REVIEW PAPER
Field phenotyping of plant roots by electrical capacitance – a standardized methodological protocol for application in plant breeding: a Review
| 1 | Department of Crop Science, Breeding and Plant Medicine, Mendel University in Brno, Czech Republic |
| 2 | Division of Crop Management Systems, Crop Research Institute, Czech Republic |
| 3 | Institute of Plant Production, University of Agriculture in Kraków, Poland |
| 4 | Department of Applied and Landscape Ecology, Mendel University in Brno, Czech Republic |
| 5 | Division of Agronomy, University of Natural Resources and Life Sciences, Austria |
CORRESPONDING AUTHOR
Tomáš Středa
Department of Crop Science, Breeding and Plant Medicine, Mendel University in Brno, Czech Republic
Department of Crop Science, Breeding and Plant Medicine, Mendel University in Brno, Czech Republic
Final revision date: 2020-01-16
Acceptance date: 2020-01-29
Publication date: 2020-03-09
Int. Agrophys. 2020, 34(2): 173–184
KEYWORDS
TOPICS
ABSTRACT
Due to the absence of a suitable method and standardized procedures, the root systems of plants have been evaluated to a much lesser extent than aboveground organs. The aim of this article is (i) to provide a detailed description and thus standardization of an upgraded procedure of electrical capacitance measurement for evaluating the root system size of plants in situ, which allows re-assessment during the growing season and subsequent harvest of seeds for the planting of selected progenies, (ii) to demonstrate, through a standardized methodological protocol, the applicability of root electrical capacitance measurement as a field phenotyping method for the selection of superior root systems to improve crop abiotic stress tolerance and resource efficiency, (iii) to suggest a standardized methodological protocol for the application of electrical capacitance measurements in breeding nurseries, and (iv) to discuss methodological aspects, development and limitations of this method. A methodological overview of the use of electrical capacitance to measure plant root systems, emerging from working groups directed by the author of this unique method, is given along with a standardized protocol. An overview of the application of electrical capacitance measurements of roots in breeding is shown along with some examples of successful applications.
REFERENCES (92)
1.
Aulen M. and Shipley B., 2012. Non-destructive estimation of root mass using electrical capacitance on ten herbaceous species. Plant Soil, 355, 41-49, https://doi.org/10.1007/s11104....
2.
Aziz M.M., Palta J.A., Siddique K.H.M., and Sadras V.O., 2017. Five decades of selection for yield reduced root length density and increased nitrogen uptake per unit root length in Australian wheat varieties. Plant Soil, 413, 181-192, https://doi.org/10.1007/s11104....
3.
Bänziger M., Edmeades G.O., Beck D., and Bellon M., 2000. Breeding for drought and nitrogen stress tolerance in maize: From theory to Practice. CIMMYT, Mexico.
4.
Bertholdsson N.-O. and Kolodinska Brantestam A., 2009. A century of Nordic barley breeding – Effects on early vigour root and shoot growth, straw length, harvest index and grain weight. Europ. J. Agronomy, 30, 266-274, https://doi.org/10.1016/j.eja.....
5.
Blum A., 2005. Drought resistance, water-use efficiency, and yield potential – are they compatible, dissonant, or mutually exclusive? Australian J. Agric. Res., 56, 1159-1168, https://doi.org/10.1071/AR0506....
6.
Blum A. and Naveh M., 1976. Improved water-use efficiency by promoted plant competition in dryland sorghum. Agron. J., 68, 111-116.
7.
Böhm W., 1979. Methods of Studying Root Systems. Springer-Verlag, Berlin, Germany, Heidelberg, New York, USA.
8.
Brown A.L.P., Day F.P., and Stover D.B., 2009. Fine root biomass estimates from minirhizotron imagery in a shrub ecosystem exposed to elevated CO2. Plant Soil, 317, 145-153, https://doi.org/10.1007/s11104....
9.
Campos H., Cooper M., Habben J.E., Edmeades G.O., and Schussler J.R., 2004. Improving drought tolerance in maize: a view from industry. Field Crops Res., 90, 19-34, https://doi.org/10.1016/j.fcr.....
10.
