Genetic responses to phosphorus deficiency

Annals of Botany

Volumn 94, Issue 3, 2004, Pages 323-332

  Hammond, John P ^a   Broadley, Martin R ^b   White, Philip J ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Arabidopsis thaliana; cis regulatory elements; Gene expression; Micro arrays; Phosphate; Phosphorus; Roots

Indexed keywords

GENE EXPRESSION; PHOSPHORUS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

PHOSPHORUS;

ARABIDOPSIS; BIOLOGICAL MODEL; GENE; GENE EXPRESSION REGULATION; GENETICS; GENOME; METABOLISM; MICROARRAY ANALYSIS; PLANT; PROMOTER REGION; REVIEW;

ARABIDOPSIS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENOME, PLANT; MICROARRAY ANALYSIS; MODELS, BIOLOGICAL; PHOSPHORUS; PLANTS; PROMOTER REGIONS (GENETICS);

EID: 6944225214     PISSN: 03057364     EISSN: None     Source Type: Journal    
DOI: 10.1093/aob/mch156     Document Type: Article

References (82)

1. Al-Ghazi Y, Muller B, Pinloche S, Tranbarger TG, Nacry P, Rossignol M, Tardieu F, Doumas P. 2003. Temporal responses of Arabidopsis root architecture to phosphate starvation: evidence for the involvement of auxin signalling. Plant, Cell and Environment 26: 1053-1066.
2. Andersson MX, Stridh MH, Larsson KE, Liljenberg C, Sandelius AE. 2003. Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyliacylglycerol. FEBS Letters 537: 128-132.
3. Bariola PA, Howard CJ, Taylor CB, Verburg MT, Jaglan VD, Green PJ. 1994. The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant Journal 6: 673-685.
4. Bates TR, Lynch JP. 1996. Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant, Cell and Environment 19: 529-538.
5. Blackwell TK, Weintraub H. 1990. Differences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection. Science 250: 1104-1110.
6. Borch K, Bouma TJ, Lynch JP, Brown KM. 1999. Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant, Cell and Environment 22: 425-431.
7. Burleigh SH, Harrison MJ. 1999. The down regulation of Mt4-like genes by phosphate fertilization occurs systematically and involves phosphate translocation to the shoots. Plant Physiology 119: 241-248.
8. Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ. 2003. Dissecting Arabidopsis lateral root development. Trends in Plant Science 8: 165-171.
9. Casson SA, Lindsey K. 2003. Genes and signalling in root development. New Phytologist 158: 11-38.
10. Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA, et al. 2002. Expression profile matrix of arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14: 559-574.
11. 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.
12. Coello P. 2002. Purification and characterisation of secreted acid phosphatase in phosphorus-deficient Arabidopsis thaliana. Physiologia Plantarum 116: 293-298.
13. Daram P, Brunner S, Rausch C, Steiner C, Amrhein N, Bucher M. 1999. Pht2;1 encodes a low affinity phosphate transporter from arabidopsis. Plant Cell 11: 2153-2166.
14. Delhaize E, Hebb DM, Ryan PR. 2001. Expression of a Pseudomonas aeruginosa citrate synthase gene in tobacco is not associated with either enhanced citrate accumulation or efflux. Plant Physiology 125: 2059-2067.
15. del Pozo JC, Allona I, Rubio V, Leyva A, de la Peña A, Aragoncillo C, Paz-Ares J. 1999. A type 5 acid phosphatase gene from Arabidopsis thaliana is induced by phosphate starvation and by some other types of phosphate mobilising/oxidative stress conditions. Plant Journal 19: 579-589.
16. Duff SMG, Plaxton WC, Lefebvre DD. 1991. Phosphate-starvation response in plant cells: De novo synthesis and degradation of acid phosphatases. Proceedings of the National Academy of Sciences of the USA 88: 9538-9542.
