Biologia plantarum 64: 406-416, 2020 | DOI: 10.32615/bp.2020.017

Mannose regulates water balance, leaf senescence, and genes related to stress tolerance in white clover under osmotic stress

S.Y. ZHAO, W.H. ZENG, Z. LI*, Y. PENG
Department of Grassland Science, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 61130, P.R. China

Mannose (MAN), an important monosaccharide, contributes to coping with abiotic stresses in plants. Objectives of this study were to examine whether exogenous MAN (30 mM) could significantly increase drought tolerance and further to reveal MAN-regulated tolerance mechanism in white clover under osmotic stress induced by 18 % (m/v) polyethylene glycol 6000 for 10 d in controlled growth chambers. Results show that the application of MAN significanlty alleviated stress damage and the inhibition of growth and photosynthesis in white clover under osmotic stress. The MAN-induced increase in endogenous MAN content and the accumulation of organic osmolytes (proline and water soluble sugars) could be responsible for a lower osmotic potential (OP) in white clover. The exogenous application of MAN also enhanced antioxidant enzyme (superoxide dismutase, peroxidase, ascorbate peroxidase, dehydroascorbate reductase, and glutathione reductase) activities and maintained ascorbic acid content in white clover during osmotic stress. As concern chlorophyll (Chl) metabolism, the MAN-treated plants showed significantly higher transcription of genes involved in Chl synthesis Mg-chelatase and protochlorophyllide reductase and lower transcription of pheophorbide a oxygenase and chlorophyllase related to Chl degradation and also a senescence associated gene 101 than untreated plants. In addition, the MAN application increased transcription of SK2-, Y2K-, and Y2SK-type dehydrin genes, and dehydrin b in leaves of white clover under osmotic stress. These results indicate that MAN plays important roles in drought tolerance not only acting as a compatible solute for OP but also delaying leaf senescence through enhancing antioxidant metabolism, decreasing Chl degradation, and increasing transcription of dehydrin genes contributing to enhanced drought tolerance in white clover.

Keywords: antioxidants, dehydrins, osmotic potential, photosynthesis, senescence, Trifolium repens.

Received: December 2, 2019; Revised: January 28, 2020; Accepted: January 29, 2020; Published online: May 26, 2020Show citation

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ZHAO, S.Y., ZENG, W.H., LI, Z., & PENG, Y. (2020). Mannose regulates water balance, leaf senescence, and genes related to stress tolerance in white clover under osmotic stress. Biologia plantarum64, 406-416. doi: 10.32615/bp.2020.017.
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References

