Site-directed mutagenesis of the Arabidopsis heterotrimeric G protein β subunit suggests divergent mechanisms of effector activation between plant and animal G proteins

Planta

Volumn 235, Issue 3, 2012, Pages 615-627

  Chakravorty, David ^a,b   Trusov, Yuri ^a   Botella, J Ramón ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

AGB1; Arabidopsis thaliana; Heterotrimeric G proteins; Signal transduction

Indexed keywords

AGB1 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT;

ANIMAL; ARABIDOPSIS; ARTICLE; FUSARIUM; GENETICS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; TRANSGENIC PLANT;

ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; FUSARIUM; GTP-BINDING PROTEIN BETA SUBUNITS; GTP-BINDING PROTEINS; MUTAGENESIS, SITE-DIRECTED; PLANTS, GENETICALLY MODIFIED; SIGNAL TRANSDUCTION;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; MAMMALIA;

EID: 84857625443     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-011-1526-5     Document Type: Article

References (74)

1. Anderson DJ, Botella JR (2007) Expression analysis and subcellular localization of the Arabidopsis thaliana G-protein β-subunit AGB1. Plant Cell Rep 26: 1469-1480.
2. Campbell EJ, Schenk PM, Kazan K, Penninckx I, Anderson JP, Maclean DJ, Cammue BPA, Ebert PR, Manners JM (2003) Pathogen-responsive expression of a putative ATP-binding cassette transporter gene conferring resistance to the diterpenoid sclareol is regulated by multiple defense signaling pathways in Arabidopsis. Plant Physiol 133: 1272-1284.
3. Chakravorty D, Botella JR (2007) Over-expression of a truncated Arabidopsis thaliana heterotrimeric G protein γ subunit results in a phenotype similar to α and β subunit knockouts. Gene 393: 163-170.
4. +-channel regulation and morphological development in Arabidopsis thaliana. Plant J 67: 840-851.
5. 2. Plant Physiol 136: 4096-4103.
6. Chen JG, Yajun G, Jones AM (2006) Differential roles of Arabidopsis heterotrimeric G-protein subunits in modulating cell division in roots. Plant Physiol 141: 887-897.
7. Clapham DE, Neer EJ (1993) New roles for G-protein βγ-dimers in transmembrane signaling. Nature 365: 403-406.
8. Clark AJ, Bissinger P, Bullock DW, Damak S, Wallace R, Whitelaw CBA, Yull F (1994) Chromosomal position effects and the modulation of transgene expression. Reprod Fertil Dev 6: 589-598.
9. Coursol S, Fan LM, Le Stunff H, Spiegel S, Gilroy S, Assmann SM (2003) Sphingolipid signalling in Arabidopsis guard cells involves heterotrimeric G proteins. Nature 423: 651-654.
10. Ding L, Pandey S, Assmann SM (2008) Arabidopsis extra-large G proteins (XLGs) regulate root morphogenesis. Plant J 53: 248-263.
11. Etheridge N, Trusov Y, Verbelen JP, Botella JR (1999) Characterization of ATDRG1, a member of a new class of GTP-binding proteins in plants. Plant Mol Biol 39: 1113-1126.
12. + and anion channels in Gβ- and RGS-deficient Arabidopsis lines. Proc Natl Acad Sci USA 105: 8476-8481.
13. Feng YQ, Lorincz MC, Fiering S, Greally JM, Bouhassira EE (2001) Position effects are influenced by the orientation of a transgene with respect to flanking chromatin. Mol Cell Biol 21: 298-309.
14. Ford CE, Skiba NP, Bae HS, Daaka YH, Reuveny E, Shekter LR, Rosal R, Weng GZ, Yang CS, Iyengar R, Miller RJ, Jan LY, Lefkowitz RJ, Hamm HE (1998) Molecular basis for interactions of G protein βγ subunits with effectors. Science 280: 1271-1274.
15. Franz S, Ehlert B, Liese A, Kurth J, Cazale AC, Romeis T (2011) Calcium-dependent protein kinase CPK21 functions in abiotic stress response in Arabidopsis thaliana. Mol Plant 4: 83-96.
16. Fredriksson R, Schioth HB (2005) The repertoire of G-protein-coupled receptors in fully sequenced genomes. Mol Pharmacol 67: 1414-1425.
17. Friedman EJ, Temple BRS, Hicks SN, Sondek J, Jones CD, Jones AM (2009) Prediction of protein-protein interfaces on G-protein β subunits reveals a novel phospholipase C β2 binding domain. J Mol Biol 392: 1044-1054.
18. Fujisawa Y, Kato T, Ohki S, Ishikawa A, Kitano H, Sasaki T, Asahi T, Iwasaki Y (1999) Suppression of the heterotrimeric G protein causes abnormal morphology, including dwarfism, in rice. Proc Natl Acad Sci USA 96: 7575-7580.
19. Grigston JC, Osuna D, Scheible WR, Liu C, Stitt M, Jones AM (2008) d-Glucose sensing by a plasma membrane regulator of G signaling protein, AtRGS1. FEBS Lett 582: 3577-3584.
20. Guerineau F, Benjdia M, Zhou DX (2003) A jasmonate-responsive element within the A. thaliana vsp1 promoter. J Exp Bot 54: 1153-1162.
21. Holtorf S, Apel K, Bohlmann H (1995) Comparison of different constitutive and inducible promoters for the overexpression of transgenes in Arabidopsis thaliana. Plant Mol Biol 29: 637-646.
22. Huang J, Taylor JP, Chen JG, Uhrig JF, Schnell DJ, Nakagawa T, Korth KL, Jones AM (2006) The plastid protein THYLAKOID FORMATION1 and the plasma membrane G-protein GPA1 interact in a novel sugar-signaling mechanism in Arabidopsis. Plant Cell 18: 1226-1238.
23. Ishikawa A (2009) The Arabidopsis G-Protein β-subunit is required for defense response against Agrobacterium tumefaciens. Biosci Biotechnol Biochem 73: 47-52.
24. Ishikawa A, Tsubouchi H, Iwasaki Y, Asahi T (1995) Molecular cloning and characterization of a cDNA for the α subunit of a G-protein from rice. Plant Cell Physiol 36: 353-359.
25. Ishikawa A, Iwasaki Y, Asahi T (1996) Molecular cloning and characterization of a cDNA for the β subunit of a G protein from rice. Plant Cell Physiol 37: 223-228.
26. Johnston CA, Taylor JP, Gao Y, Kimple AJ, Grigston JC, Chen JG, Siderovski DP, Jones AM, Willard FS (2007) GTPase acceleration as the rate-limiting step in Arabidopsis G protein-coupled sugar signaling. Proc Natl Acad Sci USA 104: 17317-17322.
27. Jones MO, Manning K, Andrews J, Wright C, Taylor IB, Thompson AJ (2008) The promoter from SlREO, a highly-expressed, root-specific Solanum lycopersicum gene, directs expression to cortex of mature roots. Funct Plant Biol 35: 1224-1233.
28. Joo JH, Wang SY, Chen JG, Jones AM, Fedoroff NV (2005) Different signaling and cell death roles of heterotrimeric G protein α and β subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 17: 957-970.
29. Kato C, Mizutani T, Tamaki H, Kumagai H, Kamiya T, Hirobe A, Fujisawa Y, Kato H, Iwasaki Y (2004) Characterization of heterotrimeric G protein complexes in rice plasma membrane. Plant J 38: 320-331.
30. Kong DY, Zhu YX, Wu HL, Cheng XD, Liang H, Ling HQ (2008) AtTHIC, a gene involved in thiamine biosynthesis in Arabidopsis thaliana. Cell Res 18: 566-576.
31. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2. 0. Bioinformatics 23: 2947-2948.
32. Lease KA, Wen JQ, Li J, Doke JT, Liscum E, Walker JC (2001) A mutant Arabidopsis heterotrimeric G-protein β subunit affects leaf, flower, and fruit development. Plant Cell 13: 2631-2641.
33. Li Y, Sternweis PM, Charnecki S, Smith TF, Gilman AG, Neer EJ, Kozasa T (1998) Sites for Gα binding on the G protein β subunit overlap with sites for regulation of phospholipase Cβ and adenylyl cyclase. J Biol Chem 273: 16265-16272.
34. Li JH, Liu YQ, Lu P, Lin HF, Bai Y, Wang XC, Chen YL (2009) A signaling pathway linking nitric oxide production to heterotrimeric G protein and hydrogen peroxide regulates extracellular calmodulin induction of stomatal closure in Arabidopsis. Plant Physiol 150: 114-124.
35. 2+-dependent binding of calmodulin to an N-terminal motif of the heterotrimeric G protein β subunit. J Biol Chem 272: 18801-18807.
36. Llorente F, Alonso-Blanco C, Sanchez-Rodriguez C, Jorda L, Molina A (2005) ERECTA receptor-like kinase and heterotrimeric G protein from Arabidopsis are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina. Plant J 43: 165-180.
37. Ma H (1994) GTP-binding proteins in plants: new members of an old family. Plant Mol Biol 26: 1611-1636.
38. Ma L, Xu X, Cui S, Sun D (1999) The presence of a heterotrimeric G protein and its role in signal transduction of extracellular calmodulin in pollen germination and tube growth. Plant Cell 11: 1351-1363.
39. Mao G, Meng X, Liu Y, Zheng Z, Chen Z, Zhang S (2011) Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23: 1639-1653.
40. Mason MG, Botella JR (2000) Completing the heterotrimer: Isolation and characterization of an Arabidopsis thaliana G protein γ-subunit cDNA. Proc Natl Acad Sci USA 97: 14784-14788.
41. Mason MG, Botella JR (2001) Isolation of a novel G-protein γ-subunit from Arabidopsis thaliana and its interaction with Gβ. Biochim Biophys Acta Gene Struct Expr 1520: 147-153.
42. Mayfield JD, Folta KM, Paul AL, Ferl RJ (2007) The 14-3-3 proteins μ and υ influence transition to flowering and early phytochrome response. Plant Physiol 145: 1692-1702.
43. McCudden CR, Hains MD, Kimple RJ, Siderovski DP, Willard FS (2005) G-protein signaling: back to the future. Cell Mol Life Sci 62: 551-577.
44. Mudgil Y, Uhrig JF, Zhou JP, Temple B, Jiang K, Jones AM (2009) Arabidopsis N-MYC DOWNREGULATED-LIKE1, a positive regulator of auxin transport in a G protein-mediated pathway. Plant Cell 21: 3591-3609.
45. Murga C, Laguinge L, Wetzker R, Cuadrado A, Gutkind JS (1998) Activation of Akt/protein kinase B by G protein-coupled receptors. a role for α and βγ subunits of heterotrimeric G proteins acting through phosphatidylinositol-3-OH kinaseγ. J Biol Chem 273: 19080-19085.
46. Myung CS, Garrison JC (2000) Role of C-terminal domains of the G protein β subunit in the activation of effecters. Proc Natl Acad Sci USA 97: 9311-9316.
47. New DC, Wong JTY (1998) The evidence for G-protein-coupled receptors and heterotrimeric G proteins in protozoa and ancestral metazoa. Biol Signals Recept 7: 98-108.
48. Oki K, Fujisawa Y, Kato H, Iwasaki Y (2005) Study of the constitutively active form of the α subunit of rice heterotrimeric G proteins. Plant Cell Physiol 46: 381-386.
49. Pandey S, Chen JG, Jones AM, Assmann SM (2006) G-protein complex mutants are hypersensitive to abscisic acid regulation of germination and postgermination development. Plant Physiol 141: 243-256.
50. Pandey S, Nelson DC, Assmann SM (2009) Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis. Cell 136: 136-148.
51. Pellegrino S, Zhang SY, Garritsen A, Simonds WF (1997) The coiled-coil region of the G protein β subunit-mutational analysis of Gγ and effector interactions. J Biol Chem 272: 25360-25366.
52. Petsch KA, Mylne J, Botella JR (2005) Cosuppression of eukaryotic release factor 1-1 in Arabidopsis affects cell elongation and radial cell division. Plant Physiol 139: 115-126.
53. Purnell MP, Botella JR (2007) Tobacco isoenzyme 1 of NAD(H)-dependent glutamate dehydrogenase catabolizes glutamate in vivo. Plant Physiol 143: 530-539.
54. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York.
55. Sternweis PC (1994) The active role of βγ in signal transduction. Curr Opin Cell Biol 6: 198-203.
56. Suharsono U, Fujisawa Y, Kawasaki T, Iwasaki Y, Satoh H, Shimamoto K (2002) The heterotrimeric G protein α subunit acts upstream of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci USA 99: 13307-13312.
57. Temple BRS, Jones AM (2007) The plant heterotrimeric G-protein complex. Annu Rev Plant Biol 58: 249-266.
58. Trusov Y, Rookes JE, Chakravorty D, Armour D, Schenk PM, Botella JR (2006) Heterotrimeric G proteins facilitate Arabidopsis resistance to necrotrophic pathogens and are involved in jasmonate signaling. Plant Physiol 140: 210-220.
59. Trusov Y, Rookes JE, Tilbrook K, Chakravorty D, Mason MG, Anderson D, Chen JG, Jones AM, Botella JR (2007) Heterotrimeric G protein γ subunits provide functional selectivity in Gβγ dimer signaling in Arabidopsis. Plant Cell 19: 1235-1250.
60. Trusov Y, Zhang W, Assmann SM, Botella JR (2008) Gγ1 + Gγ2! = Gβ: heterotrimeric G protein Gγ-deficient mutants do not recapitulate all phenotypes of Gβ-deficient mutants. Plant Physiol 147: 636-649.
61. Trusov Y, Sewelam N, Rookes JE, Kunkel M, Nowak E, Schenk PM, Botella JR (2009) Heterotrimeric G proteins-mediated resistance to necrotrophic pathogens includes mechanisms independent of salicylic acid-, jasmonic acid/ethylene- and abscisic acid-mediated defense signaling. Plant J 58: 69-81.
62. Ueguchi TM, Fujisawa Y, Kobayashi M, Ashikari M, Iwasaki Y, Kitano H, Matsuoka M (2000) Rice dwarf mutant d1, which is defective in the α subunit of the heterotrimeric G protein, affects gibberellin signal transduction. Proc Natl Acad Sci USA 97: 11638-11643.
63. Ullah H, Chen JG, Young JC, Im KH, Sussman MR, Jones AM (2001) Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis. Science 292: 2066-2069.
64. Ullah H, Chen JG, Wang SC, Jones AM (2002) Role of a heterotrimeric G protein in regulation of Arabidopsis seed germination. Plant Physiol 129: 897-907.
65. Ullah H, Chen JG, Temple B, Boyes DC, Alonso JM, Davis KR, Ecker JR, Jones AM (2003) The β-subunit of the Arabidopsis G protein negatively regulates auxin-induced cell division and affects multiple developmental processes. Plant Cell 15: 393-409.
66. Wang XQ, Ullah H, Jones AM, Assmann SM (2001) G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science 292: 2070-2072.
67. Wang TY, Zhang JH, Jing CQ, Yang XJ, Lin JT (2010) Positional effects of the matrix attachment region on transgene expression in stably transfected CHO cells. Cell Biol Int 34: 141-145.
68. Warpeha KM, Lateef SS, Lapik Y, Anderson M, Lee BS, Kaufman LS (2006) G-protein-coupled receptor 1, G-protein Gα-subunit 1, and prephenate dehydratase 1 are required for blue light-induced production of phenylalanine in etiolated Arabidopsis. Plant Physiol 140: 844-855.
69. Warpeha KM, Upadhyay S, Yeh J, Adamiak J, Hawkins SI, Lapik YR, Anderson MB, Kaufman LS (2007) The GCR1, GPA1, PRN1, NF-Y signal chain mediates both blue light and abscisic acid responses in Arabidopsis. Plant Physiol 143: 1590-1600.
70. Weiss C, Garnaat C, Mukai K, Hu Y, Ma H (1994) Isolation of cDNAs encoding guanine nucleotide-binding protein β-subunit homologues from maize (ZGB1) and Arabidopsis (AGB1). Proc Natl Acad Sci USA 91: 9554-9558.
71. 2+-permeable channel. New Phytol 176: 550-559.
72. Zhang LG, Hu GZ, Cheng YX, Huang JR (2008) Heterotrimeric G protein α and β subunits antagonistically modulate stomatal density in Arabidopsis thaliana. Dev Biol 324: 68-75.
73. Zhong HL, Wade SM, Woolf PJ, Linderman JJ, Traynor JR, Neubig RR (2003) A spatial focusing model for G protein signals: regulator of G protein signaling (RGS) protein-mediated kinetic scaffolding. J Biol Chem 278: 7278-7284.
74. Zhu HF, Li GJ, Ding L, Cui XQ, Berg H, Assmann SM, Xia YJ (2009) Arabidopsis extra large G-protein 2 (XLG2) interacts with the Gβ subunit of heterotrimeric G protein and functions in disease resistance. Mol Plant 2: 513-525.