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Plant serine/arginine-rich proteins: versatile players in RNA processing

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Abstract

Main conclusion

Serine/arginine-rich (SR) proteins participate in RNA processing by interacting with precursor mRNAs or other splicing factors to maintain plant growth and stress responses.

Abstract

Alternative splicing is an important mechanism involved in mRNA processing and regulation of gene expression at the posttranscriptional level, which is the main reason for the diversity of genes and proteins. The process of alternative splicing requires the participation of many specific splicing factors. The SR protein family is a splicing factor in eukaryotes. The vast majority of SR proteins’ existence is an essential survival factor. Through its RS domain and other unique domains, SR proteins can interact with specific sequences of precursor mRNA or other splicing factors and cooperate to complete the correct selection of splicing sites or promote the formation of spliceosomes. They play essential roles in the composition and alternative splicing of precursor mRNAs, providing pivotal functions to maintain growth and stress responses in animals and plants. Although SR proteins have been identified in plants for three decades, their evolutionary trajectory, molecular function, and regulatory network remain largely unknown compared to their animal counterparts. This article reviews the current understanding of this gene family in eukaryotes and proposes potential key research priorities for future functional studies.

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References

  • Albaqami M, Reddy ASN (2018) Development of an in vitro pre-mRNA splicing assay using plant nuclear extract. Plant Methods 14(1):1–12

    Article  PubMed  PubMed Central  Google Scholar 

  • Ali GS, Reddy AS (2006) ATP, phosphorylation and transcription regulate the mobility of plant splicing factors. J Cell Sci 119(Pt 17):3527–3538

    Article  CAS  PubMed  Google Scholar 

  • Anko M (2014) Regulation of gene expression programmes by serine–arginine rich splicing factors. Semin Cell Dev Biol 32:11–21

    Article  CAS  PubMed  Google Scholar 

  • Anko M, Mullermcnicoll M, Brandl H, Curk T, Gorup C, Henry I, Ule J, Neugebauer KM (2012) The RNA-binding landscapes of two SR proteins reveal unique functions and binding to diverse RNA classes. Genome Biol 13(3):1–17

    Article  Google Scholar 

  • Aravind L, Watanabe H, Lipman DJ, Koonin EV (2000) Lineage-specific loss and divergence of functionally linked genes in eukaryotes. Proc Natl Acad Sci USA 97(21):11319–11324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aznarez I, Nomakuchi TT, Tetenbaumnovatt J, Rahman MA, Fregoso O, Rees H, Krainer AR (2018) Mechanism of nonsense-mediated mRNA decay stimulation by splicing factor SRSF1. Cell Rep 23(7):2186–2198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barta A, Kalyna M, Lorković ZJ (2008) Plant SR proteins and their functions. Curr Top Microbiol Immunol 326:83–102

    CAS  PubMed  Google Scholar 

  • Barta A, Kalyna M, Reddy AS (2010a) Implementing a rational and consistent nomenclature for serine/arginine-rich protein splicing factors (SR proteins) in plants. Plant Cell 22(9):2926–2929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bedard KM, Daijogo S, Semler BL (2007) A nucleo-cytoplasmic SR protein functions in viral IRES-mediated translation initiation. EMBO J 26(2):459–467

    Article  CAS  PubMed  Google Scholar 

  • Blencowe BJ (2017) The relationship between alternative splicing and proteomic complexity. Trends Biochem Sci 42(6):407–408

    Article  CAS  PubMed  Google Scholar 

  • Botti V, Mcnicoll F, Steiner MC, Richter FM, Solovyeva A, Wegener M, Schwich OD, Poser I, Zarnack K, Wittig I, Neugebauer KM, Müller-Mcnicoll M (2017) Cellular differentiation state modulates the mRNA export activity of SR proteins. J Cell Biol 216(7):1993–2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brugiolo M, Botti V, Liu N, Mullermcnicoll M, Neugebauer KM (2017) Fractionation iCLIP detects persistent SR protein binding to conserved, retained introns in chromatin, nucleoplasm and cytoplasm. Nucleic Acids Res 45(18):10452–10465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Busch A, Hertel KJ (2012) Evolution of SR protein and hnRNP splicing regulatory factors. Wiley Interdiscip Rev Rna 3(1):1–12

