Skip to main content
PMC home page
Plant Physiology logoLink to Plant Physiology
. 1993 Feb;101(2):595–606. doi: 10.1104/pp.101.2.595

KDEL-Containing Auxin-Binding Protein Is Secreted to the Plasma Membrane and Cell Wall.

A M Jones 1, E M Herman 1
PMCID: PMC160609  PMID: 12231715

Abstract

The auxin-binding protein ABP1 has been postulated to mediate auxin-induced cellular changes associated with cell expansion. This protein contains the endoplasmic reticulum (ER) retention signal, the tetrapeptide lysine-aspartic acid-glutamic acid-leucine (KDEL), at its carboxy terminus, consistent with previous subcellular fractionation data that indicated an ER location for ABP1. We used electron microscopic immunocytochemistry to identify the subcellular localization of ABP1. Using maize (Zea mays) coleoptile tissue and a black Mexican sweet (BMS) maize cell line, we found that ABP1 is located in the ER as expected, but is also on or closely associated with the plasma membrane and within the cell wall. Labeling of the Golgi apparatus suggests that the transport of ABP1 to the cell wall occurs via the secretory system. Inhibition of secretion of an ABP homolog into the medium of BMS cell cultures by brefeldin A, a drug that specifically blocks secretion, is consistent with this secretion pathway. The secreted protein was recognized by an anti-KDEL peptide antibody, strongly supporting the interpretation that movement of this protein out of the ER does not involve loss of the carboxy-terminal signal. Cells starved for 2,4-dichlorophenoxyacetic acid for 72 h retained less ABP in the cell and secreted more of it into the medium. The significance of our observations is 2-fold. We have identified a KDEL-containing protein that specifically escapes the ER retention system, and we provide an explanation for the apparent discrepancy that most of the ABP is located in the ER, whereas ABP and auxin act at the plasma membrane.

