Abstract
Aims
Maize (Zea mays L.) is one of the most important crops worldwide. Despite several studies on maize roots, there is limited information on the function of different root types in extracting water from soils. Aim of this study was to investigate the location of water uptake in maize roots.
Methods
We used neutron radiography to image the spatial distribution of maize roots in soil and trace the transport of deuterated water (D2O) in soil and roots. Maize plants were grown in aluminum containers filled with a sandy soil that was kept homogeneously wet throughout the experiment. When the plants were 16 days old, we injected D2O into selected soil regions. The transport of D2O was simulated using a diffusion–convection numerical model. By fitting the observed D2O transport we quantified the diffusion coefficient and the water uptake of the different root segments.
Results
The root architecture of a 16 day-old maize consisted of a primary root, 4–5 seminal roots and many lateral roots. Laterals emerged from the proximal 15 cm of the primary and seminal roots. During both day and night measurements, D2O entered more quickly into lateral roots than into primary and seminal roots. The quick transport of D2O into laterals was caused by the small radius of lateral roots. The diffusion coefficient of lateral roots (4.68 × 10−7 cm2 s−1) was similar to that of the distal unbranched segments of seminal roots (4.72 × 10−7 cm2 s−1) and higher than that of the proximal branched segments (1.42 × 10−7 cm2 s−1). Water uptake of lateral roots (1.64 × 10−5 cm s−1) was much higher than the uptake of seminal roots, which was 5.34 × 10−10 cm s−1 in the proximal branched segments and only 1.18 × 10−12 cm s−1 in the distal unbranched segments.
Conclusions
We conclude that the function of lateral roots is to absorb water from the soil, while the function of the primary and seminal roots is to axially transport water to the shoot.
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References
Ahmed MA, Kroener E, Holz M et al (2014) Mucilage exudation facilitates root water uptake in dry soils. Funct Plant Biol 41:1129–1137
Aubin GS, Canny MJ, McCully ME (1986) Living vessel elements in the late metaxylem of sheathed maize roots. Ann Bot 58:577–588. doi:10.1093/annbot/58.4.577
Bramley H, Turner NC, Turner DW, Tyerman SD (2009) Roles of morphology, anatomy, and aquaporins in determining contrasting hydraulic behavior of roots. Plant Physiol 150:348–364. doi:10.1104/pp. 108.134098
Brodersen CR (2013) Visualizing water transport in roots: advanced imaging tools for an expanding field. Plant Soil 366:29–32. doi:10.1007/s11104-013-1657-5
Brouwer R (1953) Water absorption by the roots of vicia faba at various transpiration strength: analysis of the uptake and the factors determining it. I.
Carminati A (2012) A model of root water uptake coupled with rhizosphere dynamics. Vadose Zone J 11. doi: 10.2136/vzj2011.0106
Carminati A, Moradi AB, Vetterlein D et al (2010) Dynamics of soil water content in the rhizosphere. Plant Soil 332:163–176. doi:10.1007/s11104-010-0283-8
Carminati A, Schneider CL, Moradi AB et al (2011) How the rhizosphere May favor water availability to roots. Vadose Zone J 10:988. doi:10.2136/vzj2010.0113
Clarkson DT, Carvajal M, Henzler T et al (2000) Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. J Exp Bot 51:61–70. doi:10.1093/jexbot/51.342.61
Da Ines O, Graf W, Franck KI et al (2010) Kinetic analyses of plant water relocation using deuterium as tracer – reduced water flux of Arabidopsis pip2 aquaporin knockout mutants. Plant Biol 12:129–139. doi:10.1111/j.1438-8677.2010.00385.x
Doussan C, Pagès L, Vercambre G (1998) Modelling of the hydraulic architecture of root systems: an integrated approach to water absorption—model description. Ann Bot 81:213–223. doi:10.1006/anbo.1997.0540
