Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

GROWSCREEN-Rhizo is a novel phenotyping robot enabling simultaneous measurements of root and shoot growth for plants grown in soil-filled rhizotrons

Kerstin A. Nagel A C , Alexander Putz A , Frank Gilmer A B , Kathrin Heinz A , Andreas Fischbach A , Johannes Pfeifer A , Marc Faget A , Stephan Blossfeld A , Michaela Ernst A , Chryssa Dimaki A , Bernd Kastenholz A , Ann-Katrin Kleinert A , Anna Galinski A , Hanno Scharr A , Fabio Fiorani A and Ulrich Schurr A
+ Author Affiliations
- Author Affiliations

A Institute of Bio- and Geosciences, IBG-2: Plant Sciences, Forschungszentrum Jülich GmbH, 52425 Jülich, Germany.

B Present address: BASF SE, 67117 Limburgerhof, Germany.

C Corresponding author. Email: k.nagel@fz-juelich.de

Functional Plant Biology 39(11) 891-904 https://doi.org/10.1071/FP12023
Submitted: 21 January 2012  Accepted: 14 April 2012   Published: 7 June 2012

Abstract

Root systems play an essential role in ensuring plant productivity. Experiments conducted in controlled environments and simulation models suggest that root geometry and responses of root architecture to environmental factors should be studied as a priority. However, compared with aboveground plant organs, roots are not easily accessible by non-invasive analyses and field research is still based almost completely on manual, destructive methods. Contributing to reducing the gap between laboratory and field experiments, we present a novel phenotyping system (GROWSCREEN-Rhizo), which is capable of automatically imaging roots and shoots of plants grown in soil-filled rhizotrons (up to a volume of ~18 L) with a throughput of 60 rhizotrons per hour. Analysis of plants grown in this setup is restricted to a certain plant size (up to a shoot height of 80 cm and root-system depth of 90 cm). We performed validation experiments using six different species and for barley and maize, we studied the effect of moderate soil compaction, which is a relevant factor in the field. First, we found that the portion of root systems that is visible through the rhizotrons’ transparent plate is representative of the total root system. The percentage of visible roots decreases with increasing average root diameter of the plant species studied and depends, to some extent, on environmental conditions. Second, we could measure relatively minor changes in root-system architecture induced by a moderate increase in soil compaction. Taken together, these findings demonstrate the good potential of this methodology to characterise root geometry and temporal growth responses with relatively high spatial accuracy and resolution for both monocotyledonous and dicotyledonous species. Our prototype will allow the design of high-throughput screening methodologies simulating environmental scenarios that are relevant in the field and will support breeding efforts towards improved resource use efficiency and stability of crop yields.

Additional keywords: heritability, imaging, robotised, root-system architecture, root traits, soil strength.


References

Anithakumari AM, Dolstra O, Vosman B, Visser RGF, van der Linden CG (2011) In vitro screening and QTL analysis for drought tolerance in diploid potato. Euphytica 181, 357–369.
In vitro screening and QTL analysis for drought tolerance in diploid potato.CrossRef |

Ao J, Fu J, Tian J, Yan X, Liao H (2010) Genetic variability for root morph-architecture traits and root growth dynamics as related to phosphorus efficiency in soybean. Functional Plant Biology 37, 304–312.
Genetic variability for root morph-architecture traits and root growth dynamics as related to phosphorus efficiency in soybean.CrossRef |

Armengaud P, Zambaux K, Hills A, Sulpice R, Pattison RJ, Blatt MR, Amtmann A (2009) EZ-Rhizo: integrated software for the fast and accurate measurement of root system architecture. The Plant Journal 57, 945–956.
EZ-Rhizo: integrated software for the fast and accurate measurement of root system architecture.CrossRef | 1:CAS:528:DC%2BD1MXjslSltr0%3D&md5=d0a99b3eb76652e541d0f8d933e01caaCAS |

Arraouadi S, Chardon F, Huguet T, Aouani ME, Badri M (2011) QTLs mapping of morphological traits related to salt tolerance in Medicago truncatula. Acta Physiologiae Plantarum 33, 917–926.
QTLs mapping of morphological traits related to salt tolerance in Medicago truncatula.CrossRef |

