Molecular Biology and Epidemiology of Dianthoviruses

Okuno, Tetsuro; Hiruki, C.

doi:10.1016/b978-0-12-407698-3.00002-8

Cited by 24 publications

(23 citation statements)

References 163 publications

(193 reference statements)

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“…RNA2 encodes a movement protein that is required for viral cell-to-cell movement. p27 and p88 pol target the endoplasmic reticulum (ER) membranes and form a viral replicase complex with co-opted multiple host factors (24)(25)(26). Among them are host heat shock proteins, small GTPase ADP ribosylation factor 1 (Arf1), and a PA-generating enzyme phospholipase D (PLD) hijacked by RCNMV for robust viral replication (27)(28)(29).…”

Section: Significancementioning

confidence: 99%

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Harnessing host ROS-generating machinery for the robust genome replication of a plant RNA virus

Hyodo

Hashimoto

Kuchitsu

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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As sessile organisms, plants have to accommodate to rapid changes in their surrounding environment. Reactive oxygen species (ROS) act as signaling molecules to transduce biotic and abiotic stimuli into plant stress adaptations. It is established that a respiratory burst oxidase homolog B of Nicotiana benthamiana (NbRBOHB) produces ROS in response to microbe-associated molecular patterns to inhibit pathogen infection. Plant viruses are also known as causative agents of ROS induction in infected plants; however, the function of ROS in plant-virus interactions remains obscure. Here, we show that the replication of red clover necrotic mosaic virus (RCNMV), a plant positive-strand RNA [(+)RNA] virus, requires NbRBOHB-mediated ROS production. The RCNMV replication protein p27 plays a pivotal role in this process, redirecting the subcellular localization of NbRBOHB and a subgroup II calcium-dependent protein kinase of N. benthamiana (NbCDPKiso2) from the plasma membrane to the p27-containing intracellular aggregate structures. p27 also induces an intracellular ROS burst in an RBOH-dependent manner. NbCDPKiso2 was shown to be an activator of the p27-triggered ROS accumulations and to be required for RCNMV replication. Importantly, this RBOH-derived ROS is essential for robust viral RNA replication. The need for RBOHderived ROS was demonstrated for the replication of another (+) RNA virus, brome mosaic virus, suggesting that this characteristic is true for plant (+)RNA viruses. Collectively, our findings revealed a hitherto unknown viral strategy whereby the host ROS-generating machinery is diverted for robust viral RNA replication.positive-strand RNA virus | viral RNA replication | reactive oxygen species | respiratory burst oxidase homolog | calcium-dependent protein kinase P lants have evolved complicated and sophisticated strategies to survive environmental changes. The rapid generation of reactive oxygen species (ROS) is one of the hallmarks of plant responses to various biotic and abiotic stresses (1). Plant NADPH oxidase, termed RBOHs (respiratory burst oxidase homologs), localize at the plasma membrane (PM) and intracellular compartments including the Golgi apparatus (2, 3) and play a key role in ROS production upon the perception of environmental stresses (4). In Nicotiana benthamiana, an RBOHB (NbRBOHB) plays important roles in ROS production triggered by microbe-associated molecular patterns (MAMPs), such as bacterial flagellin and fungal chitin, and facilitates plant immunity against biotrophic pathogens including an oomycete pathogen Phytophthola infestance and tobacco mosaic virus (5-8). RBOH activity is tightly and coordinately regulated posttranslationally [e.g., activation by Ca 2+ , phosphatidic acid (PA), G proteins, or protein kinases] (9-12). It has recently been shown that receptor-like cytoplasmic kinases and calciumdependent protein kinases (CDPKs) regulate RBOHs activity via direct phosphorylation or through modulating regulators of RBOHs during recognition of MAMPs via corresponding surface-loca...

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Section: Significancementioning

confidence: 99%

“…Red clover necrotic mosaic virus (RCNMV) is a plant (+)RNA virus and a member of the genus Dianthovirus in the family Tombusviridae (24). The genome of RCNMV consists of RNA1 and RNA2.…”

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confidence: 99%

Harnessing host ROS-generating machinery for the robust genome replication of a plant RNA virus

