PPR蛋白调控叶绿体RNA编辑分子机制研究进展

doi:10.13560/j.cnki.biotech.bull.1985.2025-0506

摘要/Abstract

摘要：

作为半自主性细胞器，叶绿体自身含有基因组，其转录的部分RNA需要通过实行C→U碱基变化才能保证基因的正确表达。PPR（pentatricopeptide repeat protein）蛋白是控制叶绿体RNA编辑的核心调控因子，其家族庞大，分为P型和PLS型两个亚家族，根据它们不同的C端结构域，PLS类亚家族蛋白可以进一步分为PLS-E、PLS-E+和PLS-DYW，其中，PLS-DYW型中的DYW结构域具有脱氨酶活性能直接参与RNA编辑。PPR蛋白特有的PPR基序以N端到C端的取向第6和第1位的氨基酸组合能识别编辑位点上游5′-3′方向的RNA序列，这种模块化的识别机制使得PPR蛋白能够以单PPR基序对应单核苷酸的方式筛选编辑位点，并募集和组装编辑复合体，实施编辑过程。相关PPR蛋白调控的基因发生编辑缺陷会导致叶绿体发育异常，引发植株萎蔫或致死。本文对现阶段相关研究进展进行综述，重点介绍了不同植物中PPR蛋白是如何调控叶绿体基因进行RNA编辑的分子机制，并对RNA编辑复合体动态组装过程进行了展望，为未来深入探索PPR蛋白的靶向机制及其在农业中的应用提供借鉴。

关键词: 叶绿体, PPR蛋白, RNA编辑, 光合作用

Abstract:

As semi-autonomous organelles, chloroplasts possess their own genomes, and some of their transcribed RNAs require C-to-U base changes to ensure correct gene expression. PPR (pentatricopeptide repeat protein) proteins are the core regulatory factors controlling chloroplast RNA editing. This family is large and is divided into two subfamilies, P-type and PLS-type, based on their different C-terminal domains. The PLS-type subfamily can be further classified into PLS-E, PLS-E+, and PLS-DYW. Among them, the DYW domain in the PLS-DYW type has deaminase activity and directly participates in RNA editing. The PPR motif, which is unique to PPR proteins, recognizes the RNA sequence upstream of the editing site in the 5′-3′ direction based on the combination of the 6th and 1st amino acids from the N-terminal to the C-terminal. This modular recognition mechanism enables PPR proteins to screen editing sites in a one-PPR-motif-to-one-nucleotide manner, recruit and assemble the editing complex, and carry out the editing process. Defects in RNA editing regulated by related PPR proteins can lead to abnormal chloroplast development, causing plant wilting or death. This article reviews the current research progress, focusing on the molecular mechanisms by which PPR proteins regulate RNA editing of chloroplast genes in different plants, and prospects to the dynamic assembly process of the RNA editing complex, providing references for future in-depth exploration of the targeting mechanism of PPR proteins and their applications in agriculture.

Key words: chloroplast, PPR proteins, RNA editing, photosynthesis

李新颖, 孙晶, 吕若彤, 任亚娟, 罗蕾, 艾鹏飞, 王雁伟. PPR蛋白调控叶绿体RNA编辑分子机制研究进展[J]. 生物技术通报, 2025, 41(10): 32-42.

LI Xin-ying, SUN Jing, LYU Ruo-tong, REN Ya-juan, LUO Lei, AI Peng-fei, WANG Yan-wei. Research Progress in the Molecular Mechanism of PPR Protein-regulated Chloroplast RNA Editing[J]. Biotechnology Bulletin, 2025, 41(10): 32-42.

图/表 3

图1 胞嘧啶核苷（C）到尿嘧啶核苷（U）的RNA编辑

Fig. 1 RNA editing of cytosine nucleoside (C) to uracil nucleoside (U)

图2 PPR蛋白的结构

Fig. 2 Structure of PPR proteins

图3 用于RNA结合的PPR识别代码每个PPR基序的关键氨基酸位置6和1′分别表示为黄色和绿色的方形框。T、N、D和S分别表示氨基酸酪氨酸、天冬酰胺、天冬氨酸和丝氨酸。如Barkan等［45］提出的位置6和1′处的氨基酸组合决定了与特定碱基的结合。（T，N）（T在6，N在1′处）对应腺嘌呤（A）、（T，D）对应鸟嘌呤（G）、（N，S）对应胞嘧啶（C）、（N，D）对应尿嘧啶（U）以及（N，N）可识别C或U