Atwell BJ (1993) Response of roots to mechanical impedance. Environmental and Experimental Botany 33, 27–40.
Response of roots to mechanical impedance.CrossRef |

Beemster GTS, Masle J, Williamson RE, Farquhar GD (1996) Effects of soil resistance to root penetration on leaf expansion in wheat (Triticum aestivum L): kinematic analysis of leaf elongation. Journal of Experimental Botany 47, 1663–1678.
Effects of soil resistance to root penetration on leaf expansion in wheat (Triticum aestivum L): kinematic analysis of leaf elongation.CrossRef | 1:CAS:528:DyaK2sXjsFCntw%3D%3D&md5=f48e5ea10416f75cf47963b102886dd5CAS |

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. Journal of Experimental Botany 62, 59–68.
Root elongation, water stress, and mechanical impedance: a review of limiting stresses and beneficial root tip traits.CrossRef | 1:CAS:528:DC%2BC3cXhsFamurbI&md5=057c8554b9cb0a788a62484554d4bc46CAS |

Blossfeld S, Gansert D, Thiele B, Kuhn AJ, Lösch R (2011) The dynamics of oxygen concentration, pH value, and organic acids in the rhizosphere of Juncus spp. Soil Biology & Biochemistry 43, 1186–1197.
The dynamics of oxygen concentration, pH value, and organic acids in the rhizosphere of Juncus spp.CrossRef | 1:CAS:528:DC%2BC3MXkvFagtL8%3D&md5=b83ba310aa2c120fe6bd5b792a6474c3CAS |

Clark LJ, Whalley WR, Barraclough PB (2003) How do roots penetrate strong soil? Plant and Soil 255, 93–104.
How do roots penetrate strong soil?CrossRef | 1:CAS:528:DC%2BD3sXotV2js7g%3D&md5=ec98ef1937fa2d84bdfc61fbd9bbd0c5CAS |

Clark RT, MacCurdy RB, Jung JK, Shaff JE, McCouch SR, Aneshansley DJ, Kochian LV (2011) Three-dimensional root phenotyping with a novel imaging and software platform. Plant Physiology 156, 455–465.
Three-dimensional root phenotyping with a novel imaging and software platform.CrossRef | 1:CAS:528:DC%2BC3MXnvFWrs7k%3D&md5=49db2ac97437073bc00c679f65548e53CAS |

De Smet I, White PJ, Bengough AG, Dupuy L, Parizot B, Casimiro I, Heidstra R, Laskowski M, Lepetit M, Hochholdinger F, Draye X, Zhang H, Broadley MR, Péret B, Hammond JP, Fukaki H, Mooney S, Lynch JP, Nacry P, Schurr U, Laplaze L, Benfey P, Beeckman T, Bennett M (2012) Analyzing lateral root development: how to move forward. The Plant Cell 24, 15–20.
Analyzing lateral root development: how to move forward.CrossRef | 1:CAS:528:DC%2BC38XltVOlu7w%3D&md5=402d320087f748ac24c6a0ad4927d609CAS |

Devienne-Barret F, Richard-Molard C, Chelle M, Maury O, Ney B (2006) Ara-rhizotron: an effective culture system to study simultaneously root and shoot development of Arabidopsis. Plant and Soil 280, 253–266.
Ara-rhizotron: an effective culture system to study simultaneously root and shoot development of Arabidopsis.CrossRef | 1:CAS:528:DC%2BD28XhslOrsLk%3D&md5=f0591f36fd1704fc1f5e56258606e6d0CAS |

Dhanda SS, Sethi GS, Behl RK (2004) Indices of drought tolerance in wheat genotypes at early stages of plant growth. Journal Agronomy & Crop Science 190, 6–12.
Indices of drought tolerance in wheat genotypes at early stages of plant growth.CrossRef |

Garrigues E, Doussan C, Pierret A (2006) Water uptake by plant roots: I – Formation and propagation of a water extraction front in mature root systems as evidenced by 2D light transmission imaging. Plant and Soil 283, 83–98.
Water uptake by plant roots: I – Formation and propagation of a water extraction front in mature root systems as evidenced by 2D light transmission imaging.CrossRef | 1:CAS:528:DC%2BD28XpvVGgsbc%3D&md5=7fb49e34fbbe532495244445e8e52b07CAS |

