Abiotic and biotic stress activate the unfolded protein response in grapevine, with IRE1/bZIP60 signaling contributing to Botrytis cinerea resistance

Abstract

A wide range of stresses can lead to the accumulation of unfolded or misfolded proteins in the lumen of the endoplasmic reticulum (ER), a condition known as ER stress. To restore proteostasis, eukaryotic cells activate a signaling network called the unfolded protein response (UPR). In Vitis vinifera, two arms of the UPR have been identified: the IRE1/bZIP60 arm and the bZIP17 arm. Notably, no putative ortholog of bZIP28 has been found in V. vinifera, whereas this is the case for Arabidopsis thaliana. We demonstrated that VvbZIP60 mRNA undergoes unconventional splicing upon treatment with dithiothreitol (DTT) and tunicamycin (TM), both classical ER stress inducers. In addition, inhibition of IRE1 RNase activity directly decreases IRE1-bZIP60-related gene expression. We observed a strong transcriptional activation of UPR-related genes in response to heat stress which induced the re-localization of both VvbZIPs to the nucleus. Surprisingly, only VvbZIP17 responded to osmotic stresses. Grapevine is also subject to a broad range of microbial challenges, including pathogens such as Plasmopara viticola and Botrytis cinerea. Both pathogens triggered UPR genes activation in grapevine leaves. Interestingly, inhibition of IRE1 RNase activity induced higher susceptibility to B. cinerea. Collectively, these findings suggest that the IRE1/bZIP60 and bZIP17 arms of the UPR are not only structurally conserved in grapevine but are also transcriptionally responsive to a variety of abiotic and biotic stresses.