Skip to main content
SpringerLink
Log in

The auxin-induced transcriptome for etiolated Arabidopsis seedlings using a structure/function approach

  • Original Paper
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

To increase our understanding of the mode of action of auxin, we analyzed auxin-induced changes in the Arabidopsis transcriptome with microarrays representing 20,426 Arabidopsis genes. Treatment of etiolated seedlings with low concentrations of the auxin, indole-3-acetic acid (IAA), decreased the expression levels of 23 genes, whereas it increased the expression levels of 47 genes within 20 min. After 40 min, the directional trend in genomic change was predominantly an increase in gene expression. Among the most rapidly induced changes are those in genes encoding transcription factors. Promoter regions of transiently induced genes contained DNA motifs that bind auxin response (ARFAT) and silence element binding factors whereas genes induced by IAA during the entire experimental period contained MYC and ARFAT DNA motifs at higher frequencies. Six structurally diverse auxins were analyzed to determine genes that are unique to a specific auxin, as well as a common set of genes that are rapidly regulated by all tested auxins, thus enabling the identification of shared DNA motifs. In addition to ARFAT, analysis of promoter regions of genes induced by all six auxins revealed the presence of an abscisic-acid-responsive DC3 promoter-binding factor and low temperature responsive elements suggesting a possible role for abscisic acid in modulating auxin-induced responses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1A–C
Fig. 2
Fig. 3A-C
Fig. 4A, B

Similar content being viewed by others

References

  • Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell 9:1859–1868

    CAS  PubMed  Google Scholar 

  • Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111:9–17

    PubMed  Google Scholar 

  • Abel S, Nguyen MD, Theologis A (1995) The PS-IAA4/5-like family of early auxin-inducible mRNAs in Arabidopsis thaliana. J Mol Biol 251:533–549

    Article  CAS  PubMed  Google Scholar 

  • Boerjan W, Cervera MT, Delarue M, Beeckman T, Dewitte W, Bellini C, Caboche M, Van Oncklen H, Inze D (1995) superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell 7:1405–1419

    CAS  PubMed  Google Scholar 

  • Boyle B, Brisson N (2001) Repression of the defense gene PR-10a by the single-stranded DNA binding protein SEBF. Plant Cell 13:2525–2537

    Article  CAS  PubMed  Google Scholar 

  • Busk PK, Pages M (1998) Regulation of abscisic acid-induced transcription. Plant Mol Biol 37:425–443

    CAS  PubMed  Google Scholar 

  • Che P, Gingerich DJ, Lall S, Howell SH (2002) Global and hormone-induced gene expression changes during shoot development in Arabidopsis. Plant Cell 14:2771–2785

    Google Scholar 

  • Edgerton MD, Tropsha A, Jones AM (1994) The auxin-binding site of auxin-binding protein 1. Phytochemistry 35:1111–1123

    Article  CAS  Google Scholar 

  • Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609

    Google Scholar 

  • Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4:1251–1261

    PubMed  Google Scholar 

  • Guilfoyle TJ, Ulmasov T, Hagen G (1998) The ARF family of transcription factors and their role in plant hormone responsive transcription. Cell Mol Life Sci 54:619–627

    Article  CAS  PubMed  Google Scholar 

  • Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385

    Article  CAS  PubMed  Google Scholar 

  • Hagen G, Kleinschmidt A, Guilfoyle T (1984) Auxin regulated gene expression in intact soybean hypocotyl and excised hypocotyl sections. Planta 162:147–153

    CAS  Google Scholar 

  • Hansen H, Grossmann K (2000) Auxin-induced ethylene triggers abscisic acid biosynthesis and growth inhibition. Plant Physiol 124:1437–1448

    CAS  PubMed  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korennaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300

    CAS  PubMed  Google Scholar 

  • Hughes TR, Mao M, Jones AR, Burchard J, Marton MJ, Shannon KW, Lefkowitz SM, Ziman M, Schelter JM, Meyer MR, Kobayashi S, Davis C, Dai H, He YD, Stephaniants SB, Cavet G, Walker WL, West A, Coffey E, Shoemaker DD, Stoughton R, Blanchard AP, Friend SH, Linsley PS (2001) Expression profiling using microarrays fabricated by an ink-jet oligonucleotide synthesizer. Nat Biotechnol 19:342–347

    Article  CAS  PubMed  Google Scholar 

  • Imamura H, Tanaka K, Hihara T, Umikawa M, Kamei T, Takahashi K, Sasaki T, Takai Y (1997) Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae. EMBO J 16:2745–2755

    CAS  PubMed  Google Scholar 

  • Jiang C, Iu B, Singh J (1996) Requirement of a CCGAC cis-acting element for cold induction of the BN115 gene from winter Brassica napus. Plant Mol Biol 30:679–684

    CAS  PubMed  Google Scholar 

  • Jones AM (1994) Auxin-binding proteins. Annu Rev Plant Physiol Plant Mol Biol 45:393–420

