Skip to main content
SpringerLink
Log in

Manipulation of cellular energy reveals the relationship between ultraweak luminescence and cellular energy during senescence of strawberry (Fragaria × ananassa) fruits

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

The goal of this study was to investigate the ultraweak luminescence (UWL) of strawberry fruits in relation to mitochondrial functions and energy production during strawberry senescence. Fully ripe strawberry fruits and mitochondria isolated from those fruits were treated with either adenosine triphosphate (ATP) or the respiratory chain uncoupler 2,4-dinitrophenol (DNP). The activities of H+-ATPase and Ca2+-ATPase, the content of ATP, the free radical O2− as well as the UWL intensity were measured. Our results showed that activities of H+-ATPase and Ca2+-ATPase as well as the ATP content gradually decreased during fruit senescence in all three groups. Compared with the control, DNP treatment exacerbated, while ATP treatment reduced the decrease of H+-ATPase and Ca2+-ATPase activity, the energy charge and UWL intensity. UWL intensity was positively correlated with mitochondrial function and ATP content. Our results strongly suggest that mitochondria are a major source of UWL of strawberry fruits, and that the cellular energy ATP plays important roles in senescence of strawberry fruits, and in UWL formation. Our study provides convincing evidence of the interrelationship between cellular energy and UWL, which helps researchers to better understand the process of senescence in strawberry fruits.

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

Similar content being viewed by others

References

  • Afanas’ev I (2010) Signaling and damaging functions of free radicals in aging-free radical theory, hormesis and TOR. Aging Dis 1:75–88

    PubMed  PubMed Central  Google Scholar 

  • Alvarez-Suarez JM, Mazzoni L, Forbes-Hernandez TY, Gasparrini M, Sabbadini S, Giampieri F (2014) The effects of pre-harvest and post-harvest factors on the nutritional quality of strawberry fruits: a review. J Berry Res 4:1–10

    Article  CAS  Google Scholar 

  • Andrianjaka-Camps ZN, Heritier J, Ançay A, Andlauer W, Carlen C (2017) Evolution of the taste-related and bioactive compound profiles of the external and internal tissues of strawberry fruits (Fragaria x ananassa) cv. ‘Clery’ during ripening. J Berry Res 7:11–22

    Article  CAS  Google Scholar 

  • Atkinson DE, Walton GM (1967) Adenosine triphosphate conservation in metabolic regulation. Rat liver citrate cleavage enzyme. J Biol Chem 242:3239–3241

    PubMed  CAS  Google Scholar 

  • Chen H, Yang H, Gao H, Long J, Tao F, Fang X, Jiang Y (2013) Effect of hypobaric storage on quality, antioxidant enzyme and antioxidant capability of the Chinese bayberry fruits. Chem Cent J 7:4. https://doi.org/10.1186/1752-153X-7-4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cifra M, Pospíšil P (2014) Ultra-weak photon emission from biological samples: definition, mechanisms, properties, detection and applications. J Photochem Photobiol B 139:2–10

    Article  PubMed  CAS  Google Scholar 

  • Cocco C, Magnani S, Maltoni ML, Quacquarelli I, Cacchi M, Antunes LEC, D’Antuono LF, Faedi W, Baruzzi G (2015) Effects of site and genotype on strawberry fruits quality traits and bioactive compounds. J Berry Res 5:145–155

    Article  CAS  Google Scholar 

  • Gasparrini M, Forbes-Hernandez TY, Giampieri F, Afrin S, Alvarez-Suarez JM, Mazzoni L, Mezzetti B, Quiles JL, Battino M (2017) Anti-inflammatory effect of strawberry extract against LPS-induced stress in RAW 264.7 macrophages. Food ChemToxicol 102:1–10

    Article  CAS  Google Scholar 

  • Giampieri F, Alvarez-Suarez JM, Mazzoni L, Forbes-Hernandez TY, Gasparrini M, Gonzàlez-Paramàs AM, Santos-Buelga C, Quiles JL, Bompadre S, Mezzetti B, Battino M (2014) An anthocyanin-rich strawberry extract protects against oxidative stress damage and improves mitochondrial functionality in human dermal fibroblasts exposed to an oxidizing agent. Food Funct 5(8):1939–1948

