Abiotic environmental stress, such as salinity and drought, is a major limitation in agricultural productivity. Plants have evolved organelle-to-nucleus signaling pathways that modify nuclear gene transcription in order to sustain or restore function in stressed organelles. In Arabidopsis thaliana, such signaling triggered by mitochondrial dysfunction is termed mitochondrial retrograde regulation (MRR) and enables plant cells to tolerate abiotic stresses such as salinity. Using transcriptomics and transgenic plants, Vanderauwera et al. showed that the transcription factor WRKY15 reduced salt tolerance in A. thaliana by inducing the unfolded protein response (UPR) in the endoplasmic reticulum (ER) in response to salt stress. Transgenic plants that overexpressed WRKY15 (WRKY15OE) showed an increase in dose-dependent sensitivity to increasing NaCl concentrations compared with wild-type plants, exhibiting stunted growth, cellular degeneration, and decreased chlorophyll production. Transcriptomics in WRKY15OE plants revealed that salt intensely activated the expression of genes involved in the UPR but reduced the expression of genes in the mitochondrial dysfunction regulon (MDR), which may be critical to the MRR. Persistent activation of the UPR increases cytosolic calcium concentrations, which can result in sustained mitochondrial calcium uptake. Although MDR gene expression and energy (ATP) production are activated in the mitochondria in response to calcium uptake, which is facilitated by Ca2+/calmodulin (CaM), these mitochondrial processes are inhibited by sustained calcium uptake. Although the MDR transcriptional regulation was closely linked to cytosolic calcium concentration and mitochondrial calcium uptake, plants overexpressing WRKY15 lacking CaM binding ability exhibited a similar salt sensitivity to the WRKY15OE plants, indicating that the WRKY15-mediated transcriptional changes are likely independent of its regulation by CaM. The data suggest a model whereby WRKY15 mediates a switch from mitochondria-induced salt tolerance to ER-induced salt sensitivity by activating UPR in plant cells and suppressing MRR. Whether targeting WRKY15 could improve salt tolerance in plants is not clear; the authors found that incomplete knockdown of WRKY15 in A. thaliana had no effect on salt sensitivity compared with wild-type plants, suggesting that even a low threshold of functional WRKY15 reduces salt tolerance. These findings advance our understanding of the organellar signaling pathways that mediate salt sensitivity in plants, which is critical to engineering salt-tolerant crops.
S. Vanderauwera, K. Vandenbroucke, A. Inzé, B. van de Cotte, P. Mühlenbock, R. De Rycke, N. Naouar, T. Van Gaever, M. C. E. Van Montagu, F. Van Breusegem, AtWRKY15 perturbation abolishes the mitochondrial stress response that steers osmotic stress tolerance in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 109, 20113–20118 (2012). [PubMed]