Skip to main content

Advertisement

Log in

The involvement of gibberellin signalling in the effect of soil resistance to root penetration on leaf elongation and tiller number in wheat

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

The concept of root-sourced chemical signals that affect shoot growth in response to drought is widely reported; in particular the role of ABA in regulating stomatal conductance has received much attention. ABA, alone, does not fully explain all the effects of abiotic stresses in the root zone on shoot architecture. An increase in mechanical impedance, which can occur on even relatively modest soil drying, results in reduced root and shoot growth, processes that are potentially regulated by gibberellins (GAs).

Methods

In this study we explored the role of mechanical impedance and exogenous gibberellin (GA3) on root and shoot architecture in wheat seedlings containing the Rht-B1a (tall), Rht-B1b (semi-dwarf) or Rht-B1c (dwarf) alleles in the April-Bearded or Mercia backgrounds. Our experiments were based on the use of the sand culture system which allows the mechanical impedance of the root growth environment to remain constant and independent of water and nutrient availability. We investigated the effects of the application of exogenous GA3 to the root system.

Results

We found that impeding soil reduced leaf elongation in the tall and semi-dwarf lines, confirming the stunting effect of mechanical impedance which is widely reported. However, leaf elongation in the dwarf lines was not affected by root impedance. Application of GA3 to the roots restored leaf elongation in the tall and semi-dwarf lines growing in impeding soil, with some growth response even in the dwarf line, the longest leaves being obtained when GA was applied to impeded roots of a tall line. Both exogenous GA and root impedance reduced the number of tillers, but there was no interaction with the Rht genotype. The genetic background did not affect the results.

Conclusion

We suggest that the GA signalling pathway has an unidentified role in the leaf elongation response to mechanical impedance to root growth.

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
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Addisu M, Snape JW, Simmonds JR, Gooding MJ (2009) Reduced height (Rht) and photoperiod insensitivity (Ppd) allele associations with establishment and early growth of wheat in contrasting production systems. Euphytica 166:249–267

    Article  CAS  Google Scholar 

  • Appleford NEJ, Wilkinson MD, Ma Q, Evans DJ, Stone MC, Pearce SP, Powers SJ, Thomas SG, Jones HD, Phillips AL, Hedden P, Lenton JR (2007) Decreased shoot stature and grain alpha-amylase activity following ectopic expression of a gibberellin 2-oxidase gene in transgenic wheat. J Exp Bot 58:3213–3226

    Article  PubMed  CAS  Google Scholar 

  • Atwell BJ (1990) The effect of soil compaction on wheat during early tillering. New Phyt 115:37–41

    Article  Google Scholar 

  • Bartholomew PW, Williams RD (2010) Effects of soil bulk density and strength on seedling growth of annual ryegrass and tall fescue in controlled environment. Grass Forage Sci 65:348–357

    Google Scholar 

  • Beemster GTS, Masle J (1996) Effects of soil resistance to root penetration on leaf expansion in wheat (Triticum aestivum L.): composition, number and size of epidermal cells in mature blades. J Exp Bot 47:1651–1662

    Article  CAS  Google Scholar 

  • Bengough AG, Mullins CE (1991) Penetrometer resistance, root penetration resistance and root elongation rate in two sandy loam soils. Plant Soil 131:59–66

    Google Scholar 

  • Clark LJ, Cope RE, Whalley WR, Barraclough PB, Wade LJ (2002) Root penetration of strong soil in rainfed lowland rice: comparison of laboratory screens with field performance. Field Crop Res 76:189–198

    Article  Google Scholar 

  • Dodd IC (2005) Root-to-shoot signalling: assessing the roles of ‘up’ in the up and down world of long-distance signalling in planta. Plant Soil 274:251–270

    Article  CAS  Google Scholar 

  • Dodd IC, Whalley WR, Ober ES, Parry MAJ (2011) Genetic and management approaches to boost UK wheat yields by ameliorating water deficits. J Exp Bot 62:5241–5248

    Article  PubMed  CAS  Google Scholar 

  • Flintham JE, Borner A, Worland AJ, Gale MD (1997) Optimizing wheat grain yield: effects of Rht (gibberellin- insensitive) dwarfing genes. J Agric Sci 128:11–25

    Article  Google Scholar 

  • Gao W, Watts CW, Ren T, Whalley WR (2012a) The effects of compaction and soil drying on penetrometer resistance. Soil Till Res 125:14–22

    Article  Google Scholar 

  • Gao W, Ren T, Bengough AG, Auneau L, Watts CW, Whalley WR (2012b) Predicting penetrometer resistance from the compression characteristic of soil. Soil Sci Soc Am J 76:361–369

    Article  CAS  Google Scholar 

  • Griffiths J, Murase K, Rieu I, Zentella R, Zhang Z-L, Powers SJ, Gong F, Phillips AL, Hedden P, Sun T-P, Thomas SG (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18:3399–3414

    Article  PubMed  CAS  Google Scholar 

  • Hussain A, Black CR, Taylor IB, Mulholland BJ, Roberts JA (1999a) Novel approaches for examining the effects of differential soil compaction on xylem sap abscisic acid concentration, stomatal conductance and growth in barley (Hordeum vulgare L.). Plant Cell Environ 22:1377–1388

    Article  Google Scholar 

  • Hussain A, Black CR, Taylor IB, Mulholland BJ, Roberts JA (1999b) Soil compaction. A role for ethylene in regulating leaf expansion and shoot growth in tomato? Am Soc Plant Phys 121:1227–1237

    Article  CAS  Google Scholar 

  • Inada S, Shimmen T (2000) Regulation of elongation growth by gibberellin in root segments of Lemna minor. Plant Cell Phys 41:932–939

