Download PDF
Plant Biol (Stuttg) 2006; 8(3): 340-345
DOI: 10.1055/s-2006-923802
Review Article

Georg Thieme Verlag Stuttgart KG · New York

Indole-3-Acetic Acid Protein Conjugates: Novel Players in Auxin Homeostasis

C. Seidel1 , A. Walz1 , 2 , S. Park3 , J. D. Cohen3 , J. Ludwig-Müller1
  • 1Institut für Botanik, Technische Universität Dresden, Zellescher Weg 22, 01062 Dresden, Germany
  • 2Vital Probes Inc., 1300 Old Plank Road, Mayfield, PA 18433, USA
  • 3Department of Horticultural Science, Center for Microbial and Plant Genomics, University of Minnesota, 305 Alderman Hall, Saint Paul, MN 55108, USA
Further Information

Publication History

Received: October 4, 2005

Accepted: December 12, 2005

Publication Date:
13 March 2006 (online)

   Permissions and Reprints

Abstract

Indole-3-acetic acid (IAA) is found in plants in both free and conjugated forms. Within the group of conjugated IAA there is a unique class of proteins and peptides where IAA is attached directly to the polypeptide structure as a prosthetic group. The first gene, iap1, encoding for a protein with IAA as a prosthetic group, was cloned from bean (Phaseolus vulgaris). It was shown that the expression of IAP1 as a major IAA modified protein in bean seed (PvIAP1) was correlated to a developmental period of rapid growth during seed development. Moreover, this protein underwent rapid degradation during germination. Since further molecular analysis was difficult in bean, the iap1 gene was transformed into Arabidopsis thaliana and Medicago truncatula. Expression of the bean iap1 gene in both plant species under the control of its native promoter targeted protein expression to the seeds. In Arabidopsis no IAA was found to be attached to PvIAP1. These results show that there is specificity to protein modification by IAA and suggests that protein conjugation may be catalyzed by species specific enzymes. Furthermore, subcellular localization showed that in Arabidopsis PvIAP1 was predominantly associated with the microsomal fraction. In addition, a related protein and several smaller peptides that are conjugated to IAA were identified in Arabidopsis. Further research on this novel class of proteins from Arabidopsis will both advance our knowledge of IAA proteins and explore aspects of auxin homeostasis that were not fully revealed by studies of free IAA and lower molecular weight conjugates.

Key words

Auxin homeostasis - protein modification - Phaseolus vulgaris - Medicago truncatula - indole-3-acetic acid - IAA protein - Arabidopsis thaliana.

