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.
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.
References
Asl F.M. & Galip Ulsoy A. 2003. Analysis of a system of linear delay differential equations. ASME J. Dyn. Syst., Measure. Control 125: 215–223.10.1115/1.1568121Search in Google Scholar
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: 4668–4673.10.1073/pnas.1201498109Search in Google Scholar PubMed PubMed Central
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: 755–60.10.1073/pnas.1214301109Search in Google Scholar PubMed PubMed Central
Braam J. 2005. In touch: plant responses to mechanical stimuli. New Phytol. 165: 373–89.10.1111/j.1469-8137.2004.01263.xSearch in Google Scholar PubMed
Burbach C., Markus K., Zhang Y., Schlicht M. & Baluška F. 2012. Photophobic behavior of maize roots. Plant Signal. Behav. 7: 874–878.10.4161/psb.21012Search in Google Scholar PubMed PubMed Central
Chehab E.W., Eich E. & Braam J. 2009. Thigmomorphogenesis: a complex plant response to mechano-stimulation. J. Exp. Bot. 60: 43–56.10.1093/jxb/ern315Search in Google Scholar PubMed
Coutand C. 2010. Mechanosensing and thigmomorphogenesis, a physiological and biomechanical point of view. Plant Sci. 179: 168–182.10.1016/j.plantsci.2010.05.001Search in Google Scholar
Darwin C. & Darwin F. 1897. The power of movement in plants. Appleton.10.5962/bhl.title.56998Search in Google Scholar
Digby J. & Firn R.D. 1995. The gravitropic set-point angle (GSA): the identification of an important developmentally controlled variable governing plant architecture. Plant Cell Environ. 18: 1434–1440.10.1111/j.1365-3040.1995.tb00205.xSearch in Google Scholar PubMed
Driver R.D. 1977. Ordinary and Delay Differential Equations, New York, NY: Springer New York.10.1007/978-1-4684-9467-9Search in Google Scholar
Eapen D., Barroso M.L., Ponce G., Campos M.E., Cassab G.I. 2005. Hydrotropism: root growth responses to water. Trends Plant Sci. 10: 44–50.10.1016/j.tplants.2004.11.004Search in Google Scholar
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: 665–674.10.1387/ijdb.052028ceSearch in Google Scholar
Evans M. 2003. Touch sensitivity in plants: be aware or beware. Trends Plant Sci. 8: 312–314.10.1016/S1360-1385(03)00133-XSearch in Google Scholar
Evans M.L. 1991. Gravitropism: Interaction of sensitivity modulation and effector redistribution. Plant Physiol. 95: 1–5.10.1104/pp.95.1.1Search in Google Scholar PubMed PubMed Central
Fasano J.M., Massa G.D. & Gilroy S. 2002. Ionic signaling in plant responses to gravity and touch. J. Plant Growth Reg. 21: 71–88.10.1007/s003440010049Search in Google Scholar PubMed
Firn R.D. & Digby J. 1997. Solving the puzzle of gravitropism – has a lost piece been found? Planta 203(S1): S159–S163.10.1007/PL00008104Search in Google Scholar
Giehl R., Lima J.E. & von Wiren N. 2012. Localized iron supply triggers lateral root elongation in Arabidopsis by altering the AUX1-mediated auxin distribution. Plant Cell 24: 33–49.10.1105/tpc.111.092973Search in Google Scholar PubMed PubMed Central
Gilroy S. 2008. Plant tropisms. Curr. Biol. 18: 275–277.10.1016/j.cub.2008.02.033Search in Google Scholar PubMed
Goss M.J. & Russell R.S. 1980. Effects of mechanical impedance on root growth in barley (Hordeum vulgare L.). J. Exp. Bot. 31: 577–588.10.1093/jxb/31.2.577Search in Google Scholar
Hahn A., Firn R. & Edelmann H.G. 2006. Interacting signal transduction chains in gravity-stimulated maize roots. Signal Transd. 6: 449–455.10.1002/sita.200600109Search in Google Scholar
Iino M., Tarui Y. & Uematsu C. 1996. Gravitropism of maize and rice coleoptiles: dependence on the stimulation angle. Plant, Cell, Environ. 19: 1160–1168.10.1111/j.1365-3040.1996.tb00431.xSearch in Google Scholar
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: 762–768.10.1104/pp.100.2.762Search in Google Scholar
Israelsson D. & Johnsson A. 1967. A theory for circumnutations in Helianthus annuus. Physiol. Plant. 20: 957–976.10.1111/j.1399-3054.1967.tb08383.xSearch in Google Scholar
