Phosphate concentration and arbuscular mycorrhizal colonisation influence the growth, yield and expression of twelve PHT1 family phosphate transporters in foxtail millet (Setaria italica)

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Ceasar, S Antony ^a   Hodge, Angela ^b   Baker, Alison ^a   Baldwin, Stephen A ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATE; PHOSPHATE TRANSPORTER; PROTEIN PHT1; UNCLASSIFIED DRUG;

ARBUSCULAR MYCORRHIZA; ARTICLE; BIOINFORMATICS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENVIRONMENT; FOXTAIL MILLET; FUNGAL COLONIZATION; FUNNELIFORMIS MOSSEAE; MULTIGENE FAMILY; NONHUMAN; PHT1 GENE; PHYLOGENY; PLANT GENE; PLANT GROWTH; PLANT LEAF; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHOOT; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MYCORRHIZA; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; SETARIA (PLANT);

SETARIA ITALICA;

MYCORRHIZAE; PHOSPHATE TRANSPORT PROTEINS; PHOSPHATES; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; SETARIA PLANT;

EID: 84907584298     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0108459     Document Type: Article

References (77)

1. Raghothama KG (1999) Phosphate acquisition. Annual Review of Plant Physiology and Plant Molecular Biology 50: 665-693.
2. Atkinson D (1973) Some general effects of phosphorus deficiency on growth and development. New Phytologist 72: 101-111.
3. Sicher RC, Kremer DF (1988) Effects of phosphate deficiency on assimilate partitioning in barley seedlings. Plant Science 57: 9-17.
4. Fredeen AL, Rao IM, Terry N (1989) Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max. Plant Physiology 89: 225-230.
5. Hajabbasi MA, Schumacher TE (1994) Phosphorus effects on root-growth and development in 2 maize genotypes. Plant and Soil 158: 39-46.
6. Rao IM, Terry N (1989) Leaf phosphate status, photosynthesis, and carbon partitioning in sugar-beet. 1.Changes in growth, gas-exchange, and Calvin cycle enzymes. Plant Physiology 90: 814-819.
7. Lynch J, Lauchli A, Epstein E (1991) Vegetative growth of the common bean in response to phosphorus-nutrition. Crop Science 31: 380-387.
8. Rodriguez D, Pomar MC, Goudriaan J (1998) Leaf primordia initiation, leaf emergence and tillering in wheat (Triticum aestivum L.) grown under lowphosphorus conditions. Plant and Soil 202: 149-157.
9. Shen JB, Yuan LX, Zhang JL, Li HG, Bai ZH, et al. (2011) Phosphorus dynamics: From soil to plant. Plant Physiology 156: 997-1005.
10. Sanchez PA, Salinas JG (1981) Low-input technology for managing oxisols and ultisols in tropical America. Advances in Agronomy 34: 279-406.
11. Cordell D, Drangert JO, White S (2009) The story of phosphorus: Global food security and food for thought. Global Environmental Change-Human and Policy Dimensions 19: 292-305.
12. Gilbert N (2009) The disappearing nutrient. Nature 461: 1041-1041.
13. Schroeder JI, Delhaize E, Frommer WB, Guerinot ML, Harrison MJ, et al. (2013) Using membrane transporters to improve crops for sustainable food production. Nature 497: 60-66.
14. Ceasar SA, Ignacimuthu S (2009) Genetic engineering of millets: Current status and future prospects. Biotechnology Letters 31: 779-788.
15. Bennetzen JL, Schmutz J, Wang H, Percifield R, Hawkins J, et al. (2012) Reference genome sequence of the model plant Setaria. Nature Biotechnology 30: 555-561.
16. Li PH, Brutnell TP (2011) Setaria viridis and Setaria italica, model genetic systems for the Panicoid grasses. Journal of Experimental Botany 62: 3031-3037.
17. Zhang GY, Liu X, Quan ZW, Cheng SF, Xu X, et al. (2012) Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nature Biotechnology 30: 549-556.
18. Muchhal US, Pardo JM, Raghothama KG (1996) Phosphate transporters from the higher plant Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 93: 10519-10523.
19. Nussaume L, Kanno S, Javot H, Marin E, Pochon N, et al. (2011) Phosphate import in plants: Focus on the PHT1 transporters. Frontiers in Plant Science 2: 1-8.
20. Tamura Y, Kobae Y, Mizuno T, Hata S (2012) Identification and expression analysis of arbuscular mycorrhiza-inducible phosphate transporter genes of soybean. Bioscience, Biotechnology and Biochemistry 76: 309-313.
21. Ai P, Sun S, Zhao J, Fan X, Xin W, et al. (2009) Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation. Plant Journal 57: 798-809.
22. Preuss CP, Huang CY, Gilliham M, Tyerman SD (2010) Channel-like characteristics of the low-affinity barley phosphate transporter PHT1;6 when expressed in Xenopus oocytes. Plant Physiology 152: 1431-1441.
23. Jia H, Ren H, Gu M, Zhao J, Sun S, et al. (2011) The phosphate transporter gene OsPht1;8 is involved in phosphate homeostasis in rice. Plant Physiology 156: 1164-1175.
