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      A Role for Nonsense-Mediated mRNA Decay in Plants: Pathogen Responses Are Induced in Arabidopsis thaliana NMD Mutants

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          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.

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          Most cited references92

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          The Arabidopsis Information Resource (TAIR): gene structure and function annotation

          The Arabidopsis Information Resource (TAIR, http://arabidopsis.org) is the model organism database for the fully sequenced and intensively studied model plant Arabidopsis thaliana. Data in TAIR is derived in large part from manual curation of the Arabidopsis research literature and direct submissions from the research community. New developments at TAIR include the addition of the GBrowse genome viewer to the TAIR site, a redesigned home page, navigation structure and portal pages to make the site more intuitive and easier to use, the launch of several TAIR web services and a new genome annotation release (TAIR7) in April 2007. A combination of manual and computational methods were used to generate this release, which contains 27 029 protein-coding genes, 3889 pseudogenes or transposable elements and 1123 ncRNAs (32 041 genes in all, 37 019 gene models). A total of 681 new genes and 1002 new splice variants were added. Overall, 10 098 loci (one-third of all loci from the previous TAIR6 release) were updated for the TAIR7 release.
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            Innate immunity in plants and animals: striking similarities and obvious differences.

            Innate immunity constitutes the first line of defense against attempted microbial invasion, and it is a well-described phenomenon in vertebrates and insects. Recent pioneering work has revealed striking similarities between the molecular organization of animal and plant systems for nonself recognition and anti-microbial defense. Like animals, plants have acquired the ability to recognize invariant pathogen-associated molecular patterns (PAMPs) that are characteristic of microbial organisms but which are not found in potential host plants. Such structures, also termed general elicitors of plant defense, are often indispensable for the microbial lifestyle and, upon receptor-mediated perception, inevitably betray the invader to the plant's surveillance system. Remarkable similarities have been uncovered in the molecular mode of PAMP perception in animals and plants, including the discovery of plant receptors resembling mammalian Toll-like receptors or cytoplasmic nucleotide-binding oligomerization domain leucine-rich repeat proteins. Moreover, molecular building blocks of PAMP-induced signaling cascades leading to the transcriptional activation of immune response genes are shared among the two kingdoms. In particular, nitric oxide as well as mitogen-activated protein kinase cascades have been implicated in triggering innate immune responses, part of which is the production of antimicrobial compounds. In addition to PAMP-mediated pathogen defense, disease resistance programs are often initiated upon plant-cultivar-specific recognition of microbial race-specific virulence factors, a recognition specificity that is not known from animals.
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              Are innate immune signaling pathways in plants and animals conserved?

              Although adaptive immunity is unique to vertebrates, the innate immune response seems to have ancient origins. Common features of innate immunity in vertebrates, invertebrate animals and plants include defined receptors for microbe-associated molecules, conserved mitogen-associated protein kinase signaling cascades and the production of antimicrobial peptides. It is commonly reported that these similarities in innate immunity represent a process of divergent evolution from an ancient unicellular eukaryote that pre-dated the divergence of the plant and animal kingdoms. However, at present, data suggest that the seemingly analogous regulatory modules used in plant and animal innate immunity are a consequence of convergent evolution and reflect inherent constraints on how an innate immune system can be constructed.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                22 February 2012
                : 7
                : 2
                : e31917
                Affiliations
                [1 ]Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds, Leeds, United Kingdom
                [2 ]School of Biosciences, University of Exeter, Exeter, United Kingdom
                [3 ]Nottingham Arabidopsis Stock Centre, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, United Kingdom
                University of Melbourne, Australia
                Author notes

                Conceived and designed the experiments: SR LAR LW MG BD. Performed the experiments: SR LAR LW MDTZ. Analyzed the data: SR WT NG MG BD. Contributed reagents/materials/analysis tools: MG BD. Wrote the paper: SR BD.

                Article
                PONE-D-11-19588
                10.1371/journal.pone.0031917
                3284524
                22384098
                b7f6be10-95d4-41a1-ac49-36f93b47a800
                Rayson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 5 October 2011
                : 15 January 2012
                Page count
                Pages: 13
                Categories
                Research Article
                Biology
                Evolutionary Biology
                Genetics
                Gene Expression
                Model Organisms
                Plant and Algal Models
                Molecular Cell Biology
                Gene Expression
                Plant Science
                Plant Pathology

                Uncategorized
                Uncategorized

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