Skip to main content
SpringerLink
Log in

Exogenous Glycinebetaine Application Contributes to Abiotic Stress Tolerance in Maize

  • Research Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Plant growth and development are adversely affected by various environmental stresses. In this study, we investigated the possible function of glycinebetaine (GB) in improving abiotic stress tolerance in maize plants by exogenous application. Results indicated that GB application could effectively improve maize germination percentages, biomass weights and grain yield per plant under abiotic stresses. Moreover, GB-treated plants showed higher reactive oxygen species (ROS)-scavenging capacities, therefore less oxidative destruction than control plants under stresses. In addition, abscisic acid (ABA) levels were increased in GB-treated plants compared to control plants. The comparison of transcriptome profile was performed to analyze the possible mechanism underlying the enhanced tolerance mediated by GB. Many differentially expressed genes (DEGs) between GB-treated and control plants were found to be involved in responses to oxidative stress, abiotic stress and ABA. Taken together, these results indicated that GB might enhance abiotic stress tolerance in maize by regulating ROS-scavenging capacities and ABA-mediated stress-responsive pathways.

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
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Ahmad P, Latef A, Hashem A, Abdallah E, Gucel S, Tran L (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7:347–357

    Article  PubMed  PubMed Central  Google Scholar 

  • Alia KY, Sakamoto A, Nonaka H, Hayashi H, Saradhi P, Chen T, Murata N (1999) Enhanced tolerance to light stress of transgenic Arabidopsis plants that express the codA gene for a bacterial choline oxidase. Plant Mol Biol 40:279–288

    Article  CAS  PubMed  Google Scholar 

  • Bohnert H, Nelson D, Jensen R (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol 98:1222–1227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan Z, Shi H (2015) Improved abiotic stress tolerance of bermudagrass by exogenous small molecules. Plant Signal Behav 10:e991577

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen T, Murata N (2008) Glycinebetaine: an effective protectant against abiotic stress in plants. Trends Plant Sci 13:499–505

    Article  CAS  PubMed  Google Scholar 

  • Chen TH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20

    Article  PubMed  Google Scholar 

  • Chen W, Li P, Chen T (2000) Glycinebetaine increases chilling tolerance and reduces chilling-induced lipid peroxidation in Zea mays L. Plant Cell Environ 23:609–618

    Article  CAS  Google Scholar 

  • Chen J, Jiang H, Hsieh E, Chen H, Chien C, Hsieh H, Lin T (2012) Drought and salt stress tolerance of an Arabidopsis glutathione S-transferase U17 knockout mutant are attributed to the combined effect of glutathione and abscisic acid. Plant Physiol 158:340–351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng M, Ko K, Chang W, Kuo W, Chen G, Lin T (2015) Increased glutathione contributes to stress tolerance and global translational changes in Arabidopsis. Plant J 83:926–939

    Article  CAS  PubMed  Google Scholar 

  • Fan L, Zheng S, Wang X (1997) Antisense suppression of phospholipase Dα retards abscisic acid-and ethylene-promoted senescence of postharvest Arabidopsis leaves. Plant Cell 9:2183–2196

    CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer C, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giannopolitis C, Ries S (1977) Superoxide dismutase: I. Occurrence in higher plants. Plant Physiol 59:309–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gill S, 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 

  • Hasegawa P, Bressan R, Zhu J, Bohnert H (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Phys 51:463–499

    Article  CAS  Google Scholar 

  • Hassan M, Chaura J, Lópezgresa M, Borsai O, Daniso E, Donattorres M, Mayoral O, Vicente O, Boscaiu M (2016) Native invasive plants vs. halophytes in mediterranean salt marshes: stress tolerance mechanisms in two related species. Front Plant Sci 7:1–21

    Article  Google Scholar 

  • Hazman M, Hause B, Eiche E, Nick P, Riemann M (2015) Increased tolerance to salt stress in OPDA-deficient rice ALLENE OXIDE CYCLASE mutants is linked to an increased ROS-scavenging activity. J Exp Bot 66:3339–3352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hossain M, Asada K (1984) Purification of dehydroascorbate reductase from spinach and its characterization as a thiol Enzyme. Plant Cell Physiol 25:85–92

    CAS  Google Scholar 

  • Jagendorf A, Takabe T (2001) Inducers of glycinebetaine synthesis in barley. Plant Physiol 127:1827–1835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia J, Fu J, Zheng J, Zhou X, Huai J, Wang J, Wang M, Zhang Y, Chen X, Zhang J (2006) Annotation and expression profile analysis of 2073 full-length cDNAs from stress-induced maize (Zea mays L.) seedlings. Plant J: Cell Mol Biol 48:710–727

