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

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Abstract

The development of mutualistic interactions with arbuscular mycorrhizal (AM) fungi is one of the most important adaptation of terrestrial plants to face mineral nutrition requirements. As an essential plant nutrient, phosphorus uptake is acknowledged as a major benefit of the AM symbiosis, but the molecular mechanisms of its transport as inorganic phosphate (Pi) from the soil to root cells via AM fungi remain poorly known. Here we monitored the expression profile of the high-affinity phosphate transporter (PT) gene (GintPT) of Rhizophagus irregularis (DAOM 197198) in fungal structures (spores, extraradical mycelium and arbuscules), under different Pi availability, and in respect to plant connection. GintPT resulted constitutively expressed along the major steps of the fungal life cycle and the connection with the host plant was crucial to warrant GintPT high expression levels in the extraradical mycelium. The influence of Pi availability on gene expression of the fungal GintPT and the Medicago truncatula symbiosis-specific Pi transporter (MtPT4) was examined by qRT-PCR assay on microdissected arbusculated cells. The expression profiles of both genes revealed that these transporters are sensitive to changing Pi conditions: we observed that MtPT4 mRNA abundance is higher at 320 than at 32 μM suggesting that the flow towards the plant requires high concentrations. Taken on the whole, the findings highlight novel traits for the functioning of the GintPT gene and offer a molecular scenario to the models describing nutrient transfers as a cooperation between the mycorrhizal partners.

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Abbreviations

AM:

Arbuscular mycorrhizal

ARB:

Arbuscule-containing cells

Ct:

Threshold cycle

ERM:

Extraradical mycelium

IRM:

Intraradical mycelium

LMD:

Laser microdissection

P:

Phosphorus

Pi:

Inorganic orthophosphate

PT:

Phosphate transporter

ROCs:

Root organ cultures

References

  • Allen JW, Shachar-Hill Y (2009) Sulfur transfer through an arbuscular mycorrhiza. Plant Physiol 149:549–560

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bécard G, Fortin JA (1988) Early events of vesicular arbuscular mycorrhizal formation on Ri T-DNA transformed roots. New Phytol 108:211–218

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24:225–252

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat Commun 1:1–11

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Callow JA, Capaccio LCM, Parish G, Tinker PB (1978) Detection and estimation of polyphosphate in vesicular–arbuscular mycorrhizas. New Phytol 80:125–134

    Article  CAS  Google Scholar 

  • Doener P (2008) Phosphate starvation signaling: a threesome controls systemic Pi homeostasis. Curr Opin Plant Biol 11:536–540

    Article  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Harrison MJ, Van Buuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626–629

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition. Commonwealth Agricultural Bureaux, Farnham Royal

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hohnjec N, Vieweg ME, Pühler A, Becker A, Küster H (2005) Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol 137:1283–1301

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Javot H, Pumplin N, Harrison MJ (2007) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30:310–322

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic Press Inc, London

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Ravnskov S, Jakobsen I (1995) Functional compatibility in arbuscular mycorrhizas measured as hyphal P transport to the plant. New Phytol 129:611–618

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Selosse FA, Rousset M (2011) The plant-fungal marketplace. Science 333:828–829

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sharma NC, Sahi SV (2005) Characterization of phosphate accumulation in Lolium multiflorum for remediation of phosphorus-enriched soils. Environ Sci Technol 39:5475–5480

    Article  PubMed  CAS  Google Scholar 

  • Smith S, Read D (2008) Mycorrhizal symbiosis. Academic Press Inc, Elsevier

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Solaiman M, Ezawa T, Kojima T, Saito M (1999) Polyphosphates in intraradical and extraradical hyphae of an arbuscular mycorrhizal fungus, Gigaspora margarita. Appl Environ Microbiol 65:5604–5606

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tinker PBH, Nye PH (2000) Solute movement in the rhizosphere. Oxford Univ Press, Oxford, UK

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Verbruggen E, Kiers ET (2010) Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evol Appl 3:547–560

    Article  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Yang SY, Paszkowski U (2011) Phosphate import at the arbuscule: just a nutrient? Mol Plant Microbe Interact 24:1296–1299

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors express their thanks to Dr. Raffaella Balestrini for her constant and precious help in the microdissection experiments; to Dr. Cristina Calcagno and Dr. Marco Giovannetti for their support in the phosphate quantification; to Dr. Mara Novero for her assistance in the mycorrhization quantification. Research was funded by the National Project PRIN-Miur (2008) and the BIOBIT-Converging Technology project to PB. VF was funded by Risinnova Ager Project.

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Authors and Affiliations

  1. Institute for Plant Protection, Consiglio Nazionale Delle Ricerche, Viale Mattioli 25, 10125, Turin, Italy

    Valentina Fiorilli, Luisa Lanfranco & Paola Bonfante

  2. Department of Life Sciences and Systems Biology, University of Turin, Viale Mattioli 25, 10125, Turin, Italy

    Luisa Lanfranco & Paola Bonfante

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  1. Valentina Fiorilli
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  2. Luisa Lanfranco
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  3. Paola Bonfante
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Correspondence to Paola Bonfante.

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425_2013_1842_MOESM1_ESM.tif

Supplementary material 1 (TIFF 1069 kb) Fig. S1 Vitality assay in ERM and spores (SP) of R. irregularis visualized with nitroblue tetrazolium (NBT) staining. Freshly harvested undetached ERM (a-1, 2, 3) and detached ERM (b- 4, 5, 6) from ROC fungal compartment. Germinated spores and hyphae (a-1; b-4), metabolically active hyphae (a-2; b-5), fungal structures (ERM and SP) overview (a-3;b-6)

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Fiorilli, V., Lanfranco, L. & Bonfante, P. The expression of GintPT, the phosphate transporter of Rhizophagus irregularis, depends on the symbiotic status and phosphate availability. Planta 237, 1267–1277 (2013). https://doi.org/10.1007/s00425-013-1842-z

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