Phosphorus nutrition of proteaceae in severely phosphorus-impoverished soils: Are there lessons to be learned for future crops?

Plant Physiology

Volumn 156, Issue 3, 2011, Pages 1058-1066

  Lambers, Hans ^a   Finnegan, Patrick M ^a   Laliberté, Etienne ^a   Pearse, Stuart J ^a   Ryan, Megan H ^a   Shane, Michael W ^a   Veneklaas, Erik J ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEACEAE;

PHOSPHORUS;

CHEMISTRY; CROP; METABOLISM; PLANT LEAF; PLANT ROOT; PROTEACEAE; REVIEW; SOIL;

CROPS, AGRICULTURAL; PHOSPHORUS; PLANT LEAVES; PLANT ROOTS; PROTEACEAE; SOIL;

EID: 79960004712     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.111.174318     Document Type: Article

References (101)

1. Acharya K, Kyle M, Elser JJ (2004) Biological stoichiometry of Daphnia growth: an ecophysiological test of the growth rate hypothesis. Limnol Oceanogr 49: 656-665
2. Andersson MX, Stridh MH, Larsson KE, Liljenberg C, Sandelius AS (2003) Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Lett 537: 128-132
3. Bell LW, Bennett RG, Ryan MH, Clarke H (2011) The potential of herbaceous native Australian legumes as grain crops: a review. Renew Agric Food Syst 26: 72-91
4. Borie F, Rubio R (2003) Total and organic phosphorus in Chilean volcanic soils. Gayana Bot 60: 69-73
5. Brundrett M (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 Soil 320: 37-77
6. Cesco S, Neumann G, Tomasi N, Pinton R, Weisskopf L (2010) Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant Soil 329: 1-25
7. Chapin FS, Bieleski RL (1982) Mild phosphorus stress in barley and a related low-phosphorus-adapted barleygrass: phosphorus fractions and phosphate absorption in relation to growth. Physiol Plant 54: 309-317
8. Clements J, Prilyuk L, Quealy J, Francis G (2008) Interspecific crossing among the New World lupin species for Lupinus mutabilis crop improvement. In JA Palta, JB Berger, eds, Lupins for Health and Wealth: Proceedings of the 12th International Lupin Conference, 14-18 Sept. 2008, Fremantle, Western Australia. International Lupin Association, Canterbury, New Zealand, pp 324-327
9. Cordell D, Drangert J-O, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Change 19: 292-305
10. Denton MD, Veneklaas EJ, Freimoser FM, Lambers H (2007a) Banksia species (Proteaceae) from severely phosphorus-impoverished soils exhibit extreme efficiency in the use and re-mobilization of phosphorus. Plant Cell Environ 30: 1557-1565
11. Denton MD, Veneklaas EJ, Lambers H (2007b) Does phenotypic plasticity in carboxylate exudation differ among rare and widespread Banksia species (Proteaceae)? New Phytol 173: 592-599
12. Diehl P, Mazzarino MJ, Funes F, Fontenla S, Gobbi M, Ferrari J (2003) Nutrient conservation strategies in native Andean-Patagonian forests. J Veg Sci 14: 63-70
13. Dinkelaker B, Römheld V, Marschner H (1989) Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant Cell Environ 12: 285-292
14. Elser JJ, Dobberfuhl D, MacKay NA, Schampel JH (1996) Organism size, life history, and N:P stoichiometry: towards a unified view of cellular and ecosystem processes. Bioscience 46: 674-684
15. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78: 9-19
16. Fay P, Mitchell DT, Osborne BA (1996) Photosynthesis and nutrient-use efficiency of barley in response to low arbuscular mycorrhizal colonization and addition of phosphorus. New Phytol 132: 425-433
17. Flynn K, Raven J, Rees T, Finkel Z, Quigg A, Beardall J (2010) Is the growth rate hypothesis applicable to microalgae? J Phycol 46: 1-12
18. Foyer C, Spencer C (1986) The relationship between phosphate status and photosynthesis in leaves. Planta 167: 369-375
