Abstract
Background and aims
The main difficulty in the use of 3D root architecture models is correct parameterization. We evaluated distributions of the root traits inter-branch distance, branching angle and axial root trajectories from contrasting experimental systems to improve model parameterization.
Methods
We analyzed 2D root images of different wheat varieties (Triticum aestivum) from three different sources using automatic root tracking. Model input parameters and common parameter patterns were identified from extracted root system coordinates. Simulation studies were used to (1) link observed axial root trajectories with model input parameters (2) evaluate errors due to the 2D (versus 3D) nature of image sources and (3) investigate the effect of model parameter distributions on root foraging performance.
Results
Distributions of inter-branch distances were approximated with lognormal functions. Branching angles showed mean values <90°. Gravitropism and tortuosity parameters were quantified in relation to downwards reorientation and segment angles of root axes. Root system projection in 2D increased the variance of branching angles. Root foraging performance was very sensitive to parameter distribution and variance.
Conclusions
2D image analysis can systematically and efficiently analyze root system architectures and parameterize 3D root architecture models. Effects of root system projection (2D from 3D) and deflection (at rhizotron face) on size and distribution of particular parameters are potentially significant.
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Abbreviations
- β:
-
Root segment angle to the horizontal
- ∆β:
-
Reorientation angle of an individual root segment
- De :
-
Diffusion coefficient of a solute in soil
- ibd:
-
Inter-branch distance
- IRC:
-
Inter-root competition
- μ:
-
Mean value
- σ:
-
Standard deviation of the random deflection angle (tortuosity)
- sg:
-
Sensitivity to gravitropism
- std:
-
Standard deviation
- θ:
-
Branching angle in the vertical plane
References
Abadia-Fenoll F, Casero P, Lloret P, Vidal M (1986) Development of lateral primordia in decapitated adventitious roots of Allium cepa. Ann Bot 58:103–107
Atkinson JA, Lobet G, Noll M, Meyer PE, Griffiths M, Wells DM (2017) Combining semi-automated image analysis techniques with machine learning algorithms to accelerate large scale genetic studies. GigaScience 6:1–7
Atkinson JA, Wingen LU, Griffiths M, Pound MP, Gaju O, Foulkes MJ, Le Gouis J, Griffiths S, Bennett MJ, King J (2015) Phenotyping pipeline reveals major seedling root growth QTL in hexaploid wheat. J Exp Bot 66:2283–2292
Bao Y, Aggarwal P, Robbins NE, Sturrock CJ, Thompson MC, Tan HQ, Tham C, Duan L, Rodriguez PL, Vernoux T, Mooney SJ, Bennett MJ, Dinneny JR (2014) Plant roots use a patterning mechanism to position lateral root branches toward available water. Proc Natl Acad Sci USA 111:9319–9324
Barlow P, Adam J (1988) The position and growth of lateral roots on cultured root axes of tomato, Lycopersicon esculentum (Solanaceae). Plant Syst Evol 158:141–154
Bauke SL, Landl M, Koch M, Hofmann D, Nagel KA, Siebers N, Schnepf A, Amelung W (2017) Macropore effects on phosphorus acquisition by wheat roots – a rhizotron study. Plant Soil 416:67–82
Bingham IJ, Wu L (2011) Simulation of wheat growth using the 3D root architecture model SPACSYS: validation and sensitivity analysis. Eur J Agron 34:181–189
Bouma TJ, Yanai RD, Elkin AD, Hartmond U, Flores-Alva DE, Eissenstat DM (2001) Estimating age-dependent costs and benefits of roots with contrasting life span: comparing apples and oranges. New Phytol 150:685–695