Fig. 3 PPR recognition code for RNA bindingKey amino acid positions 6 and 1′ of each PPR motif are indicated as yellow and green colored square boxes, respectively. T, N, D, and S denote amino acids tyrosine, asparagine, aspartic acid, and serine, respectively. Combinations of amino acids at positions 6 and 1′ specify binding to specific bases as proposed in Barkan et al[45]. (T, N) (T at 6, N at 1′) specify binding to adenine (A), (T, D) to guanine (G), (N, S) to cytosine (C), (N, D) to uracil (U), and (N, N) to C or U

参考文献 97

[1]	Timmis JN, Ayliffe MA, Huang CY, et al. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes [J]. Nat Rev Genet, 2004, 5(2): 123-135.
[2]	Lee K, Kang H. Roles of organellar RNA-binding proteins in plant growth, development, and abiotic stress responses [J]. Int J Mol Sci, 2020, 21(12): 4548.
[3]	Yu QB, Jiang Y, Chong K, et al. AtECB2, a pentatricopeptide repeat protein, is required for chloroplast transcript accD RNA editing and early chloroplast biogenesis in Arabidopsis thaliana [J]. Plant J, 2009, 59(6): 1011-1023.
[4]	Eisenberg E, Levanon EY. A-to-I RNA editing—immune protector and transcriptome diversifier [J]. Nat Rev Genet, 2018, 19(8): 473-490.
[5]	Gualberto JM, Lamattina L, Bonnard G, et al. RNA editing in wheat mitochondria results in the conservation of protein sequences [J]. Nature, 1989, 341(6243): 660-662.
[6]	Hoch B, Maier RM, Appel K, et al. Editing of a chloroplast mRNA by creation of an initiation codon [J]. Nature, 1991, 353(6340): 178-180.
[7]	Castandet B, Araya A. RNA editing in plant organelles. Why make it easy? [J]. Biochemistry, 2011, 76(8): 924-931.
[8]	Ichinose M, Sugita M. RNA editing and its molecular mechanism in plant organelles [J]. Genes, 2016, 8(1): 5.
[9]	Notsu Y, Masood S, Nishikawa T, et al. The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants [J]. Mol Genet Genomics, 2002, 268(4): 434-445.
[10]	Adams KL, Qiu YL, Stoutemyer M, et al. Punctuated evolution of mitochondrial gene content: high and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution [J]. Proc Natl Acad Sci USA, 2002, 99(15): 9905-9912.
[11]	Maier RM, Zeltz P, Kössel H, et al. RNA editing in plant mitochondria and chloroplasts [J]. Plant Mol Biol, 1996, 32(1-2): 343-365.
[12]	Brennicke A, Marchfelder A, Binder S. RNA editing [J]. FEMS Microbiol Rev, 1999, 23(3): 297-316.
[13]	Sun T, Bentolila S, Hanson MR. The unexpected diversity of plant organelle RNA editosomes [J]. Trends Plant Sci, 2016, 21(11): 962-973.
[14]	Zhu Q, Dugardeyn J, Zhang CY, et al. The Arabidopsis thaliana RNA editing factor SLO2, which affects the mitochondrial electron transport chain, participates in multiple stress and hormone responses [J]. Mol Plant, 2014, 7(2): 290-310.
[15]	Lurin C, Andrés C, Aubourg S, et al. Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis [J]. Plant Cell, 2004, 16(8): 2089-2103.
[16]	Liu JM, Xu ZS, Lu PP, et al. Genome-wide investigation and expression analyses of the pentatricopeptide repeat protein gene family in foxtail millet [J]. BMC Genomics, 2016, 17(1): 840.
[17]	李景芳, 王宝祥, 刘艳, 等. PPR蛋白在水稻生长发育中的功能研究进展 [J]. 植物遗传资源学报, 2022, 23(2): 358-367.
	Li JF, Wang BX, Liu Y, et al. Progress of research in functions of PPR proteins in growth and development of rice [J]. Journal of Plant Genetic Resources, 2022, 23(2): 358-367.
