Gene expression changes in phosphorus deficient potato (Solanum tuberosum L.) leaves and the potential for diagnostic gene expression markers

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Hammond, John P ^a   Broadley, Martin R ^a   Bowen, Helen C ^b   Spracklen, William P ^b   Hayden, Rory M ^b   White, Philip J ^c  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHOCYANIN; CARBOHYDRATE; CHLOROPHYLL; LIPID; PATATIN; PHOSPHORUS; PLANT DNA; PLANT RNA; PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ABIOTIC STRESS; ARTICLE; BIOTIC STRESS; CARBOHYDRATE METABOLISM; CROP MANAGEMENT; DNA MICROARRAY; FERTILIZER APPLICATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GREENHOUSE; HYDROPONICS; LIPID METABOLISM; MARKER GENE; NONHUMAN; PHOSPHATE DEFICIENCY; PLANT GENETICS; PLANT GROWTH; PLANT LEAF; POTATO; PREDICTION; PROTEIN METABOLISM; SUPPORT VECTOR MACHINE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

SOLANUM TUBEROSUM;

GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; PHOSPHORUS; PLANT LEAVES; PLANT PROTEINS; SOLANUM TUBEROSUM; SUPPORT VECTOR MACHINES;

EID: 80052832951     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024606     Document Type: Article

References (92)

1. Holford ICR, (1997) Soil phosphorus: its measurement, and its uptake by plants. Aust J Soil Res 35: 227-239.
2. Jain A, Vasconcelos MJ, Raghothama KG, Sahi SV, (2007) Molecular mechanisms of plant adaptation to phosphate deficiency. Plant Breeding Rev 29: 359-419.
3. White PJ, Hammond JP, (2008) Phosphorus nutrition of terrestrial plants. In: White PJ, Hammond JP, editors. The Ecophysiology of Plant-Phosphorus Interactions Dordrecht Springer pp. 51-81.
4. White PJ, Hammond JP, (2009) The sources of phosphorus in the waters of Great Britain. J Environ Qual 38: 13-26.
5. Heffer P, Prud'homme MPR, Muirheid B, Isherwood KF, (2006) Phosphorus fertilisation: Issues and outlook. Proceedings 586 York International Fertiliser Society.
6. Raven JA, (2008) Phosphorus and the future. In: White PJ, Hammond JP, editors. The Ecophysiology of Plant-Phosphorus Interactions Dordrecht Springer pp. 271-283.
7. Cordell D, Drangert J-O, White S, (2009) The story of phosphorus: Global food security and food for thought. Global Environ Change 19: 292-305.
8. Frossard E, Condron LM, Oberson A, Sinaj S, Fardeau JC, (2000) Processes governing phosphorus availability in temperate soils. J Environ Qual 29: 15-23.
9. White PJ, Broadley MR, Hammond JP, Thompson AJ, (2005) Optimising the potato root system for phosphorus and water acquisition in low-input growing systems. Aspects Appl Biol 73: 111-118.
10. White PJ, Broadley MR, Greenwood DJ, Hammond JP, (2005) Genetic modifications to improve phosphorus acquisition by roots. Proceedings 568 York International Fertiliser Society.
11. George TS, Richardson AE, (2008) Potential and limitations to improving crops for enhanced phosphorus utilization. In: White PJ, Hammond JP, editors. The Ecophysiology of Plant-Phosphorus Interactions Dordrecht Springer pp. 247-270.
12. Lynch JP, Brown KM, (2008) Root strategies for phosphorus acquisition. In: White PJ, Hammond JP, editors. The Ecophysiology of Plant-Phosphorus Interactions Dordrecht Springer pp. 83-116.
13. Vance CP, (2008) Plants without arbuscular mycorrhizae. In: White PJ, Hammond JP, editors. The Ecophysiology of Plant-Phosphorus Interactions Dordrecht Springer pp. 117-142.
14. Fang Z, Shao C, Meng Y, Wu P, Chen M, (2009) Phosphate signaling in Arabidopsis and Oryza sativa. Plant Science 176: 170-180.
15. Hammond JP, Broadley MR, White PJ, King GJ, Bowen HC, et al. (2009) Shoot yield drives phosphorus use efficiency in Brassica oleracea and correlates with root architecture traits. J Exp Bot 60: 1953-1968.
16. Mengel K, Kirkby EA, (2001) Principles of Plant Nutrition. Fifth Edition Dordrecht Kluwer.
17. Müller R, Nilsson L, Nielsen LK, Nielsen TH, (2005) Interaction between phosphate starvation signalling and hexokinase-independent sugar sensing in Arabidopsis leaves. Physiol Plant 124: 81-90.