19. Galme ́s J, Flexas J, Keys AJ, Cifre J, Mitchell RAC, Madgwick PJ, Haslam RP, Medrano H, Parry MAJ (2005) Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. Plant Cell Environ 28: 571-579
20. 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: 107-124
21. Gardner WK, Boundy KA (1983) The acquisition of phosphorus by Lupinus albus L. IV. The effect of interplanting wheat and white lupin on the growth and mineral composition of the two species. Plant Soil 70: 391-402
22. Geelhoed JS, Hiemstra T, Van Riemsdijk WH (1998) Competitive interaction between phosphate and citrate on goethite. Environ Sci Technol 32: 2119-2123
23. Gilbert N (2009) The disappearing nutrient. Nature 461: 716-718
24. Grierson PF, Attiwill PM (1989) Chemical characteristics of the proteoid root mat of Banksia integrifolia L. Aust J Bot 37: 137-143
25. Grierson PF, Comerford NB (2000) Non-destructive measurement of acid phosphatase activity in the rhizosphere using nitrocellulose membranes and image analysis. Plant Soil 218: 49-57
26. Groom PK, Lamont BB (2010) Phosphorus accumulation in Proteaceae seeds: a synthesis. Plant Soil 334: 61-72
27. Gunn S, Farrar JF, Collis BE, Nason M (1999) Specific leaf area in barley: individual leaves versus whole plants. New Phytol 143: 45-51
28. Halloy S, Grau A, McKenzie B (1996) Gevuina nut (Gevuina avellana, Proteaceae), a cool climate alternative to macadamia. Econ Bot 50: 224-235
29. Handreck K (1991) Interactions between iron and phosphorus in the nutrition of Banksia ericifolia L. f var ericifolia (Proteaceae) in soil-less potting media. Aust J Bot 39: 373-384
30. Handreck KA (1997) Phosphorus requirements of Australian native plants. Aust J Soil Res 35: 241-290
31. Hassiotou F, Evans JR, Ludwig M, Veneklaas EJ (2009a) Stomatal crypts may facilitate diffusion of CO2 to adaxial mesophyll cells in thick sclerophylls. Plant Cell Environ 32: 1596-1611
32. Hassiotou F, Ludwig M, Renton M, Veneklaas EJ, Evans JR (2009b) Influence of leaf dry mass per area, CO2, and irradiance on mesophyll conductance in sclerophylls. J Exp Bot 60: 2303-2314
33. Hocking PJ, Jeffery S (2004) Cluster-root production and organic anion exudation in a group of Old-World lupins and a New-World lupin. Plant Soil 258: 135-150
34. Hopper SD (2009) OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant Soil 322: 49-86
35. Huyghe C (1997) White lupin (Lupinus albus L.). Field Crops Res 53: 147-160
36. Johnson JF, Allan DL, Vance CP (1994) Phosphorus stress-induced proteoid roots show altered metabolism in Lupinus albus. Plant Physiol 104: 657-665
37. Killingbeck KT (1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77: 1716-1727
38. Lambers H, Brundrett MC, Raven JA, Hopper SD (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant Soil 334: 11-31
39. Lambers H, Chapin FS, Pons TL (2008a) Plant Physiological Ecology, Ed 2. Springer, New York
40. 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 Soil 238: 111-122
41. Lambers H, Raven JA, Shaver GR, Smith SE (2008b) Plant nutrientacquisition strategies change with soil age. Trends Ecol Evol 23: 95-103
42. Lambers H, Shane MW (2007) Role of root clusters in phosphorus acquisition and increasing biological diversity in agriculture. In JHJ Spiertz, PC Struik, HH Van Laar, eds, Scale and Complexity in Plant Systems Research: Gene-Plant-Crop Relations. Springer, Dordrecht, The Netherlands, pp 237-250
43. 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 (Lond) 98: 693-713
