Photosynthetica 2012, 50(3):447-457 | DOI: 10.1007/s11099-012-0052-4

Physiological and biochemical responses of Theobroma cacao L. genotypes to flooding

F. Z. Bertolde1, A. A. F. Almeida1,*, C. P. Pirovani1, F. P. Gomes1, D. Ahnert1, V. C. Baligar2, R. R. Valle3
1 Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Ilhéus, BA, Brasil
2 USDA-ARS, Beltsville, USA
3 Centro de Pesquisas do Cacau, Comissão Executiva do Plano da Lavoura Cacaueira (CEPEC/CEPLAC), Ilhéus, BA, Brasil

Flooding is common in lowlands and areas with high rainfall or excessive irrigation. A major effect of flooding is the deprivation of O2 in the root zone, which affects several biochemical and morphophysiological plant processes. The objective of this study was to elucidate biochemical and physiological characteristics associated with tolerance to O2 deficiency in two clonal cacao genotypes. The experiment was conducted in a greenhouse with two contrasting clones differing in flood tolerance: TSA-792 (tolerant) and TSH-774 (susceptible). Leaf gas exchange, chlorophyll (Chl) fluorescence, chemical composition and oxidative stress were assessed during 40 d for control and flooded plants. Flooding induced a decrease in net photosynthesis, stomatal conductance and transpiration of both genotypes. In flood conditions, the flood-susceptible clone showed changes in chlorophyll fluorescence, reductions in chlorophyll content and increased activity of peroxidase and polyphenol oxidase. Flooding also caused changes in macro- and micronutrients, total soluble sugars and starch concentrations in different plant organs of both genotypes. Response curves for the relationship between photosynthetically active radiation (PAR) and net photosynthetic rate (P N) for flooded plants were similar for both genotypes. In flood conditions, the flood-susceptible clone exhibited (1) nonstomatal limitations to photosynthesis since decreased in maximum potential quantum yield of PSII (Fv/Fm) values indicated possible damage to the PSII light-harvesting complex; (2) oxidative stress; (3) increased leaf chlorosis; and (4) a reduction in root carbohydrate levels. These stresses resulted in death of several plants after 30 d of flooding.

Additional key words: chlorophyll fluorescence; flooding; genotypes; oxidative stress; chlorophyll content; peroxidase; polyphenol oxidase; soluble sugars; starch; net photosynthetic rate; photosynthetically active radiation; quantum yield; leaf chlorosis; root carbohydrate; carotenoids; compensation irradiance; apparent quantum efficiency; transpiration rate; stomatal conductance; water-use efficiency; O2 deficiency; chlorophyll a; chlorophyll b

Received: June 9, 2011; Accepted: June 14, 2012; Published: September 1, 2012  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Bertolde, F.Z., Almeida, A.A.F., Pirovani, C.P., Gomes, F.P., Ahnert, D., Baligar, V.C., & Valle, R.R. (2012). Physiological and biochemical responses of Theobroma cacao L. genotypes to flooding. Photosynthetica, 50(3), 447-457. doi: 10.1007/s11099-012-0052-4
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Almeida, A-A.F., Valle, R.R.: Ecophysiology of the cacao tree. - Braz. J. Plant Physiol. 19: 425-448, 2007. Go to original source...
    2. Almeida, A.-A.F., Valle, R.R.: Cacao: ecophysiology of growth and production. - In: DaMatta, F.M. (ed.): Ecophysiology of Tropical Tree Crops. Pp. 37-70. Nova Science Publishers Inc., Hauppauge 2009.
    3. Andersen, P.C., Lombard, P.B., Westwood, M.N.: Effect of root anaerobiosis on the water relations of several Pyrus species. - Physiol. Plant. 62: 245-252, 1984. Go to original source...
