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

Temperature responses of roots: impact on growth, root system architecture and implications for phenotyping

Kerstin A. Nagel A D , Bernd Kastenholz A , Siegfried Jahnke A , Dagmar van Dusschoten A , Til Aach B , Matthias Mühlich B , Daniel Truhn B , Hanno Scharr A , Stefan Terjung A C , Achim Walter A and Ulrich Schurr A

A Institute of Chemistry and Dynamics of the Geosphere ICG-3: Phytosphere, Forschungszentrum Jülich GmbH, 52425 Jülich, Germany.

B Lehrstuhl für Bildverarbeitung, RWTH Aachen University, 52056 Aachen, Germany.

C EMBL, EMBL Heidelberg, Meyerhofstr. 1, 69117 Heidelberg, Germany.

D Corresponding author. Email:

Functional Plant Biology 36(11) 947-959
Submitted: 20 July 2009  Accepted: 11 September 2009   Published: 5 November 2009


Root phenotyping is a challenging task, mainly because of the hidden nature of this organ. Only recently, imaging technologies have become available that allow us to elucidate the dynamic establishment of root structure and function in the soil. In root tips, optical analysis of the relative elemental growth rates in root expansion zones of hydroponically-grown plants revealed that it is the maximum intensity of cellular growth processes rather than the length of the root growth zone that control the acclimation to dynamic changes in temperature. Acclimation of entire root systems was studied at high throughput in agar-filled Petri dishes. In the present study, optical analysis of root system architecture showed that low temperature induced smaller branching angles between primary and lateral roots, which caused a reduction in the volume that roots access at lower temperature. Simulation of temperature gradients similar to natural soil conditions led to differential responses in basal and apical parts of the root system, and significantly affected the entire root system. These results were supported by first data on the response of root structure and carbon transport to different root zone temperatures. These data were acquired by combined magnetic resonance imaging (MRI) and positron emission tomography (PET). They indicate acclimation of root structure and geometry to temperature and preferential accumulation of carbon near the root tip at low root zone temperatures. Overall, this study demonstrated the value of combining different phenotyping technologies that analyse processes at different spatial and temporal scales. Only such an integrated approach allows us to connect differences between genotypes obtained in artificial high throughput conditions with specific characteristics relevant for field performance. Thus, novel routes may be opened up for improved plant breeding as well as for mechanistic understanding of root structure and function.

Additional keywords: Brassica napus, magnetic resonance imaging, positron emission tomography, root branching, temperature gradient, Zea mays.


Abbas Al-Ani MK Hay RKM 1983 The influence of growing temperature on the growth and morphology of cereal seedling root system. Journal of Experimental Botany 34 1720 1730 doi:10.1093/jxb/34.12.1720

Abramoff MD Magelhaes PJ Ram SJ 2004 Image processing with ImageJ. Biophotonics International 11 36 42

Ali IA Kafkafi U Yamaguchi I Sugimoto Y Inanaga S 1997 Gibberellin, cytokinins, nitrate content and rate of water transport in the stem in response to root temperature. Soil Science and Plant Nutrition 43 1085 1090

Ali IA Kafkafi U Yamaguchi I Sugimoto Y Inanaga S 1998 Response of oilseed rape plant to low root temperature and nitrate: ammonium ratios. Journal of Plant Nutrition 21 1463 1481

Aloni R Langhans M Aloni E Dreieicher E Ullrich CI 2005 Root-synthesized cytokinin in Arabidopsis is distributed in the shoot by the transpiration stream. Journal of Experimental Botany 56 1535 1544 doi:10.1093/jxb/eri148

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 doi:10.1111/j.1365-313X.2008.03739.x

Arsenault JL Pouleur S Messier C Guay R 1995 WIN-RHIZO, a root-measuring system with a unique overlap correction method. HortScience 30 906

Atkin OK Bruhn D Hurry VM Tjoelker MG 2005 The hot and the cold: unraveling the variable response of plant respiration to temperature. Functional Plant Biology 32 87 105

Beemster GTS Baskin TI 1998 Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiology 116 1515 1526 doi:10.1104/pp.116.4.1515

Beemster GTS Fiorani F Inze D 2003 Cell cycle: the key to plant growth control? Trends in Plant Science 8 154 158 doi:10.1016/S1360-1385(03)00046-3

Bengough AG Gordon DC Al Menaie H Ellis RP Allan D Keith R Thomas WTB Forster BP 2004 Gel observation chamber for rapid screening of root traits in cereal seedlings. Plant and Soil 262 63 70 doi:10.1023/B:PLSO.0000037029.82618.27

