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Increasing phosphorus concentration in the extraradical hyphae of Rhizophagus irregularis DAOM 197198 leads to a concomitant increase in metal minerals

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Abstract

Plants associated with arbuscular mycorrhizal fungi (AMF) acquire phosphorus via roots and extraradical hyphae. How soil P level affects P accumulation within hyphae and how P in hyphae influences the accumulation of metal minerals remains little explored. A bi-compartmented in vitro cultivation system separating a root compartment (RC), containing a Ri T-DNA transformed carrot root associated to the AMF Rhizophagus irregularis DAOM 197198, from a hyphal compartment (HC), containing only the extraradical hyphae, was used. The HC contained a liquid growth medium (i.e., the modified Strullu-Romand medium containing P in the form of KH2PO4) without (0 μM) or adjusted to 35, 100, and 700 μM of KH2PO4. The accumulation of P and metal minerals (Ca, Mg, K, Na, Fe, Cu, Mn) within extraradical hyphae and AMF-colonized roots, and the expression of the phosphate transporter gene GintPT were assessed. The expression of GintPT in the extraradical hyphae did not differ in absence of KH2PO4 or in presence of 35 and 100 μM KH2PO4 in the HC but was markedly reduced in presence of 700 μM KH2PO4. Hyphal P concentration was significantly lowest in absence of KH2PO4, intermediate at 35 and 100 μM KH2PO4 and significantly highest in presence of 700 μM KH2PO4 in the HC. The concentrations of K, Mg, and Na were positively associated with the concentration of P in the extraradical hyphae developing in the HC. Similarly, P concentration in extraradical hyphae in the HC was related to P concentration in the growth medium and influenced the concentration of K, Mg, and Na. The accumulation of the metal mineral K, Mg, and Na in the extraradical hyphae developing in the HC was possibly related to their function in neutralizing the negative charges of PolyP accumulated in the hyphae.

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References

  • Bolan NS (1991) A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant Soil 134:189–207

    Article  CAS  Google Scholar 

  • Bonneau L, Huguet S, Wipf D, Pauly N, Truong H-N (2013) Combined phosphate and nitrogen limitation generates a nutrient stress transcriptome favorable for arbuscular mycorrhizal symbiosis in Medicago truncatula. New Phytol 199:188–202

    Article  CAS  PubMed  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 165:899–912

    Article  PubMed  Google Scholar 

  • Calonne M, Fontaine J, Tisserant B, Dupré De Boulois H, Grandmougin-Ferjani A, Declerck S, Lounès-Hadj Sahraoui A (2014) Polyaromatic hydrocarbons impair phosphorus transport by the arbuscular mycorrhizal fungus Rhizophagus irregularis. Chemosphere 104:97–104

    Article  CAS  PubMed  Google Scholar 

  • Chu Q, Wang XX, Yang Y, Chen FJ, Zhang FS, Feng G (2013) Mycorrhizal responsiveness of maize (Zea mays L.) genotypes as related to releasing date and available P content in soil. Mycorrhiza 23:497–505

    Article  CAS  PubMed  Google Scholar 

  • Clark RB, Zeto SK (2000) Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 23:867–902

    Article  CAS  Google Scholar 

  • Declerck S, Strullu DG, Plenchette C (1998) Monoxenic culture of the intraradical forms of Glomus sp. isolated from a tropical ecosystem: a proposed methodology for germplasm collection. Mycologia 90:579–585

    Article  Google Scholar 

  • Declerck S, Dupré De Boulois H, Bivort C, Delvaux B (2003) Extraradical mycelium of the arbuscular mycorrhizal fungus Glomus lamellosum can take up, accumulate and translocate radiocaesium under root-organ culture conditions. Environ Microbiol 5:510–516

    Article  PubMed  Google Scholar 

  • Deng Y, Chen KR, Teng W, Zhan A, Tong YP, Feng G, Cui ZL, Zhang FS, Chen XP (2014) Is the inherent potential of maize roots efficient for soil phosphorus acquisition? PLoS One 9:e90287

    Article  PubMed  PubMed Central  Google Scholar 

  • Ezawa T, Cavagnaro TR, Smith SE, Smith FA, Ohtomo R (2004) 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  CAS  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 the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 109:2666–2671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fiorilli V, Lanfranco L, Bonfante P (2013) The expression of GintPT, the phosphate transporter of Rhizophagus irregularis, depends on the symbiotic status and phosphate availability. Planta 237:1267–1277

    Article  CAS  PubMed  Google Scholar 

  • Fortin JA, Bécard G, Declerck S, Dalpé Y, St-Arnaud M, Coughlan AP, Piché Y (2002) Arbuscular mycorrhiza on root-organ cultures. Can J Bot 80:1–20

    Article  CAS  Google Scholar 

  • Gyuricza V, Dupré De Boulois H, Declerck S (2010) Effect of potassium and phosphorus on the transport of radiocesium by arbuscular mycorrhizal fungi. J Environ Radioactiv 101:482–487

    Article  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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Irving GCJ, McLaughlin MJ (1990) A rapid and simple field test for phosphorus in Olsen and Bray No. 1 extracts of soil. Commun Soil Sci Plan 21:2245–2255

    Article  CAS  Google Scholar 

  • Kiers ET, Duhamel M, Beesetty Y et al (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882

    Article  CAS  PubMed  Google Scholar 

  • Kikuchi Y, Hijikata N, Yokoyama K, Ohtomo R, Handa Y, Kawaguchi M, Saito K, Ezawa T (2014) Polyphosphate accumulation is driven by transcriptome alterations that lead to near-synchronous and near-equivalent uptake of inorganic cations in an arbuscular mycorrhizal fungus. New Phytol 204:638–649