[18]	Qiu TC, Zhao XS, Feng HJ, et al. OsNBL3, a mitochondrion-localized pentatricopeptide repeat protein, is involved in splicing nad5 intron 4 and its disruption causes lesion mimic phenotype with enhanced resistance to biotic and abiotic stresses [J]. Plant Biotechnol J, 2021, 19(11): 2277-2290.
[19]	Zhao Y, Xu W, Zhang YZ, et al. PPR647 protein is required for chloroplast RNA editing, splicing and chloroplast development in maize [J]. Int J Mol Sci, 2021, 22(20): 11162.
[20]	Liu S, Melonek J, Boykin LM, et al. PPR-SMRs: ancient proteins with enigmatic functions [J]. RNA Biol, 2013, 10(9): 1501-1510.
[21]	Zhou W, Lu QT, Li QW, et al. PPR-SMR protein SOT1 has RNA endonuclease activity [J]. Proc Natl Acad Sci USA, 2017, 114(8): E1554-E1563.
[22]	Jia YB, Tian HY, Zhang S, et al. GUN1-interacting proteins open the door for retrograde signaling [J]. Trends Plant Sci, 2019, 24(10): 884-887.
[23]	Cheng SF, Gutmann B, Zhong X, et al. Redefining the structural motifs that determine RNA binding and RNA editing by pentatricopeptide repeat proteins in land plants [J]. Plant J, 2016, 85(4): 532-547.
[24]	Colcombet J, Lopez-Obando M, Heurtevin L, et al. Systematic study of subcellular localization of Arabidopsis PPR proteins confirms a massive targeting to organelles [J]. RNA Biol, 2013, 10(9): 1557-1575.
[25]	Gutmann B, Royan S, Schallenberg-Rüdinger M, et al. The expansion and diversification of pentatricopeptide repeat RNA-editing factors in plants [J]. Mol Plant, 2020, 13(2): 215-230.
[26]	Small I, Melonek J, Bohne AV, et al. Plant organellar RNA maturation [J]. Plant Cell, 2023, 35(6): 1727-1751.
[27]	Salone V, Rüdinger M, Polsakiewicz M, et al. A hypothesis on the identification of the editing enzyme in plant organelles [J]. FEBS Lett, 2007, 581(22): 4132-4138.
[28]	Boussardon C, Salone V, Avon A, et al. Two interacting proteins are necessary for the editing of the NdhD-1 site in Arabidopsis plastids [J]. Plant Cell, 2012, 24(9): 3684-3694.
[29]	Hayes ML, Santibanez PI. A plant pentatricopeptide repeat protein with a DYW-deaminase domain is sufficient for catalyzing C-to-U RNA editing in vitro [J]. J Biol Chem, 2020, 295(11): 3497-3505.
[30]	Takenaka M, Takenaka S, Barthel T, et al. DYW domain structures imply an unusual regulation principle in plant organellar RNA editing catalysis [J]. Nat Catal, 2021, 4(6): 510-522.
[31]	Yang YZ, Liu XY, Tang JJ, et al. GRP23 plays a core role in E-type editosomes via interacting with MORFs and atypical PPR-DYWs in Arabidopsis mitochondria [J]. Proc Natl Acad Sci USA, 2022, 119(39): e2210978119.
[32]	Wang Y, Li H, Huang ZQ, et al. Maize PPR-E proteins mediate RNA C-to-U editing in mitochondria by recruiting the trans deaminase PCW1 [J]. Plant Cell, 2023, 35(1): 529-551.
[33]	Wang Y, Huang ZQ, Tian KD, et al. Multiple factors interact in editing of PPR-E+-targeted sites in maize mitochondria and plastids [J]. Plant Commun, 2024, 5(5): 100836.
[34]	Andrés-Colás N, Zhu Q, Takenaka M, et al. Multiple PPR protein interactions are involved in the RNA editing system in Arabidopsis mitochondria and plastids [J]. Proc Natl Acad Sci USA, 2017, 114(33): 8883-8888.
[35]	Guillaumot D, Lopez-Obando M, Baudry K, et al. Two interacting PPR proteins are major Arabidopsis editing factors in plastid and mitochondria [J]. Proc Natl Acad Sci USA, 2017, 114(33): 8877-8882.
