Acta Physiologiae Plantarum

, 40:212 | Cite as

Root flooding-induced changes in the dynamic dissipation of the photosynthetic energy of common bean plants

  • Douglas Antônio Posso
  • Junior BorellaEmail author
  • Gabriela Niemeyer Reissig
  • Marcos Antonio Bacarin
Original Article


In this work, we evaluated changes in the energy dissipation on electron transport chain of photosystems of leaves of four common bean (Phaseolus vulgaris L.) genotypes (cultivars and landraces) in response to root system flooding. Common bean plants (BRS Expedito and Iraí—cultivars; TB 02–24 and TB 03–13—landraces) were grown in soil and commercial substrate (1:1). At the early reproductive stages, the root system was subjected to flooding by adding distilled water up to 2 cm above the substrate surface for 4 days. Control plants were kept under normoxia. Chlorophyll a fluorescence, gas exchange, photorespiration, antioxidative enzymes and reactive oxygen species (ROS) were measured in leaves on the 4th day of flooding. Flooding of the root system reduced gas exchange in all genotypes with strong effects in CO2 assimilation. BRS Expedito genotype had a greater energy dissipation through fluorescence and heat over Iraí, TB 02–24 and TB 03–13, with regard of metabolic regulation through photorespiration to alleviate the excess of ATP/NADPH produced by the electron transport chain (ETC). On the other hand, the genotypes Iraí, TB 02–24 and TB 03–13 induced more efficiently the antioxidative enzyme system to cope with the deleterious effects of ROS in comparison to BRS Expedito. Further, the dynamic energy dissipation of the excess absorbed energy by the photosynthetic ETC was differentially dissipated in all four common bean genotypes.


Phaseolus vulgaris L. Waterlogging Photosynthesis Photorespiration Antioxidative enzyme 



This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001 and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). We are grateful to Embrapa-Terras Baixas and Stoller® for kindly providing common bean seeds and Rhizobium tropici strain, respectively.


