Skip to main content
SpringerLink
Log in

Megasporogenesis and programmed cell death in Tillandsia (Bromeliaceae)

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

The degeneration of three of four meiotic products is a very common process in the female gender of oogamous eukaryotes. In Tillandsia (and many other angiosperms), the surviving megaspore has a callose-free wall in chalazal position while the other three megaspores are completely embedded in callose. Therefore, nutrients and signals can reach more easily the functional megaspore from the nucellus through the chalazal pole with respect to the other megaspores. The abortion of three of four megaspores was already recognized as the result of a programmed cell death (PCD) process. We investigated the process to understand the modality of this specific type of PCD and its relationship to the asymmetric callose deposition around the tetrad. The decision on which of the four megaspores will be the supernumerary megaspores in angiosperms, and hence destined to undergo programmed cell death, appears to be linked to the callose layer deposition around the tetrad. During supernumerary megaspores degeneration, events leading to the deletion of the cells do not appear to belong to a single type of cell death. The first morphological signs are typical of autophagy, including the formation of autophagosomes. The TUNEL positivity and a change in morphology of mitochondria and chloroplasts indicate the passage to an apoptotic-like PCD phase, while the cellular remnants undergo a final process resembling at least partially (ER swelling) necrotic morphological syndromes, eventually leading to a mainly lipidic cell corpse still separated from the functional megaspore by a callose layer.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Scheme 1

Similar content being viewed by others

References

  • Adrain C, Martin SJ (2001) The mitochondrial apoptosome: a killer unleashed by the cytochrome seas. Trends Biochem Sci 26:390–397

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Bouman F (1984) The ovule. In: Johri BM (ed) Embryology of angiosperms. Springer, Berlin, pp 123–157

    Google Scholar 

  • Brighigna L, Papini A (1993) The ultrastructure of the tapetum of Tillandsia albida Mez et Purpus. Phytomorphology 43(3–4):261–275

    Google Scholar 

  • Brighigna L, Milocani E, Papini A, Vesprini JL (2006) Programmed cell death in the nucellus of Tillandsia (Bromeliaceae). Caryologia 59(4):334–339

    Google Scholar 

  • Calderon-Urrea A, Dellaporta SL (1999) Cell death and cell protection genes determine the fate of pistils in maize. Development 126:435–441

    PubMed  CAS  Google Scholar 

  • Cecchi Fiordi A, Papini A, Brighigna L (2002) Programmed cell death of the nonfunctional megaspores in Larix leptolepis (Sieb. Et Zucc.) Gordon (Pinaceae): ultrastructural aspects. Phytomorphology 52(2–3):187–195

    Google Scholar 

  • Cupisti S, Conn CM, Fragouli E, Whalley K, Mills JA, Faed MJW, Delhanty JDA (2003) Sequential FISH analysis of oocytes and polar bodies reveals aneuploidy mechanisms. Prenat Diagn 23:663–668

    Article  PubMed  CAS  Google Scholar 

  • Currier HB, Shih CY (1968) Sieve tubes and callose in Elodea leaves. Am J Bot 55:145–152

    Article  Google Scholar 

  • Danon A, Sanchez Coll N, Apel K (2006) Cytochrome-1-dependent execution of programmed cell death induced by singlet oxygen in Arabidopsis thaliana. P Natl Acad Sci USA 103:17036–17041

    Article  CAS  Google Scholar 

  • Doyle SM, Diamond M, McCabe PF (2010) Chloroplast and reactive oxygen species involvement in apoptotic-like programmed cell death in Arabidopsis suspension cultures. J Exp Bot 61(2):473–482

    Article  PubMed  CAS  Google Scholar 

  • Dunbar A (1973) Pollen development in the Eleocharis palustris group (Cyperaceae). 1. Ultrastructure and ontogeny. Bot Not 126:197–254

    Google Scholar 

  • Fukuda H (2000) Programmed cell death of tracheary elements as a paradigm in plants. Plant Mol Biol 44:245–253

    Article  PubMed  CAS  Google Scholar 

  • Gibbons IR, Grimstone AV (1960) On the flagellar structure in certain flagellate. J Biophys Biochem Cytol 7:697–716

    Article  PubMed  CAS  Google Scholar 

  • Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309–1312

    Article  PubMed  CAS  Google Scholar 

  • Gunawardena AHLAN, Greenwood JS, Dengler NG (2007) Cell wall degradation and modification during programmed cell death in lace plant, Aponogeton madascariensis (Aponogetonaceae). Am J Bot 94(7):1116–1128

    Article  PubMed  CAS  Google Scholar 

  • Herr JM Jr (1995) The origin of the ovule. Am J Bot 82(4):547–564

    Article  Google Scholar 

  • Ingram GC (2010) Family life at close quarters: communication and constraint in angiosperm seed development. Protoplasma. doi:10.1007/s00709-010-0184-y

