A Role for Nonsense-mediated MRNA Decay in Plants: Pathogen Responses Are Induced in Arabidopsis Thaliana NMD Mutants

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2012 Mar 3

PMID 22384098

Citations 67

Authors

Samantha Rayson

Luis Arciga-Reyes

Lucie Wootton

Marta de Torres Zabala

William Truman

Neil Graham

Murray Grant

Brendan Davies

Affiliations

Soon will be listed here.

Abstract

Nonsense-mediated mRNA decay (NMD) is a conserved mechanism that targets aberrant mRNAs for destruction. NMD has also been found to regulate the expression of large numbers of genes in diverse organisms, although the biological role for this is unclear and few evolutionarily conserved targets have been identified. Expression analyses of three Arabidopsis thaliana lines deficient in NMD reveal that the vast majority of NMD-targeted transcripts are associated with response to pathogens. Congruently, NMD mutants, in which these transcripts are elevated, confer partial resistance to Pseudomonas syringae. These findings suggest a biological rationale for the regulation of gene expression by NMD in plants and suggest that manipulation of NMD could offer a new approach for crop protection. Amongst the few non-pathogen responsive NMD-targeted genes, one potential NMD targeted signal, the evolutionarily conserved upstream open reading frame (CuORF), was found to be hugely over-represented, raising the possibility that this feature could be used to target specific physiological mRNAs for control by NMD.

Citing Articles

An autoregulatory poison exon in Smndc1 is conserved across kingdoms and influences organism growth.

Belleville A, Thomas J, Tonnies J, Gabel A, Borrero Rossi A, Singh P PLoS Genet. 2024; 20(8):e1011363.

PMID: 39150991 PMC: 11357089. DOI: 10.1371/journal.pgen.1011363.

Genomic analysis of a spontaneous unifoliate mutant reveals gene candidates associated with compound leaf development in Vigna unguiculata [L] Walp.

Edet O, Ubi B, Ishii T Sci Rep. 2024; 14(1):10654.

PMID: 38724579 PMC: 11082238. DOI: 10.1038/s41598-024-61062-x.

Suppression of the dwarf phenotype of an Arabidopsis mutant defective in thermospermine biosynthesis by a synonymous codon change in the SAC51 uORF.

Nishii Y, Koyama D, Fukushima H, Takahashi T Mol Genet Genomics. 2023; 298(6):1505-1514.

PMID: 37845372 DOI: 10.1007/s00438-023-02076-4.

RNA degradome analysis reveals DNE1 endoribonuclease is required for the turnover of diverse mRNA substrates in Arabidopsis.

Nagarajan V, Stuart C, DiBattista A, Accerbi M, Caplan J, Green P Plant Cell. 2023; 35(6):1936-1955.

PMID: 37070465 PMC: 10226599. DOI: 10.1093/plcell/koad085.

Cell-type-specific alternative splicing in the Arabidopsis germline.

Misra C, Sousa A, Barros P, Kermanov A, Becker J Plant Physiol. 2022; 192(1):85-101.

PMID: 36515615 PMC: 10152659. DOI: 10.1093/plphys/kiac574.

References

Kim M, da Cunha L, McFall A, Belkhadir Y, DebRoy S, Dangl J . Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell. 2005; 121(5):749-59. DOI: 10.1016/j.cell.2005.03.025. View

Yoine M, Nishii T, Nakamura K . Arabidopsis UPF1 RNA helicase for nonsense-mediated mRNA decay is involved in seed size control and is essential for growth. Plant Cell Physiol. 2006; 47(5):572-80. DOI: 10.1093/pcp/pcj035. View

Glazebrook J . Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol. 2005; 43:205-27. DOI: 10.1146/annurev.phyto.43.040204.135923. View

Gonzalez C, Vasudevan S, Henry M, Peltz S . The yeast hnRNP-like protein Hrp1/Nab4 marks a transcript for nonsense-mediated mRNA decay. Mol Cell. 2000; 5(3):489-99. DOI: 10.1016/s1097-2765(00)80443-8. View

Denning G, Jamieson L, Maquat L, Thompson E, Fields A . Cloning of a novel phosphatidylinositol kinase-related kinase: characterization of the human SMG-1 RNA surveillance protein. J Biol Chem. 2001; 276(25):22709-14. DOI: 10.1074/jbc.C100144200. View