Hyodo

Hashimoto

Kuchitsu

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…The genome of RCNMV consists of RNA1 and RNA2. RNA1 encodes a p27 auxiliary replication protein, p88 pol RNA-dependent RNA polymerase (RdRp), and a coat protein [10]. RNA2 encodes a movement protein that is required for viral cell-to-cell movement [10,11].…”

mentioning

confidence: 99%

“…RNA1 encodes a p27 auxiliary replication protein, p88 pol RNA-dependent RNA polymerase (RdRp), and a coat protein [10]. RNA2 encodes a movement protein that is required for viral cell-to-cell movement [10,11]. p27, p88 pol , and host proteins form a 480-kDa replicase complex, which is a key player in the viral RNA replication [12].…”

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confidence: 99%

Phosphatidic Acid Produced by Phospholipase D Promotes RNA Replication of a Plant RNA Virus

et al. 2015

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Eukaryotic positive-strand RNA [(+)RNA] viruses are intracellular obligate parasites replicate using the membrane-bound replicase complexes that contain multiple viral and host components. To replicate, (+)RNA viruses exploit host resources and modify host metabolism and membrane organization. Phospholipase D (PLD) is a phosphatidylcholine- and phosphatidylethanolamine-hydrolyzing enzyme that catalyzes the production of phosphatidic acid (PA), a lipid second messenger that modulates diverse intracellular signaling in various organisms. PA is normally present in small amounts (less than 1% of total phospholipids), but rapidly and transiently accumulates in lipid bilayers in response to different environmental cues such as biotic and abiotic stresses in plants. However, the precise functions of PLD and PA remain unknown. Here, we report the roles of PLD and PA in genomic RNA replication of a plant (+)RNA virus, Red clover necrotic mosaic virus (RCNMV). We found that RCNMV RNA replication complexes formed in Nicotiana benthamiana contained PLDα and PLDβ. Gene-silencing and pharmacological inhibition approaches showed that PLDs and PLDs-derived PA are required for viral RNA replication. Consistent with this, exogenous application of PA enhanced viral RNA replication in plant cells and plant-derived cell-free extracts. We also found that a viral auxiliary replication protein bound to PA in vitro, and that the amount of PA increased in RCNMV-infected plant leaves. Together, our findings suggest that RCNMV hijacks host PA-producing enzymes to replicate.

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“…Although in a different family, it is closely related to the luteoviruses (Miller et al 2002). Unlike the luteoviruses and other tombusvirids, RCNMV has a bipartite genome consisting of genomic RNAs 1 and 2 (Okuno and Hiruki, 2013). Like other tombusvirids and luteoviruses, both of these positive sense RNAs have neither a 5′ cap (Mizumoto et al 2003) nor a poly(A) tail (Lommel et al 1988; Xiong et al 1989).…”

Section: Red Clover Necrotic Mosaic Virus and Other Tombusviridaementioning

confidence: 99%

Noncoding RNAs of Plant Viruses and Viroids: Sponges of Host Translation and RNA Interference Machinery

Miller

Shen

Staplin

et al. 2016

MPMI

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Noncoding sequences in plant viral genomes are well-known to control viral replication and gene expression in cis. However, plant viral and viroid noncoding RNA (ncRNA) sequences can also regulate gene expression acting in trans, often acting like “sponges” that bind and sequester host cellular machinery to favor viral infection. Noncoding sequences of small subgenomic RNAs (sgRNAs) of barley yellow dwarf virus (BYDV) and red clover necrotic mosaic virus (RCNMV) contain a cap-independent translation element that binds translation initiation factor eIF4G. We provide new evidence that an sgRNA of BYDV can globally attenuate host translation, probably by “sponging” eIF4G. Subgenomic ncRNA of RCNMV is generated via 5′ to 3′ degradation by a host exonuclease. The similar noncoding subgenomic flavivirus RNA (sfRNA), inhibits the innate immune response, enhancing viral pathogenesis. Cauliflower mosaic virus transcribes massive amounts of a 600 nt ncRNA, which is processed into small RNAs that overwhelm the host’s RNA interference (RNAi) system. Viroids use the host RNAi machinery to generate viroid-derived ncRNAs that inhibit expression of host defense genes by mimicking a microRNA. More examples of plant viral and viroid ncRNAs are likely to be discovered, revealing fascinating new weaponry in the host-virus arms race.

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Molecular Biology and Epidemiology of Dianthoviruses

Cited by 24 publications

References 163 publications

Harnessing host ROS-generating machinery for the robust genome replication of a plant RNA virus

Harnessing host ROS-generating machinery for the robust genome replication of a plant RNA virus

Phosphatidic Acid Produced by Phospholipase D Promotes RNA Replication of a Plant RNA Virus

Noncoding RNAs of Plant Viruses and Viroids: Sponges of Host Translation and RNA Interference Machinery

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