Skip to main content

Explicating physiological and biochemical responses of wheat cultivars under acidity stress: insight into the antioxidant defense and glyoxalase systems

Abstract

Soil acidity causes proton (H+) rhizotoxicity, inhibits plant growth and development, and is a major yield-limiting factor for wheat production worldwide. Therefore, we investigated the physiological and biochemical responses of wheat (Triticum aestivum L.) to acidity stress in vitro. Five popular wheat cultivars developed by Bangladesh Agricultural Research Institute (BARI), namely, BARI Gom-21, BARI Gom-24, BARI Gom-25, BARI Gom-26, and BARI Gom-30, were studied in growing media under four different pH levels (3.5, 4.5, 5.5, and 6.5). We evaluated the cultivars based on their relative water content, proline (Pro) content, growth, biomass accumulation, oxidative damage, membrane stability, and mineral composition, as well as the performance of the antioxidant defense and glyoxalase systems. Although decrements of pH significantly reduced the tested morphophysiological and biochemical attributes in all the cultivars, there was high variability among the cultivars in response to the varying pH of the growing media. Acidity stress reduced growth, biomass, water content, and chlorophyll content in all the cultivars. However, BARI Gom-26 showed the least damage, with the lowest H2O2 generation, lipid peroxidation (MDA), and greater membrane stability, which indicate better tolerance against oxidative damage. In addition, the antioxidant defense components, ascorbate (AsA) and glutathione (GSH), and their redox balance were higher in this cultivar. Maximum H2O2 scavenging due to upregulation of the antioxidant enzymes [AsA peroxidase (APX), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), GSH reductase (GR), GSH peroxidase (GPX), and GSH-S-transferase (GST)] was observed in BARI Gom-26, which also illustrated significant enhancement of methylglyoxal (MG) detoxification by upregulating glyoxalase I (Gly I) and glyoxalase II (Gly II). This study also showed that balanced essential nutrient content as well as lower toxic micronutrient content was found in BARI Gom-26. Therefore, considering the physiological and biochemical attributes and growth, we conclude that BARI Gom-26 can withstand acidity stress during the early seedling stage, by regulating the coordinated action of the antioxidant defense and glyoxalase systems as well as maintaining nutrient balance.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Addinsoft (2018) XLSTAT V. 2018.1.01: data analysis and statistics software for Microsoft Excel. Addinsoft, Paris

    Google Scholar 

  2. Amist N, Singh NB (2017) Responses of enzymes involved in proline biosynthesis and degradation in wheat seedlings under stress. Allelopathy J 42:195–205

    Article  Google Scholar 

  3. Angelini J, Taurian T, Morgante C, Ibáñez F, Castro S, Fabra A (2005) Peanut nodulation kinetics in response to low pH. Plant Physiol Biochem 43:754–759

    Article  CAS  PubMed  Google Scholar 

  4. Anugoolprasert O, Kinoshita S, Naito H, Shimizu M, Ehara H (2012) Effect of low pH on the growth, physiological characteristics and nutrient absorption of sago palm in a hydroponic system. Plant Prod Sci 15:125–131. https://doi.org/10.1626/pps.15.125

    Article  CAS  Google Scholar 

  5. Bhuyan MHMB, Hasanuzzaman M, Mahmud JA, Hossain M, Bhuiyan TF, Fujita M (2019) Unraveling morphophysiological and biochemical responses of Triticum aestivum L. to extreme pH: coordinated actions of antioxidant defense and glyoxalase systems. Plants 8(1):24. https://doi.org/10.3390/plants8010024

    Article  PubMed Central  Google Scholar 

  6. Bradford MM (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  7. Chen F, Wang F, Wu F, Mao W, Zhang G, Zhou M (2010) Modulation of exogenous glutathione in antioxidant defense system against Cd stress in the two barley genotypes differing in Cd tolerance. Plant Physiol Biochem 48:663–672