17. Essigmann B, Güler S, Narang RA, Linke D, Benning C. 1998. Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the USA 95: 1950-1955.
18. Eulgem T, Rushton PJ, Robatzek S, Somssich IE. 2000. The WRKY superfamily of plant transcription factors. Trends in Plant Science 5: 199-206.
19. Fitter AH, Hay RKM. 2002. Environmental physiology of plants. London: Academic Press.
20. Flowers TJ. 2004. Improving crop salt tolerance. Journal of Experimental Botany 55: 307-319.
21. Forde B, Lorenzo H. 2001. The nutritional control of root development. Plant and Soil 232: 51-68.
22. Franco-Zorrilla JM, González E, Bustos R, Linhares F, Leyva A, Paz-Ares J. 2004. The transcriptional control of plant responses to phosphate limitation. Journal of Experimental Botany 55: 285-293.
23. Fu YH, Marzluf GA. 1990. NIT-2, the major positive-acting nitrogen regulatory gene of Neurospora crassa, encodes a sequence-specific DNA-binding protein. Proceedings of the National Academy of Sciences of the USA 87: 5331-5335.
24. Greenwood DJ, Karpinets TV, Stone DA. 2001. Dynamic model for the effects of soil P and fertilizer P on crop growth, P uptake and soil P in arable cropping: Model description. Annals of Botany 88: 279-291.
25. 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.
26. Haran S, Logendra S, Seskar M, Bratanova M, Raskin I. 2000. Characterization of arabidopsis acid phosphatase promoter and regulation of acid phosphatase expression. Plant Physiology 124: 615-626.
27. Hoch WA, Zeldin EL, McCown BH. 2001. Physiological significance of anthocyanins during autumnal leaf senescence. Tree Physiology 21: 1-8.
28. Hodge A. 2004. The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist 162: 9-24.
29. Jungk A. 2001. Root hairs and the acquisition of plant nutrients from soil. Journal of Plant Nutrition and Soil Science 164: 121-129.
30. Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES. 2002. Expression profile analysis of the low-oxygen response in arabidopsis root cultures. Plant Cell 14: 2481-2494.
31. Kuiper D, Schuit J, Kuiper PJC. 1988. Effects of internal and external cytokinin concentrations on root growth and shoot to root ratio of Plantago major ssp pleiosperma at different nutrient conditions. Plant and Soil 111: 231-236.
32. Lee RB. 1993. Control of net uptake of nutrients by regulation of influx in barley plants recovering from nutrient deficiency. Annals of Botany 72: 223-230.
33. Li D, Zhu H, Liu K, Liu X, Leggewie G, Udvardi M, Wang D. 2002. Purple acid phosphatases of Arabidopsis thaliana. Journal of Biological Chemistry 277: 27772-27781.
34. Linkohr BI, Williamson LC, Fitter AH, Leyser HMO. 2002. Nitrate and phosphate availability and distribution effects on root system architecture of Arabidopsis. Plant Journal 29: 751-760.
35. Liu C, Muchhal US, Raghothama KG. 1997. Differential expression of TPSI1, a phosphate starvation-induced gene in tomato. Plant Molecular Biology 33: 867-874.
36. López-Bucio J, Nieto-Jacobo MF, Ramírez-Rodríguez V, Herrera-Estrella L. 2000a. Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Science 160: 1-13.
37. López-Bucio J, de la Vega OM, Guevara-García A, Herrera-Estrella L. 2000b. Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate. Nature Biotechnology 18: 450-453.
38. López-Bucio J, Hernández-Abreu E, Sánchez- Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L. 2002. Phosphate availability alters architecture and causes changes in hormone sensitivity in the arabidopsis root system. Plant Physiology 129: 244-256.
39. Luan S. 2003. Protein phosphatases in plants. Annual Review of Plant Biology 54: 63-92.
40. Lynch JP, Brown KM. 2001. Topsoil foraging - an architectural adaptation of plants to low phosphorus availability. Plant and Soil 237: 225-237.
