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Soil biology

Polyphosphate polymerizing and depolymerizing activity of VTC4 protein in an arbuscular mycorrhizal fungus

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Pages 256-267 | Received 09 Nov 2021, Accepted 10 Jan 2022, Published online: 22 Jan 2022

References

  • Aksoy, M., W. Pootakham, and A. R. Grossman. 2014. “Critical Function of a Chlamydomonas reinhardtii Putative Polyphosphate Polymerase Subunit during Nutrient Deprivation.” The Plant Cell 26 (10): 4214–4229. doi:10.1105/tpc.114.129270.
  • Austin, S., and A. Mayer. 2020. “Phosphate Homeostasis − a Vital Metabolic Equilibrium Maintained through the INPHORS Signaling Pathway.” Frontiers in Microbiology 11: 1367. doi:10.3389/fmicb.2020.01367.
  • Azevedo, C., and A. Saiardi. 2017. “Eukaryotic Phosphate Homeostasis: The Inositol Pyrophosphate Perspective.” Trends in Biochemical Sciences 42 (3): 219–231. doi:10.1016/j.tibs.2016.10.008.
  • Benedetto, A., F. Magurno, P. Bonfante, and L. Lanfranco. 2005. “Expression Profiles of a Phosphate Transporter Gene (GmosPT) from the Endomycorrhizal Fungus Glomus mosseae.” Mycorrhiza 15 (8): 620–627. doi:10.1007/s00572-005-0006-9.
  • Boyce, K. J., M. Kretschmer, and J. W. Kronstad. 2006. “The vtc4 Gene Influences Polyphosphate Storage, Morphogenesis, and Virulence in the Maize Pathogen Ustilago maydis.” Eukaryotic Cell 5 (8): 1399–1409. doi:10.1128/EC.00131-06.
  • Brundrett, M. C., and L. Tedersoo. 2018. “Evolutionary History of Mycorrhizal Symbioses and Global Host Plant Diversity.” New Phytologist 220 (4): 1108–1115. doi:10.1111/nph.14976.
  • Cohen, A., N. Perzov, H. Nelson, and N. Nelson. 1999. “A Novel Family of Yeast Chaperons Involved in the Distribution of V-ATPase and Other Membrane Proteins.” Journal of Biological Chemistry 274 (38): 26885–26893. doi:10.1074/jbc.274.38.26885.
  • Darriba, D., A. M. David Posada, A. S. Kozlov, B. Morel, and T. Flouri. 2020. “ModelTest-NG: A New and Scalable Tool for the Selection of DNA and Protein Evolutionary Models.” Molecular Biology and Evolution 37 (1): 291–294. doi:10.1093/molbev/msz189.
  • Denoncourt, A., and M. Downey. 2021. “Model Systems for Studying Polyphosphate Biology: A Focus on Microorganisms.” Current Genetics 67 (3): 331–346. doi:10.1007/s00294-020-01148-x.
  • Desfougères, Y., R. Gerasimaitė, H. J. Jessen, and A. Mayer. 2016. “Vtc5, a Novel Subunit of the Vacuolar Transporter Chaperone Complex, Regulates Polyphosphate Synthesis and Phosphate Homeostasis in Yeast.” Journal of Biological Chemistry 291 (42): 22262–22275. doi:10.1074/jbc.M116.746784.
  • Ezawa, T., and K. Saito. 2018. “How Do Arbuscular Mycorrhizal Fungi Handle Phosphate? New Insights into Fine-tuning of Phosphate Metabolism.” New Phytologist 220 (4): 1116–1121. doi:10.1111/nph.15187.
  • Ezawa, T., S. E. Smith, and F. A. Smith. 2001. “Differentiation of Polyphosphate Metabolism between the Extra- and Intraradical Hyphae of Arbuscular Mycorrhizal Fungi.” New Phytologist 149 (3): 555–563. doi:10.1046/j.1469-8137.2001.00040.x.
