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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.

IRE1-bZIP60 Pathway Is Required for Nicotiana attenuata Resistance to Fungal Pathogen Alternaria alternata