Investigation of the glyoxysome-peroxisome transition in germinating cucumber cotyledons using double-label immunoelectron microscopy

Microbodies in the cotyledons of cucumber seedlings perform two successive metabolic functions during early postgerminative development. During the first 4 or 5 d, glyoxylate cycle enzymes accumulate in microbodies called glyoxysomes. Beginning at about day 3, light-induced activities of enzymes involved in photorespiratory glycolate metabolism accumulate rapidly in microbodies. As the cotyledonary microbodies undergo a functional transition from glyoxysomal to peroxisomal metabolism, both sets of enzymes are present at the same time, either within two distinct populations of microbodies with different functions or within a single population of microbodies with a dual function. We have used protein A-gold immunoelectron microscopy to detect two glyoxylate cycle enzymes, isocitrate lyase (ICL) and malate synthase, and two glycolate pathway enzymes, serine:glyoxylate aminotransferase (SGAT) and hydroxypyruvate reductase, in microbodies of transition-stage (day 4) cotyledons. Double-label immunoelectron microscopy was used to demonstrate directly the co-existence of ICL and SGAT within individual microbodies, thereby discrediting the two-population hypothesis. Quantitation of protein A- gold labeling density confirmed that labeling was specific for microbodies. Quantitation of immunolabeling for ICL or SGAT in microbodies adjacent to lipid bodies, to chloroplasts, or to both organelles revealed very similar labeling densities in these three categories, suggesting that concentrations of glyoxysomal and peroxisomal enzymes in transition-stage microbodies probably cannot be predicted based on the apparent associations of microbodies with other organelles.

• Publication year

  1985

• Venue

  Journal of Cell Biology

• Publication date

  1985-10-01

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1083/JCB.101.4.1288PMID 3930507PMCID 2113938
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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  1983influential reference
• Purification and characterization of hydroxypyruvate reductase from cucumber cotyledons.

  1983influential reference
• Regulation of Glyoxysomal Enzymes during Germination of Cucumber: 3. IN VITRO TRANSLATION AND CHARACTERIZATION OF FOUR GLYOXYSOMAL ENZYMES.

  1980cited by this paper
• Microbodies in Higher Plants

  1979influential reference
• Regulation of Glyoxysomal Enzymes during Germination of Cucumber: I. Developmental Changes in Cotyledonary Protein, RNA, and Enzyme Activities during Germination.

  1978cited by this paper
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  1978influential reference
• Coloidal gold, ferritin and peroxidase as markers for electron microscopic double labeling lectin techniques.

  1978cited by this paper
• Apparent Catalase Synthesis in Sunflower Cotyledons during the Change in Microbody Function: A Mathematical Approach for the Quantitative Evaluation of Density-labeling Data.

  1978cited by this paper
• Encyclopedia of plant physiology, New series

  1978cited by this paper
• DENSITY LABELLING DURING MICROBODY DEVELOPMENT IN COTYLEDONS

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  1968cited by this paper
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