    4. Armstrong, W.: Aeration in higher plants. - Adv. Bot. Res. 7: 225-232, 1979. Go to original source...
    5. Barrett-Lennard, E.G., Ratingen, P.V., Mathie, M.H.: The developing pattern of damage in wheat (Triticum aestivum L.) due to the combined stresses of salinity and hypoxia: experiments under controlled conditions suggest a methodology for plant selection. - Aust. J. Agr. Res. 50: 129-136, 1999. Go to original source...
    6. Bartley, B.G.D.: The Genetic Diversity of Cacao and its Utilization. - CABI Publishing, Cambridge 2005. Go to original source...
    7. Bertolde, F.Z., Almeida, A.-A. F., Corrêa, R.X., et al.: Molecular, physiological and morphological analysis of waterlogging tolerance in clonal genotypes of Theobroma cacao L. - Tree Physiol. 30: 56-67, 2010. Go to original source...
    8. Björkman, O., Demmig, B.: Photon yield de O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. - Planta 170: 489-504, 1987. Go to original source...
    9. Braga, J.M., Defelipo, B.: [Spectrophotometric determination of phosphorus in soil extracts and plants.] - Rev. Ceres 21: 73-85, 1974. [In Portuguese.]
    10. Campbell, J.J., Pan, J., Butcher, E.C.: Developmental switches in chemokine responses during T cell maturation. - J. Immunol. 163: 2353-2357, 1999. Go to original source...
    11. Carvalho, C.J.R., Ishida, F.Y.: [Responses of peach palm (Bactris gasipaes Kunth) to flooding young.] - Pesq. Agr. Bras. 37: 1231-1237, 2002. [In Portuguese.] Go to original source...
    12. Chirkova, T.V., Gutman, T.S.: Physiological role of branch lenticels in willow and poplar under conditions of root anaerobiosis. - Sov. Plant Phys. 19: 289-295, 1972.
    13. Clegg, K.M.: The application of the anthrone reagent to the estimation of starch in cereals. - J. Sci. Food Agr. 7: 40-44, 1956. Go to original source...
    14. Crawford, R.M.M., Braendle, R.: Oxygen deprivation stress in a changing environment. - J. Exp. Bot. 47: 145-159, 1996. Go to original source...
    15. Davies, F.S., Flore, J.A.: Short-term flooding effects on gas exchange and quantum yield of rabbiteye blueberry (Vaccinium ashei Reade). - Plant Physiol. 81: 289-292, 1986. Go to original source...
    16. Dennis, E.S., Dolferus, R., Ellis, M., et al.: Molecular strategies for improving waterlogging tolerance in plants. - J. Exp. Bot. 51: 89-97, 2000. Go to original source...
    17. Dogan S, Arslan, O., Ozen, F.: Polyphenol oxidase activity of oregano at different stages. - Food Chemistry 91: 341-345, 2005. Go to original source...
    18. Drew, M.C.: Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. - Ann. Rev. Plant Physiol. Plant Mol. Biol. 48: 223-250, 1997. Go to original source...
    19. Farquhar, G.D., Sharkey, T.D.: Stomatal conductance and photosynthesis. - Ann. Rev. Plant Phys. 33: 317-345, 1982. Go to original source...
    20. Folzer, H., Capelli, N., Dat, J., Badot, P.-M.: Molecular cloning and characterization of calmodulin genes in young oak seedlings (Quercus petraea L.) during early flooding stress. - Biochim. Biophys. Acta 1727: 213-219, 2005. Go to original source...
    21. Foyer, C.H., Lelandais, M., Kunert, K.J.: Photooxidative stress in plants. - Physiol. Plant 92: 696-717, 1994. Go to original source...
    22. Gomes, A.R.S., Kozlowski, T.T.: The effects of flooding on water relations and growth of Theobroma cacao var. catongo seedlings. - J. Hort. Sci. 61: 265-276, 1986. Go to original source...
    23. Hiscox, J.D., Israelstam, G.F.: A method for the extraction of chlorophyll from leaf tissue without maceration. - Can. J. Bot. 57: 1332-1334, 1979. Go to original source...
