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Plant and Soil

, Volume 360, Issue 1–2, pp 19–35 | Cite as

Radial force development during root growth measured by photoelasticity

  • Evelyne Kolb
  • Christian Hartmann
  • Patricia Genet
Regular Article

Abstract

Background and aims

The radial growth of roots largely affects and reorganizes the porous or crack networks of soils and substrates. We studied the consequences of a radial steric constriction on the root growth and the feedback force developed by the root on the solid phase.

Methods

We developed an original method of photoelasticity to measure in situ root forces. By changing the gap width (0.5 to 2.3 mm) between two photoelastic disks we applied variable radial constrictions to root growth and simultaneously measured the corresponding radial forces. Changes in morphology and forces of primary roots of chick pea (Cicer arietinum L.) seedlings were recorded by time-lapse imaging every 24 min up to 5 days.

Results

The probability of root entering the gap depended on the gap size but was also affected by circumnutation. Compared to non-constrained root controls, no significant morphological change (elongation, diameter) was measured outside the gap zone. Inside the gap zone, outer cortex cells were compressed, the central cylinder was unaffected. Radial forces were increasing with time but no force levelling was observed even after 5 days.

Conclusions

Radial constrictions applied to roots did not significantly reduce their growth. The radial force was related to the root strain in the gap.

Keywords

Radial force development Root growth Photoelasticity Mechanical stress Cicer arietinum L. (chick pea) 

Abbreviations

E

Entering root

NE

Non entering root

δ

Gap size (mm)

ε

Radial strain (no unit)

σ

Radial stress (Pa)

νy

Root vertical velocity (mm.h−1)

dA, dB

Root diameters at 2.9 mm above (dA) and below (dB) the gap (mm)

<x>

is the averaged value of the measured variable x

Notes

Acknowledgments

We thank Laure-Emmanuelle Lecoq, Henri de Cagny, Harold Gouet, Simon Cabello-Aguilar and Lucie Guignier who worked on this subject during their undergraduate lab-training, as well as Laurent Quartier, who carefully designed the root chambers, Guillaume Clermont, who cut the photoelastic disks and Thierry Darnige, who automated one part of the experimental setup.

We are particularly grateful to Professor Tom Mullin (Manchester Centre for Non Linear Dynamics-UK) who gave us our first photoelastic disks as well as Professor Robert P. Behringer (Duke Physics, USA) who introduced us to the photoelastic technique and who constantly gives us relevant and kind advice. We also thank Anette Hosoi (MIT, USA) and her students Dawn Wendell and Katharin Luginbuhl for very fruitful interactions through our commun MIT-France Seed Fund project on “Flexible Objects in Granular Media”.

We also want to thank Professor Arezki Boudaoud (ENS Lyon, France) for our helpful discussions, Isabelle Bonnet (Institut Curie, France) and François Graner (Institut Curie and MSC, Paris 7, France) for the careful comments on the manuscript and the continuous and kind support, and Laurette S. Tuckerman (PMMH, ESPCI, France) for the English corrections. Thanks also to the friendly review of Eugénie Carnero-Diaz and the efficient help of Laurence Goury (IRD) in providing many articles and book chapter cited here.

Supplementary material

ESM 1

(MPG 3688 kb)

ESM 2

(MPG 3162 kb)

ESM 3

(MPG 2706 kb)

ESM 4

(MPG 2706 kb)