  1. Ai, T., Liao, X., Li, R., Fan, L., Luo, F., Xu, Y., Wang, S.: GDP-D-mannose pyrophosphorylase from Pogonatherum paniceum enhances salinity and drought tolerance of transgenic tobacco. - Z. Naturforsch. C. 71: 243-252, 2016. Go to original source...
  2. Ali, F., Bano, A., Fazal, A.: Recent methods of drought stress tolerance in plants. - Plant Growth Regul. 82: 1-13, 2017. Go to original source...
  3. Arnon, D.I.: Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. - Plant Physiol. 24: 1-15, 1949. Go to original source...
  4. Asada, K.: Ascorbate peroxidase - a hydrogen peroxide-scavenging enzyme in plants. - Physiol. Plant. 85: 235-241, 1992. Go to original source...
  5. Ashraf, M., Foolad, M.R.: Roles of glycine betaine and proline in improving plant abiotic stress resistance. - Environ. exp. Bot. 59: 206-216, 2007. Go to original source...
  6. Barrs, H,D., Weatherley, P.E.: A re-examination of the relative turgidity technique for estimating water deficits in leaves. - Aust. J. biol. Sci. 15: 413-428, 1962. 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. Bermejo, R., Irigoyen, J.J., Santamaria, J.M.: Short-term drought response of two white clover clones, sensitive and tolerant to O3. - Physiol. Plant. 127: 658-669, 2006. Go to original source...
  9. Bian, H.W., Wang, J.H., Lin, W.Q., Han, N., Zhu, M.Y.: Accumulation of soluble sugars, heat-stable proteins and dehydrins in cryopreservation of protocorm-like bodies of Dendrobium candidum by the air-drying method. - Plant Physiol. 159: 1139-1145, 2002. Go to original source...
  10. Biles, S.P., Cothren, J.T.: Flowering and yield response of cotton to application of mepiquat chloride and PGR-IV. - Crop Sci. 41: 1834-1837, 2001.
  11. Blum, A.: Osmotic adjustment and growth of barley genotypes under drought stress. - Crop Sci. 29: 230-233, 1989. Go to original source...
  12. Blum, A., Ebercon, A.: Cell membrane stability as a measure of drought and heat tolerance in wheat. - Crop Sci. 21: 43-47, 1981. Go to original source...
  13. Bollivar, D.W.: Recent advances in chlorophyll biosynthesis. - Photosynth. Res. 90: 173-194, 2006.
  14. 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...
  15. Buysse, J., Merckx, R.: An improved colorimetric method to quantify sugar content of plant tissue. - Environ. exp. Bot. 44: 1627-1629, 1993. Go to original source...
  16. Chu, A.X., Kong, X.S., Zhang, Y.Z.: Application of plant growth regulator on ornamental plant. - Acta hort. sin. 31: 408-412, 2004.
  17. Di Fonzo, N., Campanile, R.G., Stoppelli, M.C., Spano, G., Rascio, A., Russo, M., Trono, D., Padalino, L., Laus, M., De Vita, P., Troccoli, A., Flagella, Z., Shewry, P.R., Lawlor, D.: Resistance to abiotic stresses in durum wheat: which ideotype? - In: Royo, C. Nachit, M., Di Fonzo, N., Araus, J.L. (ed.): Durum Wheat Improvement in the Mediterranean Region: New Challenges. Pp. 215-225. CIHEAM, Zaragoza 2000.
  18. Elstner, E.F., Heupel, A.: Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. - Anal. Biochem. 70: 616-620, 1976. Go to original source...
  19. Eltayeb, A.E., Kawano, N., Badawi, G., Kaminaka, H., Sanekata, T., Morishima, I., Shibahara, T., Inanaga, S., Tanaka, K.: Enhanced tolerance to ozone and drought stresses in transgenic tobacco overexpressing dehydroascorbate reductase in cytosol. - Plant Cell Physiol. 127: 57-65, 2006. Go to original source...
  20. Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., Basra, S.M.A.: Plant drought stress: effects, mechanisms and management. - Agron. Sustain. Dev. 29: 185-212, 2009. Go to original source...
  21. Frame, J., Newbould, P.: Agronomy of white clover. - Adv. Agron. 40: 1-88, 1986. Go to original source...
  22. Giannopolitis, C.N., Ries, S.K.: Superoxide dismutases: I. occurrence in higher plants. - Plant Physiol. 59: 309-314, 1977. Go to original source...
  23. Hakimi, A.A., Monneveux, P., Galiba, G.: Soluble sugars, proline and relative water content (RWC) as traits for improving drought tolerance and divergent selection for RWC from T. polonicum into T. durum. - J. Genet. Plant Breed. 49: 237-243, 1995.
