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Dynamics of plant nutrient uptake as affected by biopore-associated root growth in arable subsoil

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Abstract

Aims

Soil biopores facilitate root growth in arable subsoil, thus improve resource acquisition potential. We aimed at determining the dynamic relationship between soil biopores and performance of two winter crops in field condition considering different biopore size classes, root characteristics and crop growth parameters.

Methods

Chicory with dominant taproot system and tall fescue with limited taproots were grown for two consecutive years as precrops. Density of soil biopores larger than 2 mm and smaller than 2 mm in diameter was measured at 45 cm of soil depth. Destructive samplings were carried out for investigation on following barley and canola roots. Shoot biomass production, nutrient uptake and final yield of the following crops were determined throughout the growth seasons.

Results

Higher shares of large or small-sized bipoores were observed after chicory (23 %) or tall fescue (20 %) precrops, respectively. On average root diameter and root dry mass of following crops were greater by 11 and 15 % after chicory than tall fescue. At anthesis chicory-barley treatment accumulated 10 % more K in comparison to tall fescue-barley treatment. P uptake of canola was greater (7 %) after tall fescue compared with chicory at the stage of fruit development.

Conclusions

Our results suggest that the subsoil heterogenization by altered soil biopores hold relevance for plant root growth and overall crop performance. However, the effects depended on biopore size classes, root characteristics and crop species. Development of direct methods that can quantify biopore-root-shoot processes, detailed investigation on drilosphere, root phenotyping for detection of the genetic variation in response to biopore systems have to be followed in the future.

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References

  • Akaike H (1974) A new look at the statistical model identification. Automatic Control, IEEE Transactions on 19:716–723. doi:10.1109/TAC.1974.1100705

    Article  Google Scholar 

  • Athmann M, Kautz T, Pude R, Köpke U (2013) Root growth in biopores-evaluation with in situ endoscopy. Plant Soil 371:179–190. doi:10.1007/s11104-013-1673-5

    Article  CAS  Google Scholar 

  • Barej JAM, Pätzold S, Perkons U, Amelung W (2014) Phosphorus fractions in bulk subsoil and its biopore systems. Eur J Soil Sci 65:553–561. doi:10.1111/ejss.12124

    Article  CAS  Google Scholar 

  • Bates TR, Lynch JP (2001) Root hairs confer a competitive advantage under low phosphorus availability. Plant Soil 236:243–250. doi:10.1023/A:1012791706800

    Article  CAS  Google Scholar 

  • Batey T (2009) Soil compaction and soil management - a review. Soil Use Manage 25:335–345. doi:10.1111/j.1475-2743.2009.00236.x

    Article  Google Scholar 

  • Bengough AG (2006) Root responses to soil physical conditions; growth dynamics from field to cell. J Exp Bot 57:437–447. doi:10.1093/jxb/erj003

    Article  CAS  PubMed  Google Scholar 

  • Bengough AG (2012) Root elongation is restricted by axial but not by radial pressures: so what happens in field soil? Plant Soil 360:15–18. doi:10.1007/s11104-012-1428-8

    Article  CAS  Google Scholar 

  • Bengough AG, Mackenzie CJ (1994) Simultaneous measurement of root force and elongation for seedling pea roots. J Exp Bot 45:95–102. doi:10.1093/jxb/45.1.95

  • Bodner G, Leitner D, Kaul HP (2014) Coarse and fine root plants affect pore size distributions differently. Plant Soil 380:133–151. doi:10.1007/s11104-014-2079-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouché MB (1975) Action de la faune sur les etats de la matiere organique dans les ecosystemes. In: Kilbertius G, Reisinger O, Mourey A, Cancela da Fonseca JA (eds) Humification et biodégradation. Pierron, Sarreguemines, pp. 157–168

  • Böhm W (1979a) Monolith methods. In: Böhm W (ed) Methods of studying root systems. Springer-Verlag, Berlin Heidelberg New York, pp. 20–29

  • Böhm W (1979b) Profile wall methods. In: Böhm W (ed) Methods of studying root systems. Springer-Verlag, Berlin Heidelberg New York, pp. 48–60

  • Chimungu JG, Maliro MFA, Nalivata PC et al (2015) Utility of root cortical aerenchyma under water limited conditions in tropical maize (Zea mays L.). Field Crop Res 171:86–98. doi:10.1016/j.fcr.2014.10.009