Clark RT, MacCurdy RB, Jung JK, Shaff JE, McCouch SR, Aneshansley DJ, Kochian LV (2011) 3-dimensional root phenotyping with a novel imaging and software platform. Plant Physiol 156:455–465
Clausnitzer V, Hopmans J (1994) Simultaneous modeling of transient three-dimensional root growth and soil water flow. Plant Soil 164:299–314
Delory BM, Baudson C, Brostaux Y, Lobet G, Du Jardin P, Pagès L, Delaplace P (2016) archiDART: an R package for the automated computation of plant root architectural traits. Plant Soil 398:351–365
Diggle AJ (1988) ROOTMAP - a model in three-dimensional coordinates of the growth and structure of fibrous root systems. Plant Soil 105:169–178
Doussan C, Pierret A, Garrigues E, Pagès L (2006) Water uptake by plant roots: II-modelling of water transfer int he soil root-system with explicit accoutn of flow within the root system - comparison with experiments. Plant Soil 283:99–117
Draye X (2002) Consequences of root growth kinetics and vascular structure on the distribution of lateral roots. Plant Cell Environ 25:1463–1474
Dunbabin V, Diggle AJ, Rengel Z, van Hugten R (2002) Modelling the interactions between water and nutrient uptake and root growth. Plant Soil 239:19–38
Dunbabin VM, Postma JA, Schnepf A, Pagès L, Javaux M, Wu L, Leitner D, Chen YL, Rengel Z, Diggle AJ (2013) Modelling root–soil interactions using three–dimensional models of root growth, architecture and function. Plant Soil 372:93–124
Fitter A, Stickland T, Harvey M, Wilson G (1991) Architectural analysis of plant root systems 1. Architectural correlates of exploitation efficiency. New Phytol 118:375–382
Forde BG (2009) Is it good noise? The role of developmental instability in the shaping of a root system. J Exp Bot 60:3989–4002
Gao S, Pan WL, Koenig RT (1998) Integrated root system age in relation to plant nutrient uptake activity. Agron J 90:505–510
Ge Z, Rubio G, Lynch JP (2000) The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model. Plant Soil 218:159–171
Hargreaves CE, Gregory PJ, Bengough AG (2009) Measuring root traits in barley (Hordeum vulgare ssp. vulgare and ssp. spontaneum) seedlings using gel chambers, soil sacs and X-ray microtomography. Plant Soil 316:285–297
Ito K, Tanakamaru K, Morita S, Abe J, Inanaga S (2006) Lateral root development, including responses to soil drying, of maize (Zea Mays) and wheat (Triticum aestivum) seminal roots. Physiol Plant 127:260–267
Javaux M, Schröder T, Vanderborght J, Vereecken H (2008) Use of a three-dimensional detailed modeling approach for predicting root water uptake. Vadose Zone J 7:1079–1079
Judd LA, Jackson BE, Fonteno WC (2015) Advancements in root growth measurement technologies and observation capabilities for container-grown plants. Plants 4:369–392
Kuchenbuch R, Ingram K (2002) Image analysis for non-destructive and non-invasive quantification of root growth and soilw ater content in rhizotrons. J Plant Nutr Soil Sci 165:573–581
Kuijken RC, van Eeuwijk FA, Marcelis LF, Bouwmeester HJ (2015) Root phenotyping: from component trait in the lab to breeding. J Exp Bot 66:5389–5401
Kutschera L (1960) Wurzelatlas mitteleuropäischer Ackerunkräuter und Kulturpflanzen. DLG-Verlag, Frankfurt/Main, pp 124, 574
Kutschera L, Lichtenegger E, Sobotik M (2009) Wurzelatlas der Kulturpflanzen gemäßigter Gebiete: mit Arten des Feldgemüsebaues. DLG-Verlag Frankfurt/Main, pp 222, 226–227
Landl M, Huber K, Schnepf A, Vanderborght J, Javaux M, Bengough AG, Vereecken H (2017) A new model for root growth in soil with macropores. Plant Soil 415:99–116
