Biosynthesis and possible functions of inositol pyrophosphates in plants

Frontiers in Plant Science

Volumn 6, Issue FEB, 2015, Pages

  Williams, Sarah P ^a   Gillaspy, Glenda E ^a   Perera, Imara Y ^b  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Energy metabolism; Inositol hexakisphosphate; Inositol pyrophosphate; Plant inositol signaling; VIP

Indexed keywords

EID: 84923251779     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00067     Document Type: Review

References (93)

1. Alejandro-Osorio, A. L., Huebert, D. J., Porcaro, D. T., Sonntag, M. E., Nillasithanukroh, S., Will, J. L., et al. (2009). The histone deacetylase Rpd3p is required for transient changes in genomic expression in response to stress.Genome Biol. 10:R57. doi: 10.1186/gb-2009-10-5-r57.
2. Anthony, R. G., Henriques, R., Helfer, A., Meszaros, T., Rios, G., Testerink, C., et al. (2004). A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J. 23, 572-581. doi: 10.1038/sj.emboj.7600068.
3. Avila, J., Gregory, O. G., Su, D., Deeter, T. A., Chen, S., Silva-Sanchez, C., et al. (2012). The beta-subunit of the SnRK1 complex is phosphorylated by the plant cell death suppressor Adi3. Plant Physiol. 159, 1277-1290. doi: 10.1104/pp.112.198432.
4. Azevedo, C., and Saiardi, A. (2006). Extraction and analysis of soluble inositol polyphosphates from yeast. Nat. Protoc. 1, 2416-2422. doi: 10.1038/nprot.2006.337.
5. Bennett, M., Onnebo, S. M., Azevedo, C., and Saiardi, A. (2006). Inositol pyrophosphates: metabolism and signaling. Cell. Mol. Life Sci. 63, 552-564. doi: 10.1007/s00018-005-5446-z.
6. Bhandari, R., Juluri, K. R., Resnick, A. C., and Snyder, S. H. (2008). Gene deletion of inositol hexakisphosphate kinase 1 reveals inositol pyrophosphate regulation of insulin secretion, growth, and spermiogenesis. Proc. Natl. Acad. Sci. U.S.A. 105, 2349-2353. doi: 10.1073/pnas.0712227105.
7. Bhandari, R., Saiardi, A., Ahmadibeni, Y., Snowman, A. M., Resnick, A. C., Kristiansen, T. Z., et al. (2007). Protein pyrophosphorylation by inositol pyrophosphates is a posttranslational event. Proc. Natl. Acad. Sci. U.S.A. 104, 15305-15310. doi: 10.1073/pnas.0707338104.
8. Brearley, C. A., and Hanke, D. E. (1996). Inositol phosphates in barley (Hordeum vulgare L.) aleurone tissue are stereochemically similar to the products of breakdown of InsP6 in vitro by wheat-bran phytase. Biochem. J. 318(Pt 1), 279-286.
9. Calleja, V., Alcor, D., Laguerre, M., Park, J., Vojnovic, B., Hemmings, B. A., et al. (2007). Intramolecular and intermolecular interactions of protein kinase B define its activation in vivo. PLoS Biol. 5:e95. doi: 10.1371/journal.pbio.0050095.
10. Carroll, A. S., and O'shea, E. K. (2002). Pho85 and signaling environmental conditions. Trends Biochem. Sci. 27, 87-93. doi: 10.1016/S0968-0004(01)02040-0.
11. Chakraborty, A., Koldobskiy, M. A., Bello, N. T., Maxwell, M., Potter, J. J., Juluri, K. R., et al. (2010). Inositol pyrophosphates inhibit Akt signaling, thereby regulating insulin sensitivity and weight gain. Cell 143, 897-910. doi: 10.1016/j.cell.2010.11.032.
12. Chini, A., Fonseca, S., Fernandez, G., Adie, B., Chico, J. M., Lorenzo, O., et al. (2007). The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448, 666-671. doi: 10.1038/nature06006.
13. Choi, J. H., Williams, J., Cho, J., Falck, J. R., and Shears, S. B. (2007). Purification, sequencing, and molecular identification of a mammalian PP-InsP5 kinase that is activated when cells are exposed to hyperosmotic stress. J. Biol. Chem. 282, 30763-30775. doi: 10.1074/jbc.M704655200.
14. Clouse, S. D. (2011). Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23, 1219-1230. doi: 10.1105/tpc.111.084475.
