Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles.

In response to the colonization by arbuscular mycorrhizal (AM) fungi, plants reprioritize their phosphate (Pi)-uptake strategies to take advantage of nutrient transfer via the fungus. The mechanisms underlying Pi transport are beginning to be understood, and recently, details of the regulation of plant and fungal Pi transporters in the AM symbiosis have been revealed. This review summarizes recent advances in this area and explores current data and hypotheses of how the plant Pi status affects the symbiosis. Finally, suggestions of an interrelationship of Pi and nitrogen (N) in the AM symbiosis are discussed.

[1]  V. Gianinazzi-Pearson,et al.  Phosphate Uptake and Arbuscular Activity in Mycorrhizal Allium cepa L.: Effects of Photon Irradiance and Phosphate Nutrition , 1990 .

[2]  J. Pate,et al.  Effects of P deficiency on assimilation and transport of nitrate and phosphate in intact plants of castor bean (Ricinus communis L.) , 1997 .

[3]  A. Johansen,et al.  Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi , 2000, Plant and Soil.

[4]  Daniel Schwarzott,et al.  A new fungal phylum, the Glomeromycota: phylogeny and evolution * * Dedicated to Manfred Kluge (Tech , 2001 .

[5]  I. Jakobsen,et al.  External hyphae of vesicular arbuscular mycorrhizal fungi associated with trifolium subterraneum l. 1. spread of hyphae and phosphorus inflow into roots , 1992 .

[6]  Ulf-Ingo Flügge,et al.  The Plastidic Pentose Phosphate Translocator Represents a Link between the Cytosolic and the Plastidic Pentose Phosphate Pathways in Plants1 , 2002, Plant Physiology.

[7]  S. Burleigh,et al.  A novel gene whose expression in Medicago truncatula roots is suppressed in response to colonization by vesicular-arbuscular mycorrhizal (VAM) fungi and to phosphate nutrition , 1997, Plant Molecular Biology.

[8]  M. J. Harrison,et al.  The arbuscular mycorrhizal symbiosis : an underground association , 1997 .

[9]  N. Amrhein,et al.  Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[10]  M. Hayatsu,et al.  A new hypothesis on the strategy for acquisition of phosphorus in arbuscular mycorrhiza: up-regulation of secreted acid phosphatase gene in the host plant. , 2005, Molecular plant-microbe interactions : MPMI.

[11]  F. W. Smith,et al.  Regulation of Expression of Genes Encoding Phosphate Transporters in Barley Roots , 1999 .

[12]  P. Lammers,et al.  The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. , 2005, The New phytologist.

[13]  U. Paszkowski,et al.  Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[14]  L. K. Porter,et al.  HYPHAL UPTAKE AND TRANSPORT OF NITROGEN FROM TWO 15N‐LABELLED SOURCES BY GLOMUS MOSSEAE, A VESICULAR‐ARBUSCULAR MYCORRHIZAL FUNGUS * , 1983 .

[15]  T. Cavagnaro,et al.  Rapid accumulation of polyphosphate in extraradical hyphae of an arbuscular mycorrhizal fungus as revealed by histochemistry and a polyphosphate kinase/luciferase system. , 2004, The New phytologist.

[16]  F. W. Smith,et al.  Characterization of two phosphate transporters from barley; evidence for diverse function and kinetic properties among members of the Pht1 family , 2003, Plant Molecular Biology.

[17]  M. J. Harrison,et al.  Improved phosphorus acquisition and biomass production in Arabidopsis by transgenic expression of a purple acid phosphatase gene from M. truncatula , 2006 .

[18]  J. Lynch,et al.  Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability , 1996 .

[19]  S. Burleigh,et al.  Effect of P Availability on Temporal Dynamics of Carbon Allocation and Glomus intraradices High-Affinity P Transporter Gene Induction in Arbuscular Mycorrhiza , 2006, Applied and Environmental Microbiology.

[20]  Y. Shachar-Hill,et al.  Carbon metabolism and transport in arbuscular mycorrhizas. , 2000, Plant physiology.

[21]  U. Flugge PHOSPHATE TRANSLOCATORS IN PLASTIDS. , 1999, Annual review of plant physiology and plant molecular biology.

