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Calcium, with magnesium, is essential for normal seedling development from partially dehydrated recalcitrant axes: a study on Trichilia dregeana Sond.

Published online by Cambridge University Press:  22 February 2007

Patricia Berjak  and
David Mycock
Patricia Berjak*
Affiliation:
School of Biological and Conservation Sciences, University of KwaZulu-Natal§Durban, 4041, South Africa
David Mycock
Affiliation:
School of Animal Plant and Environmental Sciences, University of the Witwatersrand Johannesburg, 2050, South Africa
*
*Correspondenceberjak@ukzn.ac.za
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Abstract

Assessment of the rehydration procedure has been consistently overlooked in evaluation of factors contributing to successful cryostorage of partially dehydrated, embryonic axes excised from recalcitrant seeds. Conventional rehydration of Trichilia dregeana (Sond.) axes in distilled water resulted in the lack of root pole gravitropism after culture on medium in vitro. In comparison, a strong gravitropic response was observed in axes that had not been dehydrated, and by those rehydrated in a solution containing 1 M CaCl2 and 1 mM MgCl2. However, no marked loss of either cation from the tissue could be detected, whether axes were rehydrated in distilled water or the Ca2+/Mg2+ solution. Starch-packed statoliths differentiated rapidly in both non-dehydrated axes and those rehydrated in the divalent cation solution, but these organelles failed to develop or accumulate much starch following axis rehydration in water, as was the case for the amyloplasts of root cells generally. After rehydration in the Ca2+/Mg2+ solution and 48 h in culture, axis root-cap columella cells accumulated Ca2+, whereas axes rehydrated in water or solutions containing either Ca2+ or Mg2+ alone did not take up Ca2+. Rehydration with the Ca2+/Mg2+ solution also altered distribution of the actin component of the cytoskeleton. When rehydrated in the divalent cation solution, actin was associated with the nucleus and with the statoliths, which were located distally in statocytes of axes. In contrast, actin was largely confined to the perinuclear area in root-cap columella cells of the agravitropic, water-rehydrated axes. The present results indicate a definitive primary role for Ca2+ with Mg2+ in graviperception, via starch metabolism, and in the determination of statolith morphology, which appears to be linked with maintenance of the actin component of the cytoskeleton in root-cap statocytes.

Keywords

amyloplastcalciumcryostoragecytoskeletonembryonic axesgraviperceptionmagnesiumrehydrationstarch metabolismstatocytesstatolithsTrichilia dregeana
Type
Research Article
Information
Seed Science Research , Volume 14 , Issue 2 , May 2004 , pp. 217 - 231
Copyright
Copyright © Cambridge University Press 2004

