Characterization of wound-responsive RNA-binding proteins and their splice variants in Arabidopsis

Plant Molecular Biology

Volumn 67, Issue 1-2, 2008, Pages 71-88

  Bove, Jérôme ^a,b   Kim, Cha Young ^a,c   Gibson, Caroline A ^a   Assmann, Sarah M ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

Alternative splicing; hnRNP; RNA binding protein; RNA recognition motif; UBA2; Wounding

Indexed keywords

ABSCISIC ACID; ARABIDOPSIS PROTEIN; BETA GLUCURONIDASE; MESSENGER RNA; RNA BINDING PROTEIN; UBA2A PROTEIN, ARABIDOPSIS; UBA2B PROTEIN, ARABIDOPSIS; UBA2C PROTEIN, ARABIDOPSIS; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CHEMISTRY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

ABSCISIC ACID; ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; GLUCURONIDASE; MOLECULAR SEQUENCE DATA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS THALIANA; VICIA FABA;

EID: 42149149278     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-008-9302-z     Document Type: Article

References (84)

1. Albà MM, Pagès M (1998) Plant proteins containing the RNA-recognition motif. Tr Plant Sci 3:15-21
2. Ali GS, Golovkin M, Reddy ASN (2003) Nuclear localization and in vivo dynamics of a plant-specific serine/arginine-rich protein. Plant J 36:883-893
3. Banihashemi L, Wilson GM, Das N, Brewer G (2006) Upf1/Upf2 regulation of 3′ untranslated region splice variants of AUF1 links nonsense-mediated and A + U-rich element-mediated mRNA decay. Mol Cell Biol 26:8743-8754
4. Bassett CL, Artlip TS, Callahan AM (2002) Characterization of the peach homologue of the ethylene receptor, PpETR1, reveals some unusual features regarding transcript processing. Planta 215:679-688
5. Benhamou N, Chambreland H, Pauzé FJ (1990) Implication of pectic components in cell surface interactions between tomato root cells and Fusarium oxysporum f. sp. radicis-lycopersici. Plant Physiol 92:995-1003
6. Birkenmeier FG, Ryan CA (1998) Wound signaling in tomato plants. Evidence that ABA is not a primary signal for defense gene activation. Plant Physiol 117:687-693
7. Bocobza S, Adato A, Mandel T, Shapira M, Nudler E, Aharoni A (2007) Riboswitch-dependent gene regulation and its evolution in the plant kingdom. Genes Dev 21:2874-2879
8. Braam J, Davis RW (1990) Rain-, wind- and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 60:357-364
9. Brown JWS, Shaw PJ, Shaw P, Marshall DF (2004) Arabidopsis nucleolar protein database (AtNoPDB). Nucl Acids Res 33:633-636
10. Carrington JC (1995) Targeting of proteins to the nucleus. In: Galbraith DW, Bourque DP, Bohnert HJ (eds) Methods in plant cell biology. Academic Press, San Diego, pp 283-293
11. Chan M-T, Yu S-M (1998) The 3′ untranslated region of a rice α-amylase gene functions as a sugar-dependent mRNA stability determinant. Proc Natl Acad Sci USA 95:6543-6547
12. Charrier B, Champion A, Henry Y, Kreis M (2002) Expression profiling of the whole Arabidopsis shaggy-like kinase multigene family by real-time reverse transcriptase polymerase chain reaction. Plant Physiol 130:577-590
13. Cheong YH, Chang H-S, Gupta R, Wang X, Zhu T, Jan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129:661-677
14. Chowdhury B, Tsokos CG, Krishnan S, Robertson J, Fisher CU, Warke RG, Warke VG, Nambiar MP, Tsokos GC (2005) Decreased stability and translation of T cell receptor zeta mRNA with an alternatively spliced 3′-untranslated region contribute to zeta chain down-regulation in patients with systemic lupus erythematosus. J Biol Chem 280:18959-18966
15. Clark DG, Richards C, Hilioti Z, Lind-Iversen S, Brown K (1997) Effect of pollination on accumulation of ACC synthase and ACC oxidase transcripts, ethylene production and flower petal abscission in geranium (Pelargonium x hortorum L.H. Bailey). Plant Mol Biol 34:855-865
16. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735-743
17. Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991-1995
