We previously reported that proline modulates root meristem size in Arabidopsis by control- ling the ratio between cell division and cell differentiation. Here, we show that proline metabolism affects the levels of superoxide anion (O2•−) and hydrogen peroxide (H2O2), 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, influ- encing 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 p5cs1 p5cs2/P5CS2, an Arabidopsis mutant homozygous for p5cs1 and heterozygous for p5cs2, is caused by H2O2 accumulation and is fully rescued by an effective H2O2 scavenger. Furthermore, by studying Arabidopsis 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 H2O2 production during proline degradation. Proline itself, on the contrary, may not be able to directly control the levels of H2O2, although it seems able to enhance the enzymatic activity of catalase (CAT) and ascorbate peroxidase (APX), the two most effective scavengers of H2O2 in plant cells. We propose a model in which proline metabolism participates in a delicate antioxidant network to balance H2O2 formation and degradation and fine-tune root meristem size in Arabidopsis.
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