Giuliani S, Sanguineti MC, Tuberosa R, Bellotti M, Salvi S, Landi P (2005) Root-ABA1, a major constitutive QTL, affects maize root architecture and leaf ABA concentration at different water regimes. Journal of Experimental Botany 56, 3061–3070.
Root-ABA1, a major constitutive QTL, affects maize root architecture and leaf ABA concentration at different water regimes.CrossRef | 1:CAS:528:DC%2BD2MXht1GlsbnF&md5=f0ae5acec49abb02d83275be6eeacd59CAS |

Golzarian MR, Frick RA, Rajendran K, Berger B, Roy S, Tester M, Lun DS (2011) Accurate inference of shoot biomass from high-throughput images of cereal plants. Plant Methods 7, 2
Accurate inference of shoot biomass from high-throughput images of cereal plants.CrossRef | 1:CAS:528:DC%2BC3MXisFSrtb4%3D&md5=18a63d34a63a8ddd51089f59c8e9601dCAS |

Gonzalez N, Beemster GTS, Inze D (2009) David and Goliath: what can the tiny weed Arabidopsis teach us to improve biomass production in crops? Current Opinion in Plant Biology 12, 157–164.
David and Goliath: what can the tiny weed Arabidopsis teach us to improve biomass production in crops?CrossRef | 1:CAS:528:DC%2BD1MXjsVOgtbs%3D&md5=96e86541aeb6448e74e9846675c0eeb9CAS |

Granier C, Aguirrezabal L, Chenu K, Cookson SJ, Dauzat M, Hamard P, Thioux J-J, Rolland G, Bouchier-Combaud S, Lebaudy A, Muller B, Simonneau T, Tardieu F (2006) PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit. New Phytologist 169, 623–635.
PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit.CrossRef |

Gregory PJ (1979) A periscope method for observation root growth and distribution in field soil. Journal of Experimental Botany 30, 205–214.
A periscope method for observation root growth and distribution in field soil.CrossRef |

Gregory PJ, Hutchison DJ, Read DB, Jenneson PM, Gilboy WB, Morton EJ (2003) Non-invasive imaging of roots with high resolution x-ray micro-tomography. Plant and Soil 255, 351–359.
Non-invasive imaging of roots with high resolution x-ray micro-tomography.CrossRef | 1:CAS:528:DC%2BD3sXotVyqu70%3D&md5=2192fafc327aba0ff6193d12abe372abCAS |

Gregory PJ, Bengough AG, Grinev D, Schmidt S, Thomas WBTB, Wojciechowski T, Young IM (2009) Root phenomics of crops: opportunities and challenges. Functional Plant Biology 36, 922–929.
Root phenomics of crops: opportunities and challenges.CrossRef |

Hammer GL, Dong Z, McLean G, Doherty A, Messina C, Schussler J, Zinselmeier C, Paszkiewicz S, Cooper M (2009) Can changes in canopy and/or root system architecture explain historical maize yield trends in the US corn belt? Crop Science 49, 299–312.
Can changes in canopy and/or root system architecture explain historical maize yield trends in the US corn belt?CrossRef |

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 and Soil 316, 285–297.
Measuring root traits in barley (Hordeum vulgare ssp. vulgare and ssp. spontaneum) seedlings using gel chambers, soil sacs and x-ray microtomography.CrossRef | 1:CAS:528:DC%2BD1MXhsFOksbk%3D&md5=6e273151cb91cbe6ac43dbfc79424a25CAS |

Heeraman DA, Hopmans JW, Clausnitzer V (1997) Three dimensional imaging of plant roots in situ with x-ray computed tomography. Plant and Soil 189, 167–179.
Three dimensional imaging of plant roots in situ with x-ray computed tomography.CrossRef | 1:CAS:528:DyaK2sXksVymur0%3D&md5=b99745248b6db4c2b79024e1260ec4f6CAS |

Herder GD, Isterdael GV, Beeckman T, De Smet I (2010) The roots of a new green revolution. Trends in Plant Science 15, 600–607.
The roots of a new green revolution.CrossRef |