18. Teng S, Keurentjes J, Bentsink L, Koornneef M, Smeekens S, (2005) Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene. Plant Physiol 139: 1840-1852.
19. Amtmann A, Hammond JP, Armengaud P, White PJ, (2006) Nutrient sensing and signalling in plants: potassium and phosphorus. Adv Bot Res 3: 209-257.
20. Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P, (2006) Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140: 637-646.
21. Hoch WA, Zeldin EL, McCown BH, (2001) Physiological significance of anthocyanins during autumnal leaf senescence. Tree Physiol 21: 1-8.
22. Hammond JP, White PJ, (2008) Diagnosing phosphorus deficiency in crops. In: White PJ, Hammond JP, editors. The Ecophysiology of Plant-Phosphorus Interactions Dordrecht Springer pp. 225-246.
23. Smethurst PJ, (2000) Soil solution and other soil analyses as indicators of nutrient supply: a review. Forest Ecol Manag 138: 397-411.
24. Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, et al. (2003) Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol 132: 578-596.
25. Hammond JP, Broadley MR, Craigon DJ, Higgins J, Emmerson Z, et al. (2005) Using genomic DNA-based probe-selection to improve the sensitivity of high-density oligonucleotide arrays when applied to heterologous species. Plant Methods 1: 10.
26. Uhde-Stone C, Zinn KE, Ramirez-Yáñez M, Li A, Vance CP, et al. (2003) Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorus deficiency. Plant Physiol 131: 1064-1079.
27. Wasaki J, Yonetani R, Kuroda S, Shinano T, Yazaki J, et al. (2003) Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant Cell Environ 26: 1515-1523.
28. Wasaki J, Yonetani R, Shinano T, Kai M, Osaki M, (2003) Expression of the OsPI1 gene, cloned from rice roots using cDNA microarray, rapidly responds to phosphorus status. New Phytol 158: 239-248.
29. Wasaki J, Shinano T, Onishi K, Yonetani R, Yazaki J, et al. (2006) Transcriptomic analysis indicates putative metabolic changes caused by manipulation of phosphorus availability in rice leaves. J Exp Bot 57: 2049-2059.
30. Wu P, Ma L, Hou X, Wang M, Wu Y, et al. (2003) Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol 132: 1260-1271.
31. Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, et al. (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102: 11934-11939.
32. Graham MA, Ramírez M, Valdés-López O, Lara M, Tesfaye M, et al. (2006) Identification of candidate phosphorus stress induced genes in Phaseolus vulgaris through clustering analysis across several plant species. Funct Plant Biol 33: 789-797.
33. Morcuende R, Bari R, Gibon Y, Zheng WM, Pant BD, et al. (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30: 85-112.
34. Müller 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: 156-171.
35. Calderon-Vazquez C, Ibarra-Laclette E, Caballero-Perez J, Herrera-Estrella L, (2008) Transcript profiling of Zea mays roots reveals gene responses to phosphate deficiency at the plant- and species-specific levels. J Exp Bot 59: 2479-2497.
36. Zheng L, Huang F, Narsai R, Wu J, Giraud E, et al. (2009) Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiol 151: 262-274.
37. Hernández G, Valdés-López O, Ramírez M, Goffard N, Weiller G, et al. (2009) Global changes in the transcript and metabolic profiles during symbiotic nitrogen fixation in phosphorus-stressed common bean plants. Plant Physiol 151: 1221-1238.
38. Li L, Liu C, Lian X, (2010) Gene expression profiles in rice roots under low phosphorus stress. Plant Mol Biol 72: 423-432.
39. Hammond JP, Mayes S, Bowen HC, Graham NS, Hayden RM, et al. (2011) Regulatory hotspots control plant gene expression under varying soil phosphorus (P) supply in Brassica rapa. Plant Physiol 156: 1230-1241.
40. Kloosterman B, De Koeyer D, Griffiths R, Flinn B, Steuernagel B, et al. (2008) Genes driving potato tuber initiation and growth: identification based on transcriptional changes using the POCI array. Funct Integr Genom 2008, 8: 329-340.
41. Xu Z, Li K, Liu Z, Zhang K, Zhang J, (2007) Correlations between kinetic parameter of phosphate uptake and internal phosphorus concentrations in maize plants: Making it possible to estimate the status of phosphate uptake according to shoot phosphorus concentrations. Comm Soil Sci Plant Anal 38: 2519-2533.