    Article  CAS  PubMed  Google Scholar 

  • Butt H, Bazin J, Prasad K, Awad N, Crespi M, Reddy ASN, Mahfouz MM (2022) The rice serine/arginine splicing factor RS33 regulates pre-mrna splicing during abiotic stress responses. Cells 11(11):1796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caceres JF, Misteli T, Screaton GR, Spector DL, Krainer AR (1997) Role of the modular domains of SR proteins in subnuclear localization and alternative splicing specificity. J Cell Biol 138(2):225–238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Califice S, Baurain D, Hanikenne M, Motte P (2012a) A single ancient origin for prototypical serine/arginine-rich splicing factors. Plant Physiol 158(2):546–560

    Article  CAS  PubMed  Google Scholar 

  • Chen T, Cui P, Xiong L (2015) The RNA-binding protein HOS5 and serine/arginine-rich proteins RS40 and RS41 participate in miRNA biogenesis in arabidopsis. Nucleic Acids Res 43(17):8283–8298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Q, Han Y, Liu H, Wang X, Sun J, Zhao B, Li W, Tian J, Liang Y, Yan J, Yang X, Tian F (2018) Genome-wide association analyses reveal the importance of alternative splicing in diversifying gene function and regulating phenotypic variation in maize. Plant Cell 30(7):1404–1423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen MX, Wijethunge B, Zhou SM, Yang JF, Dai L, Wang SS, Chen C, Fu LJ, Zhang J, Hao GF, Yang GF (2019a) Chemical modulation of alternative splicing for molecular-target identification by potential genetic control in agrochemical research. J Agric Food Chem 67(18):5072–5084

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Li J, Liu Y, Li H (2019b) Genome-wide analysis of serine/arginine-rich protein family in wheat and brachypodium distachyon. Plants (basel) 8(7):188

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen MX, Zhang KL, Zhang M, Das D, Fang YM, Dai L, Zhang J, Zhu FY (2020) Alternative splicing and its regulatory role in woody plants. Tree Physiol 40(11):1475–1486

    Article  CAS  PubMed  Google Scholar 

  • Chen MX, Mei LC, Wang F, Boyagane Dewayalage IKW, Yang JF, Dai L, Yang GF, Gao B, Cheng CL, Liu YG, Zhang J, Hao GF (2021) PlantSPEAD: a web resource towards comparatively analysing stress-responsive expression of splicing-related proteins in plant. Plant Biotechnol J 19(2):227–229

    Article  CAS  PubMed  Google Scholar 

  • Cho S, Hoang A, Sinha R, Zhong X, Fu X, Krainer AR, Ghosh G (2011) Interaction between the RNA binding domains of Ser-Arg splicing factor 1 and U1–70K snRNP protein determines early spliceosome assembly. Proc Natl Acad Sci USA 108(20):8233–8238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi N, Liu Y, Oh J, Ha J, Ghigna C, Zheng X, Shen H (2021) Relative strength of 5’ splice-site strength defines functions of SRSF2 and SRSF6 in alternative splicing of Bcl-x pre-mRNA. BMB Rep 54(3):176–181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dreyfuss G, Swanson MS, Piñol-Roma S (1988) Heterogeneous nuclear ribonucleoprotein particles and the pathway of mRNA formation. Trends Biochem Sci 13(3):86–91

    Article  CAS  PubMed  Google Scholar 

  • Duque P (2011) A role for SR proteins in plant stress responses. Plant Signal Behav 6(1):49–54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fededa JP, Kornblihtt AR (2008) A splicing regulator promotes transcriptional elongation. Nat Struct Mol Biol 15(8):779–781

    Article  CAS  PubMed  Google Scholar 

  • Feilner T, Hultschig C, Lee J, Meyer S, Immink RGH, Koenig A, Possling A, Seitz H, Beveridge A, Scheel D (2005) High throughput identification of potential arabidopsis mitogen-activated protein kinases substrates. Mol Cell Proteomics 4(10):1558–1568

    Article  CAS  PubMed  Google Scholar 

  • Forment J, Naranjo MA, Roldán M, Serrano R, Vicente O (2002) Expression of arabidopsis SR-like splicing proteins confers salt tolerance to yeast and transgenic plants. Plant J 30(5):511–519

    Article  CAS  PubMed  Google Scholar 

  • Fu X, Maniatis T (1990) Factor required for mammalian spliceosome assembly is localized to discrete regions in the nucleus. Nature 343(6257):437–441

    Article  CAS  PubMed  Google Scholar 

  • Giannakouros T, Nikolakaki E, Mylonis I, Georgatsou E (2011) Serine-arginine protein kinases: a small protein kinase family with a large cellular presence. FEBS J 278(4):570–586

