Plant Cell, Tissue and Organ Culture (PCTOC)

, Volume 136, Issue 3, pp 479–487 | Cite as

Response of NAC transcription factor genes against chromium stress in sunflower (Helianthus annuus L.)

  • Merve YuceEmail author
  • Mahmut Sinan Taspinar
  • Murat Aydin
  • Guleray Agar
Original Article


Abiotic stresses, such as heavy metals, adversely affect the living groups including plants. It should be ensured that plants are resistant to environmental stresses in order to increase their growth and development. In this sense, it is an important step for agriculture identify stress-related genes whose tolerance against environmental stresses can be increased. NAC transcription factor (TF) genes provide plant growth and development as well as regulate abiotic stress responses. Therefore, this study was conducted to determine expression levels of NAC TF genes (TF ID: Han682, Han2027 and Han2724) against chromium (Cr; 1 mM) stress in sunflower tolerant to heavy metals. The effects of copper (Cu; 0,25 mM), which are micronutrient elements, and exogenous ascorbic acid (AsA; 200 mg/L) treatments on the expression of these genes and some stress parameters such as chlorophyll amount, leaf relative water content, cell membrane damage are examined. According to the results obtained, Cr stress decreased chlorophyll content and leaf water content and increased cell membrane damage. Treatment of AsA and Cu in combination with Cr reduced toxicity by decreasing cell membrane damage by increasing chlorophyll content and leaf relative water content. The results obtained show that Cu and AsA can equally improve Cr stress. Expression profiles of NAC TF genes obtained by quantitative real-time PCR (q-PCR) were changed with plant tissues. NAC TF genes, which are upregulated with Cr stress in the root, have been determined to be a heavy metal response gene.


Cell membrane damage Chlorophyll Heavy metal stress Sunflower Transcription factors 


