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. 2024 Jul 9;121(28):e2405100121.
doi: 10.1073/pnas.2405100121. Epub 2024 Jul 1.

The m6A reader SlYTH2 negatively regulates tomato fruit aroma by impeding the translation process

Hanxiao Bian #  1 , Peizhe Song #  2 , Ying Gao #  1   3 , Zhiping Deng #  4 , Chenyang Huang  5 , Lei Yu  6 , Hanqing Wang  1 , Bingbing Ye  1 , Zhihe Cai  2 , Yu Pan  7 , Fengqin Wang  8 , Jianzhao Liu  5 , Xiangwei Gao  6 , Kunsong Chen  1 , Guifang Jia  2   9   10 , Harry J Klee  1 , Bo Zhang  1   11
Affiliations

The m6A reader SlYTH2 negatively regulates tomato fruit aroma by impeding the translation process

Hanxiao Bian et al. Proc Natl Acad Sci U S A. .

Abstract

N6-methyladenosine (m6A) is a fundamentally important RNA modification for gene regulation, whose function is achieved through m6A readers. However, whether and how m6A readers play regulatory roles during fruit ripening and quality formation remains unclear. Here, we characterized SlYTH2 as a tomato m6A reader protein and profiled the binding sites of SlYTH2 at the transcriptome-wide level. SlYTH2 undergoes liquid-liquid phase separation and promotes RNA-protein condensate formation. The target mRNAs of SlYTH2, namely m6A-modified SlHPL and SlCCD1B associated with volatile synthesis, are enriched in SlYTH2-induced condensates. Through polysome profiling assays and proteomic analysis, we demonstrate that knockout of SlYTH2 expedites the translation process of SlHPL and SlCCD1B, resulting in augmented production of aroma-associated volatiles. This aroma enrichment significantly increased consumer preferences for CRISPR-edited fruit over wild type. These findings shed light on the underlying mechanisms of m6A in plant RNA metabolism and provided a promising strategy to generate fruits that are more attractive to consumers.

Keywords: RNA methylation; flavor quality; phase separation; translation repression.

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Conflict of interest statement

Competing interests statement:The authors declare no competing interest.

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