The expression of GintPT, the phosphate transporter of Rhizophagus irregularis, depends on the symbiotic status and phosphate availability

Planta

Volumn 237, Issue 5, 2013, Pages 1267-1277

  Fiorilli, Valentina ^a   Lanfranco, Luisa ^a,b   Bonfante, Paola ^a,b  

^a CNR   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Arbuscular mycorrhizal symbiosis; Gene expression; Phosphate; Phosphate transporter; Rhizophagus irregularis

Indexed keywords

ARBUSCULAR; BACTERIA (MICROORGANISMS); FUNGI; MEDICAGO TRUNCATULA; RHIZOPHAGUS;

PHOSPHATE; PHOSPHATE TRANSPORTER;

ARTICLE; BARREL MEDIC; GENETICS; GLOMEROMYCOTA; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; SYMBIOSIS;

GLOMEROMYCOTA; MEDICAGO TRUNCATULA; MYCORRHIZAE; PHOSPHATE TRANSPORT PROTEINS; PHOSPHATES; SYMBIOSIS;

EID: 84876714925     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-013-1842-z     Document Type: Article

References (63)

1. Allen JW, Shachar-Hill Y (2009) Sulfur transfer through an arbuscular mycorrhiza. Plant Physiol 149: 549-560.
2. Balestrini R, Gomez-Ariza J, Lanfranco L, Bonfante P (2007) Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculated cells. Mol Plant Microbe Interact 20: 1055-1062.
3. Balzergue C, Puech-Pages V, Bécard G, Rochange SF (2011) The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signaling events. J Exp Bot 62: 1049-1060.
4. Bécard G, Fortin JA (1988) Early events of vesicular arbuscular mycorrhizal formation on Ri T-DNA transformed roots. New Phytol 108: 211-218.
5. Benedetto A, Magurno F, Bonfante P, Lanfranco L (2005) Expression profiles of a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae. Mycorrhiza 15: 620-627.
6. Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24: 225-252.
7. Boivin JR, Salifu KF, Timmer VR (2004) Late-season fertilization of Picea mariana seedlings: intensive loading and outplanting response on greenhouse bioassays. Ann For Sci 61: 737-745.
8. Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 1: 1-11.
9. Breuillin F, Schramm J, Hajirezaei M et al (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64: 1002-1017.
10. Bücking H, Shachar-Hill Y (2005) Phosphate uptake, transport and transfer by the arbuscular mycorrhizal fungus Glomus intraradices is stimulated by increased carbohydrate availability. New Phytol 165: 899-911.
11. Bun-ya M, Nishimura M, Harashima S, Oshima Y (1991) The PHO84 gene of Saccharomyces cerevisiae encodes an inorganic phosphate transporter. Mol Cell Biol 11: 3229-3238.
12. Callow JA, Capaccio LCM, Parish G, Tinker PB (1978) Detection and estimation of polyphosphate in vesicular-arbuscular mycorrhizas. New Phytol 80: 125-134.
13. Doener P (2008) Phosphate starvation signaling: a threesome controls systemic Pi homeostasis. Curr Opin Plant Biol 11: 536-540.
14. Ezawa T, Smith SE, Smith FA (2001) Differentiation of polyphosphate metabolism between the extra- and intraradical hyphae of arbuscular mycorrhizal fungi. New Phytol 149: 555-563.
15. Ezawa T, Cavagnaro TR, Smith SE, Smith FA, Ohtomo R (2003) Rapid accumulation of polyphosphate in extraradical hyphae of an arbuscular mycorrhizal fungus as revealed by histochemistry and a polyphosphate kinase/luciferase system. New Phytol 161: 387-392.
16. Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, Kiers ET, Bücking H (2012) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 109: 2666-2671.
17. Gomez-Ariza J, Balestrini R, Novero M, Bonfante P (2009) Cell-specific gene expression of phosphate transporters in mycorrhizal tomato roots. Biol Fertil Soils 45: 845-853.
18. Gonzàlez-Guerrero M, Oger E, Benabdellah K, Azcόn-Aguilar C, Lanfranco L, Ferrol N (2010) Characterization of a CuZn superoxide dismutase gene in the arbuscular mycorrhizal fungus Glomus intraradices. Curr Genet 56: 265-274.
19. Guether M, Balestrini R, Hannah MA, Udvardi MK, Bonfante P (2009) Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol 182: 200-212.
20. Hammer EC, Pallon J, Wallander H, Olsson PA (2011) Tit for tat? A mycorrhizal fungus accumulates phosphorus under low plant carbon availability. FEMS Microbiol Ecol 76: 236-244.
21. Harrison MJ, van Buuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378: 626-629.
22. Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14: 2413-2429.
23. Helber N, Wippel N, Schaarschmidt S, Hause B, Requena N (2011) A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus species. is crucial for the symbiotic relationship with plants. Plant Cell 23: 3812-3823.
24. Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition. Commonwealth Agricultural Bureaux, Farnham Royal.
25. Hijikata N, Murase M, Tani C, Ohtomo R, Osaki M, Ezawa T (2010) Polyphosphate has a central role in the rapid and massive accumulation of phosphorus in extraradical mycelium of an arbuscular mycorrhizal fungus. New Phytol 186: 285-289.
26. Hohnjec N, Vieweg ME, Pühler A, Becker A, Küster H (2005) Overlaps in the transcriptional profiles of Medicagotruncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol 137: 1283-1301.
27. Humphreys CP, Franks PJ, Rees M, Bidartondo MI, Leake JR, Beerling DJ (2010) Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants. Nat Commun 1: 103.
28. Javot H, Pumplin N, Harrison MJ (2007) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30: 310-322.
29. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333: 880-882.
30. Krüger M, Krüger C, Walker C, Stockinger H, Schüßler A (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193: 970-984.
31. Lambers H, Finnegan PM, Laliberté E, Pearse SJ, Ryan MH, Shane MW, Veneklaas EJ (2011) Phosphorus nutrition of Proteaceae in severely phosphorus-impoverished soils: are there lessons to be learned for future crops? Plant Physiol 156: 1058-1066.
32. Laparre J, Balzergue C, Rochange S, Ludwiczak P, Letisse F, Portais JC, Bécard G, Puech-Pages V (2011) Metabolite profiling of pea roots in response to phosphate availability. Plant Signal Behav 6: 837-839.
33. Lawrence D (2001) Nitrogen and phosphorus enhance growth and luxury consumption of four secondary forest tree species in Borneo. J Trop Ecol 17: 859-869.
34. Maldonado-Mendoza IE, Dewbre GR, Harrison MJ (2001) 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. Mol Plant Microbe Interact 14: 1140-1148.
35. Marschner H (1995) Mineral nutrition of higher plants. Academic Press Inc, London.
36. Nagy R, Drissner D, Amrhein N, Jakobsen I, Bucher M (2009) Mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated. New Phytol 181: 950-959.
37. Oger E, Ghignone S, Campagnac E, Fontaine J, Grandmougin-Ferjani A, Lanfranco L (2009) Functional characterization of a C-4 sterol methyl oxidase from the endomycorrhizal fungus Glomus intraradices. Fungal Genet Biol 46: 486-495.
38. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6: 763-775.
39. Pearson JN, Jakobsen I (1993) Uptake by arbuscular mycorrhizal plants, measured by dual labelling with P-32 and P-33. The relative contribution of hyphae and roots to phosphorus. New Phytol 124: 489-494.
40. Péret B, Clément M, Nussaume L, Desnos T (2011) Root developmental adaptation to phosphate starvation: better safe than sorry. Trend Plant Sci 16: 442-450.
41. Pérez Torres CA, López Bucio J, Herrera Estrella L (2009) Low phosphate signaling induces changes in cell cycle gene expression by increasing auxin sensitivity in the Arabidopsis root system. Plant Signal Behav 4: 781-783.
42. Pérez-Tienda J, Testillano PS, Balestrini R, Fiorilli V, Azcón-Aguilar C, Ferrol N (2011) GintAMT2, a new member of the ammonium transporter family in the arbuscular mycorrhizal fungus Glomus intraradices. Fungal Genet Biol 48: 1044-1055.
43. Ravnskov S, Jakobsen I (1995) Functional compatibility in arbuscular mycorrhizas measured as hyphal P transport to the plant. New Phytol 129: 611-618.
44. Ririe KM, Rasmussen RP, Wittwer CT (1997) Product differentiation by analysis of DNA melting curves during the polymerase chain reaction. Anal Biochem 245: 154-160.
45. Selosse FA, Rousset M (2011) The plant-fungal marketplace. Science 333: 828-829.
46. Sharda JN, Koide RT (2010) Exploring the role of root anatomy in P-mediated control of colonization by arbuscular mycorrhizal fungi. Botany 88: 165-173.
47. Sharma NC, Sahi SV (2005) Characterization of phosphate accumulation in Lolium multiflorum for remediation of phosphorus-enriched soils. Environ Sci Technol 39: 5475-5480.
48. Smith S, Read D (2008) Mycorrhizal symbiosis. Academic Press Inc, Elsevier.
49. Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62: 227-250.
50. Smith SE, Robson AD, Abbott LK (1992) The involvement of mycorrhizas in assessment of genetically dependent efficiency of nutrient uptake and use. Plant Soil 146: 169-179.
51. Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133: 16-20.
52. Smith SE, Smith FA, Jakobsen I (2004) 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. New Phytol 162: 511-524.
53. Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156: 1050-1057.
54. Solaiman M, Ezawa T, Kojima T, Saito M (1999) Polyphosphates in intraradical and extraradical hyphae of an arbuscular mycorrhizal fungus, Gigasporamargarita. Appl Environ Microbiol 65: 5604-5606.
55. Tian C, Kasiborski B, Koul R, Lammers PJ, Bücking H, Shachar-Hill Y (2010) Regulation of the nitrogen transfer pathway in the arbuscular mycorrhizal symbiosis: gene characterization and the coordination of expression with nitrogen flux. Plant Physiol 153: 1175-1187.
56. Tinker PBH, Nye PH (2000) Solute movement in the rhizosphere. Oxford Univ Press, Oxford, UK.
57. Tisserant E, Kohler A, Dozolme-Seddas P et al (2012) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol 193: 755-769.
58. Tripler CE, Canham CD, Inouye RS, Schnurr JL (2002) Soil nitrogen availability, plant luxury consumption, and herbivory by white-tailed deer. Oecologia 133: 517-524.
59. Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorrhization VA d'un système radiculaire. Recherche de méthodes d'estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA, Paris, pp 217-221.
60. Verbruggen E, Kiers ET (2010) Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evol Appl 3: 547-560.
61. Vierheilig H, Schweiger P, Brundrett M (2005) An overview of methods for the detection and observation of arbuscular mycorrhizal fungi in roots. Physol Plant 125: 393-404.
62. Yang SY, Paszkowski U (2011) Phosphate import at the arbuscule: just a nutrient? Mol Plant Microbe Interact 24: 1296-1299.
63. Zocco D, van Aarle IM, Oger E, Lanfranco L, Declerck S (2011) Fenpropimorph and fenhexamid impact phosphorus translocation by arbuscular mycorrhizal fungi. Mycorrhiza 21: 363-374.