Student or educator? Sign up with your school email and get 6 months of Pro free.
Cited by 2,294

The DOI matches its Crossref record; 3 of the 3 references it cites were found in a registry or an index.

Dynamic regulation of genome-wide pre-mRNA splicing and stress tolerance by the Sm-like protein LSm5 in Arabidopsis

Open access
Cui, Peng, Zhang, Shoudong, Ding, Feng, Ali, Shahjahan, Xiong, Liming·2014·Genome Biology

Abstract

Background: Sm-like proteins are highly conserved proteins that form the core of the U6 ribonucleoprotein and function in several mRNA metabolism processes, including pre-mRNA splicing. Despite their wide occurrence in all eukaryotes, little is known about the roles of Sm-like proteins in the regulation of splicing. Results: Here, through comprehensive transcriptome analyses, we demonstrate that depletion of the Arabidopsis supersensitive to abscisic acid and drought 1 gene ( SAD1 ), which encodes Sm-like protein 5 (LSm5), promotes an inaccurate selection of splice sites that leads to a genome-wide increase in alternative splicing. In contrast, overexpression of SAD1 strengthens the precision of splice-site recognition and globally inhibits alternative splicing. Further, SAD1 modulates the splicing of stress-responsive genes, particularly under salt-stress conditions. Finally, we find that overexpression of SAD1 in Arabidopsis improves salt tolerance in transgenic plants, which correlates with an increase in splicing accuracy and efficiency for stress-responsive genes. Conclusions: We conclude that SAD1 dynamically controls splicing efficiency and splice-site recognition in Arabidopsis , and propose that this may contribute to SAD1 -mediated stress tolerance through the metabolism of transcripts expressed from stress-responsive genes. Our study not only provides novel insights into the function of Sm-like proteins in splicing, but also uncovers new means to improve splicing efficiency and to enhance stress tolerance in a higher eukaryote.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1186/gb-2014-15-1-r1

