Abstract
Living roots grow in soil, which is a heterogeneous environment containing a wide variety of physical barriers. Roots must avoid these barriers to grow: first, they adopt a characteristic S-shape that can be described by the angle between the root tip and the barrier (i.e., the tip-to-barrier angle); then, they move parallel to the barrier by keeping the sensitive tip in contact with the barrier until it has been circumvented. We investigated this avoidance response in the primary roots of maize (Zea mays) by considering flat barriers oriented at 45, 60 and 90 degrees with respect to the gravity vector.
We measured the root tip orientation during growth by using time-lapse imaging and specially developed tip-tracking software (9 trials for each value of the barrier orientation). Remarkably, we found that the S-shapes formed by the roots were characterized by the same tip-to-barrier angle regardless of the barrier orientation: namely, 21.96 ± 2.97, 21.48 ± 4.75 and 20.81 ± 9.39 degrees for barriers oriented at 45, 60 and 90 degrees, respectively. We also considered the root growth after bypassing the barrier; for the barrier at 90 degrees, we observed a gravitropic recovery. Furthermore, we used a mathematical model to quantify the characteristic time of S-shape formation (95 min on average) and gravitropic recovery (approximately 42 min); the obtained values are consistent with those of previous studies.
Our results suggest that the avoidance response develops with respect to a reference frame associated with the barrier. From a biological viewpoint, the reason the root adopts the specifically observed tip-to-barrier angle is unclear, but we speculate that maize root optimizes energy expenditure during the penetration of a medium.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Asl F.M. & Galip Ulsoy A. 2003. Analysis of a system of linear delay differential equations. ASME J. Dyn. Syst., Measure. Control 125: 215–223.
Band L.R., Wells D.M., Larrieu A., Sun J., Middleton A.M., French A.P. et al. 2012. Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. Proc. Natl. Acad. Sci. USA 109: 4668–4673.
Bastien R., Bohr T., Moulia B. & Douady S. 2013. Unifying model of shoot gravitropism reveals proprioception as a central feature of posture control in plants. Proc. Natl. Acad. Sci. USA 110: 755–60.
Braam J. 2005. In touch: plant responses to mechanical stimuli. New Phytol. 165: 373–89.
Burbach C., Markus K., Zhang Y., Schlicht M. & Baluska F. 2012. Photophobie behavior of maize roots. Plant Signal. Behav. 7: 874–878.
Chehab E.W., Eich E. & Braam J. 2009. Thigmomorphogenesis: a complex plant response to mechano-stimulation. J. Exp. Bot. 60: 43–56.
Coutand C. 2010. Mechanosensing and thigmomorphogenesis, a physiological and biomechanical point of view. Plant Sci. 179: 168–182.
Darwin C. & Darwin F. 1897. The power of movement in plants. Appleton.
Digby J. & Firn R.D. 1995. The gravitropic set-point angle (GSA): the identification of an important develop mentally controlled variable governing plant architecture. Plant Cell Environ. 18: 1434–1440.
Driver R.D. 1977. Ordinary and Delay Differential Equations, New York, NY: Springer New York.
Eapen D., Barroso M.L., Ponce G., Campos M.E., Cassab G.I. 2005. Hydrotropism: root growth responses to water. Trends Plant Sci. 10: 44–50.
Esmon C.A., Pedmale U.V. & Liscum E. 2005. Plant tropisms: Providing the power of movement to a sessile organism. Inter. J. Develop. Biol. 49: 665–674.
Evans M. 2003. Touch sensitivity in plants: be aware or beware. Trends Plant Sci. 8: 312–314.
Evans M.L. 1991. Gravitropism: Interaction of sensitivity modulation and effector redistribution. Plant Physiol. 95: 1–5.
Fasano J.M., Massa G.D. & Gilroy S. 2002. Ionic signaling in plant responses to gravity and touch. J. Plant Growth Reg. 21: 71–88.
Firn R.D. & Digby J. 1997. Solving the puzzle of gravitropism - has a lost piece been found? Planta 203(S1): S159-S163.
Giehl R., Lima J.E. & von Wiren N. 2012. Localized iron supply triggers lateral root elongation in Arabidopsis by altering the AUXl-mediated auxin distribution. Plant Cell 24: 33–49.
Gilroy S. 2008. Plant tropisms. Curr. Biol. 18: 275–277.
Goss M.J. & Russell R.S. 1980. Effects of mechanical impedance on root growth in barley (Hordeum, vulgare L.). J. Exp. Bot. 31: 577–588.
Hahn A., Firn R. & Edelmann H.G. 2006. Interacting signal transduction chains in gravity-stimulated maize roots. Signal Transd. 6: 449–455.
Iino M., Tarui Y. & Uematsu C. 1996. Gravitropism of maize and rice coleoptiles: dependence on the stimulation angle. Plant, Cell, Environ. 19: 1160–1168.
Ishikawa H. & Evans M.L. 1992. Induction of curvature in maize roots by calcium or by thigmostimulation: Role of the postmitotic isodiametric growth zone. Plant Physiol. 100: 762–768.
Israelsson D. & Johnsson A. 1967. A theory for circumnutations in Helianthus annuus. Physiol. Plant. 20: 957–976.
Jin K. Shen J., Ashton, R.W., Dodd I.C., Parrz M.A.J. & Whalley W.R. 2013. How do roots elongate in a structured soil? J. Exp. Bot. 64: 4761–4777.
