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

Volumn 196, Issue 4, 2012, Pages 1098-1108

  Lambers, Hans ^a   Cawthray, Gregory R ^a   Giavalisco, Patrick ^b   Kuo, John ^a   Laliberté, Etienne ^a   Pearse, Stuart J ^a   Scheible, Wolf Rüdiger ^b,c   Stitt, Mark ^b   Teste, François ^a   Turner, Benjamin L ^a,d  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c PLANT BIOLOGY DIVISION   (United States)

^d SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

Author keywords

Banksia; Galactolipids; Hakea; Phospholipids; Photosynthetic phosphorus use efficiency (PPUE); Sulfolipids

Indexed keywords

GALACTOLIPID; LIPID; PHOSPHORUS; SULFOLIPIDS;

DICOTYLEDON; LEAF; LIPID; NUTRIENT USE EFFICIENCY; PHOSPHORUS; PHOTOSYNTHESIS; SOIL CHEMISTRY;

ARABIDOPSIS; ARTICLE; AUSTRALIA; CHEMISTRY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOTOSYNTHESIS; PLANT LEAF; PROTEACEAE; SOIL;

ARABIDOPSIS; GALACTOLIPIDS; LIPIDS; PHOSPHORUS; PHOTOSYNTHESIS; PLANT LEAVES; PROTEACEAE; SOIL; SOUTH AUSTRALIA; WESTERN AUSTRALIA;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BANKSIA; HAKEA; PROTEACEAE;

EID: 84868536316     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2012.04285.x     Document Type: Article

References (63)

