Photosynthetica 2021, 59(1):84-94 | DOI: 10.32615/ps.2021.005

Exogenous salicylic acid ameliorates waterlogging stress damages and improves photosynthetic efficiency and antioxidative defense system in waxy corn

J. WANG, S.H. SHI, D.Y. WANG, Y. SUN, M. ZHU, F.H. LI
College of Agronomy, Specialty Corn Institute, Shenyang Agricultural University, 110866 Shenyang, Liaoning Province, China

Salicylic acid (SA) is an endogenous growth regulator. It is vital for the growth and development, photosynthesis, disease resistance, and abiotic stress tolerance of plants. This study aimed to investigate the effects of exogenous SA on photosynthetic characteristics and antioxidant system in the four-leaf-stage waxy corn inbred seedlings SY-MY13 (waterlogging-resistant) and SY-XT1 (waterlogging-sensitive) under waterlogging stress. Waterlogging stress negatively influenced the morphology, plant height, biomass, photosynthetic characteristics, and chlorophyll content of waxy corn seedlings, obstructing their growth and development. SY-MY13 exhibited better growth and photosynthesis than SY-XT1 under waterlogging, this was due to SY-MY13 possessed excellent scavenging ability to reactive oxygen species (ROS). However, the application of exogenous SA could not only reduce the accumulation of ROS and regulate the activities of antioxidant enzymes but also improve photosynthesis in leaves and promote the growth of seedlings. Hence, the results revealed that the potential of SA as a promising exogenous growth regulator mediated physiological and photosynthetic adaptation of waxy corn seedlings under waterlogging stress, which might prove helpful for other plants suffering from waterlogging stress.

Additional key words: antioxidant enzyme; chlorophyll fluorescence; photosynthetic characteristics; stomatal aperture; waterlogging tolerance.

Received: November 22, 2020; Revised: December 29, 2020; Accepted: January 12, 2021; Prepublished online: February 12, 2021; Published: March 18, 2021  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
WANG, J., SHI, S.H., WANG, D.Y., SUN, Y., ZHU, M., & LI, F.H. (2021). Exogenous salicylic acid ameliorates waterlogging stress damages and improves photosynthetic efficiency and antioxidative defense system in waxy corn. Photosynthetica59(1), 84-94. doi: 10.32615/ps.2021.005
Download citation

