The ability to acclimate to stresses enables plants to grow and develop under adverse environmental conditions. Regulated intramembrane proteolysis (RIP) triggered by endoplasmic reticulum (ER) stress mediates some forms of stress signaling. Brassinosteroids (BRs) have been implicated in plant adaptation to stress, but no mechanisms for activation have been discovered. Here, we reveal a connection between ER stress signaling and BR-mediated growth and stress acclimation. Arabidopsis transcription factors bZIP17 and bZIP28 were translocated from the ER through the Golgi, where they were proteolytically cleaved by site 2 protease and released to translocate into the nucleus. Stresses, including heat and inhibition of protein glycosylation, increased translocation of these two bZIPs to the nucleus. These nuclear-localized bZIPs not only activated ER chaperone genes but also activated BR signaling, which was required for stress acclimation and growth. Thus, these bZIPs link ER stress and BR signaling, which may be a mechanism by which plant growth and stress responses can be integrated.

SUMMARYThe Arabidopsis genome has two fumarase genes, one of which encodes a protein with mitochondrial targeting information (FUM1) while the other (FUM2) does not. We show that a FUM1-green fluorescent protein fusion is directed to mitochondria while FUM2-red fluorescent protein remains in the cytosol. While mitochondrial FUM1 is an essential gene, cytosolic FUM2 is not required for plant growth. However FUM2 is required for the massive accumulation of carbon into fumarate that occurs in Arabidopsis leaves during the day. In fum2 knock-out mutants, fumarate levels remain low while malate increases, and these changes can be reversed with a FUM2 transgene. The fum2 mutant has lower levels of many amino acids in leaves during the day compared with the wild type, but higher levels at night, consistent with a link between fumarate and amino acid metabolism. To further test this relationship we grew plants in the absence or presence of nitrogen fertilizer. The amount of fumarate in leaves increased several fold in response to nitrogen in wild-type plants, but not in fum2. Malate increased to a small extent in the wild type but to a greater extent in fum2. Growth of fum2 plants was similar to that of the wild type in low nitrogen but much slower in the presence of high nitrogen. Activities of key enzymes of nitrogen assimilation were similar in both genotypes. We conclude that FUM2 is required for the accumulation of fumarate in leaves, which is in turn required for rapid nitrogen assimilation and growth on high nitrogen.