Dataset Information

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

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.

SUBMITTER: Bian H

PROVIDER: S-EPMC11253005 | biostudies-literature | 2024 Jul

REPOSITORIES: biostudies-literature

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

Bian Hanxiao H Song Peizhe P Gao Ying Y Deng Zhiping Z Huang Chenyang C Yu Lei L Wang Hanqing H Ye Bingbing B Cai Zhihe Z Pan Yu Y Wang Fengqin F Liu Jianzhao J Gao Xiangwei X Chen Kunsong K Jia Guifang G Klee Harry J HJ Zhang Bo B

Proceedings of the National Academy of Sciences of the United States of America 20240701 28

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 separa ...[more]

PMID: 38950372

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Project description:Abscisic acid (ABA) regulates plant development and adaptation to environmental conditions. The ABA biosynthesis pathway in plants has been thoroughly elucidated; however, very few transcription factors directly regulating the expression of ABA biosynthetic genes have been identified. Here we show that the tomato (Solanum lycopersicum) zinc finger transcription factor SlZFP2, which is mainly expressed in developing fruits and axillary buds, negatively regulates ABA biosynthesis. Overexpression of SlZFP2 resulted in multiple phenotypic changes, including more branches, early flowering, delayed fruit ripening, lighter seeds and faster seed germination, whereas gene silencing by RNA interference (RNAi) caused poor fruit set and inhibited seed germination. Gene expression analysis showed that SlZFP2 represses ABA biosynthesis mainly through downregulation of the ABA biosynthetic genes SITIENS (SIT), FLACCA (FLC) and aldehyde oxidase SlAO1. SlZFP2 delays the onset of ripening through suppression of the ripening regulator COLORLESS NON-RIPENING (CNR). Using bacterial one hybrid screening and a selected amplification and binding assay we identified the (A/T)(G/C)TT repeat as the core binding sequence of SlZFP2. We further identified a large number of tomato genes containing putative SlZFP2 binding sites in their promoter regions. Chromatin immunoprecipitation and electrophoretic mobility shift assays demonstrated that SIT, FLC and SlAO1 are direct targets of SlZFP2 through binding to their promoter regions. We propose that SlZFP2 represents a novel negative regulator for fine tuning ABA biosynthesis during fruit development and provides a potentially valuable tool for dissecting the role of ABA in fruit ripening.To gain further insight on transcriptome changes regulated by SlZFP2, we sequenced a representative SlZFP2 RNAi line in LA1589 background and its nontransgenic sibling (WT) on a Miseq platform. The RNAi line 207 showed defected fruit set and ABA biosynthesis were chosen for profiling gene expression via RNA sequencing. Its nontransgenic sibling was served as controls. Three biological replicates were conducted.

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

Publications

The m<sup>6</sup>A reader SlYTH2 negatively regulates tomato fruit aroma by impeding the translation process.

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