Harnessing host ROS-generating machinery for the robust genome replication of a plant RNA virus.
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 ofNicotiana 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 ofN. 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 RBOH-derived 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.
Institute of Plant Science and Resources, Okayama University, Kurashiki, Okayama 710-0046, Japan; khyodo@okayama-u.ac.jp okuno@agr.ryukoku.ac.jp.
Kiwamu
0000-0003-3849-7975
K
Hyodo
Department of Applied Biological Science, Tokyo University of Science, 2641 Yamazaki, Noda 278-8510, Japan.
Kenji
K
Hashimoto
Department of Applied Biological Science, Tokyo University of Science, 2641 Yamazaki, Noda 278-8510, Japan.|Imaging Frontier Center, Tokyo University of Science, 2641 Yamazaki, Noda 278-8510, Japan.
Kazuyuki
K
Kuchitsu
Institute of Plant Science and Resources, Okayama University, Kurashiki, Okayama 710-0046, Japan.
Nobuhiro
N
Suzuki
Laboratory of Plant Pathology, Graduate School of Agriculture, Kyoto University, Sakyo-ku, Kyoto 606-8502, Japan; khyodo@okayama-u.ac.jp okuno@agr.ryukoku.ac.jp.|Department of Plant Life Science, Faculty of Agriculture, Ryukoku University, Seta, Otsu 520-2194, Japan.
Tetsuro
T
Okuno
D016679:Genome, Viral / Q000235:genetics*; D054884:Host-Pathogen Interactions; D019255:NADPH Oxidases / Q000378:metabolism; D010940:Plant Proteins / Q000378:metabolism; D010942:Plant Viruses / Q000235:genetics* / Q000502:physiology; D011494:Protein Kinases / Q000378:metabolism; D012328:RNA Viruses / Q000235:genetics* / Q000502:physiology; D012367:RNA, Viral / Q000235:genetics; D017382:Reactive Oxygen Species / Q000378:metabolism*; D014026:Nicotiana / Q000378:metabolism / Q000821:virology; D019183:Tombusviridae / Q000235:genetics / Q000502:physiology; D014779:Virus Replication / Q000235:genetics*; D017871:Calcium-Calmodulin-Dependent Protein Kinases
D019255:NADPH Oxidases; D010940:Plant Proteins; D011494:Protein Kinases; D012367:RNA, Viral; D017382:Reactive Oxygen Species; D017871:Calcium-Calmodulin-Dependent Protein Kinases; C022709:superoxide-forming enzyme
calcium-dependent protein kinase; positive-strand RNA virus; reactive oxygen species; respiratory burst oxidase homolog; viral RNA replication