Root morphological traits that determine phosphorus-acquisition efficiency and critical external phosphorus requirement in pasture species
Rebecca E. Haling A D , Zongjian Yang A , Natalie Shadwell A , Richard A. Culvenor A , Adam Stefanski A , Megan H. Ryan B , Graeme A. Sandral C , Daniel R. Kidd B , Hans Lambers B and Richard J. Simpson A
+ Author Affiliations
- Author Affiliations
A CSIRO Agriculture, GPO Box 1600, Canberra, ACT 2601, Australia.
B School of Plant Biology and Institute of Agriculture, The University of Western Australia, Crawley, WA 6009, Australia.
C Department of Primary Industries, Wagga Wagga Agricultural Institute, Pine Gully Road, Wagga Wagga, NSW 2650, Australia.
D Corresponding author. Email: rebecca.haling@csiro.au
Functional Plant Biology 43(9) 815-826 https://doi.org/10.1071/FP16037
Submitted: 28 January 2016 Accepted: 20 April 2016 Published: 7 June 2016
Abstract
Annual pasture legume species can vary more than 3-fold in their critical external phosphorus (P) requirement (i.e. P required for 90% of maximum yield). In this work we investigated the link between root morphology, P acquisition and critical external P requirement among pasture species. The root morphology acclimation of five annual pasture legumes and one grass species to low soil P availability was assessed in a controlled-environment study. The critical external P requirement of the species was low (Dactylis glomerata L., Ornithopus compressus L., Ornithopus sativus Brot.), intermediate (Biserrula pelecinus L., Trifolium hirtum All.) or high (Trifolium subterraneum L.). Root hair cylinder volumes (a function of root length, root hair length and average root diameter) were estimated in order to assess soil exploration and its impact on P uptake. Most species increased soil exploration in response to rates of P supply near or below their critical external P requirement. The legumes differed in how they achieved their maximum root hair cylinder volume. The main variables were high root length density, long root hairs and/or high specific root length. However, total P uptake per unit surface area of the root hair cylinder was similar for all species at rates of P supply below critical P. Species that maximised soil exploration by root morphology acclimation were able to prolong access to P in moderately P-deficient soil. However, among the species studied, it was those with an intrinsic capacity for a high root-hair-cylinder surface area (i.e. long roots and long root hairs) that achieved the lowest critical P requirement.
Additional keywords: cocksfoot, orchard grass, phosphorus deficiency, phosphorus-use efficiency, rose clover, serradella, subterranean clover.
References
Barber SA (1984) ‘Soil nutrient bioavailability.’ (Wiley: New York)Blair GJ, Cordero S (1978) Phosphorus efficiency of three annual legumes. Plant and Soil 50, 387–398.
| Phosphorus efficiency of three annual legumes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXlslykurg%3D&md5=486a59855b48f0a5a01a117e7935c6eaCAS |
Bolland MDA, Paynter BH (1992) Comparative responses of annual pasture legume species to superphosphate applications in medium and high rainfall areas of Western Australia. Fertilizer Research 31, 21–33.
| Comparative responses of annual pasture legume species to superphosphate applications in medium and high rainfall areas of Western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XitlClsrs%3D&md5=23dad48600ebe19a862b5ba0fbda605aCAS |
Brouwer R (1962) Distribution of dry matter in the plant. Netherlands Journal of Agricultural Science 10, 361–376.
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 | 1:CAS:528:DC%2BD38Xks1eksL0%3D&md5=c3bc4565f276f186733ce8a47ddb5e61CAS |
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 | 1:CAS:528:DC%2BD1cXhsVCms7%2FF&md5=f3adedc22e00c0c36ce61a3bbe7fc613CAS |
Colwell JD (1963) The estimation of the phosphorus fertiliser requirements of wheat in southern New South Wales by soil analysis. Australian Journal of Experimental Agriculture 3, 190–197.
| The estimation of the phosphorus fertiliser requirements of wheat in southern New South Wales by soil analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2cXnvVOhsQ%3D%3D&md5=9f8b44a47d39199d458ae146e73418b6CAS |
Evans PS (1977) Comparative root morphology of some pasture grasses and clovers. New Zealand Journal of Agricultural Research 20, 331–335.
| Comparative root morphology of some pasture grasses and clovers.Crossref | GoogleScholarGoogle Scholar |
Föhse D, Claassen N, Jungk A (1991) Phosphorus efficiency of plants II. Significance of root radius, root hairs and cation–anion balance for phosphorus influx in seven plant species. Plant and Soil 132, 261–272.
| Phosphorus efficiency of plants II. Significance of root radius, root hairs and cation–anion balance for phosphorus influx in seven plant species.Crossref | GoogleScholarGoogle Scholar |
Gahoonia TS, Nielsen NE (1997) Variation in root hairs of barley cultivars doubled soil phosphorus uptake. Euphytica 98, 177–182.
| Variation in root hairs of barley cultivars doubled soil phosphorus uptake.Crossref | GoogleScholarGoogle Scholar |
Gahoonia TS, Nielsen NE (2003) Phosphorus (P) uptake and growth of a root hairless barley mutant (bald root barley, brb) and wild type in low- and high-P soils. Plant, Cell & Environment 26, 1759–1766.
