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Role of hydrogen peroxide in stress-induced programmed cell death during somatic embryogenesis in Fraxinus mandshurica

  • Ling Yang
  • Cheng Wei
  • Chao Huang
  • Hongnan Liu
  • Dongyan Zhang
  • Hailong ShenEmail author
  • Yuhua Li
Original Paper
  • 21 Downloads

Abstract

We examined how reactive oxygen species, in the form of hydrogen peroxide (H2O2), affect osmotic stress–induced programmed cell death during somatic embryogenesis from cotyledon explants of Manchurian ash (Fraxinus mandshurica Rupr.). We found that substantial osmotic stress was essential for Manchurian ash somatic cells to obtain embryogenic competence. The explant cells displayed hallmarks of programmed cell death, chromatin condensation, and DNA fragmentation to oligonucleotides during somatic embryogenesis. Increasing concentrations of plant growth regulators and sucrose in the medium increased osmotic stress thereby inducing H2O2 accumulation in the explant cells. We found that H2O2 concentration was significantly decreased in explant cells when the induction medium was modified, i.e., when reducing the concentration of sucrose, which reduces the osmotic pressure of the medium, or by withdrawing plant growth regulators at mid-culture. These treatments also decreased the proportion of explant cells undergoing programmed cell death. Accordingly, a decreased rate of somatic embryo induction was observed. These results show that PCD occurred during tissue browning and death of some explant cells during somatic embryogenesis in F. mandshurica. The ROS contributed to PCD in abiotic stress stimulated F. mandshurica cells.

Keywords

Manchurian ash Somatic embryos Programmed cell death Reactive oxygen species Osmotic stress 

Notes

Acknowledgements

We are very grateful for our laboratory colleagues for constructive discussions and technical support.

Author’s contributions

Y. L and S. HL conceived and designed the study. Y. L and H. C collected plant materials and prepared SE samples for analysis osmotic stress-induced PCD and intracellular H2O2 concentration. W. C and L. HN analyzed the results for experiments on osmotic stress-induced PCD and intracellular H2O2 concentration. Y. L and Z. DY contributed to the writing of the manuscript and data analyses. L. YH revised the manuscript. All authors read and approved the final manuscript.

