Skip to main content
Log in

Analysis of programmed cell death in wheat endosperm reveals differences in endosperm development between cereals

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Although maize endosperm undergoes programmed cell death during its development, it is not known whether this developmental feature is common to cereals or whether it arose inadvertently from the selection process that resulted in the enlarged endosperm of modern maize. Examination of wheat endosperm during its development revealed that this tissue undergoes a programmed cell death that shares features with the maize program but differs in some aspects of its execution. Cell death initiated and progressed stochastically in wheat endosperm in contrast to maize where cell death initiates within the upper central endosperm and expands outward. After a peak of ethylene production during early development, wheat endosperm DNA underwent internucleosomal fragmentation that was detectable from mid to late development. The developmental onset and progression of DNA degradation was regulated by the level of ethylene production and perception. These observations suggest that programmed cell death of the endosperm and regulation of this program by ethylene is not unique to maize but that differences in the execution of the program appear to exist among cereals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Aoyagi S, Sugiyama M, Fukuda H: BEN1 and ZEN1 cDNAs encoding S1-type DNases that are associated with programmed cell death. FEBS Lett 429: 134–138 (1998).

    PubMed  Google Scholar 

  2. Bachmair A, Becker F, Masterson RV, Schell J: Perturbation of the ubiquitin system causes leaf curling, vascular tissue alterations and necrotic lesions in a higher plant. EMBO J 9: 4543–4549 (1990).

    PubMed  Google Scholar 

  3. Bell PR: Megaspore abortion: a consequence of selective apoptosis. Int J Plant Sci 157: 1–7 (1996).

    Google Scholar 

  4. Beltrano J, Carbone A, Montaldi ER, Guiamet JJ: Ethylene as promoter of wheat grain maturation and ear senescence. Plant Growth Reg 15: 107–112 (1994).

    Article  Google Scholar 

  5. Bradbury D, Cull IM, MacMasters MM: Structure of the mature wheat kernel. I. Gross anatomy and relationships of parts. Cereal Chem 33: 329–342 (1956).

    Google Scholar 

  6. Bradbury D, MacMasters MM, Cull IM: Structure of the mature wheat kernel. II. Microscopic structure of pericarp, seed coat, and other coverings of the endosperm and germ of hard red winter wheat. Cereal Chem 33: 342–360 (1956).

    Google Scholar 

  7. Bradbury D, MacMasters MM, Cull IM: Structure of the mature wheat kernel. III. Microscopic structure of the endosperm of hard red winter wheat. Cereal Chem 33: 361–373 (1956).

    Google Scholar 

  8. Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248–254 (1976).

    Article  PubMed  Google Scholar 

  9. Campbell R, Drew MC: Electron microscopy of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to oxygen shortage. Planta 157: 350–357 (1983).

    Google Scholar 

  10. Chasan R: Tracing tracheary element development. Plant Cell 6: 917–919 (1994).

    Google Scholar 

  11. Chang S-C, Gallie DR: RNase activity decreases following a heat shock in wheat leaves and correlates with its posttranslational modification. Plant Physiol 113: 1253–1263 (1997).

    PubMed  Google Scholar 

  12. Dellaporta SL, Calderon-Urrea A: The sex determination process in maize. Science 266: 1501–1505 (1994).

    PubMed  Google Scholar 

  13. DeLong A, Calderon-Urrea A, Dellaporta SL: Sex determination gene tasselseed2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 74: 757–768 (1993).

    PubMed  Google Scholar 

  14. Dietrich RA, Delaney TP, Uknes SJ, Ward ER, Ryals JA, Dangl JL: Arabidopsis mutants simulating disease resistance response. Cell 77: 565–577 (1994).

    PubMed  Google Scholar 

  15. Drew MC, J ackson MB, Giffard S: Ethylene-promoted adventitious rooting and development of cortical air spaces (aerenchyma) in roots may be adaptive response to flooding in Zea mays L. Planta 147: 83–88 (1979).

