title: 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.
authors: Southern Crop Protection and Food Research, Agriculture and Agri-Food Canada, London, Ontario, Canada.
authors: Lingrui
authors: L
authors: Zhang
authors: Southern Crop Protection and Food Research, Agriculture and Agri-Food Canada, London, Ontario, Canada.
authors: Hui
authors: H
authors: Chen
authors: Department of Energy Plant Research Laboratory and Department of Plant Biology, Michigan State University, East Lansing, Michigan, USA.
authors: Federica
authors: F
authors: Brandizzi
authors: Department of Entomology and Plant Pathology, Oklahoma State University, Stillwater, Oklahoma, United States of America.
authors: Jeanmarie
authors: J
authors: Verchot
authors: Southern Crop Protection and Food Research, Agriculture and Agri-Food Canada, London, Ontario, Canada.
authors: Aiming
authors: A
authors: Wang
mesh_terms: D000595:Amino Acid Sequence; D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism* / Q000821:virology; D029681:Arabidopsis Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D053502:Arsenate Reductases / Q000235:genetics / Q000378:metabolism; D050976:Basic-Leucine Zipper Transcription Factors / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D054884:Host-Pathogen Interactions; D008969:Molecular Sequence Data; D011494:Protein Kinases / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D012326:RNA Splicing; D012441:Saccharomyces cerevisiae / Q000235:genetics / Q000378:metabolism*; D015398:Signal Transduction; D017806:Tymovirus / Q000472:pathogenicity*; D056811:Unfolded Protein Response
chemical_list: D029681:Arabidopsis Proteins; D053502:Arsenate Reductases; D050976:Basic-Leucine Zipper Transcription Factors; D011494:Protein Kinases; C000599715:HAC1 (HIGH ARSENIC CONTENT 1) protein, Arabidopsis; C446527:Ire1-1 protein, Arabidopsis