References

  • 1 Andersson B., Sandberg G.. Identification of endogenous N-(3-indoleacetyl)aspartic acid in Scots pine (Pinus sylvestris L.) by combined gas chromatography-mass spectrometry, using high-performance liquid chromatography for quantification.  Journal of Chromatography. (1982);  238 151-156
    CrossrefPubMedGoogle Scholar
  • 2 Bandurski R. S., Schulze A.. Concentrations of IAA and its derivatives in plants.  Plant Physiology. (1977);  60 211-213
    PubMedGoogle Scholar
  • 3 Bandurski R. S., Ueda M., Nicholls P. B.. Esters of indole-3-acetic acid and myo-inositol.  Annals of the New York Academy of Science. (1969);  165 655-667
    PubMedGoogle Scholar
  • 4 Bandurski R. S., Cohen J. D., Slovin J. P., Reinecke D. M.. Auxin biosynthesis and metabolism. Davies P. J., ed. Plant Hormones: Physiology, Biochemistry and Molecular Biology, 2nd ed. Boston; Kluwer Academic Publishers (1995): 39-65
    Google Scholar
  • 5 Bartel B., Fink G.. ILR1, an amidohydrolase that releases active indole-3-acetic acid from conjugates.  Science. (1995);  268 1745-1748
    PubMedGoogle Scholar
  • 6 Bartel B., LeClere S., Magidin M., Zolman B. K.. Inputs to the active indole-3-acetic acid pool: de novo synthesis, conjugate hydrolysis, and indole-3-butyric acid β-oxidation.  Journal of Plant Growth Regulation. (2001);  20 198-216
    CrossrefPubMedGoogle Scholar
  • 7 Bialek K., Cohen J. D.. Isolation and partial characterization of the major amide-linked conjugate of indole-3-acetic acid from Phaseolus vulgaris L.  Plant Physiology. (1986);  80 99-104
    PubMedGoogle Scholar
  • 12 Bialek K., Cohen J. D.. Quantitation of indole acetic acid conjugates in bean seeds by direct tissue hydrolysis.  Plant Physiology. (1989 a);  90 398-400
    PubMedGoogle Scholar
  • 13 Bialek K., Cohen J. D.. Free and conjugated indole-3-acetic acid in developing bean seeds.  Plant Physiology. (1989 b);  91 775-779
    PubMedGoogle Scholar
  • 9 Bialek K., Cohen J. D.. Amide-linked indoleacetic acid conjugates may control levels of indoleacetic acid in germinating seedlings of Phaseolus vulgaris.  Plant Physiology. (1992);  100 2002-2007
    PubMedGoogle Scholar
  • 10 Bialek K., Meudt W. J., Cohen J. D.. Indole-3-acetic acid (IAA) and IAA conjugates applied to bean stem sections: IAA content and the growth response.  Plant Physiology. (1983);  73 130-139
    PubMedGoogle Scholar
  • 14 Campanella J. J., Bakllamaja V., Restieri T., Vomacka M., Herron J., Patterson M., Shahtaheri S.. Isolation of an ILR1 auxin conjugate hydrolase homolog from Arabidopsis suecica.  Plant Growth Regulation. (2003 a);  39 175-181
    CrossrefPubMedGoogle Scholar
  • 15 Campanella J. J., Ludwig-Müller J., Bakllamaja V., Sharma V., Cartier A.. ILR1 and sILR1 IAA amidohydrolase homologs differ in expression pattern and substrate specificity.  Plant Growth Regulation. (2003 b);  41 215-223
    CrossrefPubMedGoogle Scholar
  • 16 Campanella J. J., Olajide A., Magnus V., Ludwig-Müller J.. A novel auxin conjugate hydrolase from Triticum aestivum with substrate specificity for longer side-chain auxin amide conjugates.  Plant Physiology. (2004);  135 2230-2240
    CrossrefPubMedGoogle Scholar
  • 17 Chen K.-H.. Analysis of indole-3-acetic acid in tobacco genetic tumors and wheat GA3 insensitive mutant “tom thumb”. PhD Dissertation, University of Maryland, College Park. (1987)
    Google Scholar
  • 18 Chisnell J. R., Bandurski R. S.. Translocation of radiolabeled indole-3-acetic acid and indole-3-acetyl-myo-inositol from kernel to shoot in Zea mays L.  Plant Physiology. (1988);  86 79-84
    PubMedGoogle Scholar
  • 19 Cohen J. D.. Identification and quantitative analysis of indole-3-acetyl-l-aspartate from seeds of Glycine max L.  Plant Physiology. (1982);  70 749-753
    PubMedGoogle Scholar
  • 20 Cohen J. D.. Metabolism of indole-3-acetic acid.  Plant Physiology. (1983);  14 41
    PubMedGoogle Scholar
  • 21 Cohen J. D., Bandurski R. S.. The chemistry and physiology of the bound auxins.  Annual Reviews of Plant Physiology. (1982);  33 403-430