    Article  CAS  PubMed  Google Scholar 

  8. Chen J, Wang WH, Liu TW, Wu FH, Zheng HL (2013) Photosynthetic and antioxidant responses of Liquidambar formosana and Schima superba seedlings to sulfuric-rich and nitric-rich simulated acid rain. Plant Physiol Biochem 64:41–51

    Article  CAS  PubMed  Google Scholar 

  9. CIMMYT (2017) International Maize and Wheat Improvement Center. https://wheat.org/wheat-in-the-world/. Accessed 18 Oct 2018

  10. Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

    Article  CAS  Google Scholar 

  11. Doderer A, Kokkelink I, van der Veen S, Valk B, Schram A, Douma A (1992) Purification and characterization of two lipoxygenase isoenzymes from germinating barley. Biochim Biophys Acta 112:97–104

    Article  Google Scholar 

  12. Du J, Cullen JJ, Buettner GR (2012) Ascorbic acid: chemistry, biology and the treatment of cancer. Biochim Biophys Acta 1826:443–457

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Elia AC, Galarini R, Taticchi MI, Dorr AJM, Mantilacci L (2003) Antioxidant responses and bioaccumulation in Ictalurus melas under mercury exposure. Ecotoxicol Environ Saf 55:162–167

    Article  CAS  PubMed  Google Scholar 

  14. El-Shabrawi H, Kumar B, Kaul T, Reddy MK, Singla-Pareek SL, Sopory SK (2010) Redox homeostasis, antioxidant defense, and methylglyoxal detoxification as markers for salt tolerance in Pokkali rice. Protoplasma 245:85–96

    Article  CAS  PubMed  Google Scholar 

  15. Fraire-Velázquez S, Balderas-Hernández VE (2013) Abiotic stress in plants and metabolic responses. In: Vahdati K (ed) Abiotic stress-plant responses and applications in agriculture. InTech, Rijeka, pp 25–48

    Google Scholar 

  16. Gabara B, Sklodowska M, Wyrwicka A, Glinska S, Gapinska M (2003) Changes in the ultrastructure of chloroplasts and mitochondria and antioxidant enzyme activity in Lycopersicon esculentum Mill. leaves sprayed with acid rain. Plant Sci 164:507–516

    Article  CAS  Google Scholar 

  17. George E, Horst WJ, Neumann E (2012) Adaptation of plants to adverse chemical soil conditions. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic Press, London, pp 409–472

    Chapter  Google Scholar 

  18. Gill SS, Anjum NA, Gill R, Yadav S, Hasanuzzaman M, Fujita M, Mishra P, Sabat SC, Tuteja N (2015) Superoxide dismutase—mentor of abiotic stress tolerance in crop plants. Environ Sci Pollut Res 22:10375–10394

    Article  CAS  Google Scholar 

  19. Hasanuzzaman M, Nahar K, Fujita M (2014) Alteration in chlorophylls and carotenoids in higher plants under abiotic stress condition. In: Golovko TK, Gruszecki WI, Prasad MNV, Strzałka K (eds) Photosynthetic pigments: chemical structure, biological function and ecology. Syktyvkar, Russia, pp 218–264

    Google Scholar 

  20. Hasanuzzaman M, Nahar K, Hossain MS, Mahmud JA, Rahman A, Inafuku M, Oku H, Fujita M (2017) Coordinated actions of glyoxalase and antioxidant defense systems in conferring abiotic stress tolerance in plants. Int J Mol Sci 18:200. https://doi.org/10.3390/ijms18010200

    Article  CAS  PubMed Central  Google Scholar 

  21. Hasanuzzaman M, Nahar K, Alam MM, Bhuyan MHMB, Oku H, Fujita M (2018) Exogenous nitric oxide pretreatment protects Brassica napus L. seedlings from paraquat toxicity through the modulation of antioxidant defense and glyoxalase systems. Plant Physiol Biochem 126:173–186

