Abstract
Oleosins, which are structural proteins on the surface of intracellular oil bodies, have been found in the sporophytic seeds of angiosperms. Here, we report an oleosin from the female gametophyte of gymnosperm Pinus ponderosa Laws, seed and another oleosin from the male gametophyte of Brassica napus L. With the pine seed gametophyte, we identified two putative oleosins of 15 and 10 kDa, which are similar to the oleosins in angiosperm seeds in terms of their presence in the oil bodies in massive quantity. The complete sequence of the cDNA encoding the gametophytic 15-kDa oleosin was obtained, and it has a predicted amino-acid sequence similar to those of oleosins in angiosperm sporophytic seeds. A Brassica napus pollen cDNA sequence, which was reported earlier, would encode an amino-acid sequence somewhat similar to those of seed oleosins. We tested if the dissimilarity signifies a substantially different oleosin in the Brassica male gametophyte or an analytic error. By direct sequencing of a polymerase chain reaction (PCR)-amplified fragment of genomic DNA, we obtained evidence showing that this reported dissimilarity is likely to have arisen from a sequencing error. Our predicted sequence of the Brassica pollen oleosin has all the structural characteristics of seed oleosins. A phylogenic tree of 20 oleosins, including those from sporophytic and gametophytic tissues of angiosperm and gymnosperm, was constructed based on their amino-acid sequences. We discuss the evolution of oleosins, and conclude that oleosins are ancient proteins with multiple lineages whose root cannot be determined at this time.
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Abbreviations
- PCR:
-
polymerase chain reaction
- TAG:
-
triacylglycerols
References
Aalen, R.B., Ferstad, H-G.O., Linnestad, C., Olsen, O-A. (1994) Transcripts encoding an oleosin and a dormancy related protein are present both in the aleurone layer and in the embryo of developing barley (Hordeum vulgare L.) seeds. Plant J., in press
Brackhaus, R.A., Cornish, K., Chen, S.F., Huang, D.S., Bess, V.H. (1991) Purification and characterization of an abundant rubber particle protein from guayule. Phytochemistry 30, 2493–2497
Ching, T.M. (1973) Glyoxysomes in megagametophyte of germinating ponderosa pine seeds. Plant Physiol. 46, 475–482
Cummins, I., Murphy, D.J. (1992) cDNA sequence of a sunflower oleosin and transcript tissue specificity. Plant Mol. Biol. 19, 873–876
Dayhoff, M.O. (1979) Atlas of protein sequence and structure, vol. 5, supplement 3, 1978. National Biomedical Research Foundation, Washington, DC
Durzan, D.J., Mia, A.J., Ramaiah, P.K. (1971) The metabolism and subcellular organization of the jack pine embryo (Pinus banksiana) during germination. Can. J. Bot. 49, 927–938
Felsenstein, J. (1993) PHYLIP (Phylogenetic Inference Package) version 3.5c. Distributed by the author. Dept. of Genetics, Univ. of Washington, Seattle
Frohman, M.A., Dush, M.K., Martin, G.R. (1988) Rapid production of full-length cDNAs from rare transcripts; amplification using a single gene-specific oligonucleotide primer. Proc. Natl. Acad. Sci. USA 85, 8998–9002
Genetics Computer Group (1991) Program Manual for the GCG Package, Version 7. Madison, Wis.
Hatzopoulos, P., Franz, G., Choy, L., Sung, R.Z. (1990) Interaction of nuclear factors with upstream sequences of a lipid body membrane protein gene from carrot. Plant Cell 2, 457–467
Huang, A.H.C. (1992) Oil bodies and oleosins in seeds. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43, 177–200
Huang, A.H.C. (1993) Oil bodies in maize and other species. In: Biochemistry and molecular biology of membrane and storage lipids of plants, pp. 215–227, Murata, N., Somerville, C., eds. Am. Soc. Plant Physiol., Rockville, Md.