24. Fitter AH, Merryweather JW (1992) Why are some plants more mycorrhizal than others? An ecological enquiry. Read DJ, Lewis DH, Fitter AH, Alexander IJ, editors: Mycorrhizas in ecosystems CAB International. 26-36.
25. Karasawa T, Hodge A, Fitter AH (2012) Growth, respiration and nutrient acquisition by the arbuscular mycorrhizal fungus Glomus mosseae and its host plant Plantago lanceolata in cooled soil. Plant Cell and Environment 35: 819-828.
26. Sanders FE, Tinker PB (1973) Phosphate flow into mycorrhizal roots. Pesticide Science 4: 385-395.
27. Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 3rd Edition. Academic Press, San Diego, CA, USA. 1-787.
28. Xie XA, Huang W, Liu FC, Tang NW, Liu Y, et al. (2013) Functional analysis of the novel mycorrhiza-specific phosphate transporter AsPT1 and PHT1 family from Astragalus sinicus during the arbuscular mycorrhizal symbiosis. New Phytologist 198: 836-852.
29. Harrison MJ, Dewbre GR, Liu JY (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14: 2413-2429.
30. Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the United States of America 99: 13324-13329.
31. Glassop D, Godwin RM, Smith SE, Smith FW (2007) Rice phosphate transporters associated with phosphate uptake in rice roots colonised with arbuscular mycorrhizal fungi. Canadian Journal of Botany-Revue Canadienne De Botanique 85: 644-651.
32. Rausch C, Daram P, Brunner S, Jansa J, Laloi M, et al. (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414: 462-470.
33. Nagy R, Karandashov V, Chague W, Kalinkevich K, Tamasloukht M, et al. (2005) The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant Journal 42: 236-250.
34. Willmann M, Gerlach N, Buer B, Polatajko A, Nagy R, et al. (2013) Mycorrhizal phosphate uptake pathway in maize: Vital for growth and cob development on nutrient poor agricultural and greenhouse soils. Frontiers in Plant Science 4: 1-15.
35. Chen AQ, Hu J, Sun SB, Xu GH (2007) Conservation and divergence of both phosphate-and mycorrhiza-regulated physiological responses and expression patterns of phosphate transporters in solanaceous species. New Phytologist 173: 817-831.
36. Xu GH, Chague V, Melamed-Bessudo C, Kapulnik Y, Jain A, et al. (2007) Functional characterization of LePT4: a phosphate transporter in tomato with mycorrhiza-enhanced expression. Journal of Experimental Botany 58: 2491-2501.
37. Hong JJ, Park YS, Bravo A, Bhattarai KK, Daniels DA, et al. (2012) Diversity of morphology and function in arbuscular mycorrhizal symbioses in Brachypodium distachyon. Planta 236: 851-865.
38. Marsalis MA, Lauriault LM, Trostle C (2012) Millets for forage and grain in new Mexico and west Texas. Guide (New Mexico State University Cooperative Extension Service) A-417: 1-8.
39. Lichtenthaler HK (1987) Chlorophylls and carotenoids-pigments of photosynthetic biomembranes. Methods in Enzymology 148: 350-382.
40. Krüger M, Krüger C, Walker C, Stockinger H, Schuessler A (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytologist 193: 970-984.
41. Hodge A (2001) Arbuscular mycorrhizal fungi influence decomposition of, but not plant nutrient capture from, glycine patches in soil. New Phytologist 151: 725-734.
42. Leigh J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytologist 181: 199-207.
43. Atkin OK, Sherlock D, Fitter AH, Jarvis S, Hughes JK, et al. (2009) Temperature dependence of respiration in roots colonized by arbuscular mycorrhizal fungi. New Phytologist 182: 188-199.
44. Kormanik PP, McGraw AC (1982) Quantification of vesicular-arbuscular mycorrhizae in plant roots. Ed. Schenck, N.C. In Methods and Principles of Mycorrhizal Research. The American Phytopathological Society, St. Paul, Minnesota, USA.
45. McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective-measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytologist 115: 495-501.
46. Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Methods in Enzymology 8: 115-118.
47. Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, et al. (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18: 412-421.
48. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, et al. (2012) Primer3-new capabilities and interfaces. Nucleic Acids Research 40: e115-e115.
49. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, et al. (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research 40: D1178-1186.
50. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Computer Applications in the Biosciences 8: 275-282.
51. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731-2739.