15. Da Silveira Dos Santos, A. X., Riezman, I., Aguilera-Romero, M. A., David, F., Piccolis, M., Loewith, R., et al. (2014). Systematic lipidomic analysis of yeast protein kinase and phosphatase mutants reveals novel insights into regulation of lipid homeostasis. Mol. Biol. Cell 25, 3234-3246. doi: 10.1091/mbc.E14-03-0851.
16. Desai, M., Rangarajan, P., Donahue, J. L., Williams, S. P., Land, E. S., Mandal, M. K., et al. (2014). Two inositol hexakisphosphate kinases drive inositol pyrophosphate synthesis in plants. Plant J. 80, 642-653. doi: 10.1111/tpj.12669.
17. Devarenne, T. P., Ekengren, S. K., Pedley, K. F., and Martin, G. B. (2006). Adi3 is a Pdk1-interacting AGC kinase that negatively regulates plant cell death. EMBO J. 25, 255-265. doi: 10.1038/sj.emboj.7600910.
18. Devarenne, T. P., and Martin, G. B. (2007). Manipulation of plant programmed cell death pathways during plant-pathogen interactions. Plant Signal. Behav. 2, 188-189. doi: 10.4161/psb.2.3.4150.
19. Dorsch, J. A., Cook, A., Young, K. A., Anderson, J. M., Bauman, A. T., Volkmann, C. J., et al. (2003). Seed phosphorus and inositol phosphate phenotype of barley low phytic acid genotypes. Phytochemistry 62, 691-706. doi: 10.1016/S0031-9422(02)00610-6.
20. Draskovic, P., Saiardi, A., Bhandari, R., Burton, A., Ilc, G., Kovacevic, M., et al. (2008). Inositol hexakisphosphate kinase products contain diphosphate and triphosphate groups. Chem. Biol. 15, 274-286. doi: 10.1016/j.chembiol.2008.01.011.
21. Dunlop, E. A., and Tee, A. R. (2009). Mammalian target of rapamycin complex 1: signalling inputs, substrates and feedback mechanisms. Cell. Signal. 21, 827-835. doi: 10.1016/j.cellsig.2009.01.012.
22. Flores, S., and Smart, C. C. (2000). Abscisic acid-induced changes in inositol metabolism in Spirodela polyrrhiza. Planta 211, 823-832. doi: 10.1007/s004250000348.
23. Fridy, P. C., Otto, J. C., Dollins, D. E., and York, J. D. (2007). Cloning and characterization of two human VIP1-like inositol hexakisphosphate and diphosphoinositol pentakisphosphate kinases. J. Biol. Chem. 282, 30754-30762. doi: 10.1074/jbc.M704656200.
24. Gillaspy, G. E. (2011). The cellular language of myo-inositol signaling. New Phytol. 192, 823-839. doi: 10.1111/j.1469-8137.2011.03939.x.
25. Glennon, M. C., and Shears, S. B. (1993). Turnover of inositol pentakisphosphates, inositol hexakisphosphate and diphosphoinositol polyphosphates in primary cultured hepatocytes. Biochem. J. 293(Pt 2), 583-590.
26. Gokhale, N. A., Zaremba, A., and Shears, S. B. (2011). Receptor-dependent compartmentalization of PPIP5K1, a kinase with a cryptic polyphosphoinositide binding domain. Biochem. J. 434, 415-426. doi: 10.1042/BJ20101437.
27. Hardie, D. G. (2011). AMPK and autophagy get connected. EMBO J. 30, 634-635. doi: 10.1038/emboj.2011.12.
28. Hawkins, P. T., Stephens, L. R., and Piggott, J. R. (1993). Analysis of inositol metabolites produced by Saccharomyces cerevisiae in response to glucose stimulation. J. Biol. Chem. 268, 3374-3383.
29. Heilmann, M., and Heilmann, I. (2014). Plant phosphoinositides-complex networks controlling growth and adaptation. Biochim. Biophys. Acta doi: 10.1016/j.bbalip.2014.09.018. [Epub ahead of print].
30. Hemmings, B. A., and Restuccia, D. F. (2012). PI3K-PKB/Akt pathway. Cold Spring Harb. Perspect. Biol. 4:a011189. doi: 10.1101/cshperspect.a011189.