    Article  PubMed  CAS  Google Scholar 

  • Giampieri F, Alvarez-Suarez JM, Cordero MD, Gasparrini M, Forbes-Hernandez TY, Afrin S, Santos-Buelga C, González-Paramás AM, Astolfi P, Rubini C, Zizzi A, Tulipani S, Quiles JL, Mezzetti B, Battino M (2017) Strawberry consumption improves aging-associated impairments, mitochondrial biogenesis and functionality through the AMP-activated protein kinase signaling cascade. Food Chem 234:464–471

    Article  PubMed  CAS  Google Scholar 

  • Guo J, Liu H, Liang S, Zhu G, Bai Y, Li L (2017a) Relationship between reactive oxygen species and ultraweak luminescence in strawberry fruit during senescence under various reactive oxygen regulation treatments. J Fruit Sci 34:363–369

    Google Scholar 

  • Guo J, Zhu G, Li L, Liu H, Liang S (2017b) Ultraweak photon emission in strawberry fruit during ripening and aging is related to energy level. Open Life Sci 12:393–398

    Google Scholar 

  • Gurvisch AG, Grabje S, Salkind S (1923) Die Natur des spezifischen Erregers der Zellteilung. Arch Entw Mech 100:11–40

    Google Scholar 

  • Hou X, Liao X, Li Y, Zhang X, Bu W, Jia Y, Li G (2004) Ultraweak biophoton emission and its mechanism during seed germination of Amaranthus hypochondriacus. Seed 23:23–27

    Google Scholar 

  • IuA V, Lvova OF (1964) Ultra-weak luminescence and oxidative phosphorylation. Mitochondria Biofiz 9:506–507

    Google Scholar 

  • Kamal AH, Komatsu S (2015) Involvement of reactive oxygen species and mitochondrial proteins in biophoton emission in roots of soybean plants under flooding stress. J Proteome Res 14:2219–2236. https://doi.org/10.1021/acs.jproteome.5b00007

    Article  PubMed  CAS  Google Scholar 

  • Li H (2004) The physiological experimental principle and technology of plant. Advanced Education Press, Beijing

    Google Scholar 

  • Lin G, Huang Z, Zhang C, Zheng C (2008) Changes in ultraweak luminescence intensity, respiration rate and physiological metabolism of chrysanthemum during floral differentiation. Acta Hortic Sin 35:1819–1824

    CAS  Google Scholar 

  • Liu H, Liao X, Wu L, Jiang J (2006) Effect of heat shock on biophoton and activities of antioxidant enzymes in immature wheat grains. J Food Sci Biotech 25:75–78

    CAS  Google Scholar 

  • Liu T, Qian Z, Yang E,F, Qu H, Jiang Y (2010) Respiratory activity and energy metabolism of harvested litchi fruit and their relationship to quality deterioration. J Fruit Sci 27:946–951

    CAS  Google Scholar 

  • Liu H, Liang S, Yan Y, Bai Y, Guo J (2017) The relationship between senescence and ultraweak photon emission under controlling of reactive oxygen and energy in strawberry fruit. Acta Bot Boreal-Occident Sin 37:1182–1188

    Google Scholar 

  • Popp FA, Guq L (1992) Recent advances in biophoton research and its applications Singapore: World Scientific 1

  • Popp FA, Li KH, Mei WP, Galle M, Neurohr R (1988) Physical aspects of biophotons. Experientia 44:576–585

    Article  PubMed  CAS  Google Scholar 

  • Saquet AA, Streif J, Bangerth F (2000) Changes in ATP, ADP and pyridine nucleotide levels related to the incidence of physiological disorders in Conference pears and Jonagold apples during controlled atmosphere storage. J Hortic Sci Biotechnol 75:243–249

