SlPPR138-mediated RNA editing of rpoC1 is essential for chloroplast development in tomato

Abstract

Leaf color is a crucial determinant of photosynthetic efficiency and crop yield, but the molecular mechanisms regulating chloroplast development in tomato remain incompletely understood. Here, we identified a novel tomato mutant, gret1, that exhibits yellow cotyledons and young leaves that gradually turn green upon maturation. The gret1 mutant displays significantly reduced chlorophyll content and defective chloroplast development at early leaf stages, accompanied by changes in expression of genes involved in photosynthesis and chloroplast biogenesis. Genetic analysis revealed that the gret1 phenotype is controlled by a single recessive nuclear gene. Using map-based cloning, we identified SlPPR138, encoding a DYW-type pentatricopeptide repeat (PPR) protein, as the causal gene. A T-to-C point mutation in SlPPR138 causes a Cys-to-Arg substitution, which disrupts its function. Both genetic complementation and CRISPR/Cas9 knockout experiments validated that the gret1 phenotype is caused by the loss of SlPPR138. Mechanistically, we found that SlPPR138 mediates chloroplast RNA editing, particularly affecting the C-to-U editing efficiency of rpoC1, which encodes a core subunit of plastid-encoded RNA polymerase (PEP) complex. These findings demonstrate SlPPR138 is essential for early chloroplast development through RNA editing, providing new insights into the post-transcriptional regulation of photosynthesis in plants.

Acknowledgements

We extend our sincere gratitude for the financial support provided by the Ningbo 2035 Key Technology Project of Yongjiang Science and Technology Innovation (2024Z269), National Natural Science Foundation of China (32372715; 32472751), the Zhejiang Province Key Research and Development Special Project for Breeding (2021C02065), the Harbin Key Science and Technology Project (2021ZSZZNS06), and the Starry Night Science Fund of Zhejiang University Shanghai Institute for Advanced Study (SN-ZJU-SIAS-0011).

Author contributions

G.L. and Y.L. designed the research; C.L., T.Z., and C.X. conducted experiments; Y.L. and X.S. analyzed data; Ye.L. assisted with materials; Y.L. wrote the manuscript; G.L. and C.P. revised it; and all authors approved the final version.

Data availability

The raw sequencing data from the BSA-seq have been uploaded to NCBI under accession number PRJNA1272591.

Conflict of interest statement

G.L., Y.L., C.L., X.S., and T.Z. have filed a provisional patent application related to this work.

Supplementary Data

Supplementary data is available at Horticulture Research online.

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