Skip to main content
Log in

Role of auxin in regulating Arabidopsis flower development

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

To elucidate the role of auxin in flower morphogenesis, its distribution patterns were studied during flower development in Arabidopsis thaliana (L.) Heynh. Expression of DR5::GUS was regarded to reflect sites of free auxin, while immunolocalization with auxin polyclonal antibodies visualized conjugated auxin distribution. The youngest flower bud was loaded with conjugated auxin. During development, the apparent concentration of free auxin increased in gradual patterns starting at the floral-organ tip. Anthers are major sites of high concentrations of free auxin that retard the development of neighboring floral organs in both the acropetal and basipetal directions. The IAA-producing anthers synchronize flower development by retarding petal development and nectary gland activity almost up to anthesis. Tapetum cells of young anthers contain free IAA which accumulates in pollen grains, suggesting that auxin promotes pollen-tube growth towards the ovules. High amounts of free auxin in the stigma induce a wide xylem fan immediately beneath it. After fertilization, the developing embryos and seeds show elevated concentrations of auxin, which establish their axial polarity. This developmental pattern of auxin production during floral-bud development suggests that young organs which produce high concentrations of free IAA inhibit or retard organ-primordium initiation and development at the shoot tip.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

DR5::GUS :

Auxin response element fused to β-glucuronidase

IAA:

Indole-3-acetic acid

NAA:

α-naphthaleneacetic acid

ESM:

Electronic supplementary material

References

  • Aloni R (1987) Differentiation of vascular tissues. Annu Rev Plant Physiol 38:179–204

    Article  Google Scholar 

  • Aloni R (2001) Foliar and axial aspects of vascular differentiation: hypotheses and evidence. J Plant Growth Regul 20:22–34

    Article  CAS  Google Scholar 

  • Aloni R (2004) The induction of vascular tissues by auxin. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action! Kluwer, Dordrecht, pp 471–492

    Google Scholar 

  • Aloni R, Schwalm K, Langhans K, Ullrich CI (2003) Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis. Planta 216:841–853

    PubMed  CAS  Google Scholar 

  • Alvarez J, Smyth DR (1999) CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMUS. Development 126:2377–2386

    PubMed  CAS  Google Scholar 

  • Alvarez J, Smyth DR (2002) CRABS CL A W and SPATULA genes regulate growth and pattern formation during gynoecium development in Arabidopsis thaliana. J Plant Sci 16:17–41

    Article  Google Scholar 

  • Avsian-Kretchmer O, Cheng J-C, Chen L, Moctezuma E, Sung ZR (2002) IAA distribution coincides with vascular differentiation pattern during Arabidopsis leaf ontogeny. Plant Physiol 130:199–209

    Article  PubMed  CAS  Google Scholar 

  • Baum SF, Eshed Y, Bowman JL (2001) The Arabidopsis nectary is an ABC-independent floral structure. Development 128:4657–4667

    PubMed  CAS  Google Scholar 

  • Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602

    Article  PubMed  Google Scholar 

  • Bennett SRM, Alvarez J, Bossinger G, Smyth DR (1995) Morphogenesis in pinoid mutant of Arabidopsis thaliana. Plant J 8:505–520

    Article  CAS  Google Scholar 

  • Berleth T, Chatfield S (2002) Embryogenesis: pattern formation from a single cell. In: Somerville C, Meyerowitz E (eds) The Arabidopsis book. American Society of Plant Biologists. http://www.aspb.org/publications/arabidopsis/toc.cfm

  • Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52

    Article  PubMed  CAS  Google Scholar 

  • Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20

    PubMed  CAS  Google Scholar 

  • Bowman JL, Baum SF, Eshed Y, Putterill J, and Alvarez J (1999) Molecular genetics of gynoecium development in Arabidopsis. Curr Top Develop Biol 45:155–205

    CAS  Google Scholar 

  • Christensen SK, Dagenalis N, Chory J, Weigel D (2000) Regulation of auxin response by the protein kinase PINOID. Cell 100:469–478

    Article  PubMed  CAS  Google Scholar 

  • Endress PK (1994) Diversity and evolutionary biology of tropical flowers. Cambridge University Press, Cambridge

    Google Scholar 

  • Eshed Y, Baum SF, Bowman JL (1999) Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99:199–209

    Article  PubMed  CAS  Google Scholar 

  • Friml J, Wisniewska J, Benková E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809

