Plant Somatic Embryogenesis: Modulatory Role of Oxidative Stress

Abstract

Plant somatic embryogenesis (PSE) provides several advantages when compared to other in vitro propagation methods of tissue culture. All factors affecting PSE are not known. Some prominent stress factors in tissue culture are serious injuries in explants, subcultures, unbalanced mineral composition of the culture medium and growth regulators, etc. The present review would focus on induction Reactive Oxygen Species (ROS), which lies fairly downstream of the cascade of various stress processes outlined above. The central question the present authors ask is—whether ROS generation is all for toxic or there is some amount of benefit to the somatic embryogenesis. The increasing interest in the functional meaning of ROS and the antioxidant response concomitant to growth, development and cell differentiation in plants suggest a link between ROS production and morphogenetic processes of plants. The authors in this review article consider hydrogen peroxide (H2O2) as a model ROS which is omnipresent and naturally generated in a variety of normal cell types, either constitutively or in response to various stimuli. A review of the concerned literature suggests that endogenous H2O2 acts as a cellular ‘messenger’ capable of inducing gene expression and protein synthesis, thus leading to somatic embryogenesis in some plant species.

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References

  1. 1.

    Grzybkowska D, Morończyk J, Wójcikowska B, Gaj MD (2018) Azacitidine (5-AzaC)-treatment and mutations in DNA methylase genes affect embryogenic response and expression of the genes that are involved in somatic embryogenesis in Arabidopsis. Plant Growth Regul 85:243–256

    CAS  Article  Google Scholar 

  2. 2.

    Prudente DO, Paiva R, Carpentier S, Swennen R, Nery FC, Silva LC, Panis B (2017) Characterization of the formation of somatic embryos from mature zygotic embryos of Passiflora ligularis Juss. Plant Cell Tissue Organ Cult 131:97–105

    Article  Google Scholar 

  3. 3.

    Garcia C, Marelli J-P, Motamayor JC, Villela C (2018) Somatic embryogenesis in Theobroma cacao L. In: Loyola-Vargas V, Ochoa-Alejo N (eds) Plant cell culture protocols. Springer, Berlin, pp 227–245

    Google Scholar 

  4. 4.

    Al-Khayri JM, Naik PM (2017) Date palm micropropagation: advances and applications. Ciênc Agrotecnol 41:347–358

    CAS  Article  Google Scholar 

  5. 5.

    Elhiti M, Stasolla C (2015) ROS signalling in plant embryogenesis. In: Gupta KJ, Igamberdiev AU (eds) Reactive oxygen and nitrogen species signaling and communication in plants. Springer International Publishing, Berlin, pp 197–214

    Google Scholar 

  6. 6.

    Baskaran P, Van Staden J (2014) Plant regeneration via somatic embryogenesis in Drimia robusta. Plant Cell Tissue Organ Cult 119:281–288

    CAS  Article  Google Scholar 

  7. 7.

    Pérez-Pérez Y et al (2019) Pectin De-methylesterification and AGP increase promote cell wall remodeling and are required during somatic embryogenesis of Quercus suber. Front Plant Sci 9:1915–1915

    Article  Google Scholar 

  8. 8.

    Pullman GS, Bucalo K (2014) Pine somatic embryogenesis: analyses of seed tissue and medium to improve protocol development. New For 45:353–377

    Article  Google Scholar 

  9. 9.

    Maruyama TE, Hosoi Y (2019) Progress in somatic embryogenesis of Japanese pines. Front Plant Sci 10:31. https://doi.org/10.3389/fpls.2019.00031

    Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Jo L, Santos AL, Bueno CA, Barbosa HR, Floh EI (2013) Proteomic analysis and polyamines, ethylene and reactive oxygen species levels of Araucaria angustifolia (Brazilian pine) embryogenic cultures with different embryogenic potential. Tree Physiol 34:94–104

    Article  Google Scholar 

  11. 11.

    Steiner N, Santa-Catarina C, Silveira V, Floh EI, Guerra MP (2007) Polyamine effects on growth and endogenous hormones levels in Araucaria angustifolia embryogenic cultures. Plant Cell Tissue Organ Cult 89:55–62

    CAS  Article  Google Scholar 

  12. 12.

    Lin J, Wang Y, Wang G (2006) Salt stress-induced programmed cell death in tobacco protoplasts is mediated by reactive oxygen species and mitochondrial permeability transition pore status. J Plant Physiol 163:731–739

    CAS  Article  Google Scholar 

  13. 13.

    Zayova E, Geneva M, Stancheva I, Dimitrova L, Petrova M, Hristozkova M, Salamon I (2018) Evaluation of the antioxidant potential of in vitro propagated hyssop (Hyssopus officinalis L.) with different plant growth regulators. Med Plants-Int J Phytomed Relat Ind 10:295–304

    Article  Google Scholar 

  14. 14.

