Abstract
Aims
Phosphorus (P) is usually stratified in the topsoil layer under pasture, due to the broadcast application of fertiliser, excreta and leaf-litter deposition on the soil surface, and minimal soil disturbance. The objective of this study was to investigate root proliferation and P acquisition in response to P stratification by comparing two Trifolium subterraneum cultivars with contrasting root morphologies.
Methods
Clover micro-swards were grown with deficient, constrained and sufficient P supplied in a topsoil layer overlying a P-deficient subsoil that mimicked the stratification of P that occurs under pasture. Phosphorus labelled with 33P- and 32P-radioisotope tracer was mixed throughout the topsoil and subsoil layers, respectively.
Results
The shoot yield and total plant P uptake of the cultivars increased in response to increased topsoil P supply. The length of roots produced by the cultivars was equivalent in each of the P treatments, although the specific root length achieved by the cultivars was substantially different. In the P-constrained and P-sufficient treatments, ~91% and ~ 99% of total plant P was acquired by topsoil roots, respectively. In contrast, subsoil roots acquired 60–74% of total plant P in the P-deficient treatment.
Conclusions
Topsoil roots were most important for P acquisition when P was highly stratified, whereas subsoil roots contributed to P acquisition when P was uniformly distributed throughout the P-deficient soil profile. Selection for prolific nutrient-foraging roots, in conjunction with plasticity for subsoil exploration, may improve the P-acquisition efficiency of T. subterraneum genotypes and confer adaptability across a range of soil-P environments.
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References
Barber SA (1984) Soil nutrient bioavailability: a mechanistic approach. Wiley, New York
Bolan NS (1991) A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant Soil 134:189–207. https://doi.org/10.1007/BF00012037
Bouma TJ, Nielsen KL, Koutstaal B (2000) Sample preparation and scanning protocol for computerised analysis of root length and diameter. Plant Soil 218:185–196. https://doi.org/10.1023/A:1014905104017
Brouwer R (1962) Nutritive influences on the distribution of dry matter in the plant. Neth J Agric Sci 10:399–408
Burkitt LL, Sale PWG, Gourley CJP (2008) Soil phosphorus buffering measures should not be adjusted for current phosphorus fertility. Aust J Soil Res 46:676–685. https://doi.org/10.1071/SR06126
Chakwizira E, Moot DJ, Scott WR, Fletcher AL, Maley S (2011) Leaf development, radiation interception and radiation-use efficiency of kale crops supplied with different rates of banded or broadcast phosphorus fertiliser. Crop Pasture Sci 62:840–847. https://doi.org/10.1071/cp10359
Colwell JD (1963) The estimation of the phosphorus fertilizer requirements of wheat in southern New South Wales by soil analysis. Aust J Exp Agric 3:190–197. https://doi.org/10.1071/EA9630190
Coombes NE (2006) DiGGer, a design generator. http://www.austatgen.org/files/software/downloads
Crush JR, Boulesteix-Coutelier ARL, Ouyang L (2008) Phosphate uptake by white clover (Trifolium repens L.) genotypes with contrasting root morphology. N Z J Agric Res 51:279–285. https://doi.org/10.1080/00288230809510458
Dear BS, Virgona JM (1996) Legumes in low-input perennial pastures of southern Australia: historical role and future development. N Z J Agric Res 39:579–589. https://doi.org/10.1080/00288233.1996.9513217
Drew MC (1975) Comparison of the effects of a localised supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol 75:479–490. https://doi.org/10.1111/j.1469-8137.1975.tb01409.x
Eissenstat DM (1992) Costs and benefits of constructing roots of small diameter. J Plant Nutr 15:763–782. https://doi.org/10.1080/01904169209364361
Freschet GT, Swart EM, Cornelissen JHC (2015) Integrated plant phenotypic responses to contrasting above- and below-ground resources: key roles of specific leaf area and root mass fraction. New Phytol 206:1247–1260. https://doi.org/10.1111/nph.13352
Gahoonia TS, Care D, Nielsen NE (1997) Root hairs and phosphorus acquisition of wheat and barley cultivars. Plant Soil 191:181–188. https://doi.org/10.1023/A:1004270201418
Gahoonia TS, Nielsen NE (1998) Direct evidence on participation of root hairs in phosphorus (32P) uptake from soil. Plant Soil 198:147–152. https://doi.org/10.1023/A:1004346412006
Ghamkhar K, Nichols PGH, Erskine W, Snowball R, Murillo M, Appels R, Ryan MH (2015) Hotspots and gaps in the world collection of subterranean clover (Trifolium subterraneum L.). J Agric Sci 153:1069–1083. https://doi.org/10.1017/s0021859614000793
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x
Haling RE, Brown LK, Stefanski A, Kidd DR, Ryan MH, Sandral GA, George TS, Lambers H, Simpson RJ (2018) Differences in nutrient foraging among Trifolium subterraneum cultivars deliver improved P-acquisition efficiency. Plant Soil 424:539–554. https://doi.org/10.1007/s11104-017-3511-7
Haling RE, Yang Z, Shadwell N, Culvenor RA, Stefanski A, Ryan MH, Sandral GA, Kidd DR, Lambers H, Simpson RJ (2016a) Growth and root dry matter allocation by pasture legumes and a grass with contrasting external critical phosphorus requirements. Plant Soil 407:67–79. https://doi.org/10.1007/s11104-016-2808-2
Haling RE, Yang Z, Shadwell N, Culvenor RA, Stefanski A, Ryan MH, Sandral GA, Kidd DR, Lambers H, Simpson RJ (2016b) Root morphological traits that determine phosphorus-acquisition efficiency and critical external phosphorus requirement in pasture species. Funct Plant Biol 43:815–826. https://doi.org/10.1071/fp16037
Hecht VL, Temperton VM, Nagel KA, Rascher U, Postma JA (2016) Sowing density: a neglected factor fundamentally affecting root distribution and biomass allocation of field grown spring barley (Hordeum vulgare L.). Front Plant Sci 7:1–14. https://doi.org/10.3389/fpls.2016.00944
Heuer S, Gaxiola R, Schilling R, Herrera-Estrella L, Lopez-Arredondo D, Wissuwa M, Delhaize E, Rouached H (2017) Improving phosphorus use efficiency: a complex trait with emerging opportunities. Plant J 90:868–885. https://doi.org/10.1111/tpj.13423
Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24. https://doi.org/10.1111/j.1469-8137.2004.01015.x
Hodge A (2006) Plastic plants and patchy soils. J Exp Bot 57:401–411. https://doi.org/10.1093/jxb/eri280
Howieson JG, O'Hara GW, Carr SJ (2000) Changing roles for legumes in Mediterranean agriculture: developments from an Australian perspective. Field Crop Res 65:107–122. https://doi.org/10.1016/S0378-4290(99)00081-7
Irving GCJ, McLaughlin MJ (1990) A rapid and simple field test for phosphorus in Olsen and bray no. 1 extracts of soil. Commun Soil Sci Plant Anal 21:2245–2255. https://doi.org/10.1080/00103629009368377
Isbell RF (1996) The Australian soil classification. CSIRO Publishing, Melbourne
Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots. New Phytol 120:371–380. https://doi.org/10.1111/j.1469-8137.1992.tb01800.x
Jeffery RP, Simpson RJ, Lambers H, Kidd DR, Ryan MH (2017) Plants in constrained canopy micro-swards compensate for decreased root biomass and soil exploration with increased amounts of rhizosphere carboxylates. Funct Plant Biol 44:552–562. https://doi.org/10.1071/fp16398
Kidd DR, Ryan MH, Hahne D, Haling RE, Lambers H, Sandral GA, Simpson RJ, Cawthray GR (2018) The carboxylate composition of rhizosheath and root exudates from twelve species of grassland and crop legumes with special reference to the occurrence of citramalate. Plant Soil 424:389–403. https://doi.org/10.1007/s11104-017-3534-0
Kidd DR, Ryan MH, Haling RE, Lambers H, Sandral GA, Yang Z, Culvenor RA, Cawthray GR, Stefanski A, Simpson RJ (2016) Rhizosphere carboxylates and morphological root traits in pasture legumes and grasses. Plant Soil 402:77–89. https://doi.org/10.1007/s11104-015-2770-4
Konvalinkova T, Puschel D, Rezacova V, Gryndlerova H, Jansa J (2017) Carbon flow from plant to arbuscular mycorrhizal fungi is reduced under phosphorus fertilization. Plant Soil 419:319–333. https://doi.org/10.1007/s11104-017-3350-6