[22]  M. González-Guerrero,et al.  GintAMT1 encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. , 2006, Fungal genetics and biology : FG & B.

[23]  Chun-Lin Su,et al.  pho2, a Phosphate Overaccumulator, Is Caused by a Nonsense Mutation in a MicroRNA399 Target Gene1[W] , 2006, Plant Physiology.

[24]  B. Persson,et al.  Functional analysis and cell-specific expression of a phosphate transporter from tomato , 1998, Planta.

[25]  T. Boller,et al.  Transport of 15N from a soil compartment separated by a polytetrafluoroethylene membrane to plant roots via the hyphae of arbuscular mycorrhizal fungi , 2000 .

[26]  K. Raghothama,et al.  Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. , 1998, Plant physiology.

[27]  P. Tinker,et al.  TRANSLOCATION AND TRANSFER OF NUTRIENTS IN VESICULAR‐ARBUSCULAR MYCORRHIZAS , 1978 .

[28]  R. Singer,et al.  The Biology of Mycorrhiza , 1960 .

[29]  G. Feng,et al.  Contribution of arbuscular mycorrhizal fungi to utilization of organic sources of phosphorus by red clover in a calcareous soil , 2003 .

[30]  T. Ezawa,et al.  Polyphosphates in Intraradical and Extraradical Hyphae of an Arbuscular Mycorrhizal Fungus, Gigaspora margarita , 1999, Applied and Environmental Microbiology.

[31]  D. Shibata,et al.  Overexpression of an Arabidopsis thaliana high-affinity phosphate transporter gene in tobacco cultured cells enhances cell growth under phosphate-limited conditions. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[32]  K. Yano,et al.  Phosphorus acquisition from non-labile sources in peanut and pigeonpea with mycorrhizal interaction , 2003 .

[33]  E. Joner,et al.  Arbuscular mycorrhizal phosphate transport under monoxenic conditions using radio-labelled inorganic and organic phosphate , 2000, Biotechnology Letters.

[34]  H. Kouchi,et al.  Cloning, functional expression, and mutational analysis of a cDNA for Lotus japonicus mitochondrial phosphate transporter. , 2002, Plant & cell physiology.

[35]  Y. Poirier,et al.  Phosphate Transport and Homeostasis in Arabidopsis , 2002, The arabidopsis book.

[36]  M. Saito,et al.  Possible involvement of hyphal phosphatase in phosphate efflux from intraradical hyphae isolated from mycorrhizal roots colonized by Gigaspora margarita. , 2004, Mycological research.

[37]  C. Bledsoe,et al.  Nitrogen Transfer Within and Between Plants Through Common Mycorrhizal Networks (CMNs) , 2003 .

[38]  P. Hinsinger Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review , 2001, Plant and Soil.

[39]  H. Wohlrab,et al.  Yeast mitochondrial phosphate transport protein expressed in Escherichia coli. Site-directed mutations at threonine-43 and at a similar location in the second tandem repeat (isoleucine-141). , 1994, Biochemistry.

[40]  M. J. Harrison,et al.  Transgenic expression of a novel M. truncatula phytase gene results in improved acquisition of organic phosphorus by Arabidopsis , 2005, Planta.

[41]  R. W. Blanchar,et al.  Citrate, Malate, and Succinate Concentration in Exudates from P-Sufficient and P-Stressed Medicago sativa L. Seedlings. , 1987, Plant physiology.

[42]  C. Raines,et al.  pho3: a phosphorus-deficient mutant of Arabidopsis thaliana (L.) Heynh. , 2001, Planta.

[43]  F. A. Smith,et al.  EFFECTS OF AMMONIUM AND NITRATE IONS ON MYCORRHIZAL INFECTION, NODULATION AND GROWTH OF TRIFOLIUM SUBTERRANEUM , 1980 .

[44]  Folker Meyer,et al.  Combined transcriptome profiling reveals a novel family of arbuscular mycorrhizal-specific Medicago truncatula lectin genes. , 2005, Molecular plant-microbe interactions : MPMI.

[45]  D. Bagyaraj,et al.  PHOSPHORUS CONCENTRATIONS IN PLANTS RESPONSIBLE FOR INHIBITION OF MYCORRHIZAL INFECTION , 1978 .

