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Directional cell-to-cell communication in theArabidopsis root apical meristem III. Plasmodesmata turnover and apoptosis in meristem and root cap cells during four weeks after germination - Protoplasma

  • ️Rost, T. L.
  • ️Wed Mar 01 2000

Summary

Plasmodesmata frequency and distribution in root cap cells ofArabidopsis thaliana root tips were characterized during four weeks after germination to understand the symplasmic control of apoptosis. Apoptotic cells in some of the root apical-meristem cells and in root cap cells were identified by the terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling reaction and characterized by electron microscopy. Starting at the second week after germination, cells in the outermost layers of the root cap showed typical apoptotic features, including nuclear DNA fragmentation, chromatin condensation, cytoplasmic vacuolation, and organelle destruction. Intercellular connections, indicated by the frequency and number of plasmodesmata per cell length, were significantly reduced in the walls of outer root cap cells. This shows that cells become symplasmically isolated during the apoptosis process. In apoptotic root cap cells, the majority of nonfunctional plasmodesmata were observed to be associated with degenerated endoplasmic reticulum; this state was prior to the detection of any nuclear DNA fragmentation. Other nonfunctional plasmodesmata were sealed by heterogeneous cell wall materials. However, in immature epidermal and cortical cells in 4-week-old arrested roots the endoplasmic reticulum associated with plasmodesmata became disconnected as a result of protoplast condensation and shrinkage. No degenerated endoplasmic reticulum was observed in these cells. These observations suggest that the apoptotic processes in the root body and the root cap are different.

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References

  • Baum SF (1996) The developmental organization of the root apical meristem inArabidopsis thaliana cv. WS. PhD Dissertation, University of California, Davis, California

    Google Scholar 

  • —, Rost TL (1996) Root apical organization inArabidopsis thaliana: the root cap and protoderm. Protoplasma 192: 178–188

    Google Scholar 

  • Doerner P (1993) Patterning theArabidopsis root. Curr Biol 3: 867–869

    Google Scholar 

  • Dolan L (1996) Pattern in the root epidermis: an interplay of diffusible signals and cellular geometry. Ann Bot 77: 547–553

    Google Scholar 

  • —, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organization of theArabidopsis thaliana root tip. Development 119: 71–84

    Google Scholar 

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

    Google Scholar 

  • Greenberg JT (1996) Programmed cell death: a way of life for plants. Proc Natl Acad Sci USA 93: 12094–12097

    Google Scholar 

  • Gunning BES (1978) Age-related and origin-related control of the number of plasmodesmata in cell walls of developingAzolla roots. Planta 143: 181–190

    Google Scholar 

  • Havel L, Durzan DJ (1996) Apoptosis in plants. Bot Acta 109: 268–277

    Google Scholar 

  • Hawes MC (1990) Living plant cells released from the root cap: a regulator of microbial populations in the rhizosphere. Plant Soil 129: 19–27

    Google Scholar 

  • Jones AM, Dangl JL (1996) Logjam at the styx: programmed cell death in plants. Trends Plant Sci 1: 114–119

    Google Scholar 

  • Kerk NM, Feldman LJ (1995) A biochemical model for the initiation and maintenance of the quiescent center: implications for organization of root meristems. Development 121: 825–833

    Google Scholar 

  • Kragler F, Lucas WJ, Monzer J (1988) Plasmodesmata: dynamics, domains and patterning. Ann Bot 81: 1–10

    Google Scholar 

  • Kwiatkowska M (1988) Symplasmic isolation ofChara vulgaris antheridium and mechanisms regulating the process of spermatogenesis. Protoplasma 142: 137–146

    Google Scholar 

  • Lucas WJ (1995) Plasmodesmata: intercellular channels for macromolecular transport in plants. Curr Opin Cell Biol 7: 673–680

    Google Scholar 

  • —, Ding B, van der Schoot C (1993) Plasmodesmata and the supracellular nature of plants. New Physiol 125: 435–476