[36]	Huo YZ, Cheng MX, Tang MJ, et al. GhCTSF1, a short PPR protein with a conserved role in chloroplast development and photosynthesis, participates in intron splicing of rpoC1 and ycf3-2 transcripts in cotton [J]. Plant Commun, 2024, 5(6): 100858.
[37]	Hammani K, Takenaka M, Miranda R, et al. A PPR protein in the PLS subfamily stabilizes the 5'-end of processed rpl16 mRNAs in maize chloroplasts [J]. Nucleic Acids Res, 2016, 44(9): 4278-4288.
[38]	Zhao XB, Huang JY, Chory J. GUN1 interacts with MORF2 to regulate plastid RNA editing during retrograde signaling [J]. Proc Natl Acad Sci USA, 2019, 116(20): 10162-10167.
[39]	Hegeman CE, Halter CP, Owens TG, et al. Expression of complementary RNA from chloroplast transgenes affects editing efficiency of transgene and endogenous chloroplast transcripts [J]. Nucleic Acids Res, 2005, 33(5): 1454-1464.
[40]	Sasaki T, Yukawa Y, Wakasugi T, et al. A simple in vitro RNA editing assay for chloroplast transcripts using fluorescent dideoxynucleotides: distinct types of sequence elements required for editing of ndh transcripts [J]. Plant J, 2006, 47(5): 802-810.
[41]	Yin P, Li QX, Yan CY, et al. Structural basis for the modular recognition of single-stranded RNA by PPR proteins [J]. Nature, 2013, 504(7478): 168-171.
[42]	Yan JJ, Zhang QX, Guan ZY, et al. MORF9 increases the RNA-binding activity of PLS-type pentatricopeptide repeat protein in plastid RNA editing [J]. Nat Plants, 2017, 3: 17037.
[43]	Takenaka M, Zehrmann A, Brennicke A, et al. Improved computational target site prediction for pentatricopeptide repeat RNA editing factors [J]. PLoS One, 2013, 8(6): e65343.
[44]	Yagi Y, Hayashi S, Kobayashi K, et al. Elucidation of the RNA recognition code for pentatricopeptide repeat proteins involved in organelle RNA editing in plants [J]. PLoS One, 2013, 8(3): e57286.
[45]	Barkan A, Rojas M, Fujii S, et al. A combinatorial amino acid code for RNA recognition by pentatricopeptide repeat proteins [J]. PLoS Genet, 2012, 8(8): e1002910.
[46]	Ke JY, Chen RZ, Ban T, et al. Structural basis for RNA recognition by a dimeric PPR-protein complex [J]. Nat Struct Mol Biol, 2013, 20(12): 1377-1382.
[47]	Gully BS, Cowieson N, Stanley WA, et al. The solution structure of the pentatricopeptide repeat protein PPR10 upon binding atpH RNA [J]. Nucleic Acids Res, 2015, 43(3): 1918-1926.
[48]	Tillich M, Lehwark P, Morton BR, et al. The evolution of chloroplast RNA editing [J]. Mol Biol Evol, 2006, 23(10): 1912-1921.
[49]	Huang WF, Zhang Y, Shen LQ, et al. Accumulation of the RNA polymerase subunit RpoB depends on RNA editing by OsPPR16 and affects chloroplast development during early leaf development in rice [J]. New Phytol, 2020, 228(4): 1401-1416.
[50]	Cui XA, Wang YW, Wu JX, et al. The RNA editing factor DUA1 is crucial to chloroplast development at low temperature in rice [J]. New Phytol, 2019, 221(2): 834-849.
[51]	Du YX, Mo WP, Ma TT, et al. A pentatricopeptide repeat protein DUA1 interacts with sigma factor 1 to regulate chloroplast gene expression in rice [J]. Photosynth Res, 2021, 147(2): 131-143.
[52]	Zhang JH, Guo YP, Fang Q, et al. The PPR-SMR protein ATP4 is required for editing the chloroplast rps8 mRNA in rice and maize [J]. Plant Physiol, 2020, 184(4): 2011-2021.
[53]	Wang YW, Duan Y, Ai PF. OsTHA8 encodes a pentatricopeptide repeat protein required for RNA editing and splicing during rice chloroplast development [J]. Crop J, 2023, 11(5): 1353-1367.
