519
Views
9
CrossRef citations to date
0
Altmetric
Original Articles

Molecular cloning and root specific expression of secretory acid phosphatase from phosphate deficient lupin (Lupinus albus L.)

, , , , , , , & show all
Pages 427-437 | Received 13 Sep 1999, Accepted 21 Feb 2000, Published online: 04 Jan 2012

Abstract

During the growth of lupin (Lupinus albus L.) plants, a shortage of phosphate induces the secretion of acid phosphatase (APase) from their roots. We have already isolated and characterized the lasap1 cDNA clone for an APase from phosphate-deficient roots. In this paper, we report on an another cDNA clone, designated as lasap2, encoding secretory APase (S-APase) from phosphate-deficient lupin roots. The lasap2 cDNA consisted of 1,541 bp and had an open reading frame composed of 462 amino acid residues with a signal peptide of 34 residues. Several amino acid sequences of purified lupin S-APase were completely contained in the deduced amino acid sequence (LASAP2). The mature LASAP2 was highly hydrophilic, while the signal peptide was highly hydrophobic. The PSORT prediction program indicated that the mature LASAP2 might be secreted from cells. The primary sequence of LASAP2 shared about 70% homology with that of purple APase from germinating seeds of kidney bean as well as LASAPl. RT-PCR and Western blot analyses revealed that the accumulation of mRNAs and the corresponding proteins for S-APase encoded by lasap2 was induced only in roots under phosphate-deficient conditions, while it was assumed that the LASAP1 hydrolyzed phosphate ester compounds which reached the root surfaces or were released from old organs to the apoplastic space.

