Skip to main content
SpringerLink
Log in

The SikCuZnSOD3 gene improves abiotic stress resistance in transgenic cotton

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

The expression of a gene encoding peroxisomal Cu-Zn superoxide dismutase from Saussurea involucrata Kar. et Kir. was induced by low temperature, PEG6000 treatment, and NaCl stress. To investigate the role of SikCuZnSOD3 in the mitigation of abiotic stress, we used Agrobacterium-mediated transformation to create transgenic cotton that overexpressed SikCuZnSOD3. Phenotypic analysis of T4 generation transgenic lines showed that they generally grew better than wild-type cotton under low temperature, PEG6000 treatment, and NaCl stress. Although there were no significant differences under control conditions, transgenic plants exhibited greater survival, fresh weight, and dry weight than wild-type plants under all three stress treatments. Additional physiological analyses demonstrated that the transgenic cotton had higher relative water content, proline and soluble sugar contents, and activity of antioxidant enzymes (superoxide dismutase, catalase, and peroxidase), as well as lower relative conductivity, malondialdehyde content, and H2O2 and O2− accumulation. More importantly, overexpression of SikCuZnSOD3 increased the yield of cotton fiber. Our results confirm that the overexpression of SikCuZnSOD3 can improve the abiotic stress resistance of cotton by increasing the activity of antioxidant enzymes, maintaining ROS homeostasis, and reducing cell membrane damage.

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

Similar content being viewed by others

Data availability

Datasets supporting the conclusions of this article are included within the article.

References

  • Abreu IA, Cabelli DE (2010) Superoxide dismutases—a review of the metal-associated mechanistic variations. Biochim Biophys Acta, Gen Subj 1804:263–274

    Article  CAS  Google Scholar 

  • Ahmad P, Umar S, Sharma S (2010) Mechanism of free radical scavenging and role of phytohormones in plants under abiotic stresses. Plant Adaptation and Phytoremediation 2010:99–118

    Article  Google Scholar 

  • Ahuja I, de Vos RC, Bones AM et al (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15:664–674

    Article  CAS  PubMed  Google Scholar 

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341

    Article  CAS  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ashraf M (2002) Salt tolerance of cotton: some new advances. Crit Rev Plant Sci 21:1–30

    Article  CAS  Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Azarabadi S, Abdollahi H, Torabi M, Salehi Z, Nasiri J (2017) ROS generation, oxidative burst and dynamic expression profiles of ROS-scavenging enzymes of superoxide dismutase (SOD), catalase (CAT) and ascorbate peroxidase (APX) in response to Erwinia amylovora in pear (Pyrus communis L.). Eur J Plant Pathol 147:279–294

    Article  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 1:205–207

    Article  Google Scholar 

  • Benikhlef L, L’Haridon F, Aboumansour E et al (2013) Perception of soft mechanical stress in Arabidopsis leaves activates disease resistance. BMC Plant Biol 13:1–12

    Article  CAS  Google Scholar 

  • Bowler C, Slooten L, Vandenbranden S, de Rycke R, Botterman J, Sybesma C, van Montagu M, Inzé D (1991) Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBO J 10:1723–1732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Breusegem FV, Slooten L, Stassart JM et al (1999) Effects of overproduction of tobacco MnSOD in maize chloroplasts on foliar tolerance to cold and oxidative stress. J Exp Bot 50:71–78

    Article  Google Scholar 

  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    Article  CAS  PubMed  Google Scholar 

  • Ding FZ (2008) Research progress on application of superoxide dismutases in tobacco. J Anhui Agric Sci 36:1897–1894

    CAS  Google Scholar 

  • Dong L, He YZ, Wang YL et al (2013) Research progress on application of superoxide dismutase (SOD). J Agric Sci Technol 15:53–58

    CAS  Google Scholar 

  • Du ZY, Bramlage WJ (1992) Modified thiobarbituric acid assay for measuring lipid oxidation in sugar-rich plant tissue extracts. Journal of Agricultural and Food Chemistry 40:1566–1570

    Article  CAS  Google Scholar 

  • Du XM, Yin WX, Zhao YX et al (2001) The production and scavenging of reactive oxygen species in plants. Sheng Wu Gong Cheng Xue Bao 17:121–125

    CAS  PubMed  Google Scholar 

  • Dupont CL, Neupane K, Shearer J et al (2010) Diversity, function and evolution of genes coding for putative Ni-containing superoxide dismutases. Environ Microbiol 10:1831–1843

    Article  CAS  Google Scholar 

  • Fan DY, Hope AB, Jia H, Chow WS (2008) Separation of light-induced linear, cyclic and stroma-sourced electron fluxes to P700+ in cucumber leaf discs after pre-illumination at a chilling temperature. Plant Cell Physiol 49:901–911