Cao Y., Repo T., Silvennoinen R., Lehto T., and Pelkonen P., 2010. An appraisal of the electrical resistance method for assessing root surface area. J. Exp. Bot., 61, 2491-2497, doi:10.1093/jxb/erq078.
11.
Carlson C.H. and Smart L.B., 2016. Electrical capacitance as a predictor of root dry weight in shrub willow (Salix; Salicaceae) parents and progeny. Appl. Plant Sci., 4, apps.1600031, https://doi.org/10.3732/apps.1....
12.
Chloupek O., 1977. Evaluation of the size of a plants root system using its electrical capacitance. Plant Soil, 48, 525-532, https://doi.org/10.1007/BF0218....
13.
Chloupek O., 1972. The relationship between electric capacitance and some other parameters of plant roots. Biol. Plantarum, 14, 227-230, https://doi.org/10.1007/BF0292....
14.
Chloupek O., Dostál V., Středa T., Psota V., and Dvořáčková O., 2010. Drought tolerance of barley varieties in relation to their root system size. Plant Breed., 129, 630-636, https://doi.org/10.1111/j.1439....
15.
Comas L.H., Becker S.R., Cruz V.M., Byrne P.F., and Dierig D.A., 2013. Root traits contributing to plant productivity under drought. Front. Plant Sci., 4, 442, https://doi.org/3389/fpls.2013....
16.
Cseresnyés I., Kabos S., Takács T., Végh K.R., Vozáry E., and Rajkai K., 2017. An improved formula for evaluating electrical capacitance using the dissipation factor. Plant Soil, 419, 237-256, https://doi.org/10.1007/s11104....
17.
Cseresnyés I., Rajkai K., and Takács T., 2016. Indirect monitoring of root activity in soybean cultivars under contrasting moisture regimes by measuring electrical capacitance. Acta Physiol. Plant., 38, 121, https://doi.org/10.1007/s11738....
18.
Cseresnyés I., Rajkai K., and Vozáry E., 2013a. Role of phase angle measurement in electrical impedance spectroscopy. Int. Agrophys., 27, 377-382, https://doi.org/10.2478/intag-....
19.
Cseresnyés I., Takács T., Végh K.R., Anton A., and Rajkai K., 2013b. Electrical impedance and capacitance method: A new approach for detection of functional aspects of arbuscular mycorrhizal colonization in maize. Eur. J. Soil Biol., 54, 25-31, https://doi.org/10.1016/j.ejso....
20.
Cseresnyés I., Szitár K., Rajkai K., Füzy A., Mikó P., Kovács R., and Takács T., 2018. Application of electrical capacitance method for prediction of plant root mass and activity in field-grown crops. Front. Plant Sci., 9, 93, https://doi.org/10.3389/fpls.2....
21.
Cseresnyés I., Takács T., Füzy A., and Rajkai K., 2014. Simultaneous monitoring of electrical capacitance and water uptake activity of plant root system. Int. Agrophys., 28, 537-541, https://doi.org/10.2478/intag-....
22.
Cseresnyés I., Takács T., Füzy A., Végh K.R., and Lehoczky E., 2016. Application of electrical capacitance measurement for in situ monitoring of competitive interactions between maize and weed plants. Spanish J. Agric. Res., 14, p. e0904, http://dx.doi.org/10.5424/sjar....
23.
Cseresnyés I., Takács T., Sepovics B., Kovács R., Füzy A., Parádi I., and Rajkai K., 2019. Electrical characterization of the root system: a noninvasive approach to study plant stress responses. Acta Physiol. Plant., 41, 169, https://doi.org/10.1007/s11738....
24.
Čermák J., Ulrich R., Stanek Z., Koller J., and Aubrecht L., 2006. Electrical measurement of tree root absorbing surfaces by the earth impedance method: 2. Verification based on allometric relationships and root severing experiments. Tree Physiol., 26, 1113-1121, https://doi.org/10.1093/treeph....
25.
Dalton F.N., 1995. In-situ root extent measurements by electrical capacitance methods. Plant Soil, 173, 157-165, https://doi.org/10.1007/BF0015....
26.