References

  1. Abdalla AM, Hettiaratchi DRP, Reece AR (1969) The mechanics of root growth in granular media. J agric Engng Res 14:236–248CrossRefGoogle Scholar
  2. Atwell BJ (1993) Response of roots to mechanical impedance. Environ Exp Bot 33:27–40CrossRefGoogle Scholar
  3. Bartens J, Day SD, Harris JR, Dove JE, Wynn TM (2008) Can urban tree roots improve infiltration through compacted subsoils for stromwater management? J Environ Qual 37:2048–2057PubMedCrossRefGoogle Scholar
  4. Bengough AG (2003) Root growth and function in relation to soil structure, composition, and strength. In: de Kroon H, Wisser EJW (eds) Root ecology. Springer Verlag, Berlin, pp 151–171Google Scholar
  5. Bengough AG, McKenzie BM (1997) Sloughing of root cap cells decreases the frictional resistance to maize (Zea mays L) root growth. J Exp Bot 48:885–893CrossRefGoogle Scholar
  6. Bengough AG, Mackenzie CJ, Elangwe HE (1994) Biophysics of the growth-responses of pea roots to changes in penetration resistance. Plant Soil 167:135–141CrossRefGoogle Scholar
  7. Bengough AG, Croser C, Pritchard J (1997) A biophysical analysis of root growth under mechanical stress. Plant Soil 189:155–164CrossRefGoogle Scholar
  8. Bengough AG, McKenzie BM, Hallett PD, Valentine TA (2011) Root elongation, water stress, and mechanical impedance: a review of limiting stresses and beneficial root tip traits. J Exp Bot 62:59–68PubMedCrossRefGoogle Scholar
  9. Boudaoud A (2010) An introduction to the mechanics of morphogenesis for plant biologists. Trends Plant Sci 15:353–360PubMedCrossRefGoogle Scholar
  10. Bruand A, Cousin I, Nicoullaud B, Duval O, Begon JC (1996) Backscattered electron scanning images of soil porosity for analyzing soil compaction around roots. Soil Sci Soc Am J 60:895–901CrossRefGoogle Scholar
  11. Clark LJ, Whalley WR, Dexter AR, Barraclough PB, Leigh RA (1996) Complete mechanical impedance increases the turgor of cells in the apex of pea roots. Plant Cell Environ 19:1099–1102CrossRefGoogle Scholar
  12. Clark LJ, Whalley WR, Barraclough PB (2003) How do roots penetrate strong soil? Plant Soil 255:93–104CrossRefGoogle Scholar
  13. Costello LR, Jones KS (2003) Reducing infrastructure damage by tree roots: a compendium of strategies. Western Chapter of the International Society of Arboriculture (WCISA), CohassetGoogle Scholar
  14. Cresswell HP, Kirkegaard JA (1995) Subsoil amelioration by plant-roots - the process and the evidence. Aust J Soil Res 33:221–239CrossRefGoogle Scholar
  15. Croser C, Bengough AG, Pritchard J (1999) The effect of mechanical impedance on root growth in pea (Pisum sativum). I. Rates of cell flux, mitosis, and strain during recovery. Physiol Plant 107:277–286CrossRefGoogle Scholar
  16. Croser C, Bengough AG, Pritchard J (2000) The effect of mechanical impedance on root growth in pea (Pisum sativum). II. Cell expansion and wall rheology during recovery. Physiol Plant 109:150–159CrossRefGoogle Scholar
  17. Czarnes S, Hallett PD, Bengough AG, Young IM (2000) Root- and microbial-derived mucilages affect soil structure and water transport. Eur J Soil Sci 51:435–443CrossRefGoogle Scholar
  18. Danjon F, Barker DH, Drexhage M, Stokes A (2008) Using three-dimensional plant root architecture in models of shallow-slope stability. Ann Bot 101:1281–1293PubMedCrossRefGoogle Scholar
  19. De Baets S, Torri D, Poesen J, Salvador MP, Meersmans J (2008) Modelling increased soil cohesion due to roots with EUROSEM. Earth Surf Process Landforms 33:1948–1963CrossRefGoogle Scholar
  20. Dexter A (1986) Model experiments on the behaviour of roots at the interface between a tilled seed-bed and a compacted sub-soil. Plant Soil 95:149–161CrossRefGoogle Scholar
  21. Dorgan KM, Jumars PA, Johnson B, Boudreau BP, Landis E (2005) Burrow extension by crack propagation. Nature 433:475–475PubMedCrossRefGoogle Scholar
  22. Dorgan KM, Arwade SR, Jumars PA (2007) Burrowing in marine muds by crack propagation: kinematics and forces. J Exp Biol 210:4198–4212PubMedCrossRefGoogle Scholar
  23. Doussan C, Pages L, Pierret A (2003) Soil exploration and resource acquisition by plant roots: an architectural and modelling point of view. Agronomie 23:419–431CrossRefGoogle Scholar
