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Auxin-responsive gene expression: genes, promoters and regulatory factors

  • Gretchen Hagen
  • Tom Guilfoyle

Abstract

A molecular approach to investigate auxin signaling in plants has led to the identification of several classes of early/primary auxin response genes. Within the promoters of these genes, cis elements that confer auxin responsiveness (referred to as auxin-response elements or AuxREs) have been defined, and a family of trans-acting transcription factors (auxin-response factors or ARFs) that bind with specificity to AuxREs has been characterized. A family of auxin regulated proteins referred to as Aux/IAA proteins also play a key role in regulating these auxin-response genes. Auxin may regulate transcription on early response genes by influencing the types of interactions between ARFs and Aux/IAAs.

Key words

auxin response elements (AuxREs) auxin response factors (ARFs) auxin response genes 

Abbreviation

ARF

auxin-response factor

AuxRE

auxin-response element

CHX

cycloheximide

DBD

DNA-binding domain

DR

direct repeat

ER

everted repeat

EST

expressed sequence tag

ORF

open reading frame

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References

  1. Abel, S., Oeller, P.W. and Theologis, A. 1994. Early auxin-induced genes encode short-lived nuclear proteins. Proc. Natl. Acad. Sci. USA 91: 326–330PubMedCrossRefGoogle Scholar
  2. Abel, S., Nguyen, M.D. and Theologis, A. 1995. The PS-IAA4/5-like family of early auxin-inducible mRNAs in Arabidopsis thaliana. J. Mol. Biol. 251: 533–549.PubMedCrossRefGoogle Scholar
  3. Abel, S. and Theologis, A. 1995. A polymorphic bipartite motif signals nuclear targeting of early auxin-inducible proteins related to PS-IAA4 from pea (Pisum sativum). Plant J. 8: 87–96.PubMedCrossRefGoogle Scholar
  4. Abel, S. and Theologis, A. 1996. Early genes and auxin action. Plant Physiol. 111:9–17.PubMedCrossRefGoogle Scholar
  5. Ainley, W.M., Walker, J.C., Nagao, R.T. and Key, J.L. 1988. Sequence and characterization of two auxin-regulated genes from soybean. J. Biol. Chem. 263: 10658–10666.PubMedGoogle Scholar
  6. Anai, T., Kono, N., Kosemura, S., Yamamura, S. and Hasegawa, K. 1998. Isolation and characterization of an auxin-inducible SAUR gene from radish. DNA Seq. 9: 329–333.PubMedGoogle Scholar
  7. Casimiro, I., Marchant, A., Bhalerao, R.P., Beeckman, T., Dhooge, S., Swarup, R., Graham, N., Inzé, D., Sandberg, G., Casero, P.J. and Bennett, M. 2001. Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13: 843–852.PubMedGoogle Scholar
  8. Colon-Carmona, A., Chen, D.L., Yeh, K.C. and Abel, S. 2000. Aux/IAA proteins are phosphorylated by phytochrome in vitro. Plant Physiol. 124: 1728–1738.PubMedCrossRefGoogle Scholar
  9. Conner, T.W., Goekjian, V.L., LaFayette, P.R. and Key, J.L. 1990. Structure and expression of two auxin-inducible genes from Arabidopsis. Plant Mol. Biol. 15: 623–632.PubMedCrossRefGoogle Scholar
  10. Dargeviciute, A., Roux, C., Decreux, A., Sitbon, F. and Perrot-Rechenmann, C. 1998. Molecular cloning and expression of the early auxin-responive Aux/IAA gene family in Nicotiana tabacum. Plant Cell Physiol. 39: 993–1002.PubMedCrossRefGoogle Scholar
  11. Dharmasiri, S. and Estelle, M. 2002. The role of regulated protein degradation in auxin response. Plant Mol. Biol. 49: 401–408.PubMedCrossRefGoogle Scholar