    Article  CAS  PubMed  Google Scholar 

  22. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil, 2nd edn. Circular. California agricultural experiment station, CA

  23. Hoque TS, Hossain MA, Mostofa MG, Burritt DJ, Fujita M, Tran LSP (2016) Methylglyoxal: an emerging signaling molecule in plant abiotic stress responses and tolerance. Front Plant Sci 7:1341. https://doi.org/10.3389/fpls.2016.01341

    Article  PubMed  PubMed Central  Google Scholar 

  24. Hossain MA, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in the regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol 25:385–395

    CAS  Google Scholar 

  25. Islam AKMS, Edwards DG, Asher CJ (1980) pH optima for crop growth. Results of a flowing solution culture experiment with six species. Plant Soil 54:339–357. https://doi.org/10.1007/BF02181830

    Article  Google Scholar 

  26. Ivanov Y, Savochkin Y, Kuznetsov V (2013) Effect of mineral composition and medium pH on Scots pine tolerance to toxic effect of zinc ions. Russ J Plant Physiol 60:260–269

    Article  CAS  Google Scholar 

  27. Joliot P, Johnson GN (2011) Regulation of cyclic and linear electron flow in higher plants. Proc Nat Acad Sci USA 108:13317–13322

    Article  PubMed  Google Scholar 

  28. Kaur C, Singla-Pareek SL, Sopory SK (2014) Glyoxalase and methylglyoxal as biomarkers for plant stress tolerance. Crit Rev Plant Sci 33:429–456

    Article  CAS  Google Scholar 

  29. Kaur C, Kushwaha HR, Mustafiz A, Pareek A, Sopory SK, Singla-Pareek SL (2015) Analysis of global gene expression profile of rice in response to methylglyoxal indicates its possible role as a stress signal molecule. Front Plant Sci 6:682. https://doi.org/10.3389/fpls.2015.00682

    Article  PubMed  PubMed Central  Google Scholar 

  30. Kidd PS, Proctor J (2001) Why plants grow poorly on very acid soils: are ecologists missing the obvious? J Exp Bot 52:791–799

    Article  CAS  PubMed  Google Scholar 

  31. Kochian LV, Piñeros MA, Liu J, Magalhães JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol 66:571–598

    Article  CAS  PubMed  Google Scholar 

  32. Lawson T, Vialet-Chabrand S (2018) Speedy stomata, photosynthesis and plant water use efficiency. New Phytol 122:122. https://doi.org/10.1111/nph.15330

    Article  Google Scholar 

  33. Long A, Zhang J, Yang LT, Ye X, Lai NW, Tan LL, Lin D, Chen LS (2017) Effects of low pH on photosynthesis, related physiological parameters, and nutrient profiles of Citrus. Front Plant Sci 8:185. https://doi.org/10.3389/fpls.2017.00185

    Article  PubMed  PubMed Central  Google Scholar 

  34. Mahmud JA, Hasanuzzaman M, Nahar K, Bhuyan MHMB, Fujita M (2018) Insights into citric acid-induced cadmium tolerance and phytoremediation in Brassica juncea L.: Coordinated functions of metal chelation, antioxidant defense and glyoxalase systems. Ecotoxicol Environ Saf 147:990–1001

    Article  CAS  PubMed  Google Scholar 

  35. Martins N, Goncalves S, Romano A (2013) Metabolism and aluminum accumulation in Plantago almogravensis and P. algarbiensis in response to low pH and aluminum stress. Biol Plant 57:325–331

    Article  CAS  Google Scholar 

  36. Miransari M, Balakrishnan P, Smith D, Mackenzie AF, Bahrami HA, Malakouti MJ, Rejali F (2006) Overcoming the stressful effect of low pH on soybean root hair curling using lipochitooligosacharides. Commun Soil Sci Plant Anal 37:1103–1110

