Selective autophagic receptor NbNBR1 prevents NbRFP1-mediated UPS-dependent degradation of βC1 to promote geminivirus infection.

Tingting Zhou,Mingzhen Zhang,Pan Gong,Fangfang Li,Xueping Zhou,David M Bisaro

doi:10.1371/journal.ppat.1009956

Abstract

Autophagy is an evolutionarily conserved, lysosomal/vacuolar degradation mechanism that targets cell organelles and macromolecules. Autophagy and autophagy-related genes have been studied for their antiviral and pro-viral roles in virus-infected plants. Here, we demonstrate the pro-viral role of a selective autophagic receptor NbNBR1 in geminivirus-infected Nicotiana benthamiana plants. The βC1 protein encoded by tomato yellow leaf curl China betasatellite (TYLCCNB) that is associated with tomato yellow leaf curl China virus (TYLCCNV) enhanced the expression level of NbNBR1. Then NbNBR1 interacted with βC1 to form cytoplasmic granules. Interaction of NbNBR1 with βC1 could prevent degradation of βC1 by the NbRFP1, an E3 ligase. Overexpression of NbNBR1 in N. benthamiana plants increased βC1 accumulation and promoted virus infection. In contrast, silencing or knocking out NbNBR1 expression in N. benthamiana suppressed βC1 accumulation and inhibited virus infection. A single amino acid substitution in βC1 (βC1K4A) abolished its interaction with NbNBR1, leading to a reduced level of βC1K4A. The TYLCCNV/TYLCCNBK4A mutant virus caused milder disease symptoms and accumulated much less viral genomic DNAs in the infected plants. Collectively, the results presented here show how a viral satellite-encoded protein hijacks host autophagic receptor NbNBR1 to form cytoplasmic granules to protect itself from NbRFP1-mediated degradation and facilitate viral infection.

Highlights

Autophagy, originated from a Greek word describing self-eating [1], is an evolutionary conserved degradation pathway that targets macromolecules, organelles and/or pathogens [2]
We provide new evidence to show that βC1 encoded by tomato yellow leaf curl China betasatellite (TYLCCNB) that is associated with tomato yellow leaf curl China virus (TYLCCNV) can modulate plant defense against geminivirus infection
This study demonstrates a distinct mechanism of a viral satellite-encoded protein exploits the autophagy protein NbNBR1 to the cytoplasmic granules, to prevent the NbRFP1-mediated degradation and highlight an important role for NbNBR1 in geminivirus infection

Summary

Introduction

Autophagy, originated from a Greek word describing self-eating [1], is an evolutionary conserved degradation pathway that targets macromolecules, organelles and/or pathogens [2]. Autophagosomes are double membrane-bound vesicles formed through a series of steps, and are important components involved in the autophagy pathway. These membrane-bound vesicles fuse to host cell vacuoles (yeast and plants) or lysosomes (mammals) to deliver cargos for proteolytic degradation and monomer recycling. More and more reports have shown that autophagy operates in selective ways via selective autophagic cargo adaptors [4]. Beclin (ATG6) has been shown as a new selective plant autophagy receptor that can mediate autophagic degradation and inhibit the replication and infection of turnip mosaic virus (TuMV) through interaction with viral RNA-dependent RNA polymerase NIb [7]

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Discussion

Conclusion