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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Exogenous γ-aminobutyric acid (GABA) enhances rye (Secale cereale) seedling resistance to combined freeze-thaw and cadmium stress

Huixin Wang A B C , Guozhang Bao https://orcid.org/0000-0003-0329-8001 A B C * , Lingzhi Tian A B C , Simeng Chen A B C , Yanan Xu A B C , Guomei Li D and Hongwei Zhao E
+ Author Affiliations
- Author Affiliations

A Key Laboratory of Groundwater Resources and Environment of the Ministry of Education (Jilin University), Changchun, China.

B Jilin Provincial Key Laboratory of Water Resources and Environment, Changchun, China.

C College of New Energy and Environment, Jilin University, Changchun 130012, China.

D Yushu Forestry and Grassland Comprehensive Service Center, No. 89, Qionglong East Road, Yushu City, Yushu Tibetan Autonomous Prefecture 815000, China.

E The Administration of Jingyu Water Conservation, Jingyu, Jilin Province 135200, China.

* Correspondence to: baogz@jlu.edu.cn

Handling Editor: Jian Feng Ma

Functional Plant Biology 51, FP24205 https://doi.org/10.1071/FP24205
Submitted: 13 August 2024  Accepted: 28 September 2024  Published: 14 October 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Freeze-thaw is a common stress at high altitudes in northern China. There is a risk of cadmium (Cd) contamination in the region. γ-aminobutyric acid (GABA) is a natural product that regulates plant growth. Rye (Secale cereale) was used as research material to investigate the physiological effects of exogenous GABA on rye seedlings under the single and combined stresses of freeze-thaw and cadmium. The results showed that the combined stress severely inhibited shoot length, root length, fresh weight, and dry weight, increased malondialdehyde and hydrogen peroxide contents, and significantly decreased superoxide dismutase (SOD) activity. Foliar application of 5 mM GABA alleviated the negative effects of stress on seedling growth, increased soluble protein content, and reduced malondialdehyde and hydrogen peroxide contents. Exogenous GABA application also enhanced the activities of SOD and peroxidase (POD). Additionally, the presence of exogenous GABA activated the GABA metabolic process and encouraged the accumulation of phytochelatins, glutathione, and non-protein thiol. These results indicate that exogenous GABA can effectively improve the resistance of rye seedlings to freeze-thaw and Cd by regulating the antioxidant enzyme system and enhancing its own detoxification mechanism, and they provide a basis for future applications of exogenous GABA, which is beneficial for ecological protection.

Keywords: cadmium, combined stress, correlation analysis, exogenous, freeze-thaw, hierarchical clustering analysis, resistance, γ-aminobutyric acid.

References

Abd El-Gawad HG, Mukherjee S, Farag R, Abd Elbar OH, Hikal M, Abou El-Yazied A, Abd Elhady SA, Helal N, ElKelish A, El Nahhas N, Azab E, Ismail IA, Mbarki S, Ibrahim MFM (2021) Exogenous γ-aminobutyric acid (GABA)-induced signaling events and field performance associated with mitigation of drought stress in Phaseolus vulgaris L. Plant Signaling & Behavior 16(2), 1853384.
| Crossref | Google Scholar | PubMed |

Altaf MM, Awan ZA, Ashraf S, Altaf MA, Zhu Z, Alsahli AA, Ahmad P (2024) Melatonin induced reversibility of vanadium toxicity in muskmelon by regulating antioxidant defense and glyoxalase systems. Journal of Hazardous Materials 473, 134452.
| Crossref | Google Scholar | PubMed |

Ballabio C, Jones A, Panagos P (2024) Cadmium in topsoils of the European Union – an analysis based on LUCAS topsoil database. Science of The Total Environment 912, 168710.
| Crossref | Google Scholar | PubMed |

Bao G, Ao Q, Li Q, Bao Y, Zheng Y, Feng X, Ding X (2017) Physiological characteristics of Medicago sativa L. in response to acid deposition and freeze-thaw stress. Water, Air, & Soil Pollution 228(9), 376.
| Crossref | Google Scholar |

Bao G, He F, Chen W, Sun J, Ding X (2020) Physiological effects of different concentrations of chloride deicing salt and freeze–thaw stress on Secale cereale L. seedlings. Journal of Plant Growth Regulation 39(1), 15-25.
| Crossref | Google Scholar |

Batelli G, Ruggiero A, Esposito S, Venezia A, Lupini A, Nurcato R, Costa A, Palombieri S, Vitiello A, Mauceri A, Cammareri M, Sunseri F, Grandillo S, Granell A, Abenavoli MR, Grillo S (2024) Combined salt and low nitrate stress conditions lead to morphophysiological changes and tissue-specific transcriptome reprogramming in tomato. Plant Physiology and Biochemistry 215, 108976.
| Crossref | Google Scholar | PubMed |