Berzin I Cohen B Mills D Dinstein I Merchuk JC 2000 RHIZOSCAN: a semiautomatic image processing system for characterization of the morphology and secondary metabolite concentration in hairy root cultures. Biotechnology and Bioengineering 70 17 24 doi:10.1002/1097-0290(20001005)70:1<17::AID-BIT3>3.0.CO;2-O

Bouma TJ Nielsen KL Koutstaal B 2000 Sample preparation and scanning protocol for computerised analysis of root length and diameter. Plant and Soil 218 185 196 doi:10.1023/A:1014905104017

Box JE Ramsuer EL 1993 Minirhizotron wheat root data: comparisons to soil core root data. Agronomy Journal 85 1058 1060

Ching PC Barber SA 1979 Evaluation of temperature effects on K uptake by corn. Agronomy Journal 71 1040 1044

Cumbus IP Nye PH 1982 Root zone temperature effects on growth and nitrate absorption in rape (Brassica napus cv. Emerald). Journal of Experimental Botany 33 1138 1146

DeLucia EH Heckathorn SA Day TA 1992 Effects of soil temperature on growth, biomass allocation and resource acquisition of Andropogon gerardii Vitman. New Phytologist 120 543 549 doi:10.1111/j.1469-8137.1992.tb01804.x

Dubrovsky JG Gambetta GA Hernandez-Barrera A Shishkova S Gonzalez I 2006 Lateral root initiation in Arabidopsis: developmental window, spatial pattering, density and predictability. Annals of Botany 97 903 915 doi:10.1093/aob/mcj604

Eliasson L Bollmark M 1988 Ethylene as a possible mediator of light-induced inhibition of root growth. Physiologia Plantarum 72 605 609 doi:10.1111/j.1399-3054.1988.tb09170.x

Engels C 1994 Effect of root and shoot meristem temperature on shoot to root dry matter partitioning and the internal concentrations of nitrogen and carbohydrates in maize and wheat. Annals of Botany 72 311 319

Engels CH Marschner H 1990 Effect of suboptimal root zone temperatures at varied nutrient supply an shoot meristem temperature on growth and nutrient concentrations in maize seedlings (Zea mays L.). Plant and Soil 126 215 225

Farrar JF Jones DL 2000 The control of carbon acquisition by roots. New Phytologist 147 43 53 doi:10.1046/j.1469-8137.2000.00688.x

Fiorani F Beemster GTS 2006 Quantitative analyses of cell division in plants. Plant Molecular Biology 60 963 979 doi:10.1007/s11103-005-4065-2

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 doi:10.1093/jxb/eri303

Goodman AM Crook MJ Ennos AR 2001 Anchorage mechanics of the tap root system of winter-sown oilseed rape (Brassica napus L.). Annals of Botany 87 397 404 doi:10.1006/anbo.2000.1347

Gregory PJ 1979 A periscope method for observation root growth and distribution in field soil. Journal of Experimental Botany 30 205 214 doi:10.1093/jxb/30.1.205

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 doi:10.1023/A:1026179919689

Haußecker H , Spies H (1999) Motion. In ‘Handbook on computer vision and applications’. (Eds B Jähne, H Haußecker, P Geißler) pp. 310–369. (Academic Press: New York)

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 doi:10.1023/B:PLSO.0000009694.64377.6f

Hoagland DR Arnon DI 1941 Physiological aspects of availability of nutrients for plant growth. Soil Science 51 431 444 doi:10.1097/00010694-194106000-00002

Hummel GM Schurr U Baldwin IT Walter A 2009 Herbivore-induced jasmonic acid bursts in leaves of Nicotiana attenuata mediate short-term reductions in root growth. Plant, Cell & Environment 32 134 143 doi:10.1111/j.1365-3040.2008.01905.x

Ingestad T 1982 Relative addition rate and external concentration: driving variables used in plant nutrition research. Plant, Cell & Environment 5 443 453

Jacob M Unser M 2004 Design of steerable filters for feature detection using cannylike criteria. Institute of Electrical and Electronics Engineers (IEEE) Transactions on Pattern Analysis and Machine Intelligence (PAMI) 26 1007 1019

Jahnke S Menzel MI van Dusschoten D Roeb GW Bühler J et al 2009 Combined MRI–PET dissects dynamic changes in plant structures and functions. The Plant Journal 59 634 644

Jones JB 1982 Hydroponics: its history and use in plant nutrition studies. Journal of Plant Nutrition 5 1003 1030 doi:10.1080/01904168209363035

Kaspar TC Ewing RP 1997 ROOTEDGE: software for measuring root length from desktop scanner images. Agronomy Journal 89 932 940

Lynch J 1995 Root architecture and plant productivity. Plant Physiology 109 7 13

Macduff JH Wild A 1986 Effects of temperature on parameters of root growth relevant to nutrient uptake: measurements on oilseed and barley grown in flowing nutrient solution. Plant and Soil 94 321 332

