Expression, transcriptional regulation and functional analysis of phosphate transporter genes in plants

Abstract

Phosphorus is one of the essential mineral nutrients required by all living cells. Phosphate mobilization into the plant is a complex process in which the absorption and translocation of this major nutrient are determined largely by the phosphate (Pi) transporters. In this paper, the recent progress on the plant phosphate (Pi) transporter genes, such as the molecular characterizations, expression patterns in response to Pi status, other inorganic nutrients, and the other factors, expression regulations via arbuscular mycorrhizal (AM) symbiosis, mechanisms of transcriptional regulation, functional identification approaches, and the gene engineering perspectives on improvement of plant phosphorus nutrition, etc., have been reviewed. The purpose of this paper is to provide a theoretical basis for further elucidation of the molecular mechanism of Pi transportation mediated by Pi transporters and to promote the generation of elite crop germplasms with a significant improvement in phosphorus use efficiency in the future.

Keywords

plant phosphate (Pi) transporter gene / expression / transcriptional regulation / functional analysis

References

[1] Ai P, Sun S, Zhao J, Fan X, Xin W, Guo Q, Yu L, Shen Q, Wu P, Miller A J, Xu G (2008). Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation. Plant J, 57(5): 798–809

[2] Baek S H, Chung I M, Yun S J (2001). Molecular cloning and characterization of a tobacco leaf cDNA encoding a phosphate transporter. Mol Cells, 11(1): 1–6

[3] Bucher M (2007). Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol, 173(1): 11–26

[4] Catarecha P, Segura M D, Franco-Zorrilla J M, García-Ponce B, Lanza M, Solano R, Paz-Ares J, Leyva A (2007). A mutant of the Arabidopsis phosphate transporter PHT1;1 displays enhanced arsenic accumulation. Plant Cell, 19(3): 1123–1133

[5] Chapin L J, Jones M L (2009). Ethylene regulates phosphorus remobilization and expression of a phosphate transporter (PhPT1) during petunia corolla senescence. J Exp Bot, 60(7): 2179–2190

[6] Cubero B, Nakagawa Y, Jiang X Y, Miura K J, Li F, Raghothama K G, Bressan R A, Hasegawa P M, Pardo J M (2009). The phosphate transporter PHT4;6 is a determinant of salt tolerance that is localized to the Golgi apparatus of Arabidopsis. Mol Plant, 2(3): 535–552

[7] Daram P, Brunner S, Persson B L, Amrhein N, Bucher M (1998). Functional analysis and cell-specific expression of a phosphate transporter from tomato. Planta, 206(2): 225–233

[8] 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(11): 2153–2166

[9] Drew M C, Saker L R (1984). Uptake and long-distance transport of phosphate, potassium and chloride in relation to internal ion concentrations in barley: evidence of non-allosteric regulation. Planta, 160(6): 500–507

[10] Furihata T, Suzuki M, Sakurai H (1992). Kinetic characterization of 2 phosphate-uptake systems with different affinities in suspension-cultured Catharanthus roseus protoplasts. [REMOVED HYPERLINK FIELD] Plant Cell Physiol, 33: 1151–1157

[11] Gordon-Weeks R, Tong Y, Davies T G, Leggewie G (2003). Restricted spatial expression of a high-affinity phosphate transporter in potato roots. J Cell Sci, 116(Pt 15): 3135–3144

[12] Grunwald U, Guo W, Fischer K, Isayenkov S, Ludwig-Müller J, Hause B, Yan X, Küster H, Franken P (2009). Overlapping expression patterns and differential transcript levels of phosphate transporter genes in arbuscular mycorrhizal, Pi-fertilised and phytohormone-treated Medicago truncatula roots. Planta, 229(5): 1023–1034

[13] Guo B, Jin Y, Wussler C, Blancaflor E B, Motes C M, Versaw W K (2008). Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytol, 177(4): 889–898

[14] Harrison M J, Dewbre G R, Liu J (2002). A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell, 14(10): 2413–2429

[15] Harrison M J, van Buuren M L (1995). A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature, 378(6557): 626–629

