Skip to main content
SpringerLink
Log in

5-Aminolevulinic acid modulates antioxidant defense systems and mitigates drought-induced damage in Kentucky bluegrass seedlings

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Drought stress occurs frequently and severely as a result of global climate change, and it exerts serious effects on plants. 5-Aminolevulinic acid (5-ALA) plays a crucial role in conferring abiotic stress tolerance in plants. To enhance the drought tolerance of turfgrass and investigate the effects of 5-ALA on antioxidant metabolism and gene expression under drought stress conditions, exogenous 5-ALA was applied by foliar spraying before Kentucky bluegrass (Poa pratensis L.) seedlings were exposed to drought [induced by 10% polyethylene glycol (PEG)] stress for 20 days. 5-ALA pretreatment increased turf quality (TQ) and leaf relative water content (RWC) while reducing reactive oxygen species (ROS) production including H2O2 content and O2 •− generation rate, lipoxygenase (LOX) activity, and malondialdehyde (MDA) content under drought stress. 5-ALA pretreatment maintained ascorbate (AsA) and glutathione (GSH) contents and the ASA/DHA and GSH/GSSG ratios at high levels, and it enhanced the activities of superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), glutathione peroxidase (GPX), dehydroascorbate reductase (DHAR), and glutathione reductase (GR), which are crucial for scavenging drought-induced ROS. In addition, 5-ALA upregulated the relative expression levels of Cu/ZnSOD, APX, GPX, and DHAR but downregulated those of CAT and GR under drought stress. These results indicated that the application of 5-ALA might improve turfgrass quality and promote drought tolerance in Kentucky bluegrass through reducing oxidative damage and increasing non-enzyme antioxidant levels and antioxidant enzyme activity at transcriptional and posttranscriptional levels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Abbreviations

5-ALA:

5-Aminolevulinic acid

APX:

Ascorbate peroxidase

AsA:

Ascorbic acid (ascorbate)

BSA:

Bovine serum albumin

CAT:

Catalase

CDNB:

1-Chloro-2,4-dinitrobenzene

DHA:

Dehydroascorbate

DHAR:

Dehydroascorbate reductase

DTNB:

5,5′-Dithio-bis (2-nitrobenzoic acid)

EDTA:

Ethylenediaminetetraacetic acid

GR:

Glutathione reductase

GSH:

Reduced glutathione

GSSG:

Oxidized glutathione

GPX:

Glutathione peroxidase

LOX:

Lipoxygenase

MDHAR:

Monodehydroascorbate reductase

NADPH:

Nicotinamide adenine dinucleotide phosphate

NTB:

2-nitro-5-thiobenzoic acid

SOD:

Superoxide dismutase

TBA:

Thiobarbituric acid

TCA:

Trichloroacetic acid

References

  • Akram NA, Ashraf M (2013) Regulation in plant stress tolerance by a potential plant growth regulator, 5-aminolevulinic acid. J Plant Growth Regul 32:663–679

    Article  CAS  Google Scholar 

  • Akram NA, Ashraf M, Al-Qurainy F (2012) Aminolevulinic acid-induced changes in some key physiological attributes and activities of antioxidant enzymes in sunflower (Helianthus annuus L.) plants under saline regimes. Sci Hortic-Amsterdam 142:143–148

    Article  CAS  Google Scholar 

  • Ali B, Tao Q, Zhou Y, Gill RA, Ali S, Rafiq MT, Xu L, Zhou W (2013) 5-Aminolevolinic acid mitigates the cadmium-induced changes in Brassica napus as revealed by the biochemical and ultra-structural evaluation of roots. Ecotoxicol Environ Saf 92:271

    Article  CAS  PubMed  Google Scholar 

  • Al-Khateeb SA (2006) Promotive effect of 5-aminolevulinic acid on growth, yield and gas exchange capacity of barley (Hordeum vulgare L.) grown under different irrigation regimes. J King Saud Unive Agric Sci 18(18):103–111

    Google Scholar 

  • Anjum SA, Xie XY, Wang LC, Saleem MF, Man C, Lei W (2011) Morphological, physiological and biochemical responses of plants to drought stress. Afr J Agric Res 6:2026–2032

    Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Asada K (1992) Ascorbate peroxidase - a hydrogen peroxide scavenging enzyme in plants. Physiol Plant 85:235--241

  • Balestrasse KB, Tomaro ML, Batlle A, Noriega GO (2010) The role of 5-aminolevulinic acid in the response to cold stress in soybean plants. Phytochemistry 71:2038–2045

