Is there a critical level of shoot phosphorus concentration for cluster-root formation in Lupinus albus?
Haigang Li A , Jianbo Shen A D , Fusuo Zhang A , Caixian Tang B and Hans Lambers CA Department of Plant Nutrition, Key Laboratory of Plant–Soil Interaction (Ministry of Education), China Agricultural University, Beijing 100094, China.
B Department of Agricultural Sciences, La Trobe University, Bundoora, Vic. 3086, Australia.
C School of Plant Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
D Corresponding author. Email: jbshen@cau.edu.cn
Functional Plant Biology 35(4) 328-336 https://doi.org/10.1071/FP07222
Submitted: 17 September 2007 Accepted: 4 April 2008 Published: 3 June 2008
Abstract
This study examined the effects of localised phosphorus (P) supply on cluster-root formation and citrate exudation in white lupin (Lupinus albus L. cv. Kiev Mutant). White lupin plants were grown in nutrient solutions with a range of P supplies in a split-root system with one root half deprived of P and the other root supplied with 0, 2, 5, 8, 10 or 75 μm P. Plants were also grown in soil with or without organic matter added to the top layer. The proportion of cluster roots as a percentage of the total root biomass decreased similarly on both root halves with increasing P supply in the hydroponic experiments. More than 18% of the P taken up by the P-supplied root halves was incorporated into the P-deprived halves. Irrespective of the P supply or organic matter addition in the experiments, the proportion of cluster roots and the rate of citrate exudation decreased sharply with increasing P concentration in the shoots up to a critical level of 2–3 mg P g–1 dry weight. In contrast, the rate of proton release was higher in P-deprived root halves than in P-supplied ones. The formation of cluster roots is regulated by shoot P concentration with a critical level of 2–3 mg g–1. Citrate exudation is predominantly governed by shoot P status, whereas proton release strongly responds to local P supply.
Additional keywords: citrate exudation, localised P deficiency, proton release, split-root system.
Acknowledgements
This study was supported by the National Basic Research Program (973-2007CB109302), the National Natural Science Foundation of China (No. 30471033), the Program for New Century Excellent Talents in University (No. NCET-06-0112) and the Program for Changjiang Scholar and Innovation Research Team in University (No. IRT0511) of China. We thank Professor Zed Rengel (The University of Western Australia) for comments on the manuscript.
Dinkelaker B,
Römheld V, Marschner H
(1989) Citric acid excretion precipitation of calcium in the rhizosphere of white lupin (Lupinus albus L.). Plant, Cell & Environment 12, 285–292.
| Crossref | GoogleScholarGoogle Scholar |
Dinkelaker B,
Hengeler C, Marschner H
(1995) Distribution and function of proteoid roots and other root clusters. Botanica Acta 108, 183–200.
Drew MC
(1975) Comparison of the effects of localized supply of phosphorus, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. The New Phytologist 75, 479–490.
| Crossref | GoogleScholarGoogle Scholar |
Drew MC, Saker LR
(1978) Nutrient supply and the growth of the seminal root system in barley. III. Compensatory increases in growth of lateral roots, and in rates of phosphate uptake, in response to a localized supply of phosphate. Journal of Experimental Botany 29, 435–451.
| Crossref | GoogleScholarGoogle Scholar |
Grose MJ
(1989) Phosphorus nutrition of seedling of waratah, Telopea speciosissima (Sm) R.Br. (Proteaceae). Australian Journal of Botany 37, 313–320.
| Crossref | GoogleScholarGoogle Scholar |
Handreck KA
(1991) Interactions between iron and phosphorus in the nutrition of Banksias ericifolia L. f. var. ericifolia (Proteaceae) in soil-less potting media. Australian Journal of Botany 39, 373–384.
| 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.
| Crossref | GoogleScholarGoogle Scholar |
Hodge A
(2004) The plastic plant: root responses to heterogeneous supplies of nutrients. The New Phytologist 162, 9–24.
| Crossref | GoogleScholarGoogle Scholar |
Johnson JF,
Allan DL, Vance CP
(1994) Phosphorus stress-induced proteoid roots show altered metabolism in Lupinus albus. Plant Physiology 104, 657–665.
| PubMed |
Johnson JF,
Allan DL,
Vance CP, Weiblen G
(1996) Root carbon dioxide fixation by phosphorus-deficient Lupinus albus (contribution to organic acid exudation by proteoid roots). Plant Physiology 112, 19–30.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Keerthisinghe G,
Hocking P,
Ryan PR, Delhaize E
(1998) Proteoid roots of lupin (Lupinus albus L.): effect of phosphorus supply on formation and spatial variation in citrate efflux and enzyme activity. Plant, Cell & Environment 21, 467–478.