18. Creelman RA, Tierney ML, Mullet JE (1992) Jasmonic acid/methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expression. Proc Natl Acad Sci USA 89:4938-4941
19. daSilva I, Angelo PCS, Molfetta JB, Ferraz MT, daSilva LLP, Goldman GH, Goldman MHS (2002) A tobacco cDNA reveals two different transcription patterns in vegetative and reproductive organs. Braz J Med Biol Res 35:861-868
20. Delessert D, Wilson I, Van Der Straeten D, Dennis E, Dolferus R (2004) Spatial and temporal analysis of the local response to wounding in Arabidopsis leaves. Plant Mol Biol 55:165-181
21. Didierjean L, Frendo P, Nasser W, Genot G, Marivet J, Burkard G (1996) Heavy-metal-responsive genes in maize: identification and comparison of their expression upon various forms of abiotic stress. Planta 199:1-8
22. Docquier S, Tillemans V, Deltour R, Motte P (2004) Nuclear bodies and compartmentalization of pre-mRNA splicing factors in higher plants. Chromosoma 112:255-266
23. Domon C, Lorković ZJ, Juan Valcárcel J, Filipowicz W (1998) Multiple forms of the U2 small nuclear ribonucleoprotein auxiliary factor U2AF subunits expressed in higher plants. J Biol Chem 273:34601-34610
24. Dreyfuss G, Hentze M, Lamond AI (1996) From transcript to protein. Cell 85:963-972
25. Dreyfuss G, Kim VN, Kataoka N (2002) mRNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 3:195-205
26. Ellis C, Turner JG (2001) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell 13:1025-1033
27. Fang Y, Hearn S, Spector DL (2004) Tissue-specific expression and dynamic organization of SR splicing factors in Arabidopsis. Mol Biol Cell 15:2664-2673
28. Gómez J, Sánchez-Martínez D, Stiefel V, Rigau J, Puigdomènech P, Pagès M (1988) A gene induced by the plant hormone abscisic acid in response to water stress encodes a glycine-rich protein. Nature 334:262-264
29. Heintzen C, Nater M, Appel K, Staiger S (1997) AtGRP7, a nuclear RNA-binding protein as a component of a circadian-regulated negative feedback loop in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:8515-8520
30. Hirose T, Sugita M, Sugiura M (1993) cDNA structure, expression and nucleic acid-binding properties of three RNA-binding proteins in tobacco: occurrence of tissue-specific alternative splicing. Nucl Acids Res 21:3981-3987
31. Hollams MH, Giles KM, Thomson AM, Leedman PJ (2002) mRNA stability and the control of gene expression: implications for human disease. Neurochem Res 27:957-980
32. Jambunathan N, McNellis TW (2003) Regulation of Arabidopsis COPINE 1 gene expression in response to pathogens and abiotic stimuli. Plant Physiol 132:1370-1381
33. Jia Y, del Rio HS, Robbins AL, Louzada ES (2004) Cloning and sequence analysis of a low temperature-induced gene from trifoliate orange with unusual pre-mRNA processing. Plant Cell Rep 23:159-166
34. Kim CY, Koo YD, Jin JB, Moon BC, Kang CH, Kim ST, Park BO, Lee SY, Kim ML, Hwang I, Kang KY, Bahk JD, Lee SY, Cho MJ (2003) Rice C2-domain proteins are induced and translocated to the plasma membrane in response to a fungal elicitor. Biochemistry 42:11625-11633
35. Kim YO, Kim JS, Kang H (2005) Cold-inducible zinc finger-containing glycine-rich RNA-binding protein contributes to the enhancement of freezing tolerance in Arabidopsis thaliana. Plant J 42:890-900
36. Krecic AM, Swanson MS (1999) hnRNP complexes: composition, structure, and function. Curr Opin Cell Biol 11:363-371
37. Kwak KJ, Kim YO, Kang H (2005) Characterization of transgenic Arabidopsis plants overexpressing GR-RBP4 under high salinity, dehydration, or cold stress. J Exp Bot 56:3007-3016
38. Lambermon MHL, Simpson GG, Kirk DA, Hemmings-Mieszcak M, Klahre U, Filipowicz W (2000) UBP1, a novel hnRNP-like protein that functions at multiple steps of higher plant nuclear pre-mRNA maturation. EMBO J 19:1638-1649
39. Lambermon MHL, Fu Y, Wieczorek Kirk DA, Dupasquier M, Filipowicz W, Lorković ZJ (2002) UBA1 and UBA2, two proteins that interact with UBP1, a multifunctional effector of pre-mRNA maturation in plants. Mol Cell Biol 22:4346-4357
