Advertisement

Journal of Plant Growth Regulation

, Volume 38, Issue 1, pp 315–324 | Cite as

Role of Reactive Oxygen Species in Cotyledon Senescence During Early Seedling Stage of Mung Bean [Vigna radiata (L.) Wilczek]

  • Lily Pal
  • Rup Kumar KarEmail author
Article

Abstract

Reactive oxygen species (ROS) plays an important role in senescence, which was studied for cotyledon senescence in mung bean (Vigna radiata) seeds following germination in the present work. Morphology and chlorophyll content analysis revealed that cotyledons undergo a short developmental stage followed by senescence when attached with axis while detachment prolonged such developmental changes and delayed senescence. Histolocalization and spectrophotometric analysis of ROS revealed a positive correlation between the total chlorophyll content and extracellular superoxide (O2•−) level that accumulated around chlorophyllous regions, whereas hydrogen peroxide (H2O2) was mainly localized in the peripheral cells, wherefrom storage mobilization started for both intact and isolated cotyledons. Among the antioxidant enzymes, catalase (CAT, EC 1.11.1.6) and ascorbate peroxidase (APX, EC 1.11.1.11) activity declines when peroxidase (POX, EC 1.11.1.7) and superoxide dismutase (SOD, EC 1.15.1.1) activity was maintained during cotyledon senescence. POX activity, which was mainly localized in the cell wall, showed a positive correlation with total chlorophyll content for both intact and isolated cotyledons, whereas CAT activity showed positive and negative correlation with total chlorophyll content for intact and isolated cotyledons, respectively. On the other hand, a clear negative correlation was shown by APX activity of both intact and isolated cotyledons, whereas a highly positive correlation was established for SOD activity with total chlorophyll content of intact cotyledons only. Possible association of O2•− with cotyledon development and H2O2 with storage mobilization followed by senescence has been proposed.

Keywords

Antioxidant enzymes Chlorophyll Cotyledon senescence Hydrogen peroxide Mung bean Superoxide 

Notes

Acknowledgements

Lily Pal gratefully acknowledges the financial support in the form of “UGC- Basic Scientific Research (BSR) Fellowship” [Number and date of award letter: F. 7-220/2009 (BSR) dated: 13/12/2012] from the University Grants Commission, New Delhi, India. Authors also acknowledge the kind assistance of Dr. Saran Ishika Maiti, Department of Statistics, Visva-Bharati University for statistical analyses of the data.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

344_2018_9845_MOESM1_ESM.docx (184 kb)
Supplementary material 1 (DOCX 183 KB)

