biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 66:56-66, 2022 | DOI: 10.32615/bp.2021.062

Responses of woody plant Dalbergia odorifera treated with glycine betaine to drought and cold stresses: involvement of the alternative oxidase

E.H.M. CISSE, D.-D. LI, J. ZHANG, L.-Y. GUO, L.-F. MIAO*, F. YANG*
School of Ecological and Environmental Sciences, 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

Woody plants faced multiple abiotic stresses in forest plantation that can influence their growth and development. Dalbergia odorifera T. Chen is a vulnerably endangered tree species, and references about its responses to abiotic stresses are very rare in literature. Furthermore, the mechanisms underlying the abiotic stress tolerance in plants induced by exogenous glycine betaine (GB) remains unclear. Indeed, the alternative oxidase (AOX) is one of the major components of antioxidant enzymatic machinery, and there are no studies that focused on the effects of GB on the amount of AOX protein in plants under drought or cold stresses. Thus, the aim of this study was to investigate the effect of exogenous GB on the phenotype, osmoprotectants, photosynthetic pigments, and antioxidant systems in D. odorifera under cold and drought stresses. The layout of the trial was a factorial experiment in a completely randomized design using two factors including abiotic stress (drought and cold) and GB. Moreover, the principal component analysis based on the measured parameters manifested how the selected ROS scavengers were dispersed throughout the treatments. The results showed huge beneficial impacts of GB on the phenotypic traits of D. odorifera; GB also influences positively the antioxidant machinery, photosynthetic pigments, redox-homeostasis, and water status in D. odorifera seedlings under both stresses. Moreover, exogenous GB affects more the AOX pathway in D. odorifera under cold stress than under drought stress.

Keywords: AOX, APX, CAT, chilling, chlorophyll, Dalbergia odorifera, drought, glycine betaine, homeostasis, oxidative stress, peroxidase, ROS, SOD.

Received: March 12, 2021; Revised: September 28, 2021; Accepted: October 22, 2021; Published online: March 8, 2022  Show citation

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CISSE, E.H.M., LI, D.-D., ZHANG, J., GUO, L.-Y., MIAO, L.-F., & YANG, F. (2022). Responses of woody plant Dalbergia odorifera treated with glycine betaine to drought and cold stresses: involvement of the alternative oxidase. Biologia plantarum, 66, Article 56-66. https://doi.org/10.32615/bp.2021.062
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    References

