Phosphorus recycling in photorespiration maintains high photosynthetic capacity in woody species

Plant Cell and Environment

Volumn 38, Issue 6, 2015, Pages 1142-1156

  Ellsworth, David S ^a   Crous, Kristine Y ^a   Lambers, Hans ^b   Cooke, Julia ^a,c  

^a WESTERN SYDNEY UNIVERSITY   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c MACQUARIE UNIVERSITY   (Australia)

Author keywords

Low oxygen concentration; nitrogen; Phosphate limitations; Phosphorus; Photosynthesis: carbon reactions; Sclerophyll trees

Indexed keywords

ASSIMILATION EFFICIENCY; CARBON DIOXIDE; NUTRIENT AVAILABILITY; NUTRIENT CYCLING; ORTHOPHOSPHATE; PHOSPHORUS; PHOTOSYNTHESIS; WOODY PLANT;

AUSTRALIA;

CARBON DIOXIDE; OXYGEN; PHOSPHATE; PHOSPHORUS;

BIOLOGICAL MODEL; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF; TREE;

CARBON DIOXIDE; MODELS, BIOLOGICAL; OXYGEN; PHOSPHATES; PHOSPHORUS; PHOTOSYNTHESIS; PLANT LEAVES; TREES;

EID: 84928754260     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12468     Document Type: Article

References (80)