[16] Hase A, Nishikoori M, Okuyama H (2004). Induction of high affinity phosphate transporter in the duckweed Spirodela oligorrhiza. Physiol Plant, 120(2): 271–279

[17] Haseloff J, Siemering K R, Prasher D C, Hodge S (1997). Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc Natl Acad Sci USA, 94(6): 2122–2127

[18] Huang C, Barker S J, Langridge P, Smith F W, Graham R D (2000). Zinc deficiency up-regulates expression of high-affinity phosphate transporter genes in both phosphate-sufficient and -deficient barley roots. Plant Physiol, 124(1): 415–422

[19] Huang X, Zhu W, Dai S, Gai S, Zheng G, Zheng C (2008). The involvement of mitochondrial phosphate transporter in accelerating bud dormancy release during chilling treatment of tree peony (Paeonia suffruticosa). Planta, 228(4): 545–552

[20] Hürlimann H C, Pinson B, Stadler-Waibel M, Zeeman S C, Freimoser F M (2009). The SPX domain of the yeast low-affinity phosphate transporter Pho90 regulates transport activity. EMBO Rep, 10(9): 1003–1008

[21] Javot H, Penmetsa R V, Terzaghi N, Cook D R, Harrison M J, (2007). A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA, 104(5): 1720–1725

[22] Jefferson R A, Kavanagh T A, Bevan M W (1987). GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J, 6(13): 3901–3907

[23] Karandashov V, Bucher M (2005). Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci, 10(1): 22–29

[24] Karandashov V, Nagy R, Wegmüller S, Amrhein N, Bucher M (2004). Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA, 101(16): 6285–6290

[25] Karthikeyan A S, Ballachanda D N, Raghothama K G (2009). Promoter deletion analysis elucidates the role of cis elements and 5’UTR intron in spatiotemporal regulation of AtPht1;4 expression in Arabidopsis. Physiol Plant, 136(1): 10–18

[26] Karthikeyan A S, Varadarajan D K, Mukatira U T, D’Urzo M P, Damsz B, Raghothama K G (2002). Regulated expression of Arabidopsis phosphate transporters. Plant Physiol, 130(1): 221–233

[27] Kiiskinen M, Korhonen M, Kangasjärvi J (1997). Isolation and characterization of cDNA for a plant mitochondrial phosphate translocator (Mpt1): ozone stress induces Mpt1 mRNA accumulation in birch (Betula pendula Roth). Plant Mol Biol, 35(3): 271–279

[28] Leggewie G, Willmitzer L, Riesmeier J W (1997). Two cDNAs from potato are able to complement a phosphate uptake-deficient yeast mutant: identification of phosphate transporters from higher plants. Plant Cell, 9(3): 381–392

[29] Li Q, Gao X, Sun Y, Zhang Q, Song R, Xu Z (2006). Isolation and characterization of a sodium-dependent phosphate transporter gene in Dunaliella viridis. Biochem Biophys Res Commun, 340(1): 95–104

[30] Liu C, Muchhal U S, Uthappa M, Kononowicz A K, Raghothama K G (1998a). Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. Plant Physiol, 116(1): 91–99

[31] Liu H, Trieu A T, Blaylock L A, Harrison M J (1998b). Cloning and characterization of two phosphate transporters from Medicago truncatula roots: regulation in response to phosphate and to colonization by arbuscular mycorrhizal (AM) fungi. Mol Plant Microbe Interact, 11(1): 14–22

[32] Liu J, Versaw W K, Pumplin N, Gomez S K, Blaylock L A, Harrison M J (2008). Closely related members of the Medicago truncatula PHT1 phosphate transporter gene family encode phosphate transporters with distinct biochemical activities. J Biol Chem, 283(36): 24673–24681

[33] Lunn J E, Douce R (1993). Transport of inorganic pyrophosphate across the spinach chloroplast envelope. Biochem J, 290(Pt 2): 375–379

[34] McPharlin I R, Bieleski R L (1987). Phosphate-uptake by Spirodela and Lemna during early phosphorus deficiency. Aust J Plant Physiol, 14: 561–572