    PubMed  Google Scholar 

  • Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153

    Article  PubMed  CAS  Google Scholar 

  • Goto K, Kyozuka J, Bowman JL (2001) Turning floral organs into leaves, leaves into floral organs. Curr Opin Genetics Develop 11:449–456

    Article  CAS  Google Scholar 

  • Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5:387–405

    CAS  Google Scholar 

  • Jürgens G (2001) Apical-basal pattern formation in Arabidopsis embryogenesis. EMBO J 20:3609–3616

    Article  PubMed  Google Scholar 

  • Langhans M, Ratajczak R, Lützelschwab M, Michalke W, Wächter R, Fischer-Schliebs E, Ullrich CI (2001) Immunolocalization of plasma-membrane H+ -ATPase and tonoplast-type pyrophosphatase in the plasma membrane of the sieve element-companion cell complex in the stem of Ricinus communis L. Planta 213:11–19

    Article  PubMed  CAS  Google Scholar 

  • Ljung K, Hull AK, Kowalczyk M, Marchant A, Celenza J, Cohen JD, Sandberg G (2002) Biosynthesis, conjugation, catabolism and homeostasis of indol-3-acetic acid in Arabidopsis. Plant Mol Biol 50:309–332

    Article  Google Scholar 

  • Marchant A, Bhalerao O, Casimiro I, Eklof J, Casero PJ, Bennett M, Sandberg G (2002) AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell 14:589–597

    Article  PubMed  CAS  Google Scholar 

  • Mattsson J, Ckurshumova W, Berleth T (2003) Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol 131:1327–1339

    Article  PubMed  CAS  Google Scholar 

  • Müller A, Düchting P, Weiler EW (2002) A multiple GC-MS/MS technique for the sensitive and qualitative single-run analysis of acidic phytohormones and related compounds, and its application to Arabidopsis thaliana. Planta 216:44–56

    Article  PubMed  CAS  Google Scholar 

  • Nakamura A, Higuchi K, Goda H, Fujiwara T, Sawa S, Koshiba T, Shimada Y, Yoshida S (2003) Brassinolide induces IAA5, IAA19, and DR5, a synthetic auxin response element in Arabidopsis, implying a cross talk point of brassinosteroid and auxin signaling. Plant Physiol 133:1843–1853

    Article  PubMed  CAS  Google Scholar 

  • Nemhauser JL, Zambryski PC, Roe JL (1998) Auxin signaling in Arabidopsis flower development?. Curr Opin Plant Biol 1:531–535

    Article  PubMed  CAS  Google Scholar 

  • Nemhauser JL, Feldman LJ, Zambryski PC (2000) Auxin and ETTIN in Arabidopsis gynoecium morphogenesis. Development 127:3877–3888

    PubMed  CAS  Google Scholar 

  • Oka M, Miyamoto K, Okada K, Ueda J (1999) Auxin polar transport and flower formation in Arabidopsis thaliana transformed with indoleacetamide hydrolase (iaaH) gene. Plant Cell Physiol 40:231–237

    PubMed  CAS  Google Scholar 

  • Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3:677–684

    Article  PubMed  CAS  Google Scholar 

  • Petrášek J, Černá A, Schwarzerová, K, Elčkner M, Morris DA, Zažímalova E (2003) Do phytotropins inhibit auxin efflux by impairing vesicle traffic?. Plant Physiol 131:254–263

    Article  PubMed  CAS  Google Scholar 

  • Rampey RA, LeClere S, Kowalczyk M, Ljung K, Sandberg G, Bartel B (2004) A family of auxin-conjugate hydrolases that contributes to free indole-3-acetic acid levels during Arabidopsis germination. Plant Physiol 135:978–988

    Article  PubMed  CAS  Google Scholar 

  • Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507–518

    Article  PubMed  CAS  Google Scholar 

  • Reinhardt D, Pesce E-R, Stieger P, Mandel T, Baltensperger, Bennett M, Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426:255–260

    Article  PubMed  CAS  Google Scholar 

  • Roe JL, Nemhauser JL, Zambryski PC (1997) TOUSLEND participates in apical tissue formation during gynoecium development in Arabidopsis. Plant Cell 9:335–353

    Article  PubMed  CAS  Google Scholar 

  • Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in Arabidopsis root. Cell 99:463–472

