Skip to main content
SpringerLink
Log in

Use of secondary ion mass spectrometry to image44calcium uptake in the cell walls of apple fruit

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

Summary

Calcium, an important agent in regulating cell wall autolysis during fruit ripening, interacts with pectic acid polymers to form cross-bridges that influence cell separation. In the present study, secondary ion mass spectrometry (SIMS) was used to determine whether the cell walls of apple fruit were able to take up exogenously applied44Ca, which was infiltrated into mature fruit. SIMS, which has the ability to discriminate between isotopes, allowed localization of the exogenously applied44Ca and the native40Ca. The results indicated that the total amount of calcium present in the cell walls was enriched with44Ca and that heterogeneity of44Ca distribution occurred in the pericarp. Isotope ratio images showed microdomains in the cell wall, particularly in the middle lamella intersects that oppose the intercellular spaces. These domains may be the key areas that control cell separation. These data suggest that exogenously applied calcium may influence cell wall autolysis.

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

Similar content being viewed by others

Abbreviations

SIMS:

secondary ion mass spectrometry

References

  • Bagshaw SL, Cleland RE (1993) Is wall-bound calcium redistributed during the gravireaction of stems and coleoptiles? Plant Cell Environ 16: 1081–1089

    Google Scholar 

  • Brady CJ (1987) Fruit ripening. Annu Rev Plant Physiol 38: 155–178

    Google Scholar 

  • — (1992) Molecular approaches to understanding fruit ripening. New Zealand J Crops Hort Sci 20: 107–117

    Google Scholar 

  • Braudo EE, Soshinsky AA, Yuryev TP, Toltstoguzov VB (1992) The interaction of polyuronides with calcium ions. 1: Binding isotherms of calcium ions with pectic substances. Carbohydrate Polymers 18: 165–169

    Google Scholar 

  • Burns JK, Pressey R (1987) Ca2+ in cell wall of ripening tomato and peach. J Am Soc Hort 112: 783–787

    Google Scholar 

  • Burns MS (1982) Applications of secondary ion mass spectrometry (SIMS) in biological research: a review. J Microsc 127: 237–258

    PubMed  Google Scholar 

  • — (1984) Selection of calcium isotopes for secondary ion mass spectrometric analysis of biological material. I Microsc 135: 209–212

    Google Scholar 

  • Busch MB, Körtje KH, Rahmann H, Sievers A (1993) Characteristic and differential calcium signals from cell structures of the root cap detected by energy-filtering electron microscopy (EELS/ESI). Eur J Cell Biol 60: 88–100

    PubMed  Google Scholar 

  • Bushinsky DA, Chabala JM, Levi-Setti R (1990) Comparison of in vitro and in vivo44Ca labelling of bone by scanning ion microprobe. Am J Physiol 259: 586–592

    Google Scholar 

  • Callaham DA, Hepler PK (1991) Measurement of free calcium in plant cells. In: McCormack JG, Cobbold PH (eds) Cellular calcium: a practical approach. IRL Press, Oxford, pp 348–412

    Google Scholar 

  • Campbell NA, Stika KM, Morrison GH (1979) Calcium and potassium in the motor organ of the sensitive plant: localization by ion microscopy. Science 204: 185–186

    Google Scholar 

  • Chandra S, Morrison GH (1992) Sample preparation of animal tissues and cell cultures for secondary ion mass spectrometry (SIMS) microscopy. Biol Cell 74: 31–42

    PubMed  Google Scholar 

  • —, Chabot JF, Morrison GH, Leopold AC (1982) Localization of calcium in amyloplasts of root-cap cells using ion microscopy. Science 216: 1221–1223

    Google Scholar 

  • —, Harris WC Jr, Morrison GH (1984) Distribution of calcium during interphase and mitosis as observed by ion microscopy. J Histochem Cytochem 32: 1224–1230

    PubMed  Google Scholar 

  • —, Fullmer CS, Smith CA, Wasserman RH, Morrison GH (1990) Ion microscopic imaging of calcium transport in the intestinal tissue of vitamin D-deficient and vitamine D-replete chickens: a44Ca stable isotope study. Proc Natl Acad Sci USA 87: 5715–5719

    PubMed  Google Scholar 

  • —, Ausserer WA, Morrison GH (1992) Subcellular imaging of calcium exchange in cultured cells with ion microscopy. J Cell Sci 102: 417–425

    PubMed  Google Scholar 

  • —, Fewtrell C, Millard PJ, Sandison DR, Webb WW, Morrison GH (1994) Imaging of total intracellular calcium and calcium influx and efflux in individual resting and stimulated tumor mast cells using ion microscopy. J Biochem Chem 269: 15186–15194

    Google Scholar 

  • Ferguson IB (1984) Calcium in plant senescence and fruit ripening. Plant Cell Environ 7: 477–489

    Google Scholar 

  • Fischer RL, Bennet AB (1991) Role of cell wall hydrolases in fruit ripening. Annu Rev Plant Physiol Plant Mol Biol 42: 675–703