Dietrich R.C., Bengough A.G., Jones H.G., and White P.J., 2012. A new physical interpretation of plant root capacitance. J. Exp. Bot., 63, 6149-6159, https://doi.org/10.1093/jxb/er....
27.
Dietrich R.C., Bengough A.G., Jones H.G., and White P.J., 2013. Can root electrical capacitance be used to predict root mass in soil? Ann. Bot., 112, 457-464, https://doi.org/10.1093/aob/mc....
28.
Ebrahimi E., Bodner G., Kaul H.-P., and Nassab A.D.M., 2014. Tetraploid wheat root traits are affected by soil water availability. Book of Abstracts XIIIth Congr. European Society for Agronomy (ESA), August 25-29, Debrecen, Hungary, 433-434.
29.
Ehdaie B., Merhaut D.J., Ahmadian S., Hoops A.C., Khuong T., Layne A.P., and Waines J.G., 2010. Root system size influences water-nutrient uptake and nitrate leaching potential in wheat. J. Agron. Crop Sci., 196, 455-466, https://doi.org/10.1111/j.1439....
30.
Ellis T.W., Murray W., Paul K., Kavalieris L., Brophy J., Williams Ch., and Maass M., 2013a. Electrical capacitance as a rapid and non-invasive indicator of root length. Tree Physiol., 33, 3-17, https://doi.org/10.1093/treeph....
31.
Ellis T., Murray W., and Kavalieris L., 2013b. Electrical capacitance of bean (Vicia faba) root systems was related to tissue density – a test for the Dalton Model. Plant Soil, 366, 575-584, https://doi.org/10.1007/s11104....
32.
Feng G., Zhang Y., Chen Y., Li Q., Chen F., Gao Q., and Mi G., 2016. Effects of nitrogen application on root length and grain yield of rain-fed maize under different soil types. Agron. J., 108, 1656-1665, https://doi.org/10.2134/agronj....
33.
Fitter A., 2002. Characteristics and functions of root systems. In: Plant roots: The hidden half. Marcel Dekker Inc., New York, USA, 15-32.
34.
Gewin V., 2010. Food: An underground revolution. Nature, 466, 552-553, https://doi.org/10.1038/466552....
35.
Gonzalez-Dugo V., Durand J.-L., and Gastal F., 2010. Water deficit and nitrogen nutrition of crops. A review. Agron. Sustain. Dev., 30, 529-544, https://doi.org/10.1051/agro/2....
36.
Gregory P., McGowan M., and Biscoe P., 1978. Water relations of winter wheat. 2. Soil water relations. J. Agric. Sci., 91, 103-116, https://doi.org/10.1017/S00218....
37.
Herrera J.M., Feil B., Stamp P., and Liedgens M., 2010. Root growth and nitrate-nitrogen leaching of catch crops following spring wheat. J. Environ. Quality, 39, 845-854, https://doi.org/10.2134/jeq200....
38.
Heřmanská A., Středa T., and Chloupek O., 2015. Improved wheat grain yield by a new method of root selection. Agron. Sustain. Dev., 35, 195-202, https://doi.org/10.1007/s13593....
39.
Kendall W.A., Pederson G.A., and Hill R.R., 1982. Root size estimates of red clover and alfalfa based on electrical capacitance and root diameter measurements. Grass Forage Sci., 37, 253-256, https://doi.org/10.1111/j.1365....
40.
King J., Gay A., Sylvester-Bradley R., Bingham I., Foulkes J., Gregory P., and Robinson D., 2003. Modelling cereal root systems for water and nitrogen capture: towards an economic optimum. Ann. Bot., 91, 383-390, https://doi.org/10.1093/aob/mc....
41.
Kirkegaard J.A., Lilley J.M., Howe G.N., and Graham J.M., 2007. Impact of subsoil water use on wheat yield. Australian J. Agric. Res., 58, 303-315, https://doi.org/10.1071/AR0628....
42.
Klimek-Kopyra A. and Rębilas K., 2018. Dependence of pea root mass distribution on weather conditions under varying levels of phosphorus application. Int. Agrophys., 32, 365-372, https://doi.org/10.1515/intag-....
43.
