HFR1 antagonizes ABI4 to coordinate cytosolic redox status for seed germination under high-temperature stress.

Abstract

Seed germination and dormancy represent critical phases in the life cycle of plants, tightly regulated by endogenous phytochrome levels and environment signals. High temperatures (HT) induce the overaccumulation of reactive oxygen species (ROS) and increase abscisic acid (ABA), thereby inhibiting seed germination. Our previous findings showed that HT induced the burst of reactive nitrogen species (RNS), increasing the S-nitrosylation modification of HFR1, which effectively blocks seed germination. Importantly, stabilizing HFR1 has been shown to significantly mitigate the inhibitory effect of HT on seed germination. In this study, we reported that HT increased the protein abundance of ABI4, a crucial component in ABA signaling, which in turn activates the expression of RbohD while suppressing the expression of VTC2. This leads to the rapid generation of ROS, thereby inhibiting seed germination. Consistently, the seed germination of abi4 mutant showed insensitivity to HT with lower ROS level during seed germination, whereas transgenic lines overexpressing ABI4 showed reduced germination rates accompanied by elevated ROS levels. Furthermore, we noted that HFR1 interacts with ABI4 to sequester its activity under normal conditions. However, HT-induced ROS triggered the degradation of HFR1, consequently releasing ABI4 activity. This activation of ABI4 promotes RbohD expression, culminating in a ROS burst that suppresses seed germination. Thus, our study unveils a novel function for ABI4 in regulating ROS level and seed germination under HT stress. Throughout this process, HFR1 plays a critical role in restraining ABI4 activity to maintain an optimal endogenous ROS level, thereby ensuring seed germination under favorable environmental conditions.