Bhargava P, Kumar Srivastava A, Urmil S, Chand Rai L (2005) Phytochelatin plays a role in UV-B tolerance in N2-fixing cyanobacterium Anabaena doliolum. Journal of Plant Physiology 162(11), 1220-1225.
| Crossref | Google Scholar | PubMed |

Bown AW, Shelp BJ (2016) Plant GABA: not just a metabolite. Trends in Plant Science 21(10), 811-813.
| Crossref | Google Scholar | PubMed |

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72(1–2), 248-254.
| Crossref | Google Scholar |

Chang Y, Zhang J, Bao G, Yan B, Qu Y, Zhang M, Tang W (2021) Physiological responses of highland barley seedlings to NaCl, drought, and freeze-thaw stress. Journal of Plant Growth Regulation 40(1), 154-161.
| Crossref | Google Scholar |

David OA, Labulo AH, Hassan I, Olawuni I, Oseghale CO, Terna AD, Ajayi OO, Ayegbusi SA, Owolabi MO (2024) Complexation and immobilization of arsenic in maize using green synthesized silicon nanoparticles (SiNPs). Scientific Reports 14(1), 6176.
| Crossref | Google Scholar | PubMed |

Draper HH, Hadley M (1990) [43] Malondialdehyde determination as index of lipid peroxidation. Methods in Enzymology 186, 421-431.
| Crossref | Google Scholar | PubMed |

Haider FU, Ain N-U-, Khan I, Farooq M, Habiba , Cai L, Li Y (2024) Co-application of biochar and plant growth regulators improves maize growth and decreases Cd accumulation in cadmium-contaminated soil. Journal of Cleaner Production 440, 140515.
| Crossref | Google Scholar |

Hao XH, Liu KX, Zhang MY (2024) Effect of exogenous γ-aminobutyric acid on physiological property, antioxidant activity, and cadmium uptake of quinoa seedlings under cadmium stress. Bioscience Reports 44(6), BSR20240215.
| Crossref | Google Scholar |

Hasanuzzaman M, Nahar K, Anee TI, Fujita M (2017) Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiology and Molecular Biology of Plants 23(2), 249-268.
| Crossref | Google Scholar | PubMed |

Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125(1), 189-198.
| Crossref | Google Scholar | PubMed |

Hijaz F, Killiny N (2019) Exogenous GABA is quickly metabolized to succinic acid and fed into the plant TCA cycle. Plant Signaling & Behavior 14(3), e1573096.
| Crossref | Google Scholar | PubMed |

Huang H, Ullah F, Zhou D-X, Yi M, Zhao Y (2019) Mechanisms of ROS regulation of plant development and stress responses. Frontiers in Plant Science 10, 800.
| Crossref | Google Scholar |

Javed HU, Liu Y-S, Shi P, Mahreen N, Rastegar S, Hao J-G, Dai Z-R, You G, Ali S (2024) A comprehensive meta-analysis exploring potential of GABA for postharvest chilling injury mitigation in horticultural produce. Scientia Horticulturae 338, 113558.
| Crossref | Google Scholar |

Jia Y, Zou D, Wang J, Sha H, Liu H, Inayat MA, Sun J, Zheng H, Xia N, Zhao H (2017) Effects of γ-aminobutyric acid, glutamic acid, and calcium chloride on rice (Oryza sativa L.) under cold stress during the early vegetative stage. Journal of Plant Growth Regulation 36(1), 240-253.
| Crossref | Google Scholar |

Jiang G, Wang S, Xie J, Tan P, Han L (2023) Discontinuous low temperature stress and plant growth regulators during the germination period promote roots growth in alfalfa (Medicago sativa L.). Plant Physiology and Biochemistry 197, 107624.
| Crossref | Google Scholar | PubMed |

Jin X, Liu T, Xu J, Gao Z, Hu X (2019) Exogenous GABA enhances muskmelon tolerance to salinity-alkalinity stress by regulating redox balance and chlorophyll biosynthesis. BMC Plant Biology 19(1), 48.
| Crossref | Google Scholar | PubMed |

Kandhol N, Rai P, Pandey S, Singh S, Sharma S, Corpas FJ, Singh VP, Tripathi DK (2023) Zinc induced regulation of PCR1 gene for cadmium stress resistance in rice roots. Plant Science 337, 111783.
| Crossref | Google Scholar | PubMed |

