The Crucial Role of Chloroplast-Related Proteins in Viral Genome Replication and Host Defense against Positive-Sense Single-Stranded RNA Viruses

Abstract

Plant viruses are responsible for worldwide production losses of numerous economically important crops. The most common plant RNA viruses are positivesense single-stranded RNA viruses [(+)ss RNA viruses]. These viruses have small genomes that encode a limited number of proteins. The viruses depend on their host's machinery for the replication of their RNA genome, assembly, movement, and attraction to the vectors for dispersal. Recently researchers have reported that chloroplast proteins are crucial for replicating (+)ss plant RNA viruses. Some chloroplast proteins, including translation initiation factor [eIF(iso)4E] and 75 DEAD-box RNA helicase RH8, help viruses fulfill their infection cycle in plants. In contrast, other chloroplast proteins such as PAP2.1, PSaC, and ATPsyn-α play active roles in plant defense against viruses. This is also consistent with the idea that reactive oxygen species, salicylic acid, jasmonic acid, and abscisic acid are produced in chloroplast. However, knowledge of molecular mechanisms and functions underlying these chloroplast host factors during the virus infection is still scarce and remains largely unknown. Our review briefly summarizes the latest knowledge regarding the possible role of chloroplast in plant virus replication, emphasizing chloroplast-related proteins. We have highlighted current advances regarding chloroplast-related proteins' role in replicating plant (+)ss RNA viruses.

Keywords: chloroplast; chloroplast-virus interactions; plant defense; viral replication complex; virus replication.

Fig. 1

Schematic representation of necessary steps for positive-sense single-stranded RNA [(+)ss RNA] virus genome replication. Following the entry into host cells, (1) viral genomic RNAs are released from virions into the cytoplasm, and (2) viral RNA [(+)ss RNA] translates RNA-dependent RNA polymerase (RdRp) at the early stage of infection and recruits additional factors (such as methyltransferase and chaperone). (3) The resulting viral replication proteins target themselves to recruit the host translation machinery for the successful production of viral replication proteins. (4) The recruited viral genomic (+) RNAs and host proteins are then trafficked to chloroplast membranes, where they assemble viral replication complexes (VRCs) on the host chloroplast membrane. VRCs are shown by an invagination of the plant chloroplast membrane containing the viral protein (blue shape), the viral RdRP (red shape), host proteins (green shape), and viral RNA (red line). The VRC synthesizes a complementary negative-strand RNA (green line) using the original (+)RNA as a template. The (−) RNA is then used as a template to synthesize many new (+) RNAs (red lines). Progeny viruses are released from VRCs, undergo additional translation and replication, or move to adjacent cells.

Fig. 2

Schematic representation of the important events during chloroplast host factors and potyvirus interactions in a plant cell. After entry into host plant cells, a potyvirus virion undergoes the disassembly of viral particles and releases the viral genome. Viral genomic RNA is then used as the template for translation to produce viral polyproteins (11 viral proteins indicated by grey squares). The 6K2 remodels the subcellular membranes to form the viral replication complexe (VRC)-containing vesicles for potyvirus genome replication. The 6K2-induced vesicles may subsequently target chloroplasts for robust viral replication. The NIb is recruited to the VRC, likely via its interaction with the VPg domain of 6K2–VPg-Pro. Then, NIb recruits many host factors, such as eEF1A, PSaC, and ATP-synthase α-subunit. In the figure, each viral protein is represented by a grey color-coded square in a location where they play a crucial role. A light blue color-coded semi-circle indicates chloroplast-related host proteins identified for virus infection. They are depicted in sites where they interact with viral protein or play a crucial role.