    PubMed  Google Scholar 

  • Jabs T (1999) Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem Pharmacol 57:231–245

    Article  PubMed  CAS  Google Scholar 

  • Jane WN, Chiang SHT (1996) Ultrastructure of megasporogenesis and early megagametogenesis in Arundo formosana Hack. (Poaceae). Int J Plant Sci 157(4):418–431

    Article  Google Scholar 

  • Jones AM (2001) Programmed cell death in development and defense. Plant Physiol 125:94–97

    Article  PubMed  CAS  Google Scholar 

  • Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Brit J Cancer 26:239–257

    Article  PubMed  CAS  Google Scholar 

  • Krishnamurthy KV, Krishnaraj R, Chozhaven DR, Christopher FS (2000) The programme of cell death in plants and animals—a comparison. Curr Sci 79(9):1169–1118

    CAS  Google Scholar 

  • Kroemer G, Galluzzi L, Brenner C (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87:99–163

    Article  PubMed  CAS  Google Scholar 

  • Krysko DV, Vanden Berghe T, Parthoens E, D’Herde K, Vandenabeele P (2008) Methods for distinguishing apoptotic from necrotic cells and measuring their clearance. Meth Enzymol 442:308–341

    Google Scholar 

  • Lemasters JJ (1999) Mechanisms of hepatic toxicity. V. Necroapoptosis and the mitochondrial permeability transition: shared pathways to necrosis and apoptosis. Am J Physiol Gastrointest Liver Physiol 276:G1–G6

    CAS  Google Scholar 

  • Lennon SV, Martin SJ, Cotter TG (1991) Dose-dependent induction of apoptosis in human tumour cell lines by widely diverging stimuli. Cell Prolif 24:203–214

    Article  PubMed  CAS  Google Scholar 

  • Lockshin RA, Zakeri Z (2004) Apoptosis, autophagy, and more. Int J Biochem Cell Biol 36:2405–2419

    Article  PubMed  CAS  Google Scholar 

  • Madrid EN, Friedman WE (2010) Female gametophyte and early seed development in Peperomia (Piperaceae). Am J Bot 97(1):1–14

    Article  PubMed  Google Scholar 

  • Maugini E (1953) Ricerche cito-embriologiche su Piper medium Jacq. var. ceanothifolium (H.B.K.) Trel. et Yun. Caryologia 5:282–287

    Google Scholar 

  • Milocani E, Papini A, Brighigna L (2006) Ultrastructural studies on bicellular pollen grains of Tillandsia seleriana Mez (Bromeliaceae), a neotropical epiphyte. Caryologia 59(1):88–97

    Google Scholar 

  • Mullineaux P, Karpinski S (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5:43–48

    Article  PubMed  CAS  Google Scholar 

  • Nagata S (2000) Apoptotic DNA fragmentation. Exp Cell Res 256(1):12–18

    Article  PubMed  CAS  Google Scholar 

  • Neill S (2005) NO way to die—nitric oxide, programmed cell death and xylogenesis. New Phytol 165:5–7

    Article  PubMed  Google Scholar 

  • Noodén LD (1988) The phenomena of senescence and aging. In: Noodén LD, Leopold AC (eds) Senescence and Aging in Plants. Academic Press, San Diego, pp 1–50

    Google Scholar 

  • Papini A, Mosti S, Brighigna L (1999) Programmed cell death events in the tapetum development of Angiosperms. Protoplasma 207:213–221

    Article  Google Scholar 

  • Papini A, Tani G, Di Falco P, Brighigna L (2010) The ultrastructure of the development of Tillandsia (Bromeliaceae) trichome. Flora 205(2):94–100

    Article  Google Scholar 

  • Patel S, Caplan J, Dinesh-Kumar SP (2006) Autophagy in the control of programmed cell death. Curr Opin Plant Biol 9:391–396

    Article  PubMed  CAS  Google Scholar 

  • Pennell RI, Lamb C (1997) Programmed cell death in plants. Plant Cell 9:1157–1168

    Article  PubMed  CAS  Google Scholar 

  • Potten C, Wilson J (2004) Apoptosis the life and death of cells. Cambridge University Press, Cambridge

    Google Scholar 

  • Ranganath RM, Nagashree NR (2000) Selective cell elimination during microsporogenesis in sedges. Sex Plant Reprod 13:53–60

    Article  Google Scholar 

  • Rao AN, Wee YC (1979) Embryology of the pineapple, Ananas comosus (L.) Merr. New Phytol 83(2):485–497

    Google Scholar 

  • Reape TJ, McCabe PF (2008) Apoptotic-like programmed cell death in plants. New Phytol 180:13–26

    Article  PubMed  CAS  Google Scholar 

  • Reape TJ, McCabe PF (2010) Apoptotic-like regulation of programmed cell death in plants. Apoptosis 15(3):249–256