  24. Hameed, A., Iqbal, N., Malik, S.A.: Mannose-induced modulations in antioxidants, protease activity, lipid peroxidation, and total phenolics in etiolated wheat leaves. - J. Plant Growth Regul. 28: 58-65, 2009. Go to original source...
  25. Hameed, A., Iqbal, N.: Chemo-priming with mannose, mannitol and H2O2 mitigate drought stress in wheat. - Cereal. Res. Commun. 42: 450-462, 2014. Go to original source...
  26. Hameed, A., Goher, M., Iqbal, N.: Drought induced programmed cell death and associated changes in antioxidants, proteases and lipid peroxidation in wheat leaves. - Biol. Plant. 57: 370-374, 2013. Go to original source...
  27. Hanin, M., Brini, F., Ebel, C., Toda, Y., Takeda, S., Masmoudi, K.: Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms. - Plant Signal. Behav. 6: 1503-1509, 2011. Go to original source...
  28. Hasanuzzaman, M., Fujita, M.: Selenium pretreatment upregulates the antioxidant defense and methylglyoxal detoxification system and confers enhanced tolerance to drought stress in rapeseed seedlings. - Biol. Trace Elements Res. 143: 1758-1776, 2011. Go to original source...
  29. Hasegawa, P.M., Bressan, R.A., Zhu, J.K., Bohnert, H.J.: Plant cellular and molecular responses ro high salinity. - Annu. Rev. Plant Physiol. Plant mol. Biol. 51: 463-499, 2000. Go to original source...
  30. Heyen, B.J., Alsheikh, M.K., Smith, E.A., Torvik, C.F., Seals, D.F., Randall, S.K.: The calcium-binding activity of a vacuole-associated, dehydrin-like protein is regulated by phosphorylation. - Plant Physiol. 130: 675-687, 2002. Go to original source...
  31. Hoagland, D.R., Arnon, D.I.: The water-culture method for growing plants without soil. - Calif. Agr. Exp. Sta. Circ. 347: 357-359. 1950.
  32. Jespersen, D., Zhang, J., Huang, B.: Chlorophyll loss associated with heat-induced senescence in bentgrass. - Plant Sci. 249: 1-12, 2016. Go to original source...
  33. Kamaljit, K., Gupta, A.K., Narinder, K.: Effect of water deficit on carbohydrate status and enzymes of carbohydrate metabolism in seedlings of wheat cultivars. - Indian J. Biochem. Biophys. 44: 223-230, 2007.
  34. Kocsy, G., Laurie, R., Szila, G., Szilagyi, V., Simon-Sarkadi, L., Galiba, G., De Ronde, J.A.: Genetic manipulation of proline levels affects antioxidants in soybean subjected to simultaneous drought and heat stresses. - Physiol. Plant. 124: 227-235, 2005. Go to original source...
  35. Lambers, H., Shane, M.W., Cramer, M.D., Pearse, S.J., Veneklaas, E.J.: Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. - Ann. Bot. 98: 693-713, 2006. Go to original source...
  36. Li, Z., Jing, W., Peng, Y., Zhang, X., Ma, X., Huang, L., Yan, Y.: Spermine alleviates drought stress in white clover with different resistance by influencing carbohydrate metabolism and dehydrins synthesis. - Plos ONE 10: e0120708, 2015a. Go to original source...
  37. Li, Z., Peng, Y., Huang, B.: Alteration of transcripts of stress-protective genes and transcriptional factors by γ-aminobutyric acid (GABA) associated with improved heat and drought tolerance in creeping bentgrass (Agrostis stolonifera). - Int. J. mol. Sci. 19: 1623, 2018. Go to original source...
  38. Li, Z., Peng, D., Zhang, X., Peng, Y., Chen, M., Ma, X., Huang, L., Yan, Y.: Na+ induces the tolerance to water stress in white clover associated with osmotic adjustment and aquaporins-mediated water transport and balance in root and leaf. - Environ. exp. Bot. 144: 11-24, 2017b. Go to original source...
  39. Li, Z., Yu, J., Peng, Y., Huang, B.: Metabolic pathways regulated by abscisic acid, salicylic acid and γ-aminobutyric acid in association with improved drought tolerance in creeping bentgrass (Agrostis stolonifera). - Physiol. Plant. 159: 42-58, 2017a. Go to original source...
  40. Li, Z., Zhang, Y., Zhang, X., Peng, Y., Merewitz, E., Ma, X., Huang, L., Yan, Y.: The alterations of endogenous polyamines and phytohormones induced by exogenous application of spermidine regulate antioxidant metabolism, metallothionein and relevant genes conferring drought tolerance in white clover. - Environ. exp. Bot. 124: 22-38, 2016. Go to original source...
