Polyamine oxidase 5 loss-of-function mutations in Arabidopsisthaliana trigger metabolic and transcriptional reprogrammingand promote salt stress tolerance

Abstract

The family of polyamine oxidases (PAO) in Arabidopsis(AtPAO1–5) mediates polyamine (PA) back-conversion,which reverses the PA biosynthetic pathway from spermineand its structural isomer thermospermine (tSpm) intospermidine and then putrescine. Here, we have studied the in-volvement of PA back-conversion in Arabidopsis salinit y toler-ance. AtPAO5 is the Arabidopsis PAO gene member mosttranscriptionally induced by salt stress. Two independent loss-of-function mutants (atpao5-2 and atpao5-3) were found toexhibit constitutively higher tSpm levels, with associated in-creased salt tolerance. Using global transcriptional andmetabolomic analyses, the underlying mechanisms were stud-ied. Stimulation of abscisic acid and jasmonate (JA) biosynthe-sis and accumulation of important compatible solutes, such assugars, polyols and proline, as well as TCA cycle intermediateswere observed in atpao5 mutants under salt stress. Expressionanalyses indicate that tSpm modulates the transcript levels ofseveral target genes, including many involved in the biosynthe-sis and signalling of JA, some of which are already known topromote salinity tolerance. Transcriptional modulation bytSpm is isomer-dependent, thus demonstrating the specificityof this response. Overall, we conclude that tSpm triggers meta-bolic and transcriptional reprogramming that promotes saltstress tolerance in Arabidopsis.