Hughes, D.W., Wang, H.Y.C., Galau, G.A. (1993) Cotton (Gossypium hirsutum) MatP6 and MatP7 oleosin genes. Plant Physiol. 101, 697–698
Kalinski, A., Loer, D.S., Weisemann, J.M., Mathews, B.F., Herman, E.M. (1991) Isoforms of soybean seed oil body membrane protein 24 kDa oleosin are encoded by closely related cDNAs. Plant Mol. Biol. 17, 1095–1098
Keddie, J.S., Edwards, E.W., Gibbons, T., Shaw, C.H., Murphy, D.J. (1992a) Sequence of an oleosin cDNA from Brassica napus. Plant Mol. Biol. 19, 1079–1083
Keddie, J.S., Hubner, G., Slocombe, S.P., Jarvis, R.P., Cummins, I., Edwards, E.W., Shaw, C.H., Murphy, D.J. (1992b) Cloning and characterization of an oleosin gene from Brassica napus. Plant Mol. Biol. 19, 443–453
Lammer, D.L., Gifford, D.J. (1989) Lodgepole pine seed germination. II. The seed proteins and their mobilization in the megagametophyte and embryo axis. Can. J. Bot. 67, 2544–2551
Lee, K., Huang, A.H.C. (1991) Genomic nucleotide sequence of a Brassica napus 20 kDa oleosin gene. Plant Physiol. 96, 1395–1397
Murphy, D.J. (1993) Biochemical and molecular regulation of storage product formation in oil seeds. In: Biochemistry and molecular biology of membrane and storage lipids of plants, pp. 228–235, Murata, N., Somerville, C., eds. Am. Soc. Plant Physiol., Rockville, Md.
Murphy, D.J., Keen, J.N., O'Sullivan, J.N., Au, D.M.Y., Edwards, E.W., Jackson, P.J., Cummins, I., Gibbons, T., Shaw, C.H., Ryan, A.J. (1991) A class of amphipathic proteins associated with lipid storage bodies plants. Possible similarities with animal serum apolipoproteins. Biochim. Biophys. Acta 1088, 86–94
Pearson, W. (1990) Rapid and sensitive sequence comparison with FASTP and FASTA. Methods Enzymol. 183, 63–98
Platt-Aloia, K.A., Thomson, W.W. (1981) Ultrastructure of the mesocarp of mature avocado fruit and changes associated with ripening. Ann. Bot. 48, 451–465
Qu, R., Huang, A.H.C. (1990) Oleosin KD18 on the surface of oil bodies in maize. Genomic and cDNA sequences and the deduced protein structure. J. Biol. Chem. 265, 2238–2243
Roberts, M.R., Robson, F., Foster, G.D., Draper, J., Scott, R.J. (1991) A Brassica napus mRNA expressed specifically in developing microspores. Plant Mol. Biol. 17, 295–299
Roberts, M.R., Hodge, R., Ross, J.H.E., Sorensen, A., Murphy, D.J., Draper, J., Scott, R. (1993) Characterization of a new class of oleosins suggests a male gametophyte-specific lipid storage pathway. Plant J. 3, 629–636
Saitou, N., Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425
Stanley, R.G., Linskens, H.F. (1974) Pollen. Biology, Biochemistry, Management. Springer-Verlag, Berlin
Tzen, J.T.C., Huang, A.H.C. (1992) Surface structure and properties of plant seed oil bodies. J. Cell. Biol. 117, 327–335
Tzen, J.T.C., Lai, Y.K., Chan, K.L., Huang, A.H.C. (1990) Oleosin isoforms of high and low molecular weights are present in the oil bodies of diverse seed species. Plant Physiol. 94, 1282–1289
Tzen, J.T.C., Lie, G.C., Huang, A.H.C. (1992) Characterization of the charged components and their topology on the surface of plant seed oil bodies. J. Biol. Chem. 267, 15626–15634
Tzen, J.T.C., Cao, Y.Z., Laurent, P., Ratnayake, C., Huang, A.H.C. (1993) Lipids, proteins, and structure of seed oil bodies from diverse species. Plant Physiol. 101, 267–276
van Rooijen, G.J.H., Terning, L.I., Moloney, M.M. (1991) Nucleotide sequence of an Arabidopsis thaliana oleosin gene. Plant Mol. Biol. 18, 1177–1179
Vance, V.B., Huang, A.H.C. (1987) The major protein from lipid bodies of maize: characterization and structure based on cDNA cloning. J. Biol. Chem. 262, 11275–11279
Wang, S.M., Huang, A.H.C. (1987) Biosynthesis of lipase in the scutellum of maize kernel. J. Biol. Chem. 262, 2270–2274
Yatsu, L.Y., Jacks, T.J. (1972) Spherosome membranes. Half unitmembranes. Plant Physiol. 49, 937–943
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This work was supported by USDA grant 91-01439 (AHCH). We thank Dr. Mike Lassner of Calgene, Inc., (Davis, Calif., USA) for providing us with the unpublished jojoba oleosin amino acid sequence.
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Lee, K., Bih, F.Y., Learn, G.H. et al. Oleosins in the gametophytes of Pinus and Brassica and their phylogenetic relationship with those in the sporophytes of various species. Planta 193, 461–469 (1994). https://doi.org/10.1007/BF00201827
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DOI: https://doi.org/10.1007/BF00201827