52. Chen A, Gu M, Sun S, Zhu L, Hong S, et al. (2011) Identification of two conserved cis-acting elements, MYCS and P1BS, involved in the regulation of mycorrhiza-activated phosphate transporters in eudicot species. New Phytologist 189: 1157-1169.
53. Karandashov V, Nagy R, Wegmuller S, Amrhein N, Bucher M (2004) Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the United States of America 101: 6285-6290.
54. Lota F, Wegmuller S, Buer B, Sato S, Brautigam A, et al. (2013) The cis-acting CTTC-P1BS module is indicative for gene function of LjVTI12, a Qb-SNARE protein gene that is required for arbuscule formation in Lotus japonicus. Plant Journal 74: 280-293.
55. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Research 27: 297-300.
56. Picot E, Krusche P, Tiskin A, Carre I, Ott S (2010) Evolutionary analysis of regulatory sequences (EARS) in plants. Plant Journal 64: 165-176.
57. Kumar K, Muthamilarasan M, Prasad M (2013) Reference genes for quantitative real-time PCR analysis in the model plant foxtail millet (Setaria italica L.) subjected to abiotic stress conditions. Plant Cell Tissue and Organ Culture 115: 13-22.
58. Sun S, Gu M, Cao Y, Huang X, Zhang X, et al. (2012) A constitutive expressed phosphate transporter, OsPht1;1, modulates phosphate uptake and translocation in phosphate-replete rice. Plant Physiology 159: 1571-1581.
59. Schunmann PHD, Richardson AE, Vickers CE, Delhaize E (2004) Promoter analysis of the barley Pht1;1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation. Plant Physiology 136: 4205-4214.
60. 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.
61. Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell and Environment 19: 529-538.
62. Johnson JF, Vance CP, Allan DL (1996) Phosphorus deficiency in Lupinus albus. Altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiology 112: 31-41.
63. Neumann G, Massonneau A, Langlade N, Dinkelaker B, Hengeler C, et al. (2000) Physiological aspects of cluster root function and development in phosphorus-deficient white lupin (Lupinus albus L.). Annals of Botany 85: 909-919.
64. Lopez-Bucio J, Cruz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Current Opinion in Plant Biology 6: 280-287.
65. Yang SY, Gronlund M, Jakobsen I, Grotemeyer MS, Rentsch D, et al. (2012) Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the phosphate transporter1 gene family. Plant Cell 24: 4236-4251.
66. Liu F, Chang XJ, Ye Y, Xie WB, Wu P, et al. (2011) Comprehensive sequence and whole-life-cycle expression profile analysis of the phosphate transporter gene family in rice. Molecular Plant 4: 1105-1122.
67. Secco D, Jabnoune M, Walker H, Shou H, Wu P, et al. (2013) Spatio-temporal transcript profiling of rice roots and shoots in response to phosphate starvation and recovery. The Plant Cell 25: 4285-4304.
68. Nagy R, Vasconcelos MJV, Zhao S, McElver J, Bruce W, et al. (2006) Differential regulation of five Pht1 phosphate transporters from maize (Zea mays L.). Plant Biology 8: 186-197.
69. Mudge SR, Rae AL, Diatloff E, Smith FW (2002) Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. Plant Journal 31: 341-353.
70. Shin H, Shin HS, Dewbre GR, Harrison MJ (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low-and high-phosphate environments. Plant Journal 39: 629-642.
71. Misson J, Thibaud MC, Bechtold N, Raghothama K, Nussaume L (2004) Transcriptional regulation and functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants. Plant Molecular Biolology 55: 727-741.
72. Rae AL, Cybinski DH, Jarmey JM, Smith FW (2003) Characterization of two phosphate transporters from barley; evidence for diverse function and kinetic properties among members of the Pht1 family. Plant Molecular Biology 53: 27-36.
73. Hodge A, Fitter AH (2010) Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proceedings of the National Academy of Sciences of the United States of America 107: 13754-13759.
74. Allen MF (2007) Mycorrhizal fungi: Highways for water and nutrients in arid soils. Vadose Zone Journal 6: 291-297.
75. Glassop D, Smith SE, Smith FW (2005) Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222: 688-698.
76. Sisaphaithong T, Kondo D, Matsunaga H, Kobae Y, Hata S (2012) Expression of plant genes for arbuscular mycorrhiza-inducible phosphate transporters and fungal vesicle formation in sorghum, barley, and wheat roots. Bioscience, Biotechnology, and Biochemistry 76: 2364-2367.
77. Grace EJ, Cotsaftis O, Tester M, Smith FA, Smith SE (2009) Arbuscular mycorrhizal inhibition of growth in barley cannot be attributed to extent of colonization, fungal phosphorus uptake or effects on expression of plant phosphate transporter genes. New Phytologist 181: 938-949.