31. Huang, C. F., Voglmaier, S. M., Bembenek, M. E., Saiardi, A., and Snyder, S. H. (1998). Identification and purification of diphosphoinositol pentakisphosphate kinase, which synthesizes the inositol pyrophosphate bis(diphospho)inositol tetrakisphosphate. Biochemistry 37, 14998-15004. doi: 10.1021/bi981920l.
32. Huang, K. N., and Symington, L. S. (1995). Suppressors of a Saccharomyces cerevisiae pkc1 mutation identify alleles of the phosphatase gene PTC1 and of a novel gene encoding a putative basic leucine zipper protein. Genetics141, 1275-1285.
33. Hung, C. Y., Aspesi, P. Jr., Hunter, M. R., Lomax, A. W., and Perera, I. Y. (2014). Phosphoinositide-signaling is one component of a robust plant defense response. Front. Plant Sci. 5:267. doi: 10.3389/fpls.2014.00267.
34. Jones, J. D., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329. doi: 10.1038/nature05286.
35. Kaffman, A., Herskowitz, I., Tjian, R., and O'shea, E. K. (1994). Phosphorylation of the transcription factor PHO4 by a cyclin-CDK complex, PHO80-PHO85. Science 263, 1153-1156. doi: 10.1126/science.8108735.
36. Klein, M., Perfus-Barbeoch, L., Frelet, A., Gaedeke, N., Reinhardt, D., Mueller-Roeber, B., et al. (2003). The plant multidrug resistance ABC transporter AtMRP5 is involved in guard cell hormonal signalling and water use. Plant J. 33, 119-129. doi: 10.1046/j.1365-313X.2003.016012.x.
37. Kuo, H. F., Chang, T. Y., Chiang, S. F., Wang, W. D., Charng, Y. Y., and Chiou, T. J. (2014). Arabidopsis inositol pentakisphosphate 2-kinase, AtIPK1, is required for growth and modulates phosphate homeostasis at the transcriptional level. Plant J. 80, 503-515. doi: 10.1111/tpj.12650.
38. Lam, E. (2004). Controlled cell death, plant survival and development. Nat. Rev. Mol. Cell Biol. 5, 305-315. doi: 10.1038/nrm1358.
39. Laussmann, T., Hansen, A., Reddy, K. M., Reddy, K. K., Falck, J. R., and Vogel, G. (1998). Diphospho-myo-inositol phosphates in Dictyostelium and Polysphondylium: identification of a new bisdiphospho-myo-inositol tetrakisphosphate. FEBS Lett. 426, 145-150. doi: 10.1016/S0014-5793(98)00329-9.
40. Laussmann, T., Reddy, K. M., Reddy, K. K., Falck, J. R., and Vogel, G. (1997). Diphospho-myo-inositol phosphates from Dictyostelium identified as D-6-diphospho-myo-inositol pentakisphosphate and D-5,6-bisdiphospho-myo-inositol tetrakisphosphate. Biochem. J. 322(Pt 1), 31-33.
41. Lee, Y. S., Mulugu, S., York, J. D., and O'shea, E. K. (2007). Regulation of a cyclin-CDK-CDK inhibitor complex by inositol pyrophosphates. Science 316, 109-112. doi: 10.1126/science.1139080.
42. Lemtiri-Chlieh, F., Macrobbie, E. A., and Brearley, C. A. (2000). Inositol hexakisphosphate is a physiological signal regulating the K+-inward rectifying conductance in guard cells. Proc. Natl. Acad. Sci. U.S.A. 97, 8687-8692. doi: 10.1073/pnas.140217497.
43. Lemtiri-Chlieh, F., Macrobbie, E. A., Webb, A. A., Manison, N. F., Brownlee, C., Skepper, J. N., et al. (2003). Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells. Proc. Natl. Acad. Sci. U.S.A. 100, 10091-10095. doi: 10.1073/pnas.1133289100.
44. Lenburg, M. E., and O'shea, E. K. (1996). Signaling phosphate starvation. Trends Biochem. Sci. 21, 383-387. doi: 10.1016/0968-0004(96)10048-7.
45. Lin, H., Fridy, P. C., Ribeiro, A. A., Choi, J. H., Barma, D. K., Vogel, G., et al. (2009). Structural analysis and detection of biological inositol pyrophosphates reveal that the family of VIP/diphosphoinositol pentakisphosphate kinases are 1/3-kinases. J. Biol. Chem. 284, 1863-1872. doi: 10.1074/jbc.M805686200.