  • Ezawa, T., T. R. Cavagnaro, S. E. Smith, F. A. Smith, and R. Ohtomo. 2004. “Rapid Accumulation of Polyphosphate in Extraradical Hyphae of an Arbuscular Mycorrhizal Fungus as Revealed by Histochemistry and a Polyphosphate Kinase/luciferase System.” New Phytologist 161 (2): 387–392. doi:10.1046/j.1469-8137.2003.00966.x.
  • Fontes, R., D. Fernandes, F. Peralta, H. Fraga, I. Maio, and J. C. Esteves Da Silva. 2008. “Pyrophosphate and Tripolyphosphate Affect Firefly Luciferase Luminescence because They Act as Substrates and Not as Allosteric Effectors.” FEBS Journal 275 (7): 1500–1509. doi:10.1111/j.1742-4658.2008.06309.x.
  • Funamoto, R., K. Saito, H. Oyaizu, T. Aono, and M. Saito. 2015. “pH Measurement of Tubular Vacuoles of an Arbuscular Mycorrhizal Fungus, Gigaspora margarita.” Mycorrhiza 25 (1): 55–60. doi:10.1007/s00572-014-0588-1.
  • Gerasimaitė, R., and A. Mayer. 2017. “Ppn2, a Novel Zn2+-dependent Polyphosphatase in the Acidocalcisome-like Yeast Vacuole.” Journal of Cell Science 130 (9): 1625–1636. doi:10.1242/jcs.201061.
  • Gerasimaite, R., I. Pavlovic, S. Capolicchio, A. Hofer, A. Schmidt, H. J. Jessen, and A. Mayer. 2017. “Inositol Pyrophosphate Specificity of the SPX-dependent Polyphosphate Polymerase VTC.” ACS Chemical Biology 12 (3): 648–653. doi:10.1021/acschembio.7b00026.
  • Gerasimaitė, R., S. Sharma, Y. Desfougères, A. Schmidt, and A. Mayer. 2014. “Coupled Synthesis and Translocation Restrains Polyphosphate to Acidocalcisome-like Vacuoles and Prevents Its Toxicity.” Journal of Cell Science 127 (23): 5093–5104. doi:10.1242/jcs.159772.
  • Gomes-Vieira, A. L., J. G. Wideman, L. Paes-Vieira, S. L. Gomes, T. A. Richards, and J. R. Meyer-Fernandes. 2018. “Evolutionary Conservation of a Core Fungal Phosphate Homeostasis Pathway Coupled to Development in Blastocladiella emersonii.” Fungal Genetics and Biology 115: 20–32. doi:10.1016/j.fgb.2018.04.004.
  • Harrison, M. J., and M. L. van Buuren. 1995. “A Phosphate Transporter from the Mycorrhizal Fungus Glomus versiforme.” Nature 378 (6557): 626–629. doi:10.1038/378626a0.
  • Hijikata, N., M. Murase, C. Tani, R. Ohtomo, M. Osaki, and T. Ezawa. 2010. “Polyphosphate Has a Central Role in the Rapid and Massive Accumulation of Phosphorus in Extraradical Mycelium of an Arbuscular Mycorrhizal Fungus.” New Phytologist 186 (2): 285–289. doi:10.1111/j.1469-8137.2009.03168.x.
  • Hothorn, M., H. Neumann, E. D. Lenherr, M. Wehner, V. Rybin, Hassa, P. O., Uttenweiler, A., et al. 2009. “Catalytic Core of a Membrane-associated Eukaryotic Polyphosphate Polymerase.” Science 324 (5926): 513–516. doi:10.1126/science.1168120.
  • Ishige, K., H. Zhang, and A. Kornberg. 2002. “Polyphosphate Kinase (PPK2), a Potent, Polyphosphate-driven Generator of GTP.” Proceedings of the National Academy of Sciences of the United States of America 99 (26): 16684–16688. doi:10.1073/pnas.262655299.
  • Jolicoeur, M., S. Germette, M. Gaudette, M. Perrier, and G. Bécard. 1998. “Intracellular pH in Arbuscular Mycorrhizal Fungi. A Symbiotic Physiological Marker.” Plant Physiology 116 (4): 1279–1288. doi:10.1104/pp.116.4.1279.
