Nodulation promotes cluster-root formation in Lupinus albus under low phosphorus conditions

  • Xiao Wang
  • Wenli Ding
  • Hans Lambers
Regular Article


Background and aims

Phosphorus deficiency often limits crop productivity, while phosphate rock, which is used to produce phosphorus fertilisers, is a non-renewable resource. Formation of cluster roots is an adaptation to nutrient-poor soils in Lupinus species, including L. albus. Lupinus species also produce nodules, which require a large investment of phosphorus. Our aim is to test whether nodulation promotes cluster-root formation in L. albus.


Seedlings of L. albus, either inoculated with rhizobia or non-inoculated, were grown in nutrient solution with a low phosphorus supply. Non-inoculated plants were provided with the same amount of nitrogen in the form of nitrate as the nodulated ones acquired, from both air and nutrient solution, based on preliminary experiments. We measured biomass, phosphorus and nitrogen concentrations as well as photosynthesis just prior to each harvest.


Nodulated plants and non-nodulated control plants produced the same amount of biomass. Nodulated plants had, on average, 86% more cluster roots than non-nodulated ones at the four harvests. As hypothesised, nodulation significantly promoted cluster-root formation; it also enhanced rates of photosynthesis.


Nodulation promoted cluster-root formation and photosynthesis, presumably because nodules are significant sinks for phosphorus and photosynthates. Our results do not provide evidence for a trade-off between investment of resources in nodules and cluster roots.


Nitrogen fixation nodules proteoid roots rhizobium white lupin trade-off 



We thank the editor and two reviewers for their constructive comments and advises on our manuscript. We are grateful for the help provided by Albina Ilyasova, Greg Cawthray and Haijie Zhang in Australia and by Kun Zhang, Li Shen as well as professor Weihua Guo in China. We also thank Jiayin Pang for her internal review of our manuscript. We thank the University of Western Australia and the Institute of Agriculture for support towards the research and the China Scholarship Council for a scholarship for Xiao Wang.

Supplementary material

11104_2018_3638_MOESM1_ESM.docx (17 kb)
ESM 1 (DOCX 16 kb)


