Unveiling the Secrets of Tomato Ripening: New Findings from H2O2 Research

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A team of researchers led by Prof. QIN Guozheng from the Institute of Botany at the Chinese Academy of Sciences has uncovered a previously overlooked mechanism by which the RNA N6–methyladenosine (m⁶A) demethylase SlALKBH2 undergoes reduction-oxidation (redox) modification. This change influences its stability and physiological function in the normal ripening of tomato fruits.

In a publication in Nature Plants, the investigators advanced their knowledge of hydrogen peroxide’s (H₂O₂) role, a mild oxidant acting as a critical signaling entity in various biological processes. They discovered that oxidative changes mediated by H₂O₂ regulate SlALKBH2’s functionality, crucial for the effective maturation of fleshy fruits. This maturation phase marks the conclusion of fruit development, directly affecting fruit quality and longevity.

Specifically, the researchers illustrated how H₂O₂ signaling interacts with RNA methylation modification to control plant development in a synchronized manner.

The most common chemical modification in eukaryotic mRNAs is m⁶A methylation. It governs numerous biological processes, including mRNA stability and translation efficacy by modulating mRNA metabolism.

As part of the dioxygenase family, m⁶A demethylases, such as SlALKBH2, can reversibly oxidize m⁶A methylation. This capability raises the question of whether SlALKBH2 itself is subject to oxidative modification, akin to other redox-responsive proteins.

To assess this hypothesis, the team transiently expressed the SlALKBH2 gene in Nicotiana benthamiana leaves treated with or without H₂O₂, then observed the redox condition of SlALKBH2.

The findings indicated a notable susceptibility of SlALKBH2 to oxidation induced by H₂O₂, leading to the generation of homodimers both in N. benthamiana leaves and tomato fruits. Importantly, exposure to H₂O₂ was found to hasten the ripening of tomato fruits, suggesting a role for SlALKBH2 oxidation in this process.

The production of SlALKBH2 homodimers was attributed to the participation of several cysteine (Cys) residues, with Cys39 being highlighted as a critical site; mutation at this site significantly impaired homodimer formation. Although oxidative modification increased the stability of the SlALKBH2 protein, it did not alter its m⁶A demethylase activity.

Additionally, the researchers identified NADPH-thioredoxin reductase C (SlNTRC) as a binding partner of SlALKBH2. They showed that SlNTRC modulates the redox state of SlALKBH2, thus influencing its m⁶A demethylation capability in tomatoes.

Stable SlNTRC knockout mutants were then produced in tomatoes through CRISPR–Cas9 gene editing. The homozygous mutant line exhibited significant delays in vegetative growth and was incapable of producing fruit.

This investigation established a relationship between H₂O₂ signaling and m⁶A methylation, emphasizing the importance of the redox regulation of m⁶A modifiers in the ripening of fruit.

Considering the essential function of RNA m⁶A methylation in various biological processes, researchers speculate that this regulatory mechanism may also be applicable to other developmental pathways.

In conclusion, this research not only deepens our comprehension of the molecular mechanisms driving fruit ripening but also presents new prospects and approaches for enhancing crop varieties.

Reference: Zhou L, Gao G, Tang R, et al. Redox modification of m6A demethylase SlALKBH2 in tomato regulates fruit ripening. Nat Plants. 2025. doi: 10.1038/s41477-024-01893-8

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