The UPR Branch IRE1-bZIP60 in Plants Plays an Essential Role in Viral Infection and Is Complementary to the Only UPR Pathway in Yeast

Abstract

The unfolded protein response (UPR) signaling network encompasses two pathways in plants, one mediated by inositol-requiring protein-1 (IRE1)-bZIP60 mRNA and the other by site-1/site-2 proteases (S1P/S2P)-bZIP17/bZIP28. As the major sensor of UPR in eukaryotes, IRE1, in response to endoplasmic reticulum (ER) stress, catalyzes the unconventional splicing of HAC1 in yeast, bZIP60 in plants and XBP1 in metazoans. Recent studies suggest that IRE1p and HAC1 mRNA, the only UPR pathway found in yeast, evolves as a cognate system responsible for the robust UPR induction. However, the functional connectivity of IRE1 and its splicing target in multicellular eukaryotes as well as the degree of conservation of IRE1 downstream signaling effectors across eukaryotes remains to be established. Here, we report that IRE1 and its substrate bZIP60 function as a strictly cognate enzyme-substrate pair to control viral pathogenesis in plants. Moreover, we show that the S1P/S2P-bZIP17/bZIP28 pathway, the other known branch of UPR in plants, does not play a detectable role in virus infection, demonstrating the distinct function of the IRE1-bZIP60 pathway in plants. Furthermore, we provide evidence that bZIP60 and HAC1, products of the enzyme-substrate duet, rather than IRE1, are functionally replaceable to cope with ER stress in yeast. Taken together, we conclude that the downstream signaling of the IRE1-mediated splicing is evolutionarily conserved in yeast and plants, and that the IRE1-bZIP60 UPR pathway not only confers overlapping functions with the other UPR branch in fundamental biology but also may exert a unique role in certain biological processes such as virus-plant interactions.

The Potyvirus Silencing Suppressor Protein VPg Mediates Degradation of SGS3 via Ubiquitination and Autophagy Pathways

“…The sgs3-11 (ABRC stock number CS24289), sgs3-13 (SALK_039005), and sgs3-14 (SALK_001394) mutants were obtained from the Arabidopsis Biological Resource Center (ABRC) at The Ohio State University. Screening for homozygousmutation lines was performed essentially as described previously (78,79). Arabidopsis (ecotype Col-0) plants were transformed by the floral-dip method (80).…”

The unfolded protein response and programmed cell death are induced by expression of Garlic virus X p11 in Nicotiana benthamiana

“…One is mediated by IRE1-bZIP60 and is thought to play an essential role in viral infection, whereas the other is mediated by site-1/site-2 proteases (S1P/S2P)-bZIP17/bZIP18), has a similar function to the animal ATF6 pathway and does not play a detectable role in viral invasion (Deng et al, 2011;Gao et al, 2008;Liu & Howell, 2010;Liu et al, 2007;Nagashima et al, 2011;Zhang et al, 2015). The Turnip mosaic virus (TuMV) membrane-associated 6K2 protein is an inducer of bZIP60 splicing, which is necessary for the function of the UPR branch IRE1-bZIP60 in Arabidopsis (Zhang et al, 2015).…”

“…The Turnip mosaic virus (TuMV) membrane-associated 6K2 protein is an inducer of bZIP60 splicing, which is necessary for the function of the UPR branch IRE1-bZIP60 in Arabidopsis (Zhang et al, 2015). It is known that several of these plant RNA viruses induce the UPR in order to benefit their replication and assembly (Yu et al, 2006;Zhang et al, 2015).…”

“…The Turnip mosaic virus (TuMV) membrane-associated 6K2 protein is an inducer of bZIP60 splicing, which is necessary for the function of the UPR branch IRE1-bZIP60 in Arabidopsis (Zhang et al, 2015). It is known that several of these plant RNA viruses induce the UPR in order to benefit their replication and assembly (Yu et al, 2006;Zhang et al, 2015). The common feature shared by these plant virus-encoded UPR-inducing proteins is their association with lipid membrane or ER, and it is likely that membrane-associating proteins from other plant viruses will also be involved with ER staining of leaf proteins as loading control.…”

Inositol-requiring enzyme 1 affects meristematic division in roots under moderate salt stress in Arabidopsis

“…Some external stimuli such as heat stress, salicylic acid treatment, and viral infection have been reported to activate bZIP60 and bZIP28 (Deng et al 2011;Gao et al 2008;Moreno et al 2012;Nagashima et al 2014;Ye et al 2011;Zhang et al 2015). Furthermore, it was reported that an Arabidopsis mutant defective in both IRE1A and IRE1B genes grown under high temperature contains less viable pollen grains, indicating the importance of the UPR in pollen development under high temperature (Deng et al 2016).…”