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 and Environment

Volumn 40, Issue 1, 2017, Pages 150-164

  Hu, Rongbin ^a   Zhu, Yinfeng ^a   Wei, Jia ^b   Chen, Jian ^a   Shi, Huazhong ^a   Shen, Guoxin ^b   Zhang, Hong ^a  

^a TEXAS TECH UNIVERSITY   (United States)

^b INSTITUTE OF PLANT PROTECTION AND MICROBIOLOGY   (China)

Author keywords

chloride channel; salt signalling; salt tolerance

Indexed keywords

CATALYSIS; CHLORIDE; DICOTYLEDON; ENZYME ACTIVITY; GENE EXPRESSION; GROWTH RATE; MEMBRANE; PHOSPHATASE; PROTEIN; SALINITY TOLERANCE; SALT; SHOOT GROWTH; TRANSGENIC PLANT;

ARABIDOPSIS; EUKARYOTA;

ARABIDOPSIS PROTEIN; CHLORIDE CHANNEL; PHOSPHOPROTEIN PHOSPHATASE 2; PP2A-C5 PROTEIN, ARABIDOPSIS; PROTEIN BINDING; SODIUM CHLORIDE;

ARABIDOPSIS; DRUG EFFECTS; ENZYME ACTIVE SITE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHYSIOLOGY; PLANT GENE; PLANT ROOT; REPRODUCIBILITY; SHOOT; SIGNAL TRANSDUCTION; TRANSGENIC PLANT; TWO HYBRID SYSTEM; UPREGULATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CATALYTIC DOMAIN; CHLORIDE CHANNELS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; MUTATION; PLANT ROOTS; PLANT SHOOTS; PLANTS, GENETICALLY MODIFIED; PROTEIN BINDING; PROTEIN PHOSPHATASE 2; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; SODIUM CHLORIDE; TWO-HYBRID SYSTEM TECHNIQUES; UP-REGULATION;

EID: 85000702013     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12837     Document Type: Article

References (61)

1. + antiport in Arabidopsis. Science 285, 1256–1258.
2. Ballesteros I., Teresa D., Sauer M., Paredes P., Duprat A., Rojo E., … Sanchez-Serrano J. (2013) 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 Journal 73, 862–872.
3. Banjara M., Zhu L., Shen G., Payton P. & Zhang H. (2011) Expression of an Arabidopsis sodium/proton antiporter gene (AtNHX1) in peanut to improve salt tolerance. Plant Biotech. Rep. 6, 59–67.
4. Barbier-Brygoo H., De Angeli A., Filleur S., Frachisse J.M., Gambale F., Thomine S. & Wege S. (2011) Anion channels/transporters in plants: from molecular bases to regulatory networks. Annual Review of Plant Biology 62, 25–51.
5. Blakeslee J.J., Zhou H.W., Heath J.T., Skottke K.R., Barrios J.A., Liu S.Y. & DeLong A. (2008) Specificity of RCN1-mediated protein phosphatase 2A regulation in meristem organization and stress response in roots. Plant Physiology 146, 539–553.
6. Blumwald E., Aharon G. & Apse M. (2000) Sodium transport in plant cells. Biochim. Biophy. Acta 1465, 140–151.
7. Bradford M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
8. Camilleri C., Azimzadeh J., Pastuglia M., Bellini C., Grandjean O. & Bouchez D. (2002) The Arabidopsis TONNEAU2 gene encodes a putative novel protein phosphatase 2A regulatory subunit essential for the control of the cortical cytoskeleton. Plant Cell 14, 833–845.
9. Chen J., Hu R., Zhu Y., Shen G. & Zhang H. (2014) Arabidopsis thaliana 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 Physiology 166, 1519–1534.
10. Clough S.J. & Bent A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant Journal 16, 735–743.
11. De Angeli A., Monachello D., Ephritikhine G., Frachisse J.M., Thomine S., Gambale F. & Barbier-Brygoo H. (2006) The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442, 939–942.
12. DeLong A. (2006) Switching the flip: protein phosphatase roles in signaling pathways. Current Opinion in Plant Biology 9, 470–477.
13. Farkas I., Dombrádi V., Miskei M., Szabados L. & Koncz C. (2007) Arabidopsis PPP family of serine/threonine phosphatases. Trend. Plant Sci. 12, 169–176.
14. Garbers C., DeLong A., Deruère J., Bernasconi P. & Soll D. (1996) A mutation in protein phosphatase 2A regulatory subunit A affects auxin transport in Arabidopsis. EMBO Journal 15, 2115–2124.
15. Gaxiola R.A., Rao R., Sherman A., Grisafi P., Alper S.L. & Fink G.R. (1999) The Arabidopsis thaliana proton transporters, Atnhx1 and Avp1, can function in cation detoxification in yeast. Proceedings of the National Academy of Sciences of the United States of America 96, 1480–1485.
16. Golemis E.A., Gyuris J. & Brent R. (1996) Interaction trap/two-hybrid system to identify interacting proteins. In Current Protocols in Molecular Biology (eds Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A. & Struhl K.), pp. 20.1.1–20.1.27. John Wiley and Sons, New York.
17. Halfter U., Ishitani M. & Zhu J.-K. (2000) The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proceedings of the National Academy of Sciences of the United States of America 97, 3735–3740.
18. Harada H., Kuromori T., Hirayama T., Shinozaki K. & Leigh R.A. (2004) Quantitative trait loci analysis of nitrate storage in Arabidopsis leading to an investigation of the contribution of the anion channel gene, AtCLC-c, to variation in nitrate levels. Journal of Experimental Botany 55, 2005–2014.
19. He X., Anderson J.C., Pozo O.D., Gu Y., Tang X. & Martin G.B. (2004) Silencing of subfamily I of protein phosphatase 2A catalytic subunits results in activation of plant defense responses and localized cell death. Plant Journal 38, 563–577.
20. He C., Yan J., Shen G., Fu L., Holaday S., Auld D., … Zhang H. (2005) Expression of an Arabidopsis vacuolar sodium/proton antiporter gene in cotton improves photosynthetic performance under salt conditions and increases fiber yield in the field. Plant Cell Physiology 46, 1848–1854.
21. Heidari B., Matre P., Nemie-Feyissa D., Meyer C., Rognli O.A., Møller S.G. & Lillo C. (2011) Protein phosphatase 2A B55 and A regulatory subunits interact with nitrate reductase and are essential for nitrate reductase activation. Plant Physiology 156, 165–172.
22. Hu R., Zhu Y., Shen G. & Zhang H. (2014) TAP46 plays a positive role in the abscisic acid insensitive 5-regulated gene expression in Arabidopsis. Plant Physiology 164, 721–734.
23. Ishitani M., Liu J., Halfter U., Kim C.S., Shi W. & Zhu J.K. (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell 12, 1667–1678.
24. Janssens V. & Goris J. (2001) Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochemical Journal 353, 417–439.
25. Jones A.M., MacLean D., Studholme D.J., Serna-Sanz A., Andreasson E., Rathjen J.P. & Peck S.C. (2009) Phosphoproteomic analysis of nuclei-enriched fractions from Arabidopsis thaliana. Journal of Proteomics 72, 439–451.
26. Jossier M., Kroniewicz L., Dalmas F., Le Thiec D., Ephritikhine G., Thomine S., … Leonhardt N. (2010) The Arabidopsis vacuolar anion transporter, AtCLCc, is involved in the regulation of stomatal movements and contributes to salt tolerance. Plant Journal 64, 563–576.
27. Kwak J.M., Moon J.-H., Murata Y., Kuchitsu K., Leonhardt N., DeLong A. & Schroeder J.I. (2002) Disruption of a guard cell-expressed protein phosphatase 2A regulatory subunit, RCN1, confers abscisic acid insensitivity in Arabidopsis. Plant Cell 14, 2849–2861.
28. Larsen P.B. & Cancel J.D. (2003) 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 Journal 34, 709–718.
29. Leivar P., Antoln-Llovera M., Ferrero S., Closa M., Arro M., Ferrer A., … Camposa N. (2011) Multilevel control of Arabidopsis 3-Hydroxy-3-Methylglutaryl coenzyme A reductase by protein phosphatase 2A. Plant Cell 23, 1494–1511.
30. Li W., Wong F., Tsai S., Phang T. & Shao G. (2006) Tonoplast-located GmCLC1 and GmNHX1 from soybean enhance NaCl tolerance in transgenic bright yellow (BY)-2 cells. Plant Cell Env. 29, 1122–1137.
31. Liu J. & Zhu J.-K. (1998) A calcium sensor homolog required for plant salt tolerance. Science 280, 1943–1945.
32. Liu J., Ishitani M., Halfter U., Kim C.S. & Zhu J.K. (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proceedings of the National Academy of Sciences of the United States of America 97, 3730–3734.
33. Luo J., Yan J., Shen G., He C. & Zhang H. (2006) AtCHIP functions as an E3 ubiquitin ligase of protein phosphatase 2A subunits and alters plant response to abscisic acid treatment. Plant Journal 46, 649–657.
34. Lv Q., Tang R., Liu H., Gao X., Li Y., Zheng H. & Zhang H. (2009) Cloning and molecular analyses of the Arabidopsis thaliana chloride channel gene family. Plant Science 176, 650–661.
35. McGinnis K., Chandler V., Cone K., Kaeppler H., Kaeppler S., Kerschen A., … Wulan T. (2005) Transgene-induced RNA interference as a tool for plant functional genomics. Methods in Enzymology 392, 1–24.
36. Munns R. (2005) Genes and salt tolerance: bringing them together. New Phytologist 167, 645–663.
37. Munns R. & Testers M. (2008) Mechanisms of salt tolerance. Annual Review of Plant Biology 59, 651–681.
38. +. Cl− in salt-treated plants. Methods Mol Biol. 639, 371–382.
39. Murashige T. & Skoog F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Plant Physiology 15, 473–497.
40. Pernas M., Garcia-Casado G., Rojo E., Solano R. & Sanchez-Serrano J.J. (2007) A protein phosphatase 2A catalytic subunit is a negative regulator of abscisic acid signaling. Plant Journal 51, 763–778.
41. + exchange activity in the plasma membrane of Arabidopsis. Plant Physiology 132, 1041–1052.
42. + homeostasis. Proceedings of the National Academy of Sciences of the United States of America 99, 9061–9066.
43. Rashotte A.M., DeLong A. & Muday G.K. (2001) Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth. Plant Cell 13, 1683–1697.
44. Reiland S., Messerli G., Baerenfaller K., Gerrits B., Endler A., Grossmann J., … Baginsky S. (2009) Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant physiology 150(2): 889–903.
45. + transport in plants. Plant Cell 14, 465–477.
46. Storey R. & Walker R.R. (1999) Citrus and salinity. Scientia Horticulturae 78, 39–81.
47. Storey R., Schachtman D.P. & Thomas M.R. (2003) Root structure and cellular chloride, sodium and potassium distribution in salinised grapevines. Plant, Cell & Environ. 26, 789–800.
48. Sun W., Deng D., Yang L., Zheng X., Yu J., Pan H. & Zhuge Q. (2013) Overexpression of the chloride channel gene (GmCLC1) from soybean increases salt tolerance in transgenic Populus deltoides × P. euramericana ‘Nanlin895’. POJ 6, 347–354.
49. Tang W., Yuan M., Wang R., Yang Y., Wang C., Oses-Prieto J.A., … Wang Z.Y. (2011) PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nature Cell Biology 13, 124–131.
50. − transport contributing to salt tolerance. Plant, Cell & Environment 33, 566–589.
51. Tseng T.S. & Briggs W.R. (2010) The Arabidopsis rcn1-1 mutation impairs dephosphorylation of Phot2, resulting in enhanced blue light responses. Plant Cell 22, 392–402.
52. Vialaret J. & Maurel C. (2014) Phosphorylation dynamics of membrane proteins from Arabidopsis roots submitted to salt stress. Proteomics 14, 1058–1070.
53. Wege S., De Angeli A., Droillard M.-J., Kroniewicz L., Merlot S., Cornu D., … Filleur S. (2014) Phosphorylation of the vacuolar anion exchanger AtCLCa is required for the stomatal response to abscisic acid. Science Signaling 7, ra65.
54. Whiteman S.A., Serazetdinova L., Jones A.M., Sanders D., Rathjen J., Peck S.C. & Maathuis F.J. (2008) Identification of novel proteins and phosphorylation sites in a tonoplast enriched membrane fraction of Arabidopsis thaliana. Proteomics 8, 3536–3547.
55. Wu G., Wang X., Li X., Kamiya Y., Otegui M.S. & Chory J. (2011) Methylation of a phosphatase specifies dephosphorylation and degradation of activated brassinosteroid receptors. Science Signaling 4, ra29.
56. − channel gene GmCLCnt. Agr. Sci. China 9, 199–206.
57. Zhou H.W., Nussbaumer C., Chao Y. & Delong A. (2004) Disparate roles for the regulatory A subunit isoforms in Arabidopsis protein phosphatase 2A. Plant Cell 16, 709–722.
58. Zhu J.K. (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Physiology and Plant Molecular Biology 53, 247–273.
59. Zhu J.K. (2003) Regulation of ion homeostasis under salt stress. Current Opinion in Plant Biology 6, 441–445.
60. Zhu J.K., Liu J. & Xiong L. (1998) Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell 10, 1181–1191.
61. Zifarelli G. & Pusch M. (2010) CLC transport proteins in plants. FEBS Letters 584, 2122–2127.