Hilton RJ, Bhar DS, Mason GF (1969) A rhizotron for in situ root growth studies. Canadian Journal of Plant Science 49, 101–104.
A rhizotron for in situ root growth studies.CrossRef |

Hund A, Ruta N, Liedgens M (2009) Rooting depth and water use efficiency of tropical maize inbred lines, differing in drought tolerance. Plant and Soil 318, 311–325.
Rooting depth and water use efficiency of tropical maize inbred lines, differing in drought tolerance.CrossRef | 1:CAS:528:DC%2BD1MXltVWrsLg%3D&md5=ee5703977182f7ca23379d3d332ff887CAS |

Hurd EA (1964) Root study of three wheat varieties and their resistance to drought and damage by soil cracking. Canadian Journal of Plant Science 44, 240–248.
Root study of three wheat varieties and their resistance to drought and damage by soil cracking.CrossRef |

Hutchings MJ, John EA (2004) The effects of environmental heterogeneity on root growth and root/shoot partitioning. Annals of Botany 94, 1–8.
The effects of environmental heterogeneity on root growth and root/shoot partitioning.CrossRef |

Iyer-Pascuzzi AS, Symonova O, Mileyko Y, Hao Y, Belcher H, Harer J, Weitz JS, Benfey PN (2010) Imaging and analysis platform for automated phenotyping and trait ranking of plant root systems. Plant Physiology 152, 1148–1157.
Imaging and analysis platform for automated phenotyping and trait ranking of plant root systems.CrossRef | 1:CAS:528:DC%2BC3cXmsF2ls78%3D&md5=cb1bba48b70aa8ef14faa0c525b3a8bbCAS |

Jahnke S, Menzel MI, van Dusschoten D, Roeb GW, Bühler J, Minwuyelet S, Blümler P, Temperton VM, Hombach T, Streun M, Beer S, Khodaverdi M, Ziemons K, Coenen HH, Schurr U (2009) Combined MRI–PET dissects dynamic changes in plant structures and functions. The Plant Journal 59, 634–644.
Combined MRI–PET dissects dynamic changes in plant structures and functions.CrossRef | 1:CAS:528:DC%2BD1MXhtFChtrrK&md5=0790bd18cc5392c909273062b6c0461eCAS |

Jansen M, Gilmer F, Biskup B, Nagel KA, Rascher U, Fischbach A, Briem S, Dreissen G, Tittmann S, Braun S, De Jaeger I, Metzlaff M, Schurr U, Scharr H, Walter A (2009) Simultaneous phenotyping of leaf growth and chlorophyll fluorescence via GROWSCREEN FLUORO allows detection of stress tolerance in Arabidopsis thaliana and other rosette plants. Functional Plant Biology 36, 902–914.
Simultaneous phenotyping of leaf growth and chlorophyll fluorescence via GROWSCREEN FLUORO allows detection of stress tolerance in Arabidopsis thaliana and other rosette plants.CrossRef | 1:CAS:528:DC%2BD1MXhtlOgs7rF&md5=f5e29447ec332857f8a47803fa405c61CAS |

Johnson N, Robinson HF, Comstock RE (1955) Genotypic and phenotypic correlations in sorghum and simplification in selection. Agronomy Journal 47, 477–482.
Genotypic and phenotypic correlations in sorghum and simplification in selection.CrossRef |

Johnson MG, Tingey DT, Phillips DL, Storm MJ (2001) Advancing fine root research with minirhizotrons. Environmental and Experimental Botany 45, 263–289.
Advancing fine root research with minirhizotrons.CrossRef |

Jones A (1977) Heritabilities of seven sweet potato root traits. Journal of the American Society for Horticultural Science 102, 440–442.