[35] Miao J, Sun J, Liu D, Li B, Zhang A, Li Z, Tong Y (2009). Characterization of the promoter of phosphate transporter TaPHT1.2 differentially expressed in wheat varieties. J Genet Genomics, 36(8): 455–466

[36] Ming F, Lu Q, Wang W, Zhang S, Guo B, Shen D (2006). Cloning, expression and function of phosphate transporter encoded gene in Oryza sativa L.. Sci China C Life Sci, 49(5): 409–413

[37] Ming F, Mi G H, Lu Q, Yin S, Zhang S S, Guo B, Shen D L (2005). Cloning and characterization of cDNA for the Oryza sativa phosphate transporter. 28Cell Mol. Biol Lett, 10: 401–411

[38] Misson J, Thibaud M C, 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 Mol Biol, 55(5): 727–741

[39] Mitsukawa N, Okumura S, Shirano Y, Sato S, Kato T, Harashima S, Shibata D (1997). Overexpression of an Arabidopsis thaliana high-affinity phosphate transporter gene in tobacco cultured cells enhances cell growth under phosphate-limited conditions. Proc Natl Acad Sci USA, 94(13): 7098–7102

[40] Muchhal U S, Pardo J M, Raghothama K G (1996). Phosphate transporters from the higher plant Arabidopsis thaliana. Proc Natl Acad Sci USA, 93(19): 10519–10523

[41] Muchhal U S, Raghothama K G (1999). Transcriptional regulation of plant phosphate transporters. Proc Natl Acad Sci USA, 96(10): 5868–5872

[42] Nagy R, Karandashov V, Chague V, Kalinkevich K, Tamasloukht M, Xu G, Jakobsen I, Levy A A, Amrhein N, Bucher M (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 J, 42(2): 236–250

[43] Nagy R, Vasconcelos M J, Zhao S, McElver J, Bruce W, Amrhein N, Raghothama K G, Bucher M (2006). Differential regulation of five Pht1 phosphate transporters from maize (Zea mays L.). Plant Biol (Stuttg), 8(2): 186–197

[44] Nakamori K, Takabatake R, Umehara Y, Kouchi H, Izui K, Hata S, Raghothama K G, Bucher M, Nakamori K, Takabatake R, Umehara Y, Kouchi H, Izui K, Hata S (2002). Cloning, functional expression, and mutational analysis of a cDNA for Lotus japonicus mitochondrial phosphate transporter. Plant Cell Physiol, 43(10): 1250–1253

[45] Okumura S, Mitsukawa N, Shirano Y, Shibata D (1998). Phosphate transporter gene family of Arabidopsis thaliana. DNA Res, 5(5): 261–269

[46] Ow D W, DE Wet J R, Helinski D R, Howell S H, Wood K V, Deluca M (1986). Transient and stable expression of the firefly luciferase gene in plant-cells and transgenic plants. Science, 234(4778): 856–859

[47] Paszkowski U, Kroken S, Roux C, Briggs S P (2002). Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA, 99(20): 13324–13329

[48] Pavón L R, Lundh F, Lundin B, Mishra A, Persson B L, Spetea C (2008). Arabidopsis ANTR1 is a thylakoid Na⁺-dependent phosphate transporter: functional characterization in Escherichia coli. J Biol Chem, 283(20): 13520–13527

[49] Rae A L, Cybinski D H, Jarmey J M, Smith F W (2003). Characterization of two phosphate transporters from barley; evidence for diverse function and kinetic properties among members of the Pht1 family. Plant Mol Biol, 53(1-2): 27–36

[50] Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001). A phosphate transporter expressed in arbuscule-containing cells in potato. Nature, 414(6862): 462–470

[51] Rausch C, Zimmermann P, Amrhein N, Bucher M (2004). Expression analysis suggests novel roles for the plastidic phosphate transporter Pht2;1 in auto- and heterotrophic tissues in potato and Arabidopsis. Plant J, 39(1): 13–28