    Article  PubMed  CAS  Google Scholar 

  • Sachs T (1969) Polarity and the induction of organized vascular tissues. Ann Bot 33:263–275

    Google Scholar 

  • Sessions RA, Zambryski PC (1995) Arabidopsis gynoecium structure in the wild type and ettin mutants. Development 121:1519–1532

    PubMed  CAS  Google Scholar 

  • Sessions A, Nemhauser JL, McColl A, Roe JL, Feldman KA, Zambryski PC (1997) ETTIN patterns in the Arabidopsis floral meristem and reproductive organ. Development 124:4481–4491

    PubMed  CAS  Google Scholar 

  • Skoog F, Miller CO (1965) Chemical regulation of growth and organ formation in plant tissue cultured in vitro. In: Bell E (ed) Molecular and Cellular Aspects of Development. Harper and Row, New York, pp 481–494

    Google Scholar 

  • Smyth DR (2005) Morphogenesis of flowers – our evolving view. Plant Cell 17:330–341

    Article  PubMed  CAS  Google Scholar 

  • Souter M, Lindsey K (2000) Polarity and signalling in plant embryogenesis. J Exp Bot 51:971–983

    Article  PubMed  CAS  Google Scholar 

  • Sussex I (1989) Developmental programing of shoot meristem. Cell 56:225–229

    Article  PubMed  CAS  Google Scholar 

  • Taiz L, Zeiger E (2002) Plant physiology, 3rd ed. Sinauer, Sunderland, Mass, USA

    Google Scholar 

  • Thimann KV, Skoog F (1933) Studies on the growth hormone of plants III The inhibiting action of growth substance on plant development. Proc Nat Acad Sci USA 19:712–716

    Article  Google Scholar 

  • Thimann KV, Skoog F (1934) On the inhibition of development and other functions of growth substances in Vicia faba. Proc Royal Soc London B 114:317–339

    Article  CAS  Google Scholar 

  • Thimann KV, Sachs T, Mathur KN (1971) The mechanism of apical dominance in Coleus. Physiol Plant 24:68–72

    Article  CAS  Google Scholar 

  • Turner S, Sieburth LE (2002) Vascular patterning. In CR Somerville, EM Meyerowitz, eds, The Arabidopsis Book, American Society of Plant Biologists. Rockville, MD, http://www.aspb.org/publications/arabidopsis/toc.cfm

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    Article  PubMed  CAS  Google Scholar 

  • Veselov SY, Kudoyarova GR, Egutkin NL, Gyuli-Zade VZ, Mustafina AR, Kof EM (1992) Modified solvent partitioning scheme providing increased specificity and rapidity of immunoassay for indole-3-acetic acid. Physiol Plant 86:93–96

    Article  CAS  Google Scholar 

  • Veselov D, Langhans M, Hartung W, Aloni R, Feussner I, Götz C, Veselova S, Schlomski S, Dickler C, Bächmann K, Ullrich CI (2003) Development of Agrobacterium tumefaciens C58-induced plant tumors and impact on host shoots are controlled by a cascade of jasmonic acid, auxin, cytokinin, ethylene and abscisic acid. Planta 216:512–522

    PubMed  CAS  Google Scholar 

  • Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78:203–209

    Article  PubMed  CAS  Google Scholar 

  • Zgurski JM, Shama R, Bolokoski DA, Schultz EA (2005) Asymmetric auxin response precedes asymmetric growth and differentiation of asymmetric leaf1 and asymmetric leaf2 Arabidopsis leaves. Plant Cell 17:77–91

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Profs. Tom J. Guilfoyle (University of Missouri, Columbia Mo, USA) for the kind gift of the DR5::GUS transformed seeds of Arabidopsis thaliana, Stanislav Veselov (University of Ufa, Russia) for the kind gift of polyclonal auxin antibodies, Rivka Dulberger (Tel Aviv University, Israel) for insightful advice, Dr. Martha Schwartz and Varda Wexler (Tel Aviv University, Israel) for helpful assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Roni Aloni.

Additional information

This paper is dedicated to Orna Aloni for continuous support and management over many years.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aloni, R., Aloni, E., Langhans, M. et al. Role of auxin in regulating Arabidopsis flower development. Planta 223, 315–328 (2006). https://doi.org/10.1007/s00425-005-0088-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-005-0088-9

Keywords

Navigation