| Summary: | We previously reported that proline modulates root meristem size in <i>Arabidopsis</i> by controlling the ratio between cell division and cell differentiation. Here, we show that proline metabolism affects the levels of superoxide anion (O<sub>2</sub><sup>•−</sup>) and hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>), which, in turn, modulate root meristem size and root elongation. We found that hydrogen peroxide plays a major role in proline-mediated root elongation, and its effects largely overlap those induced by proline, influencing root meristem size, root elongation, and cell cycle. Though a combination of genetic and pharmacological evidence, we showed that the short-root phenotype of the proline-deficient <i>p5cs1 p5cs2/P5CS2</i>, an <i>Arabidopsis</i> mutant homozygous for <i>p5cs1</i> and heterozygous for <i>p5cs2</i>, is caused by H<sub>2</sub>O<sub>2</sub> accumulation and is fully rescued by an effective H<sub>2</sub>O<sub>2</sub> scavenger. Furthermore, by studying <i>Arabidopsis</i> mutants devoid of ProDH activity, we disclosed the essential role of this enzyme in the modulation of root meristem size as the main enzyme responsible for H<sub>2</sub>O<sub>2</sub> production during proline degradation. Proline itself, on the contrary, may not be able to directly control the levels of H<sub>2</sub>O<sub>2</sub>, although it seems able to enhance the enzymatic activity of catalase (CAT) and ascorbate peroxidase (APX), the two most effective scavengers of H<sub>2</sub>O<sub>2</sub> in plant cells. We propose a model in which proline metabolism participates in a delicate antioxidant network to balance H<sub>2</sub>O<sub>2</sub> formation and degradation and fine-tune root meristem size in <i>Arabidopsis</i>.
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