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: 4761–4777.10.1093/jxb/ert286Search in Google Scholar
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: 843–860.10.1105/tpc.108.065052Search in Google Scholar
Leopold A.C. & Wettlaufer S.H. 1989. Springback in root gravitropism. Plant Physiol. 91: 1247–1250.10.1104/pp.91.4.1247Search in Google Scholar
Massa G.D. & Gilroy S. 2003a. Touch and gravitropic set-point angle interact to modulate gravitropic growth in roots. Adv. Space Res. 31: 2195–2202.10.1016/S0273-1177(03)00244-8Search in Google Scholar
Massa G.D. & Gilroy S. 2003b. Touch modulates gravity sensing to regulate the growth of primary roots of Arabidopsis thaliana.Plant J. 33: 435–445.10.1046/j.1365-313X.2003.01637.xSearch in Google Scholar
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: 201–212.10.1109/TMECH.2009.2038997Search in Google Scholar
McCully M.E. 1999. Roots in soil: Unearthing the complexities of roots and their rhizospheres. Ann. Rev. Plant Physiol. Plant Mol. Biol. 50: 695–718.10.1146/annurev.arplant.50.1.695Search in Google Scholar PubMed
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: 111–123.10.1046/j.1469-8137.1998.00252.xSearch in Google Scholar PubMed
Mo M., Yokava K., Wan Y. & Baluška F. 2015. How and why do root apices sense light under the soil surface? Front. Plant Sci. 6: 775.10.3389/fpls.2015.00775Search in Google Scholar PubMed PubMed Central
Monshausen G.B. & Gilroy S. 2009. Feeling green: mechanosensing in plants. Trends Cell Biol. 19: 228–35.10.1016/j.tcb.2009.02.005Search in Google Scholar PubMed
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: 2341–56.10.1105/tpc.109.068395Search in Google Scholar PubMed PubMed Central
Moulia B. & Fournier M. 2009. The power and control of gravitropic movements in plants: a biomechanical and systems biology view. J. Exp. Bot. 60: 461–86.10.1093/jxb/ern341Search in Google Scholar PubMed
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: 73–83.10.1007/BF02025958Search in Google Scholar PubMed
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: 336–342.10.1034/j.1399-3054.2002.1140302.xSearch in Google Scholar PubMed
Popova L., Russino A., Ascrizzi A. & Mazzolai B. 2012. Analysis of movement in primary maize roots. Biologia 67: 517–524.10.2478/s11756-012-0023-zSearch in Google Scholar
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): 025004.10.1088/1748-3182/8/2/025004Search in Google Scholar PubMed
Sachs J. 1887. Vorlesungen ¨urzburg uber Pflanzenphysiologie. W¨1882. Engl. transln.: Lectures on the physiology of plants. Clarendon Press, Oxford.10.5962/bhl.title.54852Search in Google Scholar
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.10.1109/ICRA.2013.6631060Search in Google Scholar
Sadeghi A., Tonazzini A., Popova L. & Mazzolai B. 2014. A novel growing device inspired by plant root soil penetration behaviors. PloS one 9(2): e90139.10.1371/journal.pone.0090139Search in Google Scholar PubMed PubMed Central
Svistoonoff S. Creff A., Reymond M., Sigoillot-Claude C., Ricaud L., Blanchet A., Nussaume L. & Desnos T. 2007. Root tip contact with low-phosphate media reprograms plant root architecture. Nat. Genet. 39: 792–796.10.1038/ng2041Search in Google Scholar PubMed
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: 2521-2526.10.1016/j.febslet.2009.07.007Search in Google Scholar PubMed PubMed Central
Yokawa K., Kagenishi T. & Baluška F. 2013. Root photomorphogenesis in laboratory-maintained Arabidopsis seedlings. Trends Plant Sci. 18: 117–119.10.1016/j.tplants.2013.01.002Search in Google Scholar PubMed
Yokawa K. Fasano R., Kagenishi T. & Baluška F. 2014. Light as stress factor to plant roots – case of root halotropism. Front. Plant Sci. 5: 718.10.3389/fpls.2014.00718Search in Google Scholar PubMed PubMed Central
Zieschang H.E., Brain P. & Barlow P.W. 1997. Modelling of root growth and bending in two dimensions. J. Theoret. Biol. 184: 237–246.10.1006/jtbi.1996.0259Search in Google Scholar PubMed
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: 3777–3788.10.1093/jxb/ers068Search in Google Scholar PubMed