    Article  Google Scholar 

  • Cresswell HP, Kirkegaard JA (1995) Subsoil amelioration by plant-roots - the process and the evidence. Aust J Soil Res 33:221–239. doi:10.1071/SR9950221

    Article  Google Scholar 

  • Ehlers W (1975) Observations on earthworm channels and infiltration on tilled and untilled loess. Soil 119:242–249. doi:10.1097/00010694-197503000-00010

    Article  Google Scholar 

  • Ehlers W, Köpke U, Hesse F, Böhm W (1983) Penetration resistance and root growth of oats in tilled and untilled loess soil. Soil Till Res 3:261–275. doi:10.1016/0167-1987(83)90027-2

    Article  Google Scholar 

  • Engels C, Neumann G, Gahoonia TS, et al. (2000) Assessing the ability of roots for nutrient acquisition. In: Smit AL, Bengough AG, Engels C, et al. (eds) Root methods. Springer-Verlag, Berlin Heidelberg New York, pp 403–459

  • Fernandez OA, Caldwell MM (1975) Phenology and dynamics of root growth of three cool semi-desert shrubs under field conditions. J Ecol 63:703–714. doi:10.2307/2258746

    Article  Google Scholar 

  • Fitter AH (1987) An architectural approach to the comparative ecology of plant root systems. New Phytol 106:61–77

    Article  Google Scholar 

  • Föhse D, Claassen N, Jungk A (1991) Phosphorus efficiency of plants. Plant Soil 132:261–272. doi:10.1007/BF00011205

    Article  Google Scholar 

  • Gaiser T, Perkons U, Küpper PM et al (2012) Evidence of improved water uptake from subsoil by spring wheat following lucerne in a temperate humid climate. Field Crop Res 126:56–62. doi:10.1016/j.fcr.2011.09.019

    Article  Google Scholar 

  • Gaiser T, Perkons U, Küpper PM, Kautz T (2013) Modeling biopore effects on root growth and biomass production on soils with pronounced sub-soil clay accumulation. Ecol Model 256:6–15. doi:10.1016/j.ecolmodel.2013.02.016

    Article  Google Scholar 

  • Girma K, Holtz S, Tubaña B et al (2014) Nitrogen accumulation in shoots as a function of growth stage of corn and winter wheat. J Plant Nutr 34:165–182. doi:10.1080/01904167.2011.533320

    Article  Google Scholar 

  • Głąb T, Ścigalska B, Łabuz B (2013) Effect of crop rotations with triticale (X Triticosecale Wittm.) on soil pore characteristics. Geoderma:202–203. doi:10.1016/j.geoderma.2013.03.002

  • Han E, Kautz T, Köpke U (2016) Precrop root system determines root diameter of subsequent crop. Biol Fert. Soils 52:113–118. doi:10.1007/s00374-015-1049-5

    Google Scholar 

  • Han E, Kautz T, Perkons U et al (2015a) Quantification of soil biopore density after perennial fodder cropping. Plant Soil 394:73–85. doi:10.1007/s11104-015-2488-3

    Article  CAS  Google Scholar 

  • Han E, Kautz T, Perkons U et al (2015b) Root growth dynamics inside and outside of soil biopores as affected by crop sequence determined with the profile wall method. Biol Fert. Soils 51:847–856. doi:10.1007/s00374-015-1032-1

    Google Scholar 

  • Hatano R, Iwanaga K, Okajima H, Sakuma T (1988) Relationship between the distribution of soil macropores and root elongation. Soil Sci Plant Nutr 34:535–546. doi:10.1080/00380768.1988.10416469

    Article  Google Scholar 

  • Hinsinger P, Bengough AG, Vetterlein D, Young IM (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152. doi:10.1007/s11104-008-9885-9

    Article  CAS  Google Scholar 

  • Hodge A, Robinson D, Griffiths BS, Fitter AH (1999) Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete. Plant Cell Environ 22:811–820. doi:10.1046/j.1365-3040.1999.00454.x

    Article  Google Scholar 

  • Huang B, Gao H (2000) Root physiological characteristics associated with drought resistance in tall fescue cultivars. Crop Sci 40:196–203. doi:10.2135/cropsci2000.401196x

    Article  Google Scholar 

  • IUSS Working Group WRB (2006) World reference base for soil resources 2006, 2nd edn. FAO, Rome