    Article  CAS  PubMed  Google Scholar 

  • Golovkin M, Reddy AS (1999) An SC35-like protein and a novel serine/arginine-rich protein interact with arabidopsis U1–70K protein. J Biol Chem 274(51):36428–36438

    Article  CAS  PubMed  Google Scholar 

  • Graveley BR, Hertel KJ, Maniatis T (2001) The role of U2AF35 and U2AF65 in enhancer-dependent splicing. RNA 7(6):806–818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grosse S, Lu YY, Coban I, Neumann B, Krebber H (2021) Nuclear SR-protein mediated mRNA quality control is continued in cytoplasmic nonsense-mediated decay. RNA Biol 18(10):1390–1407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu J, Ma S, Zhang Y, Wang D, Cao S, Wang ZY (2020) Genome-wide identification of cassava serine/arginine-rich proteins: insights into alternative splicing of pre-mrnas and response to abiotic stress. Plant Cell Physiol 61(1):178–191

    Article  CAS  PubMed  Google Scholar 

  • Hartmann L, Wiesner T, Wachter A (2018a) Subcellular compartmentation of alternatively spliced transcripts defines SERINE/ARGININE-RICH PROTEIN30 expression. Plant Physiol 176(4):2886–2903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartmann L, Wießner T, Wachter A (2018b) Subcellular compartmentation of alternatively spliced transcripts defines SERINE/ARGININE-RICH PROTEIN30 expression. Plant Physiol 176(4):2886–2903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hernandez H, Makarova OV, Makarov EM, Morgner N, Muto Y, Krummel DP, Robinson CV (2009) Isoforms of U1–70k control subunit dynamics in the human spliceosomal U1 snRNP. PLoS ONE 4(9):e7202

    Article  PubMed  PubMed Central  Google Scholar 

  • Holmes RK, Tuck AC, Zhu C, Dunn-Davies HR, Kudla G, Clauder-Munster S, Granneman S, Steinmetz LM, Guthrie C, Tollervey D (2015) Loss of the yeast SR protein Npl3 alters gene expression due to transcription readthrough. PLoS Genet 11(12):e1005735

    Article  PubMed  PubMed Central  Google Scholar 

  • Isshiki M, Tsumoto A, Shimamoto K (2006a) The serine/arginine-rich protein family in rice plays important roles in constitutive and alternative splicing of pre-mRNA. Plant Cell 18(1):146–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong S (2017) SR Proteins: binders, regulators, and connectors of RNA. Mol Cells 40(1):1–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ji X, Zhou Y, Pandit S, Huang J, Li H, Lin CY, Xiao R, Burge CB, Fu X (2013) SR proteins collaborate with 7SK and promoter-associated nascent RNA to release paused polymerase. Cell 153(4):855–868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jimenez M, Urtasun R, Elizalde M, Azkona M, Latasa MU, Uriarte I, Arechederra M, Alignani D, Barcenavarela M, Alvarezsola G (2019) Splicing events in the control of genome integrity: role of SLU7 and truncated SRSF3 proteins. Nucleic Acids Res 47(7):3450–3466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalyna M, Lopato S, Barta A (2003) Ectopic expression of atRSZ33 reveals its function in splicing and causes pleiotropic changes in development. Mol Biol Cell 14(9):3565–3577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kenan DJ, Query CC, Keene JD (1991) RNA recognition: towards identifying determinants of specificity. Trends Biochem Sci 16(6):214–220

    Article  CAS  PubMed  Google Scholar 

  • Kim K, Nguyen TD, Li S, Nguyen TA (2018) SRSF3 recruits DROSHA to the basal junction of primary microRNAs. RNA 24(7):892–898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krainer AR, Maniatis T (1985) Multiple factors including the small nuclear ribonucleoproteins U1 and U2 are necessary for Pre-mRNA splicing in vitro. Cell 42(3):725–736

    Article  CAS  PubMed  Google Scholar 

  • Laloum T, Martin G, Duque P (2017) Alternative splicing control of abiotic stress responses. Trends Plant Sci 23(2):140–150

    Article  PubMed  Google Scholar 

  • Lareau LF, Inada M, Green RE, Wengrod J, Brenner SE (2007a) Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements. Nature 446(7138):926–929