    Sun J, Wang MJ, Ding MQ, Deng SR, Liu MQ, Lu CF, Zhou XY, Shen X, Zheng XJ, Zhang ZK, Song J (2010) H2O2 and cytosolic Ca2+ signals triggered by the PM H+-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells. Plant Cell Environ 33:943–958

    CAS  Article  Google Scholar 

  15. 15.

    Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132

    CAS  Article  Google Scholar 

  16. 16.

    Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    CAS  Article  Google Scholar 

  17. 17.

    Miller G, Coutu J, Shulaev V, Mittler R (2018) Reactive oxygen signaling in plants. Annu Plant Rev Online 33:189–201

    Article  Google Scholar 

  18. 18.

    Riaz M et al (2018) Boron alleviates the aluminum toxicity in trifoliate orange by regulating antioxidant defense system and reducing root cell injury. J Environ Manag 208:149–158

    CAS  Article  Google Scholar 

  19. 19.

    Martin F et al (2018) Overexpression of EcGSH1 induces glutathione production and alters somatic embryogenesis and plant development in Hevea brasiliensis. Ind Crops Prod 112:803–814

    CAS  Article  Google Scholar 

  20. 20.

    Waszczak C, Carmody M, Kangasjärvi J (2018) Reactive oxygen species in plant signaling. Annu Rev Plant Biol 69:209–236

    CAS  Article  Google Scholar 

  21. 21.

    Fehér A, Pasternak TP, Dudits D (2003) Transition of somatic plant cells to an embryogenic state. Plant Cell Tissue Organ Cult 74:201–228

    Article  Google Scholar 

  22. 22.

    Pasternak T, Potters G, Caubergs R, Jansen MA (2005) Complementary interactions between oxidative stress and auxins control plant growth responses at plant, organ, and cellular level. J Exp Bot 56:1991–2001

    CAS  Article  Google Scholar 

  23. 23.

    Imin N, Nizamidin M, Daniher D, Nolan KE, Rose RJ, Rolfe BG (2005) Proteomic analysis of somatic embryogenesis in Medicago truncatula. Plant Physiol 137:1250–1260

    CAS  Article  Google Scholar 

  24. 24.

    Blazquez S, Olmos E, Hernández JA, Fernández-García N, Fernández JA, Piqueras A (2009) Somatic embryogenesis in saffron (Crocus sativus L.) histological differentiation and implication of some components of the antioxidant enzymatic system. Plant Cell Tissue Organ Cult 97:49–57

    CAS  Article  Google Scholar 

  25. 25.

    Pasternak TP, Prinsen E, Ayaydin F, Miskolczi P, Potters G, Asard H, Van Onckelen HA, Dudits D, Fehér A (2002) The role of auxin, Ph, and stress in the activation of embryogenic cell division in leaf protoplast-derived cells of alfalfa. Plant Physiol 129:1807–1819

    CAS  Article  Google Scholar 

  26. 26.

    Correa-Aragunde N, Graziano M, Chevalier C, Lamattina L (2006) Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. J Exp Bot 57:581–588

    CAS  Article  Google Scholar 

  27. 27.

    Gallego P, Martin L, Blazquez A, Guerra H, Villalobos N (2014) Involvement of peroxidase activity in developing somatic embryos of Medicago arborea L. identification of an isozyme peroxidase as biochemical marker of somatic embryogenesis. J Plant Physiol 171:78–84

    CAS  Article  Google Scholar 

  28. 28.

    Zhang W, Wang XM, Rong FAN, Yin GX, Ke WA, Du LP, Xiao LL, Ye XG (2015) Effects of inter-culture, arabinogalactan proteins, and hydrogen peroxide on the plant regeneration of wheat immature embryos. J Integr Agric 14:11–19

    Article  Google Scholar 

  29. 29.

    Kairong C, Ji L, Gengmei X, Jianlong L, Lihong W, Yafu W (2002) Effect of hydrogen peroxide on synthesis of proteins during somatic embryogenesis in Lycium barbarum. Plant Cell Tissue Organ Cult 68:187–193

    Article  Google Scholar 

  30. 30.

    Vranova E, Inzé D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236

    CAS  Article  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; Brasília, DF—Brazil), Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG; Belo Horizonte, MG—Brazil) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES; Brasília, DF—Brazil) for financial support.

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Correspondence to Débora de Oliveira Prudente.

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Significance Statement

The cellular oxidative stress caused by Reactive Oxygen Species (ROS) can act as a sign on the growth, development and cell differentiation in plants. Thus, some ROS such as hydrogen peroxide (H2O2) in suitable concentrations can act by activating specific morphogenic pathways to promote the induction of embryogenic cells.

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Prudente, D.O., de Souza, L. & Paiva, R. Plant Somatic Embryogenesis: Modulatory Role of Oxidative Stress. Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci. 90, 483–487 (2020). https://doi.org/10.1007/s40011-019-01136-3

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Keywords

  • Plant somatic embryogenesis
  • H2O2
  • ROS
  • Reactive oxygen species