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References

Baluška, F. and Hasenstein, K.H. (1997) Root cytoskeleton: its role in perception and response to gravity. Planta 203, (suppl.), S69–S78.CrossRefGoogle ScholarPubMed
Baluška, F., Polsakiewicz, M., Peters, M. and Volkmann, D. (2000) Tissue specific subcellular immunolocalization of myosin-like protein in maize root apices. Protoplasma 212, 137–145.CrossRefGoogle Scholar
Barlow, P.W. (2003) The root cap: Cell dynamics, cell differentiation and cap function. Journal of Plant Growth Regulation 21, 261–286.CrossRefGoogle Scholar
Belyavskaya, N.A. (1996) Calcium and graviperception in plants: inhibitor analysis. International Review of Cytology 168, 123–185.CrossRefGoogle Scholar
Berjak, P. and Pammenter, N.W. (2001) Seed recalcitrance – current perspectives. South African Journal of Botany 67, 79–89.CrossRefGoogle Scholar
Berjak, P. and Pammenter, N.W. (2004) Recalcitrant seeds. in Benech-Arnold, R.L.;, Sánchez, R.A. (Eds) Seed physiology: Applications to agriculture. New York, Haworth Press (in press).Google Scholar
Berjak, P., Mycock, D.J., Wesley-Smith, J., Dumet, D. and Watt, P. (1996) Strategies for in vitro conservation of hydrated germplasm. pp. 19–52in Normah, M.N.;, Narimah, M.K.;, Clyde, M.M. (Eds) In vitro conservation of plant genetic resources. Kuala Lumpur, Malaysia, Percetakan Watan Sdn. Bhd.Google Scholar
Berjak, P., Walker, M., Watt, M.P. and Mycock, D.J. (1999) Experimental parameters underlying failure or success in plant germplasm cryopreservation: a case study on zygotic axes of Quercus robur L. CryoLetters 20, 251–262.Google Scholar
Berjak, P., Mycock, D.J., Walker, M., Kioko, J.I., Pammenter, N.W. and Wesley-Smith, J. (2000) Conservation of genetic resources naturally occurring as recalcitrant seeds. pp. 223–228in Black, M.;, Bradford, K.J.;, Vásquez-Ramos, J.; (Eds) Seed biology: Advances and applications. Wallingford, CABI Publishing.Google Scholar
Blancaflor, E.B. and Hasenstein, K.H. (1993) Organization of cortical microtubules in graviresponding maize roots. Planta 191, 231–237.Google ScholarPubMed
Böcher, M., Erdmann, H., Heim, S. and Wylegalla, C. (1985) Protein kinase activity of in vitro cultured plant cells in relation to growth and starch metabolism. Journal of Plant Physiology 119, 209–218.CrossRefGoogle Scholar
Busch, M.B. and Sievers, A. (1990) Hormone treatment of roots causes not only a reversible loss of starch, but also of structural polarity in statocytes. Planta 181, 358–364.CrossRefGoogle ScholarPubMed
Busch, M.B., Kortje, K.H., Rahmann, H. and Sievers, A. (1993) Characteristic and differential calcium signals from cell structures of the root cap detected by energy-filtering electron microscopy (EELS/ESI). European Journal of Cell Biology 60, 88–100.Google ScholarPubMed
Chandra, S., Chabot, J.F., Morrison, G.H. and Leopold, A.C. (1982) Localization of calcium in amyloplasts of root-cap cells using ion microscopy. Science 216, 1221–1223.CrossRefGoogle ScholarPubMed
Chang, S-C., Cho, M.H., Kang, B.G. and Kaufman, P.B. (2001) Changes in starch content in oat (Avena sativa) shoot pulvini during the gravitropic response. Journal of Experimental Botany 52, 1029–1040.CrossRefGoogle ScholarPubMed
Chang, S.C., Cho, M.H., Kim, S-K., Lee, J.S., Kirakosyan, A. and Kaufman, P.B. (2003) Changes in phosphorylation of 50 and 53 kDa soluble proteins in graviresponding oat (Avena sativa) shoots. Journal of Experimental Botany 54, 1013–1022.CrossRefGoogle ScholarPubMed
Collings, D.A., Zsuppan, G., Allen, N.S. and Blancaflor, E.B. (2001) Demonstration of prominent actin filaments in the root columella. Planta 212, 392–403.CrossRefGoogle ScholarPubMed
Dauwalder, M., Roux, S.J. and Rabenberg, L.K. (1985) Cellular and subcellular localization of calcium in gravistimulated corn roots. Protoplasma 129, 137–148.CrossRefGoogle ScholarPubMed
