.2013.00140

Pedersen, O., Rich, S. M., and Colmer, T. D. 2009. Surviving floods: leaf gas films improve O₂ and CO₂ exchange, root aeration, and growth of completely submerged rice. Plant Journal 58(1):147–156. https://doi.org/10.1111/j.1365-313X.2008.03769.x" target="_blank">https://doi.org/10.1111/j.1365-313X.2008.03769.x

Peeters, A. J. M., Cox, M. C. H., Benschop, J. J., Vreeburg, R. A. M., Bou, J., and Voesenek, L. A. C. J. 2002. Submergence research using Rumex palustris as a model; looking back and going forward. Journal of Experimental Botany 53(368):391–398. https://doi.org/10.1093/jexbot/53.368.391" target="_blank">https://doi.org/10.1093/jexbot/53.368.391

Sauter, M. and Steffens, B. 2014. Biogenesis of adventitious roots and their involvement in the adaptation to oxygen limitations; pp. 299–312. in J. T. van Dongen and F. Licausi (eds.), Low-Oxygen Stress in Plants, Plant Cell Monographs. Vol. 21. Springer-Verlag, Wien. https://doi.org/10.1007/978-3-7091-1254-0_15" target="_blank">https://doi.org/10.1007/978-3-7091-1254-0_15

Schmitz, A. J., Folsom, J. J., Jikamaru, Y., Ronald, P., and Walia, H. 2013. SUB1A-mediated submergence tolerance response in rice involves differential regulation of the brassinosteroid pathway. New Phytologist 198(4):1060–1070. https://doi.org/10.1111/nph.12202" target="_blank">https://doi.org/10.1111/nph.12202

Semikhatova, O. A., and Chirkova, T. V. 2001. Fiziologiya dykhaniya rasteniy. [Physiology of plant respiration]. Izdatelstvo Sankt-Peterburgskogo Universiteta, Saint Petersburg, 220 pp.

Sinyutina, N. F., Hoang, K. L., and Chirkova, T. V. 1979. Fosfolipidy korney pshenitsy i risa v svyazi s razlichnym obespecheniem rasteniy kislorodom [Phospholipids of the roots of wheat and rice in realtion to various oxygen level]. Biological Communications (4):93–98.

Soldatenkov, S. V. and Chirkova, T. V. 1963. O roli list’ev v dykhanii korney, lishennykh kisloroda [Role of leaves in respiration of roots deprived of oxygen]. Fiziologiya Rasteniy [Soviet Plant Physiology] 10(5):535–543.

Soldatenkov, S. V. and Zhao, X.-D. 1961. Rol’ list’ev fasoli i kukuruzy v dykhanii korney, lishennykh kisloroda [Role of bean and maize leaves in the respiration of roots deprived of oxygen]. Fiziologiya Rasteniy [Soviet Plant Physiology] 8(4):385–394.

Takahashi, H., Yamauchi, T., Colmer, T. D., and Nakazono M. 2014. Aerenchyma formation in plants; pp. 247–265. in J. T. van Dongen and F. Licausi (eds.), Low-Oxygen Stress in Plants, Plant Cell Monographs. Vol. 21. Springer-Verlag, Wien. https://doi.org/10.1007/978-3-7091-1254-0_13" target="_blank">https://doi.org/10.1007/978-3-7091-1254-0_13

Tamang, B. G., and Fukao, T. 2015. Plant adaptation to multiple stresses during submergence and following desubmergence. International Journal of Molecular Sciences 16(12):30164–30180. https://doi.org/10.3390/ijms161226226" target="_blank">https://doi.org/10.3390/ijms161226226

Valyavskaya M. V., Sinyutina N. F., Chirkova T. V. 2000. Vliyanie ionov kal’tsiya na soderzhanie lipidov v kornyakh pshenitsy i risa v usloviyakh anaerobioza [Influence of Ca²⁺ ions on lipid content in the roots of weat and rice under anoxia]. Biological Communications (4):32–38.

Valyavskaya, M. V., Sinyutina, N. F., and Chirkova, T. V. 2002. Vliyanie ionov kal’tsiya na izmenenie soderzhaniya lipidov mitokhondriy pri anoksii u rasteniy s razlichnoy ustoychivost’yu k nedostatku kisloroda [Influence of Ca²⁺ ions and anoxia on lipid content of mitochondrial membranes in plants with different resistance to oxygen insufficiency]. Biological Communications (2):48–54.