  • Kikuchi, Y., N. Hijikata, K. Yokoyama, R. Ohtomo, Y. Handa, M. Kawaguchi, K. Saito, and T. Ezawa. 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 Phytologist 204 (3): 638–649. doi:10.1111/nph.12937.
  • Kikuchi, Y., N. Hijikata, R. Ohtomo, Y. Handa, M. Kawaguchi, K. Saito, C. Masuta, and T. Ezawa. 2016. “Aquaporin-mediated Long-distance Polyphosphate Translocation Directed Towards the Host in Arbuscular Mycorrhizal Symbiosis: Application of Virus-induced Gene Silencing.” New Phytologist 211 (4): 1202–1208. doi:10.1111/nph.14016.
  • Kobae, Y., M. Kawachi, K. Saito, Y. Kikuchi, T. Ezawa, M. Maeshima, S. Hata, and T. Fujiwara. 2015. “Up-regulation of Genes Involved in N-acetylglucosamine Uptake and Metabolism Suggests a Recycling Mode of Chitin in Intraradical Mycelium of Arbuscular Mycorrhizal Fungi.” Mycorrhiza 25 (5): 411–417. doi:10.1007/s00572-014-0623-2.
  • Kohl, K., H. Zangger, M. Rossi, N. Isorce, L. F. Lye, K. L. Owens, S. M. Beverley, A. Mayer, and N. Fasel. 2018. “Importance of Polyphosphate in the Leishmania Life Cycle.” Microbial Cell 5 (8): 371–384. doi:10.15698/mic2018.08.642.
  • Kozlov, A. M., D. Darriba, T. Flouri, B. Morel, and A. Stamatakis. 2019. “RAxML-NG: A Fast, Scalable and User-friendly Tool for Maximum Likelihood Phylogenetic Inference.” Bioinformatics 35 (21): 4453–4455. doi:10.1093/bioinformatics/btz305.
  • Kuga, Y., K. Saito, K. Nayuki, R. L. Peterson, and M. Saito. 2008. “Ultrastructure of Rapidly-frozen and Freeze-substituted Germ Tubes of an Arbuscular Mycorrhizal Fungus and Localization of Polyphosphate.” New Phytologist 178 (1): 189–200. doi:10.1111/j.1469-8137.2007.02345.x.
  • Kumble, K. D., and A. Kornberg. 1996. “Endopolyphosphatases for Long Chain Inorganic Polyphosphate in Yeast and Mammals.” Journal of Biological Chemistry 271 (43): 27146–27151. doi:10.1074/jbc.271.43.27146.
  • Lander, N., P. N. Ulrich, and R. Docampo. 2013. “Trypanosoma brucei Vacuolar Transporter Chaperone 4 (TbVtc4) Is an Acidocalcisome Polyphosphate Kinase Required for in Vivo Infection.” Journal of Biological Chemistry 288 (47): 34205–34216. doi:10.1074/jbc.M113.518993.
  • Letunic, I., and P. Bork. 2019. “Interactive Tree of Life (Itol) V4: Recent Updates and New Developments.” Nucleic Acids Research 47 (W1): W256–W9. doi:10.1093/nar/gkz239.
  • Lonetti, A., Z. Szijgyarto, D. Bosch, O. Loss, C. Azevedo, and A. Saiardi. 2011. “Identification of an Evolutionarily Conserved Family of Inorganic Polyphosphate Endopolyphosphatases.” Journal of Biological Chemistry 286 (37): 31966–31974. doi:10.1074/jbc.M111.266320.
  • Maldonado-Mendoza, I. E., G. R. Dewbre, and M. J. Harrison. 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.” Molecular Plant-Microbe Interactions 14 (10): 1140–1148. doi:10.1094/MPMI.2001.14.10.1140.
  • Müller, O., H. Neumann, M. J. Bayer, and A. Mayer. 2003. “Role of the Vtc Proteins in V-ATPase Stability and Membrane Trafficking.” Journal of Cell Science 116 (6): 1107–1115. doi:10.1242/jcs.00328.