Li Y, Liu B, Peng Y, Liu C, Zhang X, Zhang Z, Liang W, Ma F, Li C (2020) Exogenous GABA alleviates alkaline stress in Malus hupehensis by regulating the accumulation of organic acids. Scientia Horticulturae 261, 108982.
| Crossref | Google Scholar |

Li D, Zhang D, Zhang Z, Xing Y, Sun N, Wang S, Cai H (2022a) Exogenous application of GABA alleviates alkali damage in alfalfa by increasing the activities of antioxidant enzymes. Agronomy 12(7), 1577.
| Crossref | Google Scholar |

Li Y, Li Y, Cui Y, Xie Y, Shi Y, Shang Y, Ma F, Zhang J, Li C (2022b) GABA-mediated inhibition of cadmium uptake and accumulation in apples. Environmental Pollution 300, 118867.
| Crossref | Google Scholar | PubMed |

Li G, Yan L, Chen X, Lam SS, Rinklebe J, Yu Q, Yang Y, Peng W, Sonne C (2023a) Phytoremediation of cadmium from soil, air and water. Chemosphere 320, 138058.
| Crossref | Google Scholar | PubMed |

Li Y, Chen Y, Ma K, Bai M, Liu Y, Yu X (2023b) Physiological changes associated with enhanced cold resistance during Medicago ruthenica germination and seedling growth in response to exogenous γ-aminobutyric acid. Grassland Science 69(2), 120-131.
| Crossref | Google Scholar |

Liang Y, Liu H, Zhang Y, Li P, Fu Y, Li S, Gao Y (2024) Exogenous application of silica nanoparticles mitigates combined salt and low-temperature stress in cotton seedlings by improving the K+/Na+ ratio and antioxidant defense. Plant Stress 14, 100597.
| Crossref | Google Scholar |

Lu Y, Wang Q-F, Li J, Xiong J, Zhou L-N, He S-L, Zhang J-Q, Chen Z-A, He S-G, Liu H (2019) Effects of exogenous sulfur on alleviating cadmium stress in tartary buckwheat. Scientific Reports 9(1), 7397.
| Crossref | Google Scholar | PubMed |

Pan XY, Bao GZ, Yang YN, Zhang X, Guo JC, Fan XY, Xiang T, Li GM, Zhao HW (2023) Application of potassium fulvic acid improving tolerance of Secale cereale L. seedlings to cadmium stress and freeze-thaw environment. Applied Ecology and Environmental Research 21(3), 2761-2773.
| Crossref | Google Scholar |

Pan X, Bao G, Wang H, Hu J, Fan X, Xiang T, Tian L (2024) The freeze-thaw cycle exacerbates the ecotoxicity of polystyrene nanoplastics to Secale cereale L. seedlings. Plant Physiology and Biochemistry 211, 108716.
| Crossref | Google Scholar | PubMed |

Podlešáková K, Ugena L, Spíchal L, Doležal K, De Diego N (2019) Phytohormones and polyamines regulate plant stress responses by altering GABA pathway. New Biotechnology 48, 53-65.
| Crossref | Google Scholar | PubMed |

Qureshi MK, Gawroński P, Munir S, Jindal S, Kerchev P (2022) Hydrogen peroxide-induced stress acclimation in plants. Cellular and Molecular Life Sciences 79(2), 129.
| Crossref | Google Scholar | PubMed |

R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/

Repkina N, Talanova V, Ignatenko A, Titov A (2019) Involvement of proline and non-protein thiols in response to low temperature and cadmium stresses in wheat. Biologia Plantarum 63(1), 70-77.
| Crossref | Google Scholar |

Rezaei-Chiyaneh E, Seyyedi SM, Ebrahimian E, Moghaddam SS, Damalas CA (2018) Exogenous application of gamma-aminobutyric acid (GABA) alleviates the effect of water deficit stress in black cumin (Nigella sativa L.). Industrial Crops and Products 112, 741-748.
| Crossref | Google Scholar |

Seifikalhor M, Aliniaeifard S, Bernard F, Seif M, Latifi M, Hassani B, Didaran F, Bosacchi M, Rezadoost H, Li T (2020) γ-Aminobutyric acid confers cadmium tolerance in maize plants by concerted regulation of polyamine metabolism and antioxidant defense systems. Scientific Reports 10(1), 3356.
| Crossref | Google Scholar | PubMed |

Song Q, Zhao Y, Wu F, Guo X, Yu H, Li J, Li W, Wang Y, Li M, Xu J (2024) Physiological and molecular responses of strawberry plants to Cd stress. Plant Physiology and Biochemistry 213, 108800.
| Crossref | Google Scholar | PubMed |