Vartapetian B. B., and Jackson, M. B. 1997. Plant adaptations to anaerobic stress. Annals of Botany 79(Special Issue):3–20. https://doi.org/10.1093/oxfordjournals.aob.a010303" target="_blank">https://doi.org/10.1093/oxfordjournals.aob.a010303

Voesenek, L. A. C. J., and Bailey-Serres, J. 2015. Flood adaptive traits and processes: an overview. New Phytologist 206(1):57–73. https://doi.org/10.1111/nph.13209" target="_blank">https://doi.org/10.1111/nph.13209

Voitsekovskaya, S. A., and Chirkova, T. V. 1992. O vozmozhnosti sinteza negistonovykh belkov khromatina v prorostkakh pshenitsy i risa pri otsutstvii kisloroda [On the possibility of synthesis of non-histone chromatin proteins in wheat and rice seedlings under the absence of oxygen]. Biological Communications (3):73–79.

Voitsekovskaya, S. A., Badyina, T. G., and Chirkova, T. V. 1993. Vliyanie anaerobioza na svoystva khromatina i sostav ego negistonovykh belkov v prorostkakh pshenitsy i risa [Effect of anaerobiosis on chromatin properties and composition of non-histone proteins of chromatin in seedlings of wheat and rice]. Fiziologiya i biokhimiya kul’turnykh rasteniy 25(1):58–66.

Watanabe, K., Nishiuchi, S., Kulichikhin, K., and Nakazono, M. 2013. Does suberin accumulation in plant roots contribute to waterlogging tolerance? Frontiers in Plant Science 4:178. https://doi.org/10.3389/fpls.2013.00178" target="_blank">https://doi.org/10.3389/fpls.2013.00178

Winkel, A., Colmer, T. D., Ismail, A. M., and Pedersen, O. 2013. Internal aeration of paddy field rice (Oryza sativa) during complete submergence — importance of light and floodwater O₂. New Phytologist 197(4):1193–1203. https://doi.org/10.1111/nph.12048" target="_blank">https://doi.org/10.1111/nph.12048

Winkel, A., Pedersen, O., Ella, E., Ismail, A. M., and Colmer, T. D. 2014. Gas film retention and underwater photosynthesis during field submergence of four contrasting rice genotypes. Journal of Experimental Botany 65(12):3225–3233. https://doi.org/10.1093/jxb/eru166" target="_blank">https://doi.org/10.1093/jxb/eru166

Yemelyanov V. V. 1998. Rost i gormony rasteniy v usloviyakh anaerobioza [Plant growth and hormones under anaerobiosis]. Biological Communication (2):136–140.

Yemelyanov, V. V., and Chirkova, T. V. 1996. Svobodnye formy gormonov v rasteniyakh, razlichayushchikhsya po ustoychivosti k nedostatku kisloroda, v usloviyakh aeratsii i anaerobioza [Free forms of phytohormones in plants with different tolerance to the lack of oxygen under aeration and anaerobiosis]. Biological Communications (2):73–81.

Yemelyanov, V. V., and Shishova, M. F. 2012. The role of phytohormones in the control of plant adaptation to oxygen depletion; pp. 229–248 in N. A. Khan, R. Nazar, A. Iqbal, N. A. Anjum (eds.), Phytohormones and abiotic stress tolerance in plants. Springer-Verlag, Berlin–Heidelberg. https://doi.org/10.1007/978-3-642-25829-9_10" target="_blank">https://doi.org/10.1007/978-3-642-25829-9_10

Yin, X., Sakata, K., Nanjo, Y., Komatsu, S. 2014. Analysis of initial changes in the proteins of soybean root tip under flooding stress using gel-free and gel-based proteomic techniques. Journal of Proteomics 106:1–16. https://doi.org/10.1016/j.jprot.2014.04.004" target="_blank">https://doi.org/10.1016/j.jprot.2014.04.004

Zhukova, T. M. 1987. Vliyanie anaerobioza na soderzhanie uglevodov v kornyakh prorostkov pshenitsy i risa [The effect of anaerobiosis on the carbohydrate content in the roots of wheat and rice seedlings]. Biological Communications (2):88–93.

Zhukova, T. M., Chirkova, T. V., and Tretyakov, A. V. 1984. Adeninovye nukleotidy prorostkov pshenitsy i risa v razlichnykh usloviyakh aeratsii [Adenine nucleotides in seedlings of wheat and rice under different aeration conditions]. Biological Communications (3):74–81.