Skip to main content
SpringerLink
Log in

Genetic and environmental changes in SUMO homeostasis lead to nuclear mRNA retention in plants

  • Rapid Communication
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Protein sumoylation plays an important role in plant development, flowering-time regulation, and abiotic stress response. However, the molecular role of sumoylation in these pathways is largely unknown. It was shown previously that in mutants of the inner nuclear basket nucleoporin NUA a large increase in the abundance of high-molecular weight SUMO conjugated proteins correlated with nuclear retention of bulk mRNA. Here, the connection between sumoylation and mRNA export in plants was further investigated. Both SUMO-conjugate accumulation and mRNA retention were also found in a second nucleoporin mutant that does not affect NUA, and SUMO conjugates accumulated predominantly in the nucleus. Similarly, after heat and ethanol treatment, two abiotic stress treatments known to lead to the accumulation of sumoylated proteins, nuclear mRNA was retained. To establish a causal relationship between sumoylation and mRNA export, mutations in two enzymes in the SUMO pathway were tested. Mutating either SUMO E3 ligase or SUMO isopeptidase lead to nuclear mRNA retention, indicating that both an increase and a decrease in the pool of sumoylated nuclear proteins blocks mRNA export. Together, these data show that sumoylation acts upstream of mRNA export in plants, likely through the transient sumoylation status of one or more factors involved in mRNA trafficking.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

ADK:

Adenosine kinase

ESD4:

Early in short days 4

NPC:

Nuclear pore complex

NUA:

Nuclear pore anchor

Nup:

Nucleoporin

SUMO:

Small, ubiquitin-like modifier

ROI:

Region of interest

References

  • Achard P, Herr A, Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131:3357–3365

    Article  CAS  PubMed  Google Scholar 

  • Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, Devos D, Suprapto A, Karni-Schmidt O, Williams R, Chait BT, Rout MP, Sali A (2007) Determining the architectures of macromolecular assemblies. Nature 450:683–694

    Article  CAS  PubMed  Google Scholar 

  • Alonso J, Stepanova A, Leisse T, Kim C, Chen H, Shinn P et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

  • Budhiraja R, Hermkes R, Muller S, Schmidt J, Colby T, Panigrahi K, Coupland G, Bachmair A (2009) Substrates related to chromatin and to RNA-dependent processes are modified by Arabidopsis SUMO isoforms that differ in a conserved residue with influence on desumoylation. Plant Physiol 149:1529–1540

    Article  CAS  PubMed  Google Scholar 

  • Catala R, Ouyang J, Abreu IA, Hu Y, Seo H, Zhang X, Chua NH (2007) The Arabidopsis E3 SUMO ligase SIZ1 regulates plant growth and drought responses. Plant Cell 19:2952–2966

    Article  CAS  PubMed  Google Scholar 

  • Devos D, Dokudovskaya S, Williams R, Alber F, Eswar N, Chait BT, Rout MP, Sali A (2006) Simple fold composition and modular architecture of the nuclear pore complex. Proc Natl Acad Sci USA 103:2172–2177

    Article  CAS  PubMed  Google Scholar 

  • Dong CH, Hu X, Tang W, Zheng X, Kim YS, Lee BH, Zhu JK (2006) A putative Arabidopsis nucleoporin, AtNUP160, is critical for RNA export and required for plant tolerance to cold stress. Mol Cell Biol 26:9533–9543

    Article  CAS  PubMed  Google Scholar 

  • Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jurgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153

    Article  CAS  PubMed  Google Scholar 

  • Gong Z, Dong CH, Lee H, Zhu J, Xiong L, Gong D, Stevenson B, Zhu JK (2005) A DEAD box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell 17:256–267

    Article  CAS  PubMed  Google Scholar 

  • Hanania U, Furman-Matarasso N, Ron M, Avni A (1999) Isolation of a novel SUMO protein from tomato that suppresses EIX-induced cell death. Plant J 19:533–541

    Article  CAS  PubMed  Google Scholar 

  • Izawa S (2010) Ethanol stress response in the mRNA flux of Saccharomyces cerevisiae. Biosci Biotechnol Biochem 74:7–12

    Article  CAS  PubMed  Google Scholar 

  • Izawa S, Kita T, Ikeda K, Inoue Y (2008) Heat shock and ethanol stress provoke distinctly different responses in 3′-processing and nuclear export of HSP mRNA in Saccharomyces cerevisiae. Biochem J 414:111–119