    Article  CAS  Google Scholar 

  37. Nahar K, Hasanuzzaman M, Suzuki T, Fujita M (2017) Polyamines-induced aluminum tolerance in mung bean: a study on antioxidant defense and methylglyoxal detoxification systems. Ecotoxicology 26:58–73

    Article  CAS  PubMed  Google Scholar 

  38. Premachandra GS, Saneoka H, Ogata S (1990) Cell membrane stability, an indicator of drought tolerance, as affected by applied nitrogen in soyabean. J Agric Sci 115:63–66

    Article  CAS  Google Scholar 

  39. Principato GB, Rosi G, Talesa V, Giovanni E, Uotila L (1987) Purification and characterization of two forms of glyoxalase II from the liver and brain of Wistar rats. Biochim Biophys Acta Protein Struct Mol Enzymol 911:349–355

    Article  CAS  Google Scholar 

  40. Qiao F, Zhang XM, Liu X, Chen J, Hu WJ, Liu TW, Liu JY, Zhu CQ, Ghoto K, Zhu XY, Zheng HL (2018) Elevated nitrogen metabolism and nitric oxide production are involved in Arabidopsis resistance to acid rain. Plant Physiol Biochem 127:238–247

    Article  CAS  PubMed  Google Scholar 

  41. Rengel Z (2011) Soil pH, soil health and climate change. In: Singh B, Cowie A, Chan K (eds) soil health and climate change, vol 29. Soil biology. Springer, Berlin, pp 69–85

    Chapter  Google Scholar 

  42. Rohman MM, Talukder MZA, Hossain MG, Uddin MS, Amiruzzaman M, Biswas A, Ahsan AFMS, Chowdhury MAZ (2016) Saline sensitivity leads to oxidative stress and increases the antioxidants in presence of proline and betaine in maize (Zea mays L.) inbred. Plant Omics 9:35–47

    Article  CAS  Google Scholar 

  43. Rouphael Y, Cardarelli M, Colla G (2015) Role of arbuscular mycorrhizal fungi in alleviating the adverse effects of acidity and aluminium toxicity in zucchini squash. Sci Hortic 188:97–105

    Article  CAS  Google Scholar 

  44. Sairam RK (1994) Effects of homobrassinolide application on plant metabolism and grain yield under irrigated and moisture-stress conditions of two wheat varieties. Plant Growth Regul 14:173–181

    Article  CAS  Google Scholar 

  45. Shah ZH, Rehman HM, Akhtar T, Daur I, Nawaz MA, Ahmad MQ, Rana IA, Atif RM, Yang SH, Chung G (2017) Redox and ionic homeostasis regulations against oxidative, salinity and drought stress in wheat (a systems biology approach). Front Genet 8:141. https://doi.org/10.3389/fgene.2017.00141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Shavrukov Y, Hirai Y (2015) Good and bad protons: genetic aspects of acidity stress responses in plants. J Exp Bot 67:15–30

    Article  CAS  PubMed  Google Scholar 

  47. Shi QH, Zhu ZJ, Juan LI, Qian QQ (2006) Combined effects of excess Mn and low pH on oxidative stress and antioxidant enzymes in cucumber roots. Agric Sci China 5(10):767–772

    Article  CAS  Google Scholar 

  48. Smirnoff N (2018) Ascorbic acid metabolism and functions: a comparison of plants and mammals. Free Radical Biol Med 122:116–129

    Article  CAS  Google Scholar 

  49. Smirnoff N, Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Crit Rev Plant Sci 19:267–290

    Article  CAS  Google Scholar 

  50. Song H, Xu X, Wang H, Tao Y (2011) Protein carbonylation in barley seedling roots caused by aluminum and proton toxicity is suppressed by salicylic acid. Russ J Plant Physiol 58:653–659