40. Lamond AI, Spector DL (2003) Nuclear speckles: a model for nuclear organelles. Nat Rev Mol Cell Biol 4:605-612
41. LeBrasseur ND, MacIntosh GC, Pérez-Amador MA, Sitoh M, Green PJ (2002) Local and systemic wound-induction of RNase and nuclease activities in Arabidopsis: RNS1 as a marker for a JA-independent systemic signaling pathway. Plant J 29:393-403
42. Lee D, Polisensky DH, Braam J (2005) Genome-wide identification of touch- and darkness-regulated Arabidopsis genes: a focus on calmodulin-like and XTH genes. New Phytol 165:429-444
43. 2+/calmodulin in Arabidopsis thaliana. Mol Gen Genet 258:412-419
44. León J, Rojo E, Sánchez-Serrano JJ (2001) Wound signalling in plants. J Exp Bot 52:1-9
45. Li J, Wang XQ, Watson MB, Assmann SM (2000) Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science 287:300-303
46. Li J, Kinoshita T, Pandey S, Ng CK-Y, Gygi SP, Shimazaki K, Assmann SM (2002) Modulation of an RNA-binding protein by abscisic-acid-activated protein kinase. Nature 418:793-797
47. Lim M-H, Kim J, Kim Y-S, Chung K-S, Seo Y-H, Lee I, Kim J, Hong CB, Kim H-J, Park C-M (2004) A new Arabidopsis gene, FLK, encodes an RNA binding protein with K homology motifs and regulates flowering time via FLOWERING LOCUS C. Plant Cell 16:731-740
48. Lopato S, Forstner C, Kalyna M, Hilscher J, Langhammer U, Indrapichate K, Lorković ZJ, Barta A (2002) Network of interactions of a novel plant-specific Arg/Ser-rich protein, atRSZ33, with atSC35-like splicing factors. J Biol Chem 277:39989-39998
49. Lorković ZJ, Barta A (2002) Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucl Acids Res 30:623-635
50. Ludevid MD, Freire MA, Gómez J, Burd CG, Albericio F, Giralt E, Dreyfuss G, Pagès M (1992) RNA binding characteristics of a 16kDA glycine-rich protein from maize. Plant J 2:999-1003
51. Macknight R, Bancroft I, Page T, Lister C, Schmidt R, Love L, Westphal L, Murphy G, Sherson S, Cobbett C, Dean C (1997) FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89:737-745
52. Macknight R, Duroux M, Laurie R, Dijkwel P, Simpson G, Dean C (2002) Functional significance of the alternative transcript processing of the Arabidopsis floral promoter FCA. Plant Cell 14:877-888
53. Mili S, Shu HJ, Zhao Y, Pinol-Roma S (2001) Distinct RNP complexes of shuttling hnRNP proteins with pre-mRNA and mRNA: candidate intermediates in formation and export of mRNA. Mol Cell Biol 21:7307-7319
54. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473-497
55. Ner-Gaon H, Halachmi R, Svaldi-Goldstein S, Rubin E, Ophir R, Fluhr R (2004) Intron retention is a major phenomenon in alternative splicing in Arabidopsis. Plant J 39:877-885
56. Ng CK-Y, Kinoshita T, Pandey S, Shimazaki K, Assmann SM (2004) Abscisic acid induces rapid subnuclear reorganization in guard cells. Plant Physiol 134:1327-1331
57. Nomata T, Kabeya Y, Sato N (2004) Cloning and characterization of glycine-rich RNA-binding protein cDNAs in the moss Physcomitrella patens. Plant Cell Physiol 45:48-56
58. O'Donnell PJ, Calvert C, Atzorn R, Wasternack C, Leyser HMO, Bowles DJ (1996) Ethylene as a signal mediating the wound response of tomato plants. Science 274:1914-1917
59. 1) affects transcript stability and protein accumulation in transgenic alfalfa. Plant J 45:832-846
60. Pena-Cortes H, Fisahn J, Willmitzer L (1995) Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. Proc Natl Acad Sci USA 92:4106-4113
61. Quesada V, Macknight R, Dean C, Simpson GG (2003) Autoregulation of the site of 3 end formation in FCA pre-mRNA prevents precocious flowering. EMBO J 22:3142-3152
62. Razem FA, El-Kereamy A, Abrams SR, Hill RD (2006) The RNA-binding protein FCA is an abscisic acid receptor. Nature 439:290-294
63. Reddy ASN (2007) Alternative splicing of pre-messenger RNAs in plants in the genomic era. Annu Rev Plant Biol 58:267-294
