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Ontogeny of glyoxysomes in maturing and germinated cotton seeds—a morphometric analysis

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Abstract

Morphometric procedures were used with light and electron microscopy to examine glyoxysome number, volume, shape and distribution as well as mesophyll cell volume, in cotyledons of mature (50 d postanthesis), imbibed (5h) and germinated (24 and 37 h) cotton (Gossypium hirsutum L.) seeds. Additionally, activities of five glyoxysomal marker enzymes in cotyledon extracts were assayed at each of the above ages. Cell volume was determined from photomicrographs of Epon-embedded sections by the point-counting procedure. Analysis of variance showed that cell volume was not different among the tissue segments studied. Glyoxysomes were cytochemically stained for catalase (EC 1.11.1.6) activity with the 3,3′-diaminobenzidine-tetrahydrochloride procedure. Analyses involving both phase and electron microscopy, and two separate sterologic calculations for determining the number of glyoxysomes per cell, indicate that glyoxysomes are numerous in mature seeds, persist through desiccation and imbibition, then increase dramatically in volume (seven fold) but not number (a maximum of 1.5-fold), when enzyme activities increase two to six times (depending on the enzyme). During the entire period of increase in glyoxysomal enzyme activities, no ultrastructural evidence was found for glyoxysome formation or destruction. Our data, in contrast to some proposals in the literature, indicate that cottonseed glyoxysomes form during seed maturation, then develop following seed imbibition into pleomorphic organelles by posttranslational accumulation of proteins from the cytosol and transfer of membrane components probably from the endoplasmic reticulum.

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Abbreviations

DAB:

3,3′-diaminobenzidine tetrahydrochloride

DPA:

days postanthesis

ER:

endoplasmic reticulum

References

  • Becker, W.M., Leaver, C.J., Weir, E.M., Riezman, H. (1978) Regulation of glyoxysomal enzymes during germination of cucumber. I. Developmental changes in cotyledonary protein, RNA and enzyme activities during germination. Plant Physiol. 62, 542–549

    Google Scholar 

  • Beevers, H. (1979) Microbodies in higher plants. Annu. Rev. Plant Physiol. 30, 159–193

    Google Scholar 

  • Choinski, J.S., Jr., Trelease, R.N. (1978) control of enzyme activities in cotton cotyledons during maturation and germination. II. Glyoxysomal enzyme development in embryos. Plant Physiol. 62, 141–145

    Google Scholar 

  • Choinski, J.S., Jr., Trelease, R.N., Doman, D.C. (1981) Control of enzyme activities in cotton cotyledons during maturation and germination. III. In-vitro embryo development in the presence of abscisic acid. Planta 152, 428–435

    Google Scholar 

  • De Hoff, R.T., Rhines, F.N. (1961) Determination of the number of particles per unit volume from measurements made on random plane sections: the general cylinder and the ellipsoid. Trans. Am. Inst. Mech. Eng. 221, 975–980

    Google Scholar 

  • Doman, D.C., Trelease, R.N. (1983) Immunocytochemistry of isocitrate lyase in maturing and germinated cottonseeds (Abstr.). Plant Physiol. 72, Suppl., 53

  • Frevert, J., Köller, W., Kindl, H. (1980) Occurrence and biosynthesis of glyoxysomal enzymes in ripening cucumber seeds. Hoppe-Seyler's Z. Physiol. Chem. 361, 1557–1565

    Google Scholar 

  • Fringes, B., Reith, A., Riede, U.N. (1982) Peroxisome biogenesis in rat liver during adaptation to mild hyperthyroidism: a morphometric/stereologic study by electron microscopy. Ann. N.Y. Acad. Sci. 386, 514–518

    Google Scholar 

  • Gerhardt, B.P., Beevers, H. (1970) Developmental studies on glyoxysomes in Ricinus endosperm. J. Cell Biol. 44, 94–102

    Google Scholar 

  • Gruber, P.J., Trelease, R.N., Becker, W.M., Newcomb, E.H. (1970) A correlative ultrastructural and enzymatic study of cotyledonary microbodies following germination of fat-storing seeds. Planta 93, 269–288

    Google Scholar 

  • Huang, A.H.C., Trelease, R.N., Moore, T.S. Jr. (1983) Plant peroxisomes. Academic Press, New York

    Google Scholar 

  • Kindl, H. (1982a) Glyoxysome biogenesis via cytosolic pools in cucumber. Ann. N.Y. Acad. Sci. 386, 314–328

    Google Scholar 

  • Kindl, H. (1982b) The biosynthesis of microbodies (peroxisomes, glyoxysomes). Int. Rev. Cytol. 80, 193–229

    Google Scholar 

  • Kindl, H., Schiefer, S., Löffler, H.-G. (1980) Occurrence and biosynthesis of catalase at different stages of seed maturation. Planta 138, 199–207

    Google Scholar 

  • Köller, W., Frevert, J., Kindl, H. (1979a) Incomplete glyoxysomes appearing at a late stage of maturation of cucumber seeds. Z. Naturforsch. Teil C 34, 1232–1236

    Google Scholar 

  • Köller, W., Frevert, J., Kindl, H. (1979b) Albumins, glyoxysomal enzymes and globulins in dry seeds of Cucumis sativus: qualitative and quantitative analysis. Hoppe-Seyler's Z. Physiol. Chem. 360, 167–176