Leitz G. et al. 2009. Statolith sedimentation kinetics and force transduction to the cortical endoplasmic reticulum in gravity-sensing Arabidopsis columella cells. Plant Cell 21: 843–860.
Leopold A.C. & Wettlaufer S.H. 1989. Springback in root gravitropism. Plant Physiol. 91: 1247–1250.
Massa G.D. & Gilroy S. 2003a. Touch and gravitropic set-point angle interact to modulate gravitropic growth in roots. Adv. Space Res. 31: 2195–2202.
Massa G.D. & Gilroy S. 2003b. Touch modulates gravity sensing to regulate the growth of primary roots of Arabidopsis thaliana. Plant J. 33: 435–445.
Mazzolai B., Mondini A., Corradi P. & Laschi C. 2011. A miniaturized mechatronic system inspired by plant roots for soil exploration. IEEE/ASME Transactions on Mechatronics 16: 201–212.
McCully M.E. 1999. Roots in soil: Unearthing the complexities of roots and their rhizospheres. Ann. Rev. Plant Physiol. Plant Mol. Biol. 50: 695–718.
Meskauskas A., Moore D. & Frazer L.N. 1998. Mathematical modelling of morphogenesis in fungi: spatial organization of the gravitropic response in the mushroom stem of Coprinus cinereus. New Phytol. 140: 111–123.
MoM, Yokava K., Wan Y. & Baluška F. 2015. How and why do root apices sense light under the soil surface? Front. Plant Sci. 6: 775.
Monshausen G.B. & Gilroy S. 2009. Feeling green: mechanosens-ing in plants. Trends Cell Biol. 19: 228–35.
Monshausen G.B., Bibibkova T.N., Weisenseel M.H. & Gilroy S. 2009. Ca2+ regulates reactive oxygen species production and pH during mechanosensing in Arabidopsis roots. Plant Cell 21: 2341–56.
Moulia B. & Fournier M. 2009. The power and control of gravitropic movements in plants: a biomechanical and systems biology view. J. Exp. Bot. 60: 461–86.
Nelson A.J. & Evans M.L. 1986. Analysis of growth patterns during gravitropic curvature in roots of Zea mays by use of a computer-based video digitizer. J. Plant Growth Reg. 5: 73–83.
Perbal G., Jeune B., Lefranc A., Carnero-Diaz E. & Driss-Ecole D. 2002. The dose-response curve of the gravitropic reaction: a re-analysis. Physiol. Plant. 114: 336–342.
Popova L., Russino A., Ascrizzi A. & Mazzolai B. 2012. Analysis of movement in primary maize roots. Biologia 67: 517–524.
Russino A., Ascrizzi A., Popova L., Tonazzini A., Mancuso S. & Mazzolai B. 2013. A novel tracking tool for the analysis of plant-root tip movements. Bioinspir. Biomim. 8(2): 025004.
Sachs J. 1887. Vorlesungen über Pflanzenphysiologie. Würzburg 1882. Engl, transln.: Lectures on the physiology of plants. Clarendon Press, Oxford.
Sadeghi A., Tonazzini A., Popova L. & Mazzolai B. 2013. Innovative Robotic Mechanism for Soil Penetration Inspired by Plant Roots, pp. 3457–3463. In: Proceedings in IEEE International Conference on Robotics and Automation (ICRA), Karlsruhe, Germany.
Sadeghi A., Tonazzini A., Popova L. & Mazzolai B. 2014. A novel growing device inspired by plant root soil penetration behaviors. PloS one 9(2): e90139.
Svistoonoff S. Creff A., Reymond M., Sigoillot-Claude C., Ri-caud L., Blanchet A., Nussaume L. & Desnos T. 2007. Root tip contact with low-phosphate media reprograms plant root architecture. Nat. Genet. 39: 792–796.
Weerasinghe R., Swanson S. & Okada S. 2009. Touch induces ATP release in Arabidopsis roots that is modulated by the heterotrimeric G-protein complex. FEBS Lett. 583: 2521–2526.
Yokawa K., Kagenishi T. & Baluska F. 2013. Root photomor-phogenesis in laboratory-maintained Arabidopsis seedlings. Trends Plant Sci. 18: 117–119.
Yokawa K. Fasano R., Kagenishi T. & Baluška F. 2014. Light as stress factor to plant roots - case of root halotropism. Front. Plant Sci. 5: 718.
Zieschang H.E., Brain P. & Barlow P.W. 1997. Modelling of root growth and bending in two dimensions. J. Theoret. Biol. 184: 237–246.
Zou N., Li B., Dong G., Kronzucer H.J. & Shi W. 2012. Ammonium-induced loss of root gravitropism is related to auxin distribution and TRH1 function, and is uncoupled from the inhibition of root elongation in Arabidopsis. J. Exp. Bot. 63: 3777–3788.
Acknowledgements
This work was supported by the Future and Emerging Technologies (FET) programme within the Seventh Framework Program for Research of the European Commission, under FET-Open grant number 293431.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Popova, L., Tonazzini, A., Di Michele, F. et al. Unveiling the kinematics of the avoidance response in maize (Zea mays) primary roots. Biologia 71, 161–168 (2016). https://doi.org/10.1515/biolog-2016-0022
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1515/biolog-2016-0022