Le Bot J, Serra V, Fabre J, Draye X, Adamowicz S, Pagès L (2010) DART: a software to analyse root system architecture and development from captured images. Plant Soil 326:261–273
Leitner D, Felderer B, Vontobel P, Schnepf A (2014) Recovering root system traits using image analysis exemplified by two-dimensional neutron radiography images of lupine. Plant Physiol 164:24–35
Leitner D, Klepsch S, Bodner G, Schnepf A (2010) A dynamic root system growth model based on L-systems. Plant Soil 332:177–192
Liang J, Zhang J, Wong M (1996) Effects of air-filled soil porosity and aeration on the initiation and growth of secondary roots of maize (Zea Mays). Plant Soil 186:245–254
Lynch JP (2007) Roots of the second green revolution. Aust J Bot 55:493–512
Lynch JP, Nielsen KL, Davis RD, Jablokow AG (1997) SimRoot: modelling and visualization of root systems. Plant Soil 188:139–151
Mairhofer S, Zappala S, Tracy SR, Sturrock C, Bennett M, Mooney SJ, Pridmore T (2012) RooTrak: automated recovery of three-dimensional plant root architecture in soil from X-ray microcomputed tomography images using visual tracking. Plant Physiol 158:561–569
Mooney SJ, Pridmore TP, Helliwell J, Bennett MJ (2012) Developing X-ray computed tomography to non-invasively image 3-D root systems architecture in soil. Plant Soil 352:1–22
Nagel K, Putz A, Gilmer F, Heinz K, Fischbach A, Pfeifer J, Faget M, Bloßfeld S, Ernst M, Dimaki C, Kastenholz B, Kleinert A, Galinski A, Scharr H, Fiorani F, Schurr U (2012) GROWSCREEN-Rhizo is a novel phenotyping robot enablign simultaneous measruements of root and shoot growth for pkants grown in soil-filled rhizotrons. Funct Plant Biol 39:891–904
Nagel KA, Bonnett D, Furbank R, Walter A, Schurr U, Watt M (2015) Simultaneous effects of leaf irradiance and soil moisture on growth and root system architecture of novel wheat genotypes: implications for phenotyping. J Exp Bot 66:5441–5452
Nakamoto T (1994) Plagiogravitropism of maize roots. Plant Soil 165:327–332
Nye PH, Tinker PB (1977) Solute movement in the soil-root system. Univ of California Press, p 342
Pagès L (2011) Links between root developmental traits and foraging performance. Plant Cell Environ 34:1749–1760
Pagès L, Pellerin S (1994) Evaluation of parameters describing the root system architecture of field grown maize plants (Zea mays L.), II. Plant Soil 164:169–176
Pagès L, Picon-Cochard C (2014) Modelling the root system architecture of Poaceae. Can we simulate integrated traits from morphological parameters of growth and branching? New Phytol 204:149–158
Pagès L, Vercambre G, Drouet J-L, Lecompte F, Collet C, Le Bot J (2004) Root Typ: a generic model to depict and analyse the root system architecture. Plant Soil 258:103–119
Pellerin S, Pagès L (1994) Evaluation of parameters describing the root system architecture of field grown maize plants (Zea mays L.), I. Plant Soil 164:155–167
Pellerin S, Tabourel F (1995) Length of the apical unbranched zone of maize axile roots: its relationship to root elongation rate. Environ Exp Bot 35:193–200
Pohlmeier A, Javaux M, Vereecken H, Haber-Pohlmeier S (2013) Magnetic resonance imaging techniques for visualization of root growth and root water uptake processes. In: Anderson SH, Hopmans JW (eds) Soil–water–root processes: advances in tomography and imaging, pp 137–156. Publ, SSSA Spec, p 61
Popova L, van Dusschoten D, Nagel KA, Fiorani F, Mazzolai B (2016) Plant root tortuosity: an indicator of root path formation in soil with different composition and density. Ann Bot 118:685–698
Postma JA, Dathe A, Lynch JP (2014) The optimal lateral root branching density for maize depends on nitrogen and phosphorus availability. Plant Physiol 166:590–602
