Advertisement

Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Lipid-body lipoxygenase is expressed in cotyledons during germination prior to other lipoxygenase forms

  • 63 Accesses

  • 16 Citations

Abstract

Lipid bodies are degraded during germination. Whereas some proteins, e.g. oleosins, are synthesized during the formation of lipid bodies of maturating seeds, a new set of proteins, including a specific form of lipoxygenase (LOX; EC 1.13.11.12), is detectable in lipid bodies during the stage of fat degradation in seed germination. In cotyledons of cucumber (Cucumis sativus L.) seedlings at day 4 of germination, the most conspicuous staining with anti-LOX antibodies was observed in the cytosol. At very early stages of germination, however, the LOX form present in large amounts and synthesized preferentially was the lipid-body LOX. This was demonstrated by immunocytochemical staining of cotyledons from 1-h and 24-h-old seedlings: the immunodecoration of sections of 24-h-old seedlings with anti-LOX antiserum showed label exclusively correlated with lipid bodies of around 3 μm in diameter. In accordance, the profile of LOX protein isolated from lipid bodies during various stages of germination showed a maximum at day 1. By measuring biosynthesis of the protein in vivo we demonstrated that the highest rates of synthesis of lipid-body LOX occurred at day 1 of germination. The early and selective appearance of a LOX form associated with lipid bodies at this stage of development is discussed.

This is a preview of subscription content, log in to check access.

Abbreviations

DAPI:

4,6-diamidino-2-phenylindole

DIC:

differential interference contrast

FITC:

fluorescein-5-isothiocyanate

LOX:

lipoxygenase

References

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

  2. Brash AR, Ingram CD, Harris TM (1987) Analysis of a specific oxygenation reaction of soybean lipoxygenase-1 with fatty acids esterified in phospholipids. Biochemistry 26: 5465–5471

  3. Chapman KD, Trelease RN (1991) Acquisition of membrane lipids by differentiating glyoxysomes — role of lipid bodies. J Cell Biol 115:995–1007

  4. Choi D, Bostock RM, Avdiushko S, Hildebrand DF (1994) Lipidderived signals that discriminate wound- and pathogen-responsive isoprenoid pathways in plants — methyl jasmonate and the fungal elicitor arachidonic acid induce different 3-hydroxy-3-methylglutaryl coenzyme A reductase genes and antimicrobial isoprenoids in Solanum tuberosum L. Proc Natl Acad Sci USA 91: 2329–2333

  5. Feussner I (1993) Vergleich pflanzlicher Lipoxygenasen unter besonderer Berücksichtigung der Biosynthese einer Lipoxygenase aus Lipidkörpern. PhD thesis, Philipps-Universität, Marburg, Germany

  6. Feussner I, Kindl H (1992) A lipoxygenase is the main lipid body protein in cucumber and soybean cotyledons during the stage of triglyceride mobilization. FEBS Lett 298: 223–225

  7. Feussner I, Kindl H (1994) Particulate and soluble lipoxygenase isoenzymes — comparison of molecular and enzymatic properties. Planta 194: 22–28

  8. Gardner HW (1991) Recent investigations into the lipoxygenase pathway of plants. Biochim Biophys Acta 1084: 221–239

  9. Gardner HW, Hamberg M (1993) Oxygenation of (3Z)-nonenal to (2E)-4-hydroxy-2-nonenal in the broad bean (Vicia faba L.). J Biol Chem 268: 6971–6977

  10. Gerlach D (1984) Botanische Mikrotechnik. Thieme, Stuttgart, New York

  11. Hamberg M (1993) Pathways in the biosynthesis of oxylipins in plants. J Lipid Med 6: 375–384

  12. Hara I, Matsubara H (1980) Pumpkin (Cucurbita sp.) seed globulin. VII. Immunofluorescent study on protein bodies in ungerminated and germinating cotyledon cells. Plant Cell Physiol 21: 247–54

  13. Hatanaka A, Kajiwara T, Harada T (1975) Biosynthetic pathway of cucumber alcohol: trans-2,cis-6-nonadienol via cis-3,cis-6-nonadienal. Phytochemistry 14: 2589–92

  14. Hildebrand DF (1989) Lipoxygenases. Physiol Plant 76: 249–253

  15. Huang AHC (1992) Oil bodies and oleosins in seeds. Annu Rev Plant Physiol Plant Mol Biol 43: 177–200

  16. Huang AHC, Trelease RN, Moore TSJ (1983) Plant peroxisomes. Academic Press, New York

  17. Kara UAK, Kindl H (1982) Membranes of protein bodies. I. Isolation from cotyledons of germinating cucumber seeds. Eur J Biochem 121: 533–538

  18. Kindl H (1987) β-Oxidation of fatty acids by specific organelles. In: Stumpf PK, Conn EE (eds) The biochemistry of plants. Vol 9. Lipids: Structure and function. Academic Press, London, pp 31–52

  19. Kyhse-Andersen J (1984) Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J Biochem Biophys Methods 10: 203–209

  20. Matsui K, Irie M, Kajiwara T, Hatanaka A (1992) Developmental changes in lipoxygenase activity in cotyledons of cucumber seedlings. Plant Sci 85: 23–32

