Skip to main content
SpringerLink
Log in

Effects of three auxin-inducible LBD members on lateral root formation in Arabidopsis thaliana

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

Abstract

In Arabidopsis, two AUXIN RESPONSE FACTORs (ARF7 and ARF19) and several Aux/IAAs regulate auxin-induced lateral root (LR) formation. As direct targets of ARF7 and ARF19, LATERAL ORGAN BOUNDARIES DOMAIN 16 (LBD16), LBD29, and LBD18 have a biological function in the formation of lateral roots (LRs). However, the details of the functions of these three LBDs have remained unclear. Each single T-DNA insert mutant has been shown to have slightly fewer LRs than the wild type. We then created a triple mutant, which exhibited a dramatic defect in the LR formation. Our results show that the lbd mutations can lead to impairment in auxin-induced pericycle cell division and in the expression levels of some D-type cyclins (CYCDs). Simultaneously, PLETHORA (PLT) and PIN-FORMED (PIN), which have been well documented to promote cell mitotic activity and are required for auxin response effects, were down-regulated by these lbd mutations. Our results so far indicate that CYCDs, PLT, and PINs are the main targets of the LBDs. We believe that these three LBDs are involved in cell cycle progression of the pericycle in response to auxin. Overexpression of any of these three LBD genes in the triple mutant was found incapable of completely replacing the other two LBDs. The phenotypes of lbd29 mutants were not completely consistent with lbd16 or lbd18 mutants. This indicates that LBD29 may play a distinctive role compared with LBD16 or LBD18 and LBDs might play partially independent roles during the formation of LRs.

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. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

ARF:

Auxin response factor

Aux/IAA:

Auxin/indole-3-acetic acid

CYCD:

D-type cyclin

KRP:

CDK/kip-related protein

GFP:

Green fluorescent protein

LBD:

Lateral organ boundaries domain

LRM:

Lateral root meristem

LRP:

Lateral root primordium

PGP:

P-glycoprotein

PLT:

Plethora

PIN:

Pinformed

qPCR:

Quantitative real-time RT-PCR

SEM:

Scanning electron microscopy

SLR:

Solitary root

References

  • Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120

    Article  PubMed  CAS  Google Scholar 

  • Atta R, Laurens L, Boucheron-Dubuisson E, Guivarc’H A, Carnero E, Giraudat-Pautot V, Rech P, Chriqui D (2009) Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. Plant J 57:626–644

    Article  PubMed  CAS  Google Scholar 

  • Beeckman T, Burssens S, Inze D (2001) The peri-cell-cycle in Arabidopsis. J Exp Bot 52:403–411

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Berckmans B, Vassileva V, Schmid SP, Maes S, Parizot B, Naramoto S, Magyar Z, Kamei CL, Koncz C, Bogre L, Persiau G, De Jaeger G, Friml J, Simon R, Beeckman T, De Veylder L (2011) Auxin-dependent cell cycle reactivation through transcriptional regulation of Arabidopsis E2Fa by lateral organ boundary proteins. Plant Cell 23(10):3671–3683

    Article  PubMed  CAS  Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    Article  PubMed  CAS  Google Scholar 

  • Borghi L, Bureau M, Simon R (2007) Arabidopsis JAGGED LATERAL ORGANS is expressed in boundaries and coordinates KNOX and PIN activity. Plant Cell 19:1795–1808

    Article  PubMed  CAS  Google Scholar 

  • Bureau M, Rast MI, Illmer J, Simon R (2010) JAGGED LATERAL ORGAN (JLO) controls auxin dependent patterning during development of the Arabidopsis embryo and root. Plant Mol Biol 74:479–491

    Article  PubMed  CAS  Google Scholar 

  • Casimiro I, Marchant A, Bhalerao RP, Beeckman T, Dhooge S, Swarup R, Graham N, Inze D, Sandberg G, Casero PJ, Bennett M (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13:843–852

    PubMed  CAS  Google Scholar 

  • Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8:165–171

    Article  PubMed  CAS  Google Scholar 

  • De Smet I, Vanneste S, Inze D, Beeckman T (2006) Lateral root initiation or the birth of a new meristem. Plant Mol Biol 60:871–887