[54]	Tang JP, Zhang WW, Wen K, et al. OsPPR6, a pentatricopeptide repeat protein involved in editing and splicing chloroplast RNA, is required for chloroplast biogenesis in rice [J]. Plant Mol Biol, 2017, 95(4-5): 345-357.
[55]	Sun YG, Kuang LC, Wang JL, et al. The pentatricopeptide repeat protein TCD6 functions RNA editing and cleavage of ndhA and is required for chloroplast development in early rice seedlings [J]. Crop Des, 2024, 3(3): 100063.
[56]	Chen CZ, Wang YL, He MX, et al. OsPPR9 encodes a DYW-type PPR protein that affects editing efficiency of multiple RNA editing sites and is essential for chloroplast development [J]. J Integr Agric, 2023, 22(4): 972-980.
[57]	Wang Y, Ren YL, Zhou KN, et al. WHITE STRIPE LEAF4 encodes a novel P-type PPR protein required for chloroplast biogenesis during early leaf development [J]. Front Plant Sci, 2017, 8: 1116.
[58]	Asano T, Miyao A, Hirochika H, et al. A pentatricopeptide repeat gene of rice is required for splicing of chloroplast transcripts and RNA editing of ndhA [J]. Plant Biotechnol, 2013, 30(1): 57-64.
[59]	Liu X, Lan J, Huang YS, et al. WSL5, a pentatricopeptide repeat protein, is essential for chloroplast biogenesis in rice under cold stress [J]. J Exp Bot, 2018, 69(16): 3949-3961.
[60]	Xiao HJ, Xu YH, Ni CZ, et al. A rice dual-localized pentatricopeptide repeat protein is involved in organellar RNA editing together with OsMORFs [J]. J Exp Bot, 2018, 69(12): 2923-2936.
[61]	侯桂花, 熊杰, 罗志, 等. PPR34通过影响赤霉素代谢调控水稻种子萌发与株高 [J]. 分子植物育种, 2022, 20(12): 3938-3949.
	Hou GH, Xiong J, Luo Z, et al. PPR34 regulates rice seed germination and plant height by influencing gibberellin metabolism [J]. Mol Plant Breed, 2022, 20(12): 3938-3949.
[62]	Okuda K, Habata Y, Kobayashi Y, et al. Amino acid sequence variations in Nicotiana CRR4 orthologs determine the species-specific efficiency of RNA editing in plastids [J]. Nucleic Acids Res, 2008, 36(19): 6155-6164.
[63]	Okuda K, Myouga F, Motohashi R, et al. Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNA editing [J]. Proc Natl Acad Sci USA, 2007, 104(19): 8178-8183.
[64]	Robbins JC, Heller WP, Hanson MR. A comparative genomics approach identifies a PPR-DYW protein that is essential for C-to-U editing of the Arabidopsis chloroplast accD transcript [J]. RNA, 2009, 15(6): 1142-1153.
[65]	Fujii S, Small I. The evolution of RNA editing and pentatricopeptide repeat genes [J]. New Phytol, 2011, 191(1): 37-47.
[66]	Hayes ML, Dang KN, Diaz MF, et al. A conserved glutamate residue in the C-terminal deaminase domain of pentatricopeptide repeat proteins is required for RNA editing activity [J]. J Biol Chem, 2015, 290(16): 10136-10142.
[67]	Zhou WB, Cheng YX, Yap A, et al. The Arabidopsis gene YS1 encoding a DYW protein is required for editing of rpoB transcripts and the rapid development of chloroplasts during early growth [J]. Plant J, 2009, 58(1): 82-96.
[68]	Okuda K, Chateigner-Boutin AL, Nakamura T, et al. Pentatricopeptide repeat proteins with the DYW motif have distinct molecular functions in RNA editing and RNA cleavage in Arabidopsis chloroplasts [J]. Plant Cell, 2009, 21(1): 146-156.
[69]	Okuda K, Shikanai T. A pentatricopeptide repeat protein acts as a site-specificity factor at multiple RNA editing sites with unrelated Cis-acting elements in plastids [J]. Nucleic Acids Res, 2012, 40(11): 5052-5064.