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 3 references

Research works printed but not linked: 45

  1. Braunschweig U, Gueroussov S, Plocik AM, Graveley BR, Blencowe BJ: Dynamic integration of splicing within gene regulatory pathways. Cell. 2013, 152: 1252-1269. 10.1016/j.cell.2013.02.034. · DOI · Paper page
  2. Faustino NA, Cooper TA: Pre-mRNA splicing and human disease. Genes Dev. 2003, 17: 419-437. 10.1101/gad.1048803. · DOI · Paper page
  3. Singh RK, Cooper TA: Pre-mRNA splicing in disease and therapeutics. Trends Mol Med. 2012, 18: 472-482. 10.1016/j.molmed.2012.06.006. · DOI
  4. Mazzucotelli A, Ribet C, Castan-Laurell I, Daviaud D, Guigne C, Langin D, Valet P: The transcriptional co-activator PGC-1alpha up regulates apelin in human and mouse adipocytes. Regul Pept. 2008, 150: 33-37. 10.1016/j.regpep.2008.04.003. · DOI
  5. Palusa SG, Ali GS, Reddy AS: Alternative splicing of pre-mRNAs of Arabidopsis serine/arginine-rich proteins: regulation by hormones and stresses. Plant J. 2007, 49: 1091-1107. 10.1111/j.1365-313X.2006.03020.x. · DOI
  6. Syed NH, Kalyna M, Marquez Y, Barta A, Brown JW: Alternative splicing in plants–coming of age. Trends Plant Sci. 2012, 17: 616-623. 10.1016/j.tplants.2012.06.001. · DOI
  7. Beggs JD: LSm proteins and RNA processing. Biochem Soc Trans. 2005, 33: 433-438. · DOI
  8. Collins BM, Harrop SJ, Kornfeld GD, Dawes IW, Curmi PM, Mabbutt BC: Crystal structure of a heptameric Sm-like protein complex from archaea: implications for the structure and evolution of snRNPs. J Mol Biol. 2001, 309: 915-923. 10.1006/jmbi.2001.4693. · DOI
  9. Khusial P, Plaag R, Zieve GW: LSm proteins form heptameric rings that bind to RNA via repeating motifs. Trends Biochem Sci. 2005, 30: 522-528. 10.1016/j.tibs.2005.07.006. · DOI
  10. Fenger-Gron M, Fillman C, Norrild B, Lykke-Andersen J: Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Mol Cell. 2005, 20: 905-915. 10.1016/j.molcel.2005.10.031. · DOI
  11. Ingelfinger D, Arndt-Jovin DJ, Luhrmann R, Achsel T: The human LSm1-7 proteins colocalize with the mRNA-degrading enzymes Dcp1/2 and Xrn1 in distinct cytoplasmic foci. RNA. 2002, 8: 1489-1501. · DOI
  12. Mayes AE, Verdone L, Legrain P, Beggs JD: Characterization of Sm-like proteins in yeast and their association with U6 snRNA. EMBO J. 1999, 18: 4321-4331. 10.1093/emboj/18.15.4321. · DOI
  13. Verdone L, Galardi S, Page D, Beggs JD: LSm proteins promote regeneration of pre-mRNA splicing activity. Curr Biol. 2004, 14: 1487-1491. 10.1016/j.cub.2004.08.032. · DOI
  14. Xiong L, Gong Z, Rock CD, Subramanian S, Guo Y, Xu W, Galbraith D, Zhu JK: Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev Cell. 2001, 1: 771-781. 10.1016/S1534-5807(01)00087-9. · DOI
  15. Perea-Resa C, Hernandez-Verdeja T, Lopez-Cobollo R, del Mar Castellano M, Salinas J: LSM proteins provide accurate splicing and decay of selected transcripts to ensure normal Arabidopsis development. Plant Cell. 2012, 24: 4930-4947. 10.1105/tpc.112.103697. · DOI
  16. Golisz A, Sikorski PJ, Kruszka K, Kufel J: Arabidopsis thaliana LSM proteins function in mRNA splicing and degradation. Nucleic Acids Res. 2013, 41: 6232-6249. 10.1093/nar/gkt296. · DOI
  17. Ishitani M, Xiong LM, Stevenson B, Zhu JK: Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. Plant Cell. 1997, 9: 1935-1949. · DOI
  18. Thorvaldsdottir H, Robinson JT, Mesirov JP: Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 2012, 14: 178-192. · DOI · Paper page
  19. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP: Integrative genomics viewer. Nat Biotechnol. 2011, 29: 24-26. 10.1038/nbt.1754. · DOI · Paper page
  20. Trapnell C, Pachter L, Salzberg SL: TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009, 25: 1105-1111. 10.1093/bioinformatics/btp120. · DOI · Paper page
  21. Huang DW, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009, 4: 44-57. · DOI · Paper page
  22. Huang DW, Sherman BT, Lempicki RA: Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009, 37: 1-13. 10.1093/nar/gkn923. · DOI · Paper page
  23. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W: GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 2004, 136: 2621-2632. 10.1104/pp.104.046367. · DOI
  24. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M: MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 2004, 37: 914-939. 10.1111/j.1365-313X.2004.02016.x. · DOI · Paper page