    Article  PubMed  CAS  Google Scholar 

  • De Smet I, Tetsumura T, De Rybel B, Frey NF, Laplaze L, Casimiro I, Swarup R, Naudts M, Vanneste S, Audenaert D, Inze D, Bennett MJ, Beeckman T (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134:681–690

    Article  PubMed  Google Scholar 

  • De Smet I, Lau S, Voss U, Vanneste S, Benjamins R, Rademacher EH, Schlereth A, De Rybel B, Vassileva V, Grunewald W, Naudts M, Levesque MP, Ehrismann JS, Inze D, Luschnig C, Benfey PN, Weijers D, Van Montagu MC, Bennett MJ, Jurgens G, Beeckman T (2010) Bimodular auxin response controls organogenesis in Arabidopsis. Proc Natl Acad Sci USA 107:2705–2710

    Article  PubMed  Google Scholar 

  • Dewitte W, Riou-Khamlichi C, Scofield S, Healy JM, Jacqmard A, Kilby NJ, Murray JA (2003) Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15:79–92

    Article  PubMed  CAS  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    Article  PubMed  CAS  Google Scholar 

  • Dubrovsky JG, Gambetta GA, Hernandez-Barrera A, Shishkova S, Gonzalez I (2006) Lateral root initiation in Arabidopsis: developmental window, spatial patterning, density and predictability. Ann Bot 97:903–915

    Article  PubMed  CAS  Google Scholar 

  • Dubrovsky JG, Napsucialy-Mendivil S, Duclercq J, Cheng Y, Shishkova S, Ivanchenko MG, Friml J, Murphy AS, Benkova E (2011) Auxin minimum defines a developmental window for lateral root initiation. New Phytol 191:970–983

    Article  PubMed  CAS  Google Scholar 

  • Fan M, Xu C, Xu K, Hu Y (2012) Lateral organ boundaries domain transcription factors direct callus formation in Arabidopsis regeneration. Cell Res. doi:10.1038/cr.2012.63

    Google Scholar 

  • Feng Z, Sun X, Wang G, Liu H, Zhu J (2012) LBD29 regulates the cell cycle progression in response to auxin during lateral root formation in Arabidopsis thaliana. Ann Bot. http://aob.oxfordjournals.org/content/early/2012/02/13/aob.mcs019.abstract

  • Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29:153–168

    Article  PubMed  CAS  Google Scholar 

  • Fukaki H, Nakao Y, Okushima Y, Theologis A, Tasaka M (2005) Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alters lateral root development in Arabidopsis. Plant J 44:382–395

    Article  PubMed  CAS  Google Scholar 

  • Fukaki H, Okushima Y, Tasaka M (2007) Auxin-mediated lateral root formation in higher plants. Int Rev Cytol 256:111–137

    Article  PubMed  CAS  Google Scholar 

  • Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:1053–1057

    Article  PubMed  CAS  Google Scholar 

  • Himanen K, Boucheron E, Vanneste S, de Almeida EJ, Inze D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14:2339–2351

    Article  PubMed  CAS  Google Scholar 

  • Iwakawa H, Ueno Y, Semiarti E, Onouchi H, Kojima S, Tsukaya H, Hasebe M, Soma T, Ikezaki M, Machida C, Machida Y (2002) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol 43:467–478

    Article  PubMed  CAS  Google Scholar 

  • Laskowski M, Grieneisen VA, Hofhuis H, Hove CA, Hogeweg P, Maree AF, Scheres B (2008) Root system architecture from coupling cell shape to auxin transport. PLoS Biol 6:e307

    Article  PubMed  Google Scholar 

  • Lee HW, Kim J (2010) Ectopic expression of LBD18/ASL20 results in arrest of plant growth and development with repression of AINTEGUMENTA and PLETHORA genes. J Plant Biol 53:214–221

    Article  CAS  Google Scholar 

  • Lee HW, Kim NY, Lee DJ, Kim J (2009) LBD18/ASL20 regulates lateral root formation in combination with LBD16/ASL18 downstream of ARF7 and ARF19 in Arabidopsis. Plant Physiol 151:1377–1389