    Article  CAS  PubMed  Google Scholar 

  • Kothari SK, Marschner H, Romheld V (1991) Contribution of the VA mycorrhizal hyphae in acquisition of phosphorus and zinc by maize grown in a calcareous soil. Plant Soil 131:177–185

    Article  CAS  Google Scholar 

  • Leigh J, Fitter AH, Hodge A (2011) Growth and symbiotic effectiveness of an arbuscular mycorrhizal fungus in organic matter in competition with soil bacteria. FEMS Microbiol Ecol 76:428–438

    Article  CAS  PubMed  Google Scholar 

  • Li XL, Marschner H, George E (1991) Acquisition of phosphorus and copper by VA-mycorrhizal hyphae and root-to-shoot transport in white clover. Plant Soil 136:49–57

    Article  CAS  Google Scholar 

  • Liu A, Hamel C, Hamilton RI, Ma BL, Smith DL (2000) Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza 9:331–336

    Article  CAS  Google Scholar 

  • Maldonado-Mendoza IE, Dewbre GR, Harrison MJ (2001) Expression of a Glomus intraradices phosphate transporter gene (GiPT) in the extra-radical mycelium of an arbuscular mycorrhiza: regulation in response to phosphate. Mol Plant Microbe Interact 14:1140–1148

    Article  CAS  PubMed  Google Scholar 

  • Marschner P (2012) Rhizosphere biology. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic, San Diego, pp 369–388

    Chapter  Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102

    CAS  Google Scholar 

  • Newsham KK, Fitter AH, Watkinson AR (1995) Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol Evol 10:407–411

    Article  CAS  PubMed  Google Scholar 

  • Ning P, Liao CS, Li S, Yu P, Zhang Y, Li XX, Li CJ (2012) Maize cob plus husks mimics the grain sink to stimulate nutrient uptake by roots. Field Crop Res 130:38–45

    Article  Google Scholar 

  • Olsson PA, Burleigh SH, Van Aarle IM (2005) The influence of external nitrogen on carbon allocation to Glomus intraradices in monoxenic arbuscular mycorrhiza. New Phytol 168:677–686

    Article  CAS  PubMed  Google Scholar 

  • Olsson PA, Hammer EC, Wallander H, Pallon J (2008) Phosphorus availability influences elemental uptake in the mycorrhizal fungus Glomus intraradices, as revealed by particle-induced X-ray emission analysis. Appl Environ Microbiol 74:4144–4148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng YF, Niu JF, Peng ZP, Zhang FS, Li CJ (2010) Shoot growth potential drives N uptake in maize plants and correlates with root growth in the soil. Field Crop Res 115:85–93

    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  CAS  PubMed  Google Scholar 

  • Rufyikiri G, Thiry Y, Declerck S (2003) Contribution of hyphae and roots to uranium uptake and translocation by arbuscular mycorrhizal carrot roots under root–organ culture conditions. New Phytol 158:391–399

    Article  CAS  Google Scholar 

  • Ryan MH, McCully ME, Huang CX (2003) Location and quantification of phosphorus and other elements in fully hydrated, soil-grown arbuscular mycorrhizas: a cryo-analytical scanning electron microscopy study. New Phytol 160:429–441

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New York

    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  CAS  PubMed  PubMed Central  Google Scholar 

  • St-Arnaud M, Hamel C, Vimard B, Caron M, Fortin JA (1996) Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus Glomus intraradices in an in vitro system in the absence of host roots. Mycol Res 100:328–332

    Article  Google Scholar 

  • Tisserant E, Malbreil M, Kuo A et al (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci U S A 110:20117–20122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD (2007) Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiol Ecol 61:295–304

    Article  CAS  PubMed  Google Scholar 

  • Voets L, de la Providencia IE, Fernandez K, Ijdo M, Cranenbrouck S, Declerck S (2009) Extraradical mycelium network of arbuscular mycorrhizal fungi allows fast colonization of seedlings under in vitro conditions. Mycorrhiza 19:347–356

    Article  PubMed  Google Scholar 

  • Walder F, van der Heijden MGA (2015) Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nat Plants 1:15159

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Jiang R, Kertesz MA, Zhang FS, Feng G (2013) Arbuscular mycorrhizal fungal hyphae mediating acidification can promote phytate mineralization in the hyphosphere of maize (Zea mays L.). Soil Biol Biochem 65:69–74

    Article  CAS  Google Scholar 

  • Watts-Williams S, Cavagnaro T (2012) Arbuscular mycorrhizas modify tomato responses to soil zinc and phosphorus addition. Biol Fertil Soils 48:285–294

    Article  CAS  Google Scholar 

  • Watts-Williams SJ, Cavagnaro TR (2014) Nutrient interactions and arbuscular mycorrhizas: a meta-analysis of a mycorrhiza-defective mutant and wild-type tomato genotype pair. Plant Soil 384:79–92

    Article  CAS  Google Scholar 

  • Zhang L, Xu M, Liu Y, Zhang FS, Hodge A, Feng G (2016) Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytol 210:1022–1032

    Article  CAS  PubMed  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

This study is supported by the State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences (G2015-02-05), the National Natural Science Foundation of China (U1403285), and the Innovative Group Grant of the National Science Foundation of China (31421092). We further thank the China Scholarship Council (File No. 201306350121) for providing a scholarship for Lin Zhang.

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Correspondence to Gu Feng.

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Zhang, L., Jiang, C., Zhou, J. et al. Increasing phosphorus concentration in the extraradical hyphae of Rhizophagus irregularis DAOM 197198 leads to a concomitant increase in metal minerals. Mycorrhiza 26, 909–918 (2016). https://doi.org/10.1007/s00572-016-0722-3

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