Skip to main content
SpringerLink
Log in

Regulation of root growth by auxin and ethylene is influenced by phosphate supply in white clover (Trifolium repens L.)

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The influence of P-supply on root system architecture (primary root length, number and total length of lateral roots) through the effects of ethylene (ACC) and auxin [1-naphthylacetic acid (NAA)] has been examined in the legume white clover (Trifolium repens L.). Higher concentrations (1 and 10 μM) of ACC and NAA (100 nM) inhibited growth, while lower concentrations (100 nM ACC, 5 nM NAA) either had no effect or stimulated growth in P-sufficient (1 mM Pi) roots. In response to low (10 μM) P, a stimulation of primary root growth, number of lateral roots and mean length of lateral roots was observed, while a super-stimulation of these growth parameters occurred in response to subsequent 100 nM ACC treatment suggesting that the low P treatment increased the sensitivity of the roots to ethylene. Examination of the primary roots of DR5p::GUS transformants suggests that this change in sensitivity induced by low P occurs through the promotion of auxin signalling/transport to the root apex. These results are discussed in terms of the role of ethylene and the significance of changes in sensitivity to the hormone in modulating root system architecture in response to low P-supply.

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
Fig. 8

Similar content being viewed by others

Abbreviations

1-MCP:

1-Methylcyclopropene

ACC:

1-Aminocyclopropane-1-carboxylate

NAA:

1-Naphthylacetic acid

1-NPA:

1-N-naphthylphthalamic acid

References

  • Abel S (2011) Phosphate sensing in root development. Curr Opin Plant Biol 14:303–309

    Article  PubMed  CAS  Google Scholar 

  • Abel S, Ticconi CA, Delatorre CA (2002) Phosphate sensing in higher plants. Physiol Plantarum 115:1–8

    Article  CAS  Google Scholar 

  • Al-Ghazi Y, Muller B, Pinloche S, Tranbarger TJ, Nacry P, Rossignol M, Tardieu F, Doumas P (2003) Temporal responses of Arabidopsis root architecture to phosphate starvation: evidence for the involvement of auxin signalling. Plant Cell Environ 26:1053–1066

    Article  CAS  Google Scholar 

  • Borch K, Bouma TJ, Lynch JP, Brown KM (1999) Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant Cell Environ 22:425–431

    Article  CAS  Google Scholar 

  • Caradus JR, Hay MJM, Mackay AD, Thomas VJ, Dunlop J, Lambert MG, Hart AL, Vandenbosch J, Wewala S (1993) Variation within white clover (Trifolium repens L.) for phenotypic plasticity of morphological and yield related characters induced by phosphorus supply. New Phytol 123:175–184

    Article  CAS  Google Scholar 

  • Caradus JR, Kennedy LD, Dunn A (1998) Genetic variation for the ratio of inorganic to toal phosphorus in white clover leaves. J Plant Nut 21:2265–2272

    Article  CAS  Google Scholar 

  • Chomczynski P (1992) One-hour downward alkaline capillary transfer for blotting of DNA and RNA. Anal Biochem 201:134–139

    Article  PubMed  CAS  Google Scholar 

  • Crush JR, Boulesteix-Coutelier ARL, Ouyang L (2008) Phosphate uptake by white clover (Trifolium repens L.) genotypes with contrasting root morphology. NZ J Ag Res 51:279–285

    Article  CAS  Google Scholar 

  • Drew MC, He C-J, Morgan PW (1989) Decreased ethylene biosynthesis, and induction of aerenchyma, by nitrogen- or phosphate-starvation in adventitious roots of Zea mays L. Plant Physiol 91:266–271

    Article  PubMed  CAS  Google Scholar 

  • Dubrovsky JG, Napsucialy-Mendivil S, Duclerq 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 

  • Dunlop J, Gardiner S (1993) Phosphate uptake, proton extrusion and membrane electropotentials of phosphorus-deficient Trifolium repens L. J Expt Bot 44:1801–1808