  1. Ahmed S, Nawata E, Sakuratani T (2002) Effects of waterlogging at vegetative and reproductive growth stages on photosynthesis, leaf water potential and yield in mungbean. Plant Prod Sci 5:117–123. CrossRefGoogle Scholar
  2. António C, Päpke C, Rocha M, Diab H, Limami AM, Obata T, Fernie AR, van Dongen JT (2016) Regulation of primary metabolism in response to low oxygen availability as revealed by carbon and nitrogen isotope redistribution. Plant Physiol 170:43–56. CrossRefPubMedGoogle Scholar
  3. Armstrong W, Strange ME, Cringle S, Beckett PM (1994) Microelectrode and modeling study of oxygen distribution in roots. Ann Bot 74:287–299. CrossRefGoogle Scholar
  4. Aroca R, Porcel R, Ruiz-Lozano JM (2012) Regulation of root water uptake under abiotic stress conditions. J Exp Bot 63:43–57. CrossRefPubMedGoogle Scholar
  5. Aydogan C, Turhan E (2015) Changes in morphological and physiological traits and stress-related enzyme activities of green bean (Phaseolus vulgaris L.) genotypes in response to waterlogging stress and recovery treatment. Hort Environ Biotechnol 56:391–401. CrossRefGoogle Scholar
  6. Azevedo Neto AD, Prisco JT, Eneas Filho J, de Abreu CEB, Gomes Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56:87–94. CrossRefGoogle Scholar
  7. Bai YR, Yang P, Su YY, He ZL, Ti XN (2014) Effect of exogenous methanol on glycolate oxidase and photorespiratory intermediates in cotton. J Exp Bot 65:5331–5338. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bailey-Serres J, Fukao T, Gibbs DJ, Holdsworth MJ, Lee SC, Licausi F, Perata P, Voesenek LACJ, van Dongen JT (2012) Making sense of low oxygen sensing. Trends Plant Sci 17:129–138. CrossRefPubMedGoogle Scholar
  9. Bansal R, Srivastava JP (2015) Effect of waterlogging on photosynthetic and biochemical parameters in pigeon pea. Russ J Plant Physiol 62:322–327. CrossRefGoogle Scholar
  10. Blokhina O, Fagerstedt KV (2010) Oxidative metabolism, ROS and NO under oxygen deprivation. Plant Physiol Biochem 48:359–373. CrossRefPubMedGoogle Scholar
  11. Borella J, Oliveira HC, Oliveira DDSC, Braga EJB, de Oliveira ACB, Sodek L, do Amarante L (2017) Hypoxia-driven changes in glycolytic and tricarboxylic acid cycle metabolites of two nodulated soybean genotypes. Environ Exp Bot 133:118–127. CrossRefGoogle Scholar
  12. Bräutigam A, Gowik U (2016) Photorespiration connects C3 and C4 photosynthesis. J Exp Bot 67:2953–2962. CrossRefPubMedGoogle Scholar
  13. Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468. CrossRefGoogle Scholar
  14. Cassol D, De Silva FSP, Falqueto AR, Bacarin MA (2008) An evaluation of non-destructive methods to estimate total chlorophyll content. Photosynthetica 46:634–636. CrossRefGoogle Scholar
  15. Eullaffroy P, Frankart C, Aziz A, Couderchet M, Blaise C (2009) Energy fluxes and driving forces for photosynthesis in Lemna minor exposed to herbicides. Aquat Bot 90:172–178. CrossRefGoogle Scholar
  16. Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J (2012) Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63:637–661. CrossRefGoogle Scholar
  17. Foyer CH, Ruban AV, Noctor G (2017) Viewing oxidative stress through the lens of oxidative signaling rather than damage. Biochem J 474:877–883. CrossRefPubMedPubMedCentralGoogle Scholar
  18. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. CrossRefPubMedGoogle Scholar
  19. Gururani MA, Venkatesh J, Ganesan M, Strasser RJ, Han Y, Kim JI, Lee HY, Song PS (2015) In vivo assessment of cold tolerance through chlorophyll-a fluorescence in transgenic zoysia grass expressing mutant phytochrome A. PLos One 10:e0127200. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hanawa H, Ishizaki K, Nohira K, Takagi D, Shimakawa G, Sejima T, Shaku K, Makino A, Miyake C (2017) Land plants drive photorespiration as higher electron-sink: comparative study of post-illumination transient O2-uptake rates from liverworts to angiosperms through ferns and gymnosperms. Physiol Plant 161:138–149. CrossRefPubMedGoogle Scholar
  21. Herrera A (2013) Responses to flooding of plant water relations and leaf gas exchange in tropical tolerant trees of a black-water wetland. Front Plant Sci 4:1–12. CrossRefGoogle Scholar
  22. Hoagland DR, Arnon DI (1938) The water culture method for growing plants without soil. Cal Agric Exp Stn 347:1–39Google Scholar
  23. Ivanov BN, Borisova-Mubarakshina MM, Kozuleva MA (2018) Formation mechanisms of superoxide radical and hydrogen peroxide in chloroplasts, and factors determining the signaling by hydrogen peroxide. Funct Plant Biol 45:102–110. CrossRefGoogle Scholar
  24. Kreuzwieser J, Rennenberg H (2014) Molecular and physiological responses of trees to waterlogging stress. Plant Cell Environ 37:2245–2259. CrossRefPubMedGoogle Scholar
  25. Lanza LNM, Lanza DCF, Sodek L (2014) Utilization of 15NO3 by nodulated soybean plants under conditions of root hypoxia. Physiol Mol Biol Plants 20:287–293. CrossRefGoogle Scholar
  26. Limami A, Diab H, Lothier J (2014) Nitrogen metabolism in plants under low oxygen stress. Planta 239:531–541. CrossRefPubMedGoogle Scholar
  27. Mielke MS, Schaffer B (2011) Effects of soil flooding and changes in light intensity on photosynthesis of Eugenia uniflora L. seedlings. Acta Physiol Plant 33:1661–1668. CrossRefGoogle Scholar
  28. Osorno J, Endres G, Ashley R, Kandel H, Berglund D (2014) Dry bean production guide. NDSU Agriculture, Fargo, 144 pGoogle Scholar
  29. Rocha M, Licausi F, Araújo WL, Nunes-Nesi A, Sodek L, Fernie AR, van Dongen JT (2010) Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiol 152:1501–1513. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Santos Junior UM, Gonçalves JFC, Strasser RJ, Fearnside PM (2015) Flooding of tropical forests in central Amazonia: what do the effects on the photosynthetic apparatus of trees tell us about species suitability for reforestation in extreme environments created by hydroelectric dams? Acta Physiol Plant 37:1–17. CrossRefGoogle Scholar
  31. Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B Biol 104:236–257. CrossRefGoogle Scholar
  32. Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: the JIP-test. In: Mathis P (ed) Photosynthesis: from light to biosphere. Kluwer Academic Publishers, Montpellier, pp 977–980Google Scholar
  33. Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Spring, Dordrecht, pp 321–362CrossRefGoogle Scholar
  34. Tikkanen M, Mekala NR, Aro EM (2014) Photosystem II photoinhibition-repair cycle protects photosystem I from irreversible damage. Biochim Biophys Acta 1837:210–215. CrossRefPubMedGoogle Scholar
  35. Tsimilli-Michael M, Strasser RJ (2008) In vivo assessment of plants vitality: applications in detecting and evaluating the impact of mycorrhization on host plants. In: Varma A (ed) Mycorrhiza. Dordrecht: Springer, 3rd ed., 679–703CrossRefGoogle Scholar
  36. van Dongen JT, Licausi F (2015) Oxygen sensing and signalling. Annu Rev Plant Biol 66:345–367. CrossRefPubMedGoogle Scholar
  37. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Plant Sci 151:59–66. CrossRefGoogle Scholar
  38. Yan K, Chen P, Shao H, Shao C, Zhao S, Brestic M (2013) Dissection of photosynthetic electron transport process in sweet sorghum under heat stress. Plos One 8:special issue 62100. CrossRefGoogle Scholar
  39. Yusuf MA, Kumar D, Rajwanshi R, Strasser RJ, Tsimilli-Michael M, Govindjee; Sarin NB (2010) Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviate abiotic stress: physiological and chlorophyll a fluorescence measurements. Biochim Biophys Acta Bioenerg 1797:428–1438. CrossRefGoogle Scholar
  40. United States Department of Agriculture (USDA) (2015) Hearing: agriculture’s role in combatting global hunger. U.S. Government Publishing Office, Washington, p 126Google Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2018

Authors and Affiliations

  1. 1.Departamento de BotânicaUniversidade Federal de PelotasPelotasBrazil
  2. 2.Departamento de Ciência e Tecnologia AgroindustrialUniversidade Federal de PelotasPelotasBrazil

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