Author contributions

GA and MY planned and conducted the research. MST and MA provided tools and analyzed the data. GA and MY wrote the manuscript with the contributions of other authors. All authors have read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Amin B, Mahleghah G, Mahmood HMR, Hossein M (2009) Evaluation of interaction effect of drought stress with ascorbate and salicylic acid on some of physiological and biochemical parameters in okra (Hibiscus esculentus L.). Res J Biol Sci 4:380–387Google Scholar
  2. Aziz A, Akram NA, Ashraf M (2018) Influence of natural and synthetic vitamin C (ascorbic acid) on primary and secondary metabolites and associated metabolism in quinoa (Chenopodium quinoa Willd.) plants under water deficit regimes. Plant Physiol Biochem 123:192–203CrossRefGoogle Scholar
  3. Azooz MM, Abou-Elhamd MF, Al-Fredan MA (2012) Biphasic effect of copper on growth, proline, lipid peroxidation and antioxidant enzyme activities of wheat (Triticum aestivum cv. Hasaawi) at early growing stage. AJCS 6(4):688–694Google Scholar
  4. Cao H, Wang L, Nawaz MA, Niu M, Sun J, Xie J, Kong Q, Huang Y, Cheng F, Bie Z (2017) Ectopic expression of pumpkin NAC transcription factor CmNAC1 improves multiple abiotic stress tolerance in arabidopsis. Front Plant Sci 8:2052CrossRefGoogle Scholar
  5. Choudhury S, Panda SK (2005) Toxic effects, oxidative stress and ultrastructural changes in moss Taxıthelıum Nepalense (Schwaegr.) broth under chromium and lead phytotoxicity. Water Air Soil Pollut 167:73–90CrossRefGoogle Scholar
  6. Datta JK, Bandhyopadhyay A, Banerjee A, Mondal NK (2011) Phytotoxic effect of chromium on the germination, seedling growth of some wheat (Triticum aestivum L) cultivars under laboratory condition. J Agric Technol 7(2):395–402Google Scholar
  7. Dube BK, Tewari K, Chatterjee J, Chatterjee C (2003) Excess chromium alters uptake and translocation of certain nutrients in citrullus. Chemosphere 53:1147–1153CrossRefGoogle Scholar
  8. Farid M, Ali S, Rizwan M, Ali Q, Saeed R, Nasir T, Abbasi GH, Rehmani MIA, Ata-Ul-Karim AT, Bukhari SAH, Ahmad T (2018) Phyto-management of chromium contaminated soils through sunflower under exogenously applied 5-aminolevulinic acid. Ecotoxicol Environ Saf 151:255–265CrossRefGoogle Scholar
  9. Farkhondeh R, Nabizadeh E, Jalilnezhad N (2012) Effect of salinity stress on proline content, membrane stability and water relations in two sugar beet cultivars. Int J Agric Sci 2:385–392Google Scholar
  10. Fernandez P, Di Rienzo JA, Moschen S, Dosio GAA, Aguirrezabal LAN, Hopp HE, Paniego N, Heinz RA (2011) Comparison of predictive methods and biological validation for qPCR reference genes in sunflower leaf senescence transcript analysis. Plant Cell Rep 30:63–74CrossRefGoogle Scholar
  11. Handa N, Kohli SK, Thukral AK, Bhardwaj R, Alyemeni MN, Wijaya L, Ahmad P (2018) Protective role of selenium against chromium stress involving metabolites and essential elements in Brassica juncea L. seedlings. 3 Biotech 8:66CrossRefGoogle Scholar
  12. He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903–916CrossRefGoogle Scholar
  13. Hoagland DR, Arnon DI (1938) The water-culture method for growing plants without soil. Circular Calif Agric (Berkeley) 347:347–353Google Scholar
  14. Howladar SM (2014) A novel Moringa oleifera leaf extract can mitigate the stress effects of salinity and cadmium in bean (Phaseolus vulgaris L.) plants. Ecotoxicol Environ Saf 100:69–75CrossRefGoogle Scholar
  15. Iqgal MM, Murtaza G, Naz T, Javed W, Hussain S, Ilyas M, Anjum MA, Shahzad SM, Ashraf M, Iqbal Z (2017) Uptake, translocation of Pb and chlorophyll contents of Oryza sativa as influence by soil-applied amendments under normal and salt-affected Pb-spiked soil conditions. Asian J Agric Biol 5:15–25Google Scholar
  16. Jin C, Li KQ, Xu XY, Zhang HP, Chen HX, Chen YH, Hao J, Wang Y, Huang XS, Zhang SL (2017) A novel NAC transcription factor, PbeNAC1, of Pyrus betulifolia confers cold and drought tolerance via interacting with PbeDREBs and activating the expression of stress-responsive genes. Front Plant Sci 8:1049CrossRefGoogle Scholar
  17. Liu W, Xu L, Wang Y, Shen H, Zhu X, Zhang K, Chen Y, Yu R, Limera C, Liu L (2015) Transcriptome-wide analysis of chromium-stress responsive microRNAs to explore miRNA-mediated regulatory networks in radish (Raphanus sativus L.). Sci Rep 5:14024CrossRefGoogle Scholar