  24. Geitmann A (2006) Experimental approaches used to quantify physical parameters at cellular and subcellular levels. Am J Bot 93:1380–1390PubMedCrossRefGoogle Scholar
  25. Geitmann A, Ortega JKE (2009) Mechanics and modeling of plant cell growth. Trends Plant Sci 14:467–478PubMedCrossRefGoogle Scholar
  26. Goss MJ (1977) Effects of mechanical impedance on root-growth in barley (hordeum-vulgare-l).1. effects on elongation and branching of seminal root axes. J Exp Bot 28:96–111CrossRefGoogle Scholar
  27. Gregory PJ (2006) Roots, rhizosphere and soil: the route to a better understanding of soil science? Eur J Soil Sci 57:2–12CrossRefGoogle Scholar
  28. Hamant O, Traas J (2010) The mechanics behind plant development. New Phytol 185:369–385PubMedCrossRefGoogle Scholar
  29. Hamant O, Heisler MG, Jonsson H, Krupinski P, Uyttewaal M, Bokov P, Corson F, Sahlin P, Boudaoud A, Meyerowitz EM, Couder Y, Traas J (2008) Developmental patterning by mechanical signals in arabidopsis. Science 322:1650–1655PubMedCrossRefGoogle Scholar
  30. Hartge KH (2000) The effect of soil deformation on physical soil properties—A discourse on the common background. In: Horn R, van den Akker JJH, Arvidsson J (eds) Subsoil compaction: distribution, processes and consequences. Catena Verlag, Reiskirchen, pp 32–43Google Scholar
  31. Heinen M, Mollier A, De Willigen P (2003) Growth of a root system described as diffusion. II. Numerical model and application. Plant Soil 252:251–265CrossRefGoogle Scholar
  32. Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24CrossRefGoogle Scholar
  33. Iijima M, Barlow PW, Bengough AG (2003) Root cap structure and cell production rates of maize (Zea mays) roots in compacted sand. New Phytol 160:127–134CrossRefGoogle Scholar
  34. Iijima M, Morita S, Barlow PW (2008) Structure and function of the root cap. Plant Prod Sci 11:17–27CrossRefGoogle Scholar
  35. Jackson RB, Mooney HA, Schulze ED (1997) A global budget for fine root biomass, surface area, and nutrient contents. PNAS 94:7362–7366PubMedCrossRefGoogle Scholar
  36. Jackson RB, Moore LA, Hoffmann WA, Pockman WT, Linder CR (1999) Ecosystem rooting depth determined with caves and DNA. PNAS 96:11387–11392PubMedCrossRefGoogle Scholar
  37. Jim CY (1993) Soil compaction as a constraint to tree growth in tropical and subtropical urban habitats. Environ Conserv 20:35–49CrossRefGoogle Scholar
  38. Kuzeja PS, Lintilhac PM, Wei CF (2001) Root elongation against a constant force: experiment with a computerized feedback-controlled device. J Plant Physiol 158:673–676PubMedCrossRefGoogle Scholar
  39. Lesturgez G, Poss R, Hartmann C, Bourdon E, Noble A, Ratana-Anupap S (2004) Roots of Stylosanthes hamata create macropores in the compact layer of a sandy soil. Plant Soil 260:101–109CrossRefGoogle Scholar
  40. Liang BM, Sharp RE, Baskin TI (1997) Regulation of growth anisotropy in well-watered and water-stressed maize roots.1. Spatial distribution of longitudinal, radial, and tangential expansion rates. Plant Physiol 115:101–111PubMedGoogle Scholar
  41. Liang BC, Wang XL, Ma BL (2002) Maize root-induced change in soil organic carbon pools. Soil Sci Soc Am J 66:845–847CrossRefGoogle Scholar
  42. Lockhart JA (1967) Physical nature of irreversible deformation of plant cells. Plant Physiol 42:1545–1552PubMedCrossRefGoogle Scholar
  43. Majmudar TS, Behringer RP (2005) Contact force measurements and stress-induced anisotropy in granular materials. Nature 435:1079–1082PubMedCrossRefGoogle Scholar
  44. Materechera SA, Dexter AR, Alston AM (1992) Formation of aggregates by plant-roots in homogenized soils. Plant Soil 142:69–79Google Scholar
  45. Mirabet V, Das P, Boudaoud A and Hamant O 2011 The Role of Mechanical Forces in Plant Morphogenesis. In Annu. Rev. Plant Biol., Vol 62. Eds. SS Merchant, W R Briggs and D Ort. pp 365-385.Google Scholar
  46. Misra RK, Dexter AR, Alston AM (1986) Maximum axial and radial growth pressures of plant roots. Plant Soil 95:315–326CrossRefGoogle Scholar
