Linking root traits to superior phosphorus uptake and utilisation efficiency in three Fabales in the Core Cape Subregion, South Africa
Dunja MacAlister A , A. Muthama Muasya A and Samson B. M. Chimphango A B
+ Author Affiliations
- Author Affiliations
A Department of Biological Sciences, HW Pearson Building, University of Cape Town, Private Bag X3, Rondebosch, 7701, South Africa.
B Corresponding author. Email: samson.chimphango@uct.ac.za
Functional Plant Biology 45(7) 760-770 https://doi.org/10.1071/FP17209
Submitted: 29 November 2016 Accepted: 24 January 2018 Published: 20 February 2018
Abstract
In the low-P soil of the fynbos biome, plants have evolved several morphological and physiological P acquisition and use mechanisms, leading to variable uptake and use efficiencies. We expected that plants grown in low-P soils would exhibit greater P acquisition traits and hypothesised that Aspalathus linearis (Burm. f.) R. Dahlgren, a cluster-root-forming species adapted to drier and infertile soils, would be the most efficient at P acquisition compared with other species. Three fynbos Fabales species were studied: A. linearis and Podalyria calyptrata (Retz.) Willd, both legumes, and Polygala myrtifolia L., a nonlegume. A potted experiment was conducted where the species were grown in two soil types with high P (41.18 mg kg–1) and low P (9.79 mg kg–1). At harvest, biomass accumulation, foliar nutrients and P acquisition mechanisms were assessed. Polygala myrtifolia developed a root system with greater specific root length, root hair width and an average root diameter that exuded a greater amount of citrate and, contrary to the hypothesis, exhibited greater whole-plant P uptake efficiency. However, P. calyptrata had higher P use efficiency, influenced by N availability through N2 fixation. Specific root length, root length and root : shoot ratio were promising morphological traits for efficient foraging of P, whereas acid phosphatase exudation was the best physiological trait for solubilisation of P.
Additional keywords: Aspalathus linearis, P acquisition, Podalyria calyptrata, Polygala myrtifolia, root morphology.
References
Ae N, Arihara J, Okada K, Yoshihara T, Johansen C (1990) Phosphorus uptake by pigeon pea and its role in cropping systems of the Indian subcontinent. Science 248, 477–480.| Phosphorus uptake by pigeon pea and its role in cropping systems of the Indian subcontinent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXkslOitbw%3D&md5=87c8a1ccedaab5bec301aa29c2ac4585CAS |
Palic D, Claassens AS, Loock A, Hattingh D (1998) ‘Handbook of feeds and plant analysis.’ (Agricultural Laboratory Association of Southern Africa: Pretoria)
Allsopp N, Stock WD (1993) Mycorrhizal status of plants growing in the Cape Floristic Region, South Africa. Bothalia 23, 91–104.
Bloom AJ, Chapin FS, Mooney HA (1985) Resource limitation in plants – an economic analogy. Annual Review of Ecology and Systematics 16, 363–392.
| Resource limitation in plants – an economic analogy.Crossref | GoogleScholarGoogle Scholar |
Boulet FM, Lambers H (2005) Characterization of arbuscular mycorrhizal fungi colonization in cluster roots of Hakea verrucosa F. Muell (Proteaceae), and its effect on growth and nutrient acquisition in ultamafic soil. Plant and Soil 269, 357–367.
| Characterization of arbuscular mycorrhizal fungi colonization in cluster roots of Hakea verrucosa F. Muell (Proteaceae), and its effect on growth and nutrient acquisition in ultamafic soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1Oisr4%3D&md5=506fb8c843e9708b2118a93b0719528fCAS |
Bray RH, Kurtz LT (1945) Determination of total, organic and available forms of phosphorus in soils. Soil Science 59, 39–46.
| Determination of total, organic and available forms of phosphorus in soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaH2MXht1GjtA%3D%3D&md5=6acc2b80a298840f8b66e10684763b95CAS |
Brown G, Mitchell DT (1986) Influence of fire on the soil phosphorus status in sandplain lowland fynbos, south western Cape. South African Journal of Botany 52, 67–72.