Dauwalder, M., Roux, S.J. and Hardison, L. (1986) Distribution of calmodulin in pea seedlings: Immunocytochemical localization in plumules and root apices. Planta 168, 461–470.CrossRefGoogle ScholarPubMed
Driss-Ecole, D., Lefranc, A. and Perbal, G. (2003) A polarized cell: the root statocyte. Physiologia Plantarum 118, 305–312.CrossRefGoogle ScholarPubMed
Evans, M.L. (1991) Gravitropism: interaction of sensitivity modulation and effector redistribution. Plant Physiology 95, 1–5.CrossRefGoogle ScholarPubMed
Gibbon, B.C. and Staiger, C.J. (2000) Profilin. pp. 45–65in Staiger, C.J.;, Baluška, F.;, Volkmann, D.;, Barlow, P. (Eds) Actin: A dynamic framework for multiple plant cell functions. Dordrecht, Kluwer Publishers.CrossRefGoogle Scholar
Goveia, M.G.T., Kioko, J.I. and Berjak, P. (2004) Developmental status is a critical factor in the selection of excised recalcitrant axes as explants for cryopreservation: a study on Trichilia dregeana Sond. Seed Science Research 14, 241–248.CrossRefGoogle Scholar
Iversen, T.H. (1969) Elimination of geotropic responsiveness in roots of cress (Lepidium sativum) by removal of statolith starch. Physiologia Plantarum 22, 1251–1262.CrossRefGoogle ScholarPubMed
Kioko, J.I. (2003) Aspects of post-harvest seed physiology and cryopreservation of the germplasm of three medicinal plant species indigenous to Kenya and South Africa. PhD Thesis, University of Natal, Durban, South Africa.Google Scholar
Kioko, J., Berjak, P., Pammenter, N.W., Watt, M.P. and Wesley-Smith, J. (1998) Desiccation and cryopreservation of embryonic axes of Trichilia dregeana Sond. CryoLetters 19, 5–14.Google Scholar
Kovar, D.R., Drøbak, B.K. and Staiger, C.J. (2000) Maize profilin isoforms are functionally distinct. Plant Cell 12, 583–598.CrossRefGoogle ScholarPubMed
Lloyd, G. and McCown, B.H. (1981) Commercially feasible micropropagation of mountain laurel (Kalmia latifolia) by use of shoot-tip culture. Proceedings of the International Plant Propagators' Society 30, 421–427.Google Scholar
Macherel, D., Viale, A. and Akazawa, T. (1986) Protein phosphorylation in amyloplasts isolated from suspension-cultured cells of sycamore (Acer pseudoplatanus L.). Plant Physiology 80, 1041–1044.CrossRefGoogle ScholarPubMed
Masters, C. (1984) Interactions between glycolytic enzymes and components of the cytomatrix. Journal of Cell Biology 99, 222S – 225S.Google ScholarPubMed
Masters, C. (1996) On the role of the cytoskeleton in metabolic compartmentation. pp. 1–30in Hesketh, J.E. (Ed.) The cytoskeleton, Volume 2 Role in cell physiology. Greenwich, Connecticut JAI Press.Google Scholar
Molecular, Probes Handbook. (2003) Available at website http://www.probes.com/handbook/sections/2003.html.Google Scholar
Moore, R. (1986) Cytochemical localization of calcium in cap cells of primary roots of Zea mays L. Journal of Experimental Botany 37, 73–79.CrossRefGoogle ScholarPubMed
Norenburg, J.L. and Barrett, J.M. (1987) Steedman's polyester wax embedment and de-embedment for combined light and scanning electron microscopy. Journal of Electron Microscopy Technique 6, 35–41.CrossRefGoogle Scholar
Pammenter, N.W. and Berjak, P. (1999) A review of recalcitrant seed physiology in relation to desiccation-tolerance mechanisms. Seed Science Research 9, 13–37.CrossRefGoogle Scholar
Pammenter, N.W., Greggains, V., Kioko, J.I., Wesley-Smith, J., Berjak, P. and Finch-Savage, W.E. (1998) Effects of differential drying rates on viability retention of recalcitrant seeds of Ekebergia capensis. Seed Science Research 8, 463–471.CrossRefGoogle Scholar
Pammenter, N.W., Berjak, P., Wesley-Smith, J., Vander Willigen, C. (2002) Experimental aspects of drying and recovery. pp. 93–110in Black, M.;, Pritchard, H.W.Desiccation and survival in plants: Drying without dying. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Perán, R., Pammenter, N.W., Naicker, J. and Berjak, P. (2004) The influence of rehydration technique on the response of recalcitrant seed embryos to desiccation. Seed Science Research 14, 179–184.CrossRefGoogle Scholar