  12. Delong, A., Mockaitis, K. and Christensen, S. 2002. Protein phosphorylation in the delivery of and response to auxin signals-Plant Mol. Biol. 49: 285–303.Google Scholar
  13. Ellis, J.G., Tokuhisa, J.G., Llewellyn, D.J., Bouchez, D., Singh, K., Dennis, E.S. and Peacock, W.J. 1993. Does the ocs-element occur as a functional component of the promoters of plants? Plant J. 4: 433–443.PubMedCrossRefGoogle Scholar
  14. Franco, A., Gee, M.A. and Guilfoyle, T.J. 1990. Induction and superinduction of auxin-responsive genes with auxin and protein synthesis inhibitors. J. Biol. Chem. 265: 15845–15849.PubMedGoogle Scholar
  15. Gee, M.A., Hagen, G. and Guilfoyle, T.J. 1991. Tissue-specific and organ-specific expression of the auxin-responsive transcripts, SAURs and GH3, in soybean. Plant Cell 3: 419–430.PubMedGoogle Scholar
  16. Gil, P., Liu, Y., Orbovic, V., Verkamp, E., Poff, K.L. and Green, P. 1994. Characterization of the auxin-inducible SAUR-AC1 gene for use as a genetic tool in Arabidopsis. Plant Physiol. 104: 777–784.PubMedCrossRefGoogle Scholar
  17. Giraudat, J., Hauge, B.M., Valon, C., Smalle, J., Parcy, F. and Goodman, H.M. 1992. Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4: 1251–1261.PubMedGoogle Scholar
  18. Gray, W.M. and Estelle, M. 2000. Function of the ubiquitin-proteasome pathway in auxin response. Trends Biochem. Sci. 25: 133–138.PubMedCrossRefGoogle Scholar
  19. Guilfoyle, T.J. 1999. Auxin-regulated genes and promoters. In: P.J.J. Hooykaas, M. Hall and K.L. Libbenga (Eds.) Biochemistry and Molecular Biology of Plant Hormones, Elsevier, Leiden, Netherlands, pp. 423–459.CrossRefGoogle Scholar
  20. Guilfoyle, T.J., Hagen, G., Li, Y., Ulmasov, T., Liu, Z., Strabala, T. and Gee, M.A. 1993. Auxin-regulated transcription. Aust. J. Plant Physiol. 20: 489–502.CrossRefGoogle Scholar
  21. Guilfoyle, T.J., Ulmasov, T. and Hagen, G. 1998a. The ARF family of transcription factors and their role in plant hormone responsive transcription. Cell. Mol. Life Sci. 54: 619–627.PubMedCrossRefGoogle Scholar
  22. Guilfoyle, T.J., Hagen, G., Ulmasov, T. and Murfett, J. 1998b. How does auxin turn on genes? Plant Physiol. 118: 341–347.PubMedCrossRefGoogle Scholar
  23. Hagen, G. and Guilfoyle, T.J. 1985. Rapid induction of selective transcription by auxin. Mol. Cell. Biol. 5: 1197–1203.PubMedGoogle Scholar
  24. Hagen, G., Kleinschmidt, A.J. and Guilfoyle, T.J. 1984. Auxin-regulated gene expression in intact soybean hypocotyl and excised hypocotyl sections. Planta 16: 147–153.CrossRefGoogle Scholar
  25. Hagen, G., Martin, G., Li, Y. and Guilfoyle, T.J. 1991. Auxin-induced expression of the soybean GH3 promoter in transgenic tobacco plants. Plant Mol. Biol. 17: 567–579.PubMedCrossRefGoogle Scholar
  26. Hardtke, C.S. and Berleth, T. 1998. The Arabidopsis gene MONOPTEROUS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J. 17: 1405–1411.PubMedCrossRefGoogle Scholar
  27. Harper, R.M., Stowe-Evans, E.L., Luesse, D.R., Muto, H., Tatematsu, K., Watahiki, M.K., Yamamoto, K. and Liscum, E. 2000. The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. Plant Cell 12: 757–770.PubMedGoogle Scholar
