The Plant Cell in a Nutshell: H2O2 negatively regulates aluminum resistance

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Wei et al. show how hydrogen peroxide affects aluminum tolerance via its effects on the transcription factor SENSITIVE TO PROTON RHIZOTOXICITY 1 in Arabidopsis thaliana.

https://doi.org/10.1093/plcell/koad281

By X. Wei, Y.F. Zhu, W.X. Xie, W.W. Ren, Y. Zhang, H. Zhang, S.J. Dai, and C.-F. Huang

Background: Aluminum (Al) toxicity limits crop production on acid soils. The exposure of plants to Al stress triggers the accumulation of hydrogen peroxide (H2O2) in their roots. To combat Al toxicity, plants use the crucial transcription factor SENSITIVE TO PROTON RHIZOTOXICITY 1 (STOP1), which controls Al resistance. STOP1 undergoes various post-translational modifications, such ubiquitination, SUMOylation, and phosphorylation, to regulate its function.

Question: We wished to understand whether H2O2 plays a role in regulating Al signaling and Al resistance by affecting STOP1 through post-translational oxidation.

Findings: We identified the specific protein REGULATION OF ALMT1 EXPRESSION 6 (RAE6), which localizes to mitochondria and contains pentatricopeptide repeats (PPRs). The mutation of RAE6 disrupted the activity of complex I in the mitochondrial electron transport chain. This defect led to increased accumulation of H2O2 in mitochondria and rendered rae6 seedlings more sensitive to Al toxicity. We determined that H2O2 promotes the oxidation of STOP1 at specific cysteine residues (C8, C27 and C185), which triggers its degradation by enhancing its interaction with the F-box protein RAE1. However, to counteract the negative effects of H2O2 on STOP1, another protein, thioredoxin TRX1, can interact with STOP1 and reverse its oxidation.

Next steps: While we learned that H2O2 negatively regulates the accumulation of STOP1, it is not the signal that activates another pathway composed of a series of kinases (the MEKK1–MKK1/1–MPK4 cascade), which positively promotes STOP1 accumulation via its phosphorylation. Further research is needed to understand how plants sense Al stress and transmit the signal to the MEKK1–MKK1/1–MPK4 cascade, ultimately leading to an increase in STOP1 protein levels.

Reference:

Wei, et al. (2023). H2O2 negatively regulates aluminum resistance via oxidation and degradation of the transcription factor STOP1. https://doi.org/10.1093/plcell/koad281