  • Müller, O., M. J. Bayer, J. S. Christopher Peters, M. M. Andersen, and A. Mayer. 2002. “The Vtc Proteins in Vacuole Fusion: Coupling NSF Activity to V0 Trans-complex Formation.” The EMBO Journal 21 (3): 259–269. doi:10.1093/emboj/21.3.259.
  • Murray, J. M., and D. I. Johnson. 2000. “Isolation and Characterization of Nrf1p, a Novel Negative Regulator of the Cdc42p GTPase in Schizosaccharomyces pombe.” Genetics 154 (1): 155–165. doi:10.1093/genetics/154.1.155.
  • Nguyen, C. T., and K. Saito. 2021. “Role of Cell Wall Polyphosphates in Phosphorus Transfer at the Arbuscular Interface in Mycorrhizas.” Frontiers in Plant Science 12: 725939. doi:10.3389/fpls.2021.725939.
  • Nguyen, P., T. Mai, Y. Ishiwata-Kimata, and Y. Kimata. 2019. “Monitoring ADP/ATP Ratio in Yeast Cells Using the Fluorescent-protein Reporter PercevalHR.” Bioscience, Biotechnology, and Biochemistry 83 (5): 824–828. doi:10.1080/09168451.2019.1574204.
  • Ogawa, N., J. DeRisi, and P. O. Brown. 2000. “New Components of a System for Phosphate Accumulation and Polyphosphate Metabolism in Saccharomyces cerevisiae Revealed by Genomic Expression Analysis.” Molecular Biology of the Cell 11 (12): 4309–4321. doi:10.1091/mbc.11.12.4309.
  • Ohtomo, R., and M. Saito. 2005. “Polyphosphate Dynamics in Mycorrhizal Roots during Colonization of an Arbuscular Mycorrhizal Fungus.” New Phytologist 167 (2): 571–578. doi:10.1111/j.1469-8137.2005.01425.x.
  • Ohtomo, R., Y. Sekiguchi, T. Kojima, and M. Saito. 2008. “Different Chain Length Specificity among Three Polyphosphate Quantification Methods.” Analytical Biochemistry 383 (2): 210–216. doi:10.1016/j.ab.2008.08.002.
  • Ozalp, V. C., T. R. Pedersen, L. J. Nielsen, and L. F. Olsen. 2010. “Time-resolved Measurements of Intracellular ATP in the Yeast Saccharomyces cerevisiae Using a New Type of Nanobiosensor.” The Journal of Biological Chemistry 285 (48): 37579–37588. doi:10.1074/jbc.M110.155119.
  • Rao, N. N., M. R. Gómez-García, and A. Kornberg. 2009. “Inorganic Polyphosphate: Essential for Growth and Survival.” Annual Review of Biochemistry 78 (1): 605–647. doi:10.1146/annurev.biochem.77.083007.093039.
  • Ritz, C., F. Baty, J. C. Streibig, and D. Gerhard. 2016. “Dose-response Analysis Using R.” PLoS One 10 (12): e0146021. doi:10.1371/journal.pone.0146021.
  • Robinson, N. A., and H. G. Wood. 1986. “Polyphosphate Kinase from Propionibacterium shermanii. Demonstration that the Synthesis and Utilization of Polyphosphate Is by a Processive Mechanism.” Journal of Biological Chemistry 261 (10): 4481–4485. doi:10.1016/S0021-9258(18)61176-7.
  • Rooney, P. J., L. Ayong, C. M. Tobin, S. N. J. Moreno, and L. J. Knoll. 2011. “TgVTC2 Is Involved in Polyphosphate Accumulation in Toxoplasma gondii.” Molecular and Biochemical Parasitology 176 (2): 121–126. doi:10.1016/j.molbiopara.2010.12.012.
  • Safrany, S. T., J. J. Caffrey, X. Yang, M. E. Bembenek, M. B. Moyer, W. A. Burkhart, and S. B. Shears. 1998. “A Novel Context for the ‘Mutt’ Module, A Guardian of Cell Integrity, in A Diphosphoinositol Polyphosphate Phosphohydrolase.” The EMBO Journal 17 (22): 6599–6607. doi:10.1093/emboj/17.22.6599.