42. Eisen MB, Spellman PT, Brown PO, Botstein D, (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868.
43. Huang CY, Roessner U, Eickmeier I, Genc Y, Callahan DL, et al. (2008) Metabolite profiling reveals distinct changes in carbon and nitrogen metabolism in phosphate-deficient barley plants (Hordeum vulgare L.). Plant Cell Physiol 49: 691-703.
44. Smith AP, Jain A, Deal RB, Nagarajan VK, Poling MD, et al. (2010) Histone H2A.Z regulates the expression of several classes of phosphate starvation response genes but not as a transcriptional activator. Plant Physiol 152: 217-225.
45. Hermans C, Hammond JP, White PJ, Verbruggen N, (2006) How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci 11: 610-617.
46. Sano T, Kuraya Y, Amino S-I, Nagata T, (1999) Phosphate as a limiting factor for the cell division of tobacco BY-2 cells. Plant Cell Physiol 40: 1-16.
47. Assuero SG, Mollier A, Pellerin S, (2004) The decrease in growth of phosphorus-deficient maize leaves is related to a lower cell production. Plant Cell Environ 27: 887-895.
48. Hammond JP, White PJ, (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59: 93-109.
49. Wallace T, (1961) The diagnosis of mineral deficiencies in plants by visual symptoms: a colour atlas and guide London Her Majesty's Stationery Office.
50. Ulrich A, (1993) Potato. In: Bennett WF, editors. Nutrient deficiencies & toxicities in crop plants St Paul APS Press pp. 149-156.
51. Hammond JP, White PJ, (2011) Update on sucrose signalling in plant responses to low P availability. Plant Physiol 156: 1033-1040.
52. Lee RB, Ratcliffe RG, Southon TE, (1990) 31P NMR measurements of the cytoplasmic and vacuolar Pi content of mature maize roots: Relationships with phosphorus status and phosphate fluxes. J Exp Bot 41: 1063-1078.
53. Mimura T, Dietz K-J, Kaiser W, Schramm MJ, Kaiser G, et al. (1990) Phosphate transport across biomembranes and cytosolic phosphate homeostasis in barley leaves. Planta 180: 139-146.
54. Wissuwa M, Gamat G, Ismail AM, (2005) Is root growth under phosphorus deficiency affected by source or sink limitations? J Exp Bot 56: 1943-1950.
55. Cakmak I, Hengeler C, Marschner H, (1994) Partitioning of shoot and root dry-matter and carbohydrates in bean-plants suffering from phosphorus, potassium and magnesium-deficiency. J Exp Bot 45: 1245-1250.
56. Cakmak I, Hengeler C, Marschner H, (1994) Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium-deficiency in bean-plants. J Exp Bot 45: 1251-1257.
57. Slabas T, (1997) Galactolipid biosynthesis genes and endosymbiosis. Trends Plant Sci 2: 161-162.
58. Dörmann P, Benning C, (2002) Galactolipids rule in seed plants. Trends Plant Sci 7: 112-118.
59. 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. Proc Natl Acad Sci USA 95: 1950-1955.
60. 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.
61. Andersson MX, Larsson KE, Tjellström H, Liljenberg C, Sandelius AS, (2005) Phosphate-limited oat. The plasma membrane and the tonoplast as major targets for phospholipid-to-glycolipid replacement and stimulation of phospholipases in the plasma membrane. J Biol Chem 280: 27578-27586.
62. 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 Environ 31: 1388-1398.
63. Kobayashi K, Masuda T, Takamiya K-I, Ohta H, (2006) Membrane lipid alteration during phosphate starvation is regulated by phosphate signaling and auxin/cytokinin cross-talk. Plant J 47: 238-248.
64. Cruz-Ramírez A, Oropeza-Aburto A, Razo-Hernández F, Ramírez-Chávez E, Herrera-Estrella L, (2006) Phospholipase Dζ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc Natl Acad Sci USA 103: 6765-6770.
65. Li M, Welti R, Wang X, (2006) Quantitative profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation. Roles of phospholipases Dζ1 and Dζ2 in phosphatidylcholine hydrolysis and digalactosyldiacylglycerol accumulation in phosphorus-starved plants. Plant Physiol 142: 750-761.
66. 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 J 56: 28-39.
67. Kopriva S, Mugford SG, Matthewman C, Koprivova A, (2009) Plant sulfate assimilation genes: redundancy versus specialization. Plant Cell Rep 28: 1769-1780.