  1. Abdolzadeh A, Wang X, Veneklaas EJ, Lambers H (2010) Effects of phosphorus supply on growth, phosphate concentration and cluster-root formation in three Lupinus species. Ann Bot 105:365–374CrossRefPubMedGoogle Scholar
  2. Adams MA, Turnbull TL, Sprent JI, Buchmann N (2016) Legumes are different: Leaf nitrogen, photosynthesis, and water use efficiency. Proc Natl Acad Sci U S A 113:4098–4103CrossRefPubMedPubMedCentralGoogle Scholar
  3. Anonymous (1977) Technicon Industrial Method No. 334-74W/B+. Technicon Industrial Systems Tarrytown, NYGoogle Scholar
  4. Belay A, Claassens AS, Wehner FC (2002) Effect of direct nitrogen and potassium and residual phosphorus fertilizers on soil chemical properties, microbial components and maize yield under long-term crop rotation. Biol Fertil Soils 35:420–427CrossRefGoogle Scholar
  5. Bustan A, Goldschmidt EE (1998) Estimating the cost of flowering in a grapefruit tree. Plant Cell Environ 21:217–224CrossRefGoogle Scholar
  6. Carpenter SR, Caraco NF, Correll DL, Howarth RW, Sharpley AN, Smith VH (1998) Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecol Appl 8:559–568CrossRefGoogle Scholar
  7. Cordell D, Drangert J-O, White S (2009) The story of phosphorus: Global food security and food for thought. Glob Environ Chang 19:292–305CrossRefGoogle Scholar
  8. Drevon J-J, Hartwig UA (1997) Phosphorus deficiency increase the argon-induced decline of nodules nitrogenase activity in soybean and alfalfa. Planta 201:463–469CrossRefGoogle Scholar
  9. Fixen PE, Johnston AM (2012) World fertilizer nutrient reserves: a view to the future. J Sci Food Agric 92:1001–1005CrossRefPubMedGoogle Scholar
  10. Florez-Sarasa I, Lambers H, Wang X, Finnegan PM, Ribas-Carbo M (2014) The alternative respiratory pathway mediates carboxylate synthesis in white lupin cluster roots under phosphorus deprivation. Plant Cell Environ 37:922–928CrossRefPubMedGoogle Scholar
  11. Gardner WK, Barber DA, Parbery DG (1983) The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced. Plant Soil 70:107–124CrossRefGoogle Scholar
  12. Gerke J, Römer W, Beißner L (2000) The quantitative effect of chemical phosphate mobilization by carboxylate anions on P uptake by a single root. II. The importance of soil and plant parameters for uptake of mobilized P. J Plant Nutr Soil Sci 163:213–219CrossRefGoogle Scholar
  13. Gilbert N (2009) The dissappearing nutrient. Nature 461:716–718CrossRefPubMedGoogle Scholar
  14. Israel DW (1987) Investigation of the role of phosphorus in symbiotic dinitrogen fixation. Plant Physiol 84:835–840CrossRefPubMedPubMedCentralGoogle Scholar
  15. Johnson JF, Vance CP, Allan DL (1996) Phosphorus deficiency in Lupinus albus. Altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiol 112:31–41CrossRefPubMedPubMedCentralGoogle Scholar
  16. Jones PG, Lloyd JC, Raines CA (1996) Glucose feeding of intact wheat plants represses the expression of a number of Calvin cycle genes. Plant Cell Environ 19:231–236CrossRefGoogle Scholar
  17. Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41:1233–1244CrossRefGoogle Scholar
  18. Keerthisinghe G, Hocking PJ, Ryan PR, Delhaize E (1998) Effect of phosphorus supply on the formation and function of proteoid roots of white lupin (Lupinus albus L.) Plant Cell Environ 21:467–478CrossRefGoogle Scholar
  19. Lambers H, Ahmedi I, Berkowitz O, Dunne C, Finnegan P M, Hardy GE, Jost R, Laliberte E, Pearse SJ, Teste FP (2013a) Phosphorus nutrition of phosphorus-sensitive Australian native plants: threats to plant communities in a global biodiversity hotspot. Conserv Physiol 1: cot010Google Scholar
  20. Lambers H, Atkin OK, Millenaar FF (2002) Respiratory patterns in roots in relation to their functioning. In: Waisel Y, Eshel A, Kafkaki U (eds) Plant roots The hidden half. 3rd edn. edn. Marcel Dekker, Inc., New YorkGoogle Scholar
  21. Lambers H, Bishop JG, Hopper S, Laliberte E, Zúñiga-Feest A (2012) Phosphorus-mobilization ecosystem engineering: the role of cluster roots and carboxylate exudation in young P-limited ecosystems. Ann Bot 110:329–348CrossRefPubMedPubMedCentralGoogle Scholar