    Google Scholar 

  • Fry SC (1988) The growing plant cell wall: chemical and metabolic analysis. Longman, London

    Google Scholar 

  • Gidley MJ, Morris ER, Murray EJ, Powell DA, Rees DA (1980) Evidence for two mechanisms of interchain association in calcium pectate gels. Int J Biol Macromol 2: 332–334

    Google Scholar 

  • Gilroy S, Bethke PC, Jones RL (1993) Calcium homeostasis in plants. J Cell Sci 106: 453–462

    PubMed  Google Scholar 

  • Gormley R (1981) Dietary fibre — some properties of alcohol-insoluble solids residues from apples. J Sci Food Agric 32: 392–398

    Google Scholar 

  • Grignon N, Halpern S, Gojon A, Fragu P (1992)14N and15N imaging by SIMS microscopy in soybean leaves. Biol Cell 74: 143–146

    Google Scholar 

  • Hepler PK, Callaham DA (1993) Calcium ion imaging in plant cells. In: Bailey GW, Rieder CL (eds) Proceedings of the 51st Annual Meeting of the Microscopy Society of America. San Francisco Press, San Fancisco, pp 132–133

    Google Scholar 

  • —, Wayne RO (1985) Calcium and plant development. Annu Rev Plant Physiol 36: 397–439

    Google Scholar 

  • Hindie E, Coulomb B, Beaupain R, Galle P (1992) Mapping the cellular distribution of labelled molecules by SIMS microscopy. Biol Cell 74: 81–88

    PubMed  Google Scholar 

  • Huber DJ (1983) The role of cell wall hydrolases in fruit softening. Hortic Rev 5: 169–219

    Google Scholar 

  • Jarvis MC (1984) Structure and properties of pectin gels in plant cell walls. Plant Cell Environ 7: 153–164

    Google Scholar 

  • - (1992) The structure of pectic gels. In: Sassen MMA, Decksen JWM, Emons AMC, Wolters-Art AMC (eds) Proceedings of the VIth Cell Wall Meeting, Nijmegen, p 26

  • Jauneau A, Morvan C, Lefebvre F, Demarty M, Ripoll C, Thellier M (1992a) Differential extractibility of calcium and pectic substances in different wall regions of epicotyl cells in young flax plants. J Histochem Cytochem 40: 1183–1189

    PubMed  Google Scholar 

  • —, Ripoll C, Rihouey C, Demarty M, Thoiron A, Martini F, Thellier M (1992b) Localisation de Ca et Mg par microscopie ionique analytique dans des plantules de lin: utilisation d'une méthode de précipitation au pyroantimonate de potassium. C R Acad Sci 315: 179–188

    Google Scholar 

  • —, Ripoll C, Verdus MC, Lefebvre F, Demarty M, Thellier M (1994) Imaging the K, Mg, Na and Ca distributions in flax seeds using SIMS microscopy. Bot Acta 107: 81–89

    Google Scholar 

  • Knox JP (1992) Cell adhesion, cell separation and plant morphogenesis. Plant J 2: 137–141

    Google Scholar 

  • Lazof D, Linton RW, Volk RJ, Rufty TW (1992) The application of SIMS to nutrient tracer studies in plant physiology. Biol Cell 74: 127–134

    Google Scholar 

  • —, Goldsmith JG, Suggs C, Ruffy TW, Linton RW (1994) A method for the routine preparation of cryosections from plant tissue: suitability for secondary ion mass spectrometry. J Microsc 176: 99–109

    Google Scholar 

  • Liners F, Van Cutsem P (1992) Distribution of pectic polysaccharides throughout walls of suspension-cultured carrot cells. An immunocytochemical study. Protoplasma 170: 10–21

    Google Scholar 

  • Linton RW, Goldsmith JG (1992) The role of secondary ion mass spectrometry (SIMS) in biological microanalysis: technique comparisons and prospects. Biol Cell 74: 147–160

    PubMed  Google Scholar 

  • Lundgren T, Engström EU, Levi-Setti R, Linde A, Norén JG (1994) The use of the stable isotope44Ca in studies of calcium incorporation into dentin. J Microsc 173: 149–154

    PubMed  Google Scholar 

  • Mentré P, Escaig F (1988) Localization by pyroantiomonate. I. Influence of the fixation on the distribution of calcium and sodium. An approach by analytical ion microscopy. J Histochem Cytochem 36: 48–54

    Google Scholar 

  • Morris ER, Powell DA, Gidley MJ, Rees DA (1982) Conformations and interactions of pectins. I. Polymorphism between gel and solid states of calcium polygalacturonate. J Mol Biol 155: 507–516

    PubMed  Google Scholar 

  • Perring MA, Wilkinson BG (1965) The mineral composition of apples. IV. The radial distribution of chemical constituents in apples, and its significance in sampling for analysis. J Food Sci Agric 16: 535–541

    Google Scholar 

  • Poovaiah BW, Reddy ASN (1993) Calcium and signal transduction in plants. Crit Rev Plant Sci 12: 185–211