Jones JB (1982) Hydroponics: its history and use in plant nutrition studies. Journal of Plant Nutrition 5, 1003–1030.
Hydroponics: its history and use in plant nutrition studies.CrossRef | 1:CAS:528:DyaL38Xlt1Khsrs%3D&md5=b0837ba9307b5a3f76b07ea88af169cfCAS |

Kashiwagi J, Krishnamurthy L, Upadhyaya HD, Krishna H, Chandra S, Vadez V, Serraj R (2005) Genetic variability of drought-avoidance root traits in the mini-core germplasm collection of chickpea (Cicer arietinum L.). Euphytica 146, 213–222.
Genetic variability of drought-avoidance root traits in the mini-core germplasm collection of chickpea (Cicer arietinum L.).CrossRef |

Kuchenbuch RO, Ingram KT (2002) Image analysis for non-destructive and non-invasive quantification of root growth and soil water content in rhizotrons. Journal of Plant Nutrition and Soil Science 165, 573–581.
Image analysis for non-destructive and non-invasive quantification of root growth and soil water content in rhizotrons.CrossRef | 1:CAS:528:DC%2BD38XosFynu70%3D&md5=88b94e6db6941d9829bfb5056f4fb71cCAS |

Laperche A, Devienne-Barret F, Maury O, Le Gouis J, Ney B (2006) A simplified conceptual model of carbon/nitrogen functioning for QTL analysis of winter wheat adaptation to nitrogen deficiency. Theoretical and Applied Genetics 113, 1131–1146.
A simplified conceptual model of carbon/nitrogen functioning for QTL analysis of winter wheat adaptation to nitrogen deficiency.CrossRef | 1:CAS:528:DC%2BD28XhtVSktbfP&md5=928726ab45b2bb16fbff9ed098aebcafCAS |

Lipiec J, Hakansson I, Tarkiewicz S, Kossowski J (1991) Soil physical-properties and growth of spring barley as related to the degree of compactness of two soils. Soil & Tillage Research 19, 307–317.
Soil physical-properties and growth of spring barley as related to the degree of compactness of two soils.CrossRef |

Lynch J (1995) Root architecture and plant productivity. Plant Physiology 109, 7–13.

Lynch JP (2007) Roots of the second green revolution. Australian Journal of Botany 55, 493–512.
Roots of the second green revolution.CrossRef |

Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiology 156, 1041–1049.
Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops.CrossRef | 1:CAS:528:DC%2BC3MXptFWlurY%3D&md5=3766b15aaf04b2c238a7671c289b7b27CAS |

MacMillan K, Emrich K, Piepho H-P, Mullins CE, Price AH (2006) Assessing the importance of genotype × environment interaction for root traits in rice using a mapping population. I: a soil-filled box screen. Theoretical and Applied Genetics 113, 977–986.
Assessing the importance of genotype × environment interaction for root traits in rice using a mapping population. I: a soil-filled box screen.CrossRef | 1:CAS:528:DC%2BD28XhtVSktbbI&md5=e583eebbc0be236d96233ddc0766c06eCAS |

Malik W, Iqbal MZ, Khan AA, Noor E, Qayyum A, Hanif M (2011) Genetic basis of variation for seedling traits in Gossypium hirsutum L. African Journal of Biotechnology 10, 1099–1105.

Manschadi AM, Christopher J, deVoil P, Hammer GL (2006) The role of root architectural traits in adaptation of wheat to water-limited environments. Functional Plant Biology 33, 823–837.
The role of root architectural traits in adaptation of wheat to water-limited environments.CrossRef | 1:CAS:528:DC%2BD28XptVClsbY%3D&md5=fadef527dfee708fa40ff73ebf96cd40CAS |

Masle J (1992) Genetic variation in the effects of root impedance on growth and transpiration rates of wheat and barley. Australian Journal of Plant Physiology 19, 109–125.
Genetic variation in the effects of root impedance on growth and transpiration rates of wheat and barley.CrossRef |

Menzel MI, Oros-Peusquens A-M, Pohlmeier A, Shah NJ, Schurr U, Schneider HU (2007) Comparing 1H-NMR imaging and relaxation mapping of German white asparagus from five different cultivation sites. Journal of Plant Nutrition and Soil Science 170, 24–38.
Comparing 1H-NMR imaging and relaxation mapping of German white asparagus from five different cultivation sites.CrossRef | 1:CAS:528:DC%2BD2sXjtFylu70%3D&md5=e48a3bdfb096fc507b12b328a334b059CAS |

Moradi AB, Carminati A, Vetterlein D, Vontobel P, Lehmann E, Weller U, Hopmanns JW, Vogel HJ, Oswald SE (2011) Three-dimensional visualization and quantification of water content in the rhizosphere. New Phytologist 192, 653–663.
Three-dimensional visualization and quantification of water content in the rhizosphere.CrossRef |

Mühlich M, Truhn D, Nagel K, Walter A, Scharr H, Aach T (2008) Measuring plant root growth. Pattern recognition: 30th DAGM Symposium Munich, Germany. Lecture Notes in Computer Science 5096, 497–506.