44. Lamont B (1972a) The effect of soil nutrients on the production of proteoid roots by Hakea species. Aust J Bot 20: 27-40
45. Lamont B (1972b) The morphology and anatomy of proteoid roots in the genus Hakea. Aust J Bot 20: 155-174
46. Lamont B (1982) Mechanisms for enhancing nutrient uptake in plants, with particular reference to Mediterranean South Africa and Western Australia. Bot Rev 48: 597-689
47. Lamont BB (2003) Structure, ecology and physiology of root clusters: a review. Plant Soil 248: 1-19
48. Lott JNA, Ockenden I, Raboy V, Batten GD (2000) Phytic acid and phosphorus in crop seeds and fruits: a global estimate. Seed Sci Res 10: 11-33
49. Loughman BC, Ratcliffe RG, Southon TE (1989) Observations on the cytoplasmic and vacuolar orthophosphate pools in leaf tissues using in vivo 31P-NMR spectroscopy. FEBS Lett 242: 279-284
50. Mast AR, Jones EH, Havery SP (2005) An assessment of old and new DNA sequence evidence for the paraphyly of Banksia with respect to Dryandra (Proteaceae). Aust Syst Bot 18: 75-88
51. Matzek V, Vitousek PM (2009) N:P stoichiometry and protein:RNA ratios in vascular plants: an evaluation of the growth-rate hypothesis. Ecol Lett 12: 765-771
52. Nadeem M, Mollier A, Morel C, Vives A, Prud'Homme L, Pellerin S (2011) Relative contribution of seed phosphorus reserves and exogenous phosphorus uptake to maize (Zea mays L.) nutrition during early growth stages. Plant Soil (in press)
53. Niinemets U, Wright IJ, Evans JR (2009) Leaf mesophyll diffusion conductance in 35 Australian sclerophylls covering a broad range of foliage structural and physiological variation. J Exp Bot 60: 2433-2449
54. Pang J, Ryan MH, Tibbett M, Cawthray GR, Siddique KHM, Bolland MDA, Denton MD, Lambers H (2010a) Variation in morphological and physiological parameters in herbaceous perennial legumes in response to phosphorus supply. Plant Soil 331: 241-255
55. Pang J, Tibbett M, Denton MD, Lambers H, Siddique KHM, Bolland MDA, Revell C, Ryan MH (2010b) Variation in seedling growth of 11 perennial legumes in response to phosphorus supply. Plant Soil 328: 133-143
56. Parks SE, Haigh AM, Cresswell GC (2000) Stem tissue phosphorus as an index of the phosphorus status of Banksia ericifolia L. f. Plant Soil 227: 59-65
57. Pate JS, Dell B (1984) Economy ofmineral nutrients in sandplain species. In JS Pate, JS Beard, eds, Kwongan: Plant Life of the Sandplain. University of Western Australia Press, Nedlands, Australia, pp 227-252
58. Pate JS, Verboom WH, Galloway PD (2001) Cooccurrence of Proteaceae, laterite and related oligotrophic soils: coincidental associations or causative inter-relationships? Aust J Bot 49: 529-560
59. Pearse SJ, Veneklaas EJ, Cawthray GR, Bolland MDA, Lambers H (2006a) Carboxylate release of wheat, canola and 11 grain legume species as affected by phosphorus status. Plant Soil 288: 127-139
60. Pearse SJ, Veneklaas EJ, Cawthray GR, Bolland MDA, Lambers H (2006b) Triticum aestivum shows a greater biomass response to a supply of aluminium phosphate than Lupinus albus, despite releasing fewer carboxylates into the rhizosphere. New Phytol 169: 515-524
61. Pearse SJ, Veneklaas EJ, Cawthray GR, Bolland MDA, Lambers H (2007) Carboxylate composition of root exudates does not relate consistently to a crop species' ability to use phosphorus from aluminium, iron or calcium phosphate sources. New Phytol 173: 181-190
62. Playsted CWS, Johnston ME, Ramage CM, Edwards DG, Cawthray GR, Lambers H (2006) Functional significance of dauciform roots: exudation of carboxylates and acid phosphatase under phosphorus deficiency in Caustis blakei (Cyperaceae). New Phytol 170: 491-500