  22. Lambers H, Clements JC, Nelson MN (2013b) How a phosphorus-acquisition strategy based on carboxylate exudation powers the success and agronomic potential of lupines (Lupinus, Fabaceae). Am J Bot 100:263–288CrossRefPubMedGoogle Scholar
  23. Lambers H, Cramer MD, Shane MW, Wouterlood M, Poot P, Veneklaas EJ (2003) Introduction. Structure and functioning of cluster root and plant responses to phosphate deficiency. Plant Soil 248:ix–xixCrossRefGoogle Scholar
  24. 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. Ann Bot 98:693–713CrossRefPubMedPubMedCentralGoogle Scholar
  25. Li C, Li C, Zhang H, Liao H, Wang X (2017) The purple acid phosphatase GmPAP21 enhances internal phosphorus utilization and possibly plays a role in symbiosis with rhizobia in soybean. Physiol Plant 159:215–227CrossRefPubMedGoogle Scholar
  26. Li H, Shen J, Zhang F, Tang C, Lambers H (2008) Is there a critical level of shoot phosphorus concentration for cluster-root formation in Lupinus albus? Funct Plant Biol 35:328–336CrossRefGoogle Scholar
  27. Liu J, Samac DA, Bucciarelli B, Allan DL, Vance CP (2005) Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport. Plant J 41:257–268CrossRefPubMedGoogle Scholar
  28. Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109:7–13CrossRefPubMedPubMedCentralGoogle Scholar
  29. Lynch JP (2007) Roots of the second green revolution. Aust J Bot 55:493–512CrossRefGoogle Scholar
  30. Muller R, Morant M, Jarmer H, Nilsson L, Nielsen TH (2007) Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol 143:156–171CrossRefPubMedPubMedCentralGoogle Scholar
  31. Neumann G, Massonneau A, Martinoia E, Römheld V (1999) Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta 208:373–382CrossRefGoogle Scholar
  32. Niu YF, Chai RS, Jin GL, Wang H, Tang CX, Zhang YS (2013) Responses of root architecture development to low phosphorus availability: a review. Ann Bot 112:391–408CrossRefPubMedGoogle Scholar
  33. Patrick JW, Botha FC, Birch RG (2013) Metabolic engineering of sugars and simple sugar derivatives in plants. Plant Biotechnol J 11:142–156CrossRefPubMedGoogle Scholar
  34. Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52:1383–1400CrossRefPubMedGoogle Scholar
  35. Peret B, Clement M, Nussaume L, Desnos T (2011) Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci 16:442–450CrossRefPubMedGoogle Scholar
  36. Raghothama KG (1999) Phosphorus acquisition. Annu Rev Plant Physiol Plant Mol Biol 50:665–693CrossRefPubMedGoogle Scholar
  37. Raven JA (2012) Protein turnover and plant RNA and phosphorus requirements in relation to nitrogen fixation. Plant Sci 188-189:25–35CrossRefPubMedGoogle Scholar
  38. Raven JA (2013a) The evolution of autotrophy in relation to phosphorus requirement. J Exp Bot 64:4023–4046CrossRefPubMedGoogle Scholar
  39. Raven JA (2013b) RNA function and phosphorus use by photosynthetic organisms. Front Plant Sci 4Google Scholar
  40. Rayment GE, Lyons DJ, Rayment GE, Lyons DJ (2010) Soil chemical methods: Australasia. CSIRO PublishingGoogle Scholar
  41. 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 Soil 349:121–156CrossRefGoogle Scholar
  42. Ruan YL, Patrick JW, Bouzayen M, Osorio S, Fernie AR (2012) Molecular regulation of seed and fruit set. Trends Plant Sci 17:656–665CrossRefPubMedGoogle Scholar
  43. Sa T, Israel DW (1991) Energy status and functioning of phosphorus-deficient soybean nodules. Plant Physiol 97:982–935CrossRefGoogle Scholar
  44. Sas L, Rengel Z, Tang C (2002) The effect of nitrogen nutrition on cluster root formation and proton extrusion by Lupinus albus. Ann Bot 89:435–442CrossRefPubMedPubMedCentralGoogle Scholar
  45. Scholz RW, Wellmer F-W (2013) Approaching a dynamic view on the availability of mineral resources: What we may learn from the case of phosphorus? Glob Environ Chang 23:11–27CrossRefGoogle Scholar
  46. Schulze J, Beschow H, Merbach W (1999) The effect of an 15NH4 15NO3 fertilization at flowering on growth and nitrogen fixation of white and blue lupins. Isot Environ Healt S 35:85–95CrossRefGoogle Scholar
  47. Schulze J, Drevon JJ (2005) P-deficiency increases the O2 uptake per N2 reduced in alfalfa. J Exp Bot 56:1779–1784CrossRefPubMedGoogle Scholar