  28. Hsieh, H.L., Okamoto, H., Wang, M., Ang, L.H., Matsui, M., Goodman, H. and Deng, X.W. 2000. FIN219, an auxin-regulated gene, defines a link between phytochrome A and the downstream regulator COP1 in light control of Arabidopsis development. Genes Devel. 14: 1958–1970.PubMedGoogle Scholar
  29. Kagaya, Y., Ohmiya, K. and Hattori T. 1999. RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in plants. Nucl. Acids Res. 27: 470–478.PubMedCrossRefGoogle Scholar
  30. Katagiri, F., Lam, E. and Chua, N.-H. 1989. Two tobacco DNA-binding proteins with homology to the nuclear factor CREB. Nature 340: 727–730.PubMedCrossRefGoogle Scholar
  31. Kim, J., Harter, K. and Theologis, A. 1997. Protein-protein interactions among the Aux/IAA proteins. Proc. Natl. Acad. Sci. USA 94:11786–11791.PubMedCrossRefGoogle Scholar
  32. Kovtun, Y., Chiu, W.-L., Zeng, W. and Sheen, J. 1998. Suppression of auxin signal transduction by a MAPK cascade in higher plants. Nature 395: 716–720.PubMedCrossRefGoogle Scholar
  33. Kovtun, Y., Chiu, W.-L., Tena, G. and Sheen J. 2000. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. USA 97: 2940–2945.PubMedCrossRefGoogle Scholar
  34. Li, Y., Strabala, T.J., Hagen, G. and Guilfoyle, T.J. 1994. The SAUR open reading frame contains a cis element responsible for cycloheximide-mediated mRNA accumulation. Plant Mol. Biol. 24: 715–723.PubMedCrossRefGoogle Scholar
  35. Li, Y., Wu, Y.H., Hagen, G. and Guilfoyle, T.J. 1999. Expression of the auxin-inducible GH3 promoter GUS fusion gene as a useful molecular marker for auxin physiology. Plant Cell Physiol. 40: 675–682.CrossRefGoogle Scholar
  36. Liscum, E. and Reed, J.W. 2002. Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol. Biol. 49: 387–400.PubMedCrossRefGoogle Scholar
  37. Liu, Z.-B., Ulmasov, T., Shi, X., Hagen, G. and Guilfoyle, T.J. 1994. The soybean GH3 promoter contains multiple auxin-inducible elements. Plant Cell 6: 645–657.PubMedGoogle Scholar
  38. Luerssen, H., Kirik, V., Herrmann, P. and Misera, S. 1998. FUSCA3 encodes a protein with a conserved VPl/ABI3-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. Plant J. 15: 755–764.PubMedCrossRefGoogle Scholar
  39. McCarty, D.R., Hattori, T., Carson, C.B., Vasil, V., Lazar, M. and Vasil, I.K. 1991. The viviparous-1 developmental gene of maize encodes a novel transcriptional activator. Cell 66: 895–905.PubMedCrossRefGoogle Scholar
  40. McClure, B.A. and Guilfoyle, T. 1987. Characterization of a class of small auxin-inducible soybean polyadenylated RNAs. Plant Mol. Biol. 9:611–623.CrossRefGoogle Scholar
  41. McClure, B.A. and Guilfoyle, T.J. 1989. Rapid redistribution of auxin-regulated RNAs during gravitropism. Science 243: 91–93.PubMedCrossRefGoogle Scholar
  42. McClure, B.A., Hagen, G., Brown, C.S., Gee, M.A. and Guilfoyle, T.J. 1989. Transcription, organization, and sequence of an auxin-regulated gene cluster in soybean. Plant Cell 1: 229–239.PubMedGoogle Scholar
  43. Mockaitis, K. and Howell, S.H. 2000. Auxin induces mitogenic activated protein kinase (MAPK) activation in roots of Arabidopsis seedlings. Plant J. 24: 785–796.PubMedCrossRefGoogle Scholar
  44. Morgan, K.E., Zarembinski, T.I., Theologis, A. and Abel, S. 1999. Biochemical characterization of recombinant polypeptides corresponding to the predicted βαα fold in Aux IAA proteins. FEBS Lett. 454: 283–287.PubMedCrossRefGoogle Scholar
