Selective autophagy limits cauliflower mosaic virus infection by NBR1-mediated targeting of viral capsid protein and particles

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 114; no. 10; pp. E2026 - E2035
• Main Authors: Hafrén, Anders, Macia, Jean-Luc, Love, Andrew J., Milner, Joel J., Drucker, Martin, Hofius, Daniel
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 07.03.2017
• Series: PNAS Plus
• Subjects: Animals; Aphididae; Aphids - virology; Arabidopsis - genetics; Arabidopsis - immunology; Arabidopsis - virology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - immunology; Arabidopsis thaliana; Autophagy; Autophagy - genetics; Autophagy - immunology; Biological Sciences; Botanik; Botany; Capsid - chemistry; Capsid - metabolism; Capsid Proteins - genetics; Capsid Proteins - metabolism; Carrier Proteins - genetics; Carrier Proteins - immunology; Caulimoviridae; Caulimovirus - genetics; Caulimovirus - growth & development; Cell Biology; Cellbiologi; Deoxyribonucleic acid; DNA; Flowers & plants; Gene Expression Regulation, Plant; Host-Pathogen Interactions; Life Sciences; Microbiology; Microbiology and Parasitology; Mikrobiologi; Pathogenesis; Phytopathology and phytopharmacy; Plant Diseases - genetics; Plant Diseases - immunology; Plant Diseases - virology; Plant Immunity - genetics; PNAS Plus; Proteins; Proteolysis; Signal Transduction; Vegetal Biology; Virion - genetics; Virion - growth & development; Virology; Viruses; xenophagy; innate immunity; cauliflower mosaic virus; selective autophagy; plant virus; maladie virale; maladie des plantes; cauliflower mosaïc virus; camv
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.1610687114

Autophagy plays a paramount role in mammalian antiviral immunity including direct targeting of viruses and their individual components, andmany viruses have evolved measures to antagonize or even exploit autophagy mechanisms for the benefit of infection. In plants, however, the functions of autophagy in host immunity and viral pathogenesis are poorly understood. In this study, we have identified both anti- and proviral roles of autophagy in the compatible interaction of cauliflower mosaic virus (CaMV), a double-stranded DNA pararetrovirus, with the model plant Arabidopsis thaliana. We show that the autophagy cargo receptor NEIGHBOR OF BRCA1 (NBR1) targets nonassembled and virus particle-forming capsid proteins to mediate their autophagy-dependent degradation, thereby restricting the establishment of CaMV infection. Intriguingly, the CaMV-induced virus factory inclusions seem to protect against autophagic destruction by sequestering capsid proteins and coordinating particle assembly and storage. In addition, we found that virus-triggered autophagy prevents extensive senescence and tissue death of infected plants in a largely NBR1-independent manner. This survival function significantly extends the timespan of virus production, thereby increasing the chances for virus particle acquisition by aphid vectors and CaMV transmission. Together, our results provide evidence for the integration of selective autophagy into plant immunity against viruses and reveal potential viral strategies to evade and adapt autophagic processes for successful pathogenesis.