| Influence of fire on the soil phosphorus status in sandplain lowland fynbos, south western Cape.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XlvV2qurc%3D&md5=829cd67f7ee6d2698d34a5b9bb90d7dfCAS |
Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant and Soil 320, 37–77.
| Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvFGjt7g%3D&md5=5c32f853d5f8357b024222abfd77643dCAS |
Cocks MP, Stock WD (2001) Field patterns of nodulation in fifteen Aspalathus species and their ecological role in the fynbos vegetation of southern Africa. Basic and Applied Ecology 2, 115–125.
| Field patterns of nodulation in fifteen Aspalathus species and their ecological role in the fynbos vegetation of southern Africa.Crossref | GoogleScholarGoogle Scholar |
Comas LH, Eissenstat DM (2009) Patterns in root trait variation among 25 co-existing North American forest species. New Phytologist 182, 919–928.
| Patterns in root trait variation among 25 co-existing North American forest species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3Mvgs1OhtQ%3D%3D&md5=8cad8bd113d43a6d035bd6c1c6943cb7CAS |
Craine JM, Lee WG, Bond WJ, Williams RJ, Johnson LC (2005) Environmental constraints on a global relationship among leaf and root traits of grasses. Ecology 86, 12–19.
| Environmental constraints on a global relationship among leaf and root traits of grasses.Crossref | GoogleScholarGoogle Scholar |
Davidson E (2008) Biogeochemistry: fixing forests. Nature Geoscience 1, 421–422.
| Biogeochemistry: fixing forests.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnvFCgsbc%3D&md5=40da7bc94ec185ae5dd60327ba1231e7CAS |
Eissenstat DM, Yanai RD (1997) The ecology of root lifespan. Advances in Ecological Research 27, 1–60.
| The ecology of root lifespan.Crossref | GoogleScholarGoogle Scholar |
Fageria NK, Moreira A, Moraes LAC, Moraes MF (2014) Root growth, nutrient uptake, and nutrient-use efficiency by roots of tropical legume cover crops as influenced by phosphorus fertilization. Communications in Soil Science and Plant Analysis 45, 555–569.
| Root growth, nutrient uptake, and nutrient-use efficiency by roots of tropical legume cover crops as influenced by phosphorus fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXotFyiug%3D%3D&md5=693b0ff509a7add41bc3cea196ec4fa8CAS |
Farrar JF, Gunn S (1996) ‘Effects of temperature and atmospheric carbon dioxide on source–sink relations in the context of climate change.’ (Marcel Dekker, New York)
Fitter A (1985) Functional significance of root morphology and root system architecture. In ‘Ecological interactions in soil’. (Eds Fitter AH, Atkinson D, Read DJ, Usher MB) pp. 87–106. (Blackwell Scientific: Oxford, UK)
Gahoonia TS, Nielsen NE (2004) Barley genotypes with root hairs sustain high grain yields in low-P field. Plant and Soil 262, 55–62.
| Barley genotypes with root hairs sustain high grain yields in low-P field.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtlGnsL8%3D&md5=3cc3667e8cdbbbe86a44ae1730fd6c2cCAS |
Gahoonia TS, Nielsen NE, Joshi PA, Jahoor A (2001) A root hairless barley mutant for elucidating genetics of root hairs and phosphorus uptake. Plant and Soil 235, 211–219.
| A root hairless barley mutant for elucidating genetics of root hairs and phosphorus uptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotFahurg%3D&md5=e7ad42f17905ce8c01f73402173bae75CAS |
Garau G, Yates RJ, Deiana P, Howieson JG (2009) Novel strains of Burkholderia have a role in nitrogen fixation with papilionoid herbaceous legumes adapted to acid, infertile soils. Soil Biology & Biochemistry 41, 125–134.
| Novel strains of Burkholderia have a role in nitrogen fixation with papilionoid herbaceous legumes adapted to acid, infertile soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVOis7vF&md5=ec431f592bfc380a74dda40c13c7bdc5CAS |
Hammond JP, Broadley MR, White PJ, King GJ, Bowen HC, Hayden R, Meacham MC, Mead A, Overs T, Spracklen WP, Greenwood DJ (2009) Shoot yield drives phosphorus use efficiency in Brassica oleracea and correlates with root architecture traits. Journal of Experimental Botany 60, 1953–1968.
