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

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
+ Author Affiliations
- Author Affiliations

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: k.nagel@fz-juelich.de

Functional Plant Biology 36(11) 947-959 https://doi.org/10.1071/FP09184
Submitted: 20 July 2009  Accepted: 11 September 2009   Published: 5 November 2009

Abstract

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.


Acknowledgements

We are indebted to Arnd Kuhn for providing the temperature boxes and to Wilhelm Genzer for building the PVC-inserts for the sand-filled temperature box. We thank Richard Poiré for his help with thermocouples and Georg Dreissen for his assistance during image acquisition.


References


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.
CrossRef |

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.
CAS |


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.
CrossRef | CAS |

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.
CrossRef | CAS | PubMed |

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.
CrossRef | CAS | PubMed |

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.
CrossRef |

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.
CrossRef | CAS | PubMed |

Beemster GTS, Fiorani F, Inze D (2003) Cell cycle: the key to plant growth control? Trends in Plant Science 8, 154–158.
CrossRef | CAS | PubMed |

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.
CrossRef | CAS |

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.
CrossRef | CAS | PubMed |

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.
CrossRef | CAS |

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.
CAS |


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.
CrossRef | CAS |

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.
CrossRef |

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.
CrossRef | CAS | PubMed |

Eliasson L, Bollmark M (1988) Ethylene as a possible mediator of light-induced inhibition of root growth. Physiologia Plantarum 72, 605–609.
CrossRef | CAS |

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.
CrossRef | CAS |

Farrar JF, Jones DL (2000) The control of carbon acquisition by roots. New Phytologist 147, 43–53.
CrossRef | CAS |

Fiorani F, Beemster GTS (2006) Quantitative analyses of cell division in plants. Plant Molecular Biology 60, 963–979.
CrossRef | CAS | PubMed |

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.
CrossRef | CAS | PubMed |

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.
CrossRef |

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

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.
CrossRef | CAS |

Hoagland DR, Arnon DI (1941) Physiological aspects of availability of nutrients for plant growth. Soil Science 51, 431–444.
CrossRef | CAS |

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.
CrossRef | CAS | PubMed |

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


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.
CrossRef |


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.
CrossRef | CAS | PubMed |

Jones JB (1982) Hydroponics: its history and use in plant nutrition studies. Journal of Plant Nutrition 5, 1003–1030.
CrossRef | CAS |

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.
CAS | PubMed |


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.
CrossRef |

McMichael BL, Quisenberry JE (1993) The impact of the soil environment on the growth of root systems. Environmental and Experimental Botany 33, 53–61.
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.
CrossRef | CAS |

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.
CrossRef | CAS | PubMed |

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.
CrossRef | CAS | PubMed |

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.
CrossRef | PubMed |

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.
CrossRef | CAS |

Samson BK, Sinclair TR (1994) Soil core and minirhizotron comparison for the determination of root length density. Plant and Soil 161, 225–232.
CrossRef |

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.
CrossRef |

Seiler GJ (1998) Influence of temperature on primary and lateral root growth of sunflower seedlings. Environmental and Experimental Botany 40, 135–146.
CrossRef |

Solfjeld I, Johnsen O (2006) The influence of root-zone temperature on growth of Betula pendula. Trees (Berlin) 20, 320–328.
CrossRef |

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.
CrossRef | CAS |

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.
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.

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.
CrossRef | CAS |

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.
CrossRef | CAS | PubMed |

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.
CrossRef | CAS | PubMed |

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.
CrossRef | CAS |

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.
CrossRef | CAS | PubMed |

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.
CrossRef | PubMed |

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.
CrossRef | CAS |

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.
CAS |


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.
CrossRef | CAS |

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.
CrossRef | CAS |








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