Populus euphratica PeIDD5 regulates PeNAC029 to suppress salt tolerance in poplars

Populus euphratica downregulates the transcription factor PeNAC029 during prolonged salinity, thereby promoting long-term acclimation to salt stress. To elucidate this regulatory network, we identified PeIDD5, an INDETERMINATE DOMAIN (IDD) family member, as a direct transcriptional activator of PeNAC029. This study investigates the role of the PeIDD5-NAC029 transcriptional module in the salt tolerance of two contrasting poplars, P. euphratica (salt-tolerant) and P. × canescens (salt-sensitive). PeIDD5 directly binds the conserved cis-element TTTGTCC in the promoter regions of PeNAC029 and PcNAC029. In P. × canescens, PeIDD5 overexpression increased PcNAC029 transcript abundance, whereas virus-induced gene silencing of PeIDD5 in P. euphratica leaves reduced PeNAC029 transcript levels. Notably, overexpression of PeIDD5 or PeNAC029 in P. × canescens reduced phospholipase D (PLD) and phosphatidic acid (PA) levels, impairing growth and photosynthesis, increasing Na⁺ accumulation, and diminishing antioxidant activity relative to wild-type controls after treatment with 150 mM NaCl for 15 d. Conversely, silencing the PeIDD5-PeNAC029 module in P. euphratica leaves enhanced PLD activity and PA accumulation, thereby promoting Na⁺ and ROS homeostasis under short-term salt stress (150 mM NaCl, 48 h). Thus, PeIDD5 activates PeNAC029 and PcNAC029, suppressing PLD activity and reducing PA accumulation, which disrupts ionic and redox homeostasis in salt-stressed poplars. In P. euphratica, salt-induced suppression of PeIDD5 reduces PeNAC029 levels, thereby promoting long-term salt adaptation. Therefore, genetic engineering to suppress the PeIDD5-NAC029 regulatory pathway represents a promising approach to developing salt-tolerant poplars.