Full Text

The Full Text of this article is available as a PDF (3.9 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akasofu H., Yamauchi D., Mitsuhashi W., Minamikawa T. Nucleotide sequence of cDNA for sulfhydryl-endopeptidase (SH-EP) from cotyledons of germinating Vigna mungo seeds. Nucleic Acids Res. 1989 Aug 25;17(16):6733–6733. doi: 10.1093/nar/17.16.6733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Booth C., Koch G. L. Perturbation of cellular calcium induces secretion of luminal ER proteins. Cell. 1989 Nov 17;59(4):729–737. doi: 10.1016/0092-8674(89)90019-6. [DOI] [PubMed] [Google Scholar]
  3. Cleland R. E., Buckley G., Nowbar S., Lew N. M., Stinemetz C., Evans M. L., Rayle D. L. The pH profile for acid-induced elongation of coleoptile and epicotyl sections is consistent with the acid-growth theory. Planta. 1991;186:70–74. [PubMed] [Google Scholar]
  4. Cross J. W. Cycling of auxin-binding protein through the plant cell: pathways in auxin signal transduction. New Biol. 1991 Aug;3(8):813–819. [PubMed] [Google Scholar]
  5. Denecke J., De Rycke R., Botterman J. Plant and mammalian sorting signals for protein retention in the endoplasmic reticulum contain a conserved epitope. EMBO J. 1992 Jun;11(6):2345–2355. doi: 10.1002/j.1460-2075.1992.tb05294.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ephritikhine G., Barbier-Brygoo H., Muller J. F., Guern J. Auxin effect on the transmembrane potential difference of wild-type and mutant tobacco protoplasts exhibiting a differential sensitiity to auxin. Plant Physiol. 1987 Apr;83(4):801–804. doi: 10.1104/pp.83.4.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fontes E. B., Shank B. B., Wrobel R. L., Moose S. P., OBrian G. R., Wurtzel E. T., Boston R. S. Characterization of an immunoglobulin binding protein homolog in the maize floury-2 endosperm mutant. Plant Cell. 1991 May;3(5):483–496. doi: 10.1105/tpc.3.5.483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hicks G. R., Rayle D. L., Jones A. M., Lomax T. L. Specific photoaffinity labeling of two plasma membrane polypeptides with an azido auxin. Proc Natl Acad Sci U S A. 1989 Jul;86:4948–4952. doi: 10.1073/pnas.86.13.4948. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Inohara N., Shimomura S., Fukui T., Futai M. Auxin-binding protein located in the endoplasmic reticulum of maize shoots: molecular cloning and complete primary structure. Proc Natl Acad Sci U S A. 1989 May;86(10):3564–3568. doi: 10.1073/pnas.86.10.3564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jones A. M., Cochran D. S., Lamerson P. M., Evans M. L., Cohen J. D. Red light-regulated growth. I. Changes in the abundance of indoleacetic acid and a 22-kilodalton auxin-binding protein in the maize mesocotyl. Plant Physiol. 1991;97:352–358. doi: 10.1104/pp.97.1.352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Klausner R. D., Donaldson J. G., Lippincott-Schwartz J. Brefeldin A: insights into the control of membrane traffic and organelle structure. J Cell Biol. 1992 Mar;116(5):1071–1080. doi: 10.1083/jcb.116.5.1071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Letourneur F., Klausner R. D. A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell. 1992 Jun 26;69(7):1143–1157. doi: 10.1016/0092-8674(92)90636-q. [DOI] [PubMed] [Google Scholar]
  13. Lippincott-Schwartz J., Yuan L. C., Bonifacino J. S., Klausner R. D. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell. 1989 Mar 10;56(5):801–813. doi: 10.1016/0092-8674(89)90685-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Löbler M., Klämbt D. Auxin-binding protein from coleoptile membranes of corn (Zea mays L.). I. Purification by immunological methods and characterization. J Biol Chem. 1985 Aug 15;260(17):9848–9853. [PubMed] [Google Scholar]
  15. Macdonald H., Jones A. M., King P. J. Photoaffinity labeling of soluble auxin-binding proteins. J Biol Chem. 1991 Apr 25;266(12):7393–7399. [PubMed] [Google Scholar]
  16. Napier R. M., Venis M. A. Epitope mapping reveals conserved regions of an auxin-binding protein. Biochem J. 1992 Jun 15;284(Pt 3):841–845. doi: 10.1042/bj2840841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Picard D., Yamamoto K. R. Two signals mediate hormone-dependent nuclear localization of the glucocorticoid receptor. EMBO J. 1987 Nov;6(11):3333–3340. doi: 10.1002/j.1460-2075.1987.tb02654.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Prasad P. V., Jones A. M. Putative receptor for the plant growth hormone auxin identified and characterized by anti-idiotypic antibodies. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5479–5483. doi: 10.1073/pnas.88.13.5479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rayle D. L., Cleland R. E. Evidence that Auxin-induced Growth of Soybean Hypocotyls Involves Proton Excretion. Plant Physiol. 1980 Sep;66(3):433–437. doi: 10.1104/pp.66.3.433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ronne H., Ocklind C., Wiman K., Rask L., Obrink B., Peterson P. A. Ligand-dependent regulation of intracellular protein transport: effect of vitamin a on the secretion of the retinol-binding protein. J Cell Biol. 1983 Mar;96(3):907–910. doi: 10.1083/jcb.96.3.907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Senn A. P., Goldsmith M. H. Regulation of electrogenic proton pumping by auxin and fusicoccin as related to the growth of Avena coleoptiles. Plant Physiol. 1988 Sep;88(1):131–138. doi: 10.1104/pp.88.1.131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Tanaka T., Yamauchi D., Minamikawa T. Nucleotide sequence of cDNA for an endopeptidase (EP-C1) from pods of maturing Phaseolus vulgaris fruits. Plant Mol Biol. 1991 Jun;16(6):1083–1084. doi: 10.1007/BF00016081. [DOI] [PubMed] [Google Scholar]
  23. Tillmann U., Viola G., Kayser B., Siemeister G., Hesse T., Palme K., Löbler M., Klämbt D. cDNA clones of the auxin-binding protein from corn coleoptiles (Zea mays L.): isolation and characterization by immunological methods. EMBO J. 1989 Sep;8(9):2463–2467. doi: 10.1002/j.1460-2075.1989.tb08381.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Venis M. A., Napier R. M., Barbier-Brygoo H., Maurel C., Perrot-Rechenmann C., Guern J. Antibodies to a peptide from the maize auxin-binding protein have auxin agonist activity. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):7208–7212. doi: 10.1073/pnas.89.15.7208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wandelt C. I., Khan M. R., Craig S., Schroeder H. E., Spencer D., Higgins T. J. Vicilin with carboxy-terminal KDEL is retained in the endoplasmic reticulum and accumulates to high levels in the leaves of transgenic plants. Plant J. 1992 Mar;2(2):181–192. doi: 10.1046/j.1365-313x.1992.t01-41-00999.x. [DOI] [PubMed] [Google Scholar]
  26. Wood S. A., Park J. E., Brown W. J. Brefeldin A causes a microtubule-mediated fusion of the trans-Golgi network and early endosomes. Cell. 1991 Nov 1;67(3):591–600. doi: 10.1016/0092-8674(91)90533-5. [DOI] [PubMed] [Google Scholar]
  27. Woodward M. P., Young W. W., Jr, Bloodgood R. A. Detection of monoclonal antibodies specific for carbohydrate epitopes using periodate oxidation. J Immunol Methods. 1985 Apr 8;78(1):143–153. doi: 10.1016/0022-1759(85)90337-0. [DOI] [PubMed] [Google Scholar]
  28. Yoshimori T., Semba T., Takemoto H., Akagi S., Yamamoto A., Tashiro Y. Protein disulfide-isomerase in rat exocrine pancreatic cells is exported from the endoplasmic reticulum despite possessing the retention signal. J Biol Chem. 1990 Sep 15;265(26):15984–15990. [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES