Soybean antiviral immunity conferred by dsRNase targets the viral replication complex

Kazuhiro Ishibashi,Yuichi Katayose,Toyoaki Anai,Akito Kaga,Naohiro Yamada,Masao Ishimoto,Takehiko Shimizu,Masayasu Saruta,Masayuki Ishikawa,Kunihiko Komatsu,Miao Shu

doi:10.1038/s41467-019-12052-5

Abstract

Eukaryotic positive-strand RNA viruses replicate their genomes in membranous compartments formed in a host cell, which sequesters the dsRNA replication intermediate from antiviral immune surveillance. Here, we find that soybean has developed a way to overcome this sequestration. We report the positional cloning of the broad-spectrum soybean mosaic virus resistance gene Rsv4, which encodes an RNase H family protein with dsRNA-degrading activity. An active-site mutant of Rsv4 is incapable of inhibiting virus multiplication and is associated with an active viral RNA polymerase complex in infected cells. These results suggest that Rsv4 enters the viral replication compartment and degrades viral dsRNA. Inspired by this model, we design three plant-gene-derived dsRNases that can inhibit the multiplication of the respective target viruses. These findings suggest a method for developing crops resistant to any target positive-strand RNA virus by fusion of endogenous host genes.

Highlights

Eukaryotic positive-strand RNA viruses replicate their genomes in membranous compartments formed in a host cell, which sequesters the dsRNA replication intermediate from antiviral immune surveillance
A 3.6-kbp deletion was found in this region of the Peking genome, and only a single open reading frames (ORFs) that encodes a 259-amino-acid protein was found (Fig. 1a, Supplementary Fig. 1)
The geographical distribution of the 3.6-kbp insertion/deletion in soybean and Glycine soja shown in Fig. 3 suggests that genetic variation of this chromosome region was reduced during expansion of soybean outside its probable areas of domestication (China and Korea)

Summary

Introduction

Eukaryotic positive-strand RNA viruses replicate their genomes in membranous compartments formed in a host cell, which sequesters the dsRNA replication intermediate from antiviral immune surveillance. An active-site mutant of Rsv[4] is incapable of inhibiting virus multiplication and is associated with an active viral RNA polymerase complex in infected cells These results suggest that Rsv[4] enters the viral replication compartment and degrades viral dsRNA. We design three plant-gene-derived dsRNases that can inhibit the multiplication of the respective target viruses These findings suggest a method for developing crops resistant to any target positive-strand RNA virus by fusion of endogenous host genes. 7 Advanced Genomics Breeding Section, Institute of Crop Science, National Agriculture and Food Research Organization, 1-2 Ohwashi, Tsukuba, Ibaraki 305-8634, Japan. To protect from potyviruses, resistance genes have been introduced into many crop cultivars such as potato[5], pepper[6], papaya[7], plum[8], Brassica crops[9], and legumes[10]

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Conclusion