    Article  CAS  PubMed  Google Scholar 

  • Lazar G, Schaal TD, Maniatis T, Goodman HM (1995) Identification of a plant serine-arginine-rich protein similar to the mammalian splicing factor SF2/ASF. Proc Natl Acad Sci USA 92(17):7672–7676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lemaire R, Prasad J, Kashima T, Gustafson J, Manley JL, Lafyatis R (2002) Stability of a PKCI-1-related mRNA is controlled by the splicing factor ASF/SF2: a novel function for SR proteins. Genes Dev 16(5):594–607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Manley JL (2005) Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability. Cell 122(3):365–378

    Article  CAS  PubMed  Google Scholar 

  • Lin S, Coutinhomansfield G, Wang D, Pandit S, Fu X (2008) The splicing factor SC35 has an active role in transcriptional elongation. Nat Struct Mol Biol 15(8):819–826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopato S, Waigmann E, Barta A (1996) Characterization of a novel arginine/serine-rich splicing factor in arabidopsis. Plant Cell 8(12):2255–2264

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lorkovic ZJ, Hilscher J, Barta A (2008) Co-localisation studies of arabidopsis SR splicing factors reveal different types of speckles in plant cell nuclei. Exp Cell Res 314(17):3175–3186

    Article  CAS  PubMed  Google Scholar 

  • Ma C, Ghosh G, Fu X, Adams JA (2010) Mechanism of dephosphorylation of the SR protein ASF/SF2 by protein phosphatase 1. J Mol Biol 403(3):386–404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maertens GN, Cook N, Wang W, Hare S, Gupta SS, Oztop I, Lee K, Pye VE, Cosnefroy O, Snijders APL (2014) Structural basis for nuclear import of splicing factors by human transportin 3. Proc Natl Acad Sci USA 111(7):2728–2733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manley JL, Krainer AR (2010) A rational nomenclature for serine/arginine-rich protein splicing factors (SR proteins). Genes Dev 24(11):1073–1074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maruyama K, Sato N, Ohta N (1999) Conservation of structure and cold-regulation of RNA-binding proteins in cyanobacteria: probable convergent evolution with eukaryotic glycine-rich RNA-binding proteins. Nucleic Acids Res 27(9):2029–2036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meseguer S, Mudduluru G, Escamilla JM, Allgayer H, Barettino D (2011) MicroRNAs-10a and 10b contribute to retinoic acid-induced differentiation of neuroblastoma cells and target the alternative splicing regulatory factor SFRS1 (SF2/ASF). J Biol Chem 286(6):4150–4164

    Article  CAS  PubMed  Google Scholar 

  • Michlewski G, Sanford JR, Caceres JF (2008) The splicing factor SF2/ASF regulates translation initiation by enhancing phosphorylation of 4E-BP1. Mol Cell 30(2):179–189

    Article  CAS  PubMed  Google Scholar 

  • Morton M, Altamimi N, Butt H, Reddy ASN, Mahfouz M (2019a) Serine/Arginine-rich protein family of splicing regulators: new approaches to study splice isoform functions. Plant Sci 283:127–134

    Article  CAS  PubMed  Google Scholar 

  • Mullermcnicoll M, Botti V, Domingues AMDJ, Brandl H, Schwich OD, Steiner MC, Curk T, Poser I, Zarnack K, Neugebauer KM (2016) SR proteins are NXF1 adaptors that link alternative RNA processing to mRNA export. Genes Dev 30(5):553–566

    Article  PubMed  Google Scholar 

  • Ni JZ, Grate L, Donohue JP, Preston C, Nobida N, Obrien G, Shiue L, Clark TA, Blume JE, Ares M (2007) Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay. Genes Dev 21(6):708–718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palusa SG, Reddy ASN (2010) Extensive coupling of alternative splicing of pre-mRNAs of serine/arginine (SR) genes with nonsense-mediated decay. New Phytol 185(1):83–89

    Article  CAS  PubMed  Google Scholar 

  • Palusa SG, Ali GS, Reddy AS (2007) Alternative splicing of pre-mRNAs of arabidopsis serine/arginine-rich proteins: regulation by hormones and stresses. Plant J 49(6):1091–1107

    Article  CAS  PubMed  Google Scholar 

  • Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40(12):1413–1415

    Article  CAS  PubMed  Google Scholar 

  • Reed R, Cheng H (2005) TREX, SR proteins and export of mRNA. Curr Opin Cell Biol 17(3):269–273

