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Comprehensive analysis of plastid gene expression during fruit development and ripening of kiwifruit

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Abstract

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Global survey of plastid gene expression during fruit ripening in kiwifruit provides cis-elements for the future engineering of the plastid genome of kiwifruit.

A limitation in the application of plastid biotechnology for molecular farming is the low-level expression of transgenes in non-green plastids compared with photosynthetically active chloroplasts. Unlike other fruits, not all chloroplasts are transformed into chromoplasts during ripening of red-fleshed kiwifruit (Actinidia chinensis cv. Hongyang) fruits, which may make kiwifruit an ideal horticultural plant for recombinant protein production by plastid engineering. To identify cis-elements potentially triggering high-level transgene expression in edible tissues of the ‘Hongyang’ kiwifruit, here we report a comprehensive analysis of kiwifruit plastid gene transcription in green leaves and fruits at three different developmental stages. While transcripts of a few photosynthesis-related genes and most genetic system genes were substantially upregulated in green fruits compared with leaves, nearly all plastid genes were significantly downregulated at the RNA level during fruit development. Expression of a few genes remained unchanged, including psbA, the gene encoding the D1 polypeptide of photosystem II. However, PsbA protein accumulation decreased continuously during chloroplast-to-chromoplast differentiation. Analysis of post-transcriptional steps in mRNA maturation, including intron splicing and RNA editing, revealed that splicing and editing may contribute to regulation of plastid gene expression. Altogether, 40 RNA editing sites were verified, and 5 of them were newly discovered. Taken together, this study has generated a valuable resource for the analysis of plastid gene expression and provides cis-elements for future efforts to engineer the plastid genome of kiwifruit.

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Acknowledgements

This research was supported by grants from the National Natural Science Foundation of China (31872035, 32071477), the Science and Technology Department of Hubei Province of China (2020CFA012) and Innovation Base for Introducing Talents of Discipline of Hubei Province (2019BJH021).

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Authors and Affiliations

  1. State Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life Sciences, Hubei University, Wuhan, 430062, China

    Qiqi Chen, Pan Shen, Ralph Bock, Shengchun Li & Jiang Zhang

  2. Max-Planck-Institut für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, 14476, Potsdam-Golm, Germany

    Ralph Bock

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  1. Qiqi Chen
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  2. Pan Shen
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  3. Ralph Bock
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  4. Shengchun Li
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Contributions

SL and JZ: project design; QC and PS: performing the experiments; SL and JZ: analysis of the data; SL and JZ: writing; RB: review and editing. All the authors read and approved the final manuscript.

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Correspondence to Shengchun Li or Jiang Zhang.

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Communicated by Teodoro Cardi.

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299_2022_2840_MOESM1_ESM.pptx

Supplementary file1 (PPTX 1880 KB) Incorrect gene annotations in the published Actinidia plastome map (Yao et al. 2015). (A) The trnE-UUC needs to be annotated on the outer cycle. The trnM-CAU (B) and trnT-GGU (C) are reduntant. (D) Annotation of the rps12 5′ needs to be on the inner cycle. (E) The rps12 gene in IRB region is missing.

299_2022_2840_MOESM2_ESM.pptx

Supplementary file2 (PPTX 1880 KB) Kiwifruit samples representing different ripening stages. Cross-sections are shown for a young fruit (A), a turning fruit (B), and a mature fruit (C).

Supplementary file3 (XLSX 18 KB)

Supplementary file4 (XLSX 155 KB)

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Chen, Q., Shen, P., Bock, R. et al. Comprehensive analysis of plastid gene expression during fruit development and ripening of kiwifruit. Plant Cell Rep 41, 1103–1114 (2022). https://doi.org/10.1007/s00299-022-02840-7

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