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ARS Home » Midwest Area » Madison, Wisconsin » Vegetable Crops Research » Research » Publications at this Location » Publication #331160
Title: The IRE1/bZIP60 pathway and Bax inhibitor 1 suppress systemic accumulation of potyviruses and potexviruses in Arabidopsis and Nicotiana benthamiana plants

Author
item GAGUANCELA, OMAR - Oklahoma State University
item ZUNIGA, LIZBETH - Oklahoma State University
item ARIAS, ALEXIS - The Army Polytechnic School
item Halterman, Dennis
item FLORES, FRANCISO - The Army Polytechnic School
item JOHANSEN, IDA - University Of Copenhagen
item WANG, AIMING - Southern Crop Protection
item YAMAJI, YASUYUKI - University Of Tokyo
item VERCHOT, JEANMARIE - Oklahoma State University

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/19/2016
Publication Date: 8/31/2016
Citation: Gaguancela, O.A., Zuniga, L.P., Arias, A.V., Halterman, D., Flores, F.J., Johansen, I.E., Wang, A., Yamaji, Y., Verchot, J. 2016. The IRE1/bZIP60 pathway and Bax inhibitor 1 suppress systemic accumulation of potyviruses and potexviruses in Arabidopsis and Nicotiana benthamiana plants. Molecular Plant-Microbe Interactions. 29(10):750-766. doi: 10.1094/MPMI-07-16-0147-R.

Interpretive Summary: The endoplasmic reticulum (ER) and Golgi apparatus comprise a crucial center of the cell for protein synthesis, folding, and transport. The ER itself has multiple functions including calcium storage, protein synthesis, protein folding, membrane lipid synthesis, and cell death regulation. RNA viruses infecting animals and plants depend upon the biosynthetic and transport properties of the ER-Golgi network for success in replication and completion of their infection cycles. In this study we wanted to broadly characterize the role of genes involved in virus-induced stress using a genetic approach that includes several viruses and several host plants. This study provides a comparative analysis of four viruses to examine the role of the ER regulation pathway in virus infection. In addition, we look more closely at the role of cell death regulation at the ER by studying changes in gene expression in response to virus infection. We report very different patterns of virus infection in response to changes in expression suggesting that vital ER stress regulators monitor virus infection.

Technical Abstract: The inositol requiring enzyme (IRE1) is an endoplasmic reticulum (ER) stress sensor and when activated it splices the bZIP60 mRNA producing a truncated transcription factor that upregulates expression of genes involved in the unfolded protein response (UPR). Bax inhibitor 1 (BI-1) is another ER stress sensor that regulates cell death in response to environmental assaults. The potyvirus 6K2 and potexvirus TGB3 proteins are known to reside in the ER, serving respectively as anchors for the viral replicase and movement protein complex. This study used GFP tagged Turnip mosaic virus (TuMV), Plantago asiatica mosaic virus (PlAMV), Potato virus Y (PVY) and Potato virus X (PVX) to study changes in bZIP60 and BI-1 expression in Arabidopsis thaliana, Nicotiana benthamiana, and Solanum tuberosum. Both genes were induced early in virus infection. In addition, agro-delivery of only the potyvirus 6K2 or TGB3 genes into plant cells activated bZIP60 and BI-1 expression in Arabidopsis thaliana, Nicotiana benthamiana, and Solanum tuberosum. Homozygous ire1a-2, ire1b-4, and ire1a- 2/ire1b-4 mutant Arabidopsis were inoculated with TuMV-GFP or PlAMV-GFP. PlAMV accumulates to a higher level in ire1a-2 or ire1a-2/ire1b-4 mutant plants than in ire1b-4 or wild-type plants. TuMV-GFP accumulates to a higher level in ire1a-2, ire1b-4, or ire1a-2/ire1b-4 compared to wild type plants suggesting that both isoforms contribute to TuMV-GFP infection. Gene silencing was used to knockdown bZIP60 and BI-1 expression in N. benthamiana. PVX-GFP and PVY-GFP accumulation was significantly elevated in these silenced plants compared to control plants. This study demonstrates that two ER stress pathways, namely IRE1/bZIP60 and the BI-1 pathway limit systemic accumulation of potyvirus and potexvirus infection. Silencing BI-1 expression also resulted in systemic necrosis. These data suggest that ER stress activated pathways led by IRE1 and BI-1 respond to invading potyvirus and potexviruses to restricts virus infection and enable physiological changes enabling plants to tolerate virus assault.