[52] Schünmann P H, Richardson A E, Smith F W, Delhaize E (2004a). Characterization of promoter expression patterns derived from the Pht1 phosphate transporter genes of barley (Hordeum vulgare L.). J Exp Bot, 55(398): 855–865

[53] Schünmann P H, Richardson A E, Vickers C E, Delhaize E (2004b). Promoter analysis of the barley Pht1;1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation. Plant Physiol, 136(4): 4205–4214

[54] Seo H M, Jung Y, Song S, Kim Y, Kwon T, Kim D H, Jeung S J, Yi Y B, Yi G, Nam M H, Nam J (2008). Increased expression of OsPT1, a high-affinity phosphate transporter, enhances phosphate acquisition in rice. Biotechnol Lett, 30(10): 1833–1838

[55] Shimogawara K, Usuda H (1995). Uptake of inorganic phosphate by suspension-cultured tobacco cells: kinetics and regulation by Pi starvation. Plant Cell Physiol, 36: 341–351

[56] Shin H, Shin H S, Dewbre G R, Harrison M J (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 J, 39(4): 629–642

[57] Smith F W, Ealing P M, Dong B, Delhaize E (1997). The cloning of two Arabidopsis genes belonging to a phosphate transporter family. Plant J, 11(1): 83–92

[58] Smith F W, Rae A L, Hawkesford M J (2000). Molecular mechanisms of phosphate and sulphate transport in plants. Biochim Biophys Acta, 1465(1-2): 236–245

[59] Stefanovic A, Ribot C, Rouached H, Wang Y, Chong J, Belbahri L, Delessert S, Poirier Y (2007). Members of the PHO1 gene family show limited functional redundancy in phosphate transfer to the shoot, and are regulated by phosphate deficiency via distinct pathways. Plant J, 50(6): 982–994

[60] Takabatake R, Hata S, Taniguchi M, Kouchi H, Sugiyama T, Izui K (1999). Isolation and characterization of cDNAs encoding mitochondrial phosphate transporters in soybean, maize, rice, and Arabidopis. Plant Mol Biol, 40(3): 479–486

[61] Tatry M V, El Kassis E, Lambilliotte R, Corratgé C, van Aarle I, Amenc L K, Alary R, Zimmermann S, Sentenac H, Plassard C (2009). Two differentially regulated phosphate transporters from the symbiotic fungus Hebeloma cylindrosporum and phosphorus acquisition by ectomycorrhizal Pinus pinaster. Plant J, 57(6): 1092–1102

[62] Tittarelli A, Milla L, Vargas F, Morales A, Neupert C, Meisel L A, Salvo-G H, Peñaloza E, Muñoz G, Corcuera L J, Silva H (2007). Isolation and comparative analysis of the wheat TaPT2 promoter: identification in silico of new putative regulatory motifs conserved between monocots and dicots. J Exp Bot, 58(10): 2573–2582

[63] Vance C P, Uhde-Stone C, Allan D L (2003). Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol, 157(3): 423–447

[64] Versaw W K, Harrison M J (2002). A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell, 14(8): 1751–1766

[65] Xu G H, Chague V, Melamed-Bessudo C, Kapulnik Y, Jain A, Raghothama K G, Levy A A, Silber A (2007). Functional characterization of LePT4: a phosphate transporter in tomato with mycorrhiza-enhanced expression. J Exp Bot, 58(10): 2491–2501

[66] Yu F T, Zhang A M, Chen S Y, Zhang F S (2001). Differential accumulation of the new high-affinity phosphate transporter candidated gene fragment in rice roots in response to phosphorus deficiency stress. Yi Chuan Xue Bao, 28(2): 144–151(in Chinese)

[67] Zeng Y J, Ying J, Liu J Z, Sun J H, Li B, Xiao H S, Li Z S (2002). Function analysis of a wheat phosphate transporter in yeast mutant. Yi Chuan Xue Bao, 29(11): 1017–1020 (in Chinese)

Acknowledgements

This work was supported by a grant from the National Natural Science Foundation of China (Grant No. 30971773) and the Foundation of Key Laboratory of Crop Growth Regulation in Hebei Province., China.

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg