Thermospermine is an evolutionarily ancestral phytohormone required for organ development and stress responses in the basal land plantMarchantia polymorpha

Abstract

AbstractThermospermine, a structural isomer of spermine, suppresses auxin-inducible xylem differentiation, whereas spermine is implicated in stress responses in angiosperms. Thermospermine synthase ACAULIS5 (ACL5) is well conserved from algae to land plants, but its physiological function remains elusive in non-vascular plants. Here we focused on MpACL5, a gene in the liverwortMarchantia polymorpha, which rescued the dwarf phenotype of theacl5mutant ofArabidopsis. In the Mpacl5mutants generated by genome editing, growth of the vegetative organ, thallus, and the sexual reproductive organ, gametangiophore, was severely retarded. The mutant gametangiophore exhibited remarkable morphological defects such as short stalks, fasciation, and indeterminate growth; it was formed as a fusion of two gametangiophores and a new gametangiophore was often initiated from the old one. Furthermore, Mpacl5was shown to be hypersensitive to heat and salt stresses. Given the absence of spermine in liverworts includingM. polymorpha, these results reveal that thermospermine has a dual primordial function in organ development and stress responses in the basal land plant lineage, the latter of which may have eventually been assigned to spermine during the land plant evolution.