Populus euphratica PeMAX2 counteracts PeGRP2 to stabilize target mRNAs relating to salt tolerance

Abstract

Populus euphratica glycine-rich RNA-binding protein 2 (PeGRP2) has been previously shown to destabilize target mRNAs and negatively regulates salt tolerance of poplar. This study aimed to explore the post-translational regulation of PeGRP2 in the salt-resistant poplar. PeGRP2 was demonstrated to interact with more axillary growth 2 (PeMAX2), an F-box leucine-rich repeat protein. PeMAX2 transcription was upregulated by NaCl in P. euphratica, and an in vitro degradation assay showed that PeMAX2 promoted PeGRP2 degradation through the proteasomal degradation pathway. The PeMAX2-promoted PeGRP2 degradation and the relevance to salt tolerance were investigated using transgenic poplars of Populus × canescens and P. euphratica overexpressing PeMAX2, PeGRP2, and PeMAX2/PeGRP2. PeMAX2 overexpression improved the ability to maintain Na⁺ and reactive oxygen species (ROS) homeostasis in transgenic poplars, while PeGRP2 negatively regulates salt tolerance by impairing photosynthesis, Na⁺ and ROS homeostasis in stressed plants. PeMAX2 alleviated the PeGRP2-induced salt susceptibility by reducing the mRNA level of PeGRP2 and protein abundance in transgenic P. × canescens with dual overexpression of PeMAX2 and PeGRP2. Moreover, PeMAX2 counteracted PeGRP2 to stabilize target mRNAs encoding photosynthetic proteins, antioxidant enzymes, ATPases, and cation/H⁺ exchangers in P. × canescens. Therefore, the upregulated expression of PeMAX2 in salt-stressed P. euphratica fascilitated the degradation of PeGRP2 and thus mitigated its negative effects on salt tolerance. We proposed a schematic model illustrating the PeMAX2-PeGRP2 signaling pathway in salt response of P. euphratica.