1. Andersson MX, Larsson KE, Tjellström H, Liljenberg C, Sandelius AS. 2005. Phosphate-limited oat. Journal of Biological Chemistry 280: 27578-27586.
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 Letters 537: 128-132.
3. Bahl J, Francke B, Monéger R. 1976. Lipid composition of envelopes, prolamellar bodies and other plastid membranes in etiolated, green and greening wheat leaves. Planta 129: 193-201.
4. 2, activation of ribulose bisphosphate carboxylase and amounts of ribulose bisphosphate and 3-phosphoglycerate in spinach leaves. Photosynthesis Research 15: 133-141.
5. Burbidge AA, Hopper SD, Van Leeuwen S, eds. 1990. A report to the Environmental Protection Authority from the Department of Conservation and Land Management. Bulletin 424. Perth, Australia: Environmental Protection Authority.
6. 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. Physiologia Plantarum 54: 309-317.
7. Cheesman AW, Turner BL, Reddy KR. 2010. Interaction of phosphorus compounds with anion-exchange membranes: implications for soil analysis. Soil Science Society of America Journal 74: 1607-1612.
8. Ciereszko I, Johansson H, Hurry V, Kleczkowski LA. 2001. Phosphate status affects the gene expression, protein content and enzymatic activity of UDP-glucose pyrophosphorylase in wild-type and pho mutants of Arabidopsis. Planta 212: 598-605.
9. Conn S, Gilliham M. 2010. Comparative physiology of elemental distributions in plants. Annals of Botany 105: 1081-1102.
10. Cowan A. 2006. Phospholipids as plant growth regulators. Plant Growth Regulation 48: 97-109.
11. Cruz-Ramírez A, Oropeza-Aburto A, Razo-Hernández F, Ramírez-Chávez E, Herrera-Estrella L. 2006. Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proceedings of the National Academy of Sciences, USA 103: 6765-6770.
12. Denton MD, Veneklaas EJ, Freimoser FM, 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.
13. Dörmann P 2007. Galactolipids in plant membranes. Encyclopedia of Life Sciences: eLS. Chichester, UK: John Wiley & Sons Ltd. http://www.els.net. doi: 10.1002/9780470015902.a0020100.
14. Dörmann P, Benning C. 2002. Galactolipids rule in seed plants. Trends in Plant Science 7: 112-118.
15. Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie S, Fagan W, Schade J et al. 2003. Growth rate - stoichiometry couplings in diverse biota. Ecology Letters 6: 936-943.
16. Forde J, Steer MW. 1976. The use of quantitative electron microscopy in the study of lipid composition of membranes. Journal of Experimental Botany 27: 1137-1141.
17. Foyer C, Spencer C. 1986. The relationship between phosphate status and photosynthesis in leaves. Effects on intracellular orthophosphate distribution, photosynthesis and assimilate partitioning. Planta 167: 369-375.
18. Fredeen AL, Raab TK, Rao IM, Terry N. 1990. Effects of phosphorus nutrition on photosynthesis in Glycine max (L.) Merr. Planta 181: 399-405.
19. Gaude N, Nakamura Y, Scheible W-R, Ohta H, Dörmann P. 2008. Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis. Plant Journal 56: 28-39.
20. 34S isotope labelling, in combination with high-resolution mass spectrometry. The Plant Journal 68: 364-376.
21. Gilbert N. 2009. The disappearing nutrient. Nature 461: 716-718.
22. Griffin EA, Burbidge AA 1990. Vegetation. In: Burbidge AA, Hopper SD, Van Leeuwen D eds. A report to the Environmental Protection Authority from the Department of Conservation and Land Management. Bulletin 424. Perth, Australia: Environmental Protection Authority, 15-24.
23. Groom PK, Lamont BB, Markey AS. 1997. Influence of leaf type and plant age on leaf structure and sclerophylly in Hakea (Proteaceae). Australian Journal of Botany 45: 827-838.
24. Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May ST, Rahn C, Swarup R, Woolaway KE, White PJ. 2003. Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiology 132: 578-596.
25. Hammond JP, Broadley MR, Bowen HC, Spracklen WP, Hayden RM, White PJ. 2011. Gene expression changes in phosphorus deficient potato (Solanum tuberosum L.) leaves and the potential for diagnostic gene expression Markers. PLoS ONE 6: e24606.
26. Härtel H, Dörmann P, Benning C. 2000. DGD1-independent biosynthesis of extraplastidic galactolipids after phosphate deprivation in Arabidopsis. Proceedings of the National Academy of Sciences, USA 97: 10649-10654.
27. 2 to adaxial mesophyll cells in thick sclerophylls. Plant, Cell & Environment 32: 1596-1611.
28. 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.
29. Heldt HW, Chon CJ, Maronde D, Herold A, Stankovic ZS, Walker DA, Kraminer A, Kirk MR, Heber U. 1977. Role of orthophosphate and other factors in the regulation of starch formation in leaves and isolated chloroplasts. Plant Physiology 59: 1146-1155.
30. Hendershot WH, Lalande H, Duquette M 2008. Chapter 16: Soil reaction and exchangeable acidity. In: Carter MR, Gregorich EG, eds. Soil sampling and methods of analysis, 2nd edn. Boca Raton, FL, USA: Canadian Society of Soil Science and CRC Press, 173-178.
31. Hopper SD. 2009. OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant and Soil 322: 49-86.
32. Hopper SD, Gioia P. 2004. The Southwest Australian Floristic Region: evolution and conservation of a global hotspot of biodiversity. Annual Review of Ecology, Evolution and Systematics 35: 623-650.