64. Reed R, Magni K (2001) A new view of mRNA export: separating the wheat from the chaff. Nat Cell Biol 3:E201-E204
65. Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707-719
66. Riera M, Redko Y, Leung J (2006) Arabidopsis RNA-binding protein UBA2a relocalizes into nuclear speckles in response to abscisic acid. FEBS Lett 580:4160-4165
67. Rojo E, Titarenko E, Leon J, Berger S, Vancanneyt G, Sanchez-Serrano JJ (1998) Reversible protein phosphorylation regulates jasmonic acid-dependent and -independent wound signal transduction pathways in Arabidopsis thaliana. Plant J 13:153-165
68. Rojo E, León J, Sánchez-Serrano JJ (1999) Cross-talk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant J 20:135-142
69. Sachetto-Martins G, Franco LO, de Oliveira DE (2000) Plant glycine-rich proteins: a family or just proteins with a common motif? Biochim Biophys Acta 1492:1-14
70. Schomburg FM, Patton DA, Meinke DW, Amasino RM (2001) FPA, a gene involved in floral induction in Arabidopsis, encodes a protein containing RNA-recognition motifs. Plant Cell 13:1427-1436
71. Schöning JC, Streitner C, Page DR, Hennig S, Uchida K, Wolf E, Furuya M, Staiger D (2007) Auto-regulation of the circadian slave oscillator component AtGRP7 and regulation of its targets is impaired by a single RNA recognition motif point mutation. Plant J 52:1119-1130
72. Shopland LS, Johnson CV, Lawrence JB (2002) Evidence that all SC-35 domains contain mRNAs and that transcripts can be structurally constrained within these domains. J Struct Biol 140:131-139
73. Shopland LS, Johnson CV, Byron M, McNeil J, Lawrence JB (2003) Clustering of multiple specific genes and gene-rich R-bands around SC-35 domains: evidence for local euchromatic neighborhoods. J Cell Biol 162:981-990
74. Simpson GG (2004) The autonomous pathway: epigenetic and post-transcriptional gene regulation in the control of Arabidopsis flowering time. Curr Opin Plant Biol 7:570-574
75. Spiro MD, Kates KA, Koller AL, O'Neill MA, Albersheim P, Darvill A (1993) Purification and characterization of biologically active 1,4-linked α-D-oligogalacturonides after partial digestion of polygalacturonic acid with endopolygalacturonase. Carbohydr Res 247:9-20
76. Staiger D, Zecca L, Wieczorek Kirk DA, Appel K, Eckstein L (2003) The circadian clock regulated RNA-binding protein AtGRP7 autoregulates its expression by influencing alternative splicing of its own pre-mRNA. Plant J 33:361-371
77. Sturm A (1992) A wound-inducible glycine-rich protein from Daucus carota with homology to single-stranded nucleic acid-binding proteins. Plant Physiol 99:1689-1692
78. Thiele A, Nagamine Y, Hauschildt S, Clevers H (2006) AU-rich elements and alternative splicing in the beta-catenin 3′UTR can influence the human beta-catenin mRNA stability. Exp Cell Res 312:2367-2378
79. Tillemans V, Dispa L, Remacle C, Collinge M, Motte P (2005) Functional distribution and dynamics of Arabidopsis SR splicing factors in living plant cells. Plant J 41:567-582
80. Titarenko E, Rojo E, León J, Sánchez-Serrano JJ (1997) Jasmonic acid-dependent and independent signaling pathways control wound-induced gene activation in Arabidopsis thaliana. Plant Physiol 115:817-826
81. Vian A, Henry-Vian C, Davies E (1999) Rapid and systemic accumulation of chloroplast mRNA-binding protein transcripts after flame stimulus in tomato. Plant Physiol 121:517-524
82. Wachter A, Tunc-Ozdemir M, Grove BC, Green PJ, Shintani DK, Breaker RR (2007) Riboswitch control of gene expression in plants by splicing and alternative 3′ end processing of mRNAs. Plant Cell 19:3437-3450
83. Wang B-B, Brendel V (2004) The ASRG database: identification and survey of Arabidopsis thaliana genes involved in pre-mRNA splicing. Genome Biol 5:R102
84. Zhu W, Schlueter SD, Brendel V (2003) Refined annotation of the Arabidopsis genome by complete expressed sequence tag mapping. Plant Physiol 132:469-484