PP2A Phosphatases Take a Giant Leap in the Post-Genomics Era

Author(s): Malathi Bheri, Girdhar K. Pandey*.

Journal Name: Current Genomics

Volume 20 , Issue 3 , 2019

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Graphical Abstract:


Abstract:

Background: Protein phosphorylation is an important reversible post-translational modification, which regulates a number of critical cellular processes. Phosphatases and kinases work in a concerted manner to act as a “molecular switch” that turns-on or - off the regulatory processes driving the growth and development under normal circumstances, as well as responses to multiple stresses in plant system. The era of functional genomics has ushered huge amounts of information to the framework of plant systems. The comprehension of who’s who in the signaling pathways is becoming clearer and the investigations challenging the conventional functions of signaling components are on a rise. Protein phosphatases have emerged as key regulators in the signaling cascades. PP2A phosphatases due to their diverse holoenzyme compositions are difficult to comprehend.

Conclusion: In this review, we highlight the functional versatility of PP2A members, deciphered through the advances in the post-genomic era.

Keywords: Protein phosphorylation, protein phosphatases, Ser/Thr phosphatases, PP2A, regulatory B subunit, scaffolding A subunit, catalytic C subunit, genomics, proteomics, transcriptome profiling, stress signaling.

[1]
Bunnik, E.M.; Le Roch, K.G. An introduction to functional genomics and systems biology. Adv. Wound Care (New Rochelle), 2013, 2(9), 490-498.
[2]
Lander, E.S.; Linton, L.M.; Birren, B.; Nusbaum, C.; Zody, M.C.; Baldwin, J.; Devon, K.; Dewar, K.; Doyle, M.; FitzHugh, W.; Funke, R.; Gage, D.; Harris, K.; Heaford, A.; Howland, J.; Kann, L.; Lehoczky, J.; LeVine, R.; McEwan, P.; McKernan, K.; Meldrim, J.; Mesirov, J.P.; Miranda, C.; Morris, W.; Naylor, J.; Raymond, C.; Rosetti, M.; Santos, R.; Sheridan, A.; Sougnez, C.; Stange-Thomann, Y.; Stojanovic, N.; Subramanian, A.; Wyman, D.; Rogers, J.; Sulston, J.; Ainscough, R.; Beck, S.; Bentley, D.; Burton, J.; Clee, C.; Carter, N.; Coulson, A.; Deadman, R.; Deloukas, P.; Dunham, A.; Dunham, I.; Durbin, R.; French, L.; Grafham, D.; Gregory, S.; Hubbard, T.; Humphray, S.; Hunt, A.; Jones, M.; Lloyd, C.; McMurray, A.; Matthews, L.; Mercer, S.; Milne, S.; Mullikin, J.C.; Mungall, A.; Plumb, R.; Ross, M.; Shownkeen, R.; Sims, S.; Waterston, R.H.; Wilson, R.K.; Hillier, L.W.; McPherson, J.D.; Marra, M.A.; Mardis, E.R.; Fulton, L.A.; Chinwalla, A.T.; Pepin, K.H.; Gish, W.R.; Chissoe, S.L.; Wendl, M.C.; Delehaunty, K.D.; Miner, T.L.; Delehaunty, A.; Kramer, J.B.; Cook, L.L.; Fulton, R.S.; Johnson, D.L.; Minx, P.J.; Clifton, S.W.; Hawkins, T.; Branscomb, E.; Predki, P.; Richardson, P.; Wenning, S.; Slezak, T.; Doggett, N.; Cheng, J.F.; Olsen, A.; Lucas, S.; Elkin, C.; Uberbacher, E.; Frazier, M.; Gibbs, R.A.; Muzny, D.M.; Scherer, S.E.; Bouck, J.B.; Sodergren, E.J.; Worley, K.C.; Rives, C.M.; Gorrell, J.H.; Metzker, M.L.; Naylor, S.L.; Kucherlapati, R.S.; Nelson, D.L.; Weinstock, G.M.; Sakaki, Y.; Fujiyama, A.; Hattori, M.; Yada, T.; Toyoda, A.; Itoh, T.; Kawagoe, C.; Watanabe, H.; Totoki, Y.; Taylor, T.; Weissenbach, J.; Heilig, R.; Saurin, W.; Artiguenave, F.; Brottier, P.; Bruls, T.; Pelletier, E.; Robert, C.; Wincker, P.; Smith, D.R.; Doucette-Stamm, L.; Rubenfield, M.; Weinstock, K.; Lee, H.M.; Dubois, J.; Rosenthal, A.; Platzer, M.; Nyakatura, G.; Taudien, S.; Rump, A.; Yang, H.; Yu, J.; Wang, J.; Huang, G.; Gu, J.; Hood, L.; Rowen, L.; Madan, A.; Qin, S.; Davis, R.W.; Federspiel, N.A.; Abola, A.P.; Proctor, M.J.; Myers, R.M.; Schmutz, J.; Dickson, M.; Grimwood, J.; Cox, D.R.; Olson, M.V.; Kaul, R.; Raymond, C.; Shimizu, N.; Kawasaki, K.; Minoshima, S.; Evans, G.A.; Athanasiou, M.; Schultz, R.; Roe, B.A.; Chen, F.; Pan, H.; Ramser, J.; Lehrach, H.; Reinhardt, R.; McCombie, W.R.; de la Bastide, M.; Dedhia, N.; Blöcker, H.; Hornischer, K.; Nordsiek, G.; Agarwala, R.; Aravind, L.; Bailey, J.A.; Bateman, A.; Batzoglou, S.; Birney, E.; Bork, P.; Brown, D.G.; Burge, C.B.; Cerutti, L.; Chen, H.C.; Church, D.; Clamp, M.; Copley, R.R.; Doerks, T.; Eddy, S.R.; Eichler, E.E.; Furey, T.S.; Galagan, J.; Gilbert, J.G.; Harmon, C.; Hayashizaki, Y.; Haussler, D.; Hermjakob, H.; Hokamp, K.; Jang, W.; Johnson, L.S.; Jones, T.A.; Kasif, S.; Kaspryzk, A.; Kennedy, S.; Kent, W.J.; Kitts, P.; Koonin, E.V.; Korf, I.; Kulp, D.; Lancet, D.; Lowe, T.M.; McLysaght, A.; Mikkelsen, T.; Moran, J.V.; Mulder, N.; Pollara, V.J.; Ponting, C.P.; Schuler, G.; Schultz, J.; Slater, G.; Smit, A.F.; Stupka, E.; Szustakowki, J.; Thierry-Mieg, D.; Thierry-Mieg, J.; Wagner, L.; Wallis, J.; Wheeler, R.; Williams, A.; Wolf, Y.I.; Wolfe, K.H.; Yang, S.P.; Yeh, R.F.; Collins, F.; Guyer, M.S.; Peterson, J.; Felsenfeld, A.; Wetterstrand, K.A.; Patrinos, A.; Morgan, M.J.; de Jong, P.; Catanese, J.J.; Osoegawa, K.; Shizuya, H.; Choi, S.; Chen, Y.J.; Szustakowki, J. Initial sequencing and analysis of the human genome. Nature, 2001, 409(6822), 860-921.
[3]
Venter, J.C.; Adams, M.D.; Myers, E.W.; Li, P.W.; Mural, R.J.; Sutton, G.G.; Smith, H.O.; Yandell, M.; Evans, C.A.; Holt, R.A.; Gocayne, J.D.; Amanatides, P.; Ballew, R.M.; Huson, D.H.; Wortman, J.R.; Zhang, Q.; Kodira, C.D.; Zheng, X.H.; Chen, L.; Skupski, M.; Subramanian, G.; Thomas, P.D.; Zhang, J.; Gabor, M.G.L.; Nelson, C.; Broder, S.; Clark, A.G.; Nadeau, J.; McKusick, V.A.; Zinder, N.; Levine, A.J.; Roberts, R.J.; Simon, M.; Slayman, C.; Hunkapiller, M.; Bolanos, R.; Delcher, A.; Dew, I.; Fasulo, D.; Flanigan, M.; Florea, L.; Halpern, A.; Hannenhalli, S. Kravitz, S.; Levy, S.; Mobarry, C.; Reinert, K.; Remington, K.; Abu-Threideh, J.; Beasley, E.; Biddick, K.; Bonazzi, V.; Brandon, R.; Cargill, M.; Chandramouliswaran, I.; Charlab, R.; Chaturvedi, K.; Deng, Z.; Di Francesco, V.; Dunn, P.; Eilbeck, K.; Evangelista, C.; Gabrielian, A.E.; Gan, W.; Ge, W.; Gong, F.; Gu, Z.; Guan, P.; Heiman, T.J.; Higgins, M.E.; Ji, R.R.; Ke, Z.; Ketchum, K.A.; Lai, Z.; Lei, Y.; Li, Z.; Li, J.; Liang, Y.; Lin, X.; Lu, F.; Merkulov, G.V.; Milshina, N.; Moore, H.M.; Naik, A.K.; Narayan, V.A.; Neelam, B.; Nusskern, D.; Rusch, D.B.; Salzberg, S.; Shao, W.; Shue, B.; Sun, J.; Wang, Z.; Wang, A.; Wang, X.; Wang, J.; Wei, M.; Wides, R.; Xiao, C.; Yan, C.; Yao, A.; Ye, J.; Zhan, M.; Zhang, W.; Zhang, H.; Zhao, Q.; Zheng, L.; Zhong, F.; Zhong, W.; Zhu, S.; Zhao, S.; Gilbert, D.; Baumhueter, S.; Spier, G.; Carter, C.; Cravchik, A.; Woodage, T.; Ali, F.; An, H.; Awe, A.; Baldwin, D.; Baden, H.; Barnstead, M.; Barrow, I.; Beeson, K.; Busam, D.; Carver, A.; Center, A.; Cheng, M.L.; Curry, L.; Danaher, S.; Davenport, L.; Desilets, R.; Dietz, S.; Dodson, K.; Doup, L.; Ferriera, S.; Garg, N.; Gluecksmann, A.; Hart, B.; Haynes, J.; Haynes, C.; Heiner, C.; Hladun, S.; Hostin, D.; Houck, J.; Howland, T.; Ibegwam, C.; Johnson, J.; Kalush, F.; Kline, L.; Koduru, S.; Love, A.; Mann, F.; May, D.; McCawley, S.; McIntosh, T.; McMullen, I.; Moy, M.; Moy, L.; Murphy, B.; Nelson, K.; Pfannkoch, C.; Pratts, E.; Puri, V.; Qureshi, H.; Reardon, M.; Rodriguez, R.; Rogers, Y.H.; Romblad, D.; Ruhfel, B.; Scott, R.; Sitter, C.; Smallwood, M.; Stewart, E.; Strong, R.; Suh, E.; Thomas, R.; Tint, N.N.; Tse, S.; V.C.; Wang, G.; Wetter, J.; Williams, S.; Williams, M.; Windsor, S.; Winn-Deen, E.; Wolfe, K.; Zaveri, J.; Zaveri, K.; Abril, J.F.; Guigó, R.; Campbell, M.J.; Sjolander, K.V.; Karlak, B.; Kejariwal, A.; Mi, H.; Lazareva, B.; Hatton, T.; Narechania, A.; Diemer, K.; Muruganujan, A.; Guo, N.; Sato, S.; Bafna, V.; Istrail, S.; Lippert, R.; Schwartz, R.; Walenz, B.; Yooseph, S.; Allen, D.; Basu, A.; Baxendale, J.; Blick, L.; Caminha, M.; Carnes-Stine, J.; Caulk, P.; Chiang, Y.H.; Coyne, M.; Dahlke, C.; Mays, A.; Dombroski, M.; Donnelly, M.; Ely, D.; Esparham, S.; Fosler, C.; Gire, H.; Glanowski, S.; Glasser, K.; Glodek, A.; Gorokhov, M.; Graham, K.; Gropman, B.; Harris, M.; Heil, J.; Henderson, S.; Hoover, J.; Jennings, D.; Jordan, C.; Jordan, J.; Kasha, J.; Kagan, L.; Kraft, C.; Levitsky, A.; Lewis, M.; Liu, X.; Lopez, J.; Ma, D.; Majoros, W.; McDaniel, J.; Murphy, S.; Newman, M.; Nguyen, T.; Nguyen, N.; Nodell, M.; Pan, S.; Peck, J.; Peterson, M.; Rowe, W.; Sanders, R.; Scott, J.; Simpson, M.; Smith, T.; Sprague, A.; Stockwell, T.; Turner, R.; Venter, E.; Wang, M.; Wen, M.; Wu, D.; Wu, M.; Xia, A.; Zandieh, A.; Zhu, X. The sequence of the human genome. Science, 2001, 291(5507), 1304-1351.
[4]
Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 2000, 408(6814), 796-815.
[5]
Chen, F.; Dong, W.; Zhang, J.; Guo, X.; Chen, J.; Wang, Z.; Lin, Z.; Tang, H.; Zhang, L. The sequenced angiosperm genomes and genome databases. Front. Plant Sci., 2018, 9, 418.
[6]
Moorhead, G.B.G.; De Wever, V.; Templeton, G.; Kerk, D. Evolution of protein phosphatases in plants and animals. Biochem. J., 2009, 417(2), 401-409.
[7]
Barford, D. Molecular mechanisms of the protein serine/threonine phosphatases. Trends Biochem. Sci., 1996, 21(11), 407-412.
[8]
Hunter, T. Protein phosphorylation: what does the future hold?In: Life Sciences for the 21st Century; Ehud Keinan, I.S.; Sela, M., Eds.; Wiley: Hoboken, NJ, 2004, pp. 191-223.
[9]
Hubbard, M.J.; Cohen, P. On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem. Sci., 1993, 18(5), 172-177.
[10]
Olsen, J.V.; Vermeulen, M.; Santamaria, A.; Kumar, C.; Miller, M.L.; Jensen, L.J.; Gnad, F.; Cox, J.; Jensen, T.S.; Nigg, E.A.; Brunak, S.; Mann, M. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal., 2010, 3(104), ra3.
[11]
Sharma, K.; D’Souza, R.C.J.; Tyanova, S.; Schaab, C.; Wiśniewski, J.R.; Cox, J.; Mann, M. Ultradeep human phosphoproteome reveals a distinct regulatory nature of Tyr and Ser/Thr-based signaling. Cell Reports, 2014, 8(5), 1583-1594.
[12]
Nakagami, H.; Sugiyama, N.; Mochida, K.; Daudi, A.; Yoshida, Y.; Toyoda, T.; Tomita, M.; Ishihama, Y.; Shirasu, K. Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants. Plant Physiol., 2010, 153(3), 1161-1174.
[13]
Sugiyama, N.; Nakagami, H.; Mochida, K.; Daudi, A.; Tomita, M.; Shirasu, K.; Ishihama, Y. Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in arabidopsis. Mol. Syst. Biol., 2008, 4(1), 193.
[14]
Nguyen, T.H.N.; Brechenmacher, L.; Aldrich, J.T.; Clauss, T.R.; Gritsenko, M.A.; Hixson, K.K.; Libault, M.; Tanaka, K.; Yang, F.; Yao, Q.; Pasa-Tolić, L.; Xu, D.; Nguyen, H.T.; Stacey, G. Quantitative phosphoproteomic analysis of soybean root hairs inoculated with Bradyrhizobium japonicum. Mol. Cell. Proteomics, 2012, 11(11), 1140-1155.
[15]
Grimsrud, P.A.; den Os, D.; Wenger, C.D.; Swaney, D.L.; Schwartz, D.; Sussman, M.R.; Ane, J-M.; Coon, J.J. Large-scale phosphoprotein analysis in Medicago truncatula roots provides insight into in vivo kinase activity in legumes. Plant Physiol., 2010, 152(1), 19-28.
[16]
Olsen, J.V.; Blagoev, B.; Gnad, F.; Macek, B.; Kumar, C.; Mortensen, P.; Mann, M. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell, 2006, 127(3), 635-648.
[17]
Tonks, N.K. Protein tyrosine phosphatases-from housekeeping enzymes to master regulators of signal transduction. FEBS J., 2013, 280(2), 346-378.
[18]
Kerk, D.; Templeton, G.; Moorhead, G.B.G. Evolutionary radiation pattern of novel protein phosphatases revealed by analysis of protein data from the completely sequenced genomes of humans, green algae, and higher plants. Plant Physiol., 2008, 146(2), 351-367.
[19]
Uhrig, R.G.; Labandera, A-M.; Moorhead, G.B. Arabidopsis PPP family of serine/threonine protein phosphatases: many targets but few engines. Trends Plant Sci., 2013, 18(9), 505-513.
[20]
Keyse, S.M. An emerging family of dual specificity MAP kinase phosphatases. Biochim. Biophys. Acta, 1995, 1265(2-3), 152-160.
[21]
Brautigan, D.L. Protein Ser/ Thr phosphatases - the ugly ducklings of cell signalling. FEBS J., 2013, 280(2), 324-325.
[22]
Andreeva, A.V.; Kutuzov, M.A. Widespread presence of “Bacterial-like” PPP phosphatases in eukaryotes. BMC Evol. Biol., 2004, 4(1), 47.
[23]
Das, A.K.; Helps, N.R.; Cohen, P.T.; Barford, D. Crystal structure of the protein serine/threonine phosphatase 2C at 2.0 A resolution. EMBO J., 1996, 15(24), 6798-6809.
[24]
Ingebritsen, T.S.; Foulkes, J.G.; Cohen, P. The protein phosphatases involved in cellular regulation. 2. glycogen metabolism. Eur. J. Biochem., 1983, 132, 263-274.
[25]
Tonks, N.K. Protein tyrosine phosphatases: from genes, to function, to disease. Nat. Rev. Mol. Cell Biol., 2006, 7(11), 833-846.
[26]
Mayer-Jaekel, R.E.; Hemmings, B.A. Protein phosphatase 2A - a “Ménage à Trois.” In. Trends in Cell Biology., Elsevier Current Trends; 1994, Vol. 4(8), pp. 287-291.
[27]
Groves, M.R.; Hanlon, N.; Turowski, P.; Hemmings, B.A.; Barford, D. The structure of the protein phosphatase 2A PR65/A subunit reveals the conformation of its 15 tandemly repeated HEAT motifs. Cell, 1999, 96(1), 99-110.
[28]
Farkas, I.; Dombrádi, V.; Miskei, M.; Szabados, L.; Koncz, C. Arabidopsis PPP family of serine/threonine phosphatases. Trends Plant Sci., 2007, 12(4), 169-176.
[29]
Slabas, A.R.; Fordham-Skelton, A.P.; Fletcher, D.; Martinez-Rivas, J.M.; Swinhoe, R.; Croy, R.R.D.; Evans, I.M. Characterisation of CDNA and genomic clones encoding homologues of the 65 KDa regulatory subunit of protein phosphatase 2A in Arabidopsis thaliana. Plant Mol. Biol., 1994, 26(4), 1125-1138.
[30]
Zhou, H-W.; Nussbaumer, C.; Chao, Y.; DeLong, A. Disparate roles for the regulatory a subunit isoforms in arabidopsis protein phosphatase 2A. Plant Cell, 2004, 16(3), 709-722.
[31]
Ariño, J.; Pérez-Callejón, E.; Cunillera, N.; Camps, M.; Posas, F.; Ferrer, A. Protein phosphatases in higher plants: multiplicity of type 2A phosphatases in Arabidopsis thaliana. Plant Mol. Biol., 1993, 21(3), 475-485.
[32]
Ballesteros, I.; Domínguez, T.; Sauer, M.; Paredes, P.; Duprat, A.; Rojo, E.; Sanmartín, M.; Sánchez-Serrano, J.J. Specialized functions of the PP2A subfamily II catalytic subunits PP2A-C3 and PP2A-C4 in the distribution of auxin fluxes and development in arabidopsis. Plant J., 2013, 73(5), 862-872.
[33]
Corum, J.W.; Hartung, A.J.; Stamey, R.T.; Rundle, S.J. Characterization of DNA sequences encoding a novel isoform of the 55 KDa B regulatory subunit of the type 2A protein serine/threonine phosphatase of Arabidopsis thaliana. Plant Mol. Biol., 1996, 31(2), 419-427.
[34]
Janssens, V.; Goris, J. Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem. J., 2001, 353(Pt 3), 417-439.