Kormanek M., Głąb T., and Klimek-Kopyra A., 2016. Modification of the tree root electrical capacitance method under laboratory conditions. Tree Physiol., 36, 121-127, https://doi.org/10.1093/treeph....
44.
Lynch J.P., 2013. Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann. Bot., 112, 347-357, https://doi.org/10.1093/aob/mc....
45.
Manschadi A.M., Christopher J., deVoil P., and Hammer G.L., 2006. The role of root architectural traits in adaptation of wheat to water-limited environments. Funct. Plant Biol., 33, 823-837, https://doi.org/10.1071/FP0605....
46.
Manske G.G.B. and Vlek P.L.G., 2002. Root Architecture – Wheat as a model plant. In: Plant roots: The hidden half. Marcel Dekker Inc., New York, USA, 249-260.
47.
Martyniak L., 2008. Response of spring cereals to a deficit of atmospheric precipitation in the particular stages of plant growth and development. Agric. Water Manag., 95, 171-178, https://doi.org/10.1016/j.agwa....
48.
McBride R., Candido M., and Ferguson J., 2008. Estimating root mass in maize genotypes using the electrical capacitance method. Arch. Agron. Soil Sci., 54, 215-226, https://doi.org/10.1080/036503....
49.
Meier U., 1997. BBCH-Monograph. Growth stages of plants – Entwicklungsstadien von Pflanzen – Estadios de las plantas – Développement des Plantes. Blackwell Wissenschaftsverlag, Berlin, Wien, Germany, Austria.
50.
Messmer R., Fracheboud Y., Bänziger M., Stamp P., and Ribaut J.-M., 2011. Drought stress and tropical maize: QTLs for leaf greenness, plant senescence, and root capacitance. Field Crops Res., 124, 93-103, https://doi.org/10.1016/j.fcr.....
51.
Monneveux P., Quillérou E., Sanchez C., and Lopez-Cesati J., 2006. Effect of zero tillage and residues conservation on continuous maize cropping in a subtropical environment (Mexico). Plant Soil, 279, 95-105, https://doi.org/10.1007/s11104....
52.
Montal M. and Mueller P., 1972. Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. Proc. National Academy of Sciences of the United States of America, 69, 3561-3566, https://doi.org/10.1073/pnas.6....
53.
Nakhforoosh A., Grausgruber H., Kaul H.P., and Bodner G., 2014. Wheat root diversity and root functional characterization. Plant Soil, 380, 211-229, https://doi.org/10.1007/s11104....
54.
Ozier-Lafontaine H. and Bajazet T., 2005. Analysis of root growth by impedance spectroscopy (EIS). Plant Soil, 277, 299-313, https://doi.org/10.1007/s11104....
55.
Palta J. and Watt M., 2009. Vigorous crop root systems: Form and function for improving the capture of water and nutrients. In: Crop Physiology, Applications for Genetic Improvement and Agronomy. Academic Press, Burlington, Ontario, Canada.
56.
Palta J.A., Chen X., Milroy S.P., Rebetzke G.J., Dreccer M.F., and Watt M., 2011. Large root systems: are they useful in adapting wheat to dry environments? Funct. Plant Biol., 38, 347-354, https://doi.org/10.1071/FP1103....
57.
Passioura J.B., 1980. The transport of water from soil to shoot in wheat seedlings. J. Exp. Bot., 31, 333-345, https://doi.org/10.1093/jxb/31....
58.
Paynter B.H. and Young K.J., 2004. Grain and malting quality in two-row spring barley are influenced by grain filling moisture. Australian J. Agric. Res., 55, 539-550, https://doi.org/10.1071/AR0209....
59.
Peltonen-Sainio P., Jauhiainen L., and Hakala, K., 2011. Crop responses to temperature and precipitation according to long-term multi-location trials at high-latitude conditions. J. Agric. Sci., 149, 49-62, https://doi.org/10.1017/S00218....
60.
Pitre F.E., Brereton N.J.B., Audoire S., Richter G.M., Shield I., and Karp A., 2010. Estimating root biomass in Salix viminalis x Salix schwerinii cultivar “Olof” using the electrical capacitance method. Plant Biosyst., 144, 479-483, https://doi.org/10.1080/112635....
