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Apoptosis in barley aleurone during germination and its inhibition by abscisic acid

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Abstract

During germination of barley grains, DNA fragmentation was observed in the aleurone. The appearance of DNA fragmentation in the aleurone layer, observed by TUNEL staining in aleurone sections, started near the embryo and extended to the aleurone cells far from the embryo in a time dependent manner. The same spatial temporal activities of hydrolytic enzymes such as α-amylase were observed in aleurone. DNA fragmentation could also be seen in vitro under osmotic stress, in isolated aleurone. During aleurone protoplast isolation, a very enhanced and strong DNA fragmentation occurred which was not seen in protoplast preparations of tobacco leaves. ABA was found to inhibit DNA fragmentation occurring in barley aleurone under osmotic stress condition and during protoplast isolation, while the plant growth regulator gibberellic acid counteracted the effect of ABA. Addition of auxin or cytokinin had no significant effect on DNA fragmentation in these cells. To study the role of phosphorylation in ABA signal transduction leading to control of DNA fragmentation (apoptosis), the effects of the phosphatase inhibitor okadaic acid and of phenylarisine oxide on apoptosis were studied. We hypothesize that the regulation of DNA fragmentation in aleurone plays a very important role in spatial and temporal control of aleurone activities during germination. The possible signal transduction pathway of ABA leading to the regulation of DNA fragmentation is discussed.

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References

  1. Briggs DE: Endosperm breakdown and its regulation in germinating barley. In: S. Schweigert (ed.) Food Science and Technology. Academic Press, London pp. 441–532 (1987).

    Google Scholar 

  2. Bush DS, Biswas AK, Jones RL: Gibberellic acid-stimulated Ca2+ accumulation in endoplasmic reticulum of barley aleurone Ca2+ transport and steady-state levels. Planta 178: 411–420 (1989).

    Google Scholar 

  3. Deikman J, Jones RL: Control of α-amylase mRNA accumulation by gibberellic acid and calcium in barley aleurone layers. Plant Physiol 78: 192–198 (1985).

    Google Scholar 

  4. Fraser A, Evan G: A license to kill. Cell 85: 781–784 (1996).

    Google Scholar 

  5. Gavrieli Y, Sherman Y, Ben-Sasson SA: Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119(3): 493–501 (1992).

    Google Scholar 

  6. Gilroy S, Jones RL: Gibberellic acid and abscisic acid coordinately regulate cytoplasmic calcium and secretory activity in barley aleurone protoplasts. Proc Natl Acad Sci (USA) 89: 3591–3595 (1992).

    Google Scholar 

  7. Havel L, Durzan DJ: Apoptosis during diploid parthenogenesis and early somatic embryogenesis of norway spruce. Int J Plant Sci 157(1): 8–16 (1996).

    Google Scholar 

  8. Heimovaara-Dijkstra S, Heistek JC, Wang M: Counteractive effects of ABA and GA3 on extracellular and intracellular pH and malate in barley aleurone. Plant Physiol 106: 359–365 (1994).

    Google Scholar 

  9. Heimovaara-Dijkstra S, Nieland TJF, van der Meulen RM, Wang M: Abscisic acid-induced gene expression requires the activity of protein(s) sensitive to the protein-tyrosine phosphatase inhibitor phenylarsine oxide. Plant Growth Regul 18: 115–123 (1996).

    Google Scholar 

  10. Jacobsen JV, Beach LR: Control of transcription of α-amylase and r-RNA genes in barley aleurone protoplasts by gibberellin and abscisic acid. Nature 316: 275–277 (1985).

    Google Scholar 

  11. Jacobsen JV, Chandler PM: Gibberellin and abscisic acid in germinating cereals. In: P.J. Davies (ed.) Plant Hormones. Kluwer Academic Publishers, Dordrecht, pp. 164–193 (1987).

    Google Scholar 

  12. Knetsch MLW, Wang W, Snaar-Jagalska BE, Heimovaara-Dijkstra S: Abscisic acid induces mitogen-activated protein kinase activation in barley aleurone protoplasts. The Plant Cell 8: 1061–1067 (1996).

    Google Scholar 

  13. Kuo A, Cappelluti S, Cervantes-Cervantes M, Rodriguez M, Bush DS: Okadaic acid, a protein phosphatase inhibitor, blocks calcium changes, gene expression, and cell death induced by gibberellin in wheat aleurone cells. The Plant Cell 8: 259–269 (1996).

    Google Scholar 

  14. McConkey DJ, Orrenius S: The role of calcium in the regulation of apoptosis. J Leukocyte Biol 59(6): 775–783 (1996).

    Google Scholar 

  15. Mittler R, Shulaev V, Lam E: Coordinated activation of programmed cell death and defense mechanisms in transgenic tobacco plants expressing a bacterial proton pump. The Plant Cell 7: 29–42 (1995).

    Google Scholar 

  16. Nolan RC, Ho T-HD: Hormonal regulation of α-amylase expression in barley aleurone layers. Plant Physiol 88: 588–593 (1988).

    Google Scholar 

  17. Patel T, Gores GJ, Kaufmann SH: The role of proteinases during apoptosis. FASEB J 10: 587–597 (1996).

    Google Scholar 

  18. Ryerson DE, Heath MC: Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments. The Plant Cell 8: 393–402 (1996).

    Google Scholar 

  19. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning, a Laboratory Manual, 2nd ed. Cold Spring Harbour, NY: Cold Spring Harbour Laboratory Press. 1989.

    Google Scholar 

  20. Van Beckum JMM, Libbenga KR, Wang M: Abscisic acid and gibberellic acid regulated responses of embryos and aleurone layers isolated from dormant and nondormant barley grains. Physiol Plant 89: 483–489 (1993).

    Google Scholar 

  21. Van der Veen R, Heimovaara-Dijkstra S, Wang M: Cytosolic alkalinization mediated by abscisic acid is necessary, but not sufficient, for abscisic acid-induced gene expression in barley aleurone protoplasts. Plant Physiol 100: 699–705 (1992).

    Google Scholar 

  22. Vaux DL, Strasser A: The molecular basis of apoptosis. Proc Natl Acad Sci (USA) 93: 2239–2244 (1996).

    Google Scholar 

  23. Wang M, Van Duijn B, Schram AW: Abscisic acid induces a cytosolic calcium decrease in barley aleurone protoplasts. FEBS Lett 278(1): 69–74 (1991).

    Google Scholar 

  24. Wang M, Heimovaara-Dijkstra S, Van Duijn B: Modulation of germination of embryos isolated from dormant and nondormant barley grains by manipulation of endogenous abscisic acid. Planta 195: 586–592 (1995).

    Google Scholar 

  25. Wang H, Li J, Bostock RM, Gilchrist DG: Apoptosis: A functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. The Plant Cell 8: 375–391 (1996).

    Google Scholar 

  26. White E: Life, death, and the pursuit of apoptosis. Genes and Develop 10: 1–15 (1996).

    Google Scholar 

  27. Wyllie AH: Cell death: The significance of apoptosis. Int Rev Cytol 68: 251–306 (1980).

    Google Scholar 

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Wang, M., Oppedijk, B.J., Lu, X. et al. Apoptosis in barley aleurone during germination and its inhibition by abscisic acid. Plant Mol Biol 32, 1125–1134 (1996). https://doi.org/10.1007/BF00041396

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