Lendenmann M, Thonar C, Barnard RL, Salmon Y, Werner RA, Frossard E, Jansa J (2011) Symbiont identity matters: carbon and phosphorus fluxes between Medicago truncatula and different arbuscular mycorrhizal fungi. Mycorrhiza 21:689–702. https://doi.org/10.1007/s00572-011-0371-5
Lenth RV (2016) Least-squares means: the R package lsmeans. Journal of Statistical Software 69: 1-\. Doi: https://doi.org/10.18637/jss.v069.i01
Lynch JP (2007) Roots of the second green revolution. Aust J Bot 55:493–512. https://doi.org/10.1071/bt06118
Lynch JP, Brown KM (2001) Topsoil foraging - an architectural adaptation of plants to low phosphorus availability. Plant Soil 237:225–237. https://doi.org/10.1023/A:1013324727040
Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269:45–56. https://doi.org/10.1007/s11104-004-1096-4
Lynch JP, Wojciechowski T (2015) Opportunities and challenges in the subsoil: pathways to deeper rooted crops. J Exp Bot 66:2199–2210. https://doi.org/10.1093/jxb/eru508
McLachlan JW, Flavel RJ, Guppy CN, Simpson RJ, Haling RE (2019a) Differences in subsoil P acquisition by two subterranean clover cultivars in a P deficient soil. Proceedings of the 19th Australian Society of Agronomy Conference. http://www.agronomyaustraliaproceedings.org/, Wagga Wagga, Australia
McLachlan JW, Haling RE, Simpson RJ, Flavel RJ, Guppy CN (2020b) Root proliferation in response to P stress and space: implications for the study of root acclimation to low P supply and P acquisition efficiency. Plant Soil:1–19. https://doi.org/10.1007/s11104-020-04535-y
McLachlan JW, Haling RE, Simpson RJ, Li X, Flavel RJ, Guppy CN (2019b) Variation in root morphology and P acquisition efficiency among Trifolium subterraneum genotypes. Crop Pasture Sci 70:1015–1032. https://doi.org/10.1071/CP19078
McLaren TI, McLaughlin MJ, McBeath TM, Simpson RJ, Smernick RJ, Guppy CN, Richardson AE (2016) The fate of fertiliser P in soil under pasture and uptake by subterraneum clover - a field study using 33 P-labelled single superphosphate. Plant Soil 401:23–38. https://doi.org/10.1007/s11104-015-2610-6
McLaughlin MJ, McBeath TM, Smernik R, Stacey SP, Ajiboye B, Guppy C (2011) The chemical nature of P accumulation in agricultural soils - implications for fertiliser management and design: an Australian perspective. Plant Soil 349:69–87. https://doi.org/10.1007/s11104-011-0907-7
Nichols PGH, Foster KJ, Piano E, Pecetti L, Kaur P, Ghamkhar K, Collins WJ (2013) Genetic improvement of subterranean clover (Trifolium subterraneum L.). 1. Germplasm, traits and future prospects. Crop Pasture Sci 64:312–346. https://doi.org/10.1071/cp13118
Ozanne PG, Howes KMW, Petch A (1976) The comparative phosphate requirements of four annual pastures and two crops. Aust J Agric Res 27:479–488. https://doi.org/10.1071/AR9760479
Ozanne PG, Keay J, Biddiscombe EF (1969) The comparative applied phosphate requirements of eight annual pasture species. Aust J Agric Res 20:809–818. https://doi.org/10.1071/AR9690809
Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2018) nlme: linear and nonlinear mixed effects models. https://CRAN.R-project.org/package=nlme, R package version 3.1–137
Pinkerton A, Simpson JR (1986) Interactions of surface drying and subsurface nutrients affecting plant growth on acidic soil profiles from an old pasture. Aust J Exp Agric 26:681–689. https://doi.org/10.1071/EA9860681
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rae AL, Jarmey JM, Mudge SR, Smith FW (2004) Over-expression of a high-affinity phosphate transporter in transgenic barley plants does not enhance phosphate uptake rates. Funct Plant Biol 31:141–148. https://doi.org/10.1071/FP03159
Richardson AE, Hocking PJ, Simpson RJ, George TS (2009) Plant mechanisms to optimise access to soil phosphorus. Crop Pasture Sci 60:124–143. https://doi.org/10.1071/CP07125
Ros MBH, De Deyn GB, Koopmans GF, Oenema O, van Groenigen JW (2018) What root traits determine grass resistance to phosphorus deficiency in production grassland? J Plant Nutr Soil Sci 181:323–335. https://doi.org/10.1002/jpln.201700093
Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:527–560. https://doi.org/10.1146/annurev.arplant.52.1.527
Ryan MH, Kidd DR, Sandral GA, Yang Z, Lambers H, Culvenor RA, Stefanski A, Nichols PGH, Haling RE, Simpson RJ (2016) High variation in the percentage of root length colonised by arbuscular mycorrhizal fungi among 139 lines representing the species subterranean clover (Trifolium subterraneum). Appl Soil Ecol 98:221–232
Sandral GA, Haling RE, Ryan MH, Price A, Pitt WM, Hildebrand SM, Fuller CG, Kidd DR, Stefanski A, Lambers H, Simpson RJ (2018) Intrinsic capacity for nutrient foraging predicts critical external phosphorus requirement of 12 pasture legumes. Crop Pasture Sci 69:174–182. https://doi.org/10.1071/cp17276
Sandral GA, Price A, Hildebrand SM, Fuller CG, Haling RE, Stefanksi A, Yang Z, Culvenor RA, Ryan MH, Kidd DR, Diffey S, Lambers H, Simpson RJ (2019) Field benchmarking of the critical external phosphorus requirements of pasture legumes for southern Australia. Crop Pasture Sci 70:1080–1096. https://doi.org/10.1071/CP19014
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682. https://doi.org/10.1038/nmeth.2019
Scott BJ (1973) The response of barrel medic pasture to topdressed and placed superphosphate in central western New South Wales. Aust J Exp Agric Anim Husb 13:705–710. https://doi.org/10.1071/EA9730705
Silsbury JH, Fukai S (1977) Effects of sowing time and sowing density on the growth of subterranean clover at Adelaide. Aust J Agric Res 28:427–440. https://doi.org/10.1071/AR9770427
Simpson RJ, Richardson AE, Nichols SN, Crush JR (2014) Pasture plants and soil fertility management to improve the efficiency of phosphorus fertiliser use in temperate grassland systems. Crop Pasture Sci 65:556–575. https://doi.org/10.1071/cp13395
Simpson RJ, Stefanski A, Marshall DJ, Moore AD, Richardson AE (2015) Management of soil phosphorus fertility determines the phosphorus budget of a temperate grazing system and is the key to improving phosphorus efficiency. Agric Ecosyst Environ 212:263–277. https://doi.org/10.1016/j.agee.2015.06.026
Thomson BD, Robson AD, Abbott LK (1991) Soil mediated effects of phosphorus supply on the formation of mycorrhizas by Scutellispora calospora (Nicol. & Gerd.) Walker Sanders on subterranean clover. New Phytol 118:463–469. https://doi.org/10.1111/j.1469-8137.1991.tb00028.x
Ven A, Verlinden MS, Verbruggen E, Vicca S (2019) Experimental evidence that phosphorus fertilization and arbuscular mycorrhizal symbiosis can reduce the carbon cost of phosphorus uptake. Funct Ecol 33:1–11. https://doi.org/10.1111/1365-2435.13452
Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007. https://doi.org/10.1128/AEM.64.12.5004-5007.1998
Yang Z, Culvenor RA, Haling RE, Stefanski A, Ryan MH, Sandral GA, Kidd DR, Lambers H, Simpson RJ (2017) Variation in root traits associated with nutrient foraging among temperate pasture legumes and grasses. Grass Forage Sci 72:93–103. https://doi.org/10.1111/gfs.12199
Acknowledgements
This study was conducted as part of ‘RnD4P-15-02-016 Phosphorus Efficient Pastures’, a project supported by funding from the Australian Government Department of Agriculture, Water and the Environment as part of its Rural R&D for Profit programme, Meat and Livestock Australia, Dairy Australia, Australian Wool Innovations Ltd., and the participating research organisations and farmer groups. JWM held an Australian Government Postgraduate Award (RTP) supplemented by a CSIRO top-up scholarship. The authors thank Graeme Blair for helpful comments on the manuscript. The authors also thank Calista McLachlan, Jane Carruthers and Leanne Lisle for technical assistance.
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McLachlan, J.W., Flavel, R.J., Guppy, C.N. et al. Root proliferation and phosphorus acquisition in response to stratification of soil phosphorus by two contrasting Trifolium subterraneum cultivars. Plant Soil 452, 233–248 (2020). https://doi.org/10.1007/s11104-020-04558-5
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DOI: https://doi.org/10.1007/s11104-020-04558-5