61.
Postic F. and Doussan C., 2016. Benchmarking electrical methods for rapid estimation of root biomass. Plant Methods, 12, 33, https://doi.org/10.1186/s13007....
62.
Preston G.M., McBride R.A., Bryan J., and Candido M., 2004. Estimating root mass in young hybrid poplar trees using the electrical capacitance method. Agroforest. Syst., 60, 305-309, https://doi.org/10.1023/B:AGFO....
63.
Psarras G. and Merwin I.A., 2000. Water stress affects rhizosphere respiration rates and root morphology of young „Mutsu“ apple trees on M.9 and MM.111 rootstocks. J. Amer. Soc. Hort.. Sci., 125, 588-595, https://doi.org/10.21273/JASHS....
64.
Rajkai K., Végh K.R., and Nacsa T., 2005. Electrical capacitance of roots in relation to plant electrodes, measuring frequency and root media. Acta Agronomica Hungarica, 53, 197-210, https://doi.org/10.1556/AAgr.5....
65.
Repo T., Korhonen A., Lehto T., and Silvennoinen R., 2016. Assessment of frost damage in mycorrhizal and non-mycorrhizal roots of Scots pine seedlings using classification analysis of their electrical impedance spectra. Trees, 30, 483-495, https://doi.org/10.1007/s00468....
66.
Repo T., Laukkanen J., and Silvennoinen R., 2005. Measurement of the tree root growth using electrical impedance spectroscopy. Silva Fennica, 39, 159-166, https://doi.org/10.14214/sf.38....
67.
Richards R.A., 1991. Crop improvement for temperate Australia: Future opportunities. Field Crops Res., 26, 141-169, https://doi.org/10.1016/0378-4....
68.
Richards R.A. and Passioura J.B., 1989. A breeding program to reduce the diameter of the major xylem vessel in the seminal roots of wheat and its effect on grain yield in rain-fed environments. Australian J. Agric. Res., 40, 943-950, https://doi.org/10.1071/AR9890....
69.
Richards R.A., Rebetzke G.J., Watt M., Condon A.G., Spielmeyer W., and Dolferus R., 2010. Breeding for improved water productivity in temperate cereals: phenotyping, quantitative trait loci, markers and the selection environment. Funct. Plant Biol., 37, 85-97, https://doi.org/10.1071/FP0921....
70.
Robinson H., Kelly A., Fox G., Franckowiak J., Borrell A., and Hickey L., 2018. Root architectural traits and yield: exploring the relationship in barley breeding trials. Euphytica, 214, 151, https://doi.org/10.1007/s10681....
71.
Sabo D., McMurray G., and Rains G., 2016. Presymptomatic disease detection and nanoparticle-enhanced electrical capacitance tomography. IFAC-PapersOnLine, 49, 116-120, https://doi.org/10.1016/j.ifac....
72.
Sharma S. and Carena M.J., 2016. BRACE: A Method for high throughput maize phenotyping of root traits for short-season drought tolerance. Crop Science, 56, 2996-3004, https://doi.org/10.2135/cropsc....
73.
Smit A.L., Bengough A.G., Engels C., Noordwijk M., Pellerin S., and Geijn S.C., 2000. Root Methods. A Handbook. Springer-Verlag, Berlin Heidelberg, Germany, https://doi.org/10.1007/978-3-....
74.
Středa T., Dostál V., Horáková V., and Chloupek O., 2012. Effective use of water by wheat varieties with different root system sizes in rain-fed experiments in Central Europe. Agric. Water Manag., 104, 203-209, https://doi.org/10.1016/j.agwa....
75.
Středa T. and Chloupek O., 2013. Kit for measuring size of root system. Patent Number: CZ201100530-A3. Derwent Primary Accession Number: 2013-D47711.
76.
Svačina P., Středa T., and Chloupek O., 2014. Uncommon selection by root system size increases barley yield. Agron. Sustain. Dev., 34, 545-551, https://doi.org/10.1007/s13593....
77.
