biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 64:753-763, 2020 | DOI: 10.32615/bp.2020.116

Sex-specific responses of Populus deltoides to combined salinity and calcium under waterlogging conditions

L.-F. MIAO, D.-D. LI, F. YANG*, Z.-H. TAN*
College of Ecology and Environment, Hainan University; Center for Eco-Environmental Restoration Engineering of Hainan Province; Key Laboratory of Agro-Forestry Environmental Processes and Ecological Regulation of Hainan Province, Haikou, Hainan 570228, P.R. China

In this study, we investigated the sex-specific ion uptake and physiological and biochemical responses to combined salinity and calcium treatments of male and female Populus deltoides under waterlogging conditions. Results indicate that both P. deltoides clones were sensitive to salinity and calcium. Under well-watered conditions, salinity stress could especially increase the Na content in female P. deltoides clones, whereas salinity and calcium could increase the K and Ca content in male clones. Waterlogging could evidently stimulate Na content in leaves under salinity, especially in female P. deltoides clones. However, waterlogging had no visible effects on the amount of Ca absorption between the two clones under abundant calcium conditions. The physiological and biochemical responses to combined salinity and calcium exceeded the effects of salinity or calcium individually. However, no significant difference was observed, hence indicating the similar responses of male and female P. deltoides clones. The lower Na content and Na:Ca ratio, and the higher K and Ca content in male clones suggest that the male clones could maintain ion homeostasis better than the female clones. The sex-specific differences in net photosynthetic rate, intercellular CO2 concentration, effective quantum yield of photosystem II, photochemical quenching coefficient, non-photochemical quenching coefficient, photosynthetic electron transport rate, content of superoxide anions, hydroxyl radicals, H2O2, soluble protein, and activities of superoxide dismutase under certain conditions suggest that female P. deltoides clones are more sensitive to salinity, calcium, and the combination of both than their male counterparts.

Keywords: combined abiotic stress, ion uptake, physiological responses, poplars, sexual dimorphisms.

Received: May 27, 2020; Revised: July 22, 2020; Accepted: August 7, 2020; Published online: October 29, 2020  Show citation

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MIAO, L.-F., LI, D.-D., YANG, F., & TAN, Z.-H. (2020). Sex-specific responses of Populus deltoides to combined salinity and calcium under waterlogging conditions. Biologia plantarum, 64, Article 753-763. https://doi.org/10.32615/bp.2020.116
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    References