Nagel KA, Schurr U, Walter A (2006) Dynamics of root growth stimulation in Nicotiana tabacum in increasing light intensity. Plant, Cell & Environment 29, 1936–1945.
Dynamics of root growth stimulation in Nicotiana tabacum in increasing light intensity.CrossRef | 1:CAS:528:DC%2BD28Xht1aktLjJ&md5=d4f9e95a0060dab2bd2c8fd2dde0271bCAS |

Nagel KA, Kastenholz B, Jahnke S, van Dusschoten D, Aach T, Mühlich M, Truhn D, Scharr H, Terjung S, Walter A, Schurr U (2009) Temperature responses of roots: impact on growth, root system architecture and implications for phenotyping. Functional Plant Biology 36, 947–959.
Temperature responses of roots: impact on growth, root system architecture and implications for phenotyping.CrossRef | 1:CAS:528:DC%2BD1MXhtlOgs7vM&md5=0a4dbd33c504115a00a27c2258c9d699CAS |

Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: developments in root system architecture. Annual Review of Plant Biology 58, 93–113.
Hidden branches: developments in root system architecture.CrossRef | 1:CAS:528:DC%2BD2sXnsVahs7w%3D&md5=9e004f6fe21ce6e95191475914d42d1dCAS |

Passioura JB (2010) Scaling up: the essence of effective agricultural research. Functional Plant Biology 37, 585–591.
Scaling up: the essence of effective agricultural research.CrossRef |

Pierret A, Kirby M, Moran C (2003) Simultaneous x-ray imaging of plant root growth and water uptake in thin-slab systems. Plant and Soil 255, 361–373.
Simultaneous x-ray imaging of plant root growth and water uptake in thin-slab systems.CrossRef | 1:CAS:528:DC%2BD3sXotV2jsrs%3D&md5=7fdbda8cb164f85421229b8cb1a058c1CAS |

Rajendran K, Tester M, Roy SJ (2009) Quantifying the three main components of salinity tolerance in cereals. Plant, Cell & Environment 32, 237–249.
Quantifying the three main components of salinity tolerance in cereals.CrossRef | 1:CAS:528:DC%2BD1MXjsVKlsL4%3D&md5=6c1e55ee61a57066f799c2f0f3be9265CAS |

Richard O, Pineau C, Loubet S, Chalies C, Vile D, Marquès L, Berthomieu P (2011) Diversity analysis of the response to Zn within the Arabidopsis thaliana species revealed a low contribution of Zn translocation to Zn tolerance and a new role for Zn in lateral root development. Plant, Cell & Environment 34, 1065–1078.
Diversity analysis of the response to Zn within the Arabidopsis thaliana species revealed a low contribution of Zn translocation to Zn tolerance and a new role for Zn in lateral root development.CrossRef | 1:CAS:528:DC%2BC3MXpsVKhtLg%3D&md5=53062183e088af4f26bad0aeb0a21b70CAS |

Roy R, Mazumder PB, Sharma GD (2009) Proline, catalase and root traits as indices of drought resistance in bold grained rice (Oryza sativa) genotypes. African Journal of Biotechnology 8, 6521–6528.

Sachs J (1873) Ueber das Wachsthum der Haupt- und Nebenwurzeln. Arbeiten des Botanischen Instituts zu Würzburg 3, 395–477.

Singh V, van Oosteron EJ, Jordan DR, Hunt CH, Hammer GL (2011) Genetic variability and control of nodal root angle in sorghum. Crop Science 51, 2011–2020.
Genetic variability and control of nodal root angle in sorghum.CrossRef |

Taylor HM, Upchurch DR, McMichael BL (1990) Applications and limitations of rhizotrons and minirhizotrons for root studies. Plant and Soil 129, 29–35.
Applications and limitations of rhizotrons and minirhizotrons for root studies.CrossRef |

Thaler P, Pagès L (1995) Root apical diameter and root elongation rate of rubber seedlings (Hevea brasiliensis) show parallel responses to photoassimilate availability. Physiologia Plantarum 91, 365–371.