  25. Fujii H, Verslues PE, Zhu JK: Arabidopsis decuple mutant reveals the importance of SnRK2 kinases in osmotic stress responses in vivo. Proc Natl Acad Sci USA. 2011, 108: 1717-1722. 10.1073/pnas.1018367108. · DOI · Paper page
  26. Liu JP, Ishitani M, Halfter U, Kim CS, Zhu JK: The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci USA. 2000, 97: 3730-3734. 10.1073/pnas.97.7.3730. · DOI
  27. Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K: Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell. 2006, 18: 1292-1309. 10.1105/tpc.105.035881. · DOI
  28. Apse MP, Aharon GS, Snedden WA, Blumwald E: Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science. 1999, 285: 1256-1258. 10.1126/science.285.5431.1256. · DOI
  29. Lai Z, Li Y, Wang F, Cheng Y, Fan B, Yu JQ, Chen Z: Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in plant defense. Plant Cell. 2011, 23: 3824-3841. 10.1105/tpc.111.090571. · DOI · Paper page
  30. Jiang YQ, Deyholos MK: Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol. 2009, 69: 91-105. 10.1007/s11103-008-9408-3. · DOI
  31. Koiwa H, Li F, McCully MG, Mendoza I, Koizumi N, Manabe Y, Nakagawa Y, Zhu J, Rus A, Pardo JM, Bressan RA, Hasegawa PM: The STT3a subunit isoform of the Arabidopsis oligosaccharyltransferase controls adaptive responses to salt/osmotic stress. Plant Cell. 2003, 15: 2273-2284. 10.1105/tpc.013862. · DOI
  32. Cheng NH, Pittman JK, Zhu JK, Hirschi KD: The protein kinase SOS2 activates the Arabidopsis H+/Ca2+ antiporter CAX1 to integrate calcium transport and salt tolerance. J Biol Chem. 2004, 279: 2922-2926. · DOI · Paper page
  33. Mitsuya S, Taniguchi M, Miyake H, Takabe T: Disruption of RCI2A leads to over-accumulation of Na+ and increased salt sensitivity in Arabidopsis thaliana plants. Planta. 2005, 222: 1001-1009. 10.1007/s00425-005-0043-9. · DOI
  34. Kim S, Kang JY, Cho DI, Park JH, Kim SY: ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J. 2004, 40: 75-87. 10.1111/j.1365-313X.2004.02192.x. · DOI · Paper page
  35. Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K: AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J. 2010, 61: 672-685. 10.1111/j.1365-313X.2009.04092.x. · DOI · Paper page
  36. de la Mata M, Alonso CR, Kadener S, Fededa JP, Blaustein M, Pelisch F, Cramer P, Bentley D, Kornblihtt AR: A slow RNA polymerase II affects alternative splicing in vivo. Mol Cell. 2003, 12: 525-532. 10.1016/j.molcel.2003.08.001. · DOI · Paper page
  37. Kornblihtt AR: Coupling transcription and alternative splicing. Adv Exp Med Biol. 2007, 623: 175-189. 10.1007/978-0-387-77374-2_11. · DOI
  38. Xiong LM, Schumaker KS, Zhu JK: Cell signaling during cold, drought, and salt stress. Plant Cell. 2002, 14: S165-S183. 10.1105/tpc.010278. · DOI · Paper page
  39. Yamaguchi-Shinozaki K, Shinozaki K: Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Physiol Plant Mol Biol. 2006, 57: 781-803. · DOI
  40. Hugouvieux V, Kwak JM, Schroeder JI: An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell. 2001, 106: 477-487. 10.1016/S0092-8674(01)00460-3. · DOI
  41. Gong ZZ, Dong CH, Lee H, Zhu JH, Xiong LM, Gong DM, Stevenson B, Zhu JK: A DEAD box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell. 2005, 17: 256-267. 10.1105/tpc.104.027557. · DOI
  42. Guan QM, Wu JM, Zhang YY, Jiang CH, Liu RY, Chai CL, Zhu JH: A DEAD box RNA helicase is critical for pre-mRNA splicing, cold-responsive gene regulation, and cold tolerance in Arabidopsis. Plant Cell. 2013, 25: 342-356. 10.1105/tpc.112.108340. · DOI
  43. Moller IS, Gilliham M, Jha D, Mayo GM, Roy SJ, Coates JC, Haseloff J, Tester M: Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell. 2009, 21: 2163-2178. 10.1105/tpc.108.064568. · DOI · Paper page
  44. Shi HZ, Lee BH, Wu SJ, Zhu JK: Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nature Biotechnol. 2003, 21: 81-85. · DOI · Paper page
  45. Brooks AN, Yang L, Duff MO, Hansen KD, Park JW, Dudoit S, Brenner SE, Graveley BR: Conservation of an RNA regulatory map between Drosophila and mammals. Genome Res. 2011, 21: 193-202. 10.1101/gr.108662.110. · DOI

Cited by

Metadata

Authors
Cui, P., Zhang, S., Ding, F., Ali, S., & Xiong, L.
Venue
Genome Biology
Published
2014-01-07
Volume
15
Issue
1
Pages
R1-R1
ISSN
  • 1465-6906 (ISSN-L)
  • 1474-760X
OpenAlex
W1970707135
Cited by
2,294
References
3
FWCI
16.31
Type
journal article
Language
en
Open access
gold
Licence

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.