Skip to main content
Log in

Auxin deprivation induces a developmental switch in maize somatic embryogenesis involving redistribution of microtubules and actin filaments from endoplasmic to cortical cytoskeletal arrays

  • Cell Biology and Morphogenesis
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

A developmental switch from non-polar pre-embryogenic units to polarized transition units in maize embryogenic callus is caused by auxin deprivation from the culture medium. This switch is accompanied by cytoskeletal rearrangements in embryogenic cells. An immunofluorescence study revealed prominent endoplasmic microtubules and actin filament meshworks radiating from the nuclear surfaces in pre-embryogenic cells growing on medium supplemented with auxin. On the other hand, parallel-organized cortical microtubules and cortical actin filament networks are inherently associated with polarized embryogenic cells of transition units growing on medium without auxin. These results indicate that fine-tuning of the dynamic equilibrium between endoplasmic and cortical cytoskeletal arrays is important for progress in somatic embryogenesis.

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.

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

Abbreviations

AGP :

Arabinogalactan protein

BSA :

Bovine serum albumin

2,4-D :

2, 4-Dichlorophenoxyacetic acid

FITC:

Fluorescein isothiocyanate

MS :

Murashige and Skoog medium

PBS :

Phosphate-buffered saline

SB :

Stabilizing buffer

References

  • Baluška F, Parker JS, Barlow PW (1992) Specific patterns of cortical and endoplasmic microtubules associated with cell growth and tissue differentiation in roots of maize (Zea mays L.). J Cell Sci 103:191–200

    Google Scholar 

  • Baluška F, Parker JS, Barlow PW (1993) The microtubular cytoskeleton in cells of cold-treated roots of maize (Zea mays L.) shows tissue-specific responses. Protoplasma 172:84-96

    Google Scholar 

  • Baluška F, Barlow PW, Kubica Š, Volkmann D (1995) The effects of treatment which disrupts microtubule arrays in maize root cells. Interplay between the cytoskeleton, nuclear organization and post-mitotic cellular growth patterns. New Phytol 130:177–192

    Google Scholar 

  • Baluška F, Barlow PW, Parker JS, Volkmann D (1996a) Symmetric reorganization of radiating microtubules around pre- and post-mitotic nuclei of dividing cells organized within intact root meristems. J Plant Physiol 149:119–128

    Google Scholar 

  • Baluška F, Barlow PW, Volkmann D (1996b) Complete disintegration of the microtubular cytoskeleton precedes its auxin-mediated reconstruction in post-mitotic maize root cells. Plant Cell Physiol 37:1013–1021

    PubMed  Google Scholar 

  • Baluška F, Šamaj J, Volkmann D, Barlow PW (1997) Impact of taxol-mediated stabilization of microtubules on nuclear morphology, ploidy levels and cell growth in maize roots. Biol Cell 89:221–231

    Article  PubMed  Google Scholar 

  • Baluška F, Volkmann D, Barlow PW (2000) Actin-based domains of the 'cell periphery complex' and their associations with polarized 'cell bodies' in higher plants. Plant Biol 2:253–267

    Article  Google Scholar 

  • Barlow PW, Baluška F (2000) Cytoskeletal perspectives on root growth and morphogenesis. Annu Rev Plant Physiol Plant Mol Biol 51:289–322

    Article  CAS  Google Scholar 

  • Barlow PW, Parker JS (1996) Microtubular cytoskeleton and root morphogenesis. Plant Soil 187:23–36

    CAS  Google Scholar 

  • Baskin TI, Wilson JE (1997) Inhibitors of protein kinases and phosphatases alter root morphology and disorganize cortical microtubules. Plant Physiol 113:493–502

    CAS  PubMed  Google Scholar 

  • Brown RC, Lemmon BE (1988) Cytokinesis occurs at boundaries of domains delimited by nuclear-based microtubules in sporocytes of Conocephalum conicum (Bryophyta). Cell Motil Cytoskeleton 11:139–146

    Google Scholar 

  • Brown RC, Lemmon, BE, Olsen OA (1994) Endosperm development in barley: microtubule involvement in the morphogenetic pathway. Plant Cell 6:1241–1252

    Article  PubMed  Google Scholar 

  • Caumont C, Petitprez M, Woynaroski S, Barthou H, Brière C, Kallerhoff J, Borin C, Souvré A, Alibert G (1997) Agarose embedding affects cell wall regeneration and microtubule organization in sunflower hypocotyl protoplasts. Physiol Plant 99:129–134

    CAS  Google Scholar 

  • Collings DA, Allen NS (2000) Cortical actin interacts with the plasma membrane and microtubules. In: Staiger CJ, Baluška F, Volkmann D, Barlow PW (eds) Actin: a dynamic framework for multiple plant cell functions. Kluwer, Dordrecht, pp 145–163

    Google Scholar 

  • Dickinson HG, Sheldon JM (1984) A radial system of microtubules extending between the nucleus envelope and the plasma membrane during early male haplophase in flowering plants. Planta 161:86–90

    Google Scholar 

  • Gervais C, Newcomb W, Simmonds DH (2000) Rearrangement of the actin filament and microtubule cytoskeleton during induction of microspore embryogenesis in Brassica napus L. cv. Topas. Protoplasma 213:194–202

    Google Scholar 

  • Grolig F (1998) Nuclear centering in Spirogyra: force integration by microfilaments along microtubules. Planta 204:54–63

