Skip to main content
Log in

Putative dual pathway of auxin transport in organogenesis of Arabidopsis

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

Abstract

In Arabidopsis, damage to the superficial acropetal polar auxin transport (PAT) inhibits generative but not vegetative organ initiation. In order to verify whether in a vegetative phase auxin can be transported to the meristem in a different way, the research on wild-type and plants with defective PAT was performed. Distance from the differentiated vascular elements to the shoot apical meristem (SAM) was measured for Arabidopsis cultured in different experimental systems. The influence of this distance on the ability to induce organogenesis as well as transport of the fluorescent dye to the SAM, and the LEAFY gene expression were analyzed. The youngest protoxylem elements were used as a marker of the vascular tissues. The distance of protoxylem to the SAM and organogenesis were interrelated. Organ initiation occurred only when protoxylem was localized near to the SAM. Experimental elongation of internodes in a vegetative rosette caused an increase in the distance between protoxylem and the SAM organogenic zone. Thus, the inhibition of organ initiation took place already during the vegetative phase. The results suggest the presence of at least two pathways of acropetal transport of auxin inducing organogenesis: one superficial way through PAT, and the second, putative one, internal through the vascular system. Possibly, organogenesis is completely blocked only when both these pathways are dysfunctional.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

GA:

Gibberellic acid

IAA:

Indole-3-acetic acid

NPA:

N-1-naphthylphthalamic acid

PAT:

Polar auxin transport

SAM:

Shoot apical meristem

References

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

    CAS  PubMed  Google Scholar 

  • Avsian-Kretchmer O, Cheng JC, Chen L, Moctezuma E, Renee Sung Z (2002) Indole acetic acid distribution coincides with vascular differentiation pattern during Arabidopsis leaf ontogeny. Plant Physiol 130:199–209

    Article  CAS  PubMed  Google Scholar 

  • Bainbrigde K, Guyomarch S, Bayer E, Swarup R, Bennett M, Mandel T, Kuhlemeier C (2008) Auxin influx carriers stabilize phyllotactic patterning. Gene Dev 22:810–823

    Article  Google Scholar 

  • Baker DA (2000) Vascular transport of auxins and cytokinins in Ricinus. J Plant Growth Regul 32:157–160

    Article  CAS  Google Scholar 

  • Banasiak AS, Zagórska-Marek B (2006) Signals flowing from mature tissues to shoot apical meristem affect phyllotaxis in coniferous shoot. Acta Soc Bot Pol 75:113–121

    Google Scholar 

  • Bayer EM, Smith RS, Mandel T, Nakayama N, Sauer M, Prusinkiewicz P, Kuhlemeier C (2009) Integration of transport-based models for phyllotaxis and midvein formation. Gene Dev 23:373–384

    Article  CAS  PubMed  Google Scholar 

  • Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová 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 

  • Berleth T, Sachs T (2001) Plant morphogenesis: long distance coordination and local patterning. Curr Opin Plant Biol 4:57–62

    Article  CAS  PubMed  Google Scholar 

  • Berleth T, Mattsson J, Hardtke S (2000) Vascular continuity and auxin signals. Trends Plant Sci 5:387–393

    Article  CAS  PubMed  Google Scholar 

  • Berleth T, Scarpella E, Prusinkiewicz P (2007) Towards the systems biology of auxin-transport-mediated patterning. Trends Plant Sci 4:1360–1385

    Google Scholar 

  • Blazquez MA, Weigel D (1999) Independent regulation of flowering by phytochrome B and gibberellins in Arabidopsis. Plant Physiol 120:1025–1032

    Article  CAS  PubMed  Google Scholar 

  • Cho HT, Cosgrove DJ (2000) Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:9783–9788

    Article  CAS  PubMed  Google Scholar 

  • de Reuille PB, Bohn-Courseau I, Ljung K, Morin H, Carraro N, Godin C, Traas J (2006) Computer simulations reveal properties of the cell-cell signaling network at the shoot apex in Arabidopsis. Proc Natl Acad Sci USA 103:1627–1632

    Article  PubMed  Google Scholar 

  • Dengler NG (2001) Regulation of vascular development. J Plant Growth Regul 20:1–13

    Article  CAS  Google Scholar 

  • Dengler NG (2006) The shoot apical meristem and development of vascular architecture. Can J Bot 84:1660–1671

    Article  CAS  Google Scholar 

  • Eriksson S, Böhlenius H, Moritz T, Nilsson O (2006) GA4 is the active gibberellin in the regulation of LEAFY transcription and Arabidopsis floral initiation. Plant Cell 18:2172–2181

    Article  CAS  PubMed  Google Scholar 

  • Esau K (1965) Plant anatomy, 2nd edn. John Wiley, New York

    Google Scholar 

  • Fleming AJ, McQueen-Mason S, Mandel T, Kuhlemeier C (1997) Induction of leaf primordia by the cell wall protein expansin. Science 276:1415–1418

    Article  CAS  Google Scholar 

  • Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230

    Article  PubMed  Google Scholar 

  • Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112:219–230

    Article  CAS  PubMed  Google Scholar 

  • Girolami G (1953) Relation between phyllotaxis and primary vascular organization in Linum. Am J Bot 40:618–625

    Article  Google Scholar 

  • Hanzawa Y, Takahashi T, Michael AJ, Burtin D, Long D, Pineiro M, Coupland G, Komeda Y (2000) ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J 16:4248–4256