[35]
White, R.J.; Davis, M.; Esmon, C.A.; Myrick, T.L.; Cochran, D.S.; Rundle, S.J. Functional analysis of the B′ subunit of arabidopsis protein phosphatase type 2A. Plant Sci., 2002, 162(2), 201-209.
[36]
Camilleri, C.; Azimzadeh, J.; Pastuglia, M.; Bellini, C.; Grandjean, O.; Bouchez, D. The arabidopsis TONNEAU2 gene encodes a putative novel protein phosphatase 2A regulatory subunit essential for the control of the cortical cytoskeleton. Plant Cell, 2002, 14(4), 833-845.
[37]
Terol, J.; Bargues, M.; Carrasco, P.; Pérez-Alonso, M.; Paricio, N. Molecular characterization and evolution of the protein phosphatase 2A B’ regulatory subunit family in plants. Plant Physiol., 2002, 129(2), 808-822.
[38]
Booker, M.A.; DeLong, A. Atypical protein phosphatase 2A gene families do not expand via paleopolyploidization. Plant Physiol., 2017, 173(2), 1283-1300.
[39]
Kerk, D.; Bulgrien, J.; Smith, D.W.; Barsam, B.; Veretnik, S.; Gribskov, M. The complement of protein phosphatase catalytic subunits encoded in the genome of arabidopsis. Plant Physiol., 2002, 129(2), 908-925.
[40]
Burge, C.; Karlin, S. Prediction of complete gene structures in human genomic DNA. J. Mol. Biol., 1997, 268(1), 78-94.
[41]
Lukashin, A.V.; Borodovsky, M. GeneMark. Hmm: new solutions for gene finding. Nucleic Acids Res., 1998, 26(4), 1107-1115.
[42]
Xue, T.; Wang, D.; Zhang, S.; Ehlting, J.; Ni, F.; Jakab, S.; Zheng, C.; Zhong, Y. Genome-wide and expression analysis of protein phosphatase 2C in rice and arabidopsis. BMC Genomics, 2008, 9, 550.
[43]
Kim, S.; Park, M.; Yeom, S.I.; Kim, Y.M.; Lee, J.M.; Lee, H.A.; Seo, E.; Choi, J.; Cheong, K.; Kim, K.T.; Jung, K.; Lee, G.W.; Oh, S.K.; Bae, C.; Kim, S.B.; Lee, H.Y.; Kim, S.Y.; Kim, M.S.; Kang, B.C.; Jo, Y.D.; Yang, H.B.; Jeong, H.J.; Kang, W.H.; Kwon, J.K.; Shin, C.; Lim, J.Y.; Park, J.H.; Huh, J.H.; Kim, J.S.; Kim, B.D.; Cohen, O.; Paran, I.; Suh, M.C.; Lee, S.B.; Kim, Y.K.; Shin, Y.; Noh, S.J.; Park, J.; Seo, Y.S.; Kwon, S.Y.; Kim, H.A.; Park, J.M.; Kim, H.J.; Choi, S.B.; Bosland, P.W.; Reeves, G.; Jo, S.H.; Lee, B.W.; Cho, H.T.; Choi, H.S.; Lee, M.S.; Yu, Y.; Do Choi, Y.; Park, B.S.; van Deynze, A.; Ashrafi, H.; Hill, T.; Kim, W.T.; Pai, H.S.; Ahn, H.K.; Yeam, I.; Giovannoni, J.J.; Rose, J.K.; Sørensen, I.; Lee, S.J.; Kim, R.W.; Choi, I.Y.; Choi, B.S.; Lim, J.S.; Lee, Y.H.; Choi, D. Genome sequence of the hot pepper provides insights into the evolution of pungency in capsicum species. Nat. Genet., 2014, 46(3), 270-278.
[44]
Singh, A.; Giri, J.; Kapoor, S.; Tyagi, A.K.; Pandey, G.K. Protein phosphatase complement in rice: genome-wide identification and transcriptional analysis under abiotic stress conditions and reproductive development. BMC Genomics, 2010, 11(1), 435.
[45]
Van Hoof, C.; Goris, J. Phosphatases in apoptosis: to be or not to be, PP2A is in the heart of the question. Biochim. Biophys. Acta, 2003, 1640(2-3), 97-104.
[46]
Codreanu, S.G.; Adams, D.G.; Dawson, E.S.; Wadzinski, B.E.; Liebler, D.C. Inhibition of protein phosphatase 2A activity by selective electrophile alkylation damage. Biochemistry, 2006, 45(33), 10020-10029.
[47]
Turowski, P.; Fernandez, A.; Favre, B.; Lamb, N.J.; Hemmings, B.A. Differential methylation and altered conformation of cytoplasmic and nuclear forms of protein phosphatase 2A during cell cycle progression. J. Cell Biol., 1995, 129(2), 397-410.
[48]
Perrotti, D.; Neviani, P. Protein phosphatase 2A: a target for anticancer therapy. Lancet Oncol., 2013, 14(6), e229-e238.
[49]
Sontag, J-M.; Sontag, E. Protein phosphatase 2A dysfunction in alzheimer’s disease. Front. Mol. Neurosci., 2014, 7, 16.
