Advertisement

Plant Biotechnology Reports

, Volume 13, Issue 3, pp 293–304 | Cite as

Elevated carbon dioxide significantly improves ascorbic acid content, antioxidative properties and restricted biomass production in cruciferous vegetable seedlings

  • Muthusamy Muthusamy
  • Jung Eun Hwang
  • Suk Hee Kim
  • Jin A. Kim
  • Mi-Jeong Jeong
  • Hyeong Cheol Park
  • Soo In LeeEmail author
Original Article
  • 201 Downloads

Abstract

The rise in atmospheric CO2 concentrations has profound impact on nutritional, metabolic and physiological activities of crop plants. In this study, the impact of elevated CO2 ranging from 350 to 4000 ppm on l-ascorbic acid (AsA) content, antioxidative properties and growth characteristics of four cruciferous vegetable seedlings (Chinese cabbage, bok choy, radish and red young radish) was analyzed. Quantitative reverse transcription-polymerase chain reaction (qRT-PCR) and high performance liquid chromatography (HPLC) analysis showed that elevated CO2 markedly induced AsA biosynthetic and AsA regeneration pathway genes thus accumulating AsA at least 0.53–1.62-folds among seedlings. Subsequent analysis showed that elevated CO2 accumulated relatively more AsA in root vegetables than leafy vegetables. AsA improves the antioxidative properties either directly or indirectly via improving the radical scavenging activities of Super Oxide Dismutase (SOD) in a concentration dependent manner. Additionally, CO2 enrichment activated Ascorbate peroxidase-6 (BrAPX6) to control the accumulation of H2O2. Moreover, CO2 at 700 ppm considerably improved biomass production of Chinese cabbage (1.9%), bok choy (1.84%) and red young radish (3%) seedlings. However, further enrichment of CO2 (1000–4000 ppm) gradually decreased the growth and biomass production (4.91–17.5%) in vegetable seedlings, although it improved AsA content significantly. It is thus apparent that the positive impact of elevated CO2 is restricted to 700 ppm. This study reveals that elevated CO2 can enhance the AsA content significantly, improves antioxidant properties and biomass productions in cruciferous vegetable seedlings in a dose-dependent manner.

Keywords

Ascorbic acid synthesis Antioxidants Super oxide dismutase Biomass Vegetable seedlings HPLC analysis 

Notes

Acknowledgements

This work was supported by the Rural Program for Agricultural Science and Technology Development (Project no.: PJ01247202), Rural Development Administration and the National Institute of Ecology (NIE-C-2019-15), Republic of Korea.

Compliance with ethical standards

Conflict of interest

The authors declare that no competing interests.

Supplementary material

11816_2019_542_MOESM1_ESM.docx (19 kb)
Supplementary material 1 (DOCX 18 kb)

