Genetic and environmental changes in SUMO homeostasis lead to nuclear mRNA retention in plants
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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.
KeywordsEthanol Heatshock mRNA Nucleoporin Nuclear pore Stress SUMO
Early in short days 4
Nuclear pore complex
Nuclear pore anchor
Small, ubiquitin-like modifier
Region of interest
We are grateful to Drs Xin Li and Marcel Wiermer (University of British Columbia, Vancouver, Canada) for sharing their unpublished atnup160-3 allele with us.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.
- 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 149:1529–1540CrossRefPubMedGoogle 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 285:26022–26032CrossRefPubMedGoogle Scholar
- Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: A laboratory manual. Cold Spring Harbor Press, Cold Spring HarborGoogle 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 19:1537–1548CrossRefPubMedGoogle Scholar