    Article  CAS  PubMed  Google Scholar 

  • Hause G, Hause B, van Lammeren AAM (1993) Microtubular and actin filament configurations during microspore and pollen development in Brassica napus cv. Topas. Can J Bot 70:1369–1376

    Google Scholar 

  • Hauser M-T, Morikami A, Benfey PN (1995) Conditional root expansion mutants of Arabidopsis. Development 121:1237–1252

    CAS  PubMed  Google Scholar 

  • Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 17:159–187

    CAS  PubMed  Google Scholar 

  • Holy TE, Leibler S (1994) Dynamic instability of microtubules as an efficient way to search in space. Proc Natl Acad Sci USA 91:5682–5685

    CAS  PubMed  Google Scholar 

  • Lambert AM (1995) Microtubule-organizing centers in higher plants: evolving concepts. Bot Acta 108:535–537

    Google Scholar 

  • Li Y-Q, Moscatelli A, Cai G, Cresti M (1997) Functional interactions among cytoskeleton, membranes, and cell wall in the pollen tube of flowering plants. Int Rev Cytol 176:133–199

    CAS  PubMed  Google Scholar 

  • Lloyd CW, Pearce KJ, Rawlins DJ, Ridge RW, Shaw PJ (1987) Endoplasmic microtubules connect the advancing nucleus to the tip of legume root hairs, but F-actin is involved in basipetal migration. Cell Motil Cytoskeleton 8:27–36

    Google Scholar 

  • Meijer EGM, Simmonds DH (1988) Microtubule organization during the development of the mitotic apparatus in cultured mesophyll protoplasts of higher plants—an immunofluorescence microscopic study. Physiol Plant 74:225–232

    Google Scholar 

  • Mineyuki Y, Iida H, Anraku Y (1994) Loss of microtubules in the interphase cells of onion (Allium cepa L.) root tips from the cell cortex and their appearance in the cytoplasm after treatment with cycloheximide. Plant Physiol 104:281–284

    CAS  PubMed  Google Scholar 

  • Šamaj J, Bobák M, Blehová A, Krištín J, Auxtová-Šamajová O (1995) Developmental SEM observations of an extracellular matrix in embryogenic calli of Drosera rotundifolia and Zea mays. Protoplasma 186:45–49

    Google Scholar 

  • Šamaj J, Bobák M, Ovecka M, Blehová B, Pretová A (1997) Structural features of plant morphogenesis in vitro. Veda, Bratislava

  • Šamaj J, Baluška F, Bobák M, Volkmann D (1999a) Extracellular matrix surface network of embryogenic units of friable maize callus contains arabinogalactan-proteins recognized by monoclonal antibody JIM4. Plant Cell Rep 18:369–374

    Article  Google Scholar 

  • Šamaj J, Ensikat HJ, Baluška F, Knox JP, Barthlott W, Volkmann D (1999b) Immunogold-localization of plant surface arabinogalactan-proteins using glycerol liquid substitution and scanning electron microscopy. J Microsc 193:150–157

    Article  PubMed  Google Scholar 

  • Šamaj J, Ovecka M, Hlavacka A, Lecourieux F, Meskiene I, Lichtscheidl I, Lenart P, Salaj J, Volkmann D, Bögre L, Baluška F, Hirt H (2002) Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair tip-growth. EMBO J 21:3296–3306

    Article  PubMed  Google Scholar 

  • Sivaguru M, Yamamoto Y, Matsumoto H (1999) Differential impacts of aluminium on microtubule organization depends on growth phase in suspension-cultured tobacco cells. Physiol Plant 107:110–119

    Article  CAS  Google Scholar 

  • Staiger CJ (2000) Signaling to the actin cytoskeleton in plants. Annu Rev Plant Physiol Plant Mol Biol 51:257–288

    Google Scholar 

  • Tautorus TE, Wang H, Fowke LC, Dunstan DI (1992) Microtubule pattern and the occurrence of pre-prophase bands in embryogenic cultures of black spruce (Picea mariana Mill.) and non-embryogenic cultures of jack pine (Pinus banksiana Lamb.). Plant Cell Rep 11:419–423

    Google Scholar 

  • Timmers ACJ, Auriac MC, Truchet G (1999) Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126:3617–3628

    CAS  PubMed  Google Scholar 

  • Traas J, Bellini C, Nacry P, Kronenberger J, Bouchez D, Caboche M (1995) Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375:676–677

    Google Scholar 

  • Volkmann D, Baluška F (1999) Actin cytoskeleton in plants: from transport networks to signaling networks. Microsc Res Tech 47:135–154

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by a research fellowship from the Alexander von Humboldt Foundation (Bonn, Germany) to J. Š., and by VEGA grant Nr. 2/6016/99 from the Slovak Ministry of Science and Education.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. Šamaj.

Additional information

Communicated by H. Lörz

Rights and permissions

Reprints and permissions

About this article

Cite this article

Šamaj, J., Baluška, F., Pretová, A. et al. Auxin deprivation induces a developmental switch in maize somatic embryogenesis involving redistribution of microtubules and actin filaments from endoplasmic to cortical cytoskeletal arrays. Plant Cell Rep 21, 940–945 (2003). https://doi.org/10.1007/s00299-003-0611-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-003-0611-z

Keywords

Navigation