    1. Alhdad, G.M., Seal, C.E., Al-Azzawi, M.J., Flowers, T.J.: The effect of combined salinity and waterlogging on the halophyte Suaeda maritima: the role of antioxidants. - Environ. exp. Bot. 87: 120-125, 2013. Go to original source...
    2. An, P., Li, X., Zheng, Y., Eneji, A.E., Inanaga, S.: Calcium effects on root cell wall composition and ion contents in two soybean cultivars under salinity stress. - Can. J. Plant Sci. 94: 733-740, 2014. Go to original source...
    3. Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
    4. Bray, L., Chriqui, D., Gloux, K., Rudulier, D.L., Meyer, M., Peduzzi, J.: Betaines and free amino acids in salt stressed vitroplants and winter resting buds of Populus trichocarpa × deltoides. - Physiol. Plant. 83: 136-143, 1991. Go to original source...
    5. Cabañero, F.J., Carvajal, M.: Does calcium determine water uptake under saline conditions in pepper plants, or is it water flux which determines calcium uptake? - Plant Sci. 166: 443-450, 2004. Go to original source...
    6. Cao, F.L., Conner, W.H.: Selection of flood-tolerant Populus deltoides clones for reforestation projects in China. - Forest Ecol. Manage. 117: 211-220, 1999. Go to original source...
    7. Chen, F., Zhang, S., Jiang, H., Ma, W., Korpelainen, H., Li, C.: Comparative proteomics analysis of salt response reveals sex-related photosynthetic inhibition by salinity in Populus cathayana cuttings. - J. Proteome Res. 10: 3944-3958, 2011. Go to original source...
    8. Chen, L., Zhang, S., Zhao, H., Korpelainen, H., Li, C.: Sex-related adaptive responses to interaction of drought and salinity in Populus yunnanensis. - Plant Cell Environ. 33: 1767-1778, 2010. Go to original source...
    9. Cooper, D.J., D'Amico, D.R., Scott, M.L.: Physiological and morphological response patterns of Populus deltoides to alluvial ground water pumping. - Environ. Manage. 31: 215-226, 2003. Go to original source...
    10. Cramer, G.R.: Sodium-calcium interactions under salinity stress. Salinity: Environment - Plants - Molecules. - Springer, Dordrecht 2002. Go to original source...
    11. Fung, L.E., Wang, S.S., Altman, A., Hütterman, A.: Effect of NaCl on growth, photosynthesis, ion and water relations of four poplar genotypes. - Forest Ecol. Manage. 107: 135-146, 1998. Go to original source...
    12. Gao, H., Jia, Y., Guo, S., Lv, G., Wang, T., Juan, L.: Exogenous calcium affects nitrogen metabolism in root-zone hypoxia-stressed muskmelon roots and enhances short-term hypoxia tolerance. - J. Plant Physiol. 168: 1217-1225, 2011. Go to original source...
    13. Gladwin, D.N., Roelle, J.E.: Survival of plains cottonwood (Populus deltoides subsp. monilifera) and saltcedar (Tamarix ramossima) seedlings in response to flooding. - Wetlands 18: 669-674, 1998. Go to original source...
    14. Girija, C., Smith, B.N., Swamy, P.M.: Interactive effects of sodium chloride and calcium chloride on the accumulation of proline and glycine betaine in peanut (Arachis hypogaea L.). - Environ. exp. Bot. 47: 1-10, 2002. Go to original source...
    15. Haddadi, B.S., Hassanpour, H., Niknam, V.: Effect of salinity and waterlogging on growth, anatomical and antioxidative responses in Mentha aquatica L. - Acta Physiol. Plant. 38: 1-11, 2016. Go to original source...
    16. Han, C., Chan, Z., Yang, F.: Comparative analyses of universal extraction buffers for assay of stress related biochemical and physiological parameters. - Preparative Biochem. Biotechnol. 45: 684-695, 2015. Go to original source...
    17. He, L., Lu, X., Tian, J., Yang, Y., Li, B., Li, J., Guo. S.: Proteomic analysis of the effects of exogenous calcium on hypoxic-responsive proteins in cucumber roots. - Proteome Sci. 10: 42, 2012. Go to original source...
    18. Jian, S., Dai, S., Wang, R., Chen, S., Li, N., Zhou, X., Lu, C., Shen, X., Zheng, X., Hu, Z., Zhang, Z., Song J., Xu, Y.: Calcium mediates root K+/Na+ homeostasis in poplar species differing in salt tolerance. - Tree Physiol. 29: 1175-1186, 2009. Go to original source...
    19. Jiang, H., Peng, S., Sheng, Z., Li, X., Korpelainen, H., Li, C.: Transcriptional profiling analysis in Populus yunnanensis provides insights into molecular mechanisms of sexual differences in salinity tolerance. - J. exp. Bot. 63: 3709-3726, 2012. Go to original source...
    20. Juvany, M., Munné-Bosch, S.: Sex-related differences in stress tolerance in dioecious plants: a critical appraisal in a physiological context. - J. exp. Bot. 66: 451-454, 2015. Go to original source...
    21. Letts, M.G., Phelan, C.A., Johnson, D.R.E., Rood, S.B.: Seasonal photosynthetic gas exchange and leaf reflectance characteristics of male and female cottonwoods in a riparian woodland. - Tree Physiol. 28: 1037, 2008. Go to original source...
    22. Li, Y., Duan, B., Chen, J., Korpelainen, H., Niinemets, Ü., Li, C.: Males exhibit competitive advantages over females of Populus deltoides under salinity stress. - Tree Physiol. 36: 1573-1584, 2016. Go to original source...
    23. Lin, K.H., Chiou, Y.K., Hwang, S.Y., Chen, L.F.O., Lo, H.F.: Calcium chloride enhances the antioxidative system of sweet potato (Ipomoea batatas) under flooding stress. - Ann. Appl. Biol. 152: 157-168, 2008. Go to original source...
    24. Lopez, M.V., Satti, S.M.E.: Calcium and potassium-enhanced growth and yield of tomato under sodium chloride stress. - Plant Sci. 114: 19-27, 1996. Go to original source...