    1. Aebi, H.: Catalase in vitro. - Method. Enzymol. 105: 121-126, 1984. Go to original source...
    2. Agboma, P.C., Sinclair, T.R., Jokinen, K., Peltonen-Sainio, P., Pehu, E.: An evaluation of the effect of exogenous glycinebetaine on the growth and yield of soybean: timing of application, watering regimes and cultivars. - Field Crops Res. 54: 51-64, 1997. Go to original source...
    3. Allard, F., Houde, M., Krol, M., Ivanov, A., Huner, N.P.A., Sarhan, F.: Betaine improves freezing tolerance in wheat. - Plant Cell Physiol. 39: 1194-1202, 1998. Go to original source...
    4. Annunziata, M.G., Ciarmiello, L.F., Woodrow, P., Dell'Aversana, E., Carillo, P.: Spatial and temporal profile of glycinebetaine accumulation in plants under abiotic stresses. - Front. Plant Sci. 10: 230, 2019. Go to original source...
    5. Banu, M.N.A., Hoque, M.A., Watanabe-Sugimoto, M., Islam, M.M., Uraji, M., Matsuoka, K., Nakamura, Y., Murata, Y.: Proline and glycinebetaine ameliorated NaCl stress via scavenging of hydrogen peroxide and methylglyoxal but not superoxide or nitric oxide in tobacco cultured cells. - Biosci. Biotechnol. Biochem. 74: 2043-2049, 2010. Go to original source...
    6. Baker, J.C., Mock, N.M.: An improved method for monitoring cell death in cell suspension and leaf disc assays using evans blue. - Plant Cell Tissue Organ Cult. 39: 7-12, 1994. Go to original source...
    7. Bates, L.S., Waldren, R.P., Teare, I.D.: Rapid determination of free proline for water-stress studies. - Plant Soil 39: 205-207, 1973. Go to original source...
    8. Berthold, D.A., Andersson, M.E., Nordlund, P.: New insight into the structure and function of the alternative oxidase. - Biophys. Acta 1460: 241-254, 2000. Go to original source...
    9. 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...
    10. Caliskan, O., Radusiene, J., Temizel, K.E., Staunis, Z., Cirak, C., Kurt, D., Odabas, M.S.: The effects of salt and drought stress on phenolic accumulation in greenhouse-grown Hypericum pruinatum. - Ital. J. Agron. 12: 271-275, 2017. Go to original source...
    11. Cernoch, V., Kopecky, D.: Drought tolerance and regrowth capacity revealed in the Festuca-Lolium complex. - Biol. Plant. 64: 561-568, 2020. Go to original source...
    12. Chen, T.H.H., Murata, N.: Glycinebetaine: an effective protectant against abiotic stress in plants. - Trends Plant Sci. 13: 499-505, 2008. Go to original source...
    13. Chen, W.P., Li, P.H., Chen, T.H.H.: Glycinebetaine increases chilling tolerance and reduces chilling-induced lipid peroxidation in Zea mays L. - Plant Cell Environ. 23: 609-618, 2000. Go to original source...
    14. Cisse, E.H.M., Miao, L.F., Yang, F., Huang, J.F., Li, D.D., Zhang, J.: Glycibetaine surpasses melatonin to improve salt tolerance in Dalbergia odorifera. - Front. Plant Sci. 12: 588847, 2021a. Go to original source...
    15. Cisse, E.H.M., Zhang, L.J., Pu, Y.J., Miao, L.F., Li, DD., Zhang, J., Yang, F.: Exogenous Ca2+ associated with melatonin alleviates drought-induced damage in the woody tree Dalbergia odorifera. - J. Plant Growth Regul. 64, 2021b. Go to original source...
    16. Das, K., Roychoudhury, A.: Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. - Front. environ. Sci. 2: 53, 2014. Go to original source...
    17. Demidchik, V.: Mechanisms of oxidative stress in plants: From classical chemistry to cell biology. - Environ. exp. Bot. 109: 212-228, 2015. Go to original source...
    18. Demiral, T., Türkan, I.: Does exogenous glycinebetaine affect antioxidative system of rice seedlings under NaCl treatment? - J. Plant Physiol. 161: 1089-1100, 2004. Go to original source...
    19. Ellman, G.L.: Tissue sulfhydryl groups. - Arch. Biochem. Biophys. 82: 70-77, 1959. Go to original source...
    20. Escalante-Magaña, C., Aguilar-Caamal, L.F., Echevarría-Machado, I., Medina-Lara, F., Cach, L.S., Martínez-Estévez, M.: Contribution of glycinebetaine and proline to water deficit tolerance in pepper plants. - HortScience 54: 1044-1054, 2019. Go to original source...
    21. Fan, J., Hu, Z., Xie, Y., Chan, Z., Chen, K., Amombo, E., Chen, L., Fu, J.: Alleviation of cold damage to photosystem II and metabolisms by melatonin in Bermudagrass. - Front. Plant Sci. 6: 925, 2015. Go to original source...
