Thermospermine signaling in vascular development and stress adaptation: from translational regulation to climate-resilient crops.

Thermospermine (tSpm) is an asymmetric structural isomer of spermine found to accumulate in vascular plants and certain thermophilic bacteria. Since identification of ACAULIS5 (ACL5) as the enzyme responsible for tSpm biosynthesis in Arabidopsis thaliana, tSpm has emerged as a critical post-transcriptional regulator of vascular development, balancing xylem vessel differentiation and maintenance of procambial cell identity. Loss-of-function acl5 mutants display severe dwarfism and excessive xylem proliferation, whereas complementary gain-of-function approaches show that tSpm restrains auxin-driven xylem differentiation. Specifically, tSpm promotes the translation of SUPPRESSOR OF ACL5 (SAC51)-family bHLH transcription factors by alleviating the repressive effect of conserved upstream open reading frames embedded in their 5' leader sequence. Moreover, tSpm binds to ribosomes at a site dependent on m3U2952 methylation in the peptidyl transferase center of 25S rRNA, acting as a bifunctional translational modulator that simultaneously enhances SACL protein production and suppresses translation of LONESOME HIGHWAY. Beyond primary vascular development, tSpm regulates secondary growth in woody species, participates in root vascular patterning and lateral root formation, and mediates adaptive responses to abiotic stress, including drought and salinity. While tSpm synthesis is broadly conserved across the plant kingdom, the regulatory circuit linking tSpm to vascular cell fate emerged progressively during tracheophyte evolution through co-option of pre-existing molecular components. This review integrates foundational and cutting-edge findings to provide a comprehensive overview of tSpm biology, highlighting its central role at the interface of vascular development, post-transcriptional gene regulation, and environmental adaptation.