    Article  CAS  Google Scholar 

  • Kim M, Shin R, Schachtman D (2009) A nuclear factor regulates abscisic acid responses in Arabidopsis. Plant Physiol 151:1433–1445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lv S, Yang A, Zhang K, Wang L, Zhang J (2007) Increase of glycine betaine synthesis improves drought tolerance in cotton. Mol Breed 20:233–248

    Article  CAS  Google Scholar 

  • Maehly A, Chance B (1954) Catalases and peroxidases, part II. Methods Biochem Anal 1:357–424

    CAS  PubMed  Google Scholar 

  • Mansour M (2013) Plasma membrane permeability as an indicator of salt tolerance in plants. Biol Plant 57:1–10

    Article  CAS  Google Scholar 

  • 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 

  • Ohara K, Kokado Y, Yamamoto H, Sato F, Yazaki K (2004) Engineering of ubiquinone biosynthesis using the yeast coq2 gene confers oxidative stress tolerance in transgenic tobacco. Plant J 40:734–743

    Article  CAS  PubMed  Google Scholar 

  • Park E, Jekni Z, Sakamoto A, Denoma J, Yuwansiri R, Murata N, Chen T (2004) Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and flowers from chilling damage. Plant J 40:474–487

    Article  CAS  PubMed  Google Scholar 

  • Park E, Jeknic Z, Chen T (2006) Exogenous application of glycinebetaine increases chilling tolerance in tomato plants. Plant Cell Physiol 47:706–714

    Article  PubMed  Google Scholar 

  • Peever T, Higgins V (1989) Electrolyte leakage, lipoxygenase, and lipid peroxidation induced in tomato leaf tissue by specific and nonspecific elicitors from cladosporium fulvum. Plant Physiol 90:867–875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quan R, Shang M, Zhang H, Zhao Y, Zhang J (2004a) Improved chilling tolerance by transformation with betA gene for the enhancement of glycinebetaine synthesis in maize. Plant Sci 166:141–149

    Article  CAS  Google Scholar 

  • Quan R, Shang M, Zhang H, Zhao Y, Zhang J (2004b) Engineering of enhanced glycine betaine synthesis improves drought tolerance in maize. Plant Biotechnol J 2:477–486

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto A, Murata N (2000) Genetic engineering of glycinebetaine synthesis in plants: current status and implications for enhancement of stress tolerance. J Exp Bot 51:81–88

    Article  CAS  PubMed  Google Scholar 

  • Schaedle M (1977) Chloroplast glutathione reductase. Plant Physiol 59:1011–1012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    Article  CAS  PubMed  Google Scholar 

  • Tan B, Schwartz S, Zeevaart J, Mccarty D (1997) Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci USA 94:12235–12240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson A, Andrews J, Mulholland B, Mckee J, Hilton H, Horridge J, Farquhar G, Smeeton R, Smillie I, Black C (2007) Overproduction of abscisic acid in tomato increases transpiration efficiency and root hydraulic conductivity and influences leaf expansion. Plant Physiol 143:1905–1917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Virlouvet L, Jacquemot M, Gerentes D, Corti H, Bouton S, Gilard F, Valot B, Trouverie J, Tcherkez G, Falque M (2011) The ZmASR1 protein influences branched-chain amino acid biosynthesis and maintains kernel yield in maize under water-limited conditions. Plant Physiol 157:917–936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao L, Li Y, Zhang J, Xiao Y, Yue Y, Duan L, Zhang M, Li Z (2013) Overexpression of Arabidopsis molybdenum cofactor sulfurase gene confers drought tolerance in maize (Zea mays L.). PLoS ONE 8:e52126

    Article  Google Scholar 

  • You J, Zong W, Hu H, Li X, Xiao J, Xiong L (2014) A Stress-responsive NACl-regulated protein phosphatase gene rice protein phosphatase18 modulates drought and oxidative stress tolerance through abscisic acid-independent reactive oxygen species scavenging in rice. Plant Physiol 166:2100–2114

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu H, Chen X, Hong Y, Wang Y, Xu P, Ke S, Liu H, Zhu J, Oliver D, Xiang C (2008) Activated expression of an Arabidopsis HD-START protein confers drought tolerance with improved root system and reduced stomatal density. Plant Cell 20:1134–1151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Wang L, Meng H, Wen H, Fan Y, Zhao J (2011) Maize ABP9 enhances tolerance to multiple stresses in transgenic Arabidopsis by modulating ABA signaling and cellular levels of reactive oxygen species. Plant Mol Biol 75:365–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the Natural Science Foundation of Shandong Province (ZR2017BC099) and by the National Natural Science Foundation of China (31801278).