[50]
Samofalova, D.A.; Karpov, P.A.; Nuporko, A.Y.; Blume, Y.B. Reconstruction of the spatial structure of plant phosphatases types 1 and 2A in complexes with okadaic acid. Cytol. Genet., 2011, 45(3), 153-162.
[51]
Cho, U.S.; Xu, W. Crystal structure of a protein phosphatase 2A heterotrimeric holoenzyme. Nature, 2007, 445(7123), 53-57.
[52]
Magnusdottir, A.; Stenmark, P.; Flodin, S.; Nyman, T.; Kotenyova, T.; Gräslund, S.; Ogg, D.; Nordlund, P. The structure of the PP2A regulatory subunit B56γ: the remaining piece of the PP2A jigsaw puzzle. Proteins Struct. Funct. Bioinforma., 2009, 74(1), 212-221.
[53]
Wang, J.; Pei, L.; Jin, Z.; Zhang, K.; Zhang, J. Overexpression of the protein phosphatase 2A regulatory subunit a gene ZmPP2AA1 improves low phosphate tolerance by remodeling the root system architecture of maize. PLoS One, 2017, 12(4), e0176538.
[54]
Yang, J.; Roe, S.M.; Prickett, T.D.; Brautigan, D.L.; Barford, D. The structure of Tap42/A4 reveals a tetratricopeptide repeat-like fold and provides insights into PP2A regulation. Biochemistry, 2007, 46(30), 88078815.
[55]
Xing, Y.; Li, Z.; Chen, Y.; Stock, J.B.; Jeffrey, P.D.; Shi, Y. Structural mechanism of demethylation and inactivation of protein phosphatase 2A. Cell, 2008, 133(1), 154-163.
[56]
Wu, G.; Wang, X.; Li, X.; Kamiya, Y.; Otegui, M.S.; Chory, J. Methylation of a phosphatase specifies dephosphorylation and degradation of activated brassinosteroid receptors. Sci. Signal., 2011, 4(172), ra29.
[57]
Sents, W.; Ivanova, E.; Lambrecht, C.; Haesen, D.; Janssens, V. The biogenesis of active 2A Holoenzymes: a tightly regulated process creating protein phosphatase phosphatase specificity. FEBS J., 2013, 280(2), 644-661.
[58]
Chen, J.; Hu, R.; Zhu, Y.; Shen, G.; Zhang, H. Arabidopsis phosphotyrosyl phosphatase activator is essential for protein phosphatase 2A holoenzyme assembly and plays important roles in hormone signaling, salt stress response, and plant development. Plant Physiol., 2014, 166(3), 1519-1534.
[59]
Tang, W.; Yuan, M.; Wang, R.; Yang, Y.; Wang, C.; Oses-Prieto, J.A.; Kim, T.W.; Zhou, H.W.; Deng, Z.; Gampala, S.S.; Gendron, J.M.; Jonassen, E.M.; Lillo, C.; DeLong, A.; Burlingame, A.L.; Sun, Y.; Wang, Z.Y. PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat. Cell Biol., 2011, 13(2), 124-131.
[60]
Csordás, T.É.; Vissi, E.; Kovács, I.; Szöke, A.; Ariño, J.; Gergely, P.; Dudits, D.; Dombrádi, V. Protein phosphatase 2A holoenzyme and its subunits from Medicago sativa. Plant Mol. Biol., 2000, 43(4), 527-536.
[61]
Yu, R.; Zhou, Y.; Xu, Z-F.; Chye, M-L.; Kong, R.Y.C. Two genes encoding protein phosphatase 2A catalytic subunits are differentially expressed in rice. Plant Mol. Biol., 2003, 51(3), 295-311.
[62]
Yu, R.M.K.; Wong, M.M.L.; Jack, R.W.; Kong, R.Y.C. Structure, evolution and expression of a second subfamily of protein phosphatase 2A catalytic subunit genes in the rice plant (Oryza sativa L.). Planta, 2005, 222(5), 757-768.
[63]
País, S.M.; González, M.A.; Téllez-Iñón, M.T.; Capiati, D.A. Characterization of potato (Solanum tuberosum) and tomato (Solanum lycopersicum) protein phosphatases type 2A catalytic subunits and their involvement in stress responses. Planta, 2009, 230(1), 13-25.
[64]
Garbers, C.; DeLong, A.; Deruére, J.; Bernasconi, P.; Söll, D. A mutation in protein phosphatase 2A regulatory subunit A affects auxin transport in arabidopsis. EMBO J., 1996, 15(9), 2115-2124.
[65]
Deruère, J.; Jackson, K.; Garbers, C.; Söll, D.; Delong, A. The RCN1-encoded a subunit of protein phosphatase 2A increases phosphatase activity in vivo. Plant J., 1999, 20(4), 389-399.
[66]
Larsen, P.B.; Cancel, J.D. Enhanced ethylene responsiveness in the arabidopsis Eer1 mutant results from a loss-of-function mutation in the protein phosphatase 2A A regulatory subunit, RCN1. Plant J., 2003, 34(5), 709-718.
[67]
Rashotte, A.M.; DeLong, A.; Muday, G.K. Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth. Plant Cell, 2001, 13(7), 1683-1697.