| Phosphorus (P) uptake and growth of a root hairless barley mutant (bald root barley, brb) and wild type in low- and high-P soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptlaht7c%3D&md5=25cf86ce1a848618c6cbd043a985bc1eCAS |
Gerke J (2015) The acquisition of phosphate by higher plants: effect of carboxylate release by the roots. A critical review. Journal of Plant Nutrition and Soil Science 178, 351–364.
| The acquisition of phosphate by higher plants: effect of carboxylate release by the roots. A critical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXntFCjsbk%3D&md5=265e70584b8fe4e4d21df1777adc3cf5CAS |
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 (2016) Growth and root dry matter allocation by plants with contrasting external critical phosphorus requirements. Plant and Soil
| Growth and root dry matter allocation by plants with contrasting external critical phosphorus requirements.Crossref | GoogleScholarGoogle Scholar |
Hill JO, Simpson RJ, Moore AD, Chapman DF (2006) Morphology and response of roots of pasture species to phosphorus and nitrogen nutrition. Plant and Soil 286, 7–19.
| Morphology and response of roots of pasture species to phosphorus and nitrogen nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xps1Wju7w%3D&md5=45d75b68139a05b12eb3945be89ba700CAS |
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 | 1:CAS:528:DyaK3MXisVKgs70%3D&md5=20f201ca31c075fd468f579b8b1e2c3bCAS |
Isbell RF (1996) ‘The Australian soil classification.’ (CSIRO Publishing: Melbourne)
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 and Soil 402, 77–89.
| Rhizosphere carboxylates and morphological root traits in pasture legumes and grasses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVSksbnF&md5=92aa1c43a37e34f1a342ca0636fe9c39CAS |
Lambers H, Plaxton WC (2015) Phosphorus: back to the roots. In ‘Annual plant reviews. Vol. 48: Phosphorus metabolism in plants’. pp. 3–22. (Wiley-Blackwell Publishing: Chicester, UK)
Lynch JP, Brown KM (2001) Topsoil foraging – an architectural adaptation of plants to low phosphorus availability. Plant and Soil 237, 225–237.
| Topsoil foraging – an architectural adaptation of plants to low phosphorus availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVWltA%3D%3D&md5=15315f430f8290e2e5d64830fe0b8034CAS |
Ma Z, Walk TC, Marcus A, Lynch JP (2001) Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: a modeling approach. Plant and Soil 236, 221–235.
| Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: a modeling approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptlKhu74%3D&md5=d1020038caadb124f6563e51c2ad11c4CAS |
Ozanne PG, Keay J, Biddiscombe EF (1969) Comparative applied phosphate requirements of eight annual pasture species. Australian Journal of Agricultural Research 20, 809–818.
| Comparative applied phosphate requirements of eight annual pasture species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3cXmsF2ntA%3D%3D&md5=b4874aebb70719946c4f7c1b02e07533CAS |
Ozanne PG, Howes KMW, Petch A (1976) Comparative phosphate requirements of four annual pastures and two crops. Australian Journal of Agricultural Research 27, 479–488.
| Comparative phosphate requirements of four annual pastures and two crops.Crossref | GoogleScholarGoogle Scholar |
Paynter BH (1990) Comparative phosphate requirements of yellow serradella (Ornithopus compressus), burr medic (Medicago polymorpha var brevispina) and subterranean clover (Trifolium subterraneum). Australian Journal of Experimental Agriculture 30, 507–514.
| Comparative phosphate requirements of yellow serradella (Ornithopus compressus), burr medic (Medicago polymorpha var brevispina) and subterranean clover (Trifolium subterraneum).Crossref | GoogleScholarGoogle Scholar |
Rayment GE, Lyons DJ (2011) ‘Soil chemical methods – Australasia.’ (CSIRO Publishing: Melbourne)
Ryser P, Eek L (2000) Consequences of phenotypic plasticity vs. interspecific differences in leaf and root traits for acquisition of aboveground and belowground resources. American Journal of Botany 87, 402–411.
| Consequences of phenotypic plasticity vs. interspecific differences in leaf and root traits for acquisition of aboveground and belowground resources.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3Mngs1KhtQ%3D%3D&md5=e6155ba6ba0c1d48104019db028d4420CAS | 10719001PubMed |
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 |
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 and Pasture Science 65, 556–575.
| Pasture plants and soil fertility management to improve the efficiency of phosphorus fertiliser use in temperate grassland systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVyit7bK&md5=401c512647225ce2c90aea1071f84a34CAS |
Simpson R, Stefanski A, Marshall D, Moore A, Richardson A (2015) Management of soil phosphorus fertility determines the phosphorus budget of a temperate grazing system and is the key to improving phosphorus-balance 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-balance efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1Ogs7vM&md5=aa00b79e127c1b14b3a67df1ba7444e2CAS |
Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Applied and Environmental Microbiology 64, 5004–5007.
Wahl S, Ryser P, Edwards PJ (2001) Phenotypic plasticity of grass root anatomy in response to light intensity and nutrient supply. Annals of Botany 88, 1071–1078.
| Phenotypic plasticity of grass root anatomy in response to light intensity and nutrient supply.Crossref | GoogleScholarGoogle Scholar |
Yang Z, Culvenor R, Haling R, Stefanski A, Ryan M, Sandral G, Kidd D, Lambers H, Simpson R (2015) Variation in root traits associated with nutrient foraging amongst temperate pasture legumes and grasses. Grass and Forage Science
| Variation in root traits associated with nutrient foraging amongst temperate pasture legumes and grasses.Crossref | GoogleScholarGoogle Scholar |