References

  1. Akram NA, Shafiq F, Ashraf M (2017) Ascorbic acid-A potential oxidant scavenger and its role in plant development and abiotic stress tolerance. Front Plant Sci 8:613CrossRefPubMedPubMedCentralGoogle Scholar
  2. Athar HR, Khan A, Ashraf M (2009) Inducing salt tolerance in wheat by exogenously applied ascorbic acid through different modes. J Plant Nutr 32:1799–1817CrossRefGoogle Scholar
  3. Becker C, Kläring HP (2016) CO2 enrichment can produce high red leaf lettuce yield while increasing most flavonoid glycoside and some caffeic acid derivative concentrations. Food Chem 199:736–745CrossRefPubMedGoogle Scholar
  4. Berzina NJ, Markovs M, Apsīte S et al (2012) Concentration-dependent antioxidant/pro-oxidant activity of ascorbic acid in chickens. In: Proceedings of the Latvian Academy of Sciences. Section B. Natural, Exact, and Applied Sciences 66:256–260Google Scholar
  5. Bisbis MB, Gruda N, Blanke M (2018) Potential impacts of climate change on vegetable production and product quality—a review. J Clean Prod 170:1602–1620CrossRefGoogle Scholar
  6. Bybordi A (2012) Effect of ascorbic acid and silicium on photosynthesis, antioxidant enzyme activity, and fatty acid contents in canola exposure to salt stress. J Integr Agric 11:1610–1620CrossRefGoogle Scholar
  7. Cassia R, Nocioni M, Correa-Aragunde N, Lamattina L (2018) climate change and the impact of greenhouse gasses: CO2 and NO, friends and foes of plant oxidative stress. Front Plant Sci 9:1–11.  https://doi.org/10.3389/fpls.2018.00273 CrossRefGoogle Scholar
  8. Caverzan A, Passaia G, Rosa SB et al (2012) Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet Mol Biol 35:1011–1019CrossRefPubMedPubMedCentralGoogle Scholar
  9. Cohen I, Rapaport T, Berger RT, Rachmilevitch S (2018) The effects of elevated CO2 and nitrogen nutrition on root dynamics. Plant Sci 272:294–300CrossRefPubMedGoogle Scholar
  10. Delucia EH, Sasek TW, Strain BR (1985) Photosynthetic inhibition after long-term exposure to elevated levels of atmospheric carbon dioxide. Photosynth Res 7:175–184CrossRefPubMedGoogle Scholar
  11. Dietterich LHA, Zanobetti I, Kloog P et al (2015) Impacts of elevated atmospheric CO2 on nutrient content of important food crops. Sci Data 2:150036CrossRefPubMedPubMedCentralGoogle Scholar
  12. Dillon SA, Quentin M, Ivković R et al (2018) Photosynthetic variation and responsiveness to CO2 in a widespread riparian tree. PLoS One 13(1):e0189635CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dong JN, Gruda SK, Lam X et al (2018) Effects of elevated CO2 on nutritional quality of vegetables: a review. Front Plant Sci 9:924CrossRefPubMedPubMedCentralGoogle Scholar
  14. Ejaz B, Sajid ZA, Aftab F (2012) Effect of exogenous application of ascorbic acid on antioxidant enzyme activities, proline contents, and growth parameters of Saccharum spp. hybrid cv. HSF-240 under salt stress. Turkish J Biol 36:630–640Google Scholar
  15. Eom S, Baek S-A, Kim J, Hyun T (2018) Transcriptome analysis in Chinese cabbage (Brassica rapa ssp. pekinensis) provides the role of glucosinolate metabolism in response to drought stress. Molecules 23:1186CrossRefPubMedCentralGoogle Scholar
  16. Gamage D, Thompson M, Sutherland M et al (2018) New insights into the cellular mechanisms of plant growth at elevated atmospheric carbon dioxide. Plant Cell Environ 41:1233–1246CrossRefPubMedGoogle Scholar
  17. Geissler N, Hussin S, Koyro HW (2010) Elevated atmospheric CO2 concentration enhances salinity tolerance in Aster tripolium L. Planta 231:583–594CrossRefPubMedGoogle Scholar
  18. Gest N, Helene Gautier A, Stevens R (2012) Ascorbate as seen through plant evolution: the rise of a methylation and chrom. J Exp Bot 63:695–709CrossRefGoogle Scholar
  19. Ghasemzadeh A, Jaafar HZE, Rahmat A (2010) Elevated carbon dioxide increases contents of flavonoids and phenolic compounds, and antioxidant activities in malaysian young ginger (Zingiber officinale Roscoe.) varieties. Molecules 15:7907–7922CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gilbert L, Alhagdow M, Nunes-Nesi A et al (2009) GDP-d-mannose 3,5-epimerase (GME) plays a key role at the intersection of ascorbate and non-cellulosic cell-wall biosynthesis in tomato. Plant J 60:499–508CrossRefPubMedGoogle Scholar
