Skip to main content
Log in

RRM domain of Arabidopsis splicing factor SF1 is important for pre-mRNA splicing of a specific set of genes

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

The RNA recognition motif of Arabidopsis splicing factor SF1 affects the alternative splicing of FLOWERING LOCUS M pre-mRNA and a heat shock transcription factor HsfA2 pre-mRNA.

Abstract

Splicing factor 1 (SF1) plays a crucial role in 3′ splice site recognition by binding directly to the intron branch point. Although plant SF1 proteins possess an RNA recognition motif (RRM) domain that is absent in its fungal and metazoan counterparts, the role of the RRM domain in SF1 function has not been characterized. Here, we show that the RRM domain differentially affects the full function of the Arabidopsis thaliana AtSF1 protein under different experimental conditions. For example, the deletion of RRM domain influences AtSF1-mediated control of flowering time, but not the abscisic acid sensitivity response during seed germination. The alternative splicing of FLOWERING LOCUS M (FLM) pre-mRNA is involved in flowering time control. We found that the RRM domain of AtSF1 protein alters the production of alternatively spliced FLM-β transcripts. We also found that the RRM domain affects the alternative splicing of a heat shock transcription factor HsfA2 pre-mRNA, thereby mediating the heat stress response. Taken together, our results suggest the importance of RRM domain for AtSF1-mediated alternative splicing of a subset of genes involved in the regulation of flowering and adaptation to heat stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

AP1:

APETALA1

BBP:

Branchpoint binding protein

CCA1:

CIRCADIAN CLOCK ASSOCIATED1

LHY:

LATE ELONGATED HYPOCOTYL

LFY:

LEAFY

FLM:

FLOWERING LOCUS M

FT:

FLOWERING LOCUS T

Pre-mRNAs:

PRECURSOR MESSENGER RNAS

RRM:

RNA recognition motif

SF1:

Splicing factor 1

SOC1:

SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1

SS:

Splice site

SVP:

SHORT VEGETATIVE PHASE

TOC1:

TIMING OF CAB EXPRESSION1

References

  • Abovich N, Rosbash M (1997) Cross-intron bridging interactions in the yeast commitment complex are conserved in mammals. Cell 89:403–412

    Article  CAS  PubMed  Google Scholar 

  • Adam SA, Nakagawa T, Swanson MS, Woodruff TK, Dreyfuss G (1986) mRNA polyadenylate-binding protein: gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence. Mol Cell Biol 6:2932–2943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alba MM, Pages M (1998) Plant proteins containing the RNA-recognition motif. Trends Plant Sci 3:15–21

    Article  Google Scholar 

  • Ali GS, Palusa SG, Golovkin M, Prasad J, Manley JL, Reddy AS (2007) Regulation of plant developmental processes by a novel splicing factor. PLoS One 2:e471

    Article  PubMed  PubMed Central  Google Scholar 

  • Arning S, Gruter P, Bilbe G, Kramer A (1996) Mammalian splicing factor SF1 is encoded by variant cDNAs and binds to RNA. RNA 2:794–810

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bentley RC, Keene JD (1991) Recognition of U1 and U2 small nuclear RNAs can be altered by a 5-amino-acid segment in the U2 small nuclear ribonucleoprotein particle (snRNP) B″ protein and through interactions with U2 snRNP-A′ protein. Mol Cell Biol 11:1829–1839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berglund JA, Chua K, Abovich N, Reed R, Rosbash M (1997) The splicing factor BBP interacts specifically with the pre-mRNA branchpoint sequence UACUAAC. Cell 89:781–787

    Article  CAS  PubMed  Google Scholar 

  • Berglund JA, Fleming ML, Rosbash M (1998) The KH domain of the branchpoint sequence binding protein determines specificity for the pre-mRNA branchpoint sequence. RNA 4:998–1006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Birney E, Kumar S, Krainer AR (1993) Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res 21(25):5803–5816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burd CG, Dreyfuss G (1994) Conserved structures and diversity of functions of RNA-binding proteins. Science 265:615–621

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Manley JL (2009) Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat Rev Mol Cell Biol 10(11):741–754

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen R, Silver DL, de Bruijin FJ (1998) Nodule parenchyma-specific expression of the Sesbania rostrata early nodulin gene SrEnod2 is mediated by its 3′ untranslated region. Plant Cell 10:1585–1602

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park SY et al (2009) In vitro reconstitution of an abscisic acid signalling pathway. Nature 462(3):660–664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garrey SM, Voelker R, Berglund JA (2006) An extended RNA binding site for the yeast branch point-binding protein and the role of its zinc knuckle domains in RNA binding. J Biol Chem 281:27443–27453

    Article  CAS  PubMed  Google Scholar 

  • Glisovic T, Bachorik JL, Yong J, Dreyfuss G (2008) RNA-binding proteins and posttranscriptional gene regulation. FEBS Lett 582:1977–1986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez N, Inzé D (2015) Molecular systems governing leaf growth: from genes to networks. J Exp Bot 66(4):1045–1054