Školníková M. and Škarpa P., 2016. The influence of deficient nutrition on growth and root activity of maize (Zea mays L.) under hydroponic conditions. In: MendelNet 2016: Proc. Int. Ph.D. Students Conference. Mendel University in Brno, Czech Republic, 140-145.
78.
Šmardová M., Klimešová J., and Středa T., 2018. Improved root system for better wheat drought tolerance. In: MendelNet 2018: Proc. Int. Ph.D. Students Conf., Mendel University in Brno, Czech Republic, 90-94.
79.
Takács T., Füzy A., Rajkai K., and Cseresnyés I., 2014. Investigation of arbuscular mycorrhizal status and functionality by electrical impedance and capacitance measurement: New method for description of AMF functionality. Acta Biologica Szegediensis, 58, 55-59.
80.
Tron S., Bodner G., Laio F., Ridolfi L., and Leitner D., 2015. Can diversity in root architecture explain plant water use efficiency? A modeling study. Ecol. Model., 312, 200-210, https://doi.org/10.1016/j.ecol....
81.
Tsukahara K., Yamane K., Yamaki Y., and Honjo H., 2009. A nondestructive method for estimating the root mass of young peach trees after root pruning using electrical capacitance measurements. J. Agric. Meteorology, 65, 209-213, https://doi.org/10.2480/agrmet....
82.
Vamerali T., Bandiera M., Coletto L., Zanetti F., Dickinson N.M., and Mosca G., 2009. Phytoremediation trials on metal- and arsenic-contaminated pyrite wastes (Torviscosa, Italy). Environ. Pollution, 157, 887-894, https://doi.org/10.1016/j.envp....
83.
Vamerali T., Saccomani M., Bona S., Mosca G., Guarise M., and Ganis A., 2003. A comparison of root characteristics in relation to nutrient and water stress in two maize hybrids. Plant Soil, 255, 157-176, https://doi.org/10.1023/A:1026....
84.
van Beem J., Smith M.E., and Zobel R.W., 1998. Estimating root mass in maize using a portable capacitance meter. Agron. J., 90, 566-570, https://doi.org/10.2134/agronj....
85.
Vintrlíková E., Klimešová J., and Středa T., 2015. Possibility of selection for higher seed vigour of barley. In MendelNet 2015: Proc. Int. Ph.D. Students Conf., November 11, Mendel University in Brno, Czech Republic, 99-102.
86.
Waines J.G. and Ehdaie B., 2007. Domestication and crop physiology: roots of green-revolution wheat. Ann. Bot., 100, 991-998, https://doi.org/10.1093/aob/mc....
87.
Waisel Y., Eshel A., Beeckman T., and Kafkafi U., 1991. Plant roots: the hidden half. Marcel Dekker Inc., New-York, USA.
88.
Wang Ch., Liu W., Li Q., Ma D., Lu H., Feng W., Xie Y., Zhu Y., and Guo T., 2014. Effects of different irrigation and nitrogen regimes on root growth and its correlation with above-ground plant parts in high-yielding wheat under field conditions. Field Crops Res., 16, 138-149, https://doi.org/10.1016/j.fcr.....
89.
Wendling M., Büchi L., Amossé C., Sinaj S., Walter A., and Charles R., 2016. Influence of root and leaf traits on the uptake of nutrients in cover crops. Plant Soil, 409, 419-434, https://doi.org/10.1007/s11104....
90.
Worku M., Bänziger M., Schulte Auf’m Erley G., Friesen D., Diallo A.O., and Horst W.J., 2012. Nitrogen efficiency as related to dry matter partitioning and root system size in tropical mid-altitude maize hybrids under different levels of nitrogen stress. Field Crops Res., 130, 57-67, https://doi.org/10.1016/j.fcr.....
91.
Wu W., Duncan R.W., and Ma B., 2017. Quantification of canola root morphological traits under heat and drought stresses with electrical measurements. Plant Soil, 415, 229-244, https://doi.org/10.1007/s11104....
92.
Wu W. and Ma B.-L., 2016. A new method for assessing plant lodging and the impact of management options on lodging in canola crop production. Sci. Rep., 6, 31890, https://doi.org/10.1038/srep31....
Related articles