  21. Murphy DJ (1990) Storage lipid bodies in plants and other organisms. Prog Lipid Res 29: 299–324

  22. Murphy DJ (1993) Structure, function and biogenesis of storage lipid bodies and oleosins in plants. Prog Lipid Res 32: 247–280

  23. Nellen A, Rojahn B, Kindl H (1995) Plasma membrane localized forms of lipoxygenase and their induction by methyl jasmonate. Z Naturforsch 50c: 29–36

  24. Radetzky R, Feussner I, Theimer RR, Kindl H (1993) Transient occurrence of lipoxygenase and glycoprotein gp49 in lipid bodies during fat mobilization in anise seedlings. Planta 191: 166–172

  25. Schewe T, Kühn H (1991) Do 15-lipoxygenases have a common biological role? Trends Biochem Sci 16: 369–373

  26. Scriven R, Meloan CE (1984) (E,Z)-2,6-nonadien-1-al and (E)-2-nonen-1-al present in crushed cucumbers are natural repellents for the American cockroach (Periplaneta americana). Ohio J Sci 84: 82–5

  27. Sekiya J, Numa S, Kajiwara T, Hatanaka A (1976) Biosynthesis of leaf alcohol. Formation of 3Z-hexenal from linolenic acid in chloroplasts of Thea sinensis leaves. Agr Biol Chem 40: 185–190

  28. Sembdner G, Parthier B (1993) The biochemistry and the physiological and molecular actions of jasmonates. Annu Rev Plant Physiol Plant Mol Biol 44: 569–589

  29. Siedow JN (1991) Plant lipoxygenase: structure and function. Annu Rev Plant Physiol Plant Mol Biol 42: 145–188

  30. Song WC, Funk CD, Brash AR (1993) Molecular cloning of an allene oxide synthase — a cytochrome-P450 specialized for the metabolism of fatty acid hydroperoxides. Proc Natl Acad Sci USA 90: 8519–8523

  31. Sturm A, Schwennesen K, Kindl H (1985) Isolation of proteins assembled in lipid body membranes during fat mobilization in cucumber cotyledons. Eur J Biochem 150: 461–468

  32. Tranbarger TJ, Franceschi VR, Hildebrand DF, Grimes HD (1991) The soybean 94-kilodalton vegetative storage protein is a lipoxygenase that is localized in paraveinal mesophyll cell vacuoles. Plant Cell 3: 973–987

  33. Trelease RN, Becker WM, Gruber PJ, Newcomb EH (1971) Microbodies (glyoxysomes and peroxisomes) in cucumber cotyledons. Correlative biochemical and ultrastructural study in light- and dark-grown seedlings. Plant Physiol 48: 461–475

  34. Vance VB, Huang AHC (1988) Expression of lipid body protein gene during maize seed development. J Biol Chem 263: 1476–1481

  35. Van Lammeren AAM, Keijzer CJ, Willemse MTM, Kieft H (1985) Structure and function of the microtubular cytoskeleton during pollen development in Gasteria verrucosa (Mill.) H Duval Planta 65: 1–10

  36. Vernooy-Gerritsen M, Bos ALM, Veldink GA, Vliegenthart JFG (1983) Localization of lipoxygenases 1 and 2 in germinating soybean seeds by an indirect immunofluorescence technique. Plant Physiol 73: 262–267

  37. Vernooy-Gerritsen M, Leunissen JLM, Veldink GA, Vliegenthart JFG. (1984) Intracellular localization of lipoxygenases-1 and -2 in germinating soybean seeds by indirect labeling with protein A-colloidal gold complexes. Plant Physiol 76: 1070–1079

  38. Vick BA, Zimmerman DC (1987) Oxidative systems for modification of fatty acids: the lipoxygenase pathway. In: Stumpf PK and Conn EE (eds) The biochemistry of plants. Vol 9. Lipids: structure and function, Academic Press, London pp 53–90

  39. Wang S, Huang AHC (1987) Biosynthesis of lipase in the scutellum of maize kernel. J Biol Chem 262: 2270–2274

  40. Wanner G, Vigil EL, Theimer RR (1982) Ontogeny of microbodies (glyoxysomes) in cotyledons of dark grown watermelon (Citrullus vulgaris Schrad.) seedlings. Planta 156: 314–325

  41. Wardale DA, Lambert EA (1980) Lipoxygenase from cucumber fruit: localization and properties. Phytochem 19: 1013–1016

Download references

Author information

Additional information

This work was financially supported by the Deutsche Forschungsgemeinschaft, SFB 286 (I.F., A.N., H.K.) and SFB 363 (B.H., C.W.).

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Feussner, I., Hause, B., Nellen, A. et al. Lipid-body lipoxygenase is expressed in cotyledons during germination prior to other lipoxygenase forms. Planta 198, 288–293 (1996). https://doi.org/10.1007/BF00206255

Download citation

Key words

  • Cucumis
  • Germination
  • Lipid body (immunocytochemical staining)
  • Lipoxygenase
  • Protein synthesis (in vivo)