    Google Scholar 

  • Kim SY, Chung HJ, Thomas TL (1997) Isolation of a novel class of bZIP transcription factors that interact with ABA-responsive and embryo-specification elements in the Dc3 promoter using a modified yeast one-hybrid system. Plant J 11:1237–1251

    Article  CAS  PubMed  Google Scholar 

  • Melhado LL, Jones AM, Ho T-HD, Leonard NJ (1981) Azido auxins: synthesis and biological activity of fluorescent labeling agents. Plant Physiol 68:469–475

    CAS  Google Scholar 

  • Napier R (1995) Towards an understanding of ABP1. J. Exp Bot 46:1787–1795

    CAS  Google Scholar 

  • Overbeek J van (1964) Survey of mechanism of herbicide action. Academic Press, London

  • Reed JW, Elumalai RP, Chory J (1998) Suppressors of an Arabidopsis thaliana phyB mutation identify genes that control light signaling and hypocotyl elongation. Genetics 148:1295–1310

    CAS  PubMed  Google Scholar 

  • Seki M, Ishida J, Narusaka M, Fujita M, Nanjo T, Umezawa T, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct Integr Genom 2(6):282–291

    Article  CAS  Google Scholar 

  • Shuai B, Reynaga-Pena CG, Springer PS (2002). The lateral organ boundaries gene defines a novel, plant-specific gene family. Plant Physiol. 129:747–761

    Google Scholar 

  • Singh KB, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436

    Article  PubMed  Google Scholar 

  • Staswick P, Tiryaki I, Rowe M (2002) 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 14:1405–1415

    Google Scholar 

  • Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040

    CAS  PubMed  Google Scholar 

  • Theologis A, Huynh TV, Davis RW (1985) Rapid induction of specific mRNAs by auxin in pea epicotyl tissue. J Mol Biol 183:53–68

    CAS  PubMed  Google Scholar 

  • Thijs G, Lescot M, Marchal K, Rombauts S, De Moor B, Rouze P, Moreau Y (2001) A higher order background model improves the detection of regulatory elements by Gibbs sampling. Bioinformatics 17:1113–1122

    Article  CAS  PubMed  Google Scholar 

  • Thijs G, Marchal K, Lescot M, Rombauts S, De Moor B, Rouze P, Moreau Y (2002) A Gibbs sampling method to detect over-represented motifs in upstream regions of coexpressed genes. J Comp Biol 9:447–464

    Article  CAS  Google Scholar 

  • Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543

    Article  CAS  PubMed  Google Scholar 

  • Ulmasov T, Hagan G, Guilfoyle T (1997) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868

    CAS  PubMed  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1999) Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci USA 96:5844–5849

    CAS  PubMed  Google Scholar 

  • Watahiki MK, Yamamoto KT (1997) The massugu1 mutation of Arabidopsis identified with failure of auxin-induced growth curvature of hypocotyl confers auxin insensitivity to hypocotyl and leaf. Plant Physiol 115:419–426

    Article  CAS  PubMed  Google Scholar 

  • Weed Society of America (eds) (1989) Herbicide handbook. Weed Society of America, Champaign, Ill.

  • Woo EJ, Marshall J, Bauly JM, Chen J-G, Venis MA, Napier RM, Pickersgill RW (2002) Crystal structure of auxin-binding protein 1 in complex with auxin. EMBO J 21:2877–2885

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Kenan Foundation and the North Carolina Biotechnology Center by a grant awarded to A.M.J. and Paradigm Genetics and by grants from NSF and NIGMS to A.M.J. We are grateful to the North Carolina Collaborative Funding Program for the major support. We thank Mike Vernon and Ani Chatterjee for technical assistance in a preliminary study utilizing the 8 K Affymetrix arrays, Doug Boyes for the suggestion of a structure/function approach in the early phase of this project and Neil Hoffmann for his discussion and guidance.

Author information

Authors and Affiliations

  1. Paradigm Genetics, 108 Alexander Drive, Research Triangle Park, NC 27709-4528, USA

    John Pufky, Yang Qiu, Mulpuri V. Rao & Patrick Hurban

  2. Department of Biology and Curriculum in Genetics and Molecular Biology, University of North Carolina, Chapel Hill, NC 27599-3280, USA

    Alan M. Jones

Authors
  1. John Pufky
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yang Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mulpuri V. Rao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patrick Hurban
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alan M. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Patrick Hurban.

Additional information

J. Pufky and Y. Qiu contributed equally to this work

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pufky, J., Qiu, Y., Rao, M.V. et al. The auxin-induced transcriptome for etiolated Arabidopsis seedlings using a structure/function approach. Funct Integr Genomics 3, 135–143 (2003). https://doi.org/10.1007/s10142-003-0093-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-003-0093-7

Keywords

Search

Navigation