Transportin-SR Is Required for Proper Splicing of Genes and Plant Immunity
Transportin-SR (TRN-SR) is a member of the importin-β super-family that functions as the nuclear import receptor for serine-arginine rich (SR) proteins, which play diverse roles in RNA metabolism. Here we report the identification and cloning of mos14 (modifier of snc1-1, 14), a mutation that suppresses the immune responses conditioned by the auto-activated Resistance (R) protein snc1 (suppressor of npr1-1, constitutive 1). MOS14 encodes a nuclear protein with high similarity to previously characterized TRN-SR proteins in animals. Yeast two-hybrid assays showed that MOS14 interacts with AtRAN1 via its N-terminus and SR proteins via its C-terminus. In mos14-1, localization of several SR proteins to the nucleus was impaired, confirming that MOS14 functions as a TRN-SR. The mos14-1 mutation results in altered splicing patterns of SNC1 and another R gene RPS4 and compromised resistance mediated by snc1 and RPS4, suggesting that nuclear import of SR proteins by MOS14 is required for proper splicing of these two R genes and is important for their functions in plant immunity.
Vyšlo v časopise:
Transportin-SR Is Required for Proper Splicing of Genes and Plant Immunity. PLoS Genet 7(6): e32767. doi:10.1371/journal.pgen.1002159
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002159
Souhrn
Transportin-SR (TRN-SR) is a member of the importin-β super-family that functions as the nuclear import receptor for serine-arginine rich (SR) proteins, which play diverse roles in RNA metabolism. Here we report the identification and cloning of mos14 (modifier of snc1-1, 14), a mutation that suppresses the immune responses conditioned by the auto-activated Resistance (R) protein snc1 (suppressor of npr1-1, constitutive 1). MOS14 encodes a nuclear protein with high similarity to previously characterized TRN-SR proteins in animals. Yeast two-hybrid assays showed that MOS14 interacts with AtRAN1 via its N-terminus and SR proteins via its C-terminus. In mos14-1, localization of several SR proteins to the nucleus was impaired, confirming that MOS14 functions as a TRN-SR. The mos14-1 mutation results in altered splicing patterns of SNC1 and another R gene RPS4 and compromised resistance mediated by snc1 and RPS4, suggesting that nuclear import of SR proteins by MOS14 is required for proper splicing of these two R genes and is important for their functions in plant immunity.
Zdroje
1. MerkleT 2003 Nucleo-cytoplasmic partitioning of proteins in plants: implications for the regulation of environmental and developmental signalling. Curr Genet 44 231 260
2. ZhangYLiX 2005 A putative nucleoporin 96 Is required for both basal defense and constitutive resistance responses mediated by suppressor of npr1-1,constitutive 1. Plant Cell 17 1306 1316
3. PalmaKZhangYLiX 2005 An importin alpha homolog, MOS6, plays an important role in plant innate immunity. Curr Biol 15 1129 1135
4. ChengYTGermainHWiermerMBiDXuF 2009 Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis. Plant Cell 21 2503 2516
5. GermainHQuNChengYTLeeEHuangY 2010 MOS11: a new component in the mRNA export pathway. PLoS Genet 6 e1001250 doi:10.1371/journal.pgen.1001250
6. ZhangYGoritschnigSDongXLiX 2003 A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell 15 2636 2646
7. GorlichDDabrowskiMBischoffFRKutayUBorkP 1997 A novel class of RanGTP binding proteins. J Cell Biol 138 65 80
8. HarelAForbesDJ 2004 Importin beta: conducting a much larger cellular symphony. Mol Cell 16 319 330
9. StromACWeisK 2001 Importin-beta-like nuclear transport receptors. Genome Biol 2 REVIEWS3008
10. KataokaNBachorikJLDreyfussG 1999 Transportin-SR, a nuclear import receptor for SR proteins. J Cell Biol 145 1145 1152
11. LaiMCLinRIHuangSYTsaiCWTarnWY 2000 A human importin-beta family protein, transportin-SR2, interacts with the phosphorylated RS domain of SR proteins. J Biol Chem 275 7950 7957
12. BartaAKalynaMLorkovicZJ 2008 Plant SR proteins and their functions. Curr Top Microbiol Immunol 326 83 102
13. ReddyAS 2004 Plant serine/arginine-rich proteins and their role in pre-mRNA splicing. Trends Plant Sci 9 541 547