Rascher U, Blossfeld S, Fiorani F, Jahnke S, Jansen M, Kuhn AJ, Matsubara S, Märtin LL, Merchant A, Metzner R (2011) Non-invasive approaches for phenotyping of enhanced performance traits in bean. Funct Plant Biol 38:968–983
Rich S, Watt M (2013) Soil conditions and cereal root system architecture: review and considerations for linking Darwin and Weaver. J Exp Bot 64:1193–1208
Roose T, Schnepf A (2008) Mathematical models of plant–soil interaction. Philos Trans R Soc A 366:4597–4611
Schenk M, Barber S (1979) Phosphate uptake by corn as affected by soil characteristics and root morphology. Soil Sci Soc Am J 43:880–883
Smith S, De Smet I (2012) Root system architecture: insights from Arabidopsis and cereal crops. Philos Trans R Soc B 367:1441–1452
Tardieu F, Pellerin S (1990) Trajectory of the nodal roots of maize in fields with low mechanical constraints. Plant Soil 124:39–45
Tracy SR, Black CR, Roberts JA, Sturrock C, Mairhofer S, Craigon J, Mooney SJ (2012) Quantifying the impact of soil compaction on root system architecture in tomato (Solanum lycopersicum) by X-ray micro-computed tomography. Ann Bot 110:511–519
Tracy SR, Roberts JA, Black CR, McNeill A, Davidson R, Mooney SJ (2010) The X-factor: visualizing undisturbed root architecture in soils using X-ray computed tomography. J Exp Bot 61:311–313
Tricot F, Crozat Y, Pellerin S (1997) Root system growth and nodule establishment on pea (Pisum sativum L.) J Exp Bot 48:1935–1941
Volder A, Smart DR, Bloom AJ, Eissenstat DM (2005) Rapid decline in nitrate uptake and respiration with age in fine lateral roots of grape: implications for root efficiency and competitive effectiveness. New Phytol 165:493–502
Weaver JE, Jean FC, Crist JW (1922) Development and activities of roots of crop plants: a study in crop ecology. Agronomy & Horticulture -- Faculty Publications, paper 511
Weaver JE, Kramer J, Reed M (1924) Development of root and shoot of winter wheat under field environment. Ecology 5:26–50
Wenzel WW, Wieshammer G, Fitz WJ, Puschenreiter M (2001) Novel rhizobox design to assess rhizosphere characteristics at high spatial resolution. Plant Soil 237:37–45
Wu J, Pagès L, Wu Q, Yang B, Guo Y (2015) Three-dimensional architecture of axile roots of field-grown maize. Plant Soil 387:363–377
Wu L, McGechan M, McRoberts N, Baddeley J, Watson C (2007) SPACSYS: integration of a 3D root architecture component to carbon, nitrogen and water cycling—model description. Ecol Model 200:343–359
Wu L, McGechan M, Watson C, Baddeley J (2005) Developing existing plant root system architecture models to meet future agricultural challenges. Adv Agron 85:181–219
Yu P, Gutjahr C, Li C, Hochholdinger F (2016) Genetic control of lateral root formation in cereals. Trends Plant Sci 21:951–961
Acknowledgements
Funding by German Research Foundation within the Research Unit DFG PAK 888 is gratefully acknowledged. The James Hutton Institute receives funding from the Scottish Government. We also thank Klaas Metselaar from the Department of Environmental Sciences at Wageningen University, Netherlands, for providing high-resolution scans of wheat root images from the Root Atlas and the authors of Atkinson et al. (2017) for publicly sharing their image datasets.
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Landl, M., Schnepf, A., Vanderborght, J. et al. Measuring root system traits of wheat in 2D images to parameterize 3D root architecture models. Plant Soil 425, 457–477 (2018). https://doi.org/10.1007/s11104-018-3595-8
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DOI: https://doi.org/10.1007/s11104-018-3595-8