  21. Hachiya T, Sugiura D, Kojima M et al (2014) High CO2 triggers preferential root growth of Arabidopsis thaliana via two distinct systems under low pH and low N stresses. Plant Cell Physiol 55:269–280CrossRefPubMedPubMedCentralGoogle Scholar
  22. Jakobsen I, Smith SE, Smith FA et al (2016) Plant growth responses to elevated atmospheric CO2 are increased by phosphorus sufficiency but not by arbuscular mycorrhizas. J Exp Bot 67:6173–6186CrossRefPubMedPubMedCentralGoogle Scholar
  23. Janssen PJD, Lambreva MD, Plumerà N et al (2014) Photosynthesis at the forefront of a sustainable life. Front Chem 2:1–22CrossRefGoogle Scholar
  24. Kapoor D, Sharma R, Handa N et al (2015) Redox homeostasis in plants under abiotic stress: role of electron carriers, energy metabolism mediators and proteinaceous thiols. Front Environ Sci 3:1–12.  https://doi.org/10.3389/fenvs.2015.00013 CrossRefGoogle Scholar
  25. Keeling RF, Graven HD, Welp LR et al (2017) Atmospheric evidence for a global secular increase in carbon isotopic discrimination of land photosynthesis. Proc Natl Acad Sci.  https://doi.org/10.1073/pnas.1619240114 CrossRefPubMedGoogle Scholar
  26. Kellner J, Multsch S, Houska T et al (2017) A coupled hydrological-plant growth model for simulating the effect of elevated CO2 on a temperate grassland. Agric For Meteorol 246:42–50CrossRefGoogle Scholar
  27. Kerk NM, Jiang K, Feldman LJ (2000) Auxin metabolism in the root apical meristem. Plant Physiol 122:925–932CrossRefPubMedPubMedCentralGoogle Scholar
  28. Kim GR, Jung ES, Lee S et al (2014) Combined mass spectrometry-based metabolite profiling of different pigmented rice (Oryza sativa L.) seeds and correlation with antioxidant activities. Molecules 19:15673–15686CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kimball BA, Mauney JR, Nakayama FS, Idso SB (1993) Effects of increasing atmospheric CO2 on vegetation. Vegetatio 104:65–75CrossRefGoogle Scholar
  30. Li Y, Yu Z, Liu X et al (2017) Elevated CO2 increases nitrogen fixation at the reproductive phase contributing to various yield responses of soybean cultivars. Front Plant Sci 8:1546CrossRefPubMedPubMedCentralGoogle Scholar
  31. Lin ST, Chiou CW, Chu YL et al (2016) Enhanced ascorbate regeneration via dehydroascorbate reductase confers tolerance to photo-oxidative stress in Chlamydomonas reinhardtii. Plant Cell Physiol 57:2104–2121CrossRefPubMedGoogle Scholar
  32. Makavitskaya MD, Svistunenko I, Navaselsky P et al (2018) Novel roles of ascorbate in plants: induction of cytosolic Ca2+ signals and efflux from cells via anion channels. J Exp Bot 69:3477–3489CrossRefPubMedGoogle Scholar
  33. Mellidou I, Kanellis AK (2017) Genetic control of ascorbic acid biosynthesis and recycling in horticultural crops. Front Chem 5:1–8.  https://doi.org/10.3389/fchem.2017.00050 CrossRefGoogle Scholar
  34. Mieda T, Yabuta Y, Rapolu M et al (2004) Feedback inhibition of spinach l-galactose dehydrogenase by l-ascorbate. Plant Cell Physiol 45:1271–1279CrossRefPubMedGoogle Scholar
  35. Pehlivan FE (2017) Vitamin C: an antioxidant agent. In: Vitamin C. InTechGoogle Scholar
  36. Plumb W, Townsend AJ, Rasool B et al (2018) Ascorbate-mediated regulation of growth, photoprotection, and photoinhibition in Arabidopsis thaliana. J Exp Bot 69:2823–2835CrossRefPubMedPubMedCentralGoogle Scholar
  37. Poljsak B, Ionescu JG (2009) Pro-oxidant vs. antioxidant effects of vitamin C. In: Kucharski H, Zajac J (eds) Handbook of vitamin C research: daily requirements, dietary sources and adverse effects. 153Google Scholar
  38. Poorter H, Navas ML (2003) Plant growth and competition at elevated CO2: on winners, losers and functional groups. New Phytol 157:175–198CrossRefGoogle Scholar
  39. Pottosin I, Zepeda-Jazo I (2018) Powering the plasma membrane Ca2+-ROS self-amplifying loop. J Exp Bot 69:3317–3320CrossRefPubMedPubMedCentralGoogle Scholar
  40. Qian HF, Peng XF, Han X et al (2014) The stress factor, exogenous ascorbic acid, affects plant growth and the antioxidant system in Arabidopsis thaliana. Russ J Plant Physiol 61:467–475CrossRefGoogle Scholar