    Article  CAS  PubMed  Google Scholar 

  • Bian S, Jiang Y (2009) Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery. Sci Hortic-Amsterdam 120:264–270

    Article  CAS  Google Scholar 

  • Bowler C, Montagu MVA, Inze D (1992) Superoxide-dismutase and stress tolerance. Annu Rev Plant Biol 43:83–116

    Article  CAS  Google Scholar 

  • De Azevedo NA, Prisco JT, Eneas-Filho J, Medeiros JV, Gomes-Filho E (2005) Hydrogen peroxide pre-treatment induces salt-stress acclimation in maize plants. J Plant Physiol 162:1114–1122

    Article  Google Scholar 

  • Doderer A, Kokkelink I, Van DVS, Valk BE, Schram AW, Douma AC (1992) Purification and characterization of two lipoxygenase isoenzymes from germinating barley. Biochim Biophys Acta 1120:97–104

    Article  CAS  PubMed  Google Scholar 

  • Elia AC, Galarini R, Taticchi MI, Dörr 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 

  • Elstner EF (2003) Oxygen activation and oxygen toxicity. Annu Rev Plant Physiol 33:73–96

    Article  Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Havir EA, Mchale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He J, Li MF, Wu F, Li SP, Zhou SY (2013) Physiological response of banana seedling to exogenous ALA under drought stress. J South Agric:745–750

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  PubMed  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:357–359

    Google Scholar 

  • Hu L, Wang Z, Huang B (2012) Growth and physiological recovery of Kentucky bluegrass from drought stress as affected by a synthetic cytokinin 6-benzylaminopurine. Crop Sci 52:2332–2340

    Article  CAS  Google Scholar 

  • Huang B, DaCosta M, Jiang Y (2014) Research advances in mechanisms of turfgrass tolerance to abiotic stresses: from physiology to molecular biology. Crit Rev Plant Sci 33:141–189

    Article  CAS  Google Scholar 

  • Javed N, Ashraf M, Akram NA, Al-Qurainy F (2011) Alleviation of adverse effects of drought stress on growth and some potential physiological attributes in maize. Photochem Photobiol 87:1354–1362

    Article  CAS  PubMed  Google Scholar 

  • Jr BW, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    Article  Google Scholar 

  • Kackley KE, Grybauskas AP, Dernoeden PH, Hill RL (1990) Role of drought stress in the development of summer patch in field-inoculated Kentucky bluegrass. Phytopathology 80:655–658

    Article  Google Scholar 

  • Kampfenkel K, Van Montagu M, Inze D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Anal Biochem 225:165–167

    Article  CAS  PubMed  Google Scholar 

  • Knörzer OC, Burner J, Boger P (1996) Alterations in the antioxidative system of suspension-cultured soybean cells (Glycine max) induced by oxidative stress. Physiol Plantarum 97:388–396

    Article  Google Scholar 

  • Liu ZJ, Guo YK, Bai JG (2010) Exogenous hydrogen peroxide changes antioxidant enzyme activity and protects ultrastructure in leaves of two cucumber ecotypes under osmotic stress. J Plant Growth Regul 29:171–183

    Article  Google Scholar 

  • Liu D, Pei ZF, Naeem MS, Ming DF, Liu HB, Khan F, Zhou WJ (2011) 5-Aminolevulinic acid activates antioxidative defence system and seedling growth in Brassica napus L. under water-deficit stress. J Agron Crop Sci 197:284–295

    Article  CAS  Google Scholar 

  • Liu M, Li J, Niu J, Wang R, Song J, Lv J, Zong X, Wang S (2016) Interaction of drought and 5-aminolevulinic acid on growth and drought resistance of Leymus chinensis seedlings. Acta Ecol Sin 36:180–188

    Article  CAS  Google Scholar 

  • Loggini B, Navari-Izzo F (1999) Antioxidative defense system, pigment composition, and photosynthetic efficiency in two wheat cultivars subjected to drought. Plant Physiol 119:1091–1099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van BF (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  PubMed  Google Scholar 

  • Naeem MS, Rasheed M, Liu D, Jin ZL, Ming DF, Yoneyama K, Takeuchi Y, Zhou WJ (2011) 5-Aminolevulinic acid ameliorates salinity-induced metabolic, water-related and biochemical changes in Brassica napus L. Acta Physiol Plant 33:517–528