| Shoot yield drives phosphorus use efficiency in Brassica oleracea and correlates with root architecture traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFSjtbY%3D&md5=436854802e441cea0fe61123c7b3b424CAS |
Hassen AI, Bopape FL, Habig J, Lamprecht SC (2012) Nodulation of rooibos (Aspalathus linearis Burm. f.), an indigenous South African legume, by members of both the α-Proteobacteria and β-Proteobacteria. Biology and Fertility of Soils 48, 295–303.
| Nodulation of rooibos (Aspalathus linearis Burm. f.), an indigenous South African legume, by members of both the α-Proteobacteria and β-Proteobacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjs1Cksbc%3D&md5=db5088ff6d64a0a3d05be04671b1bd15CAS |
Hawkins H-J, Hettasch H, Mesjasz-Przybylowicz J, Przybylowicz W, Cramer MD (2008) Phosphorus toxicity in the Proteaceae: a problem in post-agricultural lands. Scientia Horticulturae 117, 357–365.
| Phosphorus toxicity in the Proteaceae: a problem in post-agricultural lands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptVWitr4%3D&md5=0ba40a8b2ab758917530ec2142c2640cCAS |
Hedley MJ, Stewart JWB, Chauhan BS (1982) Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations. Soil Science Society of America Journal 46, 970–976.
| Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXjvFCl&md5=673f50f21fa8a08edd4cda4ab43ad48bCAS |
Hernández G, Ramírez M, Valdés-López O, Tesfaye M, Graham MA, Czechowski T, Schlereth A, Wandrey M, Erban A, Cheung F, Wu HC, Lara M, Town CD, Kopka J, Udvardi MK, Vance CP (2007) Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiology 144, 752–767.
| Phosphorus stress in common bean: root transcript and metabolic responses.Crossref | GoogleScholarGoogle Scholar |
Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root induced chemical changes: a review. Plant and Soil 237, 173–195.
| Bioavailability of soil inorganic P in the rhizosphere as affected by root induced chemical changes: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVWlsQ%3D%3D&md5=8c3f7f7470252fb035f6d405b277bd88CAS |
Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454, 327–330.
| A unifying framework for dinitrogen fixation in the terrestrial biosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXosFCqs7w%3D&md5=d854db07ecfb95524c924cb439eae036CAS |
Jones DL (1998) Organic acids in the rhizosphere – a critical review. Plant and Soil 205, 25–44.
| Organic acids in the rhizosphere – a critical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtlGjs78%3D&md5=543465e828b5722b5b8568ae0e6e3d64CAS |
Jungk A (2001) Root hairs and acquisition of plant nutrients from soil. Journal of Plant Nutrition and Soil Science 164, 121–129.
| Root hairs and acquisition of plant nutrients from soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtlCqtrk%3D&md5=adb6472897be20f4b1971d2e2a13117bCAS |
Koppelaar RHEM, Weikard HP (2013) Assessing phosphate rock depletion and phosphorus recycling options. Global Environmental Change 23, 1454–1466.
| Assessing phosphate rock depletion and phosphorus recycling options.Crossref | GoogleScholarGoogle Scholar |
Lambers H, Juniper D, Cawthray GR, Veneklaas EJ, Martínez-Ferri E (2002) The pattern of carboxylate exudation in Banksia grandis (Proteaceae) is affected by the form of phosphate added to the soil. Plant and Soil 238, 111–122.
| The pattern of carboxylate exudation in Banksia grandis (Proteaceae) is affected by the form of phosphate added to the soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Gru7g%3D&md5=fbb291439979571655ab84d6386f6168CAS |
Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Annals of Botany 98, 693–713.
| Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits.Crossref | GoogleScholarGoogle Scholar |
Lamont BB (1982) Mechanisms for enhancing nutrient uptake in plants, with particular reference to Mediterranean South Africa and Western Australia. Botanical Review 48, 597–689.