46. Loewith, R., Jacinto, E., Wullschleger, S., Lorberg, A., Crespo, J. L., Bonenfant, D., et al. (2002). Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 10, 457-468. doi: 10.1016/S1097-2765(02)00636-6.
47. Lonetti, A., Szijgyarto, Z., Bosch, D., Loss, O., Azevedo, C., and Saiardi, A. (2011). Identification of an evolutionarily conserved family of inorganic polyphosphate endopolyphosphatases. J. Biol. Chem. 286, 31966-31974. doi: 10.1074/jbc.M111.266320.
48. Losito, O., Szijgyarto, Z., Resnick, A. C., and Saiardi, A. (2009). Inositol pyrophosphates and their unique metabolic complexity: analysis by gel electrophoresis. PLoS ONE 4:e5580. doi: 10.1371/journal.pone.0005580.
49. Martin, J. B., Laussmann, T., Bakker-Grunwald, T., Vogel, G., and Klein, G. (2000). Neo-inositol polyphosphates in the amoeba Entamoeba histolytica. J. Biol. Chem. 275, 10134-10140. doi: 10.1074/jbc.275.14.10134.
50. Mayr, G. W. (1988). A novel metal-dye detection system permits picomolar-range h.p.l.c. analysis of inositol polyphosphates from non-radioactively labelled cell or tissue specimens. Biochem. J. 254, 585-591.
51. Menniti, F. S., Miller, R. N., Putney, J. W. Jr., and Shears, S. B. (1993). Turnover of inositol polyphosphate pyrophosphates in pancreatoma cells. J. Biol. Chem. 268, 3850-3856.
52. Morel, J. B., and Dangl, J. L. (1997). The hypersensitive response and the induction of cell death in plants. Cell Death Differ. 4, 671-683. doi: 10.1038/sj.cdd.4400309.
53. Mosblech, A., Thurow, C., Gatz, C., Feussner, I., and Heilmann, I. (2011). Jasmonic acid perception by COI1 involves inositol polyphosphates in Arabidopsis thaliana. Plant J. 65, 949-957. doi: 10.1111/j.1365-313X.2011.04480.x.
54. Mulugu, S., Bai, W., Fridy, P. C., Bastidas, R. J., Otto, J. C., Dollins, D. E., et al. (2007). A conserved family of enzymes that phosphorylate inositol hexakisphosphate. Science 316, 106-109. doi: 10.1126/science.1139099.
55. Murphy, A. M., Otto, B., Brearley, C. A., Carr, J. P., and Hanke, D. E. (2008). A role for inositol hexakisphosphate in the maintenance of basal resistance to plant pathogens. Plant J. 56, 638-652. doi: 10.1111/j.1365-313X.2008.03629.x.
56. Nagy, R., Grob, H., Weder, B., Green, P., Klein, M., Frelet-Barrand, A., et al. (2009). The Arabidopsis ATP-binding cassette protein AtMRP5/AtABCC5 is a high affinity inositol hexakisphosphate transporter involved in guard cell signaling and phytate storage. J. Biol. Chem. 284, 33614-33622. doi: 10.1074/jbc.M109.030247.
57. Nishizawa, M., Komai, T., Morohashi, N., Shimizu, M., and Toh-e, A. (2008). Transcriptional repression by the Pho4 transcription factor controls the timing of SNZ1 expression. Eukaryot. Cell 7, 949-957. doi: 10.1128/EC.00366-07.
58. Norbis, F., Boll, M., Stange, G., Markovich, D., Verrey, F., Biber, J., et al. (1997). Identification of a cDNA/protein leading to an increased Pi-uptake in Xenopus laevis oocytes. J. Membr. Biol. 156, 19-24. doi: 10.1007/s002329900183.
59. O'neill, E. M., Kaffman, A., Jolly, E. R., and O'shea, E. K. (1996). Regulation of PHO4 nuclear localization by the PHO80-PHO85 cyclin-CDK complex. Science 271, 209-212. doi: 10.1126/science.271.5246.209.
60. Otto, J. C., Mulugu, S., Fridy, P. C., Chiou, S. T., Armbruster, B. N., Ribeiro, A. A., et al. (2007). Biochemical analysis of inositol phosphate kinases. Meth. Enzymol. 434, 171-185. doi: 10.1016/S0076-6879(07)34010-X.
61. Parry, G., Calderon-Villalobos, L. I., Prigge, M., Peret, B., Dharmasiri, S., Itoh, H., et al. (2009). Complex regulation of the TIR1/AFB family of auxin receptors. Proc. Natl. Acad. Sci. U.S.A. 106, 22540-22545. doi: 10.1073/pnas.0911967106.