    PubMedGoogle Scholar
  • 22 Cohen J. D., Slovin J. P., Bialek K., Chen K.-H., Derbyshire M.. Mass spectrometry, genetics and biochemistry: understanding the metabolism of indole-3-acetic acid. Steffens, G. L. and Rumsey, T. S., eds. Biomechanisms Regulating Growth and Development. Dordrecht; Kluwer (1988): 229-241
    Google Scholar
  • 23 Cohen J. D., Baldi B. G., Baraldi R., Bialek K., Chen K.-H., Slovin J. P.. Genetic and analytical techniques for auxin studies.  Giornale Botanico Italiano. (1989);  123 355-365
    PubMedGoogle Scholar
  • 24 Cohen J. D., Ilic N., Taylor R., Dunlap J. R., Slovin J. P.. Auxin localization and metabolism during fruit growth and ripening in cantaloupe. Lester, G. E. and Dunlap, J. R., eds. Proceedings Cucurbitaceae. Edinburgh; Gateway (1995)
    Google Scholar
  • 25 Davies P. J.. The plant hormones: their nature, occurrence, and function,. Davies P. J., ed. Plant Hormones: Biosynthesis, Signal Transduction, Action!. Dordrecht, The Netherlands; Kluwer Academic Publishers (2004): 1-15
    Google Scholar
  • 26 Davies R. T., Goetz D. H., Lasswell J., Anderson M. N., Bartel B.. IAR3 encodes an auxin conjugate hydrolase from Arabidopsis. .  Plant Cell. (1999);  11 365-376
    CrossrefPubMedGoogle Scholar
  • 27 Domagalski W., Schulze A., Bandurski R. S.. Isolation and characterization of esters of indole-3-acetic acid from liquid endosperm of the horse chestnut (Aesculus species).  Plant Physiology. (1987);  84 1107-1113
    PubMedGoogle Scholar
  • 28 Hall P. J., Bandurski R. S.. [3H]Indole-3-acetyl-myo-inositol hydrolysis by extracts of Zea mays L. vegetative tissue.  Plant Physiology. (1986);  80 374-377
    PubMedGoogle Scholar
  • 29 Jackson R. G., Lim E. K., Li Y., Kowalczyk M., Sandberg G., Hoggett J., Ashford D. A., Bowles D. J.. Identification and biochemical characterization of an Arabidopsis indole-3-acetic acid glucosyltransferase.  Journal of Biological Chemistry. (2001);  276 4350-4356
    CrossrefPubMedGoogle Scholar
  • 30 Jackson R. G., Kowalczyk M., Li Y., Higgins G., Ross J., Sandberg G., Bowles D. J.. Over-expression of an Arabidopsis gene encoding a glucosyltransferase of indole-3-acetic acid: phenotypic characterisation of transgenic lines.  The Plant Journal. (2002);  32 573-583
    CrossrefPubMedGoogle Scholar
  • 31 Jakubowska A., Kowalczyk S.. A specific enzyme hydrolyzing 6-O(4-O)-indol-3-ylacetyl-β-D-glucose in immature kernels of Zea mays.  Journal of Plant Physiology. (2005);  162 207-213
    CrossrefPubMedGoogle Scholar
  • 32 Kesy J. M., Bandurski R. S.. Partial purification and characterization of indol-3-yl-acetylglucose-myo-inositol indol-3-yl-acetyltransferase (indoleacetic acid-inositol synthase).  Plant Physiology. (1990);  94 1598-1604
    PubMedGoogle Scholar
  • 33 Kopcewicz J., Ehmann A., Bandurski R. S.. Enzymatic esterification of indole-3-acetic acid to myo-inositol and glucose.  Plant Physiology. (1974);  54 846-851
    PubMedGoogle Scholar
  • 34 Kowalczyk M., Sandberg G.. Quantitative analysis of indole-3-acetic acid metabolites of Arabidopsis.  Plant Physiology. (2001);  127 1845-1853
    CrossrefPubMedGoogle Scholar
  • 35 Kowalczyk S., Jakubowska A., Zielinska E., Bandurski R. S.. Bifunctional indole-3-acetyl transferase catalyses synthesis and hydrolysis of indole-3-acetyl-myo-inositol in immature endosperm of Zea mays. .  Physiologia Plantarum. (2003);  119 165-174
    CrossrefPubMedGoogle Scholar
  • 36 LeClere S., Tellez R., Rampey R. A., Matsuda S. P. T., Bartel B.. Characterization of a family of IAA-amino acid conjugate hydrolases from Arabidopsis.  Journal of Biological Chemistry. (2002);  277 20446-20452
    CrossrefPubMedGoogle Scholar
  • 37 Leznicki A. J., Bandurski R. S.. Enzymic synthesis of indole-3-acetyl-1-0-β‐D-glucose. II. Metabolic characteristics of the enzyme.  Plant Physiology. (1988);  88 1481-1485
    PubMedGoogle Scholar
  • 38 Ljung K., Hull A. K., Kowalczyk M., Marchant A., Celenza J., Cohen J. D., Sandberg G.. Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana.  Plant Molecular Biology. (2002);  49 249-272 Plant Molecular Biology. (2002);  50 309-332
