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Viral-Induced Systemic Necrosis in Plants Involves Both Programmed Cell Death and the Inhibition of Viral Multiplication, Which Are Regulated by Independent Pathways

March 2010 , Volume 23 , Number  3
Pages  283 - 293

Ken Komatsu,1 Masayoshi Hashimoto,1 Johji Ozeki,1 Yasuyuki Yamaji,1 Kensaku Maejima,1 Hiroko Senshu,1 Misako Himeno,1 Yukari Okano,1 Satoshi Kagiwada,2 and Shigetou Namba1

1Laboratory of Plant Pathology, Department of Agricultural and Environmental Biology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan; 2Department of Clinical Plant Science, Faculty of Bioscience and Applied Chemistry, Hosei University, Koganei, Tokyo, Japan

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Accepted 20 October 2009.

Resistant plants respond rapidly to invading avirulent plant viruses by triggering a hypersensitive response (HR). An HR is accompanied by a restraint of virus multiplication and programmed cell death (PCD), both of which have been observed in systemic necrosis triggered by a successful viral infection. Here, we analyzed signaling pathways underlying the HR in resistance genotype plants and those leading to systemic necrosis. We show that systemic necrosis in Nicotiana benthamiana, induced by Plantago asiatica mosaic virus (PlAMV) infection, was associated with PCD, biochemical features, and gene expression patterns that are characteristic of HR. The induction of necrosis caused by PlAMV infection was dependent on SGT1, RAR1, and the downstream mitogen-activated protein kinase (MAPK) cascade involving MAPKKKα and MEK2. However, although SGT1 and RAR1 silencing led to an increased accumulation of PlAMV, silencing of the MAPKKKα-MEK2 cascade did not. This observation indicates that viral multiplication is partly restrained even in systemic necrosis induced by viral infection, and that this restraint requires SGT1 and RAR1 but not the MAPKKKα-MEK2 cascade. Similarly, although both SGT1 and MAPKKKα were essential for the Rx-mediated HR to Potato virus X (PVX), SGT1 but not MAPKKKα was involved in the restraint of PVX multiplication. These results suggest that systemic necrosis and HR consist of PCD and a restraint of virus multiplication, and that the latter is induced through unknown pathways independent from the former.

© 2010 The American Phytopathological Society