    Article  CAS  Google Scholar 

  • Serlin BS, Sopory SK, Roux SJ (1984) Modulation of oat mitochondrial ATPase activity by CA2+ and phytochrome. Plant Physiol 74:827–833

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stawinski J, Grabikowski E, Majchrowicz I (1980) Ultraweak photon emission generated by germination. Biophoton Phys 1:72–100

    Google Scholar 

  • Tan S, Xing D, Tang Y, Li D (2000) Spectral studies of ultra-weak biophoton emission from plant’s leaves. Acta Photo Sin 29:961–965

    Google Scholar 

  • Tian S, Qin G, Li B (2013) Reactive oxygen species involved in regulating fruit senescence and fungal pathogenicity. Plant Mol Biol 82:593–602. https://doi.org/10.1007/s11103-013-0035-2

    Article  PubMed  CAS  Google Scholar 

  • Toroser D, Orr WC, Sohal RS (2007) Carbonylation of mitochondrial proteins in Drosophila melanogaster during aging. Biochem Biophys Res Commun 363:418–424. https://doi.org/10.1016/j.bbrc.2007.08.193

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang H (2007) Effect of respiratory metabolism associated enzymes in mitochondria on peach fruit ripening and softening. Yangzhou Univ 21:21–22

    CAS  Google Scholar 

  • Wang C, Jiang L, Wang L, Zhu W (2013) Analysis and application of ultraweak bioluminescence of serum in dairy cow. Jiangsu Agri Sci 41:187–189

    Google Scholar 

  • Yuan Z (2008) Research progress on ultraweak bioluminescence. J Anhui Agri Sci 36:3092–3094

    CAS  Google Scholar 

  • Yue X, Liu Y, Hu X, Dong Y (2008) The study of ultraweak luminescence of Anabaena Flos-Aquae Chin. J Spectr Lab 25:673–676

    CAS  Google Scholar 

  • Zhang X, Yang H (2004) Ultraweak bioluminescence of chloroplast and mitochondria in plants. Plant Physiol Com 40:111–114

    Google Scholar 

  • Zhang X, Yang H, Li F, Zhang W (2004) Changes in ultraweak luminescence, ATP and active oxygen contents during apricot florescence. J Plant Physiol Mol Biol 30:41–44

    CAS  Google Scholar 

  • Zhang J, Zhang X, Gong Z (2010) Application of ultraweak bioluminescence in vegetable research. Chin Agri Sci Bull 30:2493–2495

    Google Scholar 

  • Zhu G (2015) The change of ultraweak bioluminescence at the process of development and maturation in strawberry fruit and focus on the excitation mechanism of reactive oxygen and energy level. Master thesis, Inner Mongolia Agricultural University. http://kns.cnki.net/KCMS/detail/detail.aspx?dbcode=CMFD&dbname=CMFD201502&filename=1015428178.nh&v=MTc4NDdTN0RoMVQzcVRyV00xRnJDVVJMS2ZZT1p0Rnl6blVyL0tWRjI2RzdlNkZ0RExwNUViUElSOGVYMUx1eFk=

Download references

Acknowledgements

This work was financially supported by the Natural Science Foundation of China (Grant No. 31260455).

Author information

Authors and Affiliations

  1. College of Agronomy, Inner Mongolia Agricultural University, Hohhot, Inner Mongolia, 010019, China

    Jinli Guo, Huan Liu, Yang Bai, Yutong Yan & Lianguo Li

Authors
  1. Jinli Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yang Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yutong Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lianguo Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lianguo Li.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Human and animal rights statement

This study did not involve human participants and/or animals.

Additional information

Communicated by Pramod Kumar Nagar.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, J., Liu, H., Bai, Y. et al. Manipulation of cellular energy reveals the relationship between ultraweak luminescence and cellular energy during senescence of strawberry (Fragaria × ananassa) fruits. Acta Physiol Plant 40, 134 (2018). https://doi.org/10.1007/s11738-018-2709-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-018-2709-5

Keywords

Search

Navigation