  48. Schulze J, Temple G, Temple SJ, Beschow H, Vance CP (2006) Nitrogen fixation by white lupin under phosphorus deficiency. Ann Bot 98:731–740CrossRefPubMedPubMedCentralGoogle Scholar
  49. Shane MW, Lambers H (2005) Cluster roots: A curiosity in context. Plant Soil 274:101–125CrossRefGoogle Scholar
  50. Shane MW, Vos MD, Roock SD, Lambers H (2003) Shoot P status regulates cluster-root growth and citrate exudation in Lupinus albus grown with a divided root system. Plant Cell Environ 26:265–273CrossRefGoogle Scholar
  51. Sharkey TD, Stitt M, Heineke D, Gerhardt R, Raschke K, Heldt HW (1986) Limitation of photosynthesis by carbon metabolism. Plant Physiol 81:1123–1129CrossRefPubMedPubMedCentralGoogle Scholar
  52. Sharpley AN, McDowell RW, Kleinman PJA (2001) Phosphorus loss from land to water: integrating agricultural and environmental management. Plant Soil 237:287–307CrossRefGoogle Scholar
  53. 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 Sci 168:837–845CrossRefGoogle Scholar
  54. Shen J, Rengel Z, Tang C, Zhang F (2003) Role of phosphorus nutrition in development of cluster roots and release of carboxylates in soil-grown Lupinus albus. Plant Soil 248:199–206CrossRefGoogle Scholar
  55. Shu L, Shen J, Rengel Z, Tang C, Zhang F (2007) Cluster root formation by Lupinus Albus is modified by stratified application of phosphorus in a split-root system. J Plant Nutr 30:271–288CrossRefGoogle Scholar
  56. Simpson RJ, Oberson A, Culvenor RA, Ryan MH, Veneklaas EJ, Lambers H, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Richardson AE (2011) Strategies and agronomic interventions to improve the phosphorus-use efficiency of farming systems. Plant Soil 349:89–120CrossRefGoogle Scholar
  57. Smith VH, Schindler DW (2009) Eutrophication science: where do we go from here? Trends Ecol Evol 24:201–207CrossRefPubMedGoogle Scholar
  58. Stutter MI, Shand CA, George TS, Blackwell MS, Bol R, Mackay RL, Richardson AE, Condron LM, Turner BL, Haygarth PM (2012) Recovering phosphorus from soil: a root solution? Environ Sci Technol 46:1977–1978CrossRefPubMedGoogle Scholar
  59. 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. Ann Bot 88:131–138CrossRefGoogle Scholar
  60. Thuynsma R, Valentine A, Kleinert A (2014a) Phosphorus deficiency affects the allocation of below-ground resources to combined cluster roots and nodules in Lupinus albus. J Plant Physiol 171:285–291CrossRefPubMedGoogle Scholar
  61. Thuynsma R, Valentine A, Kleinert A (2014b) Short-term supply of elevated phosphate alters the belowground carbon allocation costs and functions of lupin cluster roots and nodules. J Plant Physiol 171:648–654CrossRefPubMedGoogle Scholar
  62. Valentine AJ, Kleinert A, Benedito VA (2017) Adaptive strategies for nitrogen metabolism in phosphate deficient legume nodules. Plant Sci 256:46–52CrossRefPubMedGoogle Scholar
  63. Vardien W, Steenkamp ET, Valentine AJ (2016) Legume nodules from nutrient-poor soils exhibit high plasticity of cellular phosphorus recycling and conservation during variable phosphorus supply. J Plant Physiol 191:73–81CrossRefPubMedGoogle Scholar
  64. Vergutz L, Manzoni S, Porporato A, Novais RF, Jackson RB (2012) Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr 82:205–220CrossRefGoogle Scholar
  65. Wang X, Pearse SJ, Lambers H (2013) Cluster-root formation and carboxylate release in three Lupinus species as dependent on phosphorus supply, internal phosphorus concentration and relative growth rate. Ann Bot 112:1449–1459CrossRefPubMedPubMedCentralGoogle Scholar
  66. Wang Z, Shen J, Ludewig U, Neumann G (2015) A re-assessment of sucrose signaling involved in cluster-root formation and function in phosphate-deficient white lupin (Lupinus albus). Physiol Plant 154:407–419CrossRefPubMedGoogle Scholar
  67. White PF, Robson AD (1989) Effect of soil pH and texture on the growth and nodulation of lupins. Aust J Agric Res 40:63–73CrossRefGoogle Scholar
  68. Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Biological Sciences and Institute of AgricultureThe University of Western AustraliaPerthAustralia
  2. 2.Institute of Ecology and Biodiversity, School of Life SciencesShandong UniversityJinanPeople’s Republic of China

Personalised recommendations