  • Saito, K., and T. Ezawa. 2016. “Phosphorus Metabolism and Transport in Arbuscular Mycorrhizal Symbiosis.” In Molecular Mycorrhizal Symbiosis, edited by F. Martin, 197–216. New Jersey: John Wiley & Sons.
  • Sanz-Luque, E., S. Saroussi, W. Huang, N. Akkawi, and A. R. Grossman. 2020. “Metabolic Control of Acclimation to Nutrient Deprivation Dependent on Polyphosphate Synthesis.” Science Advances 6 (40): eabb5351. doi:10.1126/sciadv.abb5351.
  • Scott, R. A., and G. P. Haight Jr. 1975. “Separation and Detection of Ortho-, Pyro-, and Tripolyphosphate by Anion Exchange Thin Layer Chromatography.” Analytical Chemistry 47 (14): 2439–2440. doi:10.1021/ac60364a021.
  • Secco, D., C. Wang, H. Shou, and J. Whelan. 2012. “Phosphate Homeostasis in the Yeast Saccharomyces cerevisiae, the Key Role of the SPX Domain-containing Proteins.” FEBS Letters 586 (4): 289–295. doi:10.1016/j.febslet.2012.01.036.
  • Shi, X., and A. Kornberg. 2005. “Endopolyphosphatase in Saccharomyces cerevisiae Undergoes Post-translational Activations to Produce Short-chain Polyphosphates.” FEBS Letters 579 (9): 2014–2018. doi:10.1016/j.febslet.2005.02.032.
  • Smith, S. A., and J. H. Morrissey. 2007. “Sensitive Fluorescence Detection of Polyphosphate in Polyacrylamide Gels Using 4’,6-diamidino-2-phenylindol.” Electrophoresis 28 (19): 3461–3465. doi:10.1002/elps.200700041.
  • Smith, S. A., Y. Wang, and J. H. Morrissey. 2018. “DNA Ladders Can Be Used to Size Polyphosphate Resolved by Polyacrylamide Gel Electrophoresis.” Electrophoresis 39 (19): 2454–2459. doi:10.1002/elps.201800227.
  • Smith, S. E., and D. J. Read. 2008. Mycorrhizal Symbiosis. 3rd ed. San Diego: Academic Press.
  • Solaiman, M. Z., T. Ezawa, T. Kojima, and M. Saito. 1999. “Polyphosphates in Intraradical and Extraradical Hyphae of an Arbuscular Mycorrhizal Fungus, Gigaspora margarita.” Applied and Environmental Microbiology 65 (12): 5604–5606. doi:10.1128/AEM.65.12.5604-5606.1999.
  • Spatafora, J. W., Y. Chang, G. L. Benny, K. Lazarus, M. E. Smith, M. L. Berbee, Bonito, G., et al. 2016. “A Phylum-level Phylogenetic Classification of Zygomycete Fungi Based on Genome-scale Data.” Mycologia 108 (5): 1028–1046. doi:10.3852/16-042.
  • Takaine, M., M. Ueno, K. Kitamura, H. Imamura, and S. Yoshida. 2019. “Reliable Imaging of ATP in Living Budding and Fission Yeast.” Journal of Cell Science 132 (8): jcs230649. doi:10.1242/jcs.230649.
  • Takanishi, I., R. Ohtomo, M. Hayatsu, and M. Saito. 2009. “Short-chain Polyphosphate in Arbuscular Mycorrhizal Roots Colonized by Glomus spp.: A Possible Phosphate Pool for Host Plants.” Soil Biology & Biochemistry 41 (7): 1571–1573. doi:10.1016/j.soilbio.2009.04.002.
  • Tani, C., R. Ohtomo, M. Osaki, Y. Kuga, and T. Ezawa. 2009. “ATP-dependent but Proton Gradient-independent Polyphosphate-synthesizing Activity in Extraradical Hyphae of an Arbuscular Mycorrhizal Fungus.” Applied and Environmental Microbiology 75 (22): 7044–7050. doi:10.1128/aem.01519-09.