References

  1. Arnon DI (1949) Copper enzymes in isolated chloroplasts phytophenoloxidase in Beta vulgaris. Plant Physiol 24:1–15CrossRefGoogle Scholar
  2. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396.  https://doi.org/10.1104/pp.106.082040 CrossRefGoogle Scholar
  3. Biswas AK, Choudhuri MA (1978) Differential behaviour of the flag leaf of intact rice plant during ageing. Biochem Physiol Pflanzen 173:220–228CrossRefGoogle Scholar
  4. Brown AV, Hudson KA (2015) Developmental profiling of gene expression in soybean trifoliate leaves and cotyledons. BMC Plant Biol 15:169.  https://doi.org/10.1186/s12870-015-0553-y CrossRefGoogle Scholar
  5. Das S, Kar RK (2017) Reactive oxygen species-mediated promotion of root growth under mild water stress during early seedling stage of Vigna radiata (L.) Wilczek. J Plant Growth Regul 36:338–347.  https://doi.org/10.1007/s00344-016-9643-9 CrossRefGoogle Scholar
  6. Farkas GL, Dezsi L, Horvath M, Kisban K, Udvardy J (1963/1964) Common pattern of enzymatic changes in detached leaves and tissues attacked by parasites. Phytopathol Zeit 49:343–354Google Scholar
  7. Fick NG, Qualset CO (1975) Genetic control of endosperm amylase activity and gibberellin response in standard height and short-statured wheat. Proc Natl Acad Sci 72:892–895CrossRefGoogle Scholar
  8. Foyer CH, Noctor G (2003) Redox sensing and signaling associated with reactive oxygen in chloroplasts peroxisomes and mitochondria. Physiol Plant 119:355–364CrossRefGoogle Scholar
  9. Foyer CH, Noctor G (2005) Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071CrossRefGoogle Scholar
  10. Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18.  https://doi.org/10.1104/pp.110.167569 CrossRefGoogle Scholar
  11. Gay CA, Gebicki JM (2000) A critical evaluation of the effect of sorbitol on the ferric-xylenol orange hydroperoxide assay. Anal Biochem 284:217–220CrossRefGoogle Scholar
  12. Giannopolitis CN, Ries SK (1977) Superoxide dismutase. I. Occurrence in higher plants. Plant Physiol 59:309–314CrossRefGoogle Scholar
  13. Gomes MP, Garcia QS (2013) Reactive oxygen species and seed germination. Biologia 68:351–357Google Scholar
  14. Jabs T (1999) Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem Pharmacol 57:231–245CrossRefGoogle Scholar
  15. Kar RK, Choudhuri MA (1987) Possible mechanisms of light-induced chlorophyll degradation in senescing leaves of Hydrilla verticillata. Physiol Plant 70:729–734CrossRefGoogle Scholar
  16. Ke D, Sun G (2004) The effect of reactive oxygen species on ethylene production induced by osmotic stress in etiolated mungbean seedling. Plant Growth Regul 44:199–206CrossRefGoogle Scholar
  17. Kisban K, Horvath M, Dezsi L, Udvardy J, Farkas GL (1964) Role of root system in the regulation of enzyme levels in leaf tissues. Acta Bot Acad Sci Hung 10:275–287Google Scholar
  18. Linkies A, Schuster-Sherpa U, Tintelnot S, Leubner-Metzger G, Muller K (2010) Peroxidases identified in a subtractive cDNA library approach show tissue-specific transcript abundance and enzyme activity during seed germination of Lepidium sativum. J Exp Bot 61:491–502.  https://doi.org/10.1093/jxb/erp318 CrossRefGoogle Scholar
  19. Liszkay A, van der Zalm E, Schopfer P (2004) Production of reactive oxygen intermediates (O2 •−, H2O2 and OH˙) by maize roots and their role in wall loosening and elongation growth. Plant Physiol 136:3114–3123.  https://doi.org/10.1104/pp.104.044784 CrossRefGoogle Scholar
  20. Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ Exp Bot 49:69–76CrossRefGoogle Scholar
  21. Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175Google Scholar
  22. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498CrossRefGoogle Scholar
  23. Nakano Y, Asada K (1981) Hydrogen Peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  24. Pal L, Kar RK (2015) Correlative influence of axes on senescence of cotyledons following germination of mung bean Vigna radiata (L.) Wilczek Seeds. Austin J Plant Physiol 1:1–6Google Scholar
  25. Parish RW (1968) Studies on senescing tobacco leaf disks with special reference to peroxidase.I. The effects of cutting and of inhibition of nucleic acid and protein synthesis. Planta 82:1–13CrossRefGoogle Scholar
  26. Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a swiss army knife. Plant Cell Rep 24:255–265.  https://doi.org/10.1007/s00299-005-0972-6 CrossRefGoogle Scholar
  27. Qin T, Fu J, Zhang N, Du L (2006) Comparative studies of senescence-related enzymes in the cotyledon of chlorophyll b-deficient mutant and its wild type oilseed rape during senescence. Plant Sci 171(3):293–299CrossRefGoogle Scholar
  28. Ribeiro CW, Korbes AP, Garighan JA, Jardim-Messeder D, Carvalho FEL, Sousa RHV, Caverzan A, Teixeira FK, Silveira JAG, Margis-Pinheiro M (2017) Rice peroxisomal ascorbate peroxidase knock down affects ROS signaling and triggers early leaf senescence. Plant Sci 263:55–65.  https://doi.org/10.1016/j.plantsci.2017.07.009 CrossRefGoogle Scholar
  29. Saito GY, Chang YC, Walling LL, Thomson WW (1990) Chloroplast development and nuclear gene expression in cotyledons of soybean seedlings. New Phytol 114(4):547–554CrossRefGoogle Scholar
  30. Schopfer P, Plachy C, Frahry G (2001) Production of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin, and abscisic acid. Plant Physiol 125:1591–1602.  https://doi.org/10.1104/pp.125.4.1591 CrossRefGoogle Scholar
  31. Toyooka K, Okamoto T, Minamikawa T (2001) Cotyledon cells of Vigna mungo seedlings use at least two distinct autophagic machineries for degradation of starch granules and cellular components. J Cell Biol 154(5):973–982.  https://doi.org/10.1083/jcb.200105096 CrossRefGoogle Scholar
  32. Van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141:384–390.  https://doi.org/10.1104/pp.106.078295 CrossRefGoogle Scholar
  33. Waszczak C, Melanie C, Kangasjärvi J (2018) Reactive oxygen species in plant signaling. Annu Rev Plant Biol 69: 5.1–5.28  https://doi.org/10.1146/annurev-arplant-042817-040322 CrossRefGoogle Scholar
  34. Yamauchi N, Funamoto Y, Shigyo M (2004) Peroxidase-mediated chlorophyll degradation in horticultural crops. Phytochem Rev 3:221–228.  https://doi.org/10.1023/B:PHYT.0000047796.98784.06 CrossRefGoogle Scholar
  35. Zhong S, Zhao M, Shi T, Shi H, An F, Zhao Q, Guo H (2009) EIN3/EIL1 cooperate with PIF1 to prevent photo-oxidation and to promote greening of Arabidopsis seedlings. Proc Natl Acad Sci USA 106(50):21431–21436.  https://doi.org/10.1073/pnas.0907670106 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Plant Physiology and Biochemistry Laboratory, Department of BotanyVisva-Bharati UniversitySantiniketanIndia

Personalised recommendations