| Mechanisms for enhancing nutrient uptake in plants, with particular reference to Mediterranean South Africa and Western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXntVymtA%3D%3D&md5=edf6ab54c8d52d19c314a92c70f485ecCAS |
Lamont BB, Pérez-Fernández M (2016) Total growth and root-cluster production by legumes and proteas depends on rhizobacterial strain, host species and nitrogen level. Annals of Botany 118, 725–732.
| Total growth and root-cluster production by legumes and proteas depends on rhizobacterial strain, host species and nitrogen level.Crossref | GoogleScholarGoogle Scholar |
Lamont BB, Pérez‐Fernández M, Rodríguez‐Sánchez J (2014) Soil bacteria hold the key to root cluster formation. New Phytologist 206, 1156–1162.
| Soil bacteria hold the key to root cluster formation.Crossref | GoogleScholarGoogle Scholar |
Leigh J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytologist 181, 199–207.
| Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlaktL8%3D&md5=bbd9b116cbd5e64bc051c012d90b76aeCAS |
Lemaire B, Van Cauwenberghe J, Verstraete B, Chimphango S, Stirton C, Honnay O, Smets E, Sprent J, James EK, Muasya AM (2016) Characterization of the papilionoid–Burkholderia interaction in the fynbos biome: the diversity and distribution of beta-rhizobia nodulating Podalyria calyptrata (Fabaceae, Podalyrieae). Systematic and Applied Microbiology 39, 41–48.
| Characterization of the papilionoid–Burkholderia interaction in the fynbos biome: the diversity and distribution of beta-rhizobia nodulating Podalyria calyptrata (Fabaceae, Podalyrieae).Crossref | GoogleScholarGoogle Scholar |
Lynch JP, Lauchli A, Epstein E (1991) Vegetative growth of the common bean in response to phosphorus nutrition. Crop Science 31, 380–387.
| Vegetative growth of the common bean in response to phosphorus nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXisVKgurc%3D&md5=810ef5b4019a81a94be4a5d969b9639bCAS |
Maistry PM, Cramer MD, Chimphango SBM (2013) N and P co-limitation of N2-fixing and N-supplied fynbos legumes from the Cape Floristic Region. Plant and Soil 373, 217–228.
| N and P co-limitation of N2-fixing and N-supplied fynbos legumes from the Cape Floristic Region.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptVyktbg%3D&md5=83f3da3ee4e385251614b4beb64a32f1CAS |
Maistry PM, Muasya AM, Valentine AJ, Chimphango SBM (2015a) Increasing nitrogen supply stimulates phosphorus acquisition mechanisms in the fynbos species Aspalathus linearis. Functional Plant Biology 42, 52–62.
| Increasing nitrogen supply stimulates phosphorus acquisition mechanisms in the fynbos species Aspalathus linearis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFSns7jN&md5=86930fae9993f2bbe355189901a2ad1fCAS |
Maistry PM, Muasya AM, Valentine AJ, Chimphango SBM (2015b) Balanced allocation of organic acids and biomass for phosphorus and nitrogen demand in the fynbos legume Podalyria calyptrata. Journal of Plant Physiology 174, 16–25.
| Balanced allocation of organic acids and biomass for phosphorus and nitrogen demand in the fynbos legume Podalyria calyptrata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVanu7nM&md5=093655f85eeebdc446167a6389b3e9afCAS |
Manning J, Goldblatt P (2012) The Core Cape Subregion. In ‘Plants of the greater Cape Floristic Region 1: the core Cape flora’. (Eds Steenkamp Y, Germishuizen G) pp. 1–26. (South African National Biodiversity Institute: Pretoria)
Maseko S, Dakora FD (2013) Effects of nitrogen addition on litter decomposition, soil microbial biomass, and enzyme activities between leguminous and non-leguminous forests. South African Journal of Botany 89, 289–295.