  45. Murfett, J., Wang, X-J., Hagen, G. and Guilfoyle, T.J. 2001. Identification of Arabidopsis histone deacetylase HDA6 mutants that affect transgene expression. Plant Cell 13: 1047–1061.PubMedGoogle Scholar
  46. Nakazawa, M., Yabe, N., Ichikawa, T., Yamamoto, Y.Y., Yoshizumi, T. Hasunuma, K. and Matsui, M. 2001. 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. Plant J. 25: 213–221.PubMedCrossRefGoogle Scholar
  47. Nebenfuhr, A., White, T.J. and Lomax, T.L. 2000. The diageotropica mutation alters auxin induction of a subset of the Aux/IAA gene family in tomato. Plant Mol. Biol. 44: 73–84.PubMedCrossRefGoogle Scholar
  48. Newman, T.C., Ohme-Takagi, M., Taylor, C.B. and Green, P.J. 1993. DST sequences, highly conserved among plant SAUR genes, target reporter transcripts for rapid decay in tobacco. Plant Cell 5: 701–714.PubMedGoogle Scholar
  49. Oeller, P.W., Keller, J.A., Parks, J.E., Silbert, J.E. and Theologis, A. 1993. Structural characterization of the early indoleacetic acid-inducible genes PS-IAA4/5 and PS-IAA6, of pea (Pisum sativum L). J. Mol. Biol. 233: 789–798.PubMedCrossRefGoogle Scholar
  50. Oono, Y., Chen, Q.G., Overvoorde, P.J., Kohler, C. and Theologis, A. 1998. age mutants of Arabidopsis exhibit altered auxin-regulated gene expression. Plant J. 10: 1649–1662.Google Scholar
  51. Osterlund, M.T., Ang, L.-H. and Deng, X.-W. 1999. The role of COP1 in repression of Arabidopsis photomorphogenic development. Trends Cell Biol. 9: 113–118.PubMedCrossRefGoogle Scholar
  52. Ouellet, F., Overvoorde, P.J. and Theologis, A. 2001. IAA17/AXR3. Biochemical insight into an auxin mutant phenotype. Plant Cell 13:829–842.PubMedGoogle Scholar
  53. Philippar, K., Fuchs, I., Luthen, H., Hoth, S., Bauer, C.S., Haga, K., Thiel, G., Ljung, K., Sandberg, G., Bottger, M., Becker, D. and Hedrich, R. 1999. Auxin-induced K(+) channel expression represents an essential step in coleoptile growth and gravitropism. Proc. Natl. Acad. Sci. USA 96: 12186–12191.PubMedCrossRefGoogle Scholar
  54. Reed, J.W., Elumalai, R.P. and Chory, J. 1998. Suppressors of an Arabidopsis thaliana phyB mutation identify genes that control light signaling and hypocotyl elongation. Genetics 148: 1295–1310.PubMedGoogle Scholar
  55. Rogg, L.E., Lasswell, J. and Bartel, B. 2001. A gain-of-function mutation in iaa28 suppresses lateral root development. Plant Cell 13: 465–480.PubMedGoogle Scholar
  56. Roux, C. and Perrot-Rechenmann, C. 1997. Isolation by differential display and characterizationof a tobacco auxin-responsive cDNA Nt-gh3, related to GH3. FEBS Lett. 419: 131–136.PubMedCrossRefGoogle Scholar
  57. Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J., Benfey, P., Leyser, O., Bechtold, N., Weisbeek, P. and Scheres, B. 1999. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99: 463–472.PubMedCrossRefGoogle Scholar
  58. Sessions, A., Nemhauser, J.L., McColl, A., Roe, J.L., Feldman, K.A. and Zambryski, PC. 1997. ETTIN patterns the Arabidopsis floral meristem and reproductive organs. Development 124: 4481–4491.PubMedGoogle Scholar
  59. Singh, K., Dennis, E.S., Ellis, J.G., Llewellyn, D.J., Tokuhisa, J.G., Wahleithner, J.A. and Peacock, W.J. 1990. OCSBF-1, a maize ocs enhancer binding factor: isolation and expression during development. Plant Cell 1: 891–903.Google Scholar
  60. Sitbon, F. and Perrot-Rechenmann, C. 1997. Expression of auxin-regulated genes. Physiol. Plant. 100: 443–455.CrossRefGoogle Scholar