    Article  PubMed  CAS  Google Scholar 

  • Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17:444–463

    Article  PubMed  CAS  Google Scholar 

  • Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19:118–130

    Article  PubMed  CAS  Google Scholar 

  • Overvoorde P, Fukaki H, Beeckman T (2010) Auxin control of root development. Cold Spring Harb Perspect Biol 2:a001537

    Article  PubMed  Google Scholar 

  • Santelia D, Vincenzetti V, Azzarello E, Bovet L, Fukao Y, Duchtig P, Mancuso S, Martinoia E, Geisler M (2005) MDR-like ABC transporter AtPGP4 is involved in auxin-mediated lateral root and root hair development. FEBS Lett 579:5399–5406

    Article  PubMed  CAS  Google Scholar 

  • Sanz L, Dewitte W, Forzani C, Patell F, Nieuwland J, Wen B, Quelhas P, De Jager S, Titmus C, Campilho A, Ren H, Estelle M, Wang H, Murray JA (2011) The Arabidopsis D-type cyclin CYCD2;1 and the inhibitor ICK2/KRP2 modulate auxin-induced lateral root formation. Plant Cell 23:641–660

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Sugimoto K, Jiao Y, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev Cell 18:463–471

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Swarup K, Benkova E, Swarup R, Casimiro I, Peret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, Levesque MP, Carrier D, James N, Calvo V, Ljung K, Kramer E, Roberts R, Graham N, Marillonnet S, Patel K, Jones JD, Taylor CG, Schachtman DP, May S, Sandberg G, Benfey P, Friml J, Kerr I, Beeckman T, Laplaze L, Bennett MJ (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10:946–954

    Article  PubMed  CAS  Google Scholar 

  • Terasaka K, Blakeslee JJ, Titapiwatanakun B, Peer WA, Bandyopadhyay A, Makam SN, Lee OR, Richards EL, Murphy AS, Sato F, Yazaki K (2005) PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. Plant Cell 17:2922–2939

    Article  PubMed  CAS  Google Scholar 

  • Vanneste S, De Rybel B, Beemster GT, Ljung K, De Smet I, Van Isterdael G, Naudts M, Iida R, Gruissem W, Tasaka M, Inze D, Fukaki H, Beeckman T (2005) Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell 17:3035–3050

    Article  PubMed  CAS  Google Scholar 

  • Verkest A, Weinl C, Inze D, De Veylder L, Schnittger A (2005) Switching the cell cycle. Kip-related proteins in plant cell cycle control. Plant Physiol 139:1099–1106

    Article  PubMed  CAS  Google Scholar 

  • Wilmoth JC, Wang S, Tiwari SB, Joshi AD, Hagen G, Guilfoyle TJ, Alonso JM, Ecker JR, Reed JW (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 43:118–130

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Our work was supported by the National Natural Science Foundation of China (grant no. 30970169).

Author information

Authors and Affiliations

  1. Department of Molecular and Cell Biology, School of Life Science and Technology, Tongji University, Shanghai, 200092, China

    Zhenhua Feng, Jian Zhu, Xiling Du & Xianghuan Cui

Authors
  1. Zhenhua Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jian Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiling Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xianghuan Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jian Zhu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplemental Table S1 qRT-PCR and PR-PCR primers used. (DOC 37 kb)

425_2012_1673_MOESM2_ESM.ppt

Supplemental Fig. S1 Seedlings grown in MS medium containing 10 nM NAA at 10 days old. lbd16lbd18lbd29 showed lateral root formation, but fewer lateral roots than in the wild type. Numbers of lateral roots (mean ± SD) for each genotype were shown (n > 20). Each small grid was 1 cm × 1cm (PPT 541 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Feng, Z., Zhu, J., Du, X. et al. Effects of three auxin-inducible LBD members on lateral root formation in Arabidopsis thaliana . Planta 236, 1227–1237 (2012). https://doi.org/10.1007/s00425-012-1673-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-012-1673-3

Keywords

Search

Navigation