33. Hummel J, Segu S, Li Y, Irgang S, Jueppner J, Giavalisco P. 2011. Ultra performance liquid chromatography and high resolution mass spectrometry for the analysis of plant lipids. Frontiers in Plant Science 2: 1-17.
34. Jordan GJ, Weston PH, Carpenter RJ, Dillon RA, Brodribb TJ. 2008. The evolutionary relations of sunken, covered, and encrypted stomata to dry habitats in Proteaceae. American Journal of Botany 95: 521-530.
35. Jouhet J, Maréchal E, Baldan B, Bligny R, Joyard J, Block MA. 2004. Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria. The Journal of Cell Biology 167: 863-874.
36. Kursar TA, Coley PD. 1992. Delayed greening in tropical leaves: an antiherbivore defense? Biotropica 24: 256-262.
37. Laliberté E, Turner BL, Costes T, Pearse SJ, Wyrwolll K-H, Zemunik G, Lambers H. 2012. Experimental assessment of nutrient limitation along a 2-million year dune chronosequence in the south-western Australia biodiversity hotspot. Journal of Ecology 100: 631-642.
38. Lambers H, Bishop JG, Hopper SD, Laliberté E, Zúñiga-Feest A. 2012. Phosphorus-mobilisation ecosystem engineering: the roles of cluster roots and carboxylate exudation in young P-limited ecosystems. Annals of Botany 110: 329-348.
39. 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 and Soil 334: 11-31.
40. Lambers H, Finnegan PM, Laliberté E, Pearse SJ, Ryan MH, Shane MW, Veneklaas EJ. 2011. Phosphorus nutrition of Proteaceae in severely phosphorus-impoverished soils: are there lessons to be learned for future crops? Plant Physiology 156: 1058-1066.
41. Lambers H, Raven JA, Shaver GR, Smith SE. 2008. Plant nutrient-acquisition strategies change with soil age. Trends in Ecology and Evolution 23: 95-103.
42. McArthur WM. 1991. Reference soils of south-western Australia. South Perth, Australia: Department of Agriculture Western Australia.
43. McArthur WM, Bettenay E. 1974. Development and distribution of soils of the Swan Coastal Plain, Western Australia. Melbourne, Australia: CSIRO.
44. Mimura T. 1995. Homeostasis and transport of inorganic phosphate in plants. Plant and Cell Physiology 36: 1-7.
45. Morcuende R, Bari R, Gibon Y, Zheng W, Pant BD, Blasing O, Usadel B, Czechowski T, Udvardi MK, Stitt M, et al. 2007. Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant, Cell & Environment 30: 85-112.
46. Motomizu S, Wakimoto T, Toei K. 1983. Spectrophotometric determination of phosphate in river waters with molybdate and malachite green. Analyst 108: 361-367.
47. Pate JS, Bell TL. 1999. Application of the ecosystem mimic concept to the species-rich Banksia woodlands of Western Australia. Agroforestry Systems 45: 303-341.
48. Pinheiro JC, Bates DM. 2000. Mixed-effects models in S and S-PLUS. New York, NY, USA: Springer.
49. Playford PE, Cockbain AE, Low GH. 1976. Geology of the Perth Basin, Western Australia. Perth, Australia: Geological Survey, Western Australia.
50. Poirier Y, Thoma S, Somerville C, Schiefelbein J. 1991. Mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiology 97: 1087-1093.
51. Rao IM, Terry N. 1989. Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet: I. Changes in growth, gas exchange, and Calvin cycle Enzymes. Plant Physiology 90: 814-819.
52. Reich PB, Oleksyn J, Wright IJ. 2009. Leaf phosphorus influences the photosynthesis-nitrogen relation: a cross-biome analysis of 314 species. Oecologia 160: 207-212.
53. Roth-Nebelsick A, Hassiotou F, Veneklaas EJ. 2009. Stomatal crypts have small effects on transpiration: a numerical model analysis. Plant Physiology 151: 2018-2027.
54. Shane MW, Lambers H. 2005. Manganese accumulation in leaves of Hakea prostrata(Proteaceae) and the significance of cluster roots for micronutrient uptake as dependent on phosphorus supply. Physiologia Plantarum 124: 441-450.
55. Shane MW, McCully ME, Lambers H. 2004. Tissue and cellular phosphorus storage during development of phosphorus toxicity in Hakea prostrata (Proteaceae). Journal of Experimental Botany 55: 1033-1044.
56. 2 uptake results from limitation of triose phosphate utilization. Plant Physiology 81: 1123-1129.
57. 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.
58. Stitt M, Quick WP. 1989. Photosynthetic carbon partitioning: its regulation and possibilities for manipulation. Physiologia Plantarum 77: 633-641.
59. Tjellström H, Andersson MX, Larsson KE, Sandelius AS. 2008. Membrane phospholipids as a phosphate reserve: the dynamic nature of phospholipid-to-digalactosyl diacylglycerol exchange in higher plants. Plant, Cell & Environment 31: 1388-1398.
60. Tjellström H, Hellgren LI, Wieslander Å, Sandelius AS. 2010. Lipid asymmetry in plant plasma membranes: phosphate deficiency-induced phospholipid replacement is restricted to the cytosolic leaflet. The FASEB Journal 24: 1128-1138.
61. Turner BL, Romero TE. 2009. Short-term changes in extractable inorganic nutrients during storage of tropical rain forest soils. Soil Science Society of America Journal 73: 1972-1979.
62. Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price C, Scheible W-R, Shane MW, White PJ, et al. 2012. Opportunities for improving phosphorus-use efficiency in crop plants. New Phytologist 195: 306-320.
63. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, et al. 2004. The worldwide leaf economics spectrum. Nature 428: 821-827.