Bruno I, Karam R, Huang L, Bhardwaj A, Lou C, Shum E . Identification of a microRNA that activates gene expression by repressing nonsense-mediated RNA decay. Mol Cell. 2011; 42(4):500-10. PMC: 3123134. DOI: 10.1016/j.molcel.2011.04.018. View

Nyiko T, Sonkoly B, Merai Z, Benkovics A, Silhavy D . Plant upstream ORFs can trigger nonsense-mediated mRNA decay in a size-dependent manner. Plant Mol Biol. 2009; 71(4-5):367-78. DOI: 10.1007/s11103-009-9528-4. View

Arciga-Reyes L, Wootton L, Kieffer M, Davies B . UPF1 is required for nonsense-mediated mRNA decay (NMD) and RNAi in Arabidopsis. Plant J. 2006; 47(3):480-9. DOI: 10.1111/j.1365-313X.2006.02802.x. View

Yoine M, Ohto M, Onai K, Mita S, Nakamura K . The lba1 mutation of UPF1 RNA helicase involved in nonsense-mediated mRNA decay causes pleiotropic phenotypic changes and altered sugar signalling in Arabidopsis. Plant J. 2006; 47(1):49-62. DOI: 10.1111/j.1365-313X.2006.02771.x. View

10.

Fukuhara N, Ebert J, Unterholzner L, Lindner D, Izaurralde E, Conti E . SMG7 is a 14-3-3-like adaptor in the nonsense-mediated mRNA decay pathway. Mol Cell. 2005; 17(4):537-47. DOI: 10.1016/j.molcel.2005.01.010. View

11.

Craigon D, James N, Okyere J, Higgins J, Jotham J, May S . NASCArrays: a repository for microarray data generated by NASC's transcriptomics service. Nucleic Acids Res. 2003; 32(Database issue):D575-7. PMC: 308867. DOI: 10.1093/nar/gkh133. View

12.

Zhang X, Gassmann W . Alternative splicing and mRNA levels of the disease resistance gene RPS4 are induced during defense responses. Plant Physiol. 2007; 145(4):1577-87. PMC: 2151689. DOI: 10.1104/pp.107.108720. View

13.

Singh G, Rebbapragada I, Lykke-Andersen J . A competition between stimulators and antagonists of Upf complex recruitment governs human nonsense-mediated mRNA decay. PLoS Biol. 2008; 6(4):e111. PMC: 2689706. DOI: 10.1371/journal.pbio.0060111. View

14.

Anders K, Grimson A, Anderson P . SMG-5, required for C.elegans nonsense-mediated mRNA decay, associates with SMG-2 and protein phosphatase 2A. EMBO J. 2003; 22(3):641-50. PMC: 140740. DOI: 10.1093/emboj/cdg056. View

15.

Li Y, Tian Z, Liu J, Xie C . Comparative cDNA-AFLP analysis reveals that DL-beta-amino-butyric acid induces resistance through early activation of the host-defense genes in potato. Physiol Plant. 2009; 136(1):19-29. DOI: 10.1111/j.1399-3054.2009.01209.x. View

16.

Robert-Seilaniantz A, Grant M, Jones J . Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol. 2011; 49:317-43. DOI: 10.1146/annurev-phyto-073009-114447. View

17.

Serin G, Gersappe A, Black J, ARONOFF R, Maquat L . Identification and characterization of human orthologues to Saccharomyces cerevisiae Upf2 protein and Upf3 protein (Caenorhabditis elegans SMG-4). Mol Cell Biol. 2000; 21(1):209-23. PMC: 88795. DOI: 10.1128/MCB.21.1.209-223.2001. View

18.

Truman W, Bennett M, Turnbull C, Grant M . Arabidopsis auxin mutants are compromised in systemic acquired resistance and exhibit aberrant accumulation of various indolic compounds. Plant Physiol. 2010; 152(3):1562-73. PMC: 2832264. DOI: 10.1104/pp.109.152173. View

19.

Venugopal S, Jeong R, Mandal M, Zhu S, Chandra-Shekara A, Xia Y . Enhanced disease susceptibility 1 and salicylic acid act redundantly to regulate resistance gene-mediated signaling. PLoS Genet. 2009; 5(7):e1000545. PMC: 2695777. DOI: 10.1371/journal.pgen.1000545. View

20.

Huang D, Sherman B, Lempicki R . Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009; 4(1):44-57. DOI: 10.1038/nprot.2008.211. View