[68]
Kwak, J.M.; Moon, J-H.; Murata, Y.; Kuchitsu, K.; Leonhardt, N.; DeLong, A.; Schroeder, J.I. Disruption of a guard cell-expressed protein phosphatase 2A regulatory subunit, RCN1, confers abscisic acid insensitivity in arabidopsis. Plant Cell, 2002, 14(11), 2849-2861.
[69]
Blakeslee, J.J.; Zhou, H-W.; Heath, J.T.; Skottke, K.R.; Barrios, J.A.R.; Liu, S-Y.; DeLong, A. Specificity of RCN1-mediated protein phosphatase 2A regulation in meristem organization and stress response in roots. Plant Physiol., 2007, 146(2), 539-553.
[70]
Michniewicz, M.; Zago, M.K.; Abas, L.; Weijers, D.; Schweighofer, A.; Meskiene, I.; Heisler, M.G.; Ohno, C.; Zhang, J.; Huang, F.; Schwab, R.; Weigel, D.; Meyerowitz, E.M.; Luschnig, C.; Offringa, R.; Friml, J. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell, 2007, 130(6), 1044-1056.
[71]
Heidari, B.; Matre, P.; Nemie-Feyissa, D.; Meyer, C.; Rognli, O.A.; Moller, S.G.; Lillo, C. Protein phosphatase 2A B55 and A regulatory subunits interact with nitrate reductase and are essential for nitrate reductase activation. Plant Physiol., 2011, 156(1), 165-172.
[72]
Leivar, P.; Antolín-Llovera, M.; Ferrero, S.; Closa, M.; Arró, M.; Ferrer, A.; Boronat, A.; Campos, N. Multilevel control of Arabidopsis 3-hydroxy-3-methylglutaryl coenzyme A reductase by protein phosphatase 2A. Plant Cell, 2011, 23(4), 1494-1511.
[73]
Rasool, B.; Karpinska, B.; Konert, G.; Durian, G.; Denessiouk, K.; Kangasj, Ã.S.; Foyer, C.H. Effects of light and the regulatory b-subunit composition of protein phosphatase 2A on the susceptibility of Arabidopsis thaliana to Aphid (Myzus persicae) infestation. Front. Plant Sci., 2014, 5, 405.
[74]
Heidari, B.; Nemie-Feyissa, D.; Kangasjärvi, S.; Lillo, C. Antagonistic regulation of flowering time through distinct regulatory subunits of protein phosphatase 2A. PLoS One, 2013, 8(7), e67987.
[75]
Konert, G.; Rahikainen, M.; Trotta, A.; Durian, G.; Salojärvi, J.; Khorobrykh, S.; Tyystjärvi, E.; Kangasjärvi, S. Subunits B′ γ and B′ ζ of protein phosphatase 2A regulate photo-oxidative stress responses and growth in Arabidopsis thaliana. Plant Cell Environ., 2015, 38(12), 2641-2651.
[76]
Trotta, A.; Wrzaczek, M.; Scharte, J.; Tikkanen, M.; Konert, G.; Rahikainen, M.; Holmstrom, M.; Hiltunen, H-M.; Rips, S.; Sipari, N.; Mulo, P.; Weis, E.; von Schaewen, A.; Aro, E.M.; Kangasjärvi, S. Regulatory subunit B′ of protein phosphatase 2A prevents unnecessary defense reactions under low light in arabidopsis. Plant Physiol., 2011, 156(3), 1464-1480.
[77]
Kataya, A.; Heidari, B.; Hagen, L.; Kommedal, R.; Slupphaug, G.; Lillo, C. Protein phosphatase 2A holoenzyme is targeted to peroxisomes by piggybacking and positively affects peroxisomal β-oxidation. Plant Physiol., 2015, 167(2), 493-506.
[78]
Kataya, A.; Heidari, B.; Lillo, C. Protein phosphatase 2A regulatory subunits affecting plant innate immunity, energy metabolism, and flowering time – joint functions among B’η subfamily members. Plant Signal. Behav., 2015, 10(5), e1026024.
[79]
Harris, D.M.; Myrick, T.L.; Rundle, S.J. The arabidopsis homolog of yeast TAP42 and mammalian alpha4 binds to the catalytic subunit of protein phosphatase 2A and is induced by chilling. Plant Physiol., 1999, 121(2), 609-617.
[80]
Binh, le T.; Oono, K. Molecular cloning and characterization of genes related to chilling tolerance in Rice. Plant Physiol., 1992, 99(3), 1146-1150.
[81]
Ahn, C.S.; Han, J-A.; Lee, H-S.; Lee, S.; Pai, H-S. The PP2A regulatory subunit Tap46, a component of the TOR signaling pathway, modulates growth and metabolism in plants. Plant Cell, 2011, 23(1), 185-209.
[82]
Hu, R.; Zhu, Y.; Shen, G.; Zhang, H. TAP46 plays a positive role in the Abscisic Acid Insensitive5-Regulated gene expression in arabidopsis. Plant Physiol., 2014, 164(2), 721-734.
[83]
Hu, R.; Zhu, Y.; Shen, G.; Zhang, H. Overexpression of the PP2A-C5 gene confers increased salt tolerance in Arabidopsis thaliana. Plant Signal. Behav., 2017, 12(2), e1276687.
[84]
Hu, R.; Zhu, Y.; Wei, J.; Chen, J.; Shi, H.; Shen, G.; Zhang, H. Overexpression of PP2A-C5 that encodes the catalytic subunit 5 of protein phosphatase 2A in arabidopsis confers better root and shoot development under salt conditions. Plant Cell Environ., 2017, 40(1), 150-164.
[85]
Sun, W.; Deng, D.; Yang, L.; Zheng, X.; Yu, J.; Pan, H.; Zhuge, Q. Overexpression of the chloride channel gene (GmCLC1) from soybean increases salt tolerance in transgenic Populus deltoides × P. Euramericana “Nanlin895”. Plant Omics, 2013, 6(5), 347-354.
[86]
Wei, P.; Wang, L.; Liu, A.; Yu, B.; Lam, H-M. GmCLC1 confers enhanced salt tolerance through regulating chloride accumulation in soybean. Front. Plant Sci., 2016, 7, 1082.
[87]
Jossier, M.; Kroniewicz, L.; Dalmas, F.; Le Thiec, D.; Ephritikhine, G.; Thomine, S.; Barbier-Brygoo, H.; Vavasseur, A.; Filleur, S.; Leonhardt, N. The arabidopsis vacuolar anion transporter, atclcc, is involved in the regulation of stomatal movements and contributes to salt tolerance. Plant J., 2010, 64(4), 563-576.
[88]
Pernas, M.; García-Casado, G.; Rojo, E.; Solano, R.; Sánchez-Serrano, J.J. A protein phosphatase 2A catalytic subunit is a negative regulator of abscisic acid signalling1. Plant J., 2007, 51(5), 763-778.
[89]
Xu, C.; Jing, R.; Mao, X.; Jia, X.; Chang, X. A wheat (Triticum aestivum) protein phosphatase 2A catalytic subunit gene provides enhanced drought tolerance in tobacco. Ann. Bot., 2007, 99(3), 439-450.
[90]
Liu, D.; Li, A.; Mao, X.; Jing, R. Cloning and characterization of TaPP2AbB”-α, a member of the PP2A regulatory subunit in wheat. PLoS One, 2014, 9(4), e94430.
[91]
He, X.; Anderson, J.C.; Del Pozo, O.; Gu, Y.Q.; Tang, X.; Martin, G.B. Silencing of subfamily I of protein phosphatase 2A catalytic subunits results in activation of plant defense responses and localized cell death. Plant J., 2004, 38(4), 563-577.
[92]
Dai, M.; Zhang, C.; Kania, U.; Chen, F.; Xue, Q.; Mccray, T.; Li, G.; Qin, G.; Wakeley, M.; Terzaghi, W.; Wan, J.; Zhao, Y.; Xu, J.; Friml, J.; Deng, X.W.; Wang, H.A. PP6-type phosphatase holoenzyme directly regulates PIN phosphorylation and auxin efflux in arabidopsis. Plant Cell, 2012, 24(6), 2497-2514.
[93]
Waadt, R.; Manalansan, B.; Rauniyar, N.; Munemasa, S.; Booker, M.A.; Brandt, B.; Waadt, C.; Nusinow, D.A.; Kay, S.A.; Kunz, H-H.; Schumacher, K.; DeLong, A.; Yates, J.R.; Schroeder, J.I. Identification of open stomata1-interacting proteins reveals interactions with sucrose non-fermenting1-related protein kinases2 and with type 2A protein phosphatases that function in abscisic acid responses. Plant Physiol., 2015, 169(1), 760-779.
[94]
Li, K.; Xu, C.; Fan, W.; Zhang, H.; Hou, J.; Yang, A.; Zhang, K. Phosphoproteome and proteome analyses reveal low-phosphate mediated plasticity of root developmental and metabolic regulation in maize (Zea mays L.). Plant Physiol. Biochem., 2014, 83, 232-242.
[95]
Trotta, A.; Konert, G.; Rahikainen, M.; Aro, E.M.; Kangasjärvi, S. Knock-down of protein phosphatase 2a subunit b’γ promotes phosphorylation of calreticulin 1 in Arabidopsis thaliana. Plant Signal. Behav., 2011, 6(11), 1665-1668.
[96]
Konert, G.; Trotta, A.; Kouvonen, P.; Rahikainen, M.; Durian, G.; Blokhina, O.; Fagerstedt, K.; Muth, D.; Corthals, G.L.; Kangasjärvi, S. Protein phosphatase 2A (PP2A) regulatory subunit B′γ interacts with cytoplasmic ACONITASE 3 and modulates the abundance of AOX1A and AOX1D in Arabidopsis thaliana. New Phytol., 2015, 205(3), 1250-1263.
[97]
Li, S.; Mhamdi, A.; Trotta, A.; Kangasjärvi, S.; Noctor, G. The protein phosphatase subunit PP2A-B′γ is required to suppress day length-dependent pathogenesis responses triggered by intracellular oxidative stress. New Phytol., 2014, 202(1), 145-160.


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Article Details

VOLUME: 20
ISSUE: 3
Year: 2019
Page: [154 - 171]
Pages: 18
DOI: 10.2174/1389202920666190517110605

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