  61. Swarup, R., Parry, G., Graham, N., Allen, T. and Bennett, M.S. 2002. Auxin cross-talk: integration of signalling pathways to control plant development. Plant Mol. Biol. 49: 409–424.CrossRefGoogle Scholar
  62. Theologis, A., Huynh, T.V. and Davis, R.W 1985. Rapid induction of specific mRNAs by auxin in pea epicotyl tissue. J. Mol. Biol. 183: 53–68.PubMedCrossRefGoogle Scholar
  63. Tian, Q. and Reed, J.W. 1999. Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development 126: 711–721.PubMedGoogle Scholar
  64. Timpte, C., Lincoln, C., Pickett, F.B., Turner, J. and Estelle, M. 1995. The AXR1 and AUX1 genes of Arabidopsis function in separate auxin-response pathways. Plant J. 8: 561–569.PubMedCrossRefGoogle Scholar
  65. Ulmasov, T., Liu, Z-B., Hagen, G. and Guilfoyle, T.J. 1995. Composite structure of auxin response elements. Plant Cell 7: 1611–1623.PubMedGoogle Scholar
  66. Ulmasov, T., Hagen, G. and Guilfoyle, T.J. 1994. The ocs element in the soybean GH2/4 promoter is activated by both active and inactive auxin and salicylic acid analogs. Plant Mol. Biol. 26: 1055–1064.PubMedCrossRefGoogle Scholar
  67. Ulmasov, T Hagen, G. and Guilfoyle, T.J. 1997a. ARF1, a transcription factor that binds auxin response elements. Science 276: 1865–1868.PubMedCrossRefGoogle Scholar
  68. Ulmasov, T., Murfett, J., Hagen, G. and Guilfoyle, T.J. 1997b. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963–1971.PubMedGoogle Scholar
  69. Ulmasov, T., Hagen, G. and Guilfoyle, T.J. 1999a. Activation and repression of transcription by auxin response factors. Proc. Natl. Acad. Sci. USA 96: 5844–5849.PubMedCrossRefGoogle Scholar
  70. Ulmasov, T., Hagen, G. and Guilfoyle, T.J. 1999b. Dimerization and DNA binding of auxin response factors. Plant J. 19: 309–319.PubMedCrossRefGoogle Scholar
  71. Walker, J.C. and Key, J.L. 1982. Isolation of cloned cD-NAs to auxin-responsive poly(A) RNAs of elongating soybean hypocotyl. Proc. Natl. Acad. Sci. USA 79: 7185–7189.PubMedCrossRefGoogle Scholar
  72. Worley, C.K., Zenser, N., Ramos, J., Rouse, D., Leyser, O., Theologis, A. and Callis, J. 2000. Degradation of Aux/IAA proteins is essential for normal auxin signalling. Plant J. 21: 553–562.PubMedCrossRefGoogle Scholar
  73. Wright, R., Hagen, G. and Guilfoyle, T. 1987. An auxin-induced polypeptide in dicot plants. Plant Mol. Biol. 9: 625–635.CrossRefGoogle Scholar
  74. Xie, Q., Frugis, G., Colgan, D. and Chua, N-H. 2000. Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev. 14: 3024–3036.PubMedCrossRefGoogle Scholar
  75. Yamamoto, K.T., Mori, H. and Imaseki, H. 1992 cDNA cloning of indole-3-acetic acid-regulated genes:Aux22 and SAUR from mung bean (Vigna radiata) hypocotyl tissue. Plant Cell Physiol. 33: 93–97.Google Scholar
  76. Yang, T. and Poovaiah, B.W. 2000. Molecular and biochemical evidence for the involvement of calcium/calmodulin in auxin action. J. Biol. Chem. 275: 3137–3143.PubMedCrossRefGoogle Scholar
  77. Zhao Y., Christensen, S.K., Fankhauser, C., Cashman, J.R., Cohen, J.D., Weigel, D. and Chory, J. 2001. A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291: 306–309.PubMedCrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  1. 1.Department of BiochemistryUniversity of MissouriColumbiaUSA

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