    Article  CAS  PubMed  Google Scholar 

  • Richardson DN, Rogers MF, Labadorf A, Benhur A, Guo H, Paterson AH, Reddy ASN (2011) Comparative analysis of serine/arginine-rich proteins across 27 Eukaryotes: insights into sub-family classification and extent of alternative splicing. PLoS ONE 6(9):e24542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenkranz RRE, Bachiri S, Vraggalas S, Keller M, Simm S, Schleiff E, Fragkostefanakis S (2021) Identification and regulation of tomato serine/arginine-rich proteins under high temperatures. Front Plant Sci 12:645689

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruwe H, Kupsch C, Teubner M, Schmitz-Linneweber C (2011) The RNA-recognition motif in chloroplasts. J Plant Physiol 168(12):1361–1371

    Article  CAS  PubMed  Google Scholar 

  • Sanford JR, Coutinho P, Hackett JA, Wang X, Ranahan WP, Caceres JF (2008a) Identification of nuclear and cytoplasmic mRNA targets for the shuttling protein SF2/ASF. PLoS ONE 3(10):e3369

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanford JR, Wang X, Mort M, Vanduyn N, Cooper DN, Mooney SD, Edenberg HJ, Liu Y (2008b) Splicing factor SFRS1 recognizes a functionally diverse landscape of RNA transcripts. Genome Res 19(3):381–394

    Article  PubMed  Google Scholar 

  • Savaldigoldstein S, Sessa G, Fluhr R (2000) The ethylene-inducible PK12 kinase mediates the phosphorylation of SR splicing factors. Plant J 21(1):91–96

    Article  CAS  PubMed  Google Scholar 

  • Savaldigoldstein S, Aviv D, Davydov O, Fluhr R (2003) Alternative splicing modulation by a LAMMER kinase impinges on developmental and transcriptome expression. Plant Cell 15(4):926–938

    Article  CAS  PubMed  Google Scholar 

  • Shi Y, Su Z, Yang H, Wang W, Jin G, He G, Siddique AN, Zhang L, Zhu A, Xue R, Zhang C (2019) Alternative splicing coupled to nonsense-mediated mRNA decay contributes to the high-altitude adaptation of maca (Lepidium meyenii). Gene 694:7–18

    Article  CAS  PubMed  Google Scholar 

  • Stankovic N, Schloesser M, Joris M, Sauvage E, Hanikenne M, Motte P (2016) Dynamic distribution and interaction of the arabidopsis SRSF1 subfamily splicing factors. Plant Physiol 170(2):1000–1013

    Article  CAS  PubMed  Google Scholar 

  • Sun S, Zhang Z, Sinha R, Karni R, Krainer AR (2010) SF2/ASF autoregulation involves multiple layers of post-transcriptional and translational control. Nat Struct Mol Biol 17(3):306–312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terzi LC, Simpson GG (2009) Arabidopsis RNA immunoprecipitation. Plant J 59(1):163–168

    Article  CAS  PubMed  Google Scholar 

  • Tillemans V, Leponce I, Rausin G, Dispa L, Motte P (2006) Insights into nuclear organization in plants as revealed by the dynamic distribution of arabidopsis SR splicing factors. Plant Cell 18(11):3218–3234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Velazquezdones A, Hagopian JC, Ma C, Zhong X, Zhou H, Ghosh G, Fu X, Adams JA (2005) Mass spectrometric and kinetic analysis of ASF/SF2 phosphorylation by SRPK1 and Clk/Sty. J Biol Chem 280(50):41761–41768

    Article  CAS  PubMed  Google Scholar 

  • Wan L, Deng M, Zhang H (2022) SR splicing factors promote cancer via multiple regulatory mechanisms. Genes (basel) 13(9):1659

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Jiang Y (2021) SRp20: A potential therapeutic target for human tumors. Pathol Res Pract 224:153444

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Xue L, Batelli G, Lee S, Hou Y, Van Oosten MJ, Zhang H, Tao WA, Zhu J (2013) Quantitative phosphoproteomics identifies SnRK2 protein kinase substrates and reveals the effectors of abscisic acid action. Proc Natl Acad Sci USA 110(27):11205–11210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu JY, Maniatis T (1993) Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell 75(6):1061–1070

    Article  CAS  PubMed  Google Scholar 

  • Wu H, Sun S, Tu K, Gao Y, Xie B, Krainer AR, Zhu J (2010) A splicing-independent function of SF2/ASF in microRNA processing. Mol Cell 38(1):67–77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Liu H, Lu S, Hua J, Zou B (2021) Identification and expression analysis of chloroplast ribonucleoproteins (cpRNPs) in arabidopsis and rice. Genome 64(5):515–524

