JUNGBRUNNEN1, a Reactive Oxygen Species–Responsive NAC Transcription Factor, Regulates Longevity in Arabidopsis

Abstract

The transition from juvenility over maturation to senescence is a complex process involving multiple transcription factors and regulatory circuits, most of which are currently only vaguely defined. Here we identify JUNGBRUNNEN1 (JUB1), a NAC transcription factor gene rapidly induced by hydrogen peroxide (H2O2), as a central regulator of juvenility in Arabidopsis thaliana. Overexpression of JUB1 under constitutive and inducible promoters strongly delays senescence, enhances tolerance to various abiotic stresses including oxidative stress, and dampens the intracellular H2O2 level. In contrast, precocious senescence and lowered tolerance to abiotic stress were evident in the jub1-1 knock-down line. In vitro binding site selection identified the preferred JUB1 binding site containing RRYGCCGT as its core sequence. The JUB1 binding site is present within the 5´ upstream regulatory region of DREB2A, a transcription factor playing an important role in abiotic stress responses. In accordance with this, JUB1 transactivates DREB2A expression in mesophyll cell protoplasts and transgenic plants and binds in vitro an in vivo to the DREB2A promoter. Transcriptome profiling of JUB1 overexpressors revealed elevated expression of several reactive oxygen species (ROS) responsive genes, including various heat shock protein (HSP) and ROS scavenging glutathione S-transferase (GST) genes, whose expression is further induced by H2O2 treatment. Metabolite profiling revealed that levels of proline and trehalose were significantly elevated in JUB1 overexpression plants, in accordance with their enhanced abiotic stress tolerance. We hypothesize that JUB1 constitutes a central regulator of a finely tuned control system that modulates cellular H2O2 level and primes the plants for upcoming stress through a gene regulatory network that involves DREB2A.