| Effects of nitrogen addition on litter decomposition, soil microbial biomass, and enzyme activities between leguminous and non-leguminous forests.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1CqtbbP&md5=5aa0293f7fb88a6507bf9b548a5a1595CAS |
Mortimer PE, Archer E, Valentine AJ (2005) Mycorrhizal C costs and nutritional benefits in developing grapevines. Mycorrhiza 15, 159–165.
| Mycorrhizal C costs and nutritional benefits in developing grapevines.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M3ksFWisw%3D%3D&md5=4b2a8f6b6f817f910489619651dc5f6cCAS |
Nielsen KL, Eshel A, Lynch JP (2001) The effect of phosphorus availability on the carbon economy of contrasting common bean (Phaseolus vulgaris L.) genotypes. Journal of Experimental Botany 52, 329–339.
Non-Affiliated Soil Analysis Working Committee (1990) ‘Handbook of standard soil testing methods for advisory purposes.’ (Soil Science Society of South Africa, Pretoria)
Nuruzzaman M, Lambers H, Bolland MDA, Veneklaas EJ (2006) Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes. Plant and Soil 281, 109–120.
| Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xktlyhsbw%3D&md5=30e6e4b07e8b454c0c14b830d0bea8fcCAS |
Pang J, Ryan M, Tibbett M, Cawthray GR, Siddique KHM, Bolland MDA, Denton MD, Lambers H (2010) Variation in morphological and physiological parameters in herbaceous perennial legumes in response to phosphorus supply. Plant and Soil 331, 241–255.
| Variation in morphological and physiological parameters in herbaceous perennial legumes in response to phosphorus supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvVOhs70%3D&md5=d563a9d1248446303c9728b4308605f8CAS |
Pearse SJ, Veneklaas EJ, Cawthray GR, Bolland MDA, Lambers H (2006) Carboxylate release of wheat, canola and 11 grain legume species as affected by phosphorus status. Plant and Soil 288, 127–139.
| Carboxylate release of wheat, canola and 11 grain legume species as affected by phosphorus status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFaksL7F&md5=797238583f2d9e8d1b11c14a72fe92d5CAS |
Power SC, Cramer MD, Verboom GA, Chimphango SBM (2010) Does phosphate acquisition constrain legume persistence in the fynbos of the Cape Floristic Region? Plant and Soil 334, 33–46.
| Does phosphate acquisition constrain legume persistence in the fynbos of the Cape Floristic Region?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaqur7F&md5=0bf7bce0725c072f0bef375a8b1d65eaCAS |
Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant and Soil 274, 37–49.
| Phosphate acquisition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVWiurfJ&md5=b876d29ac81a946dcaacedede4fc8810CAS |
Rath M, Weber HC, Imhof S (2013) Morpho-anatomical and molecular characterization of the mycorrhizas of European Polygala species. Plant Biology 15, 548–557.
| Morpho-anatomical and molecular characterization of the mycorrhizas of European Polygala species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXosVKks7c%3D&md5=07674c4691324e16232ac81604647be6CAS |
Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant and Soil 321, 305–339.
| Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXos1enu7w%3D&md5=df9c47b97f082277c2038b8c3b84476bCAS |
Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant and Soil 349, 121–156.
| Plant and microbial strategies to improve the phosphorus efficiency of agriculture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFKntb3N&md5=09b1745be331a702f4f78071832bbdefCAS |
Rundel PW (1989) Ecological success in relation to plant form and function in the woody legumes. In ‘Advances in legume biology’. (Eds Stirton CH, Zarucchi JL) pp. 377–398. (Monographs in Systematic Botany from the Missouri Botanical Garden: St. Louis, MO)
Sanginga N, Lyasse O, Singh BB (2000) Phosphorus use efficiency and nitrogen balance of cowpea breeding lines in a low P soil of the derived savanna zone in West Africa. Plant and Soil 220, 119–128.
| Phosphorus use efficiency and nitrogen balance of cowpea breeding lines in a low P soil of the derived savanna zone in West Africa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXks1Kltr4%3D&md5=f789f77d6bdd4203051adeed21d12922CAS |
Shane MW, Cramer MD, Funayama-Noguchi S, Cawthray G, Millar HA, Day DA, Lambers H (2004) Developmental physiology of cluster root carboxylate synthesis and exudation in Harsh Hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase. Plant Physiology 135, 549–560.
