3D imaging and mechanical modeling of helical buckling in Medicago truncatula plant roots

Edited by William R. Schowalter, Princeton University, Princeton, NJ, and approved September 5, 2012 (received for review June 4, 2012)
September 24, 2012
109 (42) 16794-16799

Abstract

We study the primary root growth of wild-type Medicago truncatula plants in heterogeneous environments using 3D time-lapse imaging. The growth medium is a transparent hydrogel consisting of a stiff lower layer and a compliant upper layer. We find that the roots deform into a helical shape just above the gel layer interface before penetrating into the lower layer. This geometry is interpreted as a combination of growth-induced mechanical buckling modulated by the growth medium and a simultaneous twisting near the root tip. We study the helical morphology as the modulus of the upper gel layer is varied and demonstrate that the size of the deformation varies with gel stiffness as expected by a mathematical model based on the theory of buckled rods. Moreover, we show that plant-to-plant variations can be accounted for by biomechanically plausible values of the model parameters.

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ACKNOWLEDGMENTS.

The authors thank A. Moore, L. Ristroph, J. Savage, Z. Chen, L. Manning, M. Lapa, M. Haataja, J. Sethna, A. Alemi, B. Davidovitch, C. Orellana, E. Kolb, the Cohen lab, and the Mahadevan lab for stimulating conversation. We also thank J. Gregoire and S. Iams for assisting in apparatus development, J. Fetcho for kindly allowing us to use Imaris, M. Venkadesan for kindly loaning the translation stage, and J. Puzey for critically reading this manuscript. This work was supported by the National Science Foundation through a Graduate Research Fellowship to J.L.S., Grant IOS-0842720 supporting R.D.N., Grant DMR-1056662 supporting I.C., and Cornell’s IGERT Program in Nonlinear Systems (National Science Foundation Grant DGE-9870631) supporting S.J.G. This work was supported by the US Department of Energy through Grant DE-FG02-89ER-45405 supporting M.S.P. and C.L.H., and Grant DE-FG02-08ER46517 supporting S.J.G.

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 109 | No. 42
October 16, 2012
PubMed: 23010923

Classifications

Submission history

Published online: September 24, 2012
Published in issue: October 16, 2012

Keywords

  1. morphogenesis
  2. plant biomechanics
  3. biological chirality
  4. root growth and remodeling

Acknowledgments

The authors thank A. Moore, L. Ristroph, J. Savage, Z. Chen, L. Manning, M. Lapa, M. Haataja, J. Sethna, A. Alemi, B. Davidovitch, C. Orellana, E. Kolb, the Cohen lab, and the Mahadevan lab for stimulating conversation. We also thank J. Gregoire and S. Iams for assisting in apparatus development, J. Fetcho for kindly allowing us to use Imaris, M. Venkadesan for kindly loaning the translation stage, and J. Puzey for critically reading this manuscript. This work was supported by the National Science Foundation through a Graduate Research Fellowship to J.L.S., Grant IOS-0842720 supporting R.D.N., Grant DMR-1056662 supporting I.C., and Cornell’s IGERT Program in Nonlinear Systems (National Science Foundation Grant DGE-9870631) supporting S.J.G. This work was supported by the US Department of Energy through Grant DE-FG02-89ER-45405 supporting M.S.P. and C.L.H., and Grant DE-FG02-08ER46517 supporting S.J.G.

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Jesse L. Silverberg1 [email protected]
Department of Physics, Cornell University, Ithaca, NY 14853; and
Roslyn D. Noar
Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, NY 14853
Present address: Department of Plant Pathology, North Carolina State University, 2510 Thomas Hall, Raleigh, NC 27695-7616.
Michael S. Packer
Department of Physics, Cornell University, Ithaca, NY 14853; and
Maria J. Harrison
Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, NY 14853
Christopher L. Henley
Department of Physics, Cornell University, Ithaca, NY 14853; and
Itai Cohen
Department of Physics, Cornell University, Ithaca, NY 14853; and
Sharon J. Gerbode
Department of Physics, Cornell University, Ithaca, NY 14853; and
Present address: Department of Physics, Harvey Mudd College, 301 Platt Blvd., Claremont, CA 91711-5990.

Notes

1
To whom correspondence should be addressed. E-mail: [email protected].
Author contributions: J.L.S., M.J.H., C.L.H., I.C., and S.J.G. designed research; J.L.S., R.D.N., M.S.P., and S.J.G. performed research; J.L.S., C.L.H., I.C., and S.J.G. analyzed data; and J.L.S., M.J.H., C.L.H., I.C., and S.J.G. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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    3D imaging and mechanical modeling of helical buckling in Medicago truncatula plant roots
    Proceedings of the National Academy of Sciences
    • Vol. 109
    • No. 42
    • pp. 16751-17141

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