Trachsel S, Kaeppler SM, Brown KM, Lynch JP (2011) Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field. Plant and Soil 341, 75–87.
Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field.CrossRef | 1:CAS:528:DC%2BC3MXjt1Wjsrc%3D&md5=ed537da3d0db882430dfb58410fbe98eCAS |

Tracy SR, Roberts JA, Black CR, McNeill A, Davidson R, Mooney SJ (2010) The x-factor: visualising undisturbed root architecture in soil using x-ray computed tomography. Journal of Experimental Botany 61, 311–313.
The x-factor: visualising undisturbed root architecture in soil using x-ray computed tomography.CrossRef | 1:CAS:528:DC%2BC3cXktlGmug%3D%3D&md5=97a003e87cee783375ee11a2fcc61bdcCAS |

Tuberosa R, Sanguineti MC, Landi P, Giuliani MM, Salvi S, Conti S (2002) Identification of QTLs for root characteristics in maize grown in hydroponics and analysis of their overlap with QTLs for grain yield in the field at two water regimes. Plant Molecular Biology 48, 697–712.
Identification of QTLs for root characteristics in maize grown in hydroponics and analysis of their overlap with QTLs for grain yield in the field at two water regimes.CrossRef | 1:CAS:528:DC%2BD38XjsFWrt70%3D&md5=a89e061f33b5c26b9871ca9749905252CAS |

van der Weele CM, Spollen WG, Sharp RE, Baskin TI (2000) Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media. Journal of Experimental Botany 51, 1555–1562.
Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media.CrossRef | 1:CAS:528:DC%2BD3cXnt12jurY%3D&md5=492d306e1107835c78071892c1e3058cCAS |

Walter A, Spies H, Terjung S, Küsters R, Kirchgeßner N, Schurr U (2002) Spatio-temporal dynamics of expansion growth in roots: automatic quantification of diurnal course and temperature response by digital image sequence processing. Journal of Experimental Botany 53, 689–698.
Spatio-temporal dynamics of expansion growth in roots: automatic quantification of diurnal course and temperature response by digital image sequence processing.CrossRef | 1:CAS:528:DC%2BD38XitlCks7g%3D&md5=00599b708a3e375b960b18ec510518b3CAS |

Walter A, Scharr H, Gilmer F, Zierer R, Nagel KA, Ernst M, Wiese A, Virnich O, Christ MM, Uhlig B, Jünger S, Schurr U (2007) Dynamics of seedling growth acclimation towards altered light conditions can be quantified via GROWSCREEN: a setup and procedure designed for rapid optical phenotyping of different plant species. New Phytologist 174, 447–455.
Dynamics of seedling growth acclimation towards altered light conditions can be quantified via GROWSCREEN: a setup and procedure designed for rapid optical phenotyping of different plant species.CrossRef |

Watt M, Silk WK, Passioura JB (2006) Rates of root and organism growth, soil conditions, and temporal and spatial development of the rhizosphere. Annals of Botany 97, 839–855.
Rates of root and organism growth, soil conditions, and temporal and spatial development of the rhizosphere.CrossRef |

Watt M, Schneebeli K, Dong P, Wilson IW (2009) The shoot and root growth of Brachypodium and its potential as a model for wheat and other cereal crops. Functional Plant Biology 36, 960–969.
The shoot and root growth of Brachypodium and its potential as a model for wheat and other cereal crops.CrossRef |

Xing Y, Zhang Q (2010) Genetic and molecular bases of rice yield. Annual Review of Plant Biology 61, 421–442.
Genetic and molecular bases of rice yield.CrossRef | 1:CAS:528:DC%2BC3cXnslSjsLY%3D&md5=4fee7feb32b6ed9ffd3a9736accdfc11CAS |

Zhu JM, Lynch JP (2004) The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays) seedlings. Functional Plant Biology 31, 949–958.
The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays) seedlings.CrossRef | 1:CAS:528:DC%2BD2cXosFSqu7k%3D&md5=1374236b30a27cb688cac4166f908af1CAS |



Rent Article (via Deepdyve) Export Citation Cited By (91)

View Altmetrics