  41. Li, Z., Zhou, H., Peng, Y., Zhang, X., Ma, X., Huang, L., Yan, Y.: Exogenously applied spermidine improves drought tolerance in creeping bentgrass associated with changes in antioxidant defense, endogenous polyamines and phytohormones. - Plant Growth Regul. 76: 71-82, 2015b. Go to original source...
  42. Ma, L., Wang, Y., Liu, W., Liu, Z.: Overexpression of an alfalfa GDP-mannose 3, 5-epimerase gene enhances acid, drought and salt tolerance in transgenic Arabidopsis by increasing ascorbate accumulation. - Biotechnol. Lett. 36: 2331-2341, 2014. Go to original source...
  43. Ma, Q., Yue, L.J., Zhang, J.L., Wu, G.Q., Bao, A.K., Wang, S.M.: Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum. - Tree Physiol. 32: 4-13, 2012. Go to original source...
  44. Mckersie, B.D., Chen, Y., Beus, M., De, Bowley, S.R., Bowler, C., Inzé, D., D'Halluin, K., Botterman, J.: Superoxide dismutase enhances tolerance of freezing stress in transgenic alfalfa (Medicago sativa L.). - Plant Physiol. 103: 1155-1163, 1993. Go to original source...
  45. Nakano, Y., Asada, K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. - Plant Cell Physiol. 22: 867-880, 1981.
  46. Rosenvasser, S., Mayak, S., Friedman, H.: Increase in reactive oxygen species (ROS) and in senescence-associated gene transcript (SAG) levels during dark-induced senescence of Pelargonium cuttings, and the effect of gibberellic acid. - Plant Sci. 170: 873-879, 2006. Go to original source...
  47. Soares, C., De Sousa, A., Pinto, A., Azenha, M., Teixeira, J., Azevedo, R.A., Fidalgo, F.: Effect of 24-epibrassinolide on ROS content, antioxidant system, lipid peroxidation and Ni uptake in Solanum nigrum L. under Ni stress. - Environ. exp. Bot. 122: 115-125, 2016. Go to original source...
  48. Vaseva, I., Akiscan, Y., Demirevska, K., Anders, I., Feller, U.: Drought stress tolerance of red and white clover - comparative analysis of some chaperonins and dehydrins. - Sci. Hort. 130: 653-659, 2011. Go to original source...
  49. Velikova, V., Yordanov, I., Edreva, A.: Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. - Plant Sci. 151: 59-66, 2000. Go to original source...
  50. Verslues, P.E., Sharp, R.E.: Proline accumulation in maize (Zea mays L.) primary roots at low water potentials. II. Metabolic source of increased proline deposition in the elongation zone. - Plant Physiol. 119: 1349-1360, 1999. Go to original source...
  51. Wang, H.S., Yu, C., Zhu, Z.J., Yu, X.C.: Overexpression in tobacco of a tomato GMPase gene improves tolerance to both low and high temperature stress by enhancing antioxidation capacity. - Plant Cell Rep. 30: 1029-1040, 2011. Go to original source...
  52. Xia, X.J., Wang, Y.J., Zhou, Y.H., Tao, Y., Mao, W.H., Shi, K., Asami, T., Chen, Z., Yu, J.Q.: Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. - Plant Physiol. 150: 801-814, 2009. Go to original source...
  53. Yancey, P.H., Clark, M.E., Hand, S.C., Bowlus, R.D., Somero, G.N.: Living with water stress: evolution of osmolyte systems. - Science 217: 1214-1222, 1982. Go to original source...
  54. Zhang, J., Li, H., Xu, B., Li, J., Huang, B.: Exogenous melatonin suppresses dark-induced leaf senescence by activating the superoxide dismutase-catalase antioxidant pathway and down-regulating chlorophyll degradation in excised leaves of perennial ryegrass (Lolium perenne L.). - Front. Plant Sci. 7: 1500, 2016. Go to original source...
  55. Zhang, J., Yu, G., Wen, W., Ma, X., Xu, B., Huang, B.: Functional characterization and hormonal regulation of the pheophytinase gene LpPPH controlling leaf senescence in perennial ryegrass. - J. exp. Bot. 67: 935-945, 2015.
  56. Zhao, D., Oosterhuis, D.: Physiological response of growth chamber-grown cotton plants to the plant growth regulator PGR-IV under water-deficit stress. - Environ. exp. Bot. 38: 7-14, 1997. Go to original source...
  57. Zhao, G.Q., Wang, S.M., Ren, J.Z.: Research progress on genetic transformation and ecological adaptability in white clover. - Acta ecol. sin. 24: 592-598, 2004.
  58. Zlatev, Z., Lidon, F.C.: An overview on drought induced changes in plant growth, water relations and photosynthesis. - J. Sci. Food Agr. 24: 520-524, 2012.