Skip to main content
SpringerLink
Log in

Antioxidant enzyme activity and microRNA are associated with growth of Poa pratensis callus under salt stress

  • Original Article
  • Published:
Plant Biotechnology Reports Aims and scope Submit manuscript

Abstract

Kentucky bluegrass (Poa pratensis L.) is an important species of turfgrass that is commonly planted on golf courses and landscapes all over the world. It is sensitive to salt stress; however, details relating to its molecular mechanisms of salt resistance are not available. We, therefore, analyzed the changes in growth, antioxidant enzyme activity, and microRNA expression in the callus 1 week after treatment with 200 mM NaCl for 12 h, 24 h, 48 h, 96 h, and 144 h. The results demonstrated that callus growth declined and thiobarbituric acid-reactive substance production and cell membrane permeability increased. Treatment with salt increased ascorbate peroxidase, glutathione reductase, superoxide dismutase, catalase, peroxidase, and polyphenol oxidase activity. Changes in the expression levels of microRNAs were observed under salt treatment. The expression of miR162, miR173, miR391, miR408, miR773, and miR857 increased by 70% after 24 h of salt treatment, after which it declined to a level similar to that of the control. The expression level of miR775 and miR827 decreased by 20% after 24 h, and then further decreased by 80% after 144 h. The expression level of miR841 increased by 50% after 24 h of salt treatment, and then stabilized. In contrast, salt treatment increased the expression of the auxin response factors ARF6, ARF8, ARF10, and ARF16 in the callus from 12 to 144 h of salt treatment, during which the expression increased twofold. Gene expression analysis indicated that salt-responsive gene families were regulated by microRNAs in the callus under salinity stress. The activity of antioxidant enzymes is also changing. MiR841 is considered to be a positive regulator of antioxidant enzyme biosynthesis. The present investigation elucidates the manner in which P. pratensis responds to salt stress in the callus, and could be used to inform further studies on the molecular mechanisms of stress tolerance.

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

Similar content being viewed by others

References

  • AbdElgawad H, Zinta G, Hegab MM, Pandey R, Asard H, Abuelsoud W (2016) High salinity induces different oxidative stress and antioxidant responses in maize seedlings organs. Front Plant Sci 7:276

    PubMed  PubMed Central  Google Scholar 

  • Amaradasa BS, Amundsen K (2016) Transcriptome profiling of buffalograss challenged with the leaf spot pathogen Curvularia inaequalis. Front Plant Sci 7:715

    PubMed  PubMed Central  Google Scholar 

  • Ambede JG, Netondo GW, Mwai GN, Musyimi DM (2012) NaCl salinity affects germination, growth, physiology, and biochemistry of bambara groundnut. Braz J Plant Physiol 24:151–160

    CAS  Google Scholar 

  • Barciszewska-Pacak M, Knop K, Jarmołowski A, Szweykowska-Kulińska Z (2016) Arabidopsis thaliana microRNA162 level is posttranscriptionally regulated via splicing and polyadenylation site selection. Acta Biochim Pol 63:811–816

    CAS  PubMed  Google Scholar 

  • Beers RF, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140

    CAS  PubMed  Google Scholar 

  • Bouzroud S, Gouiaa S, Hu N, Bernadac A, Mila I, Bendaou N, Smouni A, Bouzayen M, Zouine M (2018) Auxin response factors (ARFs) are potential mediators of auxin action in tomato response to biotic and abiotic stress (Solanum lycopersicum). PLoS One 13(2):e0193517

    PubMed  PubMed Central  Google Scholar 

  • Bushman BS, Amundsen KL, Warnke SE, Robins JG, Johnson PG (2016a) Transcriptome profiling of Kentucky bluegrass (Poapratensis L.) accessions in response to salt stress. BMC Genomics 17(1):48

    PubMed  PubMed Central  Google Scholar 

  • Bushman BS, Amundsen KL, Warnke SE, Robins JG, Johnson PG (2016b) Transcriptome profiling of Kentucky bluegrass (Poapratensis L.) accessions in response to salt stress. BMC Genomics 17:4

    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(4):1222–1227

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chu Z, Chen J, Xu H, Dong Z, Chen F, Cui D (2016) Identification and comparative analysis of microRNA in wheat (Triticumaestivum L.) callus derived from mature and immature embryos during in vitro culture. Front Plant Sci 7:1302

    PubMed  PubMed Central  Google Scholar 

  • De Bigault Du, Granrut A, Cacas JL (2016) How very-long-chain fatty acids could signal stressful conditions in plants? Front Plant Sci 7:1490

    Google Scholar 

  • Fei Y, Xiao B, Yang M, Ding Q, Tang W (2016) MicroRNAs, polyamines, and the activities antioxidant enzymes are associated with in vitro rooting in white pine (Pinusstrobus L.). Springerplus 5(1):416