Abbreviations

APase=

acid phosphatase

S-APase=

secretory acid phosphatase

References

  • Altschul , S.F. , Gish , W. , Miller , W. , Myers , E.W. and Lipman , D.J. 1990 . Basic local alignment search tool . J. Mol. Biol. , 215 : 403 – 410 .
  • Bairoch , A. , Bucher , P. and Hofmann , K. 1997 . The PROSITE database, its status in 1997 . Nucleic Acids Res. , 25 : 217 – 221 .
  • Beck , J.L. , McConachie , L.A. , Summors , A.C. , Arnold , W.N. , Dejersey , J. and Zerner , B. 1986 . Properties of a purple phosphatase from red kidney bean: A zinc-iron metalloenzyme . Biochim. Biophys. Acta , 869 : 61 – 68 .
  • Bhargawa , R. and Sachar , R.C. 1987 . Induction of acid phosphatase in cotton seedlings: Enzyme purification, subunit structure and kinetic properties . Phytochemistory , 26 : 1293 – 1297 .
  • Bieleski , R.L. and Johnson , P.N. 1972 . The external location of phosphatase activity in phosphorus-deficient Spirodela oligorrhiza . Aust. J. Biol. Sci. , 25 : 707 – 720 .
  • Biswass , T.K. and Cundiff , C. 1991 . Multiple forms of acid phosphatase in germinating seeds of Vigna sinensis . Phytochemistry , 30 : 2119 – 2125 .
  • Bosse , D. and Köck , M. 1998 . Influence of phosphate starvation on phosphohydrolases during development of tomato seedlings . Plant Cell Environ. , 21 : 325 – 332 .
  • Bucher , P. and Bairoch , A. 1994 . “ A generalized profile syntax for biomolecular sequences motifs and its function in automatic sequence interpretation ” . In Proceedings 2nd International Conference on Intelligent Systems for Molecular Biology Edited by: Altman , R. , Brutlag , D. , Karp , P. , Lathrop , R. and Searls , D. 53 – 61 . In, Ed.
  • Duff , S.M.G. , Sarath , G. and Plaxton , W.C. 1994 . The role of acid phosphatases in plant phosphorus metabolism . Physiol. Plant. , 90 : 791 – 800 .
  • Gardner , W.K. 1983 . The aquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil/root interface in enhanced . Plant Soil , 70 : 107 – 124 .
  • Gibson , D.M. and Ullah , A.H.J. 1988 . Purification and characterization of phytase from cotyledons of germinating soybean seeds . Arch. Biochem. Biophys. , 260 : 503 – 513 .
  • Gish , W. and States , D.J. 1993 . Identification of protein coding regions by database similarity search . Nat. Genet. , 3 : 266 – 272 .
  • Hall , J.L. and Davie , C.A.M. 1971 . Localization of acid hydrolase activity in Zea mays L. root tips . Ann. Bot. , 35 : 849 – 855 .
  • Haraguchi , H. , Yamauchi , D. and Minamikawa , T. 1990 . Multiple forms of acid phosphatase in cotyledons of Vigna mungo seedlings: Immunological detection and quantitation . Plant Cell Physiol. , 31 : 917 – 923 .
  • Klabunde , T. , Stahl , B. , Suerbaum , R. , Hahner , S. , Karas , M. , Hillenkamp , F. , Krebs , B. and Witzel , H. 1994 . The amino acid sequence of the red kidney bean Fe(III)-Zn(II) purple acid phosphatase . Eur. J. Biochem. , 226 : 369 – 375 .
  • Li , M. , Shinano , T. and Tadano , T. 1997 . Distribution of exudates of lupin roots in the rhizosphere under phosphorus deficient conditions . Soil Sci. Plant Nutr. , 43 : 237 – 245 .
  • Li , M. and Tadano , T. 1996 . Comparison of characteristics of acid phosphatases secreted from roots of lupin and tomato . Soil Sci. Plant Nutr. , 42 : 753 – 763 .
  • MacRae , W.D. , Buxton , F.P. , Sibley , S. , Garven , S. , Gwynne , D.I. , Davies , R.W. and Arst , H.N. 1988 . A phosphate-repressible acid phosphatase gene from Aspergillus niger: Its cloning, sequencing and transcriptional analysis . Gene , 71 : 339 – 348 .
  • Morita , N. , Nakazato , H. , Okuyama , H. , Kim , Y. and Thompson , G.A. 1996 . Evidence for a glycosylinositolphospholipid-anchored alkaline phosphatase in the aquatic plant Spirodela oligorrhiza. . Biochim. Biophys. Acta , 1290 : 53 – 62 .
  • Mullaney , E.J. , Daly , C.B. , Ehrlich , K.C. and Ullah , A.H.J. 1995 . The Aspergillus niger (ficuum) aphA gene encodes a pH 6.0-optimum acid phosphatase . Gene , 162 : 117 – 121 .
  • Mullaney , E.J. and Ullah , A.HJ. 1998 . Conservation of the active site motif in Aspergillus niger (ficuum) pH 6.0 optimum acid phosphatase and kidney bean purple acid phosphatase . Biochem. Biophys. Res. Commun. , 243 : 471 – 473 .
  • Murashige , T. and Skoog , F. 1962 . A revised medium for rapid growth and bio-assays with tobacco tissue cultures . Physiol. Plant. , 15 : 473 – 497 .
  • Nakai , K. and Kanehisa , M. 1992 . A knowledge base for predicting protein localization sites in eukaryotic cells . Genomics , 14 : 897 – 911 .