References

  1. Abedi T., Pakniyat H.: Antioxidant enzyme changes in response to drought stress in ten cultivars of oilseed rape (Brassica napus L.). - Czech J. Genet. Plant Breed. 46: 27-34, 2010. Go to original source...
  2. Ahmed S., Nawata E., Hosokawa M. et al.: Alterations in photosynthesis and some antioxidant enzymatic activities of mungbean subjected to waterlogging. - Plant Sci. 163: 117-123, 2002. Go to original source...
  3. Anee T.I., Nahar K., Rahman A. et al.: Oxidative damage and antioxidant defense in Sesamum indicum after different waterlogging durations. - Plants-Basel 8: 196, 2019. Go to original source...
  4. Arbona V., Hossain Z., López-Climent M.F. et al.: Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus. - Physiol. Plantarum 132: 452-466, 2008. Go to original source...
  5. Bai T., Li C., Ma F. et al.: Exogenous salicylic acid alleviates growth inhibition and oxidative stress induced by hypoxia stress in Malus robusta Rehd. - J. Plant. Growth Regul. 28: 358-366, 2009. Go to original source...
  6. Bansal R., Srivastava J.P.: Antioxidative defense system in pigeonpea roots under waterlogging stress. - Acta Physiol. Plant. 34: 515-522, 2012. Go to original source...
  7. Cai M.L., Zhang Q.L., Zheng X.T. et al.: Comparison of leaves and stems of Peaderia scandens (Lour.) Merr. in tolerance to low temperature. - Photosynthetica 58: 846-852, 2020. Go to original source...
  8. Chávez-Arias C.C., Gómez-Caro S., Restrepo-Díaz H.: Mitigation of the impact of vascular wilt and soil hypoxia on cape gooseberry plants by foliar application of synthetic elicitors. - HortScience 55: 121-132, 2019. Go to original source...
  9. Chavoushi M., Najafi F., Salimi A., Angaji S.A.: Effect of salicylic acid and sodium nitroprusside on growth parameters, photosynthetic pigments and secondary metabolites of safflower under drought stress. - Sci. Hortic.-Amsterdam 259: 108823, 2020. Go to original source...
  10. Dar M.H., Zaidi N.W., Waza S.A. et al.: No yield penalty under favorable conditions paving the way for successful adoption of flood tolerant rice. - Sci. Rep.-UK 8: 9245, 2018. Go to original source...
  11. Fariduddin Q., Khan T.A., Yusuf M. et al.: Ameliorative role of salicylic acid and spermidine in the presence of excess salt in Lycopersicon esculentum. - Photosynthetica 56: 750-762, 2017. Go to original source...
  12. Fukao T., Barrera-Figueroa B.E., Juntawong P., Peña-Castro J.M.: Submergence and waterlogging stress in plants: A review highlighting research opportunities and understudied aspects. - Front. Plant Sci. 10: 340, 2019. Go to original source...
  13. Gao Y., Xia J., Chen Y. et al.: Effects of extreme soil water stress on photosynthetic efficiency and water consumption characteristics of Tamarix chinensis in China's Yellow River Delta. - J. Forestry. Res. 28: 491-501, 2017. Go to original source...
  14. Gill M.B., Zeng F., Shabala L. et al.: Identification of QTL related to ROS formation under hypoxia and their association with waterlogging and salt tolerance in barley. - Int. J. Mol. Sci. 20: 699, 2019. Go to original source...
  15. Gul F., Arfan M., Shahbaz M., Basra S.M.A.: Salicylic acid seed priming modulates morphology, nutrient relations and photosynthetic attributes of wheat grown under cadmium stress. - Int. J. Agric. Biol. 23: 197-204, 2020.
  16. Jaiswal A., Srivastava J.P.: Nitric oxide mitigates waterlogging stress by regulating antioxidative defense mechanism in maize (Zea mays L.) root. - Bangl. J. Bot. 45: 517-524, 2016.
  17. Jia L., Qin X., Lyu D. et al.: ROS production and scavenging in three cherry rootstocks under short-term waterlogging conditions. - Sci. Hortic.-Amsterdam 257: 108647, 2019. Go to original source...
  18. Kamal A.H.M., Komatsu S.: Jasmonic acid induced protein response to biophoton emissions and flooding stress in soybean. - J. Proteomics 133: 33-47, 2016. Go to original source...
  19. Ketthaisong D., Suriharn B., Tangwongchai R., Lertrat K.: Combining ability analysis in complete diallel cross of waxy corn (Zea mays var. ceratina) for starch pasting viscosity characteristics. - Sci. Hortic.-Amsterdam 175: 229-235, 2014. Go to original source...
  20. Khalil N., Fekry M., Bishr M. et al.: Foliar spraying of salicylic acid induced accumulation of phenolics, increased radical scavenging activity and modified the composition of the essential oil of water stressed Thymus vulgaris L. - Plant. Physiol. Bioch. 123: 65-74, 2018. Go to original source...
  21. Kumar S.S., Kumar S.A., Padmanabh D.: Modulating effect of salicylic acid in tomato plants in response to waterlogging stress. - Int. J. Agric. Environ. Biotech. 10: 31-37, 2017. Go to original source...
  22. Lang M., Lichtenthaler H.K., Sowinska M. et al.: Fluorescence imaging of water and temperature stress in plant leaves. - J. Plant Physiol. 148: 613-621, 1996. Go to original source...
