Vascular plant one‐zinc‐finger protein 1/2 transcription factors regulate abiotic and biotic stress responses in Arabidopsis

Abstract

SUMMARYPlants adapt to abiotic and biotic stresses by activating abscisic acid-mediated (ABA) abiotic stress-responsive and salicylic acid-(SA) or jasmonic acid-mediated (JA) biotic stress-responsive pathways, respectively. Although the abiotic stress-responsive pathway interacts antagonistically with the biotic stress-responsive pathways, the mechanisms that regulate these pathways remain largely unknown. In this study, we provide insight into the function of vascular plant one-zinc-finger proteins (VOZs) that modulate various stress responses in Arabidopsis. The expression of many stress-responsive genes was changed in the voz1voz2 double mutant under normal growth conditions. Consistent with altered stress-responsive gene expression, freezing-and drought-stress tolerances were increased in the voz1voz2 double mutant. In contrast, resistance to a fungal pathogen, Colletotrichum higginsianum, and to a bacterial pathogen, Pseudomonas syringae, was severely impaired. Thus, impairing VOZ function simultaneously conferred increased abiotic tolerance and biotic stress susceptibility. In a chilling stress condition, both the VOZ1 and VOZ2 mRNA expression levels and the VOZ2 protein level gradually decreased. VOZ2 degradation during cold exposure was completely inhibited by the addition of the 26S proteasome inhibitor, MG132, a finding that suggested that VOZ2 degradation is dependent on the ubiquitin/26S proteasome system. In voz1voz2, ABA-inducible transcription factor CBF4 expression was enhanced significantly even under normal growth conditions, despite an unchanged endogenous ABA content. A finding that suggested that VOZs negatively affect CBF4 expression in an ABA-independent manner. These results suggest that VOZs function as both negative and positive regulators of the abiotic and biotic stress-responsive pathways, and control Arabidopsis adaptation to various stress conditions.

Vascular plant one-zinc-finger protein 2 is localized both to the nucleus and stress granules under heat stress in Arabidopsis

“…16 We previously reported that VOZ2 is degraded by the ubiquitin-proteasome system under cold-stress conditions. 17 These results suggest that VOZ proteins are transferred to the nucleus and function as transcriptional regulators when the plant cells perceive certain environmental signals (e.g., light, cold or heat), and then are rapidly subjected to the ubiquitin/proteasome-dependent degradation for inactivation. Nevertheless, we cannot rule out the possibility that VOZ2 continuously moves to the nucleus and subjects a subsequent degradation in non-stressful conditions, and disappears from the nucleus under heat stress conditions because of the decrease of VOZ2 transcription and the sequestration of VOZ2 in the SGs or P-bodies.…”

“…Since we previously reported that around 42 C is a critical temperature of thermotolerance of Arabidopsis (ecotype Columbia-0), 17 we decided to set 42 C as the heat stress temperature in this study. To explore the function of VOZs under heat stress conditions, we first examined the subcellular localization of VOZ2 by immunostaining with an anti-VOZ2 antibody.…”

“…17 Nevertheless, little is known about the molecular mechanism by which VOZ proteins function under heat stress conditions. In this study, we found that localization of the VOZ2 protein is dramatically changed (to the nucleus and cytoplasmic foci) under high-temperature conditions.…”

“…Thus, VOZ proteins function as negative regulators of abiotic stress response pathways. 17 Arabidopsis HsfA1 transcription factors serve as the mainpositive regulators in heat stress-responsive gene expression. The expression of DREB2A under heat stress is also regulated by HsfA1s.…”

“…16 We previously reported that the voz1voz2 double mutant shows increased cold and drought tolerance but decreased resistance to pathogens and heat stress. 17 Although the green fluorescent protein-fused VOZ2 signal was predominantly observed in the cytoplasm under normal growth conditions, nuclear-localization-signalcontaining but not nuclear-export-signal-containing VOZ2 protein can complement the late-flowering phenotype of the voz1voz2 double mutant, indicating that VOZ proteins relocate from the cytoplasm to the nucleus and regulate the flowering signaling pathways. 16 Nonetheless, no clear nuclear localization of VOZ proteins under normal growth conditions has been observed in Arabidopsis, these data indicate possible transcriptional regulatory function of VOZ proteins under particular growth conditions.…”