References

  1. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399CrossRefGoogle Scholar
  2. Balestrazzia A, Agonia V, Tavab A, Avatoc P, Biazzib E, Raimondia E, Macoveia A, Carbonera D (2011) Cell death induction and nitric oxide biosynthesis in white poplar (Populus alba) suspension cultures exposed to alfalfa saponins. Physiol Plant 141:227–238CrossRefGoogle Scholar
  3. Bozhkov PV, Filonova LH, von Arnold S (2002) A key developmental switch during Norway spruce somatic embryogenesis is induced by withdrawal of growth regulators and is associated with cell death and extracellular acidification. Biotechnol Bioeng 77:658–667CrossRefGoogle Scholar
  4. Bozhkov PV, Filonova LH, Suarez MF (2005) Programmed cell death in plant embryogenesis. Curr Top Dev Biol 67:135–179CrossRefGoogle Scholar
  5. Businge E, Brackmann K, Moritz T, Egertsdotter U (2012) Metabolite profiling reveals clear metabolic changes during somatic embryo development of Norway spruce (Picea abies). Tree Physiol 32:232–244.  https://doi.org/10.1093/treephys/tpr142 CrossRefGoogle Scholar
  6. Dan YH, Zhang S, Zhong H, Yi H, Sainz MB (2015) Novel compounds that enhance Agrobacterium-mediated plant transformation by mitigating oxidative stress. Plant Cell Rep 34:291–309CrossRefGoogle Scholar
  7. de Pinto MC, Tommasi F, Gara LD (2002) Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco Bright-Yellow 2 cells. Plant Physiol 130:698–708.  https://doi.org/10.1007/s11240-013-0345-8 CrossRefGoogle Scholar
  8. Fortes AM, Costa J, Santos F, Seguı´-Simarro JM, Palme K, Altabell T, Tiburcio AF, Pais S (2011) Arginine decarboxylase expression, polyamines biosynthesis and reactive oxigen species during organogenic nodule formation in hop. Plant Signal Behav 6:258–269CrossRefGoogle Scholar
  9. Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–1101CrossRefGoogle Scholar
  10. Greenberg JT (1996) Programmed cell death: a way of life for plants. PNAS 93:12094–12097CrossRefGoogle Scholar
  11. Groß F, Durner J, Gaupels F (2013) Nitric oxide, antioxidants and prooxidants in plant defence responses. Front Plant Sci 4:419.  https://doi.org/10.3389/fpls.2013.00419 CrossRefGoogle Scholar
  12. Helmersson A, ArnoldSV BurgK, Bozhkov PV (2004) High stability of nuclear microsatellite loci during the early stages of somatic embryogenesis in Norway spruce. Tree Physiol 24:1181–1186CrossRefGoogle Scholar
  13. Hill RD, Huang S, Stasolla C (2013) Hemoglobins, programmed cell death and somatic embryogenesis. Plant Sci 211:35–41CrossRefGoogle Scholar
  14. Hu LJ, Uchiyama K, Shen HL, Ide Y (2010) Multiple-scaled spatial genetic structures of Fraxinus mandshurica over a riparian–mountain landscape in Northeast China. Conserv Genet 11:77–87.  https://doi.org/10.1007/s10592-009-0004-0 CrossRefGoogle Scholar
  15. Kaewubon P, Hutadilok-Towatana N, Teixeira da Silva JA, Meesawat U (2015) Ultrastructural and biochemical alterations during browning of pigeon orchid (Dendrobium crumenatum Swartz) callus. Plant Cell, Tissue Organ Cult 121:53–69CrossRefGoogle Scholar
  16. Kong DM, Preece JE, Shen HL (2012a) Somatic embryogenesis in immature cotyledons of Manchurian ash (Fraxinus mandshurica Rupr.). Plant Cell, Tissue Organ Cult 108:485–492.  https://doi.org/10.1007/s11240-011-0062-0 CrossRefGoogle Scholar
  17. Kong DM, Shen HL, Li N (2012b) Influence of AgNO3 on somatic embryo induction and development in Manchurian ash (Fraxinus mandshurica Rupr). Afr J Biotechnol 11(1):120–125.  https://doi.org/10.5897/AJB11.3061 Google Scholar
  18. Kwak JM, Nguyen V, Schroeder JI (2006) The role of reactive oxygen species in hormonal responses. Plant Physiol 141:323–329.  https://doi.org/10.1104/pp.106.079004 CrossRefGoogle Scholar
  19. Laloi C, Apel K, Danon A (2004) Reactive oxygen signalling: the latest news. Curr Opin Plant Biol 7:323–328CrossRefGoogle Scholar
  20. Lara-Chave A, Flinn BS, Egertsdotter U (2011) Initiation of somatic embryogenesis from immature zygotic embryos of Oocarpa pine (Pinus oocarpa Schiede ex Schlectendal). Tree Physiol 31:539–554.  https://doi.org/10.1093/treephys/tpr040 CrossRefGoogle Scholar
  21. Lee CY, Whitaker RJ (1995) Enzymatic browning and its prevention. American Chemical Society, Washington, p 338CrossRefGoogle Scholar
  22. Leonardo J, Andre LWDS, Caroline AB, Heloisa RB, Eny ISF (2014) 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.  https://doi.org/10.1093/treephys/tpt102 CrossRefGoogle Scholar