1. Aerts R. & Chapin F.S. (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30, 1-67.
2. Archontoulis S.V., Yin X., Vos J., Danalotos N.G. & Struick P.G. (2012) Leaf photosynthesis and respiration of three bioenergy crops in relation to temperature and leaf nitrogen: how conserved are biochemical model parameters among crop species? Journal of Experimental Botany 63, 895-911.
3. Beadle N.C.W. (1966) Soil phosphate and its role in molding segments of the Australian flora and vegetation, with special reference to xeromorphy and sclerophylly. Ecology 47, 992-1007.
4. Beale S.I. (1978) Delta-aminolevulinic acid in plants - its biosynthesis, regulation, and role in plastid development. Annual Review of Plant Physiology and Plant Molecular Biology 29, 95-120.
5. Bernacchi C.J., Singsaas E.L., Pimentel C., Portis A.R. & Long S.P. (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant, Cell & Environment 24, 253-259.
6. 3 photosynthesis from the chloroplast to the ecosystem. Plant, Cell & Environment 36, 1641-1657.
7. Bonan G.B., Lawrence P.J., Oleson K.W., Levis S., Jung M., Reichstein M., ... Swenson S.C. (2011) Improving canopy processes in the Community Land Model version 4 (CLM4) using global flux fields empirically inferred from FLUXNET data. Journal of Geophysical Research-Biogeosciences 116, http://dx.doi.org/10.1029/2010JG001593.
8. Bown H.E., Watt M.S., Clinton P.W., Mason E.G. & Richardson B. (2009) Partititioning concurrent influences of nitrogen and phosphorus supply on photosynthetic model parameters of Pinus radiata. Tree Physiology 27, 335-344.
9. Brooks A. (1986) Effects of phosphorus nutrition on ribulose-1, 5-bisphosphate carboxylase activation, photosynthetic quantum yield and amounts of some Calvin-cycle metabolites in spinach leaves. Australian Journal of Plant Physiology 13, 221-237.
10. Brown S.L., Warwick N.W.M. & Prychid C.J. (2013) Does aridity influence the morphology, distribution and accumulation of calcium oxalate crystals in Acacia (Leguminosae: Mimosoideae). Plant Physiology and Biochemistry 73, 219-228.
11. Bunce J.A. (2002) Sensitivity of infrared water vapor analyzers to oxygen concentration and errors in stomatal conductance. Photosynthesis Research 71, 273-276.
12. Burch D.E., Singleton E.B. & Williams D. (1962) Absorption line broadening in the infrared. Applied Optics 1, 359-363.
13. Busch F.A. (2013) Current methods for estimating the rate of photorespiration in leaves. Plant Biology 15, 648-655.
14. von Caemmerer S. (2000) Biochemical Models of Leaf Photosynthesis. CSIRO Publishing, Melbourne, Vic., Australia.
15. von Caemmerer S. (2013) Steady-state models of photosynthesis. Plant, Cell & Environment 36, 1617-1630.
16. von Caemmerer S. & Farquhar G.D. (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376-387.
17. 2 content and P nutrition on photosynthesis in white lupin (Lupinus albus L.). Plant, Cell & Environment 29, 844-853.
18. Cernusak L.A., Hutley L.B., Beringer J., Holtum J.A. & Turner B.L. (2011) Photosynthetic physiology of eucalypts along a sub-continental rainfall gradient in northern Australia. Agricultural and Forest Meteorology 151, 1462-1470.
19. Close D.G. & Beadle C.L. (2004) Total, and chemical fractions, of nitrogen and phosphorus in Eucalyptus seedling leaves: effects of species, nursery fertiliser management and transplanting. Plant and Soil 259, 85-95.
20. Conn S. & Gilliham M. (2010) Comparative physiology of elemental distributions in plants. Annals of Botany 105, 1081-1102.
21. 2 and climate warming. Global Change Biology 19, 3790-3807.
22. Denton M.D., Veneklaas E.J., Freimoser F.M. & Lambers H. (2007) Banksia species (Proteaceae) from severely phosphorus-impoverished soils exhibit extreme efficiency in the use and re-mobilization of phosphorus. Plant, Cell & Environment 30, 1557-1565.
23. Domingues T.F., Meir P., Feldpausch T., Saiz G., Venendaal E.M., Schrodt F., ... Lloyd J. (2010) Co-limitation of photosynthetic capacity by nitrogen and phosphorus in West Africa woodlands. Plant, Cell & Environment 33, 959-980.
24. 2 enrichment experiments in forest, grassland and desert. Global Change Biology 10, 2121-2138.
25. 2 affects photosynthetic responses in canopy pine and subcanopy deciduous trees over 10 years: a synthesis from Duke FACE. Global Change Biology 18, 223-242.
26. 3 plants. Oecologia 78, 9-19.
27. 3 species. Planta 149, 78-90.
28. Farquhar G.D., von Caemmerer S. & Berry J.A. (2001) Models of photosynthesis. Plant Physiology 125, 42-45.
29. 2: an unappreciated central player in photosynthesis. Plant Science 193, 70-84.
30. Franceschi V.R. & Nakata P.A. (2005) Calcium oxalate in plants: formation and function. Annual Review of Plant Biology 56, 41-71.
31. Galmés J., Flexas J., Keys A.J., Cifre J., Mitchell R.A.C., Madgwick P.J., ... Parry M.A.J. (2005) Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. Plant, Cell & Environment 28, 571-579.
32. Griffin E.A. & Burbidge A.A. (1990) Description of the region. In Nature Conservation, Landscape and Recreational Values of the Lesueur Area (eds A.A. Burbidge, S.D. Hopper & D. Van Leeuwen ), pp. 15-24. Environmental Protection Authority, Perth, WA, Australia.
33. Groenendijk M., Dolman A.J., van der Molen M.K., Leuning R., Arneth A., Delpierre N., ... Wohlfahrt G. (2011) Assessing parameter variability in a photosynthesis model within and between plant functional types using global Fluxnet eddy covariance data. Agricultural and Forest Meteorology 151, 22-38.
34. 2 and irradiance estimated with the variable J and online isotope discrimination methods. Plant, Cell & Environment 37, 1231-1249.
35. Hammond J.P. & White P.J. (2011) Sugar signaling in root responses to low phosphorus availability. Plant Physiology 156, 1033-1040.
36. 2 sensitivity explained by lack of glycerate reentry into the chloroplast. Photosynthesis Research 27, 169-178.
37. Havrir E.A. (1984) Oxalate metabolism by tobacco leaf discs. Plant Physiology 75, 505-507.
38. Holford I.C.R. (1997) Soil phosphorus: its measurement, and its uptake by plants. Australian Journal of Soil Research 35, 227-239.