  23. Li J., Pang Z., Trivedi P. et al.: 'Candidatus Liberibacter asiaticus' encodes a functional salicylic acid (sa) hydroxylase that degrades sa to suppress plant defenses. - Mol. Plant Microbe In. 30: 620-630, 2017. Go to original source...
  24. Li R., Shang H., Wu H. et al.: Thermal inactivation kinetics and effects of drying methods on the phenolic profile and antioxidant activities of chicory (Cichorium intybus L.) leaves. - Sci. Rep.-UK 8: 9529, 2018. Go to original source...
  25. Li X.M., Zhang L.H., Li Y.Y. et al.: Changes in photosynthesis, antioxidant enzymes and lipid peroxidation in soybean seedlings exposed to UV-B radiation and/or Cd. - Plant Soil 352: 377-387, 2012. Go to original source...
  26. Lichtenthaler H.K., Langsdorf G., Lenk S., Buschmann C.: Chlorophyll fluorescence imaging of photosynthetic acti-vity with the flash-lamp fluorescence imaging system. - Photosynthetica 43: 355-369, 2005. Go to original source...
  27. Lone A.A., Khan M.H., Dar Z.A. et al.: Breeding strategies for improving growth and yield under waterlogging conditions in maize: A review. - Maydica 61: M2, 2016.
  28. Moravcová S., Tùma J., Kovalíková Duèaiová Z. et al.: Influence of salicylic acid pretreatment on seeds germination and some defence mechanisms of Zea mays plants under copper stress. - Plant. Physiol. Bioch. 122: 19-30, 2018. Go to original source...
  29. Nie W., Gong B., Chen Y. et al.: Photosynthetic capacity, ion homeostasis and reactive oxygen metabolism were involved in exogenous salicylic acid increasing cucumber seedlings tolerance to alkaline stress. - Sci. Hortic.-Amsterdam 235: 413-423, 2018. Go to original source...
  30. Ohkawa H., Ohishi N., Yagi K.: Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. - Anal. Biochem. 95: 351-358, 1979. Go to original source...
  31. Otie V., Ping A., Udo I., Eneji E.: Brassinolide effects on maize (Zea mays L.) growth and yield under waterlogged condi-tions. - J. Plant Nutr. 42: 954-969, 2019. Go to original source...
  32. Panozzo A., Dal Cortivo C., Ferrari M. et al.: Morphological changes and expressions of AOX1A, CYP81D8, and putative PFP genes in a large set of commercial maize hybrids under extreme waterlogging. - Front. Plant Sci. 10: 62, 2019. Go to original source...
  33. Park J.S., Lee E.J.: Waterlogging induced oxidative stress and the mortality of the Antarctic plant, Deschampsia antarctica. - J. Ecol. Environ. 43: 29, 2019. Go to original source...
  34. Patel M.K., Pandey S., Burritt D.J., Tran L.-S.P.: Plant responses to low-oxygen stress: Interplay between ROS and NO signaling pathways. - Environ. Exp. Bot. 161: 134-142, 2019. Go to original source...
  35. Perera-Castro A.V., Brito P., González-Rodríguez A.M.: Change in thermic limits and acclimation assessment for an alpine plant by chlorophyll fluorescence analysis: Fv/Fm vs. Rfd. - Photosynthetica 56: 527-536, 2018. Go to original source...
  36. 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...
  37. Posso D.A., Borella J., Reissig G.N., Bacarin M.A.: Root flooding-induced changes in the dynamic dissipation of the photosynthetic energy of common bean plants. - Acta Physiol. Plant. 40: 212, 2018. Go to original source...
  38. Ren B., Hu J., Zhang J. et al.: Spraying exogenous synthetic cytokinin 6-benzyladenine following the waterlogging improves grain growth of waterlogged maize in the field. - J. Agron. Crop Sci. 205: 616-624, 2019. Go to original source...
  39. Ren B., Zhang J., Dong S. et al.: Responses of carbon metabolism and antioxidant system of summer maize to waterlogging at different stages. - J. Agron. Crop Sci. 204: 505-514, 2018a. Go to original source...
  40. Ren B., Zhang J., Dong S. et al.: Exogenous 6-benzyladenine improves antioxidative system and carbon metabolism of summer maize waterlogged in the field. - J. Agron. Crop Sci. 204: 175-184, 2018b. Go to original source...
  41. Ren C.G., Kong C.C., Yan K. et al.: Elucidation of the molecular responses to waterlogging in Sesbania cannabina roots by transcriptome profiling. - Sci. Rep.-UK 7: 9256, 2017. Go to original source...
  42. Sairam R.K., Dharmar K., Chinnusamy V. et al.: NADPH oxidase as the source of ROS produced under waterlogging in roots of mung bean. - Biol. Plantarum 55: 741-746, 2011. Go to original source...
  43. Sayed S.A.E.: Ameliorative effects of salicylic acid on salt-stressed Lupinus albus plants growing under oxygen deficiency. - Phyton 54: 101-122, 2014. Go to original source...
  44. Spormann S., Soares C., Fidalgo F.: Salicylic acid alleviates glyphosate-induced oxidative stress in Hordeum vulgare L. - J. Environ. Manage. 241: 226-234, 2019. Go to original source...
  45. Sterling A., Rodríguez N., Quiceno E. et al.: Dynamics of photosynthetic responses in 10 rubber tree (Hevea brasiliensis) clones in Colombian Amazon: Implications for breeding strategies. - PLoS ONE 14: e0226254, 2019. Go to original source...
  46. Subbaiah C.C., Sachs M.M.: Clacium-mediated responses of maize to oxygen deprivation. - Russ. J. Plant Physl+ 50: 752-761, 2003. Go to original source...