    Article  CAS  Google Scholar 

  • Fukaki H, Tasaka M (2009) Hormone interactions during lateral root formation. Plant Mol Biol 69:437–449

    Article  PubMed  CAS  Google Scholar 

  • Gibeaut DM, Hulet J, Cramer GR, Seemann JR (1997) Maximal biomass of Arabidopsis thaliana using a simple, low-maintenance hydroponic method and favourable environmental conditions. Plant Physiol 115:317–319

    Article  PubMed  CAS  Google Scholar 

  • Hammond JP, White PJ (2011) Sugar signaling in root responses to low phosphorus availability. Plant Physiol 156:1033–1040

    Article  PubMed  CAS  Google Scholar 

  • He C-J, Morgan PW, Drew MC (1992) Enhanced sensitivity to ethylene in nitrogen- or phosphate-starved roots of Zea mays L. during aerenchyma formation. Plant Physiol 98:137–142

    Article  PubMed  CAS  Google Scholar 

  • Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation. TIPS 11:610–617

    CAS  Google Scholar 

  • Ivanchenko MG, Muday GK, Dubrovsky JG (2008) Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J 55:335–347

    Article  PubMed  CAS  Google Scholar 

  • Jackson MB (1992) Ethylene in root growth and development. In: Mattoo A, Suttle JC (eds) The plant hormone ehtylene. pp, CRC Press, pp 159–181

    Google Scholar 

  • Jain A, Poling MD, Karthikeyan AS, Blakeslee JJ, Peer WA, Titapiwatanakun B, Murphy AS, Raghothama KG (2007) Differential effects of sucrose and auxin on localized phosphate deficiency-induced modulation of different traits of root system architecture in Arabidopsis. Plant Physiol 144:232–247

    Article  PubMed  CAS  Google Scholar 

  • Lei M, Zhu C, Liu Y, Karthkeyan AS, Bressan RA, Raghothama K, Liu D (2011) Ethylene signalling is involved in regulation of phosphate starvation-induced gene expression and production of acid phosphatases and anthocyanin in Arabidopsis. New Phytol 189:1084–1095

    Article  PubMed  CAS  Google Scholar 

  • López-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256

    Article  PubMed  Google Scholar 

  • Lötscher M, Hay MJM (1996) Distribution of mineral nutrient from nodal roots of Trifolium repens: genotypic variation in intra-plant allocation of 32P and 45Ca. Physiol Plant 97:269–276

    Article  Google Scholar 

  • Lynch J, Brown KM (1997) Ethylene and plant responses to nutritional stress. Physiol Plant 100:613–619

    Article  CAS  Google Scholar 

  • Lynch JP, Brown KM (2001) Topsoil foraging—an architectural adaptation of plants to low phosphorus availability. Plant Soil 237:225–237

    Article  CAS  Google Scholar 

  • Ma Z, Baskin TI, Brown KM, Lynch JP (2003) Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiol 131:1381–1390

    Article  PubMed  CAS  Google Scholar 

  • Miura KM, Lee J, Gong Q, Ma S, Jin JB, Yoo CY, Miura T, Sato A, Bohnert HJ, Hasegawa PM (2011) SIZ1 regulation of phosphate starvation-induced root architecture remodelling involves the control of auxin accumulation. Plant Physiol 155:1000–1012

    Article  PubMed  CAS  Google Scholar 

  • Nacry P, Canivenc G, Muller B, Azmi A, Van Onckelen H, Rossignol M, Doumas P (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol 138:2061–2074

    Article  PubMed  CAS  Google Scholar 

  • Negi S, Ivanchenko MG, Muday GK (2008) Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. Plant J 55:175–187

    Article  PubMed  CAS  Google Scholar 

  • Peret B, Larrieu A, Bennett MB (2009) Lateral root emergence: a difficult birth. J Exp Bot 60:3637–3643

    Article  PubMed  CAS  Google Scholar 

  • Perez-Torres CA, Lopez-Bucio J, Cruz-Ramirez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20:3258–3272