    Article  CAS  PubMed  Google Scholar 

  • Jacob Y, Mongkolsiriwatana C, Veley KM, Kim SY, Michaels SD (2007) The nuclear pore protein AtTPR is required for RNA homeostasis, flowering time, and auxin signaling. Plant Physiol 144:1383–1390

    Article  CAS  PubMed  Google Scholar 

  • Kelly SM, Leung SW, Apponi LH, Bramley AM, Tran EJ, Chekanova JA, Wente SR, Corbett AH (2010) Recognition of polyadenosine RNA by the zinc finger domain of nuclear poly(A) RNA-binding protein 2 (Nab2) is required for correct mRNA 3′-end formation. J Biol Chem 285:26022–26032

    Article  CAS  PubMed  Google Scholar 

  • Kim SH, Roux SJ (2003) An Arabidopsis Ran-binding protein, AtRanBP1c, is a co-activator of Ran GTPase-activating protein and requires the C-terminus for its cytoplasmic localization. Planta 216:1047–1052

    CAS  PubMed  Google Scholar 

  • Krysan PJ, Young JC, Sussman MR (1999) T-DNA as an insertional mutagen in Arabidopsis. Plant Cell 11:2283–2290

    Article  CAS  PubMed  Google Scholar 

  • Kurepa J, Walker JM, Smalle J, Gosink MM, Davis SJ, Durham TL, Sung DY, Vierstra RD (2003) The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and -2 conjugates is increased by stress. J Biol Chem 278:6862–6872

    Article  CAS  PubMed  Google Scholar 

  • Li T, Evdokimov E, Shen RF, Chao CC, Tekle E, Wang T, Stadtman ER, Yang DC, Chock PB (2004) Sumoylation of heterogeneous nuclear ribonucleoproteins, zinc finger proteins, and nuclear pore complex proteins: a proteomic analysis. Proc Natl Acad Sci USA 101:8551–8556

    Article  CAS  PubMed  Google Scholar 

  • Lu Q, Tang X, Tian G, Wang F, Liu K, Nguyen V, Kohalmi SE, Keller WA, Tsang EW, Harada JJ, Rothstein SJ, Cui Y (2010) Arabidopsis homolog of the yeast TREX-2 mRNA export complex: components and anchoring nucleoporin. Plant J 61:259–270

    Article  CAS  PubMed  Google Scholar 

  • Martin S, Nishimune A, Mellor JR, Henley JM (2007) SUMOylation regulates kainate-receptor-mediated synaptic transmission. Nature 447:321–325

    Article  CAS  PubMed  Google Scholar 

  • Meier I, Brkljacic J (2009) The nuclear pore and plant development. Curr Opin Plant Biol 12:87–95

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Hasegawa PM (2010) Sumoylation and other ubiquitin-like post-translational modifications in plants. Trends Cell Biol 20:223–232

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, Yun DJ, Hasegawa PM (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci USA 102:7760–7765

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Jin JB, Hasegawa PM (2007) Sumoylation, a post-translational regulatory process in plants. Curr Opin Plant Biol 10:495–502

    Article  CAS  PubMed  Google Scholar 

  • Murtas G, Reeves PH, Fu YF, Bancroft I, Dean C, Coupland G (2003) A nuclear protease required for flowering-time regulation in Arabidopsis reduces the abundance of SMALL UBIQUITIN-RELATED MODIFIER conjugates. Plant Cell 15:2308–2319

    Article  CAS  PubMed  Google Scholar 

  • Parry G, Ward S, Cernac A, Dharmasiri S, Estelle M (2006) The Arabidopsis SUPPRESSOR OF AUXIN RESISTANCE proteins are nucleoporins with an important role in hormone signaling and development. Plant Cell 18:1590–1603

    Article  CAS  PubMed  Google Scholar 

  • Rollenhagen C, Hodge CA, Cole CN (2004) The nuclear pore complex and the DEAD box protein Rat8p/Dbp5p have nonessential features which appear to facilitate mRNA export following heat shock. Mol Cell Biol 24:4869–4879

    Article  CAS  PubMed  Google Scholar 

  • Rose A, Meier I (2001) A domain unique to plant RanGAP is responsible for its targeting to the plant nuclear rim. Proc Natl Acad Sci USA 98:15377–15382

    Article  CAS  PubMed  Google Scholar 

  • Roux KJ, Crisp ML, Liu Q, Kim D, Kozlov S, Stewart CL, Burke B (2009) Nesprin 4 is an outer nuclear membrane protein that can induce kinesin-mediated cell polarization. Proc Natl Acad Sci USA 106:2194–2199