    PubMed  Google Scholar 

  • —, Gleen GM, Reddy ASN (1988) Calcium and fruit softening: physiology and biochemistry. Hortic Rev 10: 107–151

    Google Scholar 

  • Powell DA, Morris ER, Gidley JM, Rees DA (1982) Conformations and interactions of pectins. II. Influence of residue sequence on chain association in calcium pectate gels. J Mol Biol 155: 517–531

    PubMed  Google Scholar 

  • Read ND, Allan WTG, Knight H, Knight MR, Malhó R, Russell A, Shacklock PS, Trewavas AJ (1992) Imaging and measurement of cytosolic free calcium in plant and fungal cells. J Microsc 166: 57–86

    Google Scholar 

  • —, Shacklock PS, Knight MR, Trewavas AJ (1993) Imaging calcium dynamics in living plant cells and tissues. Cell Biol Int 17: 111–125

    Google Scholar 

  • Rees DA (1977) Polysaccharides shapes. Chapman and Hall, London

    Google Scholar 

  • Ripoll C, Jauneau A, Lefebvre F, Demarty M, Thellier M (1992) SIMS determination of the distribution of the main mineral cations in the depth of the cuticle and pecto-celluosic wall of epidermal cells of flax stems: problems encountered with SIMS depth profiling. Biol Cell 74: 135–142

    Google Scholar 

  • —, Pariot C, Jauneau A, Verdus MC, Catesson AM, Morvan C, Demarty M, Thellier M (1993) Involvement of sodium in a process of cell differentiation in plants. C R Acad Sci 316: 1433–1437

    Google Scholar 

  • Roland JC, Vian B (1991) General preparation and staining of thin sections. In: Hall JL, Hawes C (eds) Electron microscopy of plant cells. Academic Press, London, pp 1–66

    Google Scholar 

  • Roy S, Vian B, Roland JC (1992) Immunocytochemical study of the deesterification patterns during cell wall autolysis in the ripening of cherry tomato. Plant Physiol Biochem 30: 135–146

    Google Scholar 

  • —, Jauneau A, Vian B (1994a) Analytical detection of calcium ions and immunocytochemical visualization of homogalacturonic sequences in the ripe cherry tomato. Plant Physiol Biochem 32: 1–5

    Google Scholar 

  • —, Conway WS, Watada AE, Sams CE, Pooley CD, Wergin WP (1994b) Distribution of the anionic sites in the cell wall of apple fruit after calcium treatment: quantitation and visualization by a cationic colloidal gold probe. Protoplasma 178: 156–167

    Google Scholar 

  • Schaumann L, Galle P, Ullrich W, Thellier M (1986) Application de la microscopie ionique analytique á l'utilisation des isotopes stables14N et15N comme traceurs, et pour faire l'image de la distribution de l'azote chezLemna gibba L. C R Acad Sci 302: 109–115

    Google Scholar 

  • Thellier M, Ripoll C, Berry JP (1991) Biological applications of secondary ion mass spectrometry. Eur Microsc Anal 11: 9–11

    Google Scholar 

  • Thibault JF, Rinaudo M (1985) Interactions of mono- and divalent counterions with alkali- and enzyme-deesterified pectins in salt free solutions. Biopolymers 24: 2131–2143

    Google Scholar 

  • — — (1986) Chain association of pectic molecules during calciuminduced gelation. Biopolymers 25: 455–468

    Google Scholar 

  • Touchard P, Rippoll C, Morvan C, Demarty M (1987) Ion transport properties of plant cell walls: Ca/Mg selectivity. Food Hydrocolloids 1: 473–475

    Google Scholar 

  • Van Buren JP (1991) Functions of pectin in plant tissue structure and firmness. In: Walter RH (ed) The chemistry and technology of pectin. Academic Press, London, pp 1–22

    Google Scholar 

  • Wick SM, Hepler PK (1982) Selective localization of intracellular Ca2+ with potassium antimonate. J Histochem Cytochem 30: 1190–1201

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. U.S. Department of Agriculture, Horticultural Crops Quality Laboratory, ARS, BARC-West, Bldg. 002, 20705, Beltsville, MD, USA

    S. Roy, W. S. Conway & A. E. Watada

  2. U.S. Department ofAgriculture, Electron Microscopy Laboratory, Agricultural Research Service, Beltsville, Maryland

    S. Roy & W. P. Wergin

  3. Surface and Microanalysis Science Division, National Institute of Standards and Technology, Gaithersburg, Maryland

    G. Gillen

Authors
  1. S. Roy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Gillen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. W. S. Conway
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. E. Watada
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. W. P. Wergin
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Roy, S., Gillen, G., Conway, W.S. et al. Use of secondary ion mass spectrometry to image44calcium uptake in the cell walls of apple fruit. Protoplasma 189, 163–172 (1995). https://doi.org/10.1007/BF01280170

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01280170

Keywords

Search

Navigation