41. Ma Z, Bielenberg DG, Brown KM, Lynch JP. 2001. Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant, Cell and Environment 24: 459-467.
42. Ma Z, Baskin TI, Brown KM, Lynch JP. 2003. Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiology 131: 1381-1390.
43. Maathuis FJM, Filatov V, Herzyk P, Krijger GC, Axelsen KB, Chen SX, Green BJ, Li Y, Madagan KL, Sánchez-Fernández R, et al. 2003. Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress. Plant Journal 35: 675-692.
44. Martin C, Paz-Ares J. 1997. MYB transcription factors in plants. Trends in Genetics 13: 67-73.
45. Martín AC, del Pozo JC, Iglesias J, Rubio V, Solano R, de la Peña A, Leyva A, Paz-Ares J. 2000. Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant Journal 24: 559-567.
46. Michael G. 2001. The control of root hair formation: suggested mechanisms. Journal of Plant Nutrition and Soil Science 164: 111-119.
47. Miller SS, Liu J, Allan DL, Menzhuber CJ, Fedorova M, Vance CP. 2001. Molecular control of acid phosphatase secretion into the rhizosphere of proteoid roots from phosphorus-stressed white lupin. Plant Physiology 127: 594-606.
48. Mudge SR, Rae AL, Diatloff E, Smith FW. 2002. Expression analysis suggests novel roles for members of Pht1 family of phosphate transporters in Arabidopsis. Plant Journal 31: 341-353.
49. Mudge SR, Smith FW, Richardson AE. 2003. Root-specific and phosphate-regulated expression of phytase under the control of a phosphate transporter promoter enables Arabidopsis to grow on phytate as a sole P source. Plant Science 165: 871-878.
50. Mukatira UT, Liu C, Varadarajan DK, Raghothama KG. 2001. Negative regulation of phosphate starvation-inducible genes. Plant Physiology 127: 1854-1862.
51. Müller M, Schmidt W. 2004. Environmentally induced plasticity of root hair development in arabidopsis. Plant Physiology 134: 409-419.
52. Oshima Y, Ogawa N, Harashima S. 1996. Regulation of phosphatase synthesis in Saccharomyces cerevisiae - a review. Gene 179: 171-177.
53. Plaxton WC, Carswell MC. 1999. Metabolic aspects of phosphate starvation in plants. In: HR Lerner, ed. Plant responses to environmental stresses: from phytohormones to genome reorganisation. New York: Dekker, 349-372.
54. Rae AL, Jarmey JM, Mudge SR, Smith FW. 2004. Over-expression of a high-affinity phosphate transporter in transgenic barley plants does not enhance phosphate uptake rates. Functional Plant Biology 31: 141-148.
55. Raghothama KG. 1999. Phosphate acquisition. Annual Review of Plant Physiology and Plant Molecular Biology 50: 665-693.
56. Rausch C, Bucher M. 2002. Molecular mechanisms of phosphate transport in plants. Planta 216: 23-37.
57. Richardson AE, Hodobas PA, Hayes JE. 2001. Extracellular secretion of Aspergillus phytate from Arabidopsis roots enables plants to obtain phosphorus from phytate. Plant Journal 25: 641-649.
58. Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, Paz-Ares J. 2001. A conserved MYB transcription factor in phosphate starvation signalling both in vascular plants and in unicellular algae. Genes and Development 15: 2122-2133.
59. Runge-Metzger A. 1995. Closing the cycle: obstacles to efficient P management for improved global security. In: H Tiessen, ed. Phosphorus in the global environment: transfers, cycles and management. Chichester: John Wiley and Sons, 27-42.
60. Schindler U, Beckmann H, Cashmore AR. 1992. TGA1 and G-box binding factors: two distinct classes of arabidopsis leucine zipper proteins compete for the G-box-like element TGACGTGG. Plant Cell 4: 1309-1319.
61. Schmidt W, Schikora A. 2001. Different pathways are involved in phosphate and iron stress-induced alterations of root epidermal cell development. Plant Physiology 125: 2078-2084.