62. Prasad, A., Jia, Y., Chakraborty, A., Li, Y., Jain, S. K., Zhong, J., et al. (2011). Inositol hexakisphosphate kinase 1 regulates neutrophil function in innate immunity by inhibiting phosphatidylinositol-(3,4,5)-trisphosphate signaling. Nat. Immunol. 12, 752-760. doi: 10.1038/ni.2052.
63. Pulloor, N. K., Nair, S., Kostic, A. D., Bist, P., Weaver, J. D., Riley, A. M., et al. (2014). Human genome-wide RNAi screen identifies an essential role for inositol pyrophosphates in Type-I interferon response. PLoS Pathog. 10:e1003981. doi: 10.1371/journal.ppat.1003981.
64. Raboy, V. (2003). myo-Inositol-1,2,3,4,5,6-hexakisphosphate. Phytochemistry 64, 1033-1043. doi: 10.1016/S0031-9422(03)00446-1.
65. Raboy, V. (2007). The ABCs of low-phytate crops. Nat. Biotechnol. 25, 874-875. doi: 10.1038/nbt0807-874.
66. Remington, D. L., Vision, T. J., Guilfoyle, T. J., and Reed, J. W. (2004). Contrasting modes of diversification in the Aux/IAA and ARF gene families. Plant Physiol. 135, 1738-1752. doi: 10.1104/pp.104.039669.
67. Saiardi, A. (2012). How inositol pyrophosphates control cellular phosphate homeostasis? Adv. Biol. Regul. 52, 351-359. doi: 10.1016/j.jbior.2012.03.002.
68. Saiardi, A., Bhandari, R., Resnick, A. C., Snowman, A. M., and Snyder, S. H. (2004). Phosphorylation of proteins by inositol pyrophosphates. Science 306, 2101-2105. doi: 10.1126/science.1103344.
69. Saiardi, A., Erdjument-Bromage, H., Snowman, A. M., Tempst, P., and Snyder, S. H. (1999). Synthesis of diphosphoinositol pentakisphosphate by a newly identified family of higher inositol polyphosphate kinases. Curr. Biol. 9, 1323-1326. doi: 10.1016/S0960-9822(00)80055-X.
70. Scheffzek, K., and Welti, S. (2012). Pleckstrin homology (PH) like domains - versatile modules in protein-protein interaction platforms. FEBS Lett. 586, 2662-2673. doi: 10.1016/j.febslet.2012.06.006.
71. Sheard, L. B., Tan, X., Mao, H., Withers, J., Ben-Nissan, G., Hinds, T. R., et al. (2010). Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468, 400-405. doi: 10.1038/nature09430.
72. Shears, S. B., Gokhale, N. A., Wang, H., and Zaremba, A. (2011). Diphosphoinositol polyphosphates: what are the mechanisms? Adv. Enzyme Regul. 51, 13-25. doi: 10.1016/j.advenzreg.2010.09.008.
73. Shears, S. B., Weaver, J. D., and Wang, H. (2013). Structural insight into inositol pyrophosphate turnover. Adv. Biol. Regul. 53, 19-27. doi: 10.1016/j.jbior.2012.10.002.
74. Shi, J., Wang, H., Schellin, K., Li, B., Faller, M., Stoop, J. M., et al. (2007). Embryo-specific silencing of a transporter reduces phytic acid content of maize and soybean seeds. Nat. Biotechnol. 25, 930-937. doi: 10.1038/nbt1322.
75. Smith, A. P., Jain, A., Deal, R. B., Nagarajan, V. K., Poling, M. D., Raghothama, K. G., et al. (2010). Histone H2A.Z regulates the expression of several classes of phosphate starvation response genes but not as a transcriptional activator. Plant Physiol. 152, 217-225. doi: 10.1104/pp.109.145532.
76. Stephens, L., Radenberg, T., Thiel, U., Vogel, G., Khoo, K. H., Dell, A., et al. (1993). The detection, purification, structural characterization, and metabolism of diphosphoinositol pentakisphosphate(s) and bisdiphosphoinositol tetrakisphosphate(s). J. Biol. Chem. 268, 4009-4015.
77. Stevenson-Paulik, J., Bastidas, R. J., Chiou, S. T., Frye, R. A., and York, J. D. (2005). Generation of phytate-free seeds in Arabidopsis through disruption of inositol polyphosphate kinases. Proc. Natl. Acad. Sci. U.S.A. 102, 12612-12617. doi: 10.1073/pnas.0504172102.