    Google Scholar 

  • Lazarow, P.B., Robbi, M., Fujiki, Y., Wong, L. (1982) Biogenesis of peroxisomal proteins in vivo and in vitro. Ann. N.Y. Acad. Sci. 386, 285–300

    Google Scholar 

  • Lord, J.M. (1980) Biogenesis of peroxisomes and glyoxysomes. Subcell. Biochem. 7, 171–211

    Google Scholar 

  • Lord, J.M., Roberts, L.M. (1983) Formation of glyoxysomes. Int. Rev. Cytol. Suppl., 15, 115–156

    Google Scholar 

  • Lott, J.N.A. (1970) Changes in the cotyledons of Cucurbita maxima during germination. I. General characteristics. Can. J. Bot. 48, 2227–2231

    Google Scholar 

  • Miernyk, J.A., Thomas, J., Trelease, R.N. (1982) A novel role for peroxisomes in oilseed development. Ann. N.Y. Acad. Sci. 386, 426–429

    Google Scholar 

  • Miernyk, J.A., Trelease, R.N. (1981a) Control of enzyme activities in cotton cotyledons during maturation and germination. IV. β-Oxidation. Plant Physiol. 67, 341–346

    Google Scholar 

  • Miernyk, J.A., Trelease, R.N. (1981b) Role of malate synthase in citric acid synthesis by maturing cotton embryos: a proposal. Plant Physiol. 67, 875–881

    Google Scholar 

  • Miernyk, J.A., Trelease, R.N., Choinski, J.S. Jr. (1979) Malate synthase activity in cotton and other ungerminated oilseeds. A survey. Plant Physiol. 63, 1068–1071

    Google Scholar 

  • Mollenhauer, H.H., Totten, C. (1970) Studies on seeds. V. Microbodies, glyoxysomes, and ricinosomes in castor bean endosperm. Plant Physiol. 46, 794–799

    Google Scholar 

  • Steel, R.G.D., Torrie, J.H. (1980) Principles and procedures of statistics. A biometrical approach, 2nd edn. McGraw-Hill, New York

    Google Scholar 

  • Tanaka, A., Osumi, M., Fukui, S. (1982) Peroxisomes of alkane-grown yeast: fundamental and practical aspects. Ann. N.Y. Acad. Sci. 386, 183–199

    Google Scholar 

  • Trelease, R.N., Becker, W.M., Gruber, P.J., Newcomb, E.H. (1971) Microbodies (glyoxysomes and peroxisomes) in cucumber cotyledons. Correlative biochemical and ultrastructural study in light- and dark-grown seedlings. Plant Physiol. 48, 461–475

    Google Scholar 

  • van Dijken, J.P., Veehuis, M., Harder, W. (1982) Peroxisomes of methanol-grown yeasts. Ann. N.Y. Acad. Sci. 386, 200–216

    Google Scholar 

  • Vigil, E.L. (1970) Cytochemical and developmental changes in microbodies (glyoxysomes) and related organelles of castor bean endosperm. J. Cell Biol. 46, 435–454

    Google Scholar 

  • Walbot, V., Dure, L.S. III (1976) Developmental biochemistry of cotton seed embryogenesis and germination. VII. Characterization of the cotton genome. J. Mol. Biol. 101, 503–536

    Google Scholar 

  • Wanner, G., Vigil, E.L., Theimer, R.R. (1982) Ontogeny of microbodies (glyoxysomes) in cotyledons of dark-grown watermelon (Citrullis vulgaris Scharad.) seedlings. Ultrastructural evidence. Planta 156, 314–325

    Google Scholar 

  • Weibel, E.R. (1979) Stereologic methods — practical methods for biological morphometry, vol. 1 Academic press, New York London

    Google Scholar 

  • Weibel, E.R., Gomez, D.M. (1962) A principle for counting tissue structures on random sections. J. Appl. Physiol. 17, 343–348

    Google Scholar 

  • Weidner, M. (1967) Der DNS-Gehalt von Kotyledon und Hypokotyl des Senfkeimlings (Sinapsis alba L.) bei der phytochromgesteuerten Photomorphogenese. Planta 75, 94–98

    Google Scholar 

  • Weir, E.M., Riezman, H., Grieneberger, J.-M., Becker, W.M., Leaver, C.J. (1980) Regulation of glyoxysomal enzymes during germination of cucumber. Temporal changes in translatable mRNAs for isocitrate lyase and malate synthase. Eur. J. Biochem. 112, 469–477

    Google Scholar 

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Authors and Affiliations

  1. Department of Botany and Microbiology, Arizona State University, 85287, Tempe, AZ, USA

    Christine M. Kunce, Richard N. Trelease & Diane C. Doman

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  1. Christine M. Kunce
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  2. Richard N. Trelease
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  3. Diane C. Doman
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Kunce, C.M., Trelease, R.N. & Doman, D.C. Ontogeny of glyoxysomes in maturing and germinated cotton seeds—a morphometric analysis. Planta 161, 156–164 (1984). https://doi.org/10.1007/BF00395476

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  • DOI: https://doi.org/10.1007/BF00395476

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