    Article  CAS  Google Scholar 

  • Jia Q, Zhang X-Q, Westcott S, Broughton S, Cakir M, Yang J, Lance R, Li C (2011) Expression level of a gibberellin 20-oxidase gene is associated with multiple agronomic and quality traits in barley. Theor Appl Genet 122:1451–1460

    Article  PubMed  CAS  Google Scholar 

  • Martin-Vertedor AI, Dodd IC (2011) Root-to-shoot signalling when soil moisture is heterogeneous: increasing the proportion of root biomass in drying soil inhibits leaf growth and increases leaf abscisic acid concentration. Plant Cell Environ 34:1164–1175

    Article  PubMed  CAS  Google Scholar 

  • Masle J (1998) Growth and stomatal responses of wheat seedlings to spatial and temporal variations in soil strength of bi-layered soils. J Exp Bot 49:1245–1257

    CAS  Google Scholar 

  • Masle J, Passioura JB (1987) The effect of soil strength on the growth of young wheat plants. Aust J Plant Phys 14:643–656

    Article  Google Scholar 

  • Mckee GW (1964) A coefficient for computing leaf area in hybrid corn. Agron J 56:240–241

    Article  Google Scholar 

  • Peterson CM, Klepper B, Pumphrey FV, Rickman RW (1984) Restricted rooting decreases tillering and growth of winter wheat. Agron J 76:861–863

    Article  Google Scholar 

  • Richards RA (1988) A tiller inhibitor gene in wheat and its effect on plant growth. Aust J Agr Res 39:749–757

    Article  Google Scholar 

  • Rieu I, Ruiz-Rivero O, Fernandez-Garcia N, Griffiths J, Powers SJ, Gong F, Linhartova T, Eriksson S, Nilsson O, Thomas SG, Phillips AL, Hedden P (2008) The gibberellin biosynthetic genes AtGA20ox1 and AtGA20ox2 act, partially redundantly, to promote growth and development throughout the Arabidopsis life cycle. Plant J 53:488–504

    Article  PubMed  CAS  Google Scholar 

  • Tanimoto E (1987) Gibberellin-dependent root elongation in Lactuca sativa - recovery from growth retardant-suppressed elongation with thickening by low concentration of GA3. Plant Cell Phys 28:963–973

    CAS  Google Scholar 

  • Tanimoto E (2005) Regulation of root growth by plant hormones - Roles for auxin and gibberellin. Crit Rev Plant Sci 24:249–265

    Article  CAS  Google Scholar 

  • Tanimoto E (2012) Tall or short? Slender or thick? A plant strategy for regulating elongation growth of roots by low concentrations of gibberellin. Ann Bot 110:373–381

    Article  PubMed  CAS  Google Scholar 

  • Ubeda-Tomas S, Swarup R, Coates J, Swarup K, Laplaze L, Beemster GTS, Hedden P, Bhalerao R, Bennett MJ (2008) Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat Cell Biol 10:625–628

    Article  PubMed  CAS  Google Scholar 

  • Ubeda-Tomas S, Federici F, Casimiro I, Beemster GTS, Bhalerao R, Swarup R, Doerner P, Haseloff J, Bennett MJ (2009) Gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Curr Biol 19:1194–1199

    Article  PubMed  CAS  Google Scholar 

  • Webster R (2007) Analysis of variance, inference, multiple comparisons and sampling effects in soil research. Eur J Soil Sci 58:74–82

    Article  Google Scholar 

  • Whalley WR, Finch-Savage WE, Cope RE, Rowse HR, Bird NRA (1999) The response of carrot (Daucus carota L.) and onion (Allium cepa L.) seedlings to mechanical impedance and water stress at sub-optimal temperatures. Plant Cell Environ 22:229–242

    Article  Google Scholar 

  • Whalley WR, Clark LJ, Gowing DJG, Cope RE, Lodge RJ, Leeds-Harrison PB (2006) Does soil strength play a role in wheat yield losses caused by soil drying? Plant Soil 280:279–290

    Article  CAS  Google Scholar 

  • Whalley WR, To J, Kay BD, Whitmore AP (2007) Prediction of the penetrometer resistance of agricultural soils with models with few parameters. Geoderma 137:370–377

    Article  Google Scholar 

  • Whalley WR, Watts CW, Gregory AS, Mooney SJ, Clark LJ, Whitmore AP (2008) The effect of soil strength on the yield of wheat. Plant Soil 306:237–247

    Article  CAS  Google Scholar 

  • Wojciechowski T, Gooding MJ, Ramsay L, Gregory PJ (2009) The effects of dwarfing genes on seedling root growth of wheat. J Exp Bot 60:2565–2573

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Rothamsted Research is grant-aided by the Biotechnology and Biological Sciences Research Council (BBSRC) of the UK. M.A.C.F. was supported by Embrapa in Brasil to work at Rothamsted as visiting researcher. P.H., A.L.P. and W.R.W. are funded by the 20:20 Wheat® project. E.H.C was funded by BBSRC grant BB/H007334/1. D.P.A.L. was funded by a BBSRC-Quota studentship and affiliated to Nottingham University. We thank Rodger White and Professor Richard Webster for advice and assistance with the statistical analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to William R. Whalley.

Additional information

Responsible Editor: Alexia Stokes.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Coelho Filho, M.A., Colebrook, E.H., Lloyd, D.P.A. et al. The involvement of gibberellin signalling in the effect of soil resistance to root penetration on leaf elongation and tiller number in wheat. Plant Soil 371, 81–94 (2013). https://doi.org/10.1007/s11104-013-1662-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-013-1662-8

Keywords

Navigation