  • Nakazato , H. , Okamoto , T. , Ishikawa , K. and Okuyama , H. 1997 . Purification and characterization of phosphatase inducibly synthesized in Spirodela oligorrhiza grown under phosphate-deficient conditions . Plant Physiol. Biochem. , 35 : 437 – 446 .
  • Nakazato , H. , Okamoto , T. , Nishikoori , M. , Washio , K. , Morita , N. , Haraguchi , K. , Thompson , G.A. and Okuyama , H. 1998 . The glycosylphosphatidylinositol-anchored phosphatase from Spirodela oligorrhiza is a purple acid phosphatase . Plant Physiol. , 118 : 1015 – 1020 .
  • Okuda , S. , Kaneko , J. , Ogawa , T. , Yamaguchi , T. , Izaki , K. and Takahashi , H. 1987 . Increase in enzyme activities in embryonic axes of soybean seeds during germination . Agric. Biol. Chem. , 51 : 109 – 113 .
  • Oparka , K.J. and Johnson , R.P.C. 982 . Acid phosphatase activity in intercellular spaces in roots of Nymphoides peltata (S.G. Gmel) O. Kuntze . Plant Cell Environ. , 5 : 237 – 240 .
  • Ozawa , K. , Osaki , M. , Matsui , H. , Honma , M. and Tadano , T. 1995 . Purification and properties of acid phosphatase secreted from lupin roots under phosphorus-deficiency conditions . Soil Sci. Plant Nutr. , 41 : 461 – 469 .
  • Palmiter , R.D. 1974 . Magnesium precipitation of ribonucleoprotein complexes. Expedient techniques for the isolation of undergraded polysomes and messenger ribonucleic acid . Biochemistry , 13 : 3606 – 3615 .
  • Rasband , W.S. and Bright , D.S. 1995 . NIH Image: A public domain image processing program for the macintosh . Microbeam Anal. Soc. J. , 4 : 137 – 148 .
  • Sakai , H. and Tadano , T. 1993 . Characteristics of response of acid phosphatase secreted by the roots of several crops to various conditions in the growth media . Soil Sci. Plant Nutr. , 39 : 437 – 444 .
  • Sanger , F. , Nicklen , S. and Coulson , A.R. 1977 . DNA sequencing with chain-terminating inhibitors . Proc. Natl. Acad. Sci. U.S.A. , 74 : 5463 – 5467 .
  • Sarker , S. , Caddick , M.X. , Bingel , E. , Tilburn , J. and Arst , H.N. 1996 . Regulation of gene expression by ambient pH in Aspergillus: Genes expressed at acid pH . Biochem. Soc. Trans. , 24 : 360 – 363 .
  • Shah , D.M. , Hightower , R.C. and Meagher , R.B. 1983 . Genes encoding actin in higher plants: Intron positions are highly conserved but the coding sequences are not . J. Mol. Appl. Genet. , 2 : 111 – 126 .
  • Silberbush , M. , Shomer-Ilan , A. and Waisel , Y. 1981 . Root surface phosphatase activity in ecotypes of Aegilops peregrina . Physiol. Plant. , 53 : 501 – 504 .
  • Sträter , N. , Klabunde , T. , Tucker , P. , Witzel , H. and Krebs , B. 1995 . Crystal structure of a purple acid phosphatase containing a dinuclear Fe(III)-Zn(II) active site . Science , 268 : 1489 – 1492 .
  • Tadano , T. and Komatsu , K. 1994 . Utilization of organic phosphorus in soil by plant roots . Trans. 15th World Congr. Soil Sci. , 9 : 521 – 522 .
  • Tadano , T. and Sakai , H. 1991 . Secretion of acid phosphatase by the roots of several crop species under phosphorus-deficient conditions . Soil Sci. Plant Nutr. , 37 : 129 – 140 .
  • Tamura , T. , Minamikawa , T. and Koshiba , T. 1982 . Multiple forms of acid phosphatase in cotyledons of Vigna mungo seedlings . J. Exp. Bot. , 33 : 1332 – 1339 .
  • Tarafdar , J.C. and Jungk , A. 1987 . Phosphatase activity in the rhizosphere and its relation to the depletion of soil organic phosphorus . Biol. Fertil. Soil , 3 : 199 – 204 .
  • Thompson , J.D. , Higgins , D.G. and Gibson , T.J. 1994 . Clustal W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice . Nucleic Acids Res. , 22 : 4673 – 4680 .
  • UJlah , A.H.J. , Mullaney , E.M. and Dischinger , H.C. 1994 . The complete primary structure elucidation of Aspergillus jicuum (niger), pH 6.0, optimum acid phosphatase by Edman degradation . Biochem. Biophys. Res. Commun. , 203 : 182 – 189 .
  • Wasaki , J. , Ando , M. , Ozawa , K. , Omura , M. , Osaki , M. , Ito , H. , Matsui , H. and Tadano , T. 1997 . Properties of secretory acid phosphatase from lupin roots under phosphorus-deficient conditions . Soil Sci. Plant Nutr. , 43 : 981 – 986 .
  • Wasaki , J. , Omura , M. , Osaki , M. , Ito , H. , Matsui , H. , Shinano , T. and Tadano , T. 1999 . Structure of a cDNA for an acid phosphatase from phosphate deficient lupin (Lupinus albus L.) roots . Soil Sci. Plant Nutr. , 45 : 439 – 449 .

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.