  • Tisserant, E., M. Malbreil, A. Kuo, A. Kohler, A. Symeonidi, R. Balestrini, P. Charron, et al. 2013. “Genome of an Arbuscular Mycorrhizal Fungus Provides Insight into the Oldest Plant Symbiosis.” Proceedings of the National Academy of Sciences of the United States of America 110 (50): 20117–20122. doi:10.1073/pnas.1313452110.
  • Uetake, Y., T. Kojima, T. Ezawa, and M. Saito. 2002. “Extensive Tubular Vacuole System in an Arbuscular Mycorrhizal Fungus, Gigaspora margarita.” New Phytologist 154 (3): 761–768. doi:10.1046/j.1469-8137.2002.00425.x.
  • Ulrich, P. N., N. Lander, S. P. Kurup, L. Reiss, J. Brewer, L. C. Soares Medeiros, K. Miranda, and R. Docampo. 2014. “The Acidocalcisome Vacuolar Transporter Chaperone 4 Catalyzes the Synthesis of Polyphosphate in Insect-stages of Trypanosoma brucei and T. Cruzi.” Journal of Eukaryotic Microbiology 61 (2): 155–165. doi:10.1111/jeu.12093.
  • Uttenweiler, A., H. Schwarz, H. Neumann, and A. Mayer. 2006. “The Vacuolar Transporter Chaperone (VTC) Complex Is Required for Microautophagy.” Molecular Biology of the Cell 18 (1): 166–175. doi:10.1091/mbc.e06-08-0664.
  • Viereck, N., P. E. Hansen, and I. Jakobsen. 2004. “Phosphate Pool Dynamics in the Arbuscular Mycorrhizal Fungus Glomus intraradices Studied by in Vivo 31P NMR Spectroscopy.” New Phytologist 162 (3): 783–794. doi:10.1111/j.1469-8137.2004.01048.x.
  • Walther, T., M. Novo, K. Rössger, F. Létisse, M.-O. Loret, J.-C. Portais, and F. Jean-Marie. 2010. “Control of ATP Homeostasis during the Respiro-fermentative Transition in Yeast.” Molecular Systems Biology 6 (1): 344. doi:10.1038/msb.2009.100.
  • Wang, L., X. Q. Jia, Y. X. Zhang, L. Xu, B. Menand, H. Y. Zhao, H. Q. Zeng, L. Dolan, Y. Y. Zhu, and K. K. Yi. 2021. “Loss of Two Families of SPX Domain-containing Proteins Required for Vacuolar Polyphosphate Accumulation Coincides with the Transition to Phosphate Storage in Green Plants.” Molecular Plant 14 (5): 838–846. doi:10.1016/j.molp.2021.01.015.
  • Wild, R., R. Gerasimaite, J.-Y. Jung, V. Truffault, I. Pavlovic, A. Schmidt, A. Saiardi, et al. 2016. “Control of Eukaryotic Phosphate Homeostasis by Inositol Polyphosphate Sensor Domains.” Science 352 (6288): 986–990. doi:10.1126/science.aad9858.
  • Wurst, H., and A. Kornberg. 1994. “A Soluble Exopolyphosphatase of Saccharomyces cerevisiae. Purification and Charcterization.” Journal of Biological Chemistry 269 (15): 10996–11001. doi:10.1016/S0021-9258(19)78082-X.
  • Wurst, H., T. Shiba, and A. Kornberg. 1995. “The Gene for a Major Exopolyphosphatase of Saccharomyces cerevisiae.” Journal of Bacteriology 177 (4): 898–906. doi:10.1128/jb.177.4.898-906.1995.
  • Zhang, H., K. Ishige, and A. Kornberg. 2002. “A Polyphosphate Kinase (PPK2) Widely Conserved in Bacteria.” Proceedings of the National Academy of Sciences of the United States of America 99 (26): 16678–16683. doi:10.1073/pnas.262655199.

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