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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.

SUBMITTER: Zhang L

PROVIDER: S-EPMC4398384 | biostudies-literature | 2015 Apr

REPOSITORIES: biostudies-literature

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The UPR branch IRE1-bZIP60 in plants plays an essential role in viral infection and is complementary to the only UPR pathway in yeast.

Zhang Lingrui L Chen Hui H Brandizzi Federica F Verchot Jeanmarie J Wang Aiming A

PLoS genetics 20150415 4

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, ...[more]

PMID: 25875739

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Project description:Endoplasmic reticulum (ER)-mediated protein secretion and quality control have been shown to play an important role in immune responses in both animals and plants. In mammals, the ER membrane-located IRE1 kinase/endoribonuclease, a key regulator of unfolded protein response (UPR), is required for plasma cell development to accommodate massive secretion of immunoglobulins. Plant cells can secrete the so-called pathogenesis-related (PR) proteins with antimicrobial activities upon pathogen challenge. However, whether IRE1 plays any role in plant immunity is not known. Arabidopsis thaliana has two copies of IRE1, IRE1a and IRE1b. Here, we show that both IRE1a and IRE1b are transcriptionally induced during chemically-induced ER stress, bacterial pathogen infection and treatment with the immune signal salicylic acid (SA). However, we found that IRE1a plays a predominant role in the secretion of PR proteins upon SA treatment. Consequently, the ire1a mutant plants show enhanced susceptibility to a bacterial pathogen and are deficient in establishing systemic acquired resistance (SAR), whereas ire1b is unaffected in these responses. We further demonstrate that the immune deficiency in ire1a is due to a defect in SA- and pathogen-triggered, IRE1-mediated cytoplasmic splicing of the bZIP60 mRNA, which encodes a transcription factor involved in the expression of UPR-responsive genes. Consistently, IRE1a is preferentially required for bZIP60 splicing upon pathogen infection, while IRE1b plays a major role in bZIP60 processing upon Tunicamycin (Tm)-induced stress. We also show that SA-dependent induction of UPR-responsive genes is altered in the bzip60 mutant resulting in a moderate susceptibility to a bacterial pathogen. These results indicate that the IRE1/bZIP60 branch of UPR is a part of the plant response to pathogens for which the two Arabidopsis IRE1 isoforms play only partially overlapping roles and that IRE1 has both bZIP60-dependent and bZIP60-independent functions in plant immunity.

Project description:As an endoplasmic reticulum (ER) stress sensor, inositol-requiring enzyme 1 (IRE1) splices the bZIP60 mRNA, and produces an active bZIP60 transcription factor that regulates genes involved in the unfolded protein response (UPR) during ER stresses. This IRE1-bZIP60 pathway is conserved in plant species and recently implicated in plant-pathogen interaction. However, it is unclear whether this IRE1-bZIP60 pathway is involved in Nicotiana attenuata resistance to necrotic fungal pathogen, Alternaria alternata. In this study, transcriptional levels of chaperone protein genes, including luminal binding protein (BiP), protein disulfide isomerase (PDI), calnexin 1-like (CNX 1-like), and calreticulin (CRT), and genes involved in IRE1-bZIP60 pathway, were all significantly induced in N. attenuata leaves after A. alternata inoculation. Silencing IRE1 or bZIP60 led to N. attenuata plants more susceptible to A. alternata, which were associated with reduced gene expressions of Feruloyl-CoA 6'-hydroxylase 1 (F6'H1), a gene encoding a key enzyme for phytoalexin scopoletin and scopolin biosynthesis. Further, electromobility shift assays (EMSA) indicated that bZIP60 protein of spliced form could directly bind to the promoter region of F6'H1 in vitro. JA signaling pathway is required for N. attenuata resistance to A. alternata. Interestingly, the fungus-elicited transcriptional levels of BiP, PDI, CNX 1-like, CRT, IRE1, and bZIP60(s) were all significantly decreased in JA-deficient or JA-insensitive plants. Meanwhile, those genes were significantly induced by methyl jasmonate (MeJA) when applied exogenously. However, the transcriptional levels of JA-regulated genes allene oxide synthase (AOS) and lipoxygenease 3 (LOX3) were not affected in plants impaired with IRE1-bZIP60 pathway. Thus, it is concluded that IRE1-bZIP60 pathway is required for N. attenuata resistance to A. alternata, and JA signaling pathway plays an important role in the elicitation of chaperone protein genes and IRE1-bZIP60 pathway.

Dataset Information

The UPR branch IRE1-bZIP60 in plants plays an essential role in viral infection and is complementary to the only UPR pathway in yeast.

Publications

The UPR branch IRE1-bZIP60 in plants plays an essential role in viral infection and is complementary to the only UPR pathway in yeast.

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