  18. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Nat Methods 25:402–408Google Scholar
  19. Lutts S, Kinet JM, Bouharmont J (1996) NaCl- induced senescence in leaves of rice cultivars differing in salinity resistance. Ann Bot 78:389–398CrossRefGoogle Scholar
  20. Lv X, Lan S, Guy KM, Yang J, Zhang M, Hu Z (2016) Global expressions landscape of NAC transcription factor family and their responses to abiotic stresses in Citrullus lanatus. Sci Rep 6:30574CrossRefGoogle Scholar
  21. Malik S, Ashraf M (2012) Exogenous application of ascorbic acid stimulates growth and photosynthesis of wheat (Triticum aestivum). Soil Environ 31:72–77Google Scholar
  22. Mata CG, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 126:1196–1204CrossRefGoogle Scholar
  23. Naz H, Akram NA, Ashraf M (2016) Impact of ascorbic acid on growth and some physiological attributes of cucumber (Cucumis sativus) plants under water-deficit conditions. Pak J Bot 48:877–883Google Scholar
  24. Nezami A, Khazaei HR, Rezazadeh ZB, Hosseini A (2008) Effects of drought stress and defoliation on sunflower (Helianthus annuus) in controlled conditions. Desert 12:99–104Google Scholar
  25. Nguyen KH, Ha CV, Watanabe Y, Tran UT, Nasr Esfahani M, Nguyen DV, Tran LS (2015) Correlation between differential drought tolerability of two contrasting drought-responsive chickpea cultivars and differential expression of a subset of CaNAC genes under normal and dehydration conditions. Front Plant Sci 6:449Google Scholar
  26. Rady MM (2011) Effect of 24-epibrassinolide on growth, yield, antioxidant system and cadmium content of bean (Phaseolus vulgaris L.) plants under salinity and cadmium stress. Sci Hortic 129:232–237CrossRefGoogle Scholar
  27. Rady MM, Howladar MM, Howladar SM (2016) Ascorbic acid application mitigate the salt stress effects on Helianthus annuus L. plants grown on a reclaimed saline soil. Miami USA Mar 24–25 18:1732–1736Google Scholar
  28. Rivelli AR, De Maria S, Puschenreiter M, Gherbin P (2012) Accumulation of cadmium, zinc, and copper by Helianthus annuus L.: impact on plant growth and uptake of nutritional elements. Int J Phytorem 14:320–334CrossRefGoogle Scholar
  29. Sarwar N, Malhi SS, Zia MH, Naeem A, Bibi S, Farid G (2010) Role of mineral nutrition in minimizing cadmium accumulation by plants. J Sci Food Agric 90:925–937Google Scholar
  30. Shao H, Wang H, Tang X (2015) NAC transcription factors in plant multiple abiotic stress responses: progress and prospects. Front Plant Sci 6:902CrossRefGoogle Scholar
  31. Singh HP, Mahajan P, Kaur S, Batish DR, Kohli RK (2013) Chromium toxicity and tolerance in plants. Environ Chem Lett 11:229–254CrossRefGoogle Scholar
  32. Vajpayee P, Tripathi RD, Rai UN, Ali MB, Singh SN (2000) Chromium (VI) accumulation reduces chlorophyll biosynthesis, nitrate reductase activity and protein content in Nymphaea alba L. Chemosphere 41:1075–1082CrossRefGoogle Scholar
  33. Wang R, Liu S, Zhou F, Ding C, Hua C (2014) Exogenous ascorbic acid and glutathione alleviate oxidative stress induced by salt stress in the chloroplasts of Oryza sativa L. Z Naturforsch C 69:226–236CrossRefGoogle Scholar
  34. Xia N, Zhang G, Liu XY, Deng L, Cai GL, Zhang Y, Wang XJ, Zhao J, Huang LL, Kang ZS (2010) Characterization of a novel wheat NAC transcription factor gene involved in defense response against stripe rust pathogen infection and abiotic stresses. Mol Biol Rep 37:3703–3712CrossRefGoogle Scholar
  35. Zeid IM (2001) Responses of Phaseolus vulgaris to chromium and cobalt treatments. Biol Plant 44:111–115CrossRefGoogle Scholar
  36. Zeng F, Qiu B, Wu X, Niu S, Wu F, Zhang G (2012) Glutathione-mediated alleviation of chromium toxicity in rice plants. Biol Trace Elem Res 148:255–263CrossRefGoogle Scholar
  37. Zhang L, Zhang L, Xia C, Zhao G, Jia J, Kong X (2015) The novel wheat transcription factor TaNAC47 enhances multiple abiotic stress tolerances in transgenic plants. Front Plant Sci 6:1174Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Merve Yuce
    • 1
    Email author
  • Mahmut Sinan Taspinar
    • 2
  • Murat Aydin
    • 2
  • Guleray Agar
    • 1
  1. 1.Department of Biology, Faculty of ScienceAtaturk UniversityErzurumTurkey
  2. 2.Department of Agricultural Biotechnology, Faculty of AgricultureAtaturk UniversityErzurumTurkey

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