[46]  I. Paulsen,et al.  Major Facilitator Superfamily , 1998, Microbiology and Molecular Biology Reviews.

[47]  A. Kornberg,et al.  Inorganic polyphosphate: a molecule of many functions. , 1999, Progress in molecular and subcellular biology.

[48]  J. Jansa,et al.  A phosphate transporter expressed in arbuscule-containing cells in potato , 2001, Nature.

[49]  H. Leyser,et al.  Phosphate availability regulates root system architecture in Arabidopsis. , 2001, Plant physiology.

[50]  W. Frommer,et al.  The molecular physiology of ammonium uptake and retrieval. , 2000, Current opinion in plant biology.

[51]  W. Plaxton Plant Response to Stress: Biochemical Adaptations to Phosphate Deficiency , 2004 .

[52]  V. Gianinazzi-Pearson,et al.  Differential activation of H+-ATPase genes by an arbuscular mycorrhizal fungus in root cells of transgenic tobacco , 2000, Planta.

[53]  S. Burleigh,et al.  The influence of external nitrogen on carbon allocation to Glomus intraradices in monoxenic arbuscular mycorrhiza. , 2005, The New phytologist.

[54]  M. J. Harrison,et al.  Cloning and characterization of two phosphate transporters from Medicago truncatula roots: regulation in response to phosphate and to colonization by arbuscular mycorrhizal (AM) fungi. , 1998, Molecular plant-microbe interactions : MPMI.

[55]  C. Vance,et al.  Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. , 2003, The New phytologist.

[56]  D. Read,et al.  European and African maize cultivars differ in their physiological and molecular responses to mycorrhizal infection. , 2005, The New phytologist.

[57]  D. Schachtman,et al.  A Lycopersicon esculentum phosphate transporter (LePT1) involved in phosphorus uptake from a vesicular-arbuscular mycorrhizal fungus. , 1999, The New phytologist.

[58]  N. Amrhein,et al.  Pht2;1 Encodes a Low-Affinity Phosphate Transporter from Arabidopsis , 1999, Plant Cell.

[59]  I. Jakobsen,et al.  Mycorrhizal Fungi Can Dominate Phosphate Supply to Plants Irrespective of Growth Responses1 , 2003, Plant Physiology.

[60]  F. W. Smith,et al.  Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. , 2002, The Plant journal : for cell and molecular biology.

[61]  A. Ashford,et al.  Phosphorus Effects on Metabolic Processes in Monoxenic Arbuscular Mycorrhiza Cultures1 , 2002, Plant Physiology.

[62]  A. Johansen,et al.  Nitrogen metabolism of external hyphae of the arbuscular mycorrhizal fungus Glomus intraradices , 1996 .

[63]  P. Zimmermann,et al.  Expression analysis suggests novel roles for the plastidic phosphate transporter Pht2;1 in auto- and heterotrophic tissues in potato and Arabidopsis. , 2004, The Plant journal : for cell and molecular biology.

[64]  M. Bucher,et al.  Symbiotic phosphate transport in arbuscular mycorrhizas. , 2005, Trends in plant science.

[65]  V. Rubio,et al.  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. , 1999, The Plant journal : for cell and molecular biology.

[66]  A. Richardson,et al.  Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate. , 2001, The Plant journal : for cell and molecular biology.

[67]  Jian-Kang Zhu,et al.  A miRNA Involved in Phosphate-Starvation Response in Arabidopsis , 2005, Current Biology.

[68]  A. Weber,et al.  Solute transporters of the plastid envelope membrane. , 2005, Annual review of plant biology.

[69]  M. J. Harrison,et al.  A Phosphate Transporter from Medicago truncatula Involved in the Acquisition of Phosphate Released by Arbuscular Mycorrhizal Fungi Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.004861. , 2002, The Plant Cell Online.

[70]  H. Kouchi,et al.  Gene silencing by expression of hairpin RNA in Lotus japonicus roots and root nodules. , 2003, Molecular plant-microbe interactions : MPMI.