    Article  CAS  PubMed  Google Scholar 

  • Xiao R, Sun Y, Ding J, Lin S, Rose DW, Rosenfeld MG, Fu X, Li X (2007) Splicing regulator sc35 is essential for genomic stability and cell proliferation during mammalian organogenesis. Mol Cell Biol 27(15):5393–5402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao R, Chen J, Liang Z, Luo D, Chen G, Lu ZJ, Chen Y, Zhou B, Li H, Du X (2019) Pervasive chromatin-RNA binding protein interactions enable RNA-based regulation of transcription. Cell 178(1):107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xing D, Wang Y, Hamilton M, Ben-Hur A, Reddy AS (2015) Transcriptome-wide identification of RNA targets of arabidopsis SERINE/ARGININE-RICH45 uncovers the unexpected roles of this RNA binding protein in RNA processing. Plant Cell 27(12):3294–3308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu S, Zhang Z, Jing B, Gannon P, Ding J, Xu F, Li X, Zhang Y (2011) Transportin-SR is required for proper splicing of resistance genes and plant immunity. PLoS Genet 7(6):e1002159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan Q, Xia X, Sun Z, Fang Y (2017) Depletion of Arabidopsis SC35 and SC35-like serine/arginine-rich proteins affects the transcription and splicing of a subset of genes. PLoS Genet 13(3):e1006663

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Krainer AR (2004) Involvement of SR proteins in mRNA Surveillance. Mol Cell 16(4):597–607

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Shi Y, Powers JJ, Gowda NB, Zhang C, Ibrahim HM, Ball HB, Chen SL, Lu H, Mount SM (2017) Transcriptome analyses reveal SR45 to be a neutral splicing regulator and a suppressor of innate immunity in Arabidopsis thaliana. BMC Genomics 18(1):772–772

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao X, Tan L, Wang S, Shen Y, Guo L, Ye X, Liu S, Feng Y, Wu W (2021) The SR splicing factors: providing perspectives on their evolution, expression, alternative splicing, and function in populus trichocarpa. Int J Mol Sci 22(21):11369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu FY, Chen MX, Ye NH, Shi L, Ma KL, Yang JF, Cao YY, Zhang Y, Yoshida T, Fernie AR, Fan GY, Wen B, Zhou R, Liu TY, Fan T, Gao B, Zhang D, Hao GF, Xiao S, Liu YG, Zhang J (2017a) Proteogenomic analysis reveals alternative splicing and translation as part of the abscisic acid response in arabidopsis seedlings. Plant J 91(3):518–533

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the Guizhou Provincial Basic Research Program (Natural Science)-ZK[2023]-099, the National Natural Science Foundation of China (NSFC81401561, 91535109, 32001452), and the Hong Kong Research Grant Council (AoE/M-05/12, AoE/M-403/16, GRF14160516, 14177617, 12100318).

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Author notes

  1. Zi-Chang Jia and Debatosh Das contributed equally to this work.

Authors and Affiliations

  1. National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang, 550025, China

    Zi-Chang Jia & Moxian Chen

  2. College of Agriculture, Food and Natural Resources (CAFNR), Division of Plant Sciences and Technology, 52 Agricultural Building, University of Missouri, Columbia, MO, 65201, USA

    Debatosh Das

  3. Department of Biology, Hong Kong Baptist University, and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin, Hong Kong

    Debatosh Das & Jianhua Zhang

  4. Center of Plant System Biology and Biotechnology, 4000, Plovdiv, Bulgaria

    Youjun Zhang & Alisdair R. Fernie

  5. Max-Planck-Institut Für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, 14476, Potsdam-Golm, Germany

    Youjun Zhang & Alisdair R. Fernie

  6. State Key Laboratory of Crop Biology, College of Life Science, Shandong Agricultural University, Taian, Shandong, China

    Ying-Gao Liu

  7. CAS Key Laboratory of Quantitative Engineering Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, 518055, China

    Moxian Chen

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  1. Zi-Chang Jia
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Jia, ZC., Das, D., Zhang, Y. et al. Plant serine/arginine-rich proteins: versatile players in RNA processing. Planta 257, 109 (2023). https://doi.org/10.1007/s00425-023-04132-0

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