    25. McKown, A.D., Kláp¹tì, J., Guy, R.D., Soolanayakanahally, R.Y., La Mantia, J., Porth, I., Skyba, O., Unda, F., Douglas, C.J., El-Kassaby, Y.A., Hamelin, R.C., Mansfield, S.D., Cronk, Q.: Sexual homomorphism in dioecious trees: extensive tests fail to detect sexual dimorphism in Populus. - Sci. Rep. 7: 1831, 2017. Go to original source...
    26. Miao, L.F., Yang, F., Han, C.Y., Pu, Y.J., Ding, Y., Zhang, L.J.: Sex-specific responses to winter flooding, spring waterlogging and post-flooding recovery in Populus deltoides. - Sci. Rep. 7: 2534, 2017. Go to original source...
    27. Murillo-Amador, B., Jones, H.G., Kaya, C., Aguilar, R.L., García-Hernández, J.L., Troyo-Diéguez, E., Avila-Serrano, N.Y., Rueda-Puente, E.: Effects of foliar application of calcium nitrate on growth and physiological attributes of cowpea (Vigna unguiculata L. Walp.) grown under salt stress. - Environ. exp. Bot. 58: 188-196, 2006. Go to original source...
    28. Nielsen, J.L., Rood, S.B., Pearce, D.W., Letts, M.G., Jiskoot, H., Ehleringer, J.: Streamside trees: responses of male, female and hybrid cottonwoods to flooding. - Tree Physiol. 30: 1479-1488, 2010. Go to original source...
    29. Oh, M.W., Nanjo, Y., Komatsu, S.: Gel-free proteomic analysis of soybean root proteins affected by calcium under flooding stress. - Front. Plant Sci. 5: 559, 2014. Go to original source...
    30. Parvin, K., Ahamed, K.U., Islam, M.M., Haque, N.: Modulation of ion uptake in tomato (Lycopersicon esculentum L.) plants with exogenous application of calcium under salt stress condition. - J. Plant Sci. 22: 40-49, 2016. Go to original source...
    31. Regehr, D.L., Bazzaz, F.A., Boggess, W.R.: Photosynthesis, transpiration and leaf conductance in Populus deltoides in relation to flooding and drought. - Photosynthetica 9: 52-61, 1975.
    32. Rengel, Z.: The role of calcium in salt toxicity. - Plant Cell Environ. 15: 625-632, 1992. Go to original source...
    33. Robinson, K.M., Delhomme, N., Mähler, N., Schiffthaler, B., Onskog, J., Albrectsen, B.R., Ingvarsson, P.K., Hvidsten, T.R., Jansson, S., Street, N.R.: Populus tremula (European aspen) shows no evidence of sexual dimorphism. - BMC Plant Biol. 14: 276, 2014. Go to original source...
    34. Rood, S.B., Nielsen, J.L., Shenton, L., Gill, K.M., Letts, M.G.: Effects of flooding on leaf development, transpiration, and photosynthesis in narrow leaf cottonwood, a willow-like poplar. - Photosynth. Res. 104: 31-39, 2010. Go to original source...
    35. Rowland, D.L.: Diversity in physiological and morphological characteristics of four cottonwood (Populus deltoides var. wislizenii) populations in New Mexico: evidence for a genetic component of variation. - Can. J. Forest Res. 31: 845-853, 2001. Go to original source...
    36. Salahshoor, F., Kazemi, F.: Effect of calcium on reducing salt stress in seed germination and early growth stage of Festuca ovina L. - Plant Soil Environ. 62: 460-467, 2016. Go to original source...
    37. Singh, M., Jain, M., Pant, R.C.: Clonal variability in photosynthetic and growth characteristics of Populus deltoides under saline irrigation. - Photosynthetica 36: 605-609, 2000. Go to original source...
    38. Srivastava, A.K., Rai, A.N., Patade, V.Y., Suprasanna, P.: Calcium signaling and its significance in alleviating salt stress in plants. - In: Ahmad, P., Azooz, M.M., Prasad, M.N.V. (ed.): Salt Stress in Plants: Signalling, Omics and Adaptations. Pp.197-218. - Springer, New York 2013. Go to original source...
    39. Tattini, M., Traversi, M.L.: On the mechanism of salt tolerance in olive (Olea europaea L.) under low- or high-Ca2+ supply. - Environ. exp. Bot. 65: 72-81, 2009. Go to original source...
    40. Tuna, A.L., Kaya, C., Ashraf, M., Altunlu, H., Yokas, I., Yagmur, B.: The effects of calcium sulphate on growth, membrane stability and nutrient uptake of tomato plants grown under salt stress. - Environ. exp. Bot. 59: 173-178, 2007. Go to original source...
    41. Williams, V., Twine, S.: Flame photometeric method for sodium, potassium, and calcium. - In: Paech, K., Tracey, M.V. (ed.): Modern Methods of Plant Analysis. Vol. 5. Pp. 535. - Springer, Berlin 1960.
    42. Xu, X., Li, Y., Wang, B., Hu, J., Liao, Y.: Salt stress induced sex-related spatial heterogeneity of gas exchange rates over the leaf surface in Populus cathayana, Rehd.. - Acta Physiol. Plant. 37: 1709, 2015. Go to original source...
    43. Yang, B.Z., Liu, Z.B., Zhou, S.D., Ou, L.J., Dai, X.Z., Ma, Y.Q., Zhang, Z.Q., Chen, W.C., Li, X.F., Liang, C.L., Yang, S., Zou, X.X.: Exogenous Ca2+ alleviates waterlogging caused damages to pepper. - Photosynthetica 54: 1-11, 2016. Go to original source...
    44. Yang, F., Han, C., Li, Z., Guo, Y., Chan, Z.: Dissecting tissue- and species-specific responses of two Plantago species to waterlogging stress at physiological level. - Environ. exp. Bot. 109: 177-185, 2015. Go to original source...
    45. Yang, F., Wang, Y., Wang, J., Deng, W., Liao, L., Li, M.: Different eco-physiological responses between male and female Populus deltoides clones to waterlogging stress. - Forest Ecol. Manage. 262: 1963-1971, 2011. Go to original source...
    46. Yang, F., Wang, Y., Chan, Z.: Perspectives on screening winter-flood-tolerant woody species in the riparian protection forests of the Three Gorges Reservoir. - PLoS ONE 9: e108725, 2014. Go to original source...
    47. Zeng, F., Shabala, L., Zhou, M., Zhang, G., Shabala, S.: Barley responses to combined waterlogging and salinity stress: separating effects of oxygen deprivation and elemental toxicity. - Front. Plant Sci. 4: 313, 2013. Go to original source...

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