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez N, Vanhaeren H, Inzé D (2012) Leaf size control: complex coordination of cell division and expansion. Trends Plant Sci 17:332–340

    Article  CAS  PubMed  Google Scholar 

  • Hong S, Song HR, Lutz K, Kerstetter RA, Michael TP, McClung CR (2010) Type II protein arginine methyltransferase 5 (PRMT5) is required for circadian period determination in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:21211–21216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacewicz A, Chico L, Smith P, Schwer B, Shuman S (2015) Structural basis for recognition of intron branchpoint RNA by yeast Msl5 and selective effects of interfacial mutations on splicing of yeast pre-mRNAs. RNA 21:401–414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jang YH, Park HY, Lee KC, May PT, Kim SK, Suh MC et al (2014) A homolog of splicing factor SF1 is essential for development and is involved in the alternative splicing of pre-mRNA in Arabidopsis thaliana. Plant J 78:591–603

    Article  CAS  PubMed  Google Scholar 

  • Jones MA, Williams BA, McNicol J, Simpson CG, Brown JW, Harmer SL (2012) Mutation of Arabidopsis spliceosomal timekeeper locus1 causes circadian clock defects. Plant Cell 24:4066–4082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jurica MS, Moore MJ (2003) Pre-mRNA splicing: awash in a sea of proteins. Mol Cell 12:5–14

    Article  CAS  PubMed  Google Scholar 

  • Kim SK, Yun CH, Lee JH, Jang YH, Park HY, Kim JK (2008) OsCO3, a CONSTANS-LIKE gene, controls flowering by negatively regulating the expression of FT-like genes under SD conditions in rice. Planta 228:355

    Article  CAS  PubMed  Google Scholar 

  • Lee JH, Yoo SJ, Park SH, Hwang I, Lee JS, Ahn JH (2007) Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev 21(4):397–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JH, Ryu HS, Chung KS, Pose D, Kim SK, Schmid M et al (2013) Regulation of temperature-responsive flowering by MADS-box transcription factor repressors. Science 342(6158):628–632

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Lee HJ, Jung JH, Park CM (2015) The Arabidopsis thaliana RNA-binding protein FCA regulates thermotolerance by modulating the detoxification of reactive oxygen species. New Phytol 205:555–569

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Luyten I, Bottomley M, Messias A, Houngninou-Molango S, Sprangers R et al (2001) Structural basis for recognition of the intron branch site by splicing factor 1. Science 294:1098–1102

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Sun N, Liu M, Liu J, Du B, Wang X et al (2013) An autoregulatory loop controlling Arabidopsis HsfA2 expression: role of heat shock-induced alternative splicing. Plant Physiol 162:512–521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loerch S, Kielkopf CL (2016) Unmasking the U2AF homology motif family: a bona fide protein-protein interaction motif in disguise. RNA 22:1795–1807

    Article  CAS  PubMed  Google Scholar 

  • Lorković ZJ (2009) Role of plant RNA-binding proteins in development, stress response and genome organization. Trends Plant Sci 14:229–236

    Article  PubMed  Google Scholar 

  • Lorkvić ZJ, Barta A (2002) Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA binding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Res 30(3):623–635

    Article  Google Scholar 

  • Lorković ZJ, Kirk DAW, Lambermon MHL, Filipowicz W (2000) Pre-mRNA splicing in higher plants. Trends Plant Sci 5:160–167

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maris C, Dominguez C, Allain FH (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 272(9):2118–2131

    Article  CAS  PubMed  Google Scholar 

  • Nilsson O, Lee I, Blazquez MA, Weigel D (1998) Flowering-time genes modulate the response to LEAFY activity. Genetics 150:403–410

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J 48:535–547

    Article  CAS  PubMed  Google Scholar 

  • Pose D, Verhage L, Ott F, Yant L, Mathieu J, Angenent GC et al (2013) Temperature-dependent regulation of flowering by antagonistic FLM variants. Nature 503:414–417

    Article  CAS  PubMed  Google Scholar 

  • Rain JC, Rafi Z, Rhani Z, Legrain P, Kramer A (1998) Conservation of functional domains involved in RNA binding and protein–protein interactions in human and Saccharomyces cerevisiae pre-mRNA splicing factor SF1. RNA 4:551–565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rutz B, Séraphin B (2000) A dual role for BBP/ScSF1 in nuclear pre-mRNA retention and splicing. EMBO J 19:1873–1886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sachs AB, Bond MW, Kornberg RD (1986) A single gene from yeast for both nuclear and cytoplasmic polyadenylate-binding proteins: domain structure and expression. Cell 45:827–835

    Article  CAS  PubMed  Google Scholar 

  • Schwartz SH, Silva J, Burstein D, Pupko T, Eyras E, Ast G (2008) Large-scale comparative analysis of splicing signals and their corresponding splicing factors in eukaryotes. Genome Res 18:88–103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Selenko P, Gregorovic G, Sprangers R, Stier G, Rhani Z, Kramer A et al (2003) Structural basis for the molecular recognition between human splicing factors U2AF65 and SF1/mBBP. Mol Cell 11:965–976