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, 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 

  • Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18:2021–2034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta, Gen Subj 990:87–92

    Article  CAS  Google Scholar 

  • Getzoff ED, Tainer JA, Stempien MM, Bell GI, Hallewell RA (1989) Evolution of CuZn superoxide dismutase and the Greek key beta-barrel structural motif. Proteins 5:322–336

    Article  CAS  PubMed  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases. 1. Occurrence in higher plants [corn, oats, peas]. Plant Physiol 59:309–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gil R, Lull C, Boscaiu M et al (2011) Soluble carbohydrates as osmolytes in several halophytes from a Mediterranean salt marsh. Not Bot Horti Agrobo 39:9–17

  • Greenway A, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Biol 31:61–69

    Google Scholar 

  • Guo YY, Tian SS, Liu SS et al (2017) Energy dissipation and antioxidant enzyme system protect photosystem II of sweet sorghum under drought stress. Photosynthetica 2017:1–12

    Google Scholar 

  • Holmberg N, Bu Low L (1998) Improving stress tolerance in plants by gene transfer. Trends Plant Sci 3:61–66

    Article  Google Scholar 

  • Huang W, Zhang SB, Cao KF (2011) Cyclic electron flow plays an important role in photoprotection of tropical trees illuminated at temporal chilling temperature. Plant Cell Physiol 52:297–305

    Article  CAS  PubMed  Google Scholar 

  • Jiang HF, Ren X (2004) The effect on sod activity and protein content in groundnut leaves by drought stress. Acta Agron Sin 3:1–4

    Google Scholar 

  • Jiang Z, Zhu S, Ye R, Xue Y, Chen A, An L, Pei ZM (2013) Relationship between NaCl- and H2O2-induced cytosolic Ca2+ increases in response to stress in Arabidopsis. PLoS One 8:e76130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218

    Article  CAS  PubMed  Google Scholar 

  • Kurepa J, Smalle J, Van MM et al (1998) Oxidative stress tolerance and longevity in Arabidopsis: the late-flowering mutant gigantea is tolerant to paraquat. Plant J Cell Mol Biol 14:759–764

    Article  CAS  Google Scholar 

  • Lara MV, Disante KB, Podesta FE et al (2003) Induction of a Crassulacean acid like metabolism in the C4 succulent plant, Portulaca oleracea L.: physiological and morphological changes are accompanied by specific modifications in phosphoenolpyruvate carboxylase. Photosynth Res 77:241–254

    Article  CAS  PubMed  Google Scholar 

  • Leclercq J, Martin F, Sanier C, Clément-Vidal A, Fabre D, Oliver G, Lardet L, Ayar A, Peyramard M, Montoro P (2012) Overexpression of a cytosolic isoform of the HbCuZnSOD gene in Hevea brasiliensis changes its response to a water deficit. Plant Mol Biol 80:255–272

    Article  CAS  PubMed  Google Scholar 

  • Lin QB, Ding YG, Wang HB et al (2009) The effects of the SOD mimics on the biomass and SOD activities of rice seedlings under salt stress. Chin J Soil Sci 40:1163–1166

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78:389–398

    Article  CAS  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S et al (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Zilinskas BA (1994) Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought. Plant J 5:397–405

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Moses JC (2012) Cu/Zn superoxide dismutase activity and respective gene expression during cold acclimation and freezing stress in barley cultivars. Biol Plant 56:693–698

    Article  CAS  Google Scholar 

  • Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1247

    Article  CAS  PubMed  Google Scholar 

  • Pham HM, Kebede H, Ritchie G, Trolinder N, Wright RJ (2018) Alternative oxidase (AOX) over-expression improves cell expansion and elongation in cotton seedling exposed to cool temperatures. Theor Appl Genet 131:2287–2298

    Article  CAS  PubMed  Google Scholar 

  • Pinhero RG, Rao MV, Paliyath G, Murr DP, Fletcher RA (1997) Changes in activities of antioxidant enzymes and their relationship to genetic and paclobutrazol-induced chilling tolerance of maize seedlings. Plant Physiol 114:695–704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pitzschke A, Forzani C, Hirt H (2006) Reactive oxygen species signaling in plants. Antioxid Redox Signal 8:1757–1764

    Article  CAS  PubMed  Google Scholar 

  • Quan LJ, Zhang B, Shi WW et al (2010) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. J Integr Plant Biol 50:2–18

    Article  CAS  Google Scholar 

  • Razali N, Aziz AA, Lim CY et al (2015) Investigation into the effects of antioxidant-rich extract of Tamarindus indica leaf on antioxidant enzyme activities, oxidative stress and gene expression profiles in HepG2 cells. PeerJ 3:1227–1238