Stefanov MA, Rashkov GD, Borisova PB, Apostolova EL (2024) Changes in photosystem II complex and physiological activities in pea and maize plants in response to salt stress. Plants 13(7), 1025.
| Crossref | Google Scholar |

Tajti J, Janda T, Majláth I, Szalai G, Pál M (2018) Comparative study on the effects of putrescine and spermidine pre-treatment on cadmium stress in wheat. Ecotoxicology and Environmental Safety 148, 546-554.
| Crossref | Google Scholar | PubMed |

Timori Z, Amirinejad AA, Ghobadi M (2024) Biochar improves Pb and Cd-induced stress in mung bean (Vigna radiata L. Wilczek). Environmental Challenges 16, 100992.
| Crossref | Google Scholar |

Wang Q-Y, Hu N-W, Yu H-W, Wang Q-R, Liu Y-X, Yue J, Hu B (2021a) Do freeze-thaw cycles affect the cadmium accumulation, subcellular distribution, and chemical forms in spinach (Spinacia oleracea L.)? Ecotoxicology and Environmental Safety 228, 112952.
| Crossref | Google Scholar | PubMed |

Wang R, Lin K, Chen H, Qi Z, Liu B, Cao F, Chen H, Wu F (2021b) Metabolome analysis revealed the mechanism of exogenous glutathione to alleviate cadmium stress in maize (Zea mays L.) Seedlings. Plants 10(1), 105.
| Crossref | Google Scholar |

Wang X, Shi M, Zhang R, Wang Y, Zhang W, Qin S, Kang Y (2024) Dynamics of physiological and biochemical effects of heat, drought and combined stress on potato seedlings. Chemical and Biological Technologies in Agriculture 11(1), 109.
| Crossref | Google Scholar |

Wu G-L, Cheng Z, Alatalo JM, Zhao J, Liu Y (2021) Climate warming consistently reduces grassland ecosystem productivity. Earth’s Future 9(6), e2020EF001837.
| Crossref | Google Scholar |

Xu M, Yang Q, Bai G, Li P, Yan J (2022) Polyamine pathways interconnect with GABA metabolic processes to mediate the low-temperature response in plants. Frontiers in Plant Science 13, 1035414.
| Crossref | Google Scholar |

Xue W, Zhang C, Huang Y, Wang C, Zhang X, Liu Z (2022) Rice organs concentrate cadmium by chelation of amino acids containing dicarboxyl groups and enhance risks to human and environmental health in Cd-contaminated areas. Journal of Hazardous Materials 426, 128130.
| Crossref | Google Scholar | PubMed |

Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. South African Journal of Botany 76(2), 167-179.
| Crossref | Google Scholar |

Yang LP, Zhu J, Wang P, Zeng J, Tan R, Yang YZ, Liu ZM (2018) Effect of Cd on growth, physiological response, Cd subcellular distribution and chemical forms of Koelreuteria paniculata. Ecotoxicology and Environmental Safety 160, 10-18.
| Crossref | Google Scholar | PubMed |

Yang J, Wu G, Jiao J, Dyck M, He H (2022) Freeze-thaw induced landslides on grasslands in cold regions. CATENA 219, 106650.
| Crossref | Google Scholar |

Zhang W, Bao G, Tang W, Dai G, Xiao J, Liu J, Wang Z, Xi J (2022) Physiological response of barley seedlings to salinity and artemisinin combined stresses under freeze-thaw environment. Environmental Science and Pollution Research 29(46), 70552-70563.
| Crossref | Google Scholar | PubMed |

Zhang D, Wang H, Zhang Y, Su Z, Hu T, Liu J, Ding Q, Niu N, Ma L (2024) Methyl jasmonate enhances the safe production ability of Cd-stressed wheat by regulating the antioxidant capacity, Cd absorption, and distribution in wheat. Plant Physiology and Biochemistry 212, 108788.
| Crossref | Google Scholar | PubMed |

Zhu T, Li L, Duan Q, Liu X, Chen M (2021) Progress in our understanding of plant responses to the stress of heavy metal cadmium. Plant Signaling & Behavior 16(1), 1836884.
| Crossref | Google Scholar | PubMed |

Zhuang Z, Wang Q, Huang S, NiñoSavala AG, Wan Y, Li H, Schweiger AH, Fangmeier A, Franzaring J (2023) Source-specific risk assessment for cadmium in wheat and maize: towards an enrichment model for China. Journal of Environmental Sciences 125, 723-734.
| Crossref | Google Scholar |