  • Jakobsen BE, Dexter AR (1988) Influence of biopores on root growth, water uptake and grain yield of wheat (Triticum aestivum) based on predictions from a computer model. Biol Fert. Soils 6:315–321. doi:10.1007/BF00261020

    Google Scholar 

  • Jungk A, Claassen N (1997) Ion diffusion in the soil-root system. Adv Agron 61:53–110. doi:10.1016/S0065-2113(08)60662-8

    Article  CAS  Google Scholar 

  • Kautz T (2015) Research on subsoil biopores and their functions in organically managed soils: a review. Renew Agr Food Syst 30:318–327. doi:10.1017/S1742170513000549

    Article  Google Scholar 

  • Kautz T, Amelung W, Ewert F et al (2013a) Nutrient acquisition from arable subsoils in temperate climates: a review. Soil Biol Biochem 57:1003–1022. doi:10.1016/j.soilbio.2012.09.014

    Article  CAS  Google Scholar 

  • Kautz T, Lüsebrink M, Pätzold S et al (2014) Contribution of anecic earthworms to biopore formation during cultivation of perennial ley crops. Pedobiologia - international journal of soil. Biology 57:47–52. doi:10.1016/j.pedobi.2013.09.008

    Google Scholar 

  • Kautz T, Perkons U, Athmann M et al (2013b) Barley roots are not constrained to large-sized biopores in the subsoil of a deep Haplic Luvisol. Biol Fert. Soils 49:959–963. doi:10.1007/s00374-013-0783-9

    Google Scholar 

  • Kolb E, Hartmann C, Genet P (2012) Radial force development during root growth measured by photoelasticity. Plant Soil 360:19–35. doi:10.1007/s11104-012-1316-2

    Article  CAS  Google Scholar 

  • Köpke U (1995) Nutrient management in organic farming systems: The case of nitrogen. Biol. Agr. Hort, Copenhagen, pp 15–29

  • Köpke U, Athmann M, Han E, Kautz T (2015) Optimising cropping techniques for nutrient and environmental management in organic agriculture. SAR 4:15–11. doi:10.5539/sar.v4n3p15

    Article  Google Scholar 

  • Lamandé M, Hallaire V, Curmi P et al (2003) Changes of pore morphology, infiltration and earthworm community in a loamy soil under different agricultural managements. Catena 54:637–649. doi:10.1016/S0341-8162(03)00114-0

    Article  Google Scholar 

  • Lancashire PD, Bleiholder H, Van Den Boom T et al (1991) A uniform decimal code for growth-stages of crops and weeds. Ann applied. Biology 119:561–601

    Google Scholar 

  • Lauenroth WK, Gill R (2003) Turnover of root systems. In: Kroon H de, Visser EJW (eds) Root ecology. Springer-Verlag, Berlin Heidelberg New York, pp 61–89

  • Loades KW, Bengough AG, Bransby MF, Hallett PD (2015) Effect of root age on the biomechanics of seminal and nodal roots of barley (Hordeum vulgare L.) in contrasting soil environments. Plant Soil 395:253–261. doi:10.1007/s11104-015-2560-z

    Article  CAS  Google Scholar 

  • Lynch JP, Wojciechowski T (2015) Opportunities and challenges in the subsoil: pathways to deeper rooted crops. J Exp Bot 66:2199–2210. doi:10.1093/jxb/eru508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Materechera SA, Alston AM, Kirby JM, Dexter AR (1992) Influence of root diameter on the penetration of seminal roots into a compacted subsoil. Plant Soil 144:297–303. doi:10.1007/BF00012888

    Article  Google Scholar 

  • McCallum MH, Kirkegaard JA, Green TW et al (2004) Improved subsoil macroporosity following perennial pastures. Aust J Exp Agr 44:299–307. doi:10.1071/EA03076

    Article  Google Scholar 

  • McCormack ML, Dickie IA, Eissenstat DM et al (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518. doi:10.1111/nph.13363

    Article  PubMed  Google Scholar 

  • McKenzie BM, Bengough AG, Hallett PD et al (2009) Deep rooting and drought screening of cereal crops: a novel field-based method and its application. Field Crop Res 112:165–171. doi:10.1016/j.fcr.2009.02.012

    Article  Google Scholar 

  • Moran CJ, Pierret A, Stevenson AW (2000) X-ray absorption and phase contrast imaging to study the interplay between plant roots and soil structure. Plant Soil 223:101–117. doi:10.1023/A:1004835813094