    Article  PubMed  CAS  Google Scholar 

  • Reape TJ, Molony EM, McCabe PF (2008) Programmed cell death in plants: distinguishing between different modes. J Exp Bot 59(3):435–444

    Article  PubMed  CAS  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain for electron microscopy. J Cell Biol 17:208–212

    Article  PubMed  CAS  Google Scholar 

  • Rodkiewicz B (1970) Callose in cell walls during megasporogenesis in angiosperms. Planta 93(1):39–47

    Article  Google Scholar 

  • Rodrigues-Garcia MI, Majewska-Sawka A (1992) Is the special callose wall of microsporocytes an impermeable barrier? J Exp Bot 43(12):1659–1663

    Article  Google Scholar 

  • Rogers HJ (2006) Programmed cell death in floral organs: how and why do flowers die? Ann Bot 97:09–315

    Google Scholar 

  • Russell SD (1979) Fine structure of megagametophyte development in Zea mays. Can J Bot 57(10):1093–1110

    Article  Google Scholar 

  • Sanders FJ, Wride MA (1995) Programmed cell death in development. Int Rev Cytol 163:105–173

    Article  PubMed  CAS  Google Scholar 

  • Sanmartìn M, Jaroszewski L, Raikhel NV, Rojo E (2005) Caspases, regulating death since the origin of life? Plant Physiol 137:841–847

    Article  PubMed  Google Scholar 

  • Schulze-Osthoff K, Walczak H, Droege W, Krammer PH (1994) Cell nucleus and DNA fragmentation are not required for apoptosis. J Cell Biol 127:15–20

    Article  PubMed  CAS  Google Scholar 

  • Schwab CA (1971) Callose in megasporogenesis of Diarrhena (Gramineae). Can J Bot 49(8):1523–1524

    Article  Google Scholar 

  • Schweichel JU, Merker HJ (1973) The morphology of various types of cell death in prenatal tissues. Teratology 7:253–266

    Article  Google Scholar 

  • Southworth D (1971) Incorporation of radioactive precursors into developing pollen walls. In: Heslop Harrison J (ed) Pollen: development and physiology. Butterworths, London, pp 115–120

    Google Scholar 

  • Spurr AR (1969) A low viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  PubMed  CAS  Google Scholar 

  • Strandhede S (1973) Pollen development in the Eleocharis palustris group (Cyperaceae). II. Cytokinesis and microspore degeneration. Bot Not 126:255–265

    Google Scholar 

  • Tinari A, Giammarioli AM, Manganelli V, Ciarlo L, Malori W (2008) Analyzing morphological and ultrastructural features in cell death. Methods Enzymol 442:1–26

    Article  PubMed  Google Scholar 

  • Van Doorn W, Woltering EJ (2005) Many waysto exit? Cell death categories in plants. Trends in Plant Sci 10(3):117–122

    Article  Google Scholar 

  • Vianello A, Zancani M, Peresson C, Petrussa E, Casolo V, Krajňáková J, Patui S, Braidot E, Macrì F (2007) Plant mitochondrial pathway leading to programmed cell death. Physiol Plant 129(1):242–252

    Article  CAS  Google Scholar 

  • Willemse MTM, Van Went JL (1984) The female gametophyte. In: Johri BM (ed) Embryology of angiosperms. Springer-Verlag, Berlin, Germany, pp 159–196

    Google Scholar 

  • Wyllie AH, Kerr JFR, Currie AR (1980) Cell death, the significance of apoptosis. Int Rev Cytol 68:251–306

    Article  PubMed  CAS  Google Scholar 

  • Yang W-C, Shi D-Q, Chen Y-H (2010) Female gametophyte development in flowering plants. Annu Rev Plant Biol 61:89–108

    Article  PubMed  CAS  Google Scholar 

  • Zakeri Z, Melendez A, Lockshin RA (2008) Detection of autophagy in cell death. Meth Enzymol 442:289–306

    Article  PubMed  Google Scholar 

Download references

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Dipartimento di Biologia Vegetale, Università di Firenze, Via La Pira, 4, 50132, Florence, Italy

    Alessio Papini, Stefano Mosti, Eva Milocani, Gabriele Tani, Pietro Di Falco & Luigi Brighigna

Authors
  1. Alessio Papini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stefano Mosti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eva Milocani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gabriele Tani
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pietro Di Falco
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Luigi Brighigna
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alessio Papini.

Additional information

Handling Editor: Peter Nick

Alessio Papini and Stefano Mosti contributed equally to this article.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(JPEG 1125 kb)

ESM 2

(JPEG 1385 kb)

ESM 3

(JPEG 1341 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Papini, A., Mosti, S., Milocani, E. et al. Megasporogenesis and programmed cell death in Tillandsia (Bromeliaceae). Protoplasma 248, 651–662 (2011). https://doi.org/10.1007/s00709-010-0221-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-010-0221-x

Keywords

Search

Navigation