  41. Schütz M, Fangmeier A (2001) Growth and yield responses of spring wheat (Triticum aestivum L. cv. Minaret) to elevated CO2 and water limitation. Environ Pollut 114:187–194CrossRefPubMedGoogle Scholar
  42. Seo Y, Ide K, Kitahata N et al (2017) Environmental impact and nutritional improvement of elevated CO2 treatment: a case study of spinach production. Sustainability 9:1854.  https://doi.org/10.3390/su9101854 CrossRefGoogle Scholar
  43. Shao HB, Chu LY, Lu ZH, Kang CM (2008) Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells. Int J Biol Sci 4:8–14CrossRefGoogle Scholar
  44. Smirnoff N (2018) Ascorbic acid metabolism and functions: a comparison of plants and mammals. Free Radic Biol Med 122:116–129CrossRefPubMedPubMedCentralGoogle Scholar
  45. Suraweera DD, Groom T, Nicolas ME (2015) Impact of elevated atmospheric carbon dioxide and water deficit on flower development and pyrethrin accumulation in Pyrethrum. Proc Environ Sci 29:5–6CrossRefGoogle Scholar
  46. Swann ALS, Hoffman FM, Koven CD, Randerson JT (2016) Plant responses to increasing CO2 reduce estimates of climate impacts on drought severity. Proc Natl Acad Sci 113:10019–10024CrossRefPubMedGoogle Scholar
  47. Taub DR, Seemann JR, Coleman JS (2000) Growth in elevated CO2 protects photosynthesis against high-temperature damage. Plant Cell Environ 23:649–656CrossRefGoogle Scholar
  48. Thompson M, Gamage D, Hirotsu N et al (2017) Effects of elevated carbon dioxide on photosynthesis and carbon partitioning: a Perspective on root sugar sensing and hormonal crosstalk. Front Physiol 8:1–13.  https://doi.org/10.3389/fphys.2017.00578 CrossRefGoogle Scholar
  49. Trivedi DK, Gill SS, Yadav S, Tuteja N (2013) Genome-wide analysis of glutathione reductase (GR) genes from rice and Arabidopsis. Plant Signal Behav 8:1–7.  https://doi.org/10.4161/psb.23021 CrossRefGoogle Scholar
  50. Wang SY, Bunce JA, Maas JL (2003) Elevated carbon dioxide increases contents of antioxidant compounds in field-grown strawberries. J Agric Food Chem 51:4315–4320CrossRefPubMedGoogle Scholar
  51. Wang Y, Du ST, Li LL et al (2009) Effect of CO2 elevation on root growth and its relationship with indole acetic acid and ethylene in tomato seedlings. Pedosphere 19:570–576CrossRefGoogle Scholar
  52. Weiss I, Mizrahi Y, Raveh E (2010) Effect of elevated CO2 on vegetative and reproductive growth characteristics of the CAM plants Hylocereus undatus and Selenicereus megalanthus. Sci Hort 123:531–536CrossRefGoogle Scholar
  53. Wu X-J, Sun S, Xing G-M et al (2017) Elevated carbon dioxide altered morphological and anatomical characteristics, ascorbic acid accumulation, and related gene expression during taproot development in carrots. Front Plant Sci 7:1–11.  https://doi.org/10.3389/fpls.2016.02026 CrossRefGoogle Scholar
  54. Yu C, Li Y, Li B et al (2010) Molecular analysis of phosphomannomutase (PMM) genes reveals a unique PMM duplication event in diverse Triticeae species and the main PMM isozymes in bread wheat tissues. BMC Plant Biol 10:214CrossRefPubMedPubMedCentralGoogle Scholar
  55. Zhang GY, Liu RR, Zhang CQ et al (2015) Manipulation of the rice l-galactose pathway: evaluation of the effects of transgene overexpression on ascorbate accumulation and abiotic stress tolerance. PLoS One 10:1–14.  https://doi.org/10.1371/journal.pone.0125870 CrossRefGoogle Scholar
  56. Zhu C, Kobayashi K, Loladze I et al (2018) Carbon dioxide levels this century will alter the protein, micronutrients and vitamin content of rice grains with potential health consequences for the poorest rice-dependent countries. Sci Adv 4:1–9Google Scholar

Copyright information

© Korean Society for Plant Biotechnology 2019

Authors and Affiliations

  • Muthusamy Muthusamy
    • 1
  • Jung Eun Hwang
    • 2
  • Suk Hee Kim
    • 1
  • Jin A. Kim
    • 1
  • Mi-Jeong Jeong
    • 1
  • Hyeong Cheol Park
    • 2
  • Soo In Lee
    • 1
    Email author
  1. 1.Department of Agricultural BiotechnologyNational Institute of Agricultural Sciences (NAS), RDAJeonjuKorea
  2. 2.Division of Ecological Conservation ResearchNational Institute of EcologySeocheonKorea

Personalised recommendations