    24. Isaac, R.A., Kerber, J.O.: Atomic absorption and flame photometry: technique and uses in soil, plant and water analysis. - In: Walsh, L.M. ed. Instrumental Methods of Analysis of Soils and Plant Tissue. Pp. 17-37. Soil Sci. Soc. Amer. J., Madison 1971. Go to original source...
    25. Jackson, M.L.: Nitrogen determinations for soil and plant tissue. - In: Jackson M.L. (ed.): Soil Chemical Analysis. Pp. 183-204, Prentice Hall Chiffis, Englewood 1958.
    26. Jackson, M.B.: The impact of flooding stress on plants and crops. - http://www.plantstress.com/Articles/waterlogging_i/waterlog_i.htm, 2004.
    27. Kozlowski, T.T.: Responses of woody plants to flooding and salinity. - Tree Physiol. Mon. 1: 1-29, 1997. Go to original source...
    28. Kozlowski, T.T.: Acclimation and adaptive responses of woody plants to environmental stresses. - Bot. Rev. 68: 270-334, 2002. Go to original source...
    29. Kozlowski, T.T., Pallardy, S.G.: Effect of flooding on water, carbohydrate, and mineral relations. - In: Kozlowski, T.T. (ed.): Flooding and Plant Growth. Pp. 165-193. Acad. Press, Orlando 1984. Go to original source...
    30. Krause, G.H., Weis, E.: Chlorophyll fluorescence and photosynthesis: the basis. - Ann. Rev. Plant Physiol. Plant Mol. Biol. 42: 313-349, 1991. Go to original source...
    31. Laing, W., Greer, D., Sun, O., Beets, P., Lowe, A., Payn, T.: Physiological impacts of Mg deficiency in Pinus radiata: growth and photosynthesis. - New Phytol. 146: 47-57, 2000. Go to original source...
    32. Lopez, O.R., Kursar, T.A.: Flood tolerance of four tropical tree species. - Tree Physiol. 19: 925-932, 1999. Go to original source...
    33. Maxwell, K., Johnson, G.N.: Chlorophyll fluorescence - a practical guide. - J. Exp. Bot. 51: 659-668, 2000. Go to original source...
    34. Mccready, R.M., Guggolz, J., Silveira, V., Owens, H.S.: Determination of starch and amylase in vegetables. - Analyt. Chem. 22: 1156-1158, 1950. Go to original source...
    35. Medri, M.E.: [Aspects morpho-anatomical and physiological Peltophorum dubium (Spr.) Dr. Taub. subject to flooding and the application of etrel.] - Rev. Bras. Bot. 21: 261-267, 1998. [In Portuguese.] Go to original source...
    36. Mielke, M.S., Almeida, A-A.F., Gomes, F.P., et al.: Leaf gas exchange, chlorophyll fluorescence and growth responses of Genipa americana seedlings to soil flooding. - Environ. Exp. Bot. 50: 221-231, 2003. Go to original source...
    37. Mielke, M.S., Almeida, A-A.F., Gomes, F.P., et al.: Effects of soil flooding on leaf gas exchange and growth of two neotropical pioneer tree species. - New Forest. 29: 161-168, 2005. Go to original source...
    38. Oliveira, J.G. de, Alves, P.L.C.A., Magalhães, A.C.: The effect of chilling on the photosynthetic activity in coffee (Coffea Arabica L.) seedlings. The protective action of chloroplastid pigments. - Braz. J. Plant Physiol. 14: 95-104, 2002. Go to original source...
    39. Pachepsky, L.B., Acock, B.: An adequate model of photosynthesis - II. Dependence of parameters on environmental factors. - Agric. Syst. 50, 227-238, 1996. Go to original source...
    40. Pezeshki, S.R.: Differences in patterns of photosynthetic responses to hypoxia in flood-tolerant and flood-sensitive tree species. - Photosynthetica 28: 423-430, 1993.