    Article  Google Scholar 

  • Heisler MG, Jönsson H (2006) Modeling auxin transport and plant development. J Plant Growth Regul 25:302–312

    Article  CAS  Google Scholar 

  • Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 15:1899–1911

    Article  CAS  PubMed  Google Scholar 

  • Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Company, Inc, New York and London

    Google Scholar 

  • Jones SE, DeMeo JS, Davies NW, Noonan SE, Ross JJ (2005) Stems of the Arabidopsis pin1–1 mutant are not deficient in free indole-3-acetic acid. Planta 222:530–534

    Article  CAS  PubMed  Google Scholar 

  • Jönsson H, Heisler MG, Shapiro BE, Meyerowitz EM, Mjolsness E (2006) An auxin-driven polarized transport model for phyllotaxis. Proc Natl Acad Sci USA 103:1633–1638

    Article  PubMed  Google Scholar 

  • Larson PR (1975) Development and organization of the primary vascular system in Populus deltoides according to phyllotaxy. Am J Bot 62:1084–1099

    Article  Google Scholar 

  • Larson PR (1977) Phyllotactic transitions in the vascular system of Populus deltoids Bartr. as determined by 14C labeling. Planta 134:241–249

    Article  Google Scholar 

  • Mattsson J, Sung ZR, Berleth T (1999) Responses of plant vascular systems to auxin transport inhibition. Development 126:2979–2991

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230

    Article  PubMed  Google Scholar 

  • Peaucelle A, Louvet R, Johansen JN, Höfte H, Laufs P, Pelloux J, Mouille G (2008) Arabidopsis phyllotaxis is controlled by methyl-estrification status of cell-wall pectins. Curr Biol 18:1943–1948

    Article  CAS  PubMed  Google Scholar 

  • Pien S, Wyrzykowska J, McQueen-Mason S, Smart C, Flaming A (2001) Local expression of expansin induces the entire process of leaf development and modifies leaf shape. Proc Natl Acad Sci USA 98:11812–11817

    Article  CAS  PubMed  Google Scholar 

  • Reinhardt D (2005) Phyllotaxis—a new chapter in an old tale about beauty and magic numbers. Curr Opin Plant Biol 8:487–493

    Article  CAS  PubMed  Google Scholar 

  • Reinhardt D, Wittwer F, Mandel T, Kuhlemeier C (1998) Localized upregulation of a new expansin gene predicts the site of leaf formation in the tomato meristem. Plant Cell 10:1427–1437

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ruzin SE (1999) Plant microtechnique and microscopy. Oxford University Press, New York

    Google Scholar 

  • Schwabe WW (1984) Phyllotaxis. In: Barlow PW, Carr DJ (eds) Positional controls in plant development. Cambridge University Press, Cambridge, pp 403–440

    Google Scholar 

  • Smith RS, Guyomarc`h S, Mandel T, Reinhardt D, Kuhlemeier C, Prusinkiewicz P (2006) A plausible model of phyllotaxis. Proc Natl Acad Sci USA 5:1301–1306

    Google Scholar 

  • Steeves TA, Sussex IM (1989) Patterns in plant develompent, 2nd edn. Cambridge University Press, New York

    Book  Google Scholar 

  • Stieger PA, Reinhardt D, Kuhlemeier C (2002) The auxin influx carrier is essential for correct leaf positioning. Plant J 32:509–517

    Article  CAS  PubMed  Google Scholar 

  • Stoma S, Lucas M, Chopard J, Schaedel M, Traas J, Godin C (2008) Flux-based transport enhancement as a plausible unifying mechanism for auxin transport in meristem development. PLoS Comput Biol 4(10):e1000207

    Google Scholar 

  • Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M (2001) Localization of the auxin permease AUX1 suggest two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Gene Dev 15:2648–2653

    Article  CAS  PubMed  Google Scholar 

  • Tocquin P, Corbesier L, Havelange A, Pieltain A, Kurtem E, Bernier G, Périlleux (2003) A novel high efficiency, low maitenance, hydroponic system for synchronous growth and flowering of Arabidopsis thaliana. BMC Plant Biol 3:2

  • Weberling F (1989) Morphology of flowers and inflorescences. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Zagórska-Marek B, Banasiak A (2000) Related to phyllotaxis interlocked systems of vascular sympodia and cortical resin canals in Abies and Picea shoots. Acta Soc Bot Pol 3:165–172

    Google Scholar 

  • Zažimalová E, Křeček P, Skůpa P, Hoyerová K, Petrášek J (2007) Polar transport of plant hormone auxin—the role of PIN-FORMED (PIN) proteins. Cell Mol Life Sci 64:1621–1637

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

I would like to thank Professor B. Zagórska-Marek (Uniwersity of Wrocław, Poland), Professor E. Mellerowicz (SLU, Sweden) and colleagues from department (E. Gola, E. Myskow, K. Sokołowska) for all suggestions and discussions; P. Otręba (M.Sc.), A. Waligóra and M. Turzańska (M.Sc.) for technical help. This research was supported by the Ministry of Science and Higher Education (grant no. NN303 027037).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alicja Banasiak.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Banasiak, A. Putative dual pathway of auxin transport in organogenesis of Arabidopsis . Planta 233, 49–61 (2011). https://doi.org/10.1007/s00425-010-1280-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-010-1280-0

Keywords

Navigation