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; Chen, Hui; Brandizzi, Federica; Verchot, Jeanmarie; Wang, Aiming

doi:10.1371/journal.pgen.1005164

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

Journal Article · Wed Apr 15 00:00:00 EDT 2015 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1005164· OSTI ID:1904889

Zhang, Lingrui ^[1]; Chen, Hui ^[2]; Brandizzi, Federica ^[3]; Verchot, Jeanmarie ^[4]; Wang, Aiming ^[2]

Agriculture and Agri-Food Canada, London, ON (Canada). Southern Crop Protection and Food Research; OSTI
Agriculture and Agri-Food Canada, London, ON (Canada). Southern Crop Protection and Food Research
Michigan State University, East Lansing, MI (United States).
Oklahoma State University, Stillwater, OK (United States)

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 enzymesubstrate 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.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge Inst. for Science and Education (ORISE), Oak Ridge, TN (United States)

Sponsoring Organization:: National Institutes of Health (NIH); Natural Sciences and Engineering Research Council of Canada (NSERC); US Department of Agriculture (USDA); USDOE Office of Science (SC)

Grant/Contract Number:: SC0014664

OSTI ID:: 1904889

Journal Information:: PLoS Genetics, Journal Name: PLoS Genetics Journal Issue: 4 Vol. 11; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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