[71]  Ezawa Tatsuhiro,et al.  Differentiation of polyphosphate metabolism between the extra- and intraradical hyphae of arbuscular mycorrhizal fungi. , 2001, The New phytologist.

[72]  T. Taylor,et al.  Four hundred-million-year-old vesicular arbuscular mycorrhizae. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[73]  Maria J. Harrison The Arbuscular Mycorrhizal Symbiosis , 1997 .

[74]  G. Sarath,et al.  The role of acid phosphatases in plant phosphorus metabolism , 1994 .

[75]  Chun-Lin Su,et al.  Regulation of Phosphate Homeostasis by MicroRNA in Arabidopsis[W] , 2005, The Plant Cell Online.

[76]  S. Johnson,et al.  Role of Organic Acids in Phosphate Mobilization from Iron Oxide , 2006 .

[77]  A. Johansen,et al.  Hyphal transport of 15 N-labelled nitrogen by a vesicular-arbuscular mycorrhizal fungus and its effect on depletion of inorganic soil N. , 1992, The New phytologist.

[78]  C. Ticconi,et al.  Phosphate sensing in higher plants. , 2002, Physiologia plantarum.

[79]  Y. Poirier,et al.  Structure and Expression Profile of the Arabidopsis PHO1 Gene Family Indicates a Broad Role in Inorganic Phosphate Homeostasis1[w] , 2004, Plant Physiology.

[80]  T. Ezawa,et al.  Specific inhibitor and substrate specificity of alkaline phosphatase expressed in the symbiotic phase of the arbuscular mycorrhizal fungus, Glomus etunicatum , 1999 .

[81]  T. Ezawa,et al.  Extensive tubular vacuole system in an arbuscular mycorrhizal fungus, Gigaspora margarita. , 2002, The New phytologist.

[82]  W. Versaw,et al.  A phosphate-repressible, high-affinity phosphate permease is encoded by the pho-5+ gene of Neurospora crassa. , 1995, Gene.

[83]  M. Gouy,et al.  Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[84]  R. Koide,et al.  Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. , 2000, The New phytologist.

[85]  C. Ticconi,et al.  Short on phosphate: plant surveillance and countermeasures. , 2004, Trends in plant science.

[86]  M. Laloi Plant mitochondrial carriers: an overview , 1999, Cellular and Molecular Life Sciences CMLS.

[87]  B. Bago,et al.  Branched absorbing structures (BAS): a feature of the extraradical mycelium of symbiotic arbuscular mycorrhizal fungi , 1998 .

[88]  P. Mäkelä,et al.  Ectopic expression of ABI3 gene enhances freezing tolerance in response to abscisic acid and low temperature in Arabidopsis thaliana. , 2008, The Plant journal : for cell and molecular biology.

[89]  F. Martin,et al.  15N‐NMR studies of nitrogen assimilation and amino acid biosynthesis in the ectomycorrhizal fungus Cenococcum graniforme , 1985 .

[90]  D. Bartel,et al.  Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. , 2004, Molecular cell.

[91]  J. Schiefelbein,et al.  Mutant of Arabidopsis deficient in xylem loading of phosphate. , 1991, Plant physiology.

[92]  P. Olsson,et al.  Microscopic detection of phosphatase activity of saprophytic and arbuscular mycorrhizal fungi using a fluorogenic substrate , 2001 .

[93]  M. J. Harrison,et al.  Characterization of the Mt4 gene from Medicago truncatula. , 1998, Gene.

[94]  M. J. Harrison,et al.  Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. , 2006, The Plant journal : for cell and molecular biology.

[95]  I. Jakobsen,et al.  The relative contribution of hyphae and roots to phosphorus uptake by arbuscular mycorrhizal plants, measured by dual labelling with 32P and 33P , 1993 .

[96]  H. Brinch-Pedersen,et al.  Engineering crop plants: getting a handle on phosphate. , 2002, Trends in plant science.

[97]  A. Osbourn,et al.  Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[98]  M. J. Harrison,et al.  A phosphate transporter from the mycorrhizal fungus Glomus versiforme , 1995, Nature.

[99]  M. Saier A Functional-Phylogenetic Classification System for Transmembrane Solute Transporters , 2000, Microbiology and Molecular Biology Reviews.