    PubMed  PubMed Central  Google Scholar 

  • Ganesan M, Lee HY, Kim JI, Song PS (2017) Development of transgenic crops based on photo-biotechnology. Plant Cell Environ 40(11):2469–2486

    CAS  PubMed  Google Scholar 

  • Hadle JJ, Konrade LA, Beasley RR, Lance SL, Jones KL, Beck JB (2016) Development of microsatellite markers for buffalograss (Buchloë dactyloides; Poaceae), a drought-tolerant turfgrass alternative. Appl Plant Sci 4(8):1600033

    Google Scholar 

  • Houston K, McKim SM, Comadran J, Bonar N, Druka I, Uzrek N, Cirillo E, Guzy-Wrobelska J, Collins NC, Halpin C, Hansson M, Dockter C, Druka A, Waugh R (2013) Variation in the interaction between alleles of HvAPETALA2 and microRNA172 determines the density of grains on the barley inflorescence. Proc Nat Acad Sci 110(41):16675–16680

    CAS  PubMed  Google Scholar 

  • Hu W, Zuo J, Hou X, Yan Y, Wei Y, Liu J, Li M, Xu B, Jin Z (2015) The auxin response factor gene family in banana: genome-wide identification and expression analyses during development, ripening, and abiotic stress. Front Plant Sci 6:742

    PubMed  PubMed Central  Google Scholar 

  • Jeffries MD, Gannon TW, Brosnan JT, Breeden GK (2016) Comparing dislodgeable 2,4-d residues across athletic field turfgrass species and time. PLoS One 11:e0168086

    PubMed  PubMed Central  Google Scholar 

  • Kim YH, Yoo YJ (1996) Peroxidase production from carrot hairy root cell culture. Enzyme Microb Technol 18:531–535

    CAS  Google Scholar 

  • Kurum R, Ulukapi K, Aydinsakir K, Onus AN (2013) The influence of salinity on seedling growth of some pumpkin varieties used as rootstock. Not Bot Horti Agrobo 41:219–225

    CAS  Google Scholar 

  • Li SB, Xie ZZ, Hu CG, Zhang JZ (2016) A review of auxin response factors (ARFs) in plants. Front Plant Sci 7:47

    PubMed  PubMed Central  Google Scholar 

  • Liang H, Xia Y, Du F, Zhang P (2001) Study on the effects of salt stress on physiological and biochemical indexes of resistance of two turf grasses. Grassl China 23(5):27–30

    Google Scholar 

  • Liang G, Ai Q, Yu D (2015) Uncovering miRNAs involved in crosstalk between nutrient deficiencies in Arabidopsis. Sci Rep 5:11813

    PubMed  PubMed Central  Google Scholar 

  • Martinez G, Choudury SG, Slotkin RK (2017) tRNA-derived small RNAs target transposable element transcripts. Nucleic Acids Res 45(9):5142–5152

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miura K, Ikeda M, Matsubara A, Song XJ, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42(6):545–549

    CAS  PubMed  Google Scholar 

  • Mohammadi MHS, Etemadi N, Arab MM, Aalifar M, Arab M, Pessarakli M (2017) Molecular and physiological responses of Iranian perennial ryegrass as affected by trinexapac ethyl, paclobutrazol and abscisic acid under drought stress. Plant Physiol Biochem 111:129–143

    Google Scholar 

  • Ni Y, Guo N, Zhao Q, Guo Y (2016) Identification of candidate genes involved in wax deposition in Poa pratensis by RNA-seq. BMC Genomics 17(1):314

    PubMed  PubMed Central  Google Scholar 

  • Nosaka M, Itoh JI, Nagato Y, Ono A, Ishiwata A, Sato Y (2012) Role of transposon-derived small RNAs in the interplay between genomes and parasitic DNA in rice. PLoS Genet 8(9):e1002953

    CAS  PubMed  PubMed Central  Google Scholar 

  • Podio M, Felitti SA, Siena LA, Delgado L, Mancini M, Seijo JG, González AM, Pessino SC, Ortiz JPA (2014) Characterization and expression analysis of SOMATIC EMBRYOGENESIS RECEPTOR KINASE (SERK) genes in sexual and apomictic Paspalum notatum. Plant Mol Biol 84(4–5):479–495

    CAS  PubMed  Google Scholar 

  • Ruuhola T, Nybakken L, Julkunen-Tiitto R (2013) Sex-related differences of two ecologically divergent Salix species in the responses of enzyme activities to atmospheric CO2 enrichment. Biol Plant 57:732–738