63. Purnell H (1960) Studies of the family Proteaceae. I. Anatomy and morphology of the roots of some Victorian species. Aust J Bot 8: 38-50
64. Raboy V (2001) Seeds for a better future: 'low phytate' grains help to overcome malnutrition and reduce pollution. Trends Plant Sci 6: 458-462
65. Raboy V, Gerbasi PF, Young KA, Stoneberg SD, Pickett SG, Bauman AT, Murthy PPN, Sheridan WF, Ertl DS (2000) Origin and seed phenotype of maize low phytic acid 1-1 and low phytic acid 2-1. Plant Physiol 124: 355-368
66. Ramirez GC, Valenzuela FE, San Martin PC (2004) Nuevos antecedents sobre desarrollo temprano, morfologi{dotless} ́a y anatomi{dotless} ́a de las rai{dotless} ́ces proteiformes de Gevuina avellana. Agro Sur 32: 33-44
67. Raven JA (2008) Phosphorus and the future. In PJ White, JP Hammond, eds, The Ecophysiology of Plant-Phosphorus Interactions. Springer, Dordrecht, The Netherlands, pp 271-283
68. Roy NN, Gladstones JS (1985) Prospects for interspecific hybridization of Lupinus atlanticus Gladst. with L. cosentini Guss. Theor Appl Genet 71: 238-241
69. Ryan MH, Angus JF (2003) Arbuscular mycorrhizae in wheat and field pea crops on a low P soil: increased Zn-uptake but no increase in P-uptake or yield. Plant Soil 250: 225-239
70. Ryan MH, Ehrenberg S, Bennett RG, Tibbett M (2009) Putting the P in Ptilotus: a phosphorus-accumulating herb native to Australia. Ann Bot (Lond) 103: 901-911
71. Ryan MH, McCully ME, Huang CX (2003) Location and quantification of phosphorus and other elements in fully hydrated, soil-grown arbuscular mycorrhizas: a cryo-analytical scanning electron microscopy study. New Phytol 160: 429-441
72. Ryan MH, Norton RM, Kirkegaard JA, McCormick KM, Knights SE, Angus JF (2002) Increasing mycorrhizal colonisation does not improve growth and nutrition of wheat on Vertosols in south-eastern Australia. Aust J Agric Res 53: 1173-1181
73. Ryan MH, Van Herwaarden AF, Angus JF, Kirkegaard JA (2005) Reduced growth of autumn-sown wheat in a low-P soil is associated with high colonisation by arbuscular mycorrhizal fungi. Plant Soil 270: 275-286
74. Shane M, Szota C, Lambers H (2004a) A root trait accounting for the extreme phosphorus sensitivity of Hakea prostrata (Proteaceae). Plant Cell Environ 27: 991-1004
75. Shane MW, Cawthray GR, Cramer MD, Kuo J, Lambers H (2006) Specialized 'dauciform' roots of Cyperaceae are structurally distinct, but functionally analogous with 'cluster' roots. Plant Cell Environ 29: 1989-1999
76. Shane MW, Cramer MD, Funayama-Noguchi S, Cawthray GR, Millar AH, Day DA, Lambers H (2004b) Developmental physiology of cluster-root carboxylate synthesis and exudation in harsh hakea: expression of phosphoenolpyruvate carboxylase and the alternative oxidase. Plant Physiol 135: 549-560
77. 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 Environ 31: 1825-1833
78. Shane MW, Dixon KW, Lambers H (2005) The occurrence of dauciform roots amongst Western Australian reeds, rushes and sedges, and the impact of phosphorus supply on dauciform-root development in Schoenus unispiculatus (Cyperaceae). New Phytol 165: 887-898
79. Shane MW, Lambers H (2005) Cluster roots: a curiosity in context. Plant Soil 274: 101-125
80. Shane MW, Lambers H (2006) Systemic suppression of cluster-root formation and net P-uptake rates in Grevillea crithmifolia at elevated P supply: a proteacean with resistance for developing symptoms of 'P toxicity'. J Exp Bot 57: 413-423
81. Shane MW, McCully ME, Lambers H (2004c) Tissue and cellular phosphorus storage during development of phosphorus toxicity in Hakea prostrata (Proteaceae). J Exp Bot 55: 1033-1044