[100]  T. Chiou,et al.  The spatial expression patterns of a phosphate transporter (MtPT1) from Medicago truncatula indicate a role in phosphate transport at the root/soil interface. , 2001, The Plant journal : for cell and molecular biology.

[101]  Yasunori Nakamura,et al.  Expression profiling of starch metabolism-related plastidic translocator genes in rice , 2005, Planta.

[102]  I. Jakobsen Transport of Phosphorus and Carbon in VA Mycorrhizas , 1995 .

[103]  B. Frey,et al.  Acquisition of nitrogen by external hyphae of arbuscular mycorrhizal fungi associated with Zea mays L. , 1993, The New phytologist.

[104]  Luis Herrera-Estrella,et al.  Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate , 2000, Nature Biotechnology.

[105]  R. Bieleski Phosphate Pools, Phosphate Transport, and Phosphate Availability , 1973 .

[106]  I. Maldonado-Mendoza,et al.  A phosphate transporter gene from the extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response to phosphate in the environment. , 2001, Molecular plant-microbe interactions : MPMI.

[107]  I. Jakobsen,et al.  External hyphae of vesicular–arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. , 1992 .

[108]  M. Saito,et al.  Polyphosphate dynamics in mycorrhizal roots during colonization of an arbuscular mycorrhizal fungus. , 2005, The New phytologist.

[109]  R. Krämer,et al.  Kinetic mechanism of phosphate/phosphate and phosphate/OH- antiports catalyzed by reconstituted phosphate carrier from beef heart mitochondria. , 1994, The Journal of biological chemistry.

[110]  R. Metzenberg,et al.  Nucleotide sequence of pho-4+, encoding a phosphate-repressible phosphate permease of Neurospora crassa. , 1989, Gene.

[111]  M. Hodges,et al.  The growing family of mitochondrial carriers in Arabidopsis. , 2004, Trends in plant science.

[112]  S. Harashima,et al.  The PHO84 gene of Saccharomyces cerevisiae encodes an inorganic phosphate transporter , 1991, Molecular and cellular biology.

[113]  C. Town,et al.  Transcript Profiling Coupled with Spatial Expression Analyses Reveals Genes Involved in Distinct Developmental Stages of an Arbuscular Mycorrhizal Symbiosis Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tp , 2003, The Plant Cell Online.

[114]  B. Bago,et al.  Nitrate depletion and pH changes induced by the extraradical mycelium of the arbuscular mycorrhizal fungus Glomus intraradices grown in monoxenic culture. , 1996, The New phytologist.

[115]  J. Lynch,et al.  Regulation of root hair density by phosphorus availability in Arabidopsis thaliana , 2001 .

[116]  Chris Somerville,et al.  Identification and Characterization of the Arabidopsis PHO1 Gene Involved in Phosphate Loading to the Xylem Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000745. , 2002, The Plant Cell Online.

[117]  P. Hansen,et al.  31P NMR for the study of P metabolism and translocation in arbuscular mycorrhizal fungi , 2000, Plant and Soil.

[118]  A Weber,et al.  A new class of plastidic phosphate translocators: a putative link between primary and secondary metabolism by the phosphoenolpyruvate/phosphate antiporter. , 1997, The Plant cell.

[119]  A. Pühler,et al.  Overlaps in the Transcriptional Profiles of Medicago truncatula Roots Inoculated with Two Different Glomus Fungi Provide Insights into the Genetic Program Activated during Arbuscular Mycorrhiza1[w] , 2005, Plant Physiology.

[120]  W. Plaxton,et al.  Response to Phosphate Deprivation in Brassica nigra Suspension Cells : Enhancement of Intracellular, Cell Surface, and Secreted Phosphatase Activities Compared to Increases in Pi-Absorption Rate. , 1990, Plant physiology.

[121]  N. Amrhein,et al.  Differential regulation of five Pht1 phosphate transporters from maize (Zea mays L.). , 2006, Plant biology.

[122]  F. W. Smith,et al.  Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots , 2005, Planta.

[123]  B. Persson,et al.  Structural modeling of dual‐affinity purified Pho84 phosphate transporter , 2004, FEBS letters.

