Intrinsic root morphology determines the phosphorus acquisition efficiency of five annual pasture legumes irrespective of mycorrhizal colonisation
Jonathan W. McLachlan A B D , Adeline Becquer B C , Rebecca E. Haling B , Richard J. Simpson B , Richard J. Flavel A and Chris N. Guppy AA University of New England, School of Environmental and Rural Science, Armidale, NSW 2351, Australia.
B CSIRO Agriculture and Food, GPO Box 1700, Canberra, ACT 2601, Australia.
C INRA, UMR EcoandSols, 2 Place Pierre Viala, 34060 Montpellier, Cedex 1, France.
D Corresponding author. Email: jmclach7@une.edu.au
Functional Plant Biology 48(2) 156-170 https://doi.org/10.1071/FP20007
Submitted: 7 January 2020 Accepted: 13 August 2020 Published: 11 September 2020
Abstract
Mycorrhizal fungi are ubiquitous in agroecosystems and form symbiotic associations that contribute to the phosphorus (P) acquisition of many plants. The impact of mycorrhizas is most pronounced in P-deficient soil and commonly involves modifications to the root morphology of colonised plants. However, the consequences of mycorrhizal colonisation on root acclimation responses to P stress are not well described. Five annual pasture legumes, with differing root morphologies, were grown to determine the effect of mycorrhizal colonisation on shoot yield, root morphology and P uptake. Micro-swards of each legume were established in pots filled with a topsoil layer that had been amended with five rates of P fertiliser. The topsoil overlaid a low-P subsoil that mimicked the stratification of P that occurs under pasture. Mycorrhizal colonisation improved P acquisition and shoot yield in the low-P soil treatments, but did not reduce the critical external P requirement of the legumes for near-maximum yield. The yield responses of the mycorrhizal plants were associated with reduced dry matter allocation to topsoil roots, which meant that the P acquisition benefit associated with mycorrhizal colonisation was not additive in the P-deficient soil. The contribution of the mycorrhizal association to P acquisition was consistent among the legumes when they were compared at an equivalent level of plant P stress, and was most pronounced below a P stress index of ~0.5. The intrinsic root morphology of the legumes determined their differences in P-acquisition efficiency irrespective of mycorrhizal colonisation.
Additional keywords: critical external P requirement, French serradella, Ornithopus sativus, pasture legume, phosphorus acquisition, root acclimation, subterranean clover, Trifolium subterraneum.
References
Abbott LK, Robson AD (1977) Growth stimulation of subterranean clover with vesicular arbuscular mycorrhizas. Australian Journal of Agricultural Research 28, 639–649.| Growth stimulation of subterranean clover with vesicular arbuscular mycorrhizas.Crossref | GoogleScholarGoogle Scholar |
Abbott LK, Robson AD, Hall IR (1983) Introduction of vesicular arbuscular mycorrhizal fungi into agricultural soils. Australian Journal of Agricultural Research 34, 741–749.
| Introduction of vesicular arbuscular mycorrhizal fungi into agricultural soils.Crossref | GoogleScholarGoogle Scholar |
Bolan NS, Robson AD, Barrow NJ (1987) Effects of vesicular-arbuscular mycorrhiza on the availability of iron phosphates to plants. Plant and Soil 99, 401–410.
| Effects of vesicular-arbuscular mycorrhiza on the availability of iron phosphates to plants.Crossref | GoogleScholarGoogle Scholar |
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.
| Sample preparation and scanning protocol for computerised analysis of root length and diameter.Crossref | GoogleScholarGoogle Scholar |
Brouwer R (1962) Nutritive influences on the distribution of dry matter in the plant. Netherlands Journal of Agricultural Science 10, 399–408.
| Nutritive influences on the distribution of dry matter in the plant.Crossref | GoogleScholarGoogle Scholar |
Burkitt LL, Moody PW, Gourley CJP, Hannah MC (2002) A simple phosphorus buffering index for Australian soils. Australian Journal of Soil Research 40, 497–513.
| A simple phosphorus buffering index for Australian soils.Crossref | GoogleScholarGoogle Scholar |
Burkitt LL, Sale PWG, Gourley CJP (2008) Soil phosphorus buffering measures should not be adjusted for current phosphorus fertility. Australian Journal of Soil Research 46, 676–685.
| Soil phosphorus buffering measures should not be adjusted for current phosphorus fertility.Crossref | GoogleScholarGoogle Scholar |
Colwell JD (1963) The estimation of the phosphorus fertilizer requirements of wheat in southern New South Wales by soil analysis. Australian Journal of Experimental Agriculture 3, 190–197.
| The estimation of the phosphorus fertilizer requirements of wheat in southern New South Wales by soil analysis.Crossref | GoogleScholarGoogle Scholar |
Crawley MJ (2013) ‘The R book.’ (John Wiley & Sons Ltd: Chichester, UK)
Cruz-Paredes C, Svenningsen NB, Nybroe O, Kjoller R, Froslev TG, Jakobsen I (2019) Suppression of arbuscular mycorrhizal fungal activity in a diverse collection of non-cultivated soils. FEMS Microbiology Ecology 95, 1–10.
| Suppression of arbuscular mycorrhizal fungal activity in a diverse collection of non-cultivated soils.Crossref | GoogleScholarGoogle Scholar |
de Mendiburu F (2019) agricolae: Statistical procedures for agricultural research. R package version 1.3-0. Available at https://CRAN.R-project.org/package=agricolae [Verified 18 August 2020]
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 Phytologist 206, 1247–1260.
| Integrated plant phenotypic responses to contrasting above- and below-ground resources: key roles of specific leaf area and root mass fraction.Crossref | GoogleScholarGoogle Scholar | 25783781PubMed |
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.). The Journal of Agricultural Science 153, 1069–1083.
| Hotspots and gaps in the world collection of subterranean clover (Trifolium subterraneum L.).Crossref | GoogleScholarGoogle Scholar |
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytologist 84, 489–500.
| An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots.Crossref | GoogleScholarGoogle Scholar |
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 and Soil 407, 67–79.
| Growth and root dry matter allocation by pasture legumes and a grass with contrasting external critical phosphorus requirements.Crossref | GoogleScholarGoogle Scholar |
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. Functional Plant Biology 43, 815–826.
| Root morphological traits that determine phosphorus-acquisition efficiency and critical external phosphorus requirement in pasture species.Crossref | GoogleScholarGoogle Scholar | 32480506PubMed |
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 and Soil 424, 539–554.
| Differences in nutrient foraging among Trifolium subterraneum cultivars deliver improved P-acquisition efficiency.Crossref | GoogleScholarGoogle Scholar |
Hodge A (2006) Plastic plants and patchy soils. Journal of Experimental Botany 57, 401–411.
| Plastic plants and patchy soils.Crossref | GoogleScholarGoogle Scholar | 16172138PubMed |
Irving GCJ, McLaughlin MJ (1990) A rapid and simple field test for phosphorus in Olsen and Bray No. 1 extracts of soil. Communications in Soil Science and Plant Analysis 21, 2245–2255.
| A rapid and simple field test for phosphorus in Olsen and Bray No. 1 extracts of soil.Crossref | GoogleScholarGoogle Scholar |
Isbell RF (1996) ‘The Australian soil classification.’ (CSIRO Publishing: Melbourne, Vic., Australia)
Jackson NE, Franklin RE, Miller RH (1972) Effects of vesicular-arbuscular mycorrhizae on growth and phosphorus content of three agronomic crops. Soil Science Society of America Journal 36, 64–67.
| Effects of vesicular-arbuscular mycorrhizae on growth and phosphorus content of three agronomic crops.Crossref | GoogleScholarGoogle Scholar |
Jakobsen I, Abbott LK, Robson AD (1992a) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots. New Phytologist 120, 371–380.
| External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots.Crossref | GoogleScholarGoogle Scholar |
Jakobsen I, Abbott LK, Robson AD (1992b) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 2. Hyphal transport of 32P over defined distances. New Phytologist 120, 509–516.
| External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 2. Hyphal transport of 32P over defined distances.Crossref | GoogleScholarGoogle Scholar |
Jakobsen I, Gazey C, Abbott LK (2001) Phosphate transport by communities of arbuscular mycorrhizal fungi in intact soil cores. New Phytologist 149, 95–103.
| Phosphate transport by communities of arbuscular mycorrhizal fungi in intact soil cores.Crossref | GoogleScholarGoogle Scholar |
Jakobsen I, Chen B, Munkvold L, Lundsgaard T, Zhu Y (2005) Contrasting phosphate acquisition of mycorrhizal fungi with that of root hairs using the root hairless barley mutant. Plant, Cell & Environment 28, 928–938.
| Contrasting phosphate acquisition of mycorrhizal fungi with that of root hairs using the root hairless barley mutant.Crossref | GoogleScholarGoogle Scholar |
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. Functional Plant Biology 44, 552–562.
| Plants in constrained canopy micro-swards compensate for decreased root biomass and soil exploration with increased amounts of rhizosphere carboxylates.Crossref | GoogleScholarGoogle Scholar | 32480587PubMed |
Lazarevic B, Losak T, Manschadi AM (2018) Arbuscular mycorrhizae modify winter wheat root morphology and alleviate phosphorus deficit stress. Plant, Soil and Environment 64, 47–52.
| Arbuscular mycorrhizae modify winter wheat root morphology and alleviate phosphorus deficit stress.Crossref | GoogleScholarGoogle Scholar |
Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant and Soil 269, 45–56.
| Rhizoeconomics: carbon costs of phosphorus acquisition.Crossref | GoogleScholarGoogle Scholar |
Mai W, Xue X, Feng G, Yang R, Tian C (2019) Arbuscular mycorrhizal fungi – 15-fold enlargement of the soil volume of cotton roots for phosphorus uptake in intensive planting conditions. European Journal of Soil Biology 90, 31–35.
| Arbuscular mycorrhizal fungi – 15-fold enlargement of the soil volume of cotton roots for phosphorus uptake in intensive planting conditions.Crossref | GoogleScholarGoogle Scholar |
McLachlan JW, Haling RE, Simpson RJ, Li X, Flavel RJ, Guppy CN (2019) Variation in root morphology and P acquisition efficiency among Trifolium subterraneum genotypes. Crop and Pasture Science 70, 1015–1032.
| Variation in root morphology and P acquisition efficiency among Trifolium subterraneum genotypes.Crossref | GoogleScholarGoogle Scholar |
McLachlan JW, Flavel RJ, Guppy CN, Simpson RJ, Haling RE (2020) Root proliferation and phosphorus acquisition in response to stratification of soil phosphorus by two contrasting Trifolium subterraneum cultivars. Plant and Soil 452, 233–248.
| Root proliferation and phosphorus acquisition in response to stratification of soil phosphorus by two contrasting Trifolium subterraneum cultivars.Crossref | GoogleScholarGoogle Scholar |
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 and Soil 349, 69–87.
| The chemical nature of P accumulation in agricultural soils - implications for fertiliser management and design: an Australian perspective.Crossref | GoogleScholarGoogle Scholar |
Mosse B, Powell CL, Hayman DS (1976) Plant growth responses to vesicular-arbuscular mycorrhizae. IX. Interactions between VA mycorrhiza, rock phosphate and symbiotic nitrogen fixation. New Phytologist 76, 331–342.
| Plant growth responses to vesicular-arbuscular mycorrhizae. IX. Interactions between VA mycorrhiza, rock phosphate and symbiotic nitrogen fixation.Crossref | GoogleScholarGoogle Scholar |
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 and Pasture Science 64, 312–346.
| Genetic improvement of subterranean clover (Trifolium subterraneum L.). 1. Germplasm, traits and future prospects.Crossref | GoogleScholarGoogle Scholar |
Nielsen KL, Bouma TJ, Lynch JP, Eissenstat DM (1998) Effects of phosphorus availability and vesicular-arbuscular mycorrhizas on the carbon budget of common bean (Phaseolus vulgaris). New Phytologist 139, 647–656.
| Effects of phosphorus availability and vesicular-arbuscular mycorrhizas on the carbon budget of common bean (Phaseolus vulgaris).Crossref | GoogleScholarGoogle Scholar |
Ozanne PG, Keay J, Biddiscombe EF (1969) The comparative applied phosphate requirements of eight annual pasture species. Australian Journal of Agricultural Research 20, 809–818.
| The comparative applied phosphate requirements of eight annual pasture species.Crossref | GoogleScholarGoogle Scholar |
Pairunan AK, Robson AD, Abbott LK (1980) The effectiveness of vesicular-arbuscular mycorrhizas in increasing growth and phosphorus uptake of subterranean clover from phosphorus sources of different solubilities. New Phytologist 84, 327–338.
| The effectiveness of vesicular-arbuscular mycorrhizas in increasing growth and phosphorus uptake of subterranean clover from phosphorus sources of different solubilities.Crossref | GoogleScholarGoogle Scholar |
Poorter H, Fiorani F, Stitt M, Schurr U, Finck A, Gibon Y, Usadel B, Munns R, Atkin OK, Tardieu F, Pons TL (2012) The art of growing plants for experimental purposes: a practical guide for the plant biologist. Functional Plant Biology 39, 821–838.
| The art of growing plants for experimental purposes: a practical guide for the plant biologist.Crossref | GoogleScholarGoogle Scholar | 32480833PubMed |
R Core Team (2018) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at http://www.R-project.org/ [Verified 18 August 2020]
Raven JA, Lambers H, Smith SE, Westoby M (2018) Costs of acquiring phosphorus by vascular land plants: patterns and implications for plant coexistence. New Phytologist 217, 1420–1427.
| Costs of acquiring phosphorus by vascular land plants: patterns and implications for plant coexistence.Crossref | GoogleScholarGoogle Scholar | 29292829PubMed |
Rayment GE, Lyons DJ (2011) ‘Soil chemical methods – Australiasia.’ (CSIRO Publishing: Melbourne, Vic., Australia)
Ryan M, Ash J (1999) Effects of phosphorus and nitrogen on growth of pasture plants and VAM fungi in SE Australian soils with contrasting fertiliser histories (conventional and biodynamic). Agriculture, Ecosystems & Environment 73, 51–62.
| Effects of phosphorus and nitrogen on growth of pasture plants and VAM fungi in SE Australian soils with contrasting fertiliser histories (conventional and biodynamic).Crossref | GoogleScholarGoogle Scholar |
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). Applied Soil Ecology 98, 221–232.
| High variation in the percentage of root length colonised by arbuscular mycorrhizal fungi among 139 lines representing the species subterranean clover (Trifolium subterraneum).Crossref | GoogleScholarGoogle Scholar |
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 and Pasture Science 69, 174–182.
| Intrinsic capacity for nutrient foraging predicts critical external phosphorus requirement of 12 pasture legumes.Crossref | GoogleScholarGoogle Scholar |
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 and Pasture Science 70, 1080–1096.
| Field benchmarking of the critical external phosphorus requirements of pasture legumes for southern Australia.Crossref | GoogleScholarGoogle Scholar |
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. Nature Methods 9, 676–682.
| Fiji: an open-source platform for biological-image analysis.Crossref | GoogleScholarGoogle Scholar | 22743772PubMed |
Schweiger PF, Robson AD, Barrow NJ (1995) Root hair length determines beneficial effect of a Glomus species on shoot growth of some pasture species. New Phytologist 131, 247–254.
| Root hair length determines beneficial effect of a Glomus species on shoot growth of some pasture species.Crossref | GoogleScholarGoogle Scholar |
Silsbury JH, Fukai S (1977) Effects of sowing time and sowing density on the growth of subterranean clover at Adelaide. Australian Journal of Agricultural Research 28, 427–440.
| Effects of sowing time and sowing density on the growth of subterranean clover at Adelaide.Crossref | GoogleScholarGoogle Scholar |
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. Agriculture, Ecosystems & Environment 212, 263–277.
| Management of soil phosphorus fertility determines the phosphorus budget of a temperate grazing system and is the key to improving phosphorus efficiency.Crossref | GoogleScholarGoogle Scholar |
Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology 133, 16–20.
| Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses.Crossref | GoogleScholarGoogle Scholar | 12970469PubMed |
Svenningsen NB, Watts-Williams SJ, Joner EJ, Battini F, Efthymiou A, Cruz-Paredes C, Nybroe O, Jakobsen I (2018) Suppression of the activity of arbuscular mycorrhizal fungi by the soil microbiota. ISME Journal 12, 1296–1307.
| Suppression of the activity of arbuscular mycorrhizal fungi by the soil microbiota.Crossref | GoogleScholarGoogle Scholar | 29382946PubMed |
Tran BTT, Watts-Williams SJ, Cavagnaro TR (2019) Impact of an arbuscular mycorrhizal fungus on the growth and nutrition of fifteen crop and pasture plant species. Functional Plant Biology 46, 732–742.
| Impact of an arbuscular mycorrhizal fungus on the growth and nutrition of fifteen crop and pasture plant species.Crossref | GoogleScholarGoogle Scholar | 31092308PubMed |
Unger S, Friede M, Hundacker J, Volkmar K, Beyschlag W (2016) Allocation trade-off between root and mycorrhizal surface defines nitrogen and phosphorus relations in 13 grassland species. Plant and Soil 407, 279–292.
| Allocation trade-off between root and mycorrhizal surface defines nitrogen and phosphorus relations in 13 grassland species.Crossref | GoogleScholarGoogle Scholar |
Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Applied and Environmental Microbiology 64, 5004–5007.
| Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar | 9835596PubMed |
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 and Forage Science 72, 93–103.
| Variation in root traits associated with nutrient foraging among temperate pasture legumes and grasses.Crossref | GoogleScholarGoogle Scholar |
Zhu YG, Smith FA, Smith SE (2003) Phosphorus efficiencies and responses of barley (Hordeum vulgare L.) to arbuscular mycorrhizal fungi grown in highly calcareous soil. Mycorrhiza 13, 93–100.
| Phosphorus efficiencies and responses of barley (Hordeum vulgare L.) to arbuscular mycorrhizal fungi grown in highly calcareous soil.Crossref | GoogleScholarGoogle Scholar | 12682831PubMed |