82. Smith SE, Jakobsen I, Groenlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156: 1050-1057
83. Sterner R, Elser JJ (2002) Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere. Princeton University Press, Princeton, NJ
84. Suriyagoda LD, Ryan MH, Renton M, Lambers H (2010) Multiple adaptive responses of Australian native perennial legumes with pasture potential to grow in phosphorus- and moisture-limited environments. Ann Bot (Lond) 105: 755-767
85. Tcherkez GGB, Farquhar GD, Andrews TJ (2006) Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc Natl Acad Sci USA 103: 7246-7251
86. Thompson J (1987) Decline of vesicular-arbuscular mycorrhizae in long fallow disorder of field crops and its expression in phosphorus deficiency of sunflower. Aust J Agric Res 38: 847-867
87. Tiessen H, Monaco S, Ramirez A, Santos M, Shang C (1996) Phosphate minerals in a lateritic crust from Venezuela. Biogeochemistry 34: 1-17
88. Tomasi N, Kretzschmar T, Espen L, Weisskopf L, Fuglsang AT, Palmgren MG, Neumann G, Varanini Z, Pinton R, Martinoia E, et al (2009) Plasma membrane H-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin. Plant Cell Environ 32: 465-475
89. Tomasi N, Weisskopf L, Renella G, Landi L, Pinton R, Varanini Z, Nannipieri P, Torrent J, Martinoia E, Cesco S (2008) Flavonoids of white lupin roots participate in phosphorus mobilization from soil. Soil Biol Biochem 40: 1971-1974
90. Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157: 423-447
91. 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 Soil 248: 187-197
92. Von Baer E (2006) Relevant points for the production and use of sweet lupin in Chile. In JA Palta, JB Berger, eds, Proceedings of the 12th International Lupin Conference, 14-18 Sept. 2008, Fremantle, Western Australia. International Lupin Association, Canterbury, New Zealand, pp 116-119
93. Watt M, Evans JR (1999) Proteoid roots: physiology and development. Plant Physiol 121: 317-324
94. Weisskopf L, Abou-Mansour E, Fromin N, Tomasi N, Santelia D, Edelkott I, Neumann G, Aragno M, Tabacchi R, Martinoia E (2006a) White lupin has developed a complex strategy to limit microbial degradation of secreted citrate required for phosphate acquisition. Plant Cell Environ 29: 919-927
95. Weisskopf L, Fromin N, Tomasi N, Aragno M, Martinoia E (2005) Secretion activity of white lupin's cluster roots influences bacterial abundance, function and community structure. Plant Soil 268: 181-194
96. Weisskopf L, Tomasi N, Santelia D, Martinoia E, Langlade NB, Tabacchi R, Abou-Mansour E (2006b) Isoflavonoid exudation from white lupin roots is influenced by phosphate supply, root type and cluster-root stage. New Phytol 171: 657-668
97. Welch RM, Graham RD (2004) Breeding for micronutrients in staple food crops from a human nutrition perspective. J Exp Bot 55: 353-364
98. Witkowski ETF, Lamont BB (1996) Disproportionate allocation of mineral nutrients and carbon between vegetative and reproductive structures in Banksia hookeriana. Oecologia 105: 38-42
99. Wright IJ, Reich PB, Westoby M (2001) Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high- and low-nutrient habitats. Funct Ecol 15: 423-434
100. Zhao H-J, Liu Q-L, Fu H-W, Xu X-H, Wu D-X, Shu Q-Y (2008) Effect of nonlethal low phytic acid mutations on grain yield and seed viability in rice. Field Crops Res 108: 206-211
101. Zúñiga-Feest A, Delgado M, Alberdi M(2010) The effect of phosphorus on growth and cluster-root formation in the Chilean Proteaceae: Embothrium coccineum (R. et J. Forst.). Plant Soil 334: 113-121