  23. Liu CP, Yang L, Shen HL (2015) Proteomic analysis of immature Fraxinus mandshurica cotyledon tissues during somatic embryogenesis: effects of explant browning on somatic embryogenesis. Int J Mol Sci 16:13692–13713.  https://doi.org/10.3390/ijms160613692 CrossRefGoogle Scholar
  24. Maraschin SDF, Gaussand G, Pulido A, Olmedilla A, Lamers GEM, Korthout H, Spaink HP, Wang M (2005) Programmed cell death during the transition from multicellular structures to globular embryos in barley androgenesis. Planta 221:459–470CrossRefGoogle Scholar
  25. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410CrossRefGoogle Scholar
  26. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498CrossRefGoogle Scholar
  27. Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van BF (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309.  https://doi.org/10.1016/j.tplants.2011.03.007 CrossRefGoogle Scholar
  28. Naik SK, Chand PK (2011) Tissue culture-mediated biotechnological intervention in pomegranate: a review. Plant Cell Rep 30:707–721.  https://doi.org/10.1007/s00299-010-0969-7 CrossRefGoogle Scholar
  29. Nowak K, Gaj MD (2016) Stress-related function of bHLH109 in somatic embryo induction in Arabidopsis. J Plant Physiol 193:119–126CrossRefGoogle Scholar
  30. Petrov V, Hille J, Mueller-Roeber B, Gechev TS (2015) ROS-mediated abiotic stress-induced programmed cell death in plants. Front Plant Sci 18:69.  https://doi.org/10.3389/fpls.2015.00069 Google Scholar
  31. Petrussa E, Bertolini A, Casolo V, Krajnáková J, Macrì F, Vianello A (2009) Mitochondrial bioenergetics linked to the manifestation of programmed cell death during somatic embryogenesis of Abies alba. Planta 231:93–107.  https://doi.org/10.1007/s00425-009-1028-x CrossRefGoogle Scholar
  32. Pirttilä A, Podolich O, Koskimäki JJ, Esa H, Hohtola A (2008) Role of origin and endophyte infection in browning of bud-derived tissue cultures of Scots pine (Pinus sylvestris L.). Plant Cell, Tissue Organ Cult 95:47–55.  https://doi.org/10.1007/s11240-008-9413-x CrossRefGoogle Scholar
  33. Rani D, Dantu PK (2014) Sustained shoot multiplication and method for overcoming in vitro browning in medicinally important plant, Piper chaba hunt. Proc Natl Acad Sci India Sect B Biol Sci 86:407–413.  https://doi.org/10.1007/s40011-014-0461-1 CrossRefGoogle Scholar
  34. Sun J, Zhang CL, Zhang X, Deng SR, Zhao R, Shen X, Chen SL (2012) Extracellular ATP signaling and homeostasis in plant cells. Plant Signal Behav 7:566–569.  https://doi.org/10.4161/psb.19857 CrossRefGoogle Scholar
  35. Tang QY, Feng GM (2002) Practical statistical analysis and DPS data handling system. Science Publishing, BeijingGoogle Scholar
  36. van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J, Mur LA, Petersen M, Smertenko A, Taliansky M, Van Breusegem F, Wolpert T, Woltering E, Zhivotovsky B, Bozhkov PV (2011) Morphological classification of plant cell deaths. Cell Death Differ 18:1241–1246.  https://doi.org/10.1038/cdd.2011.36 CrossRefGoogle Scholar
  37. von Arnold S, Bozhkov P, Clapham D, Dyachok J, Filonova L, Högberg KA, Ingouff M, Wiweger M (2005) Propagation of Norway spruce via somatic embryogenesis. Plant Cell, Tissue Organ Cult 81:323–329CrossRefGoogle Scholar
  38. Wang Y, Loake GJ, Chu CC (2013) Cross-talk of nitric oxide and reactive oxygen species in plant programed cell death. Front Plant Sci 4:314.  https://doi.org/10.3389/fpls.2013.00314 Google Scholar
  39. Wu JH, Zhang XL, Nie YC (2003) Programmed cell death during somatic proliferation and embryogenesis of cotton (Gossypium hirsutum L.). J Plant Physiol Mol Biol 29:515–520Google Scholar
  40. Yang L, Bian L, Shen HL, Li YH (2013) Somatic embryogenesis and plantlet regeneration from mature zygotic embryos of Manchurian ash (Fraxinus mandshurica Rupr.). Plant Cell, Tissue Organ Cult 115:115–125.  https://doi.org/10.1007/s11240-013-0345-8 CrossRefGoogle Scholar
  41. Zimmerman JL (1993) Somatic embryogenesis: a model for early development in higher plants. Plant Cell 5:1411–1423.  https://doi.org/10.1105/tpc.5.10.1411 CrossRefGoogle Scholar

Copyright information

© Northeast Forestry University 2019

Authors and Affiliations

  • Ling Yang
    • 1
  • Cheng Wei
    • 1
  • Chao Huang
    • 1
  • Hongnan Liu
    • 1
  • Dongyan Zhang
    • 1
  • Hailong Shen
    • 1
    Email author
  • Yuhua Li
    • 1
  1. 1.State Key Laboratory of Tree Genetics and Breeding, School of ForestryNortheast Forestry UniversityHarbinPeople’s Republic of China

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