McMichael BL Quisenberry JE 1993 The impact of the soil environment on the growth of root systems. Environmental and Experimental Botany 33 53 61 doi:10.1016/0098-8472(93)90055-K

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 doi:10.1002/jpln.200625114

Minchin PEH Thorpe MR Farrar JF Koroleva OA 2002 Source–sink coupling in young barley plants and control of phloem loading. Journal of Experimental Botany 53 1671 1676 doi:10.1093/jxb/erf003

Mühlich M , Truhn D , Nagel KA , Walter A , Scharr H , Aach T (2008) Measuring plant root growth. In ‘Lecture notes in computer science 5096’. (Ed. G Rigoll) pp. 497–506. (Springer-Verlag: Heidelberg, Germany)

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 doi:10.1111/j.1365-3040.2006.01569.x

Pahlavanian AM Silk WK 1988 Effect of temperature on spatial and temporal aspects of growth in the primary maize root. Plant Physiology 87 529 532 doi:10.1104/pp.87.2.529

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 doi:10.1023/A:1026130532683

Samson BK Sinclair TR 1994 Soil core and minirhizotron comparison for the determination of root length density. Plant and Soil 161 225 232 doi:10.1007/BF00046393

Scharr H (2004) ‘Optimal filters for extended optical flow. International workshop on complex motion.’ (Springer-Verlag: Heidelberg, Germany)

Scheffer F , Schachtschabel P , Blume H-P , Brümmer G , Hartge K-H , Schwertmann U (2002) ‘Lehrbuch der Bodenkunde.’ (Spektrum Akademischer Verlag GmbH: Heidelberg, Germany)

Schmundt D Stitt M Jähne B Schurr U 1998 Quantitative analysis of the local rates of growth of dicot leaves at a high temporal and spatial resolution, using image sequence analysis. The Plant Journal 16 505 514 doi:10.1046/j.1365-313x.1998.00314.x

Seiler GJ 1998 Influence of temperature on primary and lateral root growth of sunflower seedlings. Environmental and Experimental Botany 40 135 146 doi:10.1016/S0098-8472(98)00027-6

Solfjeld I Johnsen O 2006 The influence of root-zone temperature on growth of Betula pendula. Trees (Berlin) 20 320 328 doi:10.1007/s00468-005-0043-1

Sowinski P Richner W Soldati A Stamp P 1998 Assimilate transport in maize (Zea mays L.) seedlings at vertical low temperature gradients in the root zone. Journal of Experimental Botany 49 747 752 doi:10.1093/jexbot/49.321.747

Stone JA Taylor HM 1983 Temperature and the development of the taproot and lateral roots of four indeterminate soybean cultivars. Agronomy Journal 75 613 618

Streun M Brandenburg G Larue H Parl C Ziemons K 2006 The data acquisition system of ClearPET neuro – a small animal PET scanner. IEEE Transactions on Nuclear Science 53 700 703

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

Thorup-Kristensen K 1993 Root development of nitrogen catch crops and of a succeeding crop of broccoli. Acta Agriculturae Scandinavica Section B-Soil and Plant Science 43 58 64

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 doi:10.1023/A:1014897607670

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 doi:10.1093/jexbot/53.369.689

Walter A Feil R Schurr U 2003 Expansion dynamics, metabolite composition and substance transfer of the primary root growth zone of Zea mays L. grown in different external nutrient availabilities. Plant, Cell & Environment 26 1451 1466 doi:10.1046/j.0016-8025.2003.01068.x

Walter A Silk WK Schurr U 2009 Environmental effects on spatial and temporal patterns of leaf and root growth. Annual Review of Plant Biology 60 279 304 doi:10.1146/annurev.arplant.59.032607.092819

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 doi:10.1093/aob/mcl028

Weber S Morel C Simon L Krieguer M Rey M Gundlich B Khodaverdi M 2006 Image reconstruction for the ClearPET_Neuro. Nuclear Instruments and Methods in Physics. Research Section A 569 381 385 doi:10.1016/j.nima.2006.08.048

Williams SM Weil RR 2004 Crop cover root channels may alleviate soil compaction effects on soybean crop. Soil Science Society of America Journal 68 1403 1409

Ye Z Huang L Bell RW Dell B 2003 Low root zone temperature favours shoot B partitioning into young leaves of oilseed rape (Brassica napus). Physiologia Plantarum 118 213 220

Ye Z Bell RW Dell B Huang L Qiufang X 2006 Effect of root zone temperature on oilseed rape (Brassica napus) response to boron. Communications in Soil Science and Plant Analysis 37 2791 2803 doi:10.1080/00103620600832514

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