  47. Syed N.H., Prince S.J., Mutava R.N. et al.: Core clock, SUB1, and ABAR genes mediate flooding and drought responses via alternative splicing in soybean. - J. Exp. Bot. 66: 7129-7149, 2015. Go to original source...
  48. Tian L.X., Li J., Bi W.S. et al.: Effects of waterlogging stress at different growth stages on the photosynthetic characteristics and grain yield of spring maize (Zea mays L.) under field conditions. - Agr. Water Manage. 218: 250-258, 2019. Go to original source...
  49. Wang C.Y.: Effect of temperature preconditioning on catalase, peroxidase, and superoxide dismutase in chilled zucchini squash. - Postharvest Biol. Tec. 5: 67-76, 1995. Go to original source...
  50. Wang H., Chen Y., Hu W. et al.: Short-term soil-waterlogging contributes to cotton cross tolerance to chronic elevated temperature by regulating ROS metabolism in the subtending leaf. - Plant Physiol. Bioch. 139: 333-341, 2019b. Go to original source...
  51. Wang J., Lv X., Wang H. et al.: Morpho-anatomical and physiological characteristics responses of a paired near-isogenic lines of waxy corn to waterlogging. - Emir. J. Food Agr. 31: 951-957, 2019a. Go to original source...
  52. Wassie M., Zhang W., Zhang Q. et al.: Exogenous salicylic acid ameliorates heat stress-induced damages and improves growth and photosynthetic efficiency in alfalfa (Medicago sativa L.). - Ecotox. Environ. Safe. 191: 110206, 2020. Go to original source...
  53. 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...
  54. Wollmer A.-C., Pitann B., Mühling K.H.: Waterlogging events during stem elongation or flowering affect yield of oilseed rape (Brassica napus L.) but not seed quality. - J. Agron. Crop Sci. 204: 165-174, 2018. Go to original source...
  55. Xia X.J., Wang Y.J., Zhou Y.H. et al.: Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. - Plant Physiol. 150: 801-814, 2009. Go to original source...
  56. Xu J., Zhu Y., Ge Q. et al.: Comparative physiological responses of Solanum nigrum and Solanum torvum to cadmium stress. - New Phytol. 196: 125-138, 2012. Go to original source...
  57. Xu L., Pan R., Shabala L. et al.: Temperature influences waterlogging stress-induced damage in Arabidopsis through the regulation of photosynthesis and hypoxia-related genes. - Plant Growth Regul. 89: 143-152, 2019. Go to original source...
  58. Xu X., Ji J., Ma X. et al.: Comparative proteomic analysis provides insight into the key proteins involved in cucumber (Cucumis sativus L.) adventitious root emergence under waterlogging stress. - Front. Plant Sci. 7: 1515, 2016. Go to original source...
  59. Yan K., Zhao S., Cui M. et al.: Vulnerability of photosynthesis and photosystem I in Jerusalem artichoke (Helianthus tuberosus L.) exposed to waterlogging. - Plant. Physiol. Bioch. 125: 239-246, 2018. Go to original source...
  60. Yang F., Miao L.F.: Adaptive responses to progressive drought stress in two poplar species originating from different altitudes. - Silva Fenn. 44: 23-37, 2010. Go to original source...
  61. Yin X., Hiraga S., Hajika M. et al.: Transcriptomic analysis reveals the flooding tolerant mechanism in flooding tolerant line and abscisic acid treated soybean. - Plant Mol. Biol. 93: 479-496, 2017. Go to original source...
  62. Yin X., Komatsu S.: Comprehensive analysis of response and tolerant mechanisms in early-stage soybean at initial-flooding stress. - J. Proteomics 169: 225-232, 2017. Go to original source...
  63. Yousefzadeh Najafabadi M., Ehsanzadeh P.: Photosynthetic and antioxidative upregulation in drought-stressed sesame (Sesamum indicum L.) subjected to foliar-applied salicylic acid. - Photosynthetica 55: 611-622, 2017. Go to original source...
  64. Zaid A., Mohammad F., Wani S.H., Siddique K.M.H.: Salicylic acid enhances nickel stress tolerance by up-regulating antioxidant defense and glyoxalase systems in mustard plants. - Ecotox. Environ. Safe. 180: 575-587, 2019. Go to original source...
  65. Zhang M., He S., Zhan Y. et al.: Exogenous melatonin reduces the inhibitory effect of osmotic stress on photosynthesis in soybean. - PLoS ONE 14: e0226542, 2019b. Go to original source...
  66. Zhang R.D., Zhou Y.F., Yue Z.X. et al.: Changes in photosynthesis, chloroplast ultrastructure, and antioxidant metabolism in leaves of sorghum under waterlogging stress. - Photosynthetica 57: 1076-1083, 2019a. Go to original source...
  67. Zheng C., Jiang D., Liu F. et al.: Effects of salt and waterlogging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat. - Plant Sci. 176: 575-582, 2009. Go to original source...
  68. Zhu M., Wang J., Li F., Shi Z.: Physiological and photosynthesis response of popcorn inbred seedings to waterlogging stress. - Pak. J. Bot. 47: 2069-2075, 2015.
  69. Zhu X., Shi H., Li X., Jin S.: Salicylic acid induces physiological and biochemical changes in peony under waterlogging stress. - Acta Sci. Pol.-Hortoru. 19: 41-52, 2020. Go to original source...