PagSAMDC4a-Mediated Polyamine Synthesis Regulate Vessel Differentiation Under Drought Stress Conditions in Poplar

Frequent and prolonged drought stress is a primary factor limiting the growth and development of perennial woody plants. Xylem vessel cells are crucial for water transport in woody plants; however, the molecular mechanisms governing the changes in their morphogenesis in response to water deprivation remain unclear. Here, we report that the alterations in polyamine (PA) levels under drought stress, mediated by the key enzyme PagSAMDC4a in PA synthesis, influence vessel morphogenesis through the modulation of hydrogen peroxide (H₂O₂) concentration in poplar 84 K (Populus alba × Populus glandulosa). PagSAMDC4a expression was predominantly observed in the phloem and cambium zones of stems and was upregulated under drought conditions. Overexpression of PagSAMDC4a (PagSAMDC4a-OE) resulted in increased PA content, leading to reduced vessel size and density in stem xylem. Conversely, PagSAMDC4a mutant lines exhibited the opposite phenotype, resembling 84 K plants treated with the PA synthesis inhibitor methylglyoxal-bis (guanylhydrazone). In addition, PagSAMDC4a-OE exhibited improved drought tolerance compared to nontransgenic 84 K plants and PagSAMDC4a mutant lines. Interestingly, the H₂O₂ level was significantly decreased in PagSAMDC4a-OE plants but markedly increased in PagSAMDC4a mutants relative to 84 K plants, suggesting that changes in vessel size may result from altered H₂O₂ levels. Supporting this hypothesis, H₂O₂ application rescued the small vessel phenotype in PagSAMDC4a-OE, whereas the scavenger potassium iodide reduced the size of xylem vessels in PagSAMDC4a mutants. Collectively, these findings provide evidence for the role of PAs in enhancing drought tolerance through the regulation of vessel differentiation.