    Article  PubMed  CAS  Google Scholar 

  • Pierek R, Tholen D, Poorter H, Visser EJW, Voesenek LACJ (2006) The Janis face of ethylene: growth inhibition and stimulation. TIPS 11:178–183

    Google Scholar 

  • Prasad ME, Schofield A, Lyzenga W, Liu H, Stone SL (2010) Arabidopsis RING E3 ligase XBAT32 regulates lateral root production through its role in ethylene biosynthesis. Plant Physiol 153:1587–1596

    Article  PubMed  CAS  Google Scholar 

  • Roldan MB (2008) Expression of ACC oxidase genes in white clover (Trifolium repens L) roots in response to phosphate supply. Unpublished PhD Thesis, Massey University, Palmerston North, New Zealand, p 242

  • Ruzicka K, Ljung K, Vanneste S, Podhorska R, Beeckman T, Friml J, Benkova E (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19:2197–2212

    Article  PubMed  CAS  Google Scholar 

  • Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453

    Article  PubMed  CAS  Google Scholar 

  • Strader LC, Chen GL, Bartel B (2010) Ethylene directs auxin to control root cell expansion. Plant J 64:874–884

    Article  PubMed  CAS  Google Scholar 

  • Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GTS, Sandberg G, Bhalerao R, Ljung K, Bennett MJ (2007) Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19:2186–2196

    Article  PubMed  CAS  Google Scholar 

  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a non-renewable resource. New Phytol 157:427–447

    Article  Google Scholar 

  • Williamson LC, Ribrioux S, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882

    Article  PubMed  CAS  Google Scholar 

  • Zhang C, McManus MT (2000) Identification and characterisation of two distinct acid phosphatases in cell walls of roots of white clover. Plant Physiol Biochem 38:259–270

    Article  CAS  Google Scholar 

  • Zhang YJ, Lynch JP, Brown KM (2003) Ethylene and phosphorus availability have interacting yet distinct effects on root hair development. J Exp Bot 54:2351–2361

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The research was funded by the New Zealand Foundation for Research, Science and Technology (C02X0406), a NZAid scholarship to PTYD and a Massey University Doctoral scholarship to MR.

Author information

Author notes

  1. Phuong T. Y. Dinh & Marissa Roldan

    Present address: Department of Plant Pathology, Washington State University, Pullman, WA, USA

Authors and Affiliations

  1. Institute of Molecular Biosciences, Massey University, Private Bag 11222, Palmerston North, New Zealand

    Phuong T. Y. Dinh, Marissa Roldan, Susanna Leung & Michael T. McManus

  2. AgResearch Limited, Private Bag 11008, Tennent Drive, Palmerston North, New Zealand

    Marissa Roldan

Authors
  1. Phuong T. Y. Dinh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marissa Roldan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susanna Leung
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael T. McManus
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael T. McManus.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10725_2011_9642_MOESM1_ESM.doc

Fig. S1. A white clover stolon grown hydroponically with a single well developed root subtending from node 3. PR, primary root; LR, lateral root. Supplementary material 1 (DOC 32 kb)

10725_2011_9642_MOESM2_ESM.doc

Fig. S2. The effects of P treatment (1 mM, P+; 10 μM, P-) as indicated, on root morphology of the rooted stolon cuttings of the transgenic (DR5p::GUS) line, TR29. Changes in the mean length of the PR (A) and the mean number of LRs (B). Values are means of six individual stolons with standard deviations of the means (represented as error bars). * indicates significant differences (P ≤ 0.05). Supplementary material 2 (DOC 956 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dinh, P.T.Y., Roldan, M., Leung, S. et al. Regulation of root growth by auxin and ethylene is influenced by phosphate supply in white clover (Trifolium repens L.). Plant Growth Regul 66, 179–190 (2012). https://doi.org/10.1007/s10725-011-9642-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-011-9642-6

Keywords

Search

Navigation