| Crossref | GoogleScholarGoogle Scholar |
Lambers H,
Shane MW,
Cramer MD,
Pearse S, Veneklaas EJ
(2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Annals of Botany 98, 693–713.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lambers H,
Shaver G,
Raven JA, Smith SE
(2008) N- and P-acquisition change as soils age. Trends in Ecology & Evolution 23, 95–103.
| Crossref | GoogleScholarGoogle Scholar |
Lamont B
(1972) The morphology and anatomy of proteoid roots in the genus Hakea. Australian Journal of Botany 20, 155–174.
| Crossref | GoogleScholarGoogle Scholar |
Ligaba A,
Yamaguchi M,
Shen H,
Sasaki T,
Yamamoto Y, Matsumoto H
(2004) Phosphorus deficiency enhances plasma membrane H+-ATPase activity and citrate exudation in greater purple lupin (Lupinus pilosus). Functional Plant Biology 31, 1075–1083.
| Crossref | GoogleScholarGoogle Scholar |
Marschner H,
Römheld V, Cakmak I
(1987) Root-induced changes of nutrient availability in the rhizosphere. Journal of Plant Nutrition 10, 1175–1184.
Neumann G, Römheld V
(1999) Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant and Soil 211, 121–130.
| Crossref | GoogleScholarGoogle Scholar |
Pate JS,
Verboom WH, Galloway PD
(2001) Co-occurrence of Proteaceae, lateritic and related oligotrophic soils: coincidental associations or causative inter-relationships? Australian Journal of Botany 49, 529–560.
| Crossref | GoogleScholarGoogle Scholar |
Sas L,
Tang C, Rengel Z
(2001) Excess cation uptake, and extrusion of proton and organic acid anion by Lupinus albus under phosphorus deficiency. Plant Science 160, 1191–1198.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shane MW, Lambers H
(2005) Cluster roots: a curiosity in context. Plant and Soil 274, 101–125.
| Crossref | GoogleScholarGoogle Scholar |
Shane MW,
De VM,
De RS, Lambers H
(2003a) Shoot phosphorus status regulates citrate exudation and cluster root growth in divided root systems of Lupinus albus. Plant, Cell & Environment 26, 265–273.
| Crossref | GoogleScholarGoogle Scholar |
Shane MW,
De Vos M,
De Roock S,
Cawthray GR, Lambers H
(2003b) Effect of external phosphorus supply on internal phosphorus concentration and the initiation, growth and exudation of cluster roots in Hakea prostrata R.Br. Plant and Soil 248, 209–219.
| Crossref | GoogleScholarGoogle Scholar |
Shen J,
Tang C,
Rengel Z, Zhang F
(2004) Root-induced acidification and excess cation uptake by N2-fixing Lupinus albus grown in phosphorus-deficient soil. Plant and Soil 260, 69–77.
| Crossref | GoogleScholarGoogle Scholar |
Shen J,
Li H,
Neumann G, Zhang F
(2005) Nutrient uptake, cluster root formation and exudation of protons and citrate in Lupinus albus as affected by localized supply of phosphorus in a split-root system. Plant Science 168, 837–845.
| Crossref | GoogleScholarGoogle Scholar |
Shu L,
Shen J,
Rengal Z,
Tang C, Zhang F
(2005) Growth medium and phosphorus supply affect cluster root formation and citrate exudation by Lupinus albus grown in a sand/solution split-root system. Plant and Soil 276, 85–94.
| Crossref | GoogleScholarGoogle Scholar |
Shu L,
Shen J,
Rengel Z,
Tang C,
Zhang F, Cawthray GR
(2007) Formation of cluster roots and citrate exudation by Lupinus albus in response to localized application of different phosphorus sources. Plant Science 172, 1017–1024.
| Crossref | GoogleScholarGoogle Scholar |
Tang C,
McLay CDA, Barton L
(1997) A comparison of proton excretion of twelve pasture legumes grown in nutrient solution. Australian Journal of Agricultural Research 37, 563–570.
Tang C,
Hinsinger P,
Drevon JJ, Jaillard B
(2001) Phosphorus deficiency impairs early nodule functioning and enhances proton release in roots of Medicago truncatula L. Annals of Botany 88, 131–138.
| Crossref | GoogleScholarGoogle Scholar |
Wouterlood M,
Lambers H, Veneklaas EJ
(2005) Plant phosphorus status has a limited influence on the concentration of phosphorus-mobilising carboxylates in the rhizosphere of chickpea. Functional Plant Biology 32, 153–159.
| Crossref | GoogleScholarGoogle Scholar |
Yan F,
Zhu Y,
Müller C,
Zörb C, Schubert S
(2002) Adaptation of H+-pumping and plasma membrane H+ ATPase activity in proteoid roots of white lupin under phosphate deficiency. Plant Physiology 129, 50–63.
| Crossref | GoogleScholarGoogle Scholar | PubMed |