    41. Pezeshki, S.R.: Responses of baldcypress (Taxodium distichum) seedlings to hypoxia: leaf protein content, ribulose-1,5-bisphosphate carboxylase/oxygenase activity and photosynthesis. - Photosynthetica 30: 59-68, 1994.
    42. Pezeshki, S.R., Pardue, J.H., DeLaune, R.D.: Leaf gas exchange and growth of flood-tolerant and flood-sensitive tree species to soil oxygen deficiency. - Tree Physiol. 16: 453-458, 1996. Go to original source...
    43. Pezeshki, S.R.: Wetland plant responses to soil flooding. - Environ. Exp. Bot. 46: 299-312, 2001. Go to original source...
    44. Pirovani, C.P., Carvalho, H.A.S., Machado, R.C.R., et al.: Protein extraction for proteome analysis from cacao leaves and meristems, organs infected by Moniliophthora perniciosa, the causal agent of the witches' broom disease. - Electrophoresis 29: 2391-2401, 2008. Go to original source...
    45. Ponnamperuma, F.N.: The chemistry of submerged soils. - Adv. Agron. 24: 29-96, 1972. Go to original source...
    46. Sánchez, E., Soto, J.M., Garcia, P.C., et al.: Phenolic compounds and oxidative metabolism in green bean plants under nitrogen toxicity. - Austr. J. Plant Physiol. 27: 973-978, 2000. Go to original source...
    47. Schaffer, B., Andersen, P.C., Ploetz, R.C.: Responses of fruit crops to flooding. - Hort. Rev. 13: 257-313, 1992. Go to original source...
    48. Siegel, B.Z.: Plant peroxidases - an organismic perspective. - Plant Growth Regulation 12: 303-312, 1993. Go to original source...
    49. Smethurst, C.F., Shabala, S.: Screening methods for waterlogging tolerance in lucerne: comparative analysis of waterlogging effects on chlorophyll fluorescence, photosynthesis, biomass and chlorophyll content. - Funct. Plant Biol. 30: 335-343, 2003. Go to original source...
    50. Souza, C.A.F., Sodek, L.: The metabolic response of plants to oxygen deficiency. - Braz. J. Plant Physiol. 14: 83-94, 2002. Go to original source...
    51. Souza, J.O., Jr.: [Substrates and Fertilization for Cocoa Seedlings.] - PhD. Thesis, Universid. São Paulo, São Paulo 2007. [In Portuguese.]
    52. Steel, R.G.D., Torrie, J.H.: Principles and Procedures of Statistics. McGraw-Hill Book Co., New York 1980.
    53. Vartapetian, B. B.: Flood-sensitive plants under primary and secondary anoxia: ultrastructural and metabolic responses. - In: Jackson, M.B., Davis, D.D., Lambers, H. (ed.): Plant Life under Oxygen Deprivation: Ecology, Physiology and Biochemistry. Pp. 201-216. SPB Academic, The Hague 1996.
    54. Vartapetian, B.B., Jackson, M.B.: Plant adaptations to anaerobic stress. - Ann. Bot. 79(Suppl. A): 3-20, 1997. Go to original source...
    55. Vaughn, K.C., Duke, S.O.: Function of polyphenol oxidase in higher plants. - Physiol. Plant 60: 106-112, 1984. Go to original source...
    56. von Caemmerer, S., Farquhar, G.D.: Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. - Planta 153: 376-387, 1981. Go to original source...
    57. Wellburn, A.R.: The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. - J. Plant. Physiol. 144: 307-313, 1994. Go to original source...
    58. Yordanova, R.Y., Christov, K.N., Popova, L.P.: Antioxidative enzymes in barley plants subjected to soil flooding. - Environ. Exp. Bot. 51: 93-101, 2004. Go to original source...
    59. Yu, Q., Rengel, Z.: Waterlogging influences plant growth and activities of superoxide dismutases in narrow-leafed lupine and transgenic tobacco plants. - J. Plant Physiol. 155: 431-438, 1999. Go to original source...

    Return to the content