Perbal, G., Driss-Ecole, D., Tewinkel, M. and Volkmann, D. (1997) Statocyte polarity and gravisensing in seedling roots grown in microgravity. Planta 203, (suppl.) S57–S62.CrossRefGoogle ScholarPubMed
Plieth, C. and Trewavas, A.J. (2002) Reorientation of seedlings in the earth's gravitational field induces cytosolic calcium transients. Plant Physiology 129, 786–796.CrossRefGoogle ScholarPubMed
Sack, F.D. (1991) Plant gravity sensing. International Review of Cytology 127, 193–252.CrossRefGoogle ScholarPubMed
Sinclair, W. and Trewavas, A.J. (1997) Calcium in gravitropism: a re-examination. Planta 203, (suppl.) S85–S90.CrossRefGoogle ScholarPubMed
Sinclair, W., Oliver, I., Maher, P. and Trewavas, A. (1996) The role of calmodulin in the gravitropic response of the Arabidopsis thaliana agr-3 mutant. Planta 199, 343–351.CrossRefGoogle ScholarPubMed
Slocum, R.D. and Roux, S.J. (1982) An improved method for the subcellular localization of calcium using a modification of the antimonate precipitation technique. Journal of Histochemistry and Cytochemistry 30, 617–629.CrossRefGoogle ScholarPubMed
Slocum, R.D. and Roux, S.J. (1983) Cellular and subcellular localization of calcium in gravistimulated oat coleoptiles and its possible significance in the establishment of tropic curvature. Planta 157, 481–492.CrossRefGoogle ScholarPubMed
Spurr, A.R. (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. Journal of Ultrastructural Research 26, 31–43.CrossRefGoogle ScholarPubMed
Trewavas, A. (1992) What remains of the Cholodny–Went theory? Plant Cell and Environment 15, 761–794.Google ScholarPubMed
Volkmann, D., Baluška, F. (2000) Actin cytoskeleton related to gravisensing in higher plants. pp. 557–571in Staiger, C.J.;, Baluška, F.;, Volkmann, D.;, Barlow, P. (Eds) Actin: A dynamic framework for multiple plant cell functions. Dordrecht, Kluwer Publishers.CrossRefGoogle Scholar
Walters, C., Pammenter, N.W., Berjak, P. and Crane, J. (2001) Desiccation damage, accelerated ageing and respiration in desiccation tolerant and sensitive seeds. Seed Science Research 11, 135–148.Google Scholar
Wesley-Smith, J., Walters, C., Pammenter, N.W. and Berjak, P. (2001) Interactions among water content, rapid (non-equilibrium) cooling to –196°C and survival of embryonic axes of Aesculus hippocastanum L. seeds. Cryobiology 42, 196–206.CrossRefGoogle Scholar
Winter, H. and Huber, S. (2000) Sucrose metabolism and the actin cytoskeleton: SuSy as actin-binding protein. pp. 119–128in Staiger, C.J.;, Baluška, F.;, Volkmann, D.;, Barlow, P. (Eds) Actin: A dynamic framework for multiple plant cell functions. Dordrecht, Kluwer Publishers.CrossRefGoogle Scholar
Winter, H., Huber, J.L. and Huber, S.C. (1997) Membrane association of sucrose synthase: changes during the graviresponse and possible control by protein phosphorylation. FEBS Letters 420, 151–155.CrossRefGoogle ScholarPubMed
Winter, H., Huber, J.L. and Huber, S.C. (1998) Identification of sucrose synthase as an actin-binding protein. FEBS Letters 430, 205–208.CrossRefGoogle ScholarPubMed
Wolfe, S.L. (1993) Molecular and cellular biology. Belmont, California Wadsworth.Google Scholar
Yoder, T.I., Zheng, H-Q., Todd, P. and Staehelin, L.A. (2001) Amyloplast sedimentation dynamics in maize columella cells support a new model for the gravity-sensing apparatus of roots. Plant Physiology 125, 1045–1060.CrossRefGoogle ScholarPubMed
Yokota, E. and Shimmen, T. (2000) Characterization of native actin-binding proteins from pollen: myosin and the actin-bundling proteins, 135-ABP and 115-ABP. pp. 103–118in Staiger, C.J.;, Baluška, F.;, Volkmann, D.;, Barlow, P. (Eds) Actin: A dynamic framework for multiple plant cell functions. Dordrecht, Kluwer Publishers.CrossRefGoogle Scholar
Young, L.M. and Evans, M.L. (1994) Calcium-dependent asymmetric movement of 3H-indole-3-acetic acid across gravistimulated isolated root caps of maize. Plant Growth Regulation 14, 235–242CrossRefGoogle Scholar