    CAS  Google Scholar 

  • Salvador-Guirao R, Baldrich P, Weigel D, Rubio-Somoza I, San Segundo B (2018) The MicroRNA miR773 is involved in the Arabidopsis immune response to fungal pathogens. Mol Plant Microbe Interact 31:249–259

    CAS  PubMed  Google Scholar 

  • Senadheera P, Tirimanne S, Maathuis FJM (2012) Long term salinity stress reveals variety specific differences in root oxidative stress response. Rice Sci 19:36–43

    Google Scholar 

  • Stief A, Altmann S, Hoffmann K, Pant BD, Scheible WR, Bäurle I (2014) Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell 26(4):1792–1807

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tang W, Newton RJ (2005) Plant regeneration from callus cultures derived from mature zygotic embryos in white pine (Pinus strobus L.). Plant Cell Rep 24:1–9

    CAS  PubMed  Google Scholar 

  • Tang W, Page M (2013) Transcription factor AtbZIP60 regulates expression of Ca2+-dependent protein kinase genes in transgenic cells. Mol Biol Rep 40:2723–2732

    CAS  PubMed  Google Scholar 

  • Tang W, Tang AY (2016) MicroRNAs associated with molecular mechanisms for plant root formation and growth. J For Res 27(1):1–12

    CAS  Google Scholar 

  • Wei JZ, Tirajoh A, Effendy J, Plant AL (2000) Characterization of salt-induced changes in gene expression in tomato (Lycopersicon esculentum) roots and the role played by abscisic acid. Plant Sci 159(1):135–148

    CAS  PubMed  Google Scholar 

  • Wieners RR, Fei S, Johnson RC (2006) Characterization of a USDA Kentucky bluegrass (Poapratensis L.) core collection for reproductive mode and DNA content by flow cytometry. Genet Resour Crop Evol 53(8):1531–1541

    Google Scholar 

  • Wu C, Yang J, Yan L, Yu L (2007) Salt-resistant characteristic of four grass varieties for lawn. South China Agric 2:59–61

    Google Scholar 

  • Xie Q, Liu X, Zhang Y, Tang J, Yin D, Fan B, Zhu L, Han L, Song G, Li D (2017) Identification and characterization of microRNA319a and its putative target gene, PvPCF5, in the bioenergy grass switchgrass (Panicum virgatum). Front Plant Sci 8:396

    PubMed  PubMed Central  Google Scholar 

  • Xu R, Fujiyama H (2013) Comparison of ionic concentration, organic solute accumulation and osmotic adaptation in Kentucky bluegrass and tall fescue under NaCl stress. Soil Sci Plant Nutr 59(2):168–179

    CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6(2):251–264

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamane K, Mitsuya S, Kawasaki M, Taniguchi M, Miyake H (2009) Antioxidant capacity and damages caused by salinity stress in apical and basal regions of rice leaf. Plant Prod Sci 12:319–326

    CAS  Google Scholar 

  • Yoshikawa M, Iki T, Numa H, Miyashita K, Meshi T, Ishikawa M (2016) A short open reading frame encompassing the microRNA173 target site plays a role in trans-acting small interfering RNA biogenesis. Plant Physiol 171(1):359–368

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Li L (2013) SQUAMOSA promoter binding protein-like7 regulated microRNA408 is required for vegetative development in Arabidopsis. Plant J 74(1):98–109

    CAS  PubMed  Google Scholar 

  • Zhang Z, Liu M, Liang Y, Qi H (2009) Effects of salt stress on the growth of three cold-season turf grasses. J Ecol Environ 18(5):1877–1880

    CAS  Google Scholar 

  • Zhao Y, Lin S, Qiu Z, Cao D, Wen J, Deng X, Wang X, Lin J, Li X (2015) MicroRNA857 is involved in the regulation of secondary growth of vascular tissues in Arabidopsis. Plant Physiol 169(4):2539–2552

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This program was supported by the National Natural Science Foundation of China (No. 31672477).

Author information

Authors and Affiliations

  1. Turfgrass Research Institute, College of Grassland Science, Beijing Forestry University, Beijing, 100083, China

    Hongsong Luo, Zhixiang Zhou, Guilong Song & Liebao Han

  2. Beijing No. 161 High School, Beijing, 100053, China

    Hongxiang Yao

Authors
  1. Hongsong Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhixiang Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guilong Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hongxiang Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Liebao Han
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Liebao Han.

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 file1 (XLSX 12 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luo, H., Zhou, Z., Song, G. et al. Antioxidant enzyme activity and microRNA are associated with growth of Poa pratensis callus under salt stress. Plant Biotechnol Rep 14, 429–438 (2020). https://doi.org/10.1007/s11816-020-00620-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11816-020-00620-x

Keywords

Search

Navigation