  47. Nichol SA, Silk WK (2001) Empirical evidence of a convection-diffusion model for pH patterns in the rhizospheres of root tips. Plant Cell Environ 24:967–974CrossRefGoogle Scholar
  48. Oelbermann M, Voroney RP, Gordon AM (2004) Carbon sequestration in tropical and temperate agroforestry systems: a review with examples from Costa Rica and southern Canada. Agric Ecosyst Environ 104:359–377CrossRefGoogle Scholar
  49. Pages L, Pellerin S (1996) Study of differences between vertical root maps observed in a maize crop and simulated maps obtained using a model for the three-dimensional architecture of the root system. Plant Soil 182:329–337Google Scholar
  50. Pierret A, Moran CJ, Doussan C (2005) Conventional detection methodology is limiting our ability to understand the roles and functions of fine roots. New Phytol 166:967–980PubMedCrossRefGoogle Scholar
  51. Pierret A, Hartmann C, Maeght J, Pagès L (2011) Biotic regulation: plants. In: Ritz K, Young IM (eds) The architecture and biology of soils. Life in inner space. CABI, Wallingford, Oxfordshire, Cambridge, pp 88–103Google Scholar
  52. Pritchard J (1994) The control of cell expansion in roots. New Phytol 127:3–26CrossRefGoogle Scholar
  53. Rasse DP, Smucker AJM (1998) Root recolonization of previous root channels in corn and alfalfa rotations. Plant Soil 204:203–212CrossRefGoogle Scholar
  54. Schenk HJ (2008) Soil depth, plant rooting strategies and species’ niches. New Phytol 178:223–225PubMedCrossRefGoogle Scholar
  55. Scholefield D, Hall DM (1985) Constricted growth of grass roots through rigid pores. Plant Soil 85:153–162CrossRefGoogle Scholar
  56. Sharp RE, Silk WK, Hsiao TC (1988) Growth of the maize primary root at Low water potentials. I. Spatial distribution of expansive growth. Plant Physiol 87:50–57PubMedCrossRefGoogle Scholar
  57. Souty N (1987) Mechanical-behavior of growing roots.1. measurement of penetration force. Agronomie 7:623–630 (in French)CrossRefGoogle Scholar
  58. Stolarz M (2009) Circumnutation as a visible plant action and reaction. Physiological, cellular and molecular basis for circumnutations. Plant Signal Behav 4:380–387PubMedCrossRefGoogle Scholar
  59. Thompson MV, Holbrook NM (2004) Root-gel interactions and the root waving behavior of Arabidopsis. Plant Physiol 135:1822–1837PubMedCrossRefGoogle Scholar
  60. Tracy SR, Black CR, Roberts JA, Mooney SJ (2011) Soil compaction: a review of past and present techniques for investigating effects on root growth. J Sci Food Agric 91:1528–1537PubMedCrossRefGoogle Scholar
  61. Tsegaye T, Mullins CE (1994) Effect of mechanical impedance on root-growth and morphology of 2 varieties of pea (pisum-sativum l). New Phytol 126:707–713CrossRefGoogle Scholar
  62. Wendell DM, Luginbuhl K, Guerrero J, Hosoi AE (2011) Experimental investigation of plant root growth through granular substrates. Exp Mech. doi: 10.1007/s11340-011-9569-x
  63. Wiersum K (1957) The relationship of the size and structural rigidity of pores to their penetration by roots. Plant Soil 9:75–85CrossRefGoogle Scholar
  64. Wilson AJ, Robards AW, Goss MJ (1977) Effects of mechanical impedance on root growth in barley, Hordeum vulgare L. II. Effects on cell development in seminal roots. J Exp Bot 28:1216–1227CrossRefGoogle Scholar
  65. Young IM (1998) Biophysical interactions at the root-soil interface: a review. J Agric Sci 130:1–7CrossRefGoogle Scholar
  66. Zuriguel I, Mullin T, Rotter J (2007) Effect of particle shape on the stress dip under a sandpile. Phys Rev Lett 98:028001PubMedCrossRefGoogle Scholar
  67. Zwieniecki MA, Newton M (1995) Roots growing in rock fissures - their morphological adaptation. Plant Soil 172:181–187CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Evelyne Kolb
    • 1
    • 5
  • Christian Hartmann
    • 2
  • Patricia Genet
    • 3
    • 4
  1. 1.PMMH ESPCI – CNRS UMR 7636Paris Cedex 05France
  2. 2.IRD – UMR 211 ‘BIOEMCO’Paris Cedex 05France
  3. 3.UPMC Paris 6 – CNRS UMR 7618Paris Cedex 05France
  4. 4.Université Paris Diderot – Paris 7Paris Cedex 13France
  5. 5.UPMC Paris 6Paris Cedex 05France

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