The IRE1/bZIP60 Pathway and Bax Inhibitor 1 Suppress Systemic Accumulation of Potyviruses and Potexviruses in Arabidopsis and Nicotiana benthamiana Plants
The inositol requiring enzyme (IRE1) is an endoplasmic reticulum (ER) stress sensor. When activated, it splices the bZIP60 mRNA, producing a truncated transcription factor that upregulates genes involved in the unfolded protein response. Bax inhibitor 1 (BI-1) is another ER stress sensor that regula...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
The American Phytopathological Society
2016-10-01
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| Series: | Molecular Plant-Microbe Interactions |
| Online Access: | https://apsjournals.apsnet.org/doi/10.1094/MPMI-07-16-0147-R |
| _version_ | 1818647219626049536 |
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| author | Omar Arias Gaguancela Lizbeth Peña Zúñiga Alexis Vela Arias Dennis Halterman Francisco Javier Flores Ida Elisabeth Johansen Aiming Wang Yasuyuki Yamaji Jeanmarie Verchot |
| author_facet | Omar Arias Gaguancela Lizbeth Peña Zúñiga Alexis Vela Arias Dennis Halterman Francisco Javier Flores Ida Elisabeth Johansen Aiming Wang Yasuyuki Yamaji Jeanmarie Verchot |
| author_sort | Omar Arias Gaguancela |
| collection | DOAJ |
| description | The inositol requiring enzyme (IRE1) is an endoplasmic reticulum (ER) stress sensor. When activated, it splices the bZIP60 mRNA, producing a truncated transcription factor that upregulates genes involved in the unfolded protein response. 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 green fluorescent protein (GFP)-tagged Turnip mosaic virus (TuMV), Plantago asiatica mosaic virus (PlAMV), Potato virus Y (PVY), and Potato virus X (PVX) to determine that the IRE1/bZIP60 pathway and BI-1 machinery are induced early in virus infection in Arabidopsis thaliana, Nicotiana benthamiana, and Solanum tuberosum. Agrodelivery of only the potyvirus 6K2 or TGB3 genes into plant cells activated bZIP60 and BI-1 expression in Arabidopsis thaliana, N. benthamiana, and S. tuberosum. Homozygous ire1a-2, ire1b-4, and ire1a-2/ire1b-4 mutant Arabidopsis plants 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 with wild-type plants, suggesting that both isoforms contribute to TuMV-GFP infection. Gene silencing was used to knock down bZIP60 and BI-1 expression in N. benthamiana. PVX-GFP and PVY-GFP accumulation was significantly elevated in these silenced plants compared with 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 restrict virus infection and enable physiological changes enabling plants to tolerate virus assault. |
| first_indexed | 2024-12-17T00:59:03Z |
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| id | doaj.art-52f7305970ef486491366a39c5a57361 |
| institution | Directory Open Access Journal |
| issn | 0894-0282 1943-7706 |
| language | English |
| last_indexed | 2024-12-17T00:59:03Z |
| publishDate | 2016-10-01 |
| publisher | The American Phytopathological Society |
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| series | Molecular Plant-Microbe Interactions |
| spelling | doaj.art-52f7305970ef486491366a39c5a573612022-12-21T22:09:31ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062016-10-01291075076610.1094/MPMI-07-16-0147-RThe IRE1/bZIP60 Pathway and Bax Inhibitor 1 Suppress Systemic Accumulation of Potyviruses and Potexviruses in Arabidopsis and Nicotiana benthamiana PlantsOmar Arias Gaguancela0Lizbeth Peña Zúñiga1Alexis Vela Arias2Dennis Halterman3Francisco Javier Flores4Ida Elisabeth Johansen5Aiming Wang6Yasuyuki Yamaji7Jeanmarie Verchot8Department of Entomology & Plant Pathology, Oklahoma State University, Stillwater, OK 74078, U.S.A.;Department of Entomology & Plant Pathology, Oklahoma State University, Stillwater, OK 74078, U.S.A.;Departamento de Ciencias de la Vida y la Agricultura, Universidad de las Fuerzas Armadas-ESPE, Av. General Rumiñahui s/n, Sangolquí, Pichincha, Ecuador;Agricultural Research Service, Vegetable Crops Research Unit, U.S. Department of Agriculture ARS, Madison, WI, U.S.A.;Departamento de Ciencias de la Vida y la Agricultura, Universidad de las Fuerzas Armadas-ESPE, Av. General Rumiñahui s/n, Sangolquí, Pichincha, Ecuador;Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark;Southern Crop Protection and Food Research Centre, AAFC, 1391 Sandford Street, London, Ontario N5V 4T3, Canada; andLaboratory of Plant Pathology, Department of Agricultural and Environmental Biology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, JapanDepartment of Entomology & Plant Pathology, Oklahoma State University, Stillwater, OK 74078, U.S.A.;The inositol requiring enzyme (IRE1) is an endoplasmic reticulum (ER) stress sensor. When activated, it splices the bZIP60 mRNA, producing a truncated transcription factor that upregulates genes involved in the unfolded protein response. 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 green fluorescent protein (GFP)-tagged Turnip mosaic virus (TuMV), Plantago asiatica mosaic virus (PlAMV), Potato virus Y (PVY), and Potato virus X (PVX) to determine that the IRE1/bZIP60 pathway and BI-1 machinery are induced early in virus infection in Arabidopsis thaliana, Nicotiana benthamiana, and Solanum tuberosum. Agrodelivery of only the potyvirus 6K2 or TGB3 genes into plant cells activated bZIP60 and BI-1 expression in Arabidopsis thaliana, N. benthamiana, and S. tuberosum. Homozygous ire1a-2, ire1b-4, and ire1a-2/ire1b-4 mutant Arabidopsis plants 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 with wild-type plants, suggesting that both isoforms contribute to TuMV-GFP infection. Gene silencing was used to knock down bZIP60 and BI-1 expression in N. benthamiana. PVX-GFP and PVY-GFP accumulation was significantly elevated in these silenced plants compared with 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 restrict virus infection and enable physiological changes enabling plants to tolerate virus assault.https://apsjournals.apsnet.org/doi/10.1094/MPMI-07-16-0147-R |
| spellingShingle | Omar Arias Gaguancela Lizbeth Peña Zúñiga Alexis Vela Arias Dennis Halterman Francisco Javier Flores Ida Elisabeth Johansen Aiming Wang Yasuyuki Yamaji Jeanmarie Verchot 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 |
| title | The IRE1/bZIP60 Pathway and Bax Inhibitor 1 Suppress Systemic Accumulation of Potyviruses and Potexviruses in Arabidopsis and Nicotiana benthamiana Plants |
| title_full | The IRE1/bZIP60 Pathway and Bax Inhibitor 1 Suppress Systemic Accumulation of Potyviruses and Potexviruses in Arabidopsis and Nicotiana benthamiana Plants |
| title_fullStr | The IRE1/bZIP60 Pathway and Bax Inhibitor 1 Suppress Systemic Accumulation of Potyviruses and Potexviruses in Arabidopsis and Nicotiana benthamiana Plants |
| title_full_unstemmed | The IRE1/bZIP60 Pathway and Bax Inhibitor 1 Suppress Systemic Accumulation of Potyviruses and Potexviruses in Arabidopsis and Nicotiana benthamiana Plants |
| title_short | The IRE1/bZIP60 Pathway and Bax Inhibitor 1 Suppress Systemic Accumulation of Potyviruses and Potexviruses in Arabidopsis and Nicotiana benthamiana Plants |
| title_sort | ire1 bzip60 pathway and bax inhibitor 1 suppress systemic accumulation of potyviruses and potexviruses in arabidopsis and nicotiana benthamiana plants |
| url | https://apsjournals.apsnet.org/doi/10.1094/MPMI-07-16-0147-R |
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