68. Nakamura Y, Awai K, Masuda T, Yoshioka Y, Takamiya K, et al. (2005) A novel phosphatidylcholine-hydrolyzing phospholipase C induced by phosphate starvation in Arabidopsis. J Biol Chem 280: 7469-7476.
69. Li M, Qin C, Welti R, Wang X, (2006): Double knockouts of phospholipases Dζ1 and Dζ2 in Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiol 140: 761-770.
70. Shewry PR, (2003) Tuber storage proteins. Ann Bot 91: 755-769.
71. Senda K, Yoshioka H, Doke N, Kawakita K, (1996) A cytosolic phospholipase A2 from potato tissues appears to be patatin. Plant Cell Physiol 37: 347-353.
72. Mansfeld J, (2009) Plant phospholipases A2: perspectives on biotechnological applications. Biotechnol Lett 31: 1373-1380.
73. Rocha-Sosa M, Sonnewald U, Frommer W, Stratmann M, Schell J, et al. (1989) Both developmental and metabolic signals activate the promoter of a class I patatin gene. EMBO J 8: 23-29.
74. Rietz S, Dermendjiev G, Oppermann E, Tafesse FG, Effendi Y, et al. (2010) Roles of Arabidopsis patatin-related phospholipases A in root development are related to auxin responses and phosphate deficiency. Mol Plant 3: 524-538.
75. Furey TS, Cristianini N, Duffy N, Bednarski DW, Schummer M, et al. (2000) Support vector machine classification and validation of cancer tissue samples using microarray expression data. Bioinformatics 16: 6-914.
76. Statnikov A, Aliferis CF, Tsamardinos I, Hardin D, Levy S, (2005) A comprehensive evaluation of multicategory classification methods for microarray gene expression cancer diagnosis. Bioinformatics 21: 631-643.
77. Walworth JL, Muniz JE, (1993) A compendium of tissue nutrient concentrations for field-grown potatoes. Am Potato J 70: 579-597.
78. Khiari L, Parent L-E, Tremblay N, (2001) The phosphorus compositional nutrient diagnosis range for potato. Agron J 93: 815-819.
79. White PJ, Wheatley RE, Hammond JP, Zhang K, (2007) Minerals, soils and roots. In: Vreugdenhil D, editors. Potato biology and biotechnology: advances and perspectives Oxford Elsevier Science pp. 739-752.
80. Craigon DJ, James N, Okyere J, Higgins J, Jotham J, et al. (2005) NASCArrays: A repository for microarray data generated by NASC's transcriptomics service. Nucleic Acids Res 32: D575-D577.
81. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
82. Scheible WR, Morcuende R, Czechowski T, Fritz C, Osuna D, et al. (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136: 2483-2499.
83. Wang R, Okamoto M, Xing X, Crawford NM, (2004) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6-pPhosphate, iron, and sulfate metabolism. Plant Physiol 132: 556-567.
84. Poirier Y, Thoma S, Somerville C, Schiefelbein J, (1991) A mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiol 97: 1087-1093.
85. Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, et al. (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50: 347-363.
86. Hurry V, Strand Å, Furbank R, Stitt M, (2000) The role of inorganic phosphate in the development of freezing tolerance and the acclimatization of photosynthesis to low temperature is revealed by the pho mutants of Arabidopsis thaliana. Plant J 24: 383-396.
87. Broadley MR, Bowen HC, Cotterill HL, Hammond JP, Meacham MC, et al. (2003) Variation in the shoot calcium content of angiosperms. J Exp Bot 54: 1431-1446.
88. Bradstreet RB, (1965) The Kjeldahl method for organic nitrogen London Academic Press.
89. Broadley MR, Hammond JP, King GJ, Astley D, Bowen HC, et al. (2008) Shoot calcium (Ca) and magnesium (Mg) concentrations differ between subtaxa, are highly heritable, and associate with potentially pleiotropic loci in Brassica oleracea. Plant Physiol 146: 1707-1720.
90. Olsen SR, Cole CV, Watanabe FS, Dean LA, (1954) Estimation of available phosphorus by extraction with sodium bicarbonate (Circular 39) Washington DC USDA.
91. Department for Environment, Food and Rural Affairs (2000) Fertiliser recommendations for agricultural and horticultural crops (RB209): 7th Ed London HMSO.
92. Hammond JP, Bowen HC, White PJ, Mills V, Pyke KA, et al. (2006) A comparison of the Thlaspi caerulescens and Thlaspi arvense transcriptomes. New Phytol 170: 239-260.