    Article  CAS  Google Scholar 

  51. Sumner ME, Noble AD (2003) Soil acidification: the world story. In: Rengel Z (ed) Handbook of soil acidity. Marcel Dekker, New York, pp 1–28

    Google Scholar 

  52. Tang C, Rengel Z (2003) Role of plant cation/anion uptake ratio in soil acidification. In: Rengel Z (ed) Handbook of soil acidity. Marcel Dekker, New York, pp 56–80

    Google Scholar 

  53. Van Den Berg LJ, Dorland E, Vergeer P, Hart MA, Bobbink R, Roelofs JG (2005) Decline of acid-sensitive plant species in heathland can be attributed to ammonium toxicity in combination with low pH. New Phytol 166:551–564

    Article  CAS  PubMed  Google Scholar 

  54. Wellburn AR (1994) 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

    Article  CAS  Google Scholar 

  55. Wenzl P, Mancilla LI, Mayer JE, Albert R, Rao IM (2003) Simulating infertile acid soils with nutrient solutions. Soil Sci Soc Am J 67:1457–1469

    Article  CAS  Google Scholar 

  56. Wilkinson RE, Duncan RR (1993) Interaction of hydrogen (H+) and manganese (Mn2+) concentrations on the shoot growth of sorghum cultivars. J Plant Nutr 16(6):983–998

    Article  CAS  Google Scholar 

  57. Yang Y, Qin Y, Xie C, Zhao F, Zhao J, Liu D, Chen S, Fuglsang AT, Palmgren MG, Schumaker KS, Deng XW (2010) The Arabidopsis chaperone J3 regulates the plasma membrane H+-ATPase through interaction with the PKS5 kinase. Plant Cell 22:1313–1332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Zhang YK, Zhu DF, Zhang YP, Chen HZ, Xiang J, Lin XQ (2015) Low pH-induced changes of antioxidant enzyme and ATPase activities in the roots of rice (Oryza sativa L.) seedlings. PLoS ONE 10(2):e0116971. https://doi.org/10.1371/journal.pone.0116971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Zhang KX, Wen T, Dong J, Ma FW, Bai TH, Wang K, Li CY (2016) Comprehensive evaluation of tolerance to alkali stress by 17 genotypes of apple rootstocks. J Integr Agric 15:1499–1509

    Article  CAS  Google Scholar 

Download references

Acknowledgement

This research was funded by the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan. We thank Dr. Akinari Sonoda and Dr. Yoji Makita, Health Environment Control Research group, Health Research Institute, Advanced Industrial Science and Technology (AIST), Japan, for their kind support in analyzing the mineral contents. Thanks to Asst. Professor Khursheda Parvin and Asst. Professor Sayed Mohammad Mohsin, Sher-e-Bangla Agricultural University for their critical review and comments regarding manuscript preparation. We also acknowledge Abdul Awal Chowdhury Masud and Md. Shahadat Hossen, Laboratory of Plant Stress Response, Faculty of Agriculture, Kagawa University, Japan, for their kind assistance conducting the research.

Author information

Affiliations

Authors

Contributions

MHMBB conceived, designed, and performed the experiment and prepared the manuscript. MSH, JAM and MUA actively participated in executing the experiment. MH designed the experiment, analyzed the data and edited the manuscript. MF conceived, designed, and monitored the experiment. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Masayuki Fujita.

Ethics declarations

Conflict of interest

The authors declare that the research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1414 kb)

Supplementary material 2 (DOCX 38 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bhuyan, M.H.M.B., Hasanuzzaman, M., Mahmud, J.A. et al. Explicating physiological and biochemical responses of wheat cultivars under acidity stress: insight into the antioxidant defense and glyoxalase systems. Physiol Mol Biol Plants 25, 865–879 (2019). https://doi.org/10.1007/s12298-019-00678-0

Download citation

Keywords

  • Acidity stress
  • H+ rhizotoxicity
  • Reactive oxygen species
  • Antioxidant defense
  • Methylglyoxal