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Planta

, Volume 221, Issue 5, pp 607–618 | Cite as

Programmed cell death and leaf morphogenesis in Monstera obliqua (Araceae)

  • Arunika H. L. A. N. Gunawardena
  • Kathy Sault
  • Petra Donnelly
  • John S. Greenwood
  • Nancy G. Dengler
Review

Abstract

The unusual perforations in the leaf blades of Monstera obliqua (Araceae) arise through programmed cell death early in leaf development. At each perforation site, a discrete subpopulation of cells undergoes programmed cell death simultaneously, while neighboring protoderm and ground meristem cells are unaffected. Nuclei of cells within the perforation site become terminal deoxynucleotidyl transferase-mediated dUTP nick end labeling (TUNEL)-positive, indicating that DNA cleavage is an early event. Gel electrophoresis indicates that DNA cleavage is random and does not result in bands that represent multiples of internucleosomal units. Ultrastructural analysis of cells at the same stage reveals misshapen, densely stained nuclei with condensed chromatin, disrupted vacuoles, and condensed cytoplasm. Cell walls within the perforation site remain intact, although a small disk of dying tissue becomes detached from neighboring healthy tissues as the leaf expands and stretches the minute perforation. Exposed ground meristem cells at the rim of the perforation differentiate as epidermal cells. The cell biology of perforation formation in Monstera resembles that in the aquatic plant Aponogeton madagascariensis (Aponogetonaceae; Gunawardena et al. 2004), but the absence of cell wall degradation and the simultaneous execution of programmed cell death throughout the perforation site reflect the convergent evolution of this distinct mode of leaf morphogenesis in these distantly related plants.

Keywords

Leaf development Monstera Perforation formation Programmed cell death TUNEL assay Ultrastructure 

Abbreviations

PCD

Programmed cell death

TUNEL

Terminal deoxynucleotidyl transferase-mediated dUTP nick end labeling

Notes

Acknowledgements

We thank Dr Pauline Wang, Dr Keiko Yoshioka and Danielle Vidaurre for helpful advice on gel electrophoresis and Dr Ron Dengler for photography. We acknowledge funding from the Natural Sciences and Engineering Research Council of Canada for Discovery Grants to NGD and JSG and for a Postdoctoral Fellowship to AHLANG.