| Developmental physiology of cluster root carboxylate synthesis and exudation in Harsh Hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkt12ms78%3D&md5=9b4c9c0c84144cf3b9687b5423e5f4a2CAS |
Shane MW, Cramer MD, Lambers H (2008) Root of edaphically controlled Proteaceae turnover on the Agulhas Plain, South Africa: phosphate uptake regulation and growth. Plant, Cell & Environment 31, 1825–1833.
| Root of edaphically controlled Proteaceae turnover on the Agulhas Plain, South Africa: phosphate uptake regulation and growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmt1yqsQ%3D%3D&md5=fe7d9689ddfc27b4e81f5d2e6b321e53CAS |
Skene KR (1998) Cluster roots: some ecological considerations. Journal of Ecology 86, 1060–1064.
| Cluster roots: some ecological considerations.Crossref | GoogleScholarGoogle Scholar |
Sommers LE, Nelson DW (1972) Determination of total phosphorus in soils: a rapid perchloric acid digestion procedure. Soil Science Society of America Journal 36, 902–904.
| Determination of total phosphorus in soils: a rapid perchloric acid digestion procedure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXjslKmsQ%3D%3D&md5=73c516e93b1bfc7a7ab87de2f2b28f5fCAS |
Stock WD, Verboom GA (2012) Phylogenetic ecology of foliar N and P concentrations and N : P ratios across Mediterranean-type ecosystems. Global Ecology and Biogeography 21, 1147–1156.
| Phylogenetic ecology of foliar N and P concentrations and N : P ratios across Mediterranean-type ecosystems.Crossref | GoogleScholarGoogle Scholar |
Tang C, Han XZ, Qiao YF, Zheng SJ (2009) Phosphorus deficiency does not enhance proton release by roots of soybean [Glycine max (L.) Merr.]. Environmental and Experimental Biology 67, 228–234.
Treseder KK, Vitousek PM (2001) Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82, 946–954.
| Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests.Crossref | GoogleScholarGoogle Scholar |
Turner BL, Paphazy MJ, Haygarth PM, McKelvie ID (2002) Inositol phosphatises in the environment. Philosophical Transactions of the Royal Society of London 357, 449–469.
| Inositol phosphatises in the environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVSls7k%3D&md5=a0cd632b42c6f1295f16af5770d3da33CAS |
van der Bank M, van der Bank FH, van Wyk B-E (1999) Evolution of sprouting versus seeding in Aspalathus linearis. Plant Systematics and Evolution 219, 27–38.
| Evolution of sprouting versus seeding in Aspalathus linearis.Crossref | GoogleScholarGoogle Scholar |
Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a non-renewable resource. New Phytologist 157, 423–447.
| Phosphorus acquisition and use: critical adaptations by plants for securing a non-renewable resource.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisF2gu70%3D&md5=964eb8503e1c19512772c381545d0555CAS |
Vandamme E, Renkens M, Pypers P, Smolders E, Vanlauwe B, Merckx R (2013) Root hairs explain P uptake efficiency of soybean genotypes grown in a P-deficient Ferralsol. Plant and Soil 369, 269–282.
| Root hairs explain P uptake efficiency of soybean genotypes grown in a P-deficient Ferralsol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVyqtrzL&md5=db67ee31d40b83789d3c2226c988f165CAS |
Veneklaas EJ, Stevens J, Cawthray GR, Turner S, Grigg AM, Lambers H (2003) Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant and Soil 248, 187–197.
| Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtFCqs7k%3D&md5=f8bf177fe6615c8036509a28301d9842CAS |
Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science 37, 29–38.
| An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaA2cXitlGmug%3D%3D&md5=053fae3a18cd568969dbaf9d6bb900b1CAS |
Watt M, Evans JR (1999) Proteoid roots. Physiology and development. Plant Physiology 121, 317–323.
| Proteoid roots. Physiology and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmslKjs7Y%3D&md5=710e48e175c4cda1991a99106f9378e0CAS |