    Google Scholar 

  • —, Bouche-Pillion S, Jackson DP, Nguyen L, Baker L, Ding B, Hake S (1995) Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270: 1980–1983

    Google Scholar 

  • Mezitt LA, Lucas WJ (1996) Plasmodesmal cell-to-cell transport of proteins and nucleic acids. Plant Mol Biol 32: 251–273

    Google Scholar 

  • Mittler R, Lam E (1995) In situ detection of nDNA fragmentation during the differentiation of tracheary elements in higher plants. Plant Physiol 108: 489–493

    Google Scholar 

  • Oparka KJ (1993) Signaling via plasmodesmata: the neglected pathway. Sem Cell Biol 4: 131–138

    Google Scholar 

  • —, Duckett CM, Prior DAM, Fisher DB (1994) Real-time imaging of phloem unloading in the root tip ofArabidopsis. Plant J 6: 759–766

    Google Scholar 

  • Palevitz BA, Hepler PK (1985) Changes in dye coupling of stomatal cells ofAllium andCommelina demonstrated by microinjection of Lucifer yellow. Planta 164: 473–479

    Google Scholar 

  • Rost TL, Bryant JA (1996) Root organisation and gene expression patterns. J Exp Bot 47: 1613–1628

    Google Scholar 

  • —, Baum SF, Nichol S (1996) Root apical organization inArabidopsis thaliana ecotype ‘WS’ and a comment on root cap structure. Plant Soil 187: 91–95

    Google Scholar 

  • Ruzin, SE (1999) Plant microtechnique and microscopy. Oxford University Press, New York

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Stephenson MB, Hawes MC (1994) Correlation of pectin methylesterase activity in root caps of pea with root border cell separation. Plant Physiol 106: 739–745

    Google Scholar 

  • van den Berg C, Willemsen V, Hage W, Scheres B (1995) Determination of cell fate in theArabidopsis root meristem by directional signaling. Nature 378: 62–65

    Google Scholar 

  • — —, Hendriks G, Weisbeek P, Scheres B (1997) Short-range control of cell differentiation in theArabidopsis root meristem. Nature 390: 287–289

    Google Scholar 

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

    Google Scholar 

  • Wille AC, Lucas WJ (1984) Ultrastructural and histochemical studies on guard cells. Planta 160: 129–142

    Google Scholar 

  • Young SJ, Royer SM, Groves PM, Kinnamon JC (1987) Three-dimensional reconstructions from serial micrographs using the IBM PC. J Electron Microsc Tech 6: 207–218

    Google Scholar 

  • Zhu T, Lucas WJ, Rost TL (1998a) Directional cell-to-cell communication in theArabidopsis apical meristem I: an ultrastructural and functional analysis. Protoplasma 203: 35–47

    Google Scholar 

  • —, O'Quinn RL, Lucas WJ, Rost TL (1998b) Directional cell-to-cell communication in theArabidopsis root apical meristem II: dynamics of plasmodesmata formation. Protoplasma 204: 84–93

    Google Scholar 

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Author notes

  1. T. Zhu

    Present address: Novartis Agricultural Discovery Institute, Inc., San Diego, California, USA

Authors and Affiliations

  1. Section of Plant Biology, Division of Biological Science, University of California, One Shields Avenue, 95616, Davis, CA, USA

    T. Zhu & T. L. Rost

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  1. T. Zhu

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  2. T. L. Rost

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Zhu, T., Rost, T.L. Directional cell-to-cell communication in theArabidopsis root apical meristem III. Plasmodesmata turnover and apoptosis in meristem and root cap cells during four weeks after germination. Protoplasma 213, 99–107 (2000). https://doi.org/10.1007/BF01280510

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  • Received: 15 June 1999

  • Accepted: 15 February 2000

  • Issue Date: March 2000

  • DOI: https://doi.org/10.1007/BF01280510

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