    Google Scholar 

  16. Esau K: Seed Plant Anatomy. Academic Press, New York (1977).

    Google Scholar 

  17. Goldberg RB, Beals TP, Sanders PM: Anther development: basic principles and practical applications. Plant Cell 5: 1217–1228 (1993).

    PubMed  Google Scholar 

  18. Greenberg JT, Ausubel FM: Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging. Plant J 4: 327–341 (1993).

    PubMed  Google Scholar 

  19. Greenberg JT, Guo A, Klessig DF, Ausubel FM: Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77: 551–563 (1994).

    Article  PubMed  Google Scholar 

  20. He C-J, Morgan PW, Drew MC: Transduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia. Plant Physiol 112: 463–472 (1996).

    PubMed  Google Scholar 

  21. Kaplan DR: In: White RA, Dickenson WC (eds) Contemporary Problems in Plant Anatomy, pp. 261–300. Academic Press, New York (1984).

    Google Scholar 

  22. Kerr JFR, Gobe GC, Winterford CM, Harmon BV: Anatomical methods in cell death. Meth Cell Biol 46: 1–27 (1995).

    Google Scholar 

  23. Lamb CJ: Plant disease resistance genes in signal perception and transduction. Cell 76: 419–422 (1994).

    Article  PubMed  Google Scholar 

  24. Mittler R, Lam E: Characterization of nuclease activities and DNAfragmentation induced upon hypersensitive response cell death and mechanical stress. Plant Mol Biol 34: 209–221 (1997).

    Google Scholar 

  25. Mittler R, Lam E: Identification, characterization, and purification of a tobacco endonuclease activity induced upon hypersensitive response cell death. Plant Cell 7: 1951–1962 (1995).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  27. O'Neill SD, Nadeau JA, Zhang XS, Bui AQ, Halevy AH: Interorgan regulation of ethylene biosynthesis genes by pollination. Plant Cell 5: 419–432 (1993).

    Article  PubMed  Google Scholar 

  28. Orzaez D, Granell A: DNA fragmentation is regulated by ethylene during carpel senescence in Pisum sativum. Plant J 11: 137–144 (1997).

    Google Scholar 

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

    PubMed  Google Scholar 

  30. Serek M, Sisler EC, Reid MS: Effect of 1-MCP on the vase life and ethylene response on cut flowers. Plant Growth Reg 16: 93–97 (1995).

    Google Scholar 

  31. Serek M, Sisler EC, Reid MS: Novel gaseous ethylene binding inhibitor prevents ethylene effects in potted flowering plants. J Am Soc Hort Sci 119: 1230–1233 (1994).

    Google Scholar 

  32. Sisler EC, Dupille E, Serek M: Effect of 1-methylcyclopropene and-methylenecyclopropane on ethylene binding and ethylene action on cut carnations. Plant Growth Reg 18: 79–86 (1996).

    Google Scholar 

  33. Thelen MP, Northcote DH: Identification and purification of a nuclease from Zinnia elegans L.: a potential molecular marker for xylogenesis. Planta 179: 181–195 (1989).

    Google Scholar 

  34. Wang H, Bostock RM, Gilchrist DG: Apoptosis: a functional paradigm for programmed cell death induced by a hostselective phytotoxin and invoked during development. Plant Cell 8: 375–391 (1996).

    PubMed  Google Scholar 

  35. Wang M, Oppedijk BJ, Lu X, van Duijn B, Schilperoort RA: Apoptosis in barley aleurone during germination and its inhibition by abscisic acid. Plant Mol Biol 32: 1125–1134 (1996).

    PubMed  Google Scholar 

  36. Young TE, Gallie DR, DeMason DA: Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken2 genotypes. Plant Physiol 115: 737–747 (1997).

    PubMed  Google Scholar 

  37. Zhang XS, O'Neil SD: Ovary and gametophyte development are coordinately regulated by auxin and ethylene following pollination. Plant Cell 5: 403–418 (1993).

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Young, T.E., Gallie, D.R. Analysis of programmed cell death in wheat endosperm reveals differences in endosperm development between cereals. Plant Mol Biol 39, 915–926 (1999). https://doi.org/10.1023/A:1006134027834

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006134027834

Navigation