[124]  J. Pate,et al.  Transport, synthesis and catabolism of abscisic acid (ABA) in intact plants of castor bean (Ricinus communis L.) under phosphate deficiency and moderate salinity , 1997 .

[125]  Peter J. Lammers,et al.  Nitrogen transfer in the arbuscular mycorrhizal symbiosis , 2005, Nature.

[126]  K. Izui,et al.  Knockdown of an arbuscular mycorrhiza-inducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis. , 2006, Plant & cell physiology.

[127]  M. J. Harrison,et al.  Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. , 2004, The Plant journal : for cell and molecular biology.

[128]  I. Jakobsen,et al.  Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake , 2004 .

[129]  K. Fischer,et al.  The triose phosphate‐3‐phosphoglycerate‐phosphate translocator from spinach chloroplasts: nucleotide sequence of a full‐length cDNA clone and import of the in vitro synthesized precursor protein into chloroplasts. , 1989, The EMBO journal.

[130]  Guohua Xu,et al.  The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. , 2005, The Plant journal : for cell and molecular biology.

[131]  Damien Blaudez,et al.  Ammonia: a candidate for nitrogen transfer at the mycorrhizal interface. , 2006, Trends in plant science.

[132]  P. Tinker,et al.  IV. EFFECT OF ENVIRONMENTAL VARIABLES ON MOVEMENT OF PHOSPHORUS , 1981 .

[133]  A. Weber,et al.  Using mutants to probe the in vivo function of plastid envelope membrane metabolite transporters. , 2004, Journal of experimental botany.

[134]  M. Stitt,et al.  PHO2, MicroRNA399, and PHR1 Define a Phosphate-Signaling Pathway in Plants1[W][OA] , 2006, Plant Physiology.

[135]  L. Abbott,et al.  Phosphorus and the formation of vesicular-arbuscular mycorrhizas , 1979 .

[136]  P. McInerney,et al.  Inorganic polyphosphate interacts with ribosomes and promotes translation fidelity in vitro and in vivo , 2006, Molecular microbiology.

[137]  K. Fischer,et al.  Analysis of the Plastidic phosphate translocator Gene Family in Arabidopsis and Identification of New phosphate translocator-Homologous Transporters, Classified by Their Putative Substrate-Binding Site1 , 2003, Plant Physiology.

[138]  L. Lanfranco,et al.  Expression profiles of a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae , 2005, Mycorrhiza.

[139]  I. Jakobsen,et al.  Physiological and molecular evidence for Pi uptake via the symbiotic pathway in a reduced mycorrhizal colonization mutant in tomato associated with a compatible fungus. , 2005, The New phytologist.

[140]  V. Wray,et al.  Is stimulation of carotenoid biosynthesis in arbuscular mycorrhizal roots a general phenomenon? , 2005, Phytochemistry.

[141]  M. J. Harrison,et al.  A Chloroplast Phosphate Transporter, PHT2;1, Influences Allocation of Phosphate within the Plant and Phosphate-Starvation Responses Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.002220. , 2002, The Plant Cell Online.

[142]  L. Willmitzer,et al.  Two cDNAs from potato are able to complement a phosphate uptake-deficient yeast mutant: identification of phosphate transporters from higher plants. , 1997, The Plant cell.

[143]  Michael Gutensohn,et al.  Molecular Characterization of a Carbon Transporter in Plastids from Heterotrophic Tissues: The Glucose 6-Phosphate/Phosphate Antiporter , 1998, Plant Cell.

[144]  I. Maldonado-Mendoza,et al.  Expression of alkaline phosphatase genes in arbuscular mycorrhizas , 2004 .

[145]  A. Fitter What is the link between carbon and phosphorus fluxes in arbuscular mycorrhizas? A null hypothesis for symbiotic function. , 2006, The New phytologist.

[146]  C. Rausch,et al.  Molecular mechanisms of phosphate transport in plants , 2002, Planta.

[147]  M. J. Harrison,et al.  A phosphate transporter from Medicago truncatula is expressed in the photosynthetic tissues of the plant and located in the chloroplast envelope. , 2003, The New phytologist.

[148]  A. Hodge,et al.  An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material , 2001, Nature.