14. LongJCCaceresJF 2009 The SR protein family of splicing factors: master regulators of gene expression. Biochem J 417 15 27
15. LopatoSWaigmannEBartaA 1996 Characterization of a novel arginine/serine-rich splicing factor in Arabidopsis. Plant Cell 8 2255 2264
16. LopatoSGattoniRFabiniGSteveninJBartaA 1999 A novel family of plant splicing factors with a Zn knuckle motif: examination of RNA binding and splicing activities. Plant Mol Biol 39 761 773
17. LazarGSchaalTManiatisTGoodmanHM 1995 Identification of a plant serine-arginine-rich protein similar to the mammalian splicing factor SF2/ASF. Proc Natl Acad Sci U S A 92 7672 7676
18. LopatoSKalynaMDornerSKobayashiRKrainerAR 1999 atSRp30, one of two SF2/ASF-like proteins from Arabidopsis thaliana, regulates splicing of specific plant genes. Genes Dev 13 987 1001
19. WhithamSDinesh-KumarSPChoiDHehlRCorrC 1994 The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78 1101 1115
20. HaltermanDZhouFWeiFWiseRPSchulze-LefertP 2001 The MLA6 coiled-coil, NBS-LRR protein confers AvrMla6-dependent resistance specificity to Blumeria graminis f. sp. hordei in barley and wheat. Plant J 25 335 348
21. YiHRichardsEJ 2007 A cluster of disease resistance genes in Arabidopsis is coordinately regulated by transcriptional activation and RNA silencing. Plant Cell 19 2929 2939
22. GassmannWHinschMEStaskawiczBJ 1999 The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. Plant J 20 265 277
23. ZhangXCGassmannW 2003 RPS4-mediated disease resistance requires the combined presence of RPS4 transcripts with full-length and truncated open reading frames. Plant Cell 15 2333 2342
24. ZhangXCGassmannW 2007 Alternative splicing and mRNA levels of the disease resistance gene RPS4 are induced during defense responses. Plant Physiol 145 1577 1587
25. ZhuZXuFZhangYChengYTWiermerM 2010 Arabidopsis resistance protein SNC1 activates immune responses through association with a transcriptional corepressor. Proc Natl Acad Sci U S A 107 13960 13965
26. ZhangYXuSDingPWangDChengYT 2010 Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc Natl Acad Sci U S A
27. LorkovicZJHilscherJBartaA 2004 Use of fluorescent protein tags to study nuclear organization of the spliceosomal machinery in transiently transformed living plant cells. Mol Biol Cell 15 3233 3243
28. GolovkinMReddyAS 1996 Structure and expression of a plant U1 snRNP 70K gene: alternative splicing of U1 snRNP 70K pre-mRNAs produces two different transcripts. Plant Cell 8 1421 1435
29. Savaldi-GoldsteinSAvivDDavydovOFluhrR 2003 Alternative splicing modulation by a LAMMER kinase impinges on developmental and transcriptome expression. Plant Cell 15 926 938
30. AllemandEDokudovskayaSBordonneRTaziJ 2002 A conserved Drosophila transportin-serine/arginine-rich (SR) protein permits nuclear import of Drosophila SR protein splicing factors and their antagonist repressor splicing factor 1. Mol Biol Cell 13 2436 2447
31. BartaAKalynaMReddyAS 2010 Implementing a rational and consistent nomenclature for serine/arginine-rich protein splicing factors (SR proteins) in plants. Plant Cell 22 2926 2929
32. LongmanDJohnstoneILCaceresJF 2000 Functional characterization of SR and SR-related genes in Caenorhabditis elegans. Embo J 19 1625 1637
33. Dinesh-KumarSPBakerBJ 2000 Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. Proc Natl Acad Sci U S A 97 1908 1913
34. LiYTessaroMJLiXZhangY 2010 Regulation of the expression of plant Resistance gene SNC1 by a protein with a conserved BAT2 domain. Plant Physiol 153 1425 1434
35. PalusaSGAliGSReddyAS 2007 Alternative splicing of pre-mRNAs of Arabidopsis serine/arginine-rich proteins: regulation by hormones and stresses. Plant J 49 1091 1107
36. BiDChengYTLiXZhangY 2010 Activation of plant immune responses by a gain-of-function mutation in an atypical receptor-like kinase. Plant Physiol 153 1771 1779
37. LiXZhangYClarkeJDLiYDongX 1999 Identification and cloning of a negative regulator of systemic acquired resistance, SNI1, through a screen for suppressors of npr1-1. Cell 98 329 339
38. YooSDChoYHSheenJ 2007 Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Pronto 2 1565 1572
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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