    Article  Google Scholar 

  • Nakamoto T (1997) The distribution of maize roots as influenced by artificial vertical macropores. Japanese. J Crop Sci 66:331–332. doi:10.1626/jcs.66.331

    Article  Google Scholar 

  • Neukirchen D, Himken M, Lammel J et al (1999) Spatial and temporal distribution of the root system and root nutrient content of an established Miscanthus crop. Eur J Agron 11:301–309. doi:10.1016/S1161-0301(99)00031-3

    Article  Google Scholar 

  • Pagenkemper SK, Athmann M, Uteau D et al (2014) The effect of earthworm activity on soil bioporosity – investigated with X-ray computed tomography and endoscopy. Soil Till Res 146:79–88. doi:10.1016/j.still.2014.05.007

    Article  Google Scholar 

  • Pankhurst CE, Pierret A, Hawke BG, Kirby JM (2002) Microbiological and chemical properties of soil associated with macropores at different depths in a red-duplex soil in NSW Australia. Plant Soil 238:11–20. doi:10.1023/a:1014289632453

    Article  CAS  Google Scholar 

  • Passioura JB (1991) Soil structure and plant growth. Aust J Soil Res 29:717–728. doi:10.1071/Sr9910717

    Article  Google Scholar 

  • Peng Y, Li X, Li C (2012) Temporal and spatial profiling of root growth revealed novel response of maize roots under various nitrogen supplies in the field. PLoS One 7:e37726. doi: 10.1371/journal.pone.0037726

  • Perkons U, Kautz T, Uteau D et al (2014) Root-length densities of various annual crops following crops with contrasting root systems. Soil Till Res 137:50–57. doi:10.1016/j.still.2013.11.005

    Article  Google Scholar 

  • Piepho HP, Büchse A, Richter C (2004) A mixed modelling approach for randomized experiments with repeated measures 190:230–247. doi: 10.1111/j.1439-037X.2004.00097.x

  • Pierret A, Moran CJ, Doussan C (2005) Conventional detection methodology is limiting our ability to understand the roles and functions of fine roots. New Phytol 166:967–980. doi:10.1111/j.1469-8137.2005.01389.x

    Article  PubMed  Google Scholar 

  • Pierret A, Moran CJ, Pankhurst CE (1999) Differentiation of soil properties related to the spatial association of wheat roots and soil macropores. Plant Soil 211:51–58. doi:10.1023/a:1004490800536

    Article  CAS  Google Scholar 

  • Pietola L, Alakukku L (2005) Root growth dynamics and biomass input by Nordic annual field crops. Agric Ecosyst Environ 108:135–144. doi:10.1016/j.agee.2005.01.009

    Article  Google Scholar 

  • Pii Y, Mimmo T, Tomasi N et al (2015) Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biol Fert. Soils 51:403–415. doi:10.1007/s00374-015-0996-1

    CAS  Google Scholar 

  • Pinheiro J, Bates D (2000) Mixed-effects models in S and S-PLUS. Springer, New York

    Book  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing.

  • Reinhardt DR, Miller RM (1990) Size classes of root diameter and mycorrhizal fungal colonization in 2 temperate grassland communities. New Phytol 116:129–136. doi:10.1111/j.1469-8137.1990.tb00518.x

    Article  Google Scholar 

  • Schultz-Lupitz A (1895) Zwischenfruchtbau auf leichtem Boden. Berlin

  • Smucker AJM (1993) Soil environmental modifications of root dynamics and measurement. Annu Rev Phytopathol 31:191–218

    Article  Google Scholar 

  • Stewart JB, Moran CJ, Wood JT (1999) Macropore sheath: quantification of plant root and soil macropore association. Plant Soil 211:59–67. doi:10.1023/A:1004405422847

    Article  CAS  Google Scholar 

  • Stirzaker RJ, Passioura JB, Wilms Y (1996) Soil structure and plant growth: impact of bulk density and biopores. Plant Soil 185:151–162. doi:10.1007/bf02257571

    Article  CAS  Google Scholar 

  • Thorup-Kristensen K, Cortasa MS, Loges R (2009) Winter wheat roots grow twice as deep as spring wheat roots, is this important for N uptake and N leaching losses? Plant Soil 322:101–114. doi:10.1007/s11104-009-9898-z