References

  1. Barlow PW (1982) Cell death—an integral part of plant development. In: Jackson MB, Grout B, Mackenzie IA (eds) Growth regulators in plant senescence. Monograph 8, British plant growth regulator group, Wantage, UK, pp 27–45Google Scholar
  2. Beers EP (1997) Programmed cell death during plant growth and development. Cell Death Differ 4:649–661Google Scholar
  3. Brown VK, Lawton JH (1991) Herbivory and the evolution of leaf shape and size. Philos Trans Roy Soc Lond B 333:265–272Google Scholar
  4. Calderon-Urrea A, Dellaporta S (1999) Cell death and cell protection genes determine the fate of pistils in maize. Development 126:435–441Google Scholar
  5. Cheng PC, Greyson RI, Walden DB (1983) Organ initiation and the development of unisexual flowers in the tassel and ear of Zea mays. Am J Bot 70:450–462Google Scholar
  6. Clarke PGH (1990) Developmental cell death—Morphological diversity and multiple mechanisms. Anat Embryol 181:195–213Google Scholar
  7. Dangl JL, Dietrich RA, Thomas H (2000) Cell death and senescence. In: Buchanan B, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, Maryland, pp 1044–1100Google Scholar
  8. Greenberg JT (1996) Programmed cell death: a way of life for plants. Proc Natl Acad Sci USA 93:12094–12097Google Scholar
  9. Greenwood JS, Helm M, Gietl C (2005) Ricinosomes and endosperm transfer cell structure in programmed cell death of the nucellus during Ricinus seed development. Proc Natl Acad Sci USA 102:2238–2243Google Scholar
  10. Groover A, DeWitt N, Heidel A, Jones A (1997) Programmed cell death of plant tracheary elements differentiating in vitro. Protoplasma 196:197–211Google Scholar
  11. Gunawardena AHLAN, Dengler NG (2005) Alternative modes of leaf dissection in monocotyledons. Bot J Linn Soc (in press)Google Scholar
  12. Gunawardena AHLAN, Pearce DM, Jackson MB, Hawes CR, Evans DE (2001a) Characterization of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.) Planta 212:205–214Google Scholar
  13. Gunawardena AHLAN, Pearce DM, Jackson MB, Hawes CR, Evans DE (2001b) Rapid changes in cell wall pectic polysaccharides are closely associated with early stages of aerenchyma formation, a spatially localized form of programmed cell death in roots of maize promoted by ethylene. Plant Cell Environ 24:1369–1375Google Scholar
  14. Gunawardena AHLAN, Greenwood JS, Dengler NG (2004) Programmed cell death remodels lace plant leaf shape during leaf development. Plant Cell 16:60–73Google Scholar
  15. Hoeberichts FA, Woltering EJ (2002) Multiple mediators of plant programmed cell death: interplay of conserved cell death mechanisms and plant-specific regulators. Bioessays 25:47–57Google Scholar
  16. Hoffman A, Gross G (2001) BMP signaling pathways in cartilage and bone formation. Crit Rev Eukaryot Gene Expr 11:23–45Google Scholar
  17. Huelskamp M, Schnittger A (2004) Programmed cell death in development of plant vegetative tissue (leaf and root). In: Gray J (ed) Programmed cell death in plants. Blackwell Publishing, Oxford, UK, pp 106–130Google Scholar
  18. Ito J, Fukuda H (2002) ZEN1 is a key enzyme in the degradation of nuclear DNA during programmed cell death of tracheary elements. Plant Cell 14:3201–3211Google Scholar
  19. Jones AM (2001) Programmed cell death in development and defense. Plant Physiol 125:94–97Google Scholar
  20. Jones AM, Dangl JL (1996) Logjam at the Styx: Programmed cell death in plants. Trends Plant Sci 1:114–119Google Scholar
  21. Kaplan DR (1984) Alternative modes of organogenesis in higher plants. In: White RA, Dickison WC (eds) Contemporary problems in plant anatomy. Academic, New York, USA, pp 261–300Google Scholar
  22. Lockshin RA (2004) When cells die. II. A comprehensive evaluation of apoptosis and programmed cell death. Wiley, LondonGoogle Scholar
  23. Madison M (1977) A revision of Monstera (Araceae). Contrib Gray Herb 207:3–100Google Scholar
  24. Mayo SJ, Bogner J, Boyce PC (1997) The genera of Araceae. Royal Botanical Gardens, Kew, UKGoogle Scholar
  25. Mayo SJ, Bogner J, Boyce PC (1998) Araceae. In: Kubitzki K (ed) The families and genera of vascular plants. IV. Flowering plants—Monocotyledons. Alismatanae and Commelinanae (except Gramineae). Springer Verlag, Berlin, Newyork, Heidelberg, pp 26–73Google Scholar
  26. Melville R, Wrigley FA (1969) Fenstration in the leaves of Monstera and its bearing on the morphogenesis and colour patterns of leaves. Bot J Linn Soc 62:1–16Google Scholar
  27. Merino R, Ganan Y, Macias D, Rodriguez-Leon J, Hurle JM (1999) Bone morphogenetic proteins regulate intrdigital cell death in the avian embryo. Ann NY Acad Sci 887:120–132Google Scholar
  28. Morgan PW, Drew MC (2004) Plant cell death and cell differentiation. In: Noodén LD (ed) Plant cell death processes. Elsevier, Amsterdam, pp 19–36Google Scholar
  29. Nakashima J, Takabe K, Fujita M, Fukuda H (2000) Autolysis during in vitro tracheary element differentiation: formation and location of the perforation. Plant Cell Physiol 4:1267–1271Google Scholar
  30. Nelson T, Dengler N (1997) Leaf vascular pattern formation. Plant Cell 9: 1121–1135Google Scholar
  31. Noodén LD (2004) Introduction. In: Noodén LD (ed) Plant cell death processes. Elsevier, Amsterdam, pp 1–18Google Scholar
  32. Obara K, Fukuda H (2004) Programmed cell death in xylem differentiation. In: Gray J (ed) Programmed cell death in plants. Blackwell, Oxford, pp 131–154Google Scholar
  33. Obara K, Kuriyama H, Fukuda H (2001) Direct evidence of active and rapid nuclear degradation triggered by vacuole rupture during programmed cell death in Zinnia. Plant Physiol 125:615–626Google Scholar
  34. Pennell RI, Lamb C (1997) Programmed cell death in plants. Plant Cell 9:1157–1168Google Scholar
  35. Schwartz F (1878) Ũber die Entstehung der Lõcher und Einbuchtungen an dem Blätte von Philodendron pertusum Schott. Sitzber K Akad Wiss Wien Abt 1 77:267–274Google Scholar
  36. Serguéeff M (1907) Contribution á la morphologie et la biologie des Aponogetonacèes PhD dissertation. University of Geneva, GenevaGoogle Scholar
  37. Trecul A (1854) Notes sur la formation des perforations que presenteen les feuilles de quelques Aroidees. Ann Sci Nat Bot Biol Veg Ser 3 20:235–314Google Scholar
  38. Young TE, Gallie DR (1999) Analysis of programmed cell death in wheat endosperm reveals differences in endosperm development between cereals. Plant Mol Biol 39:915–926Google Scholar
  39. Young TE, Gallie DR, DeMason DA (1997) Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken2 genotypes. Plant Physiol 115:737–751Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Arunika H. L. A. N. Gunawardena
    • 1
  • Kathy Sault
    • 1
  • Petra Donnelly
    • 1
  • John S. Greenwood
    • 2
  • Nancy G. Dengler
    • 1
  1. 1.Department of BotanyUniversity of TorontoTorontoCanada
  2. 2.Department of BotanyUniversity of GuelphGuelphCanada

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