    Article  CAS  PubMed  Google Scholar 

  • Severing EI, Van Dijk ADJ, Morabito G, Busscher-Lange J, Immink RGH, Van Ham RCHJ (2012) Predicting the impact of alternative splicing on plant MADS domain protein function. PLoS One 7:e30524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shitashige M, Satow R, Honda K, Ono M, Hirohashi S, Yamada T (2007) Increased susceptibility of Sf1+/− mice to azoxymethane-induced colon tumorigenesis. Cancer Sci 98:1862–1867

    Article  CAS  PubMed  Google Scholar 

  • Sugio A, Dreos R, Aparicio F, Maule A (2009) The cytosolic protein response as a subcomponent of the wider heat shock response in Arabidopsis. Plant Cell 21:642–654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sureshkumar S, Dent C, Seleznev A, Tasset C, Balasubramanian S (2016) Nonsense-mediated mRNA decay modulates FLM-dependent thermosensory flowering response in Arabidopsis. Nat Plants 29:16055

    Article  Google Scholar 

  • Tanackovic G, Krämer A (2005) Human splicing factor SF3a, but not SF1, is essential for pre-mRNA splicing in vivo. Mol Biol Cell 16:1366–1377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tao S, Arnaud G, Ludovic G, Kamel H, Alice B, Maureen RH et al (2013) An RNA recognition motif-containing protein is required for plastid RNA editing in Arabidopsis and maize. Proc Natl Acad Sci USA 110(12):E1169–E1178

    Article  Google Scholar 

  • Thickman KR, Swenson MC, Kabogo JM, Gryczynski Z, Kielkopf CL (2006) Multiple U2AF65 binding sites within SF3b155: thermodynamic and spectroscopic characterization of protein–protein interactions among pre-mRNA splicing factors. J Mol Biol 356:664–683

    Article  CAS  PubMed  Google Scholar 

  • Vanhaeren H, Gonzalez N, Coppens F, De Milde L, Van Daele T, Vermeersch M et al (2014) Combining growth-promoting genes leads to positive epistasis in Arabidopsis thaliana. eLife 3:e02252

    Article  PubMed  PubMed Central  Google Scholar 

  • Von Koskull-Döring, Scharf KD, Lutz Nover (2007) The diversity of plant heat stress transcription factors. Trends Plant Sci 12(10):1360–1385

    Article  Google Scholar 

  • Wang BB, Brendel V (2006) Genome wide comparative analysis of alternative splicing in plants. Proc Natl Acad Sci USA 103:7175–7180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Li J (2008) Molecular basis of plant architecture. Annu Rev Plant Biol 59:253–279

    Article  CAS  PubMed  Google Scholar 

  • Wang ZY, Nakano T, Gendron J, He J, Chen M, Vafeados D et al (2002) Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev Cell 2:505–513

    Article  CAS  PubMed  Google Scholar 

  • Webb CJ, Lakhe-Reddy S, Romfo CM, Wise JA (2005) Analysis of mutant phenotypes and splicing defects demonstrates functional collaboration between the large and small subunits of the essential splicing factor U2AF in vivo. Mol Biol Cell 16(2):584–596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weigel D, Glazebrook J (2006) In planta transformation of Arabidopsis. Cold Spring Harb Protoc. doi:10.1101/pdb.prot4668

    Google Scholar 

  • Will CL, Luhrmann R (2011) Spliceosome structure and function. Cold Spring Harbor Perspect Biol 3:a003707

    Article  CAS  Google Scholar 

  • Yoshida H, Park SY, Akiyoshi T, Sato M, Shirouzu M, Tsuda K, Kuwasako K, Unzai S, Muto Y, Urano T, Obayashi E (2015) A novel 3'splice site recognition by the two zinc fingers in the U2AF small subunit. Genes Dev 29(15):1649–1660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Zhang S, Zhang Y, Wang X, Li D, Li Q et al (2011) Arabidopsis floral initiator SKB1 confers high salt tolerance by regulating transcription and pre-mRNA splicing through altering histone H4R3 and small nuclear ribonucleoprotein LSM4 methylation. Plant Cell 23:396–411

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Peng P, Schmitz RJ, Decker AD, Tax FE, Li J (2002) Two putative BIN2 substrates are nuclear components of brassinosteroid signaling. Plant Physiol 130:1221–1229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Education (2014R1A1A2055796 to J.-K. Kim) and a Korea University Grant (to J.-K. Kim).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jeong Hwan Lee or Jeong-Kook Kim.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Additional information

Communicated by Jeong Sheop Shin.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 28073 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, K.C., Jang, Y.H., Kim, SK. et al. RRM domain of Arabidopsis splicing factor SF1 is important for pre-mRNA splicing of a specific set of genes. Plant Cell Rep 36, 1083–1095 (2017). https://doi.org/10.1007/s00299-017-2140-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-017-2140-1

Keywords

Navigation