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Single-point mutation in the <i>ACTIN2</i> gene of the <i>der1–3</i> mutant revealed that ACTIN2 is an essential actin isovariant required for root hair tip growth, and leads to shorter, thinner and more randomly oriented actin filaments in comparison to the wild-type C24 genotype. The actin cytoskeleton has been linked to plant defense against oxidative stress, but it is not clear how altered structural organization and dynamics of actin filaments may help plants to cope with oxidative stress. In this study, we characterized root growth, plant biomass, actin organization and antioxidant activity of the <i>der1–3</i> mutant under oxidative stress induced by paraquat and H₂O₂. Under these conditions, plant growth was better in the <i>der1–3</i> mutant, while the actin cytoskeleton in the <i>der1–3</i> carrying <i>pro35S::GFP:FABD2</i> construct showed a lower bundling rate and higher dynamicity. Biochemical analyses documented a lower degree of lipid peroxidation, and an elevated capacity to decompose superoxide and hydrogen peroxide. These results support the view that the <i>der1–3</i> mutant is more resistant to oxidative stress. We propose that alterations in the actin cytoskeleton, increased sensitivity of ACTIN to reducing agent dithiothreitol (DTT), along with the increased capacity to decompose reactive oxygen species encourage the enhanced tolerance of this mutant against oxidative stress.