The IRE1/bZIP60 Pathway and Bax Inhibitor 1 Suppress Systemic Accumulation of Potyviruses and Potexviruses in Arabidopsis and Nicotiana benthamiana Plants

Abstract

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.

Cell death triggered by the P25 protein in Potato virus X‐associated synergisms results from endoplasmic reticulum stress in Nicotiana benthamiana

“…These data indicate that UPR partially restricts PVX infection in N. benthamiana , as has been reported by others at the local level using bZIP60‐silenced plants (Arias Gaguancela et al. , ). However, other examples support the idea that UPR facilitates virus infection.…”

“…However, bZIP60 silencing did not induce necrosis in PVX‐infected plants (Arias Gaguancela et al. , ). In addition, the TGB3 protein elicited PCD when expressed either from the Tobacco mosaic virus (TMV) genome or from the Cauliflower mosaic virus (CaMV) 35S promoter (Ye et al.…”

AtIRE1C, an unconventional isoform of the UPR master regulator AtIRE1, is functionally associated with AtIRE1B in Arabidopsis gametogenesis

“…Although our data show that IRE1C is localized to the ER, the absence of a lumenal sensor domain, which is present in the other IRE1 isoforms, raises the question on whether IRE1C may function in the UPR trigged by ER stress. The remaining low levels of bZIP60 mRNA splicing in the ire1a ire1b mutant in both this study and previous work on the UPR (Angelos & Brandizzi, 2018;Chen & Brandizzi, 2012;Gaguancela et al, 2016) prompted us to test whether this may be due to IRE1C. Our data showed that both IRE1A and IRE1B had nearly no ribonuclease domain expressed in the ire1a ire1b mutant and therefore support the hypothesis that IRE1C may have ribonuclease activity.…”

Comparative transcriptome profiling uncovers a Lilium regale NAC transcription factor, LrNAC35, contributing to defence response against cucumber mosaic virus and tobacco mosaic virus

“…Numerous virus‐responsive genes have essential roles in the innate immunity system, such as the resistance ( R ) gene (Kang et al , ), tobacco N gene (Marathe et al , ; Whitham et al , ), and the genes associated with RNA silencing (Agius et al ., ; Sun et al , ) and translation suppression (Zorzatto et al , ). The transcription of these genes is potentially controlled by specific transcription factors (TFs), of which many members of various families, including MYB (Yang and Klessig, ), zinc finger (Guo et al , ), WRKY (Park et al , ), AP2/ERF (Huang et al , ), bZIP (Gaguancela et al , ), bHLH (Aparicio and Pallás, ) and NAC (Huang et al , ), have been revealed to be implicated in the response to viral stimuli. In particular, NAC domain‐containing proteins comprise a large TF family in plants and play essential roles in plant growth, development and stress responses (Puranik et al , ).…”