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: A laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor

    Google Scholar 

  • Saracco SA, Miller MJ, Kurepa J, Vierstra RD (2007) Genetic analysis of SUMOylation in Arabidopsis: conjugation of SUMO1 and SUMO2 to nuclear proteins is essential. Plant Physiol 145:119–134

    Article  CAS  PubMed  Google Scholar 

  • Schwartz TU (2005) Modularity within the architecture of the nuclear pore complex. Curr Opin Struct Biol 15:221–226

    Article  CAS  PubMed  Google Scholar 

  • Stutz F, Izaurralde E (2003) The interplay of nuclear mRNP assembly, mRNA surveillance and export. Trends Cell Biol 13:319–327

    Article  CAS  PubMed  Google Scholar 

  • Takemura R, Inoue Y, Izawa S (2004) Stress response in yeast mRNA export factor: reversible changes in Rat8p localization are caused by ethanol stress but not heat shock. J Cell Sci 117:4189–4197

    Article  CAS  PubMed  Google Scholar 

  • Tempe D, Piechaczyk M, Bossis G (2008) SUMO under stress. Biochem Soc Trans 36:874–878

    Article  CAS  PubMed  Google Scholar 

  • Thompson AR, Doelling JH, Suttangkakul A, Vierstra RD (2005) Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol 138:2097–2110

    Article  CAS  PubMed  Google Scholar 

  • Walther TC, Alves A, Pickersgill H, Loiodice I, Hetzer M, Galy V, Hulsmann BB, Kocher T, Wilm M, Allen T, Mattaj IW, Doye V (2003) The conserved Nup107–160 complex is critical for nuclear pore complex assembly. Cell 113:195–206

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson KA, Henley JM (2010) Mechanisms, regulation and consequences of protein SUMOylation. Biochem J 428:133–145

    Article  CAS  PubMed  Google Scholar 

  • Xu XM, Meier I (2008) The nuclear pore comes to the fore. Trends Plant Sci 13:20–27

    Article  CAS  PubMed  Google Scholar 

  • Xu XM, Rose A, Muthuswamy S, Jeong SY, Venkatakrishnan S, Zhao Q, Meier I (2007) NUCLEAR PORE ANCHOR, the Arabidopsis homolog of Tpr/Mlp1/Mlp2/Megator, is involved in mRNA export and SUMO homeostasis and affects diverse aspects of plant development. Plant Cell 19:1537–1548

    Article  CAS  PubMed  Google Scholar 

  • Yelina NE, Smith LM, Jones AME, Patel K, Kelly KA, Baulcombe DC (2010) Putative Arabidopsis THO/TREX mRNA export complex is involved in transgene and endogenous siRNA biosynthesis. Proc Natl Acad Sci USA 107:13948–13953

    Article  CAS  PubMed  Google Scholar 

  • Yoo CY, Miura K, Jin JB, Lee J, Park HC, Salt DE, Yun DJ, Bressan RA, Hasegawa PM (2006) SIZ1 small ubiquitin-like modifier E3 ligase facilitates basal thermotolerance in Arabidopsis independent of salicylic acid. Plant Physiol 142:1548–1558

    Article  CAS  PubMed  Google Scholar 

  • Zhou W, Ryan JJ, Zhou H (2004) Global analyses of sumoylated proteins in Saccharomyces cerevisiae. Induction of protein sumoylation by cellular stresses. J Biol Chem 279:32262–32268

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Drs Xin Li and Marcel Wiermer (University of British Columbia, Vancouver, Canada) for sharing their unpublished atnup160-3 allele with us. We would like to thank Drs Paul Hasegawa (Purdue University, Lafayette, IN, USA) for siz1-2, George Coupland (Max Planck Institute, Cologne, Germany) for esd4-2, and David Bisaro (Ohio State University, Columbus, OH, USA) for the anti-ADK antibody. This work has been supported by a grant from the National Science Foundation to IM.

Author information

Authors and Affiliations

  1. Department of Plant Cellular and Molecular Biology, The Ohio State University, Columbus, OH, 43210, USA

    Sivaramakrishnan Muthuswamy & Iris Meier

Authors
  1. Sivaramakrishnan Muthuswamy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Iris Meier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Iris Meier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Muthuswamy, S., Meier, I. Genetic and environmental changes in SUMO homeostasis lead to nuclear mRNA retention in plants. Planta 233, 201–208 (2011). https://doi.org/10.1007/s00425-010-1278-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-010-1278-7

Keywords

Search

Navigation