    22. Farooq, M., Basra, S.M.A., Wahid, A., Cheema, Z.A., Cheema, M.A., Khaliq, A.: Physiological role of exogenously applied glycinebetaine to improve drought tolerance in fine grain aromatic rice (Oryza sativa L.). - J. Agron. Crop Sci. 194: 325-333, 2008. Go to original source...
    23. Fielding, J.L., Hall, J.L.: A biochemical and cytochemical study of peroxidase activity in roots of Pisum sativum. - J. exp. Bot. 29: 983-991, 1978. Go to original source...
    24. Khan, M.I.R., Asgher, M., Khan, N.A.: Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). - Plant Physiol. Biochem. 80: 67-74, 2014. Go to original source...
    25. Kumar, P.: Stress amelioration response of glycine betaine and arbuscular mycorrhizal fungi in sorghum under Cr toxicity. - PLoS ONE 16: e0253878, 2021a. Go to original source...
    26. Kumar, P.: Soil applied glycine betaine with arbuscular mycorrhizal fungi reduces chromium uptake and ameliorates chromium toxicity by suppressing the oxidative stress in three genetically different sorghum (Sorghum bicolor L.) cultivars. - BMC Plant Biol. 21: 336, 2021b. Go to original source...
    27. Kumar, P.: Evaluation of toxic effects of hexavalent chromium on the yield and quality of sorghum. - Enliven J. Diet. Res. Nutr. 7: 1-11, 2020. Go to original source...
    28. Kumar, P., Tokas, J., Singal, H.R.: Amelioration of chromium VI toxicity in sorghum (Sorghum bicolor L.) using glycine betaine. - Sci. Rep. 9: 1-15, 2019. Go to original source...
    29. Li, X.W., Chen, Q.X., Lei, H.Q., Wang, J.W., Yang, S., Wei, H.X.: Nutrient uptake and utilization by fragrant rosewood (Dalbergia odorifera) seedlings cultured with oligosaccharide addition under different lighting spectra. - Forests 9: 29, 2018. Go to original source...
    30. Lichtenthaler, H.K., Wellburn, A.R.: Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. - Biochem. Soc. Trans. 11: 591-592, 1983. Go to original source...
    31. Ma, Q.Q., Wang, W., Li, Y.H., Li, D.Q., Zou, Q.: Alleviation of photoinhibition in drought-stressed wheat (Triticum aestivum) by foliar-applied glycinebetaine. - J. Plant Physiol. 163: 165-175, 2006. Go to original source...
    32. Ma, X.L., Wang, Y.J., Xie, S.L., Wang, C., Wang, W.: Glycine betaine application ameliorates negative effects of drought stress in tobacco. - Russ. J. Plant Physiol. 54: 472, 2007. Go to original source...
    33. Mäkelä, P., Kleemola, J., Jokinen, K., Mantila, J., Pehu, E., Peltonen-Sainio, P.: Growth response of pea and summer turnip rape to foliar application of glycinebetaine. - Acta agr. scand. Sect. B - Soil Plant Sci. 47: 168-175, 1997. Go to original source...
    34. Mäkelä, P., Kontturi, M., Pehu, E., Somersalo, S.: Photosynthetic response of drought- and salt-stressed tomato and turnip rape plants to foliar-applied glycinebetaine. - Physiol. Plant. 105: 45-50, 1999. Go to original source...
    35. Mäkelä, P., Mantila, J., Hinkkanen, R., Pehu, E., Peltonen-Sainio, P.: Effect of foliar applications of glycine betaine on stress tolerance, growth, and yield of spring cereals and summer turnip rape in Finland. - J. Agron. Crop Sci. 176: 223-234, 1996. Go to original source...
    36. Malekzadeh, P.: Influence of exogenous application of glycinebetaine on antioxidative system and growth of salt-stressed soybean seedlings (Glycine max L.). - Physiol. mol. Biol. Plants 21: 225-32, 2015. Go to original source...
    37. Mróz, T.L., Havey, M.J., Bartoszewski, G.: Cucumber possesses a single terminal alternative oxidase gene that is upregulated by cold stress and in the mosaic (MSC) mitochondrial mutants. - Plant mol. Biol. Rep. 33: 1893-1906, 2015. Go to original source...
    38. Osman, H.S.: Enhancing antioxidant-yield relationship of pea plant under drought at different growth stages by exogenously applied glycine betaine and proline. - Ann. agr. Sci. 60: 389-402, 2015. Go to original source...
    39. Park, E.J., Jeknic, Z., Chen, T.H.H.: Exogenous application of glycine betaine increases chilling tolerance in tomato plants. - Plant Cell Physiol. 47: 706-714, 2006. Go to original source...
    40. Pu, Y.-J., Cisse, E.H.M., Zhang, L.-J., Nawaz, M., Yang, F.: Coupling exogenous melatonin with Ca2+ alleviated chillimng stress in Dalbergia odorifera T. Chen. - Trees 65: 1541-1554, 2021. Go to original source...
