NIK1-mediated translation suppression functions as a plant antiviral immunity mechanism

• Published in: Nature (London) Vol. 520; no. 7549; pp. 679 - 682
• Main Authors: Zorzatto, Cristiane, Machado, João Paulo B., Lopes, Kênia V. G., Nascimento, Kelly J. T., Pereira, Welison A., Brustolini, Otávio J. B., Reis, Pedro A. B., Calil, Iara P., Deguchi, Michihito, Sachetto-Martins, Gilberto, Gouveia, Bianca C., Loriato, Virgílio A. P., Silva, Marcos A. C., Silva, Fabyano F., Santos, Anésia A., Chory, Joanne, Fontes, Elizabeth P. B.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 30.04.2015; Nature Publishing Group
• Subjects: 13/106; 13/107; 13/109; 13/51; 13/95; 14/19; 14/63; 38/111; 38/15; 38/22; 38/39; 38/43; 38/77; 631/337/574; 631/449/2169; 631/449/2675; 82/29; Active Transport, Cell Nucleus; Arabidopsis - immunology; Arabidopsis - virology; Arabidopsis Proteins - metabolism; Begomovirus - immunology; Cell Nucleus - metabolism; Deoxyribonucleic acid; DNA; Down-Regulation; Food security; Gene expression; Gene Expression Regulation, Plant; Genetic aspects; Genotype & phenotype; Health aspects; Humanities and Social Sciences; Immune Tolerance; Immunity, Innate; Kinases; Leaves; letter; multidisciplinary; Pathogens; Plant defenses; Plant Immunity; Plant pathology; Plant-pathogen relationships; Protein Binding; Protein Biosynthesis - genetics; Protein Biosynthesis - immunology; Protein Serine-Threonine Kinases - metabolism; Protein synthesis; Proteins; Ribosomal Protein L10; Ribosomal Proteins - metabolism; Science; Transcription factors; Transcription Factors - metabolism; Translation (Genetics); Translocation; Viral infections
• ISSN: 0028-0836; 1476-4687; 1476-4687
• DOI: 10.1038/nature14171

A new mechanism that plants use to combat begomoviruses—one of the most pathogenic groups of plant viruses, causing severe disease in major crops worldwide—is uncovered: plants inhibit the transcription of genes associated with the translational apparatus, thus causing a general reduction in protein synthesis. Novel defence against plant viruses There is something of an 'arms race' between plants and their viral pathogens. Plants mainly tackle viruses through mechanisms that involve RNA silencing. Viruses counter with suppressors, becoming more pathogenic. In turn, plants use both resistance proteins, which trigger immunity in response to viral effector molecules, and innate immunity to limit viral infection. Elizabeth Fontes and colleagues now describe yet another tactic deployed by plants in their battle with viruses. The authors show that in response to infection with begomovirus, Arabidopsis plants inhibit the transcription of genes associated with viral targets within the translational apparatus, thus causing a general reduction in protein synthesis. This work suggests novel strategies that might be used to control begomoviruses, one of the most pathogenic groups of plant viruses and the cause of severe crop infections such as potato yellow mosaic and bean golden yellow mosaic disease. Plants and plant pathogens are subject to continuous co-evolutionary pressure for dominance, and the outcomes of these interactions can substantially impact agriculture and food security 1 , 2 , 3 . In virus–plant interactions, one of the major mechanisms for plant antiviral immunity relies on RNA silencing, which is often suppressed by co-evolving virus suppressors, thus enhancing viral pathogenicity in susceptible hosts 1 . In addition, plants use the nucleotide-binding and leucine-rich repeat (NB-LRR) domain-containing resistance proteins, which recognize viral effectors to activate effector-triggered immunity in a defence mechanism similar to that employed in non-viral infections 2 , 3 . Unlike most eukaryotic organisms, plants are not known to activate mechanisms of host global translation suppression to fight viruses 1 , 2 . Here we demonstrate in Arabidopsis that the constitutive activation of NIK1, a leucine-rich repeat receptor-like kinase (LRR-RLK) identified as a virulence target of the begomovirus nuclear shuttle protein (NSP) 4 , 5 , 6 , leads to global translation suppression and translocation of the downstream component RPL10 to the nucleus, where it interacts with a newly identified MYB-like protein, L10-INTERACTING MYB DOMAIN-CONTAINING PROTEIN (LIMYB), to downregulate translational machinery genes fully. LIMYB overexpression represses ribosomal protein genes at the transcriptional level, resulting in protein synthesis inhibition, decreased viral messenger RNA association with polysome fractions and enhanced tolerance to begomovirus. By contrast, the loss of LIMYB function releases the repression of translation-related genes and increases susceptibility to virus infection. Therefore, LIMYB links immune receptor LRR-RLK activation to global translation suppression as an antiviral immunity strategy in plants.