62. Schünmann PHD, Richardson AE, Smith FW, Delhaize E. 2004. Characterisation of promoter expression patterns derived from the Pht1 phosphate transporter genes of barley (Hordeum vulgare L.). Journal of Experimental Botany 55: 855-865.
63. Shinozaki K, Yamaguchi-Shinozaki K. 2000. Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signalling pathways. Current Opinion in Plant Biology 3: 217-223.
64. Sinclair TR, Purcell LC, Sneller CH. 2004. Crop transformation and the challenge to increase yield potential. Trends in Plant Science 9: 70-75.
65. Smith FW, Mudge SR, Rae AL, Glassop D. 2003. Phosphate transport in plants. Plant and Soil 248: 71-83.
66. Stitt M, Hurry V. 2002. A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. Current Opinion in Plant Biology 5: 199-206.
67. Tang Z, Sadka A, Morrishige DT, Mullet JE. 2001. Homeodomain leucine zipper proteins bind to the phosphate response domain of the soybean VspB tripartite promoter. Plant Physiology 125: 797-809.
68. Tanimoto M, Roberts K, Dolan L. 1995. Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. Plant Journal 8: 943-948.
69. Toyota K, Koizumi N, Sato F. 2003. Transcriptional activation of phosphoenolpyruvate carboxylase by phosphorus deficiency in tobacco. Journal of Experimental Botany 54: 961-969.
70. Uhde-Stone C, Zinn KE, Ramirez-Yáñez M, Li A, Vance CP, Allan DL. 2003. Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorous deficiency. Plant Physiology 131: 1064-1079.
71. Vance CP, Uhde-Stone C, Allan DL. 2003. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytologist 157: 423-447.
72. van der Rest B, Boisson A-M, Gout E, Bligny R, Douce R. 2003. Glycerophosphocholine metabolism in higher plant cells. Evidence of a new glyceryl-phosphodiester phosphodiesterase. Plant Physiology 130: 244-255.
73. Venter M, Botha FC. 2004. Promoter analysis and transcriptional profiling: Integration of genetic data enhances understanding of gene expression. Physiologia Plantarum 120: 74-83.
74. Versaw WK, Harrison MJ. 2002. A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell 14: 1751-1766.
75. Wang Y-H, Garvin DF, Kochian LV. 2002. Rapid induction of regulatory and transporter genes in response to phosphorus, potassium, and iron deficiencies in tomato roots. Evidence for cross talk and root/rhizosphere-mediated signals. Plant Physiology 130: 1361-1370.
76. Wasaki J, Yonetani R, Shinano T, Kai M, Osaki M. 2003a. Expression of the OsPI1 gene, cloned from rice roots using cDNA microarray, rapidly responds to phosphorus status. New Phytologist 158: 239-248.
77. Wasaki J, Yonetani R, Kuroda S, Shinano T, Yazaki J, Fujii F, Shimbo K, Yamamoto K, Sakata K, Sasaki T, et al. 2003b. Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant, Cell and Environment 26: 1515-1523.
78. Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO. 2001. Phosphate availability regulates root system architecture in arabidopsis. Plant Physiology 126: 875-882.
79. Withers PJA, Edwards AC, Foy RH. 2001. Phosphorus cycling in UK agriculture and implications for phosphorus loss from soil. Soil Use and Management 17: 139-149.
80. Wu P, Ma L, Hou X, Wang M, Wu Y, Liu F, Deng XW. 2003. Phosphate starvation triggers distinct alterations of genome expression in arabidopsis roots and leaves. Plant Physiology 132: 1260-1271.
81. Wykoff DD, Grossman AR, Weeks DP, Usuda H, Shimogawara K. 1999. Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. Proceedings of the National Academy of Sciences of the USA 96: 15336-15341.
82. Yu B, Xu C, Benning C. 2002. Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proceedings of the National Academy of Sciences of the USA 99: 5732-5737.