Doussan C, Pierret A, Garrigues E, Pagès L (2006) Water uptake by plant roots: II – modelling of water transfer in the soil root-system with explicit account of flow within the root system – comparison with experiments. Plant Soil 283:99–117. doi:10.1007/s11104-004-7904-z
Frensch J, Steudle E (1989) Axial and radial hydraulic resistance to roots of maize (Zea mays L.). Plant Physiol 91:719–726
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 Soil 283:83–98. doi:10.1007/s11104-004-7903-0
Hochholdinger F (2009) Handbook of Maize: Its Biology. In: Bennetzen JL, Hake SC (eds) The Maize Root System: Morphology, Anatomy, and Genetics. Springer, New York, pp 145–160
Hochholdinger F, Park WJ, Sauer M, Woll K (2004a) From weeds to crops: genetic analysis of root development in cereals. Trends Plant Sci 9:42–48. doi:10.1016/j.tplants.2003.11.003
Hochholdinger F, Woll K, Sauer M, Dembinsky D (2004b) Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programmes. Ann Bot 93:359–368. doi:10.1093/aob/mch056
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. doi:10.2136/vzj2007.0115
Koebernick N, Weller U, Huber K, et al (2014) In situ visualization and quantification of three-dimensional root system architecture and growth using x-ray computed tomography. Vadose Zone J 13. doi: 10.2136/vzj2014.03.0024
Landsberg JJ, Fowkes ND (1978) Water movement through plant roots. Ann Bot 42:493–508. doi:10.1093/oxfordjournals.aob.a085488
Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109:7–13
Lynch JP, Chimungu JG, Brown KM (2014) Root anatomical phenes associated with water acquisition from drying soil: targets for crop improvement. J Exp Bot. doi:10.1093/jxb/eru162
Marris E (2008) Water: more crop per drop. Nat New 452:273–277. doi:10.1038/452273a
Matsushima U, Kardjilov N, Hilger A et al (2012) Application potential of cold neutron radiography in plant science research. J Appl Bot Food Qual 82:90–98
Maurel C, Verdoucq L, Luu D-T, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624. doi:10.1146/annurev.arplant.59.032607.092734
McCully ME (1999) Roots in soil: unearthing the complexities of roots and their rhizospheres. Annu Rev Plant Physiol Plant Mol Biol 50:695–718. doi:10.1146/annurev.arplant.50.1.695
McCully ME, Canny MJ (1988) Pathways and processes of water and nutrient movement in roots. Plant Soil 111:159–170. doi:10.1007/BF02139932
Menon M, Robinson B, Oswald SE et al (2007) Visualization of root growth in heterogeneously contaminated soil using neutron radiography. Eur J Soil Sci 58:802–810. doi:10.1111/j.1365-2389.2006.00870.x
Moradi AB, Conesa HM, Robinson B et al (2008) Neutron radiography as a tool for revealing root development in soil: capabilities and limitations. Plant Soil 318:243–255. doi:10.1007/s11104-008-9834-7
Moradi AB, Carminati A, Vetterlein D et al (2011) Three-dimensional visualization and quantification of water content in the rhizosphere. New Phytol 192:653–663. doi:10.1111/j.1469-8137.2011.03826.x
Morison JIL, Baker NR, Mullineaux PM, Davies WJ (2008) Improving water use in crop production. Philos Trans R Soc B Biol Sci 363:639–658. doi:10.1098/rstb.2007.2175
North GB, Nobel PS (1997) Drought-induced changes in soil contact and hydraulic conductivity for roots of Opuntia ficus-indica with and without rhizosheaths. Plant Soil 191:249–258
Ordin L, Kramer PJ (1956) Permeability of vicia faba root segments to water as measured by diffusion of deuterium hydroxide. 12. Plant Physiol 31:468–471
Oswald SE, Menon M, Carminati A et al (2008) Quantitative imaging of infiltration, root growth, and root water uptake via neutron radiography. Vadose Zone J 7:1035. doi:10.2136/vzj2007.0156
Parry MAJ, Hawkesford MJ (2010) Food security: increasing yield and improving resource use efficiency. Proc Nutr Soc 69:592–600. doi:10.1017/S0029665110003836
Pohlmeier A, Javaux M, Vereecken H, et al (2013) Magnetic Resonance Imaging Techniques for Visualization of Root Growth and Root Water Uptake Processes. In: SSSA Special Publication. The Soil Science Society of America, Inc.
