PeBBX24 suppresses GRP2 transcription in contrasting poplars differing in salt tolerance

Populus euphratica glycine-rich RNA-binding protein 2 (PeGRP2) negatively regulates salt tolerance by destabilizing target mRNAs encoding Na⁺/H⁺ antiporters, ATPases, and antioxidant enzymes in transgenic poplars. Downregulated PeGRP2 contributes to the adaptation of P. euphratica to long-term salt conditions; however, the regulatory loop governing the transcription of PeGRP2 is poorly understood. To explore the transcription network of PeGRP2 during salt stress, we identified that the B-box zinc finger protein PeBBX24 could bind to the PeGRP2 promoter. Subsequently, PeBBX24 was transferred to P. euphratica (salt-tolerant) and P. × canescens (salt-sensitive) to validate the transcriptional regulation of PeGRP2 and PcGRP2 and the relevance to salt tolerance in poplar species. PeBBX24-overexpressing poplars exhibited increased stem growth, less accumulated Na⁺, and enhanced antioxidant capacity compared with non-transgenic controls under NaCl treatment (100 mM, 24 h to 15 d). Functional characterization revealed that PeBBX24 transcriptionally suppresses PeGRP2 and PcGRP2, thereby counteracting their detrimental effects on Na⁺ homeostasis in transgenic poplars. Moreover, PeBBX24-drived repression of PeGRP2 and PcGRP2 could lessen their negative impact on reactive oxygen species scavenging, ultimately reinforcing the antioxidant defense machinery in transgenic poplars. Consequently, salt-induced PeBBX24 leads to downregulation of PeGRP2 and enhances salt adaptation in P. euphratica. Furthermore, PeBBX24-dependent repression of PcGRP2 offers a conceptual framework and promising genetic resources for breeding salt-tolerant and fast-growing poplars.