    Article  CAS  Google Scholar 

  • Uksa M, Schloter M, Kautz T et al (2015) Spatial variability of hydrolytic and oxidative potential enzyme activities in different subsoil compartments. Biol Fert. Soils 51:517–521. doi:10.1007/s00374-015-0992-5

    CAS  Google Scholar 

  • Valentine TA, Hallett PD, Binnie K et al (2012) Soil strength and macropore volume limit root elongation rates in many UK agricultural soils. Ann Bot-London 110:259–270. doi:10.1093/Aob/Mcs118

    Article  CAS  Google Scholar 

  • van Schaik L, Palm J, Klaus J et al (2014) Linking spatial earthworm distribution to macropore numbers and hydrological effectiveness. Ecohydrol 7:401–408. doi:10.1002/eco.1358

    Article  Google Scholar 

  • Veen BW, van Noordwijk M, de Willigen P et al (1992) Root-soil contact of maize, as measured by a thin-section technique. III. Effects on shoot growth, nitrate and water-uptake efficiency. Plant Soil 139:131–138. doi:10.1007/Bf00012850

    Article  Google Scholar 

  • Vetterlein D, Kühn T, Kaiser K, Jahn R (2013) Illite transformation and potassium release upon changes in composition of the rhizophere soil solution. Plant Soil 371:267–279. doi:10.1007/s11104-013-1680-6

    Article  CAS  Google Scholar 

  • Volkmar KM (1996) Effects of biopores on the growth and N-uptake of wheat at three levels of soil moisture. Can J Soil Sci 76:453–458. doi:10.1007/s00248-012-0132-9

    Article  CAS  Google Scholar 

  • Watt M, Kirkegaard JA, Rebetzke GJ (2005) A wheat genotype developed for rapid leaf growth copes well with the physical and biological constraints of unploughed soil. Funct Plant Biol 32:695–706. doi:10.1071/FP05026

    Article  Google Scholar 

  • White RG, Kirkegaard JA (2010) The distribution and abundance of wheat roots in a dense, structured subsoil - implications for water uptake. Plant Cell Environ 33:133–148. doi:10.1111/j.1365-3040.2009.02059.x

    Article  PubMed  Google Scholar 

  • Wu Q, Pagès L, Wu J (2016) Relationships between root diameter, root length and root branching along lateral roots in adult, field-grown maize. Ann Bot-London mcv:185–112. doi:10.1093/aob/mcv185

  • York LM, Carminati A, Mooney SJ et al (2016) The holistic rhizosphere: integrating zones, processes, and semantics in the soil influenced by roots. J Exp Bot 67:3629–3643. doi:10.1093/jxb/erw108

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Brown KM, Lynch JP (2010) Root cortical aerenchyma improves the drought tolerance of maize (Zea mays L.). Plant Cell Environ 33:740–749. doi:10.1111/j.1365-3040.2009.02099.x

    PubMed  Google Scholar 

  • Zobel RW, Waisel Y (2010) A plant root system architectural taxonomy: a framework for root nomenclature. Plant Biosyst 144:507–512. doi:10.1080/11263501003764483

    Article  Google Scholar 

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Acknowledgements

We are grateful to the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG) for financing this study under the research units DFG FOR 1320 and DFG PAK 888. Special thanks shall go to the project coordinators, Miriam Athmann and Ute Perkons, and also to the technicians, Christian Dahn, Frank Täufer, Henning Riebeling and Johannes Siebigteroth.

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Authors and Affiliations

  1. Institute of Organic Agriculture, University of Bonn, Katzenburgweg 3, 53115, Bonn, Germany

    Eusun Han, Timo Kautz, Ning Huang & Ulrich Köpke

  2. Campus Klein-Altendorf, Klein-Altendorf 2, 53359, Rheinbach, Germany

    Eusun Han, Timo Kautz, Ning Huang & Ulrich Köpke

  3. Department of Plant and Environmental Sciences, University of Copenhagen, Højbakkegård Alle 13, 2630, Taastrup, Denmark

    Eusun Han

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  1. Eusun Han
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Han, E., Kautz, T., Huang, N. et al. Dynamics of plant nutrient uptake as affected by biopore-associated root growth in arable subsoil. Plant Soil 415, 145–160 (2017). https://doi.org/10.1007/s11104-016-3150-4

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