Rewald B, Ephrath JE, Rachmilevitch S (2011) A root is a root is a root? Water uptake rates of citrus root orders. Plant Cell Environ 34:33–42. doi:10.1111/j.1365-3040.2010.02223.x
Sanderson J (1983) Water uptake by different regions of the barley root. Pathways of radial flow in relation to development of the endodermis. J Exp Bot 34:240–253. doi:10.1093/jxb/34.3.240
Sierp H, Brewig A (1935) Quantitative untersuchungen über die wasserabsorptionszone der wurzeln. Jahrb Wiss Bot 82:99–122
Sposito G (2013) Green water and global food security. Vadose Zone J 12. doi: 10.2136/vzj2013.02.0041
Steudle E (2000) Water uptake by plant roots: an integration of views. Plant Soil 226:45–56
Tumlinson LG, Liu H, Silk WK, Hopmans JW (2008) Thermal neutron computed tomography of soil water and plant roots. Soil Sci Soc Am J 72:1234. doi:10.2136/sssaj2007.0302
Varney GT, Canny MJ (1993) Rates of water uptake into the mature root system of maize plants. New Phytol 775–786
Wallace JS (2000) Increasing agricultural water use efficiency to meet future food production. Agric Ecosyst Environ 82:105–119. doi:10.1016/S0167-8809(00)00220-6
Wang X-L, Canny MJ, McCully ME (1991) The water status of the roots of soil-grown maize in relation to the maturity of their xylem. Physiol Plant 82:157–162. doi:10.1111/j.1399-3054.1991.tb00075.x
Warren JM, Bilheux H, Kang M et al (2013) Neutron imaging reveals internal plant water dynamics. Plant Soil 366:683–693. doi:10.1007/s11104-012-1579-7
Watt M, McCully ME, Canny MJ (1994) Formation and stabilization of rhizosheaths of Zea mays L. (Effect of soil water content). Plant Physiol 106:179–186
Zarebanadkouki M, Carminati A (2014) Reduced root water uptake after drying and rewetting. J Plant Nutr Soil Sci 177:227–236. doi:10.1002/jpln.201300249
Zarebanadkouki M, Kim YX, Moradi AB, et al (2012) Quantification and modeling of local root water uptake using neutron radiography and deuterated water. Vadose Zone J 11. doi: 10.2136/vzj2011.0196
Zarebanadkouki M, Kim YX, Carminati A (2013) Where do roots take up water? Neutron radiography of water flow into the roots of transpiring plants growing in soil. New Phytol 199:1034–1044. doi:10.1111/nph.12330
Zarebanadkouki M, Kroener E, Kaestner A, Carminati A (2014) Visualization of root water uptake: Quantification of deuterated water transport in roots using neutron radiography and numerical modeling. Plant Physiol 114.243212. doi: 10.1104/pp.114.243212
Zwieniecki MA, Thompson MV, Holbrook NM (2003) Understanding the hydraulics of porous pipes: tradeoffs between water uptake and root length utilization. J Plant Growth Regul 21:315–323. doi:10.1007/s00344-003-0008-9
Acknowledgments
The doctoral position of Mutez Ahmed was funded by the German Academic Exchange Service (DAAD). We are grateful to the staff at the ICON imaging station of the Paul Scherrer Institute (PSI), Villigen, Switzerland for their technical support during the measurements with neutron radiography. KWS is appreciated for providing Maize seeds. Finally, we would like to thank Claude Doussan for his comments on a former presentation of this study and two anonymous reviewers for the constructive comments on the former version of the manuscript.
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Ahmed, M.A., Zarebanadkouki, M., Kaestner, A. et al. Measurements of water uptake of maize roots: the key function of lateral roots. Plant Soil 398, 59–77 (2016). https://doi.org/10.1007/s11104-015-2639-6
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DOI: https://doi.org/10.1007/s11104-015-2639-6