    Article  CAS  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Mahmud JA, Suzuki T, Fujita M (2016) Insights into spermine-induced combined high temperature and drought tolerance in mung bean: osmoregulation and roles of antioxidant and glyoxalase system Protoplasma 1–16

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nishihara E, Kondo KParvez MM, Takahashi K, Watanabe K, Tanaka K (2003) Role of 5-aminolevulinic acid (ALA) on active oxygen-scavenging system in NaCl-treated spinach (Spinacia oleracea). J Plant Physiol 160:1085–1091

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Plant Biol 49:249–279

    CAS  Google Scholar 

  • Ot CP, Jones (1975) Protoheme turnover and chlorophyll synthesis in greening barley tissue. Plant Physiol 55:485–490

    Article  Google Scholar 

  • Puyang X, An M, Xu L, Han L, Zhang X (2015a) Antioxidant responses to waterlogging stress and subsequent recovery in two Kentucky bluegrass (Poa pratensis L.) cultivars. Acta Physiol Plant 37:1–12

    Article  CAS  Google Scholar 

  • Puyang X, An M, Han L, Zhang X (2015b) Protective effect of spermidine on salt stress induced oxidative damage in two Kentucky bluegrass (Poa pratensis L.) cultivars. Ecotoxicol Environ Saf 117:96–106

    Article  CAS  PubMed  Google Scholar 

  • Scandalios JG (1993) Oxygen stress and superoxide dismutases. Plant Physiol 101:7–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schneider K, Schlegel HG (1981) Production of superoxide radicals by soluble hydrogenase from Alcaligenes eutrophus H16. Biochem J 193:99–107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka R, Tanaka A (2011) Chlorophyll cycle regulates the construction and destruction of the light-harvesting complexes. Biochim Biophys Acta 1807:968–976

    Article  CAS  PubMed  Google Scholar 

  • Turgeon AJ (1991) Turfgrass management. 3rd ed

  • Xing X, Zhou Q, Xing H, Jiang H, Wang S (2016) Early abscisic acid accumulation regulates ascorbate and glutathione metabolism in soybean leaves under progressive water stress. J Plant Growth Regul:1–12

  • Xu L (2011) Antioxidant enzyme activities and gene expression patterns in leaves of Kentucky bluegrass in response to drought and post-drought recovery. J Am Soc Hortic 136:247–255

    CAS  Google Scholar 

  • Xu Z, Zhou G, Shimizu H (2010) Plant responses to drought and rewatering. Plant Signal Behav 5:649–654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Chang Z, Sun L, Yu J, Huang B (2014) Physiological and metabolic effects of 5-aminolevulinic acid for mitigating salinity stress in creeping bentgrass. PLoS One 9:e116283–e116283

    Article  PubMed  PubMed Central  Google Scholar 

  • Youssef T, Awad MA (2008) Mechanisms of enhancing photosynthetic gas exchange in date palm seedlings (Phoenix dactylifera L.) under salinity stress by a 5-aminolevulinic acid-based fertilizer. J Plant Growth Regul 27:1–9

    Article  CAS  Google Scholar 

  • Yu GH, Weinstein JD (1997) Heme synthesis and breakdown in isolated developing pea chloroplasts. Plant Physiol Biochem 35:223–234

    CAS  Google Scholar 

Download references

Acknowledgements

This work was funded by National Natural Science Foundation of China (NSFC) (project no. 3131160482).

Author information

Authors and Affiliations

  1. Key Laboratory of Grassland Ecosystem of Ministry of Education, College of Grassland Science, Gansu Agricultural University, Lanzhou, 730070, People’s Republic of China

    Kuiju Niu & Huiling Ma

  2. Academy of Animal Sciences and Veterinary, Qinghai University, Xining, 810016, People’s Republic of China

    Xiang Ma, Guoling Liang, Zhifeng Jia & Wenhui Liu

  3. College of Horticulture, South China Agricultural University, Guangzhou, 510642, People’s Republic of China

    Qianqian Yu

Authors
  1. Kuiju Niu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiang Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guoling Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Huiling Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhifeng Jia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wenhui Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Qianqian Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Huiling Ma.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Bhumi Nath Tripathi

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Niu, K., Ma, X., Liang, G. et al. 5-Aminolevulinic acid modulates antioxidant defense systems and mitigates drought-induced damage in Kentucky bluegrass seedlings. Protoplasma 254, 2083–2094 (2017). https://doi.org/10.1007/s00709-017-1101-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-017-1101-4

Keywords

Search

Navigation