    CrossrefPubMedGoogle Scholar
  • 39 Ludwig-Müller J.. Indole-3-butyric acid in plant growth and development.  Plant Growth Regulation. (2000);  32 219-230
    CrossrefPubMedGoogle Scholar
  • 40 Ludwig-Müller J., Epstein E., Hilgenberg W.. Auxin-conjugate hydrolysis in Chinese cabbage: characterization of an amidohydrolase and its role during infection with clubroot disease.  Physiologia Plantarum. (1996);  97 627-634
    CrossrefPubMedGoogle Scholar
  • 41 Michalczuk L., Bandurski R. S.. Enzymic synthesis of 1-O-indol-3-ylacetyl-β‐D-glucose and indol-3-ylacetyl-myo-inositol.  Biochemical Journal. (1982);  207 273-281
    PubMedGoogle Scholar
  • 42 Nakazawa M., Yabe N., Ichikawa T., Yamamoto Y. Y., Yoshizumi T., Hasunuma K., Matsui M.. DFL1, an auxin-responsive GH3 gene homologue, negatively regulates shoot cell elongation and lateral root formation, and positively regulates the light response of hypocotyl length.  The Plant Journal. (2001);  25 213-221
    CrossrefPubMedGoogle Scholar
  • 43 Östin A., Moritz T., Sandberg G.. Liquid chromatography/mass spectrometry of conjugates and oxidative metabolites of indole-3-acetic acid.  Biological Mass Spectrometry. (1992);  21 292-298
    CrossrefPubMedGoogle Scholar
  • 44 Schuller A., Ludwig-Müller J.. Isolation of differentially expressed genes involved in clubroot disease.  Plant Protection Science. (2002);  38 483-486
    PubMedGoogle Scholar
  • 45 Slovin J. P., Bandurski R. S., Cohen J. D.. Auxin. Hooykaas P. J. J., Hall, M. A., and Libbenga K. R., eds. Biochemistry and Molecular Biology of Plant Hormones. Amsterdam, The Netherlands; Elsevier (1999): 115-140
    Google Scholar
  • 46 Sonner J. M., Purves W. K.. Natural occurrence of indole-3-acetyl aspartate and indole-3-acetyl glutamate in cucumber shoot tissue.  Plant Physiology. (1985);  77 784-785
    PubMedGoogle Scholar
  • 47 Staswick P. E., Tiryaki I., Rowe M. L.. Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic and indole-3-acetic acids in an assay for adenylation.  Plant Cell. (2002);  14 1405-1415
    CrossrefPubMedGoogle Scholar
  • 48 Staswick P. E., Serban B., Rowe M., Tiryaki I., Maldonado M. T., Maldonado M. C., Suza W.. Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid.  Plant Cell. (2005);  17 616-627
    CrossrefPubMedGoogle Scholar
  • 49 Szerszen J. D., Szczyglowski K., Bandurski R. S.. iaglu, a gene from Zea mays involved in conjugation of growth hormone indole-3-acetic acid.  Science. (1994);  265 1699-1701
    PubMedGoogle Scholar
  • 50 Takase T., Nakazawa M., Ishikawa A., Manabe K., Matsui M.. DFL2, a new member of the Arabidopsis GH3 gene family, is Involved in red light-specific hypocotyl elongation.  Plant Cell Physiology. (2003);  44 1071-1080
    CrossrefPubMedGoogle Scholar
  • 51 Takase T., Nakazawa M., Ishikawa A., Kawashima M., Ichikawa T., Takahashi N., Shimada H., Manabe K., Matsui M.. ydk1-D, an auxin-responsive GH3 mutant that is involved in hypocotyls and root elongation.  The Plant Journal. (2004);  37 471-483
    CrossrefPubMedGoogle Scholar
  • 52 Tam Y. Y., Epstein E., Normanly J.. Characterisation of auxin conjugates in Arabidopsis. Low steady-state levels of indole-3-acetyl-aspartate, indole-3-acetyl-glutamate and indole-3-acetyl-glucose.  Plant Physiology. (2000);  123 589-595
    CrossrefPubMedGoogle Scholar
  • 53 Tsurumi S., Wada S.. Identification of 3-hydroxy-2-indolone-3-acetylaspartic acid as a new indole-3-acetic acid metabolite in Vicia seedlings.  Plant Cell Physiology. (1986);  27 562-599
    PubMedGoogle Scholar
  • 54 Walz A., Park S., Slovin J. P., Ludwig-Müller J., Momonoki Y. S., Cohen J. D.. A gene encoding a protein modified by the phytohormone indoleacetic acid.  Proceedings of the National Academy of Sciences of the USA. (2002);  99 1718-1723
    CrossrefPubMedGoogle Scholar

J. Ludwig-Müller

Institut für Botanik
Technische Universität Dresden

Zellescher Weg 22

01062 Dresden

Germany

Email: jutta.ludwig-mueller@mailbox.tu-dresden.de

Guest Editor: R. Reski

      >