    Article  CAS  Google Scholar 

  • Song XS, Wang YJ, Mao WH, Shi K, Zhou YH, Nogués S, Yu JQ (2009) Effects of cucumber mosaic virus infection on electron transport and antioxidant system in chloroplasts and mitochondria of cucumber and tomato leaves. Physiol Plant 135:246–257

    Article  CAS  PubMed  Google Scholar 

  • Sugimoto M, Oono Y, Gusev O, Matsumoto T, Yazawa T, Levinskikh MA, Sychev VN, Bingham GE, Wheeler R, Hummerick M (2014) Genome-wide expression analysis of reactive oxygen species gene network in mizuna plants grown in long-term spaceflight. BMC Plant Biol 14:4–4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Takemura S, Hanagata N, Sugihara K et al (2000) Physiological and biochemical responses to salt stress in the mangrove, Bruguiera gymnorrhiza. Aquat Bot 68:15–28

    Article  CAS  Google Scholar 

  • Tepperman JM, Dunsmuir P (1990) Transformed plants with elevated levels of chloroplastic SOD are not more resistant to superoxide toxicity. Plant Mol Biol 14:501–511

    Article  CAS  PubMed  Google Scholar 

  • Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chemico-Biological Interactions 160:1–40

    Article  CAS  PubMed  Google Scholar 

  • Whittaker JW (2010) Metal uptake by manganese superoxide dismutase. BBA-Proteins and Proteomics 1804:298–307

  • Xia M, Wang W, Yuan R et al (2015) Superoxide dismutase and its research in plant stress-tolerance. Mol Plant Breed 13:2633–2646

    CAS  Google Scholar 

  • Yan ZL, Niu JY, Xi LL et al (2009) Effect of soil water on protective enzyme activity and membrane lipid peroxidation in pea. Chin J Eco-Agric 17:554–559

    Article  CAS  Google Scholar 

  • Youn HD, Kim EJ, Roe JH et al (1996) A novel nickel-containing superoxide dismutase from Streptomyces spp. Biochem J 318:889–896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng XC, Liu ZG, Shi PH et al (2014) Cloning and expression analysis of copper and zinc superoxide dismutase (Cu/Zn-SOD) gene from Brassica campestris L. Acta Agronomica Sinica 40:636–643

    Article  CAS  Google Scholar 

  • Zhang Y, Tan J, Guo Z et al (2010) Increased abscisic acid levels in transgenic tobacco over-expressing 9 cis-epoxycarotenoid dioxygenase influence H2O2 and NO production and antioxidant defences. Plant Cell Environ 32:509–519

    Article  CAS  Google Scholar 

  • Zhang YT, Gao JM, Zhang QL et al (2016) Research progress on plant superoxide dismutase. AHFS 37:28–31

  • Zhu JB, Liu HL, Wang Z et al (2006) Construction of full-length cDNA library from the Saussurea involucrata Kar.et Kir Laminae. AABOS 15:170–173

Download references

Funding

This work was supported by the Xinjiang 2019 Postgraduate Scientific Research Innovation Project (Grant number XJ2019G084), Shihezi University–independently funded and supported project (Grant number ZZZC202082B), National GMO Major Project (Grant number 2016ZX080005004-009), and Key Scientific and Technological Projects for the Cultivation of New Varieties of Genetically Modified Organisms (Grant number 2018ZX0800501B-005).

Author information

Author notes

  1. Li Zhang, Wenhui Tian, and Gang Huang contributed equally to this manuscript and are co-first authors.

Authors and Affiliations

  1. Department of Preventive Medicine, School of Medicine, Key laboratory of Preventive Medicine, Shihezi University, Shihezi, 832000, China

    Li Zhang

  2. College of Life Science, Shihezi University, Shihezi, 832000, China

    Wenhui Tian, Gang Huang, Bucang Liu, Aiying Wang, Jianbo Zhu & Xinyong Guo

Authors
  1. Li Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wenhui Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gang Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bucang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aiying Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jianbo Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xinyong Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LZ: data curation and visualization; WHT: supervision and methodology; GH, major revision and formal analysis; BCL: software; AYW: writing (reviewing and editing); JBZ: validation and investigation; XYG: conceptualization and writing (original draft preparation). All authors read and approved the manuscript.

Corresponding authors

Correspondence to Aiying Wang, Jianbo Zhu or Xinyong Guo.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interest

The authors declare no competing interests.

Code availability

Not applicable.

Additional information

Publisher’s note

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

Supplementary information

ESM 1

(DOCX 7659 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, L., Tian, W., Huang, G. et al. The SikCuZnSOD3 gene improves abiotic stress resistance in transgenic cotton. Mol Breeding 41, 26 (2021). https://doi.org/10.1007/s11032-021-01217-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-021-01217-0

Keywords

Search

Navigation