Author information

Author notes

  1. Laming Pei and Hongmei Li contributed equally to this work.

Authors and Affiliations

  1. School of Biological Science and Technology, University of Jinan, Jinan, 250022, China

    Laming Pei, Hongmei Li, Yuanyuan Zhou, Weijun Li, Yuhang Jiang & Hui Li

Authors
  1. Laming Pei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hongmei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuanyuan Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Weijun Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuhang Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hui Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hui Li.

Ethics declarations

Conflict of Interest

The authors have declared that no competing interests exist.

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.

12374_2020_9265_MOESM1_ESM.jpg

Effects of glycinebetaine (GB) application on expression levels of antioxidase coding genes. Fourteen day-old maize seedlings were watered with 0-mM (control) or 3.0-mM (GB-treated) GB solutions and placed under normal or stress conditions. At indicated stages, the relative expression levels of antioxidase coding genes in maize roots were determined by real-time PCR using maize actin1 as an internal control. Data were presented as mean ± standard deviation (SD). *Indicates statistically significant differences between GB-treated maize plants and control plants under same conditions at p < 0.05 level using the Student’s t-test. d day, R recovery. (JPG 4605 kb)

12374_2020_9265_MOESM2_ESM.jpg

Effects of glycinebetaine (GB) application on activities of enzymes in ASC–GSH cycle. Fourteen-day-old maize seedlings were watered with 0-mM (control) or 3.0-mM (GB-treated) GB solutions and placed under normal and stress conditions. At indicated stages, ascorbate peroxidase (APX), glutathione reductase (GR) and dehydroascorbate reductase (DHAR) activities in maize roots were determined. Data were presented as mean ± standard deviation (SD). *Indicates statistically significant differences between GB-treated maize plants and control plants under same conditions at p < 0.05 level using the Student’s t-test. d day, R recovery, FW fresh weight. (JPG 1364 kb)

12374_2020_9265_MOESM3_ESM.jpg

Effects of glycinebetaine (GB) application on expression levels of genes in non-enzymatic antioxidant system. Fourteen-day-old maize seedlings were watered with 0-mM (control) or 3.0-mM (GB-treated) GB solutions and placed under normal and stress conditions. At indicated stages, relative expression levels of glutathione reductase coding genes, GSR1 and GSR2, glutathione synthetase coding genes, GSH1 and GSH2, were determined in maize roots. Data were presented as mean ± standard deviation (SD). *Indicates statistically significant differences between GB-treated maize plants and control plants under same conditions at p < 0.05 level using the Student’s t-test. d day, R recovery. (JPG 3515 kb)

12374_2020_9265_MOESM4_ESM.png

Gene ontology (GO) enrichment analysis of differentially expressed genes (DEGs). Gene ontology (GO) enrichment analysis of differentially expressed genes was performed by the clusterProfiler R package. GO terms with adjusted p value (padj) less than 0.05 were considered significantly enriched by differential expressed genes. (PNG 3243 kb)

12374_2020_9265_MOESM5_ESM.jpg

Fourteen-day-old maize seedlings were watered with 0-mM (control) or 3.0-mM (GB-treated) GB solutions and placed under normal and stress conditions for 7 days. Then, relative expression levels of some differentially expressed genes (DEGs) between GB-treated plants and control plants were determined by real-time PCR using maize actin1 as an internal control in maize roots. Data were presented as mean ± standard deviation (SD). *Indicates statistically significant differences between GB-treated maize plants and control plants under same conditions at p < 0.05 level using the Student’s t-test. (JPG 3474 kb)

Primers used for real-time RT PCR analysis (DOC 84 kb)

Yield character parameter of control and GB-treated maize plants (DOCX 16 kb)

Differentially expressed genes (DEG) between GB-treated plants and control plants (XLSX 244 kb)

Gene ontology (GO) enrichment analysis of differentially expressed genes (DEGs) (XLSX 27 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pei, L., Li, H., Zhou, Y. et al. Exogenous Glycinebetaine Application Contributes to Abiotic Stress Tolerance in Maize. J. Plant Biol. 65, 517–529 (2022). https://doi.org/10.1007/s12374-020-09265-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-020-09265-3

Keywords

Search

Navigation