© 2016 Institute of Botany, Slovak Academy of Sciences
Articles in the same Issue
- Cellular and Molecular Biology
- Antimicrobial resistance and molecular characterisation of human campylobacters from Slovakia
- Cellular and Molecular Biology
- Application of violet pigment from Chromobacterium violaceum UTM5 in textile dyeing
- Cellular and Molecular Biology
- Chemical composition and antioxidant activity of some important betel vine landraces
- Cellular and Molecular Biology
- Development of conventional and real time PCR assay for detection and quantification of Rhizoctonia solani infecting pulse crops
- Botany
- Somatic embryogenesis and in vitro shoot propagation of Gentianautriculosa
- Botany
- Effect of cold treatment on germination of Saxifraga aizoides and S. paniculata: a comparison of central (eastern Alps) and southern populations (northern Apennines)
- Botany
- Environmental factors and phytohormones enhancing expression of α-momorcharin gene in Momordica charantia
- Botany
- Unveiling the kinematics of the avoidance response in maize (Zen mays) primary roots
- Zoology
- Review of the species allocated to the genus Satchellius (Oligochaeta: Lumbricidae) with description of a new species
- Cellular and Molecular Biology
- Cation metals specific hemocyanin exhibits differential antibacterial property in mud crab, Scylla serrata
- Zoology
- Dynamics of soil Collembola communities (Hexapoda: Collembola) along the mesoclimatic gradient in a deep karst valley
- Zoology
- Hidden invertebrate diversity – phytotelmata in Bromeliaceae from palm houses and florist wholesalers (Poland)
- Zoology
- Species composition of mosquitoes (Diptera: Culicidae) in relation to climate conditions in South-Eastern Slovakia
- Zoology
- Effect of supplemental feeds on liver and intestine of common carp (Cyprinus carpio) in semi-intensive rearing system: histological implications
- Zoology
- Trace element enrichment in the eggshells of Grus japonensis and its association witheggshell thinningin ZhalongWetland (Northeastern China)
Articles in the same Issue
- Cellular and Molecular Biology
- Antimicrobial resistance and molecular characterisation of human campylobacters from Slovakia
- Cellular and Molecular Biology
- Application of violet pigment from Chromobacterium violaceum UTM5 in textile dyeing
- Cellular and Molecular Biology
- Chemical composition and antioxidant activity of some important betel vine landraces
- Cellular and Molecular Biology
- Development of conventional and real time PCR assay for detection and quantification of Rhizoctonia solani infecting pulse crops
- Botany
- Somatic embryogenesis and in vitro shoot propagation of Gentianautriculosa
- Botany
- Effect of cold treatment on germination of Saxifraga aizoides and S. paniculata: a comparison of central (eastern Alps) and southern populations (northern Apennines)
- Botany
- Environmental factors and phytohormones enhancing expression of α-momorcharin gene in Momordica charantia
- Botany
- Unveiling the kinematics of the avoidance response in maize (Zen mays) primary roots
- Zoology
- Review of the species allocated to the genus Satchellius (Oligochaeta: Lumbricidae) with description of a new species
- Cellular and Molecular Biology
- Cation metals specific hemocyanin exhibits differential antibacterial property in mud crab, Scylla serrata
- Zoology
- Dynamics of soil Collembola communities (Hexapoda: Collembola) along the mesoclimatic gradient in a deep karst valley
- Zoology
- Hidden invertebrate diversity – phytotelmata in Bromeliaceae from palm houses and florist wholesalers (Poland)
- Zoology
- Species composition of mosquitoes (Diptera: Culicidae) in relation to climate conditions in South-Eastern Slovakia
- Zoology
- Effect of supplemental feeds on liver and intestine of common carp (Cyprinus carpio) in semi-intensive rearing system: histological implications
- Zoology
- Trace element enrichment in the eggshells of Grus japonensis and its association witheggshell thinningin ZhalongWetland (Northeastern China)