    41. Raza, M.A., Saleem, M., Shah, G., Khan, I., Raza, A.: Exogenous application of glycinebetaine and potassium for improving water relations and grain yield of wheat under drought. - J. Soil Sci. Plant Nutr. 14: 348-364, 2014. Go to original source...
    42. Raza, S.H., Athar, H.R., Ashraf, M., Hameed, A.: Glycinebetaine-induced modulation of antioxidant enzymes activities and ion accumulation in two wheat cultivars differing in salt tolerance. - Environ. exp. Bot. 60: 368-376, 2007. Go to original source...
    43. Ritonga, F.N., Chen, S.: Physiological and molecular mechanism involved in cold stress tolerance in plants. - Plants 9: 560, 2020. Go to original source...
    44. Saha, B., Borovskii, G., Panda, S.K.: Alternative oxidase and plant stress tolerance. - Plant Signal. Behav. 11: e125630, 2016. Go to original source...
    45. Shan, T., Jin, P., Zhang, Y., Huang, Y., Wang, X., Zheng, Y.: Exogenous glycine betaine treatment enhances chilling tolerance of peach fruit during cold storage. - Postharvest Biol. Technol. 114: 104-110, 2016. Go to original source...
    46. Sharma, A., Kumar, V., Shahzad, B., Ramakrishnan, M., Singh Sidhu, G.P., Bali, A., Handa, N., Kapoor, D., Yadav, P., Khanna, K., Bakshi, P., Rehman, A., Kohli, S.K., Khan, E.A., Parihar, R.D., Yuan, H., Thukral, A.K., Bhardwaj, R., Zheng, B.: Photosynthetic response of plants under different abiotic stresses: a review. - J. Plant Growth Regul. 39: 509-531, 2020. Go to original source...
    47. Sharma, A., Shahzad, B., Kumar, V., Kohli, S.K., Sidhu, G.P.S., Bali, A.S., Handa, N., Kapoor, D., Bhardwaj, R., Zheng, B.: Phytohormones regulate accumulation of osmolytes under abiotic stress. - Biomolecules 9: 285, 2019. Go to original source...
    48. Sies, H.: Strategies of antioxidant defence. - Eur. J. Biochem. 215: 213-219, 1993. Go to original source...
    49. Staniak, M., Bojarszczuk, J., Kraska, P., Kwiatkowski, C., Harasim, E.: Prolonged drought stress induced changes in yield and physiological processes of Trifolium repens and Festulolium braunii. - Biol. Plant. 64: 701-709, 2020. Go to original source...
    50. Swain, T., Hillis, W.E.: The phenolic constituents of Prunus domestica. I. The quantitative analysis of phenolic constituents. - J. Sci. Food Agr. 10: 63-68, 1959. Go to original source...
    51. Tian, F., Wang, W., Liang, C., Wang, X., Wang, G., Wang, W.: Overaccumulation of glycine betaine makes the function of the thylakoid membrane better in wheat under salt stress. - Crop J. 5: 73-82, 2017. Go to original source...
    52. Varela, M.C., Arslan, I., Reginato, M.A., Cenzano, A.M., Luna, M.V.: Phenolic compounds as indicators of drought resistance in shrubs from Patagonian shrublands (Argentina). - Plant Physiol. Biochem. 104: 81-91, 2016. Go to original source...
    53. Wanner, L.A., Junttila, O.: Cold-induced freezing tolerance in Arabidopsis. - Plant Physiol. 120: 391-400, 1999. Go to original source...
    54. Wikberg, J., Ogren, E.: Variation in drought resistance, drought acclimation and water conservation in four willow cultivars used for biomass production. - Tree Physiol. 27: 1339-1346, 2007. Go to original source...
    55. Xu, Z., Sun, M., Jiang, X., Sun, H., Dang, X., Cong, H., Qiao, F.: Glycine betaine biosynthesis in response to osmotic stress depends on jasmonate signaling in watermelon suspension cells. Front. Plant Sci. 9: 1469, 2018. Go to original source...
    56. Yancey, P.H.: Compatible and counteracting solutes. - In Strange, K. (ed.): Cellular and Molecular Physiology of Cell Volume Regulation. Vol. 5. Pp. 81-109. CRC-Press, Boca Raton 1994. Go to original source...
    57. Yang, F., Wang, Y., Miao, L.F.: Comparative physiological and proteomic responses to drought stress in two poplar species originating from different altitudes. - Physiol. Plant. 139: 388-400, 2010. Go to original source...
    58. Yemm, E.W., Willis, A.J.: The estimation of carbohydrates in plant extracts by anthrone. - Biochem. J. 57: 508-514, 1954. Go to original source...
    59. Zagorchev, L., Seal, C., Kranner, I., Odjakova, M.: A central role for thiols in plant tolerance to abiotic stress. - Int. J. Mol. Sci. 14: 7405-32, 2013. Go to original source...

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