78. Suh, S. J., Wang, Y. F., Frelet, A., Leonhardt, N., Klein, M., Forestier, C., et al. (2007). The ATP binding cassette transporter AtMRP5 modulates anion and calcium channel activities in Arabidopsis guard cells. J. Biol. Chem. 282, 1916-1924. doi: 10.1074/jbc.M607926200.
79. Szijgyarto, Z., Garedew, A., Azevedo, C., and Saiardi, A. (2011). Influence of inositol pyrophosphates on cellular energy dynamics. Science 334, 802-805. doi: 10.1126/science.1211908.
80. Tan, X., Calderon-Villalobos, L. I., Sharon, M., Zheng, C., Robinson, C. V., Estelle, M., et al. (2007). Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446, 640-645. doi: 10.1038/nature05731.
81. Trinchieri, G. (2010). Type I interferon: friend or foe? J. Exp. Med. 207, 2053-2063. doi: 10.1084/jem.20101664.
82. Vanholme, B., Grunewald, W., Bateman, A., Kohchi, T., and Gheysen, G. (2007). The tify family previously known as ZIM. Trends Plant Sci. 12, 239-244. doi: 10.1016/j.tplants.2007.04.004.
83. Van Leeuwen, W., Okresz, L., Bogre, L., and Munnik, T. (2004). Learning the lipid language of plant signalling.Trends Plant Sci. 9, 378-384. doi: 10.1016/j.tplants.2004.06.008.
84. Voglmaier, S. M., Bembenek, M. E., Kaplin, A. I., Dorman, G., Olszewski, J. D., Prestwich, G. D., et al. (1996). Purified inositol hexakisphosphate kinase is an ATP synthase: diphosphoinositol pentakisphosphate as a high-energy phosphate donor. Proc. Natl. Acad. Sci. U.S.A. 93, 4305-4310. doi: 10.1073/pnas.93.9.4305.
85. Wang, H., Derose, E. F., London, R. E., and Shears, S. B. (2014). IP6K structure and the molecular determinants of catalytic specificity in an inositol phosphate kinase family. Nat. Commun. 5:4178. doi: 10.1038/ncomms5178.
86. Wang, H., Falck, J. R., Hall, T. M., and Shears, S. B. (2012). Structural basis for an inositol pyrophosphate kinase surmounting phosphate crowding. Nat. Chem. Biol. 8, 111-116. doi: 10.1038/nchembio.733.
87. Watson, P. J., Fairall, L., Santos, G. M., and Schwabe, J. W. (2012). Structure of HDAC3 bound to co-repressor and inositol tetraphosphate. Nature 481, 335-340. doi: 10.1038/nature10728.
88. Worley, J., Luo, X., and Capaldi, A. P. (2013). Inositol pyrophosphates regulate cell growth and the environmental stress response by activating the HDAC Rpd3L. Cell Rep. 3, 1476-1482. doi: 10.1016/j.celrep.2013.03.043.
89. Wundenberg, T., Grabinski, N., Lin, H., and Mayr, G. W. (2014). Discovery of InsP6-kinases as InsP6-dephosphorylating enzymes provides a new mechanism of cytosolic InsP6 degradation driven by the cellular ATP/ADP ratio. Biochem. J. 462, 173-184. doi: 10.1042/BJ20130992.
90. Xiong, Y., and Sheen, J. (2014). The role of target of rapamycin signaling networks in plant growth and metabolism.Plant Physiol. 164, 499-512. doi: 10.1104/pp.113.229948.
91. Yagci, A., Werner, A., Murer, H., and Biber, J. (1992). Effect of rabbit duodenal mRNA on phosphate transport inXenopus laevis oocytes: dependence on 1,25-dihydroxy-vitamin-D3. Pflugers Arch. 422, 211-216. doi: 10.1007/BF00376204.
92. Yan, Z., Zhao, J., Peng, P., Chihara, R. K., and Li, J. (2009). BIN2 functions redundantly with other Arabidopsis GSK3-like kinases to regulate brassinosteroid signaling. Plant Physiol. 150, 710-721. doi: 10.1104/pp.109.138099.
93. Zhang, Z., Liao, H., and Lucas, W. J. (2014). Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. J. Integr. Plant Biol. 56, 192-220. doi: 10.1111/jipb.12163.