39. Jacob J. & Lawlor D.W. (1993) In vivo photosynthetic electron transport does not limit photosynthetic capacity in phosphate deficient sunflower and maize leaves. Plant, Cell & Environment 16, 785-795.
40. 2 concentration, and light intensity on oxygen inhibition of photosynthesis in wheat leaves. Plant Physiology 43, 902-906.
41. Kattge J., Knorr W., Raddatz T. & Wirth C. (2009) Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global-scale terrestrial biosphere models. Global Change Biology 15, 976-991.
42. 2, and ribulose 1, 5-diphosphate carboxylase. Plant Physiology 54, 678-685.
43. Lambers H., Brundrett M.C., Raven J.A. & Hopper S.D. (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant and Soil 334, 11-31.
44. Lambers H., Cawthray G.R., Giavalisco P., Kuo J., Laliberté E., Pearse S.J., ... Turner B.L. (2012) Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use-efficiency. New Phytologist 196, 1098-1108.
45. Lambers H., Clode P., Hawkins H.-J., Laliberté E., Oliveira R.S., Reddell P., ... Weston P. (2015) Metabolic adaptations of the non-mycotrophic Proteaceae to soils with low phosphorus availability. In Phosphorus Metabolism in Plants in the Post-genomic Era: From Gene to Ecosystem (eds W.C. Plaxton & H. Lambers ), in press. Wiley-Blackwell, London.
46. Li-Cor (2008) Using the Li-6400/Li-6400XT Portable Photosynthesis System. Li-Cor, Lincoln, NE, USA.
47. Long S.P. & Bernacchi C. (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. Journal of Experimental Botany 54, 2393-2401.
48. Loustau D., Brahim M.B., Gaudillere J.-P. & Dreyer E. (1999) Photosynthetic responses to phosphorus nutrition in two-year-old maritime pine seedlings. Tree Physiology 19, 707-715.
49. Manter D.K. & Kerrigan J. (2004) A/C-i curve analysis across a range of woody plant species: influence of regression analysis parameters and mesophyll conductance. Journal of Experimental Botany 55, 2581-2588.
50. Matzek V. & Vitousek P.M. (2009) N:P stoichiometry and protein:RNA ratios in vascular plants: an evaluation of the growth-rate hypothesis. Ecology Letters 12, 765-771.
51. 13C, carbohydrates, and amino acid concentrations in Eucalyptus globulus change systematically according to flooding and water deficit treatment. Journal of Experimental Botany 61, 1785-1793.
52. Niklas K.J., Owens T., Reich P.B. & Cobb E.D. (2005) Nitrogen/phosphorus leaf stoichiometry and the scaling of plant growth. Ecology Letters 8, 636-642.
53. Ogren W.L. (1984) Photorespiration: pathways, regulation, and modification. Annual Review of Plant Physiology 35, 415-442.
54. Paul M.J. & Foyer C.H. (2001) Sink regulation of photosynthesis. Journal of Experimental Botany 52, 1383-1400.
55. 2 trends. Global Change Biology 19, 2117-2132.
56. i deficiency. Journal of Experimental Botany 52, 1083-1091.
57. 2: methodology, potential errors, and recommendations. Journal of Experimental Botany 60, 2217-2234.
58. R Core Development Team (2014) A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.
59. Raven J.A. (2012) Protein turnover and plant RNA and phosphorus requirements in relation to nitrogen fixation. Plant Science 188, 25-35.
60. Reich P.B., Oleksyn J. & Wright I.J. (2009) Leaf phosphorus influences the photosynthesis-nitrogen relation: a cross-biome analysis of 314 species. Oecologia 160, 207-212.
61. 2 cycle have become filled - others remain. Biochimica et Biophysica Acta 1763, 1496-1510.
62. c, max in earth system models. Photosynthesis Research 119, 15-29.
63. 2-insensitive photosynthesis in field grown plants. Plant Physiology 84, 658-664.
64. Sharkey T.D. (1985) Photosynthesis in intact leaves of C3 plants - physics, physiology and rate limitations. Botanical Review 51, 53-105.
65. Sharkey T.D. (1988) Estimating the rate of photorespiration in leaves. Physiologia Plantarum 73, 147-152.
66. Sharkey T.D. & Vassey T.L. (1989) Low oxygen inhibition of photosynthesis is caused by inhibition of starch synthesis. Plant Physiology 90, 385-387.
67. 3 leaves. Plant, Cell & Environment 30, 1035-1040.
68. Stitt M., Lunn J. & Usadel B. (2010) Arabidopsis and primary photosynthetic metabolism - more than the icing on the cake. The Plant Journal 61, 1067-1091.
69. Sulpice R., Ishihara H., Schlereth A., Cawthray G.R., Encke B., Giavalisco P., ... Lambers H. (2014) Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species. Plant, Cell & Environment 37, 1276-1298.
70. 2 concentrations. Plant, Cell & Environment 34, 580-591.
71. Thomas D.S., Montagu K.D. & Conroy J.P. (2006) Leaf inorganic phosphorus as a potential indicator of phosphorus status, photosynthesis and growth of Eucalyptus grandis seedlings. Forest Ecology and Management 223, 267-274.
72. Veneklaas E.J., Lambers H., Bragg J., Finnegan P.M., Lovelock C.E., Plaxton W.C., ... Raven J.A. (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytologist 195, 306-320.
73. Vitousek P.M., Porder S., Houlton B.Z. & Chadwick O.A. (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications 20, 5-15.
74. max - to leaf nitrogen, leaf phosphorus, and specific leaf area: a meta-analysis and modeling study. Ecology and Evolution 4, 3218-3235.
75. Walker B., Ariza L.S., Kaines S., Badger M.R. & Cousins A.B. (2013) Temperature response of in vivo Rubisco kinetics and mesophyll conductance in Arabidopsis thaliana: comparisons to Nicotiana tabacum. Plant, Cell & Environment 36, 2108-2119.
76. Wang Y.P., Law R.M. & Pak B. (2010) A global model of carbon, nitrogen and phosphorus cycles for the terrestrial biosphere. Biogeosciences 7, 2261-2282.
77. Williams M., Rastetter E.B., Fernandes D.N., Goulden M.L., Shaver G.R. & Johnson L.C. (1997) Predicting gross primary productivity in terrestrial ecosystems. Ecological Applications 7, 882-894.
78. Wingler A., Lea P.J., Quick W.P. & Leegood R.C. (2000) Photorespiration: metabolic pathways and their role in stress protection. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355, 1517-1529.
79. Yang X. & Post W.M. (2011) Phosphorus transformations as a function of pedogenesis: a synthesis of soil phosphorus data using Hedley fractionation method. Biogeosciences 8, 2907-2916.
80. 2 enrichment studies. New Phytologist 202, 803-822.