[70]	Wagoner JA, Sun T, Lin L, et al. Cytidine deaminase motifs within the DYW domain of two pentatricopeptide repeat-containing proteins are required for site-specific chloroplast RNA editing [J]. J Biol Chem, 2015, 290(5): 2957-2968.
[71]	Chateigner-Boutin AL, Ramos-Vega M, Guevara-García A, et al. CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts [J]. Plant J, 2008, 56(4): 590-602.
[72]	Sun YK, Gutmann B, Yap A, et al. Editing of chloroplast rps14 by PPR editing factor EMB2261 is essential for Arabidopsis development [J]. Front Plant Sci, 2018, 9: 841.
[73]	Cai WH, Ji DL, Peng LW, et al. LPA66 is required for editing psbF chloroplast transcripts in Arabidopsis [J]. Plant Physiol, 2009, 150(3): 1260-1271.
[74]	Hammani K, Okuda K, Tanz SK, et al. A study of new Arabidopsis chloroplast RNA editing mutants reveals general features of editing factors and their target sites [J]. Plant Cell, 2009, 21(11): 3686-3699.
[75]	Okuda K, Hammani K, Tanz SK, et al. The pentatricopeptide repeat protein OTP82 is required for RNA editing of plastid ndhB and ndhG transcripts [J]. Plant J, 2010, 61(2): 339-349.
[76]	Chateigner-Boutin AL, des Francs-Small CC, Delannoy E, et al. OTP70 is a pentatricopeptide repeat protein of the E subgroup involved in splicing of the plastid transcript rpoC1 [J]. Plant J, 2011, 65(4): 532-542.
[77]	Liu XY, Jiang RC, Wang Y, et al. ZmPPR26, a DYW-type pentatricopeptide repeat protein, is required for C-to-U RNA editing at atpA-1148 in maize chloroplasts [J]. J Exp Bot, 2021, 72(13): 4809-4821.
[78]	Liu Y, He JN, Chen ZZ, et al. ABA overly-sensitive 5 (ABO5), encoding a pentatricopeptide repeat protein required for cis-splicing of mitochondrial nad2 intron 3, is involved in the abscisic acid response in Arabidopsis [J]. Plant J, 2010, 63(5): 749-765.
[79]	Zoschke R, Kroeger T, Belcher S, et al. The pentatricopeptide repeat-SMR protein ATP4 promotes translation of the chloroplast atpB/E mRNA [J]. Plant J, 2012, 72(4): 547-558.
[80]	Zoschke R, Watkins KP, Miranda RG, et al. The PPR-SMR protein PPR53 enhances the stability and translation of specific chloroplast RNAs in maize [J]. Plant J, 2016, 85(5): 594-606.
[81]	Miranda RG, Rojas M, Montgomery MP, et al. RNA-binding specificity landscape of the pentatricopeptide repeat protein PPR10 [J]. RNA, 2017, 23(4): 586-599.
[82]	Prikryl J, Rojas M, Schuster G, et al. Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein [J]. Proc Natl Acad Sci U S A, 2011, 108(1): 415-420.
[83]	He H, Cheng MX, Bao BW, et al. GhCTEF2 encodes a PLS-type PPR protein required for chloroplast development and plastid RNA editing in cotton [J]. Plant Sci, 2025, 355: 112478.
[84]	Hirose T, Kusumegi T, Sugiura M. Translation of tobacco chloroplast rps14 mRNA depends on a Shine-Dalgarno-like sequence in the 5'-untranslated region but not on internal RNA editing in the coding region [J]. FEBS Lett, 1998, 430(3): 257-260.
[85]	杜晓芬, 王智兰, 韩康妮, 等. 谷子叶绿体基因RNA编辑位点的鉴定与分析 [J]. 作物学报, 2022, 48(4): 873-885.
	Du XF, Wang ZL, Han KN, et al. Identification and analysis of RNA editing sites of chloroplast genes in foxtail millet [Setaria italica(L.) P.Beauv. [J]. Acta Agron Sin, 2022, 48(4): 873-885.
[86]	Royan S, Gutmann B, Colas des Francs-Small C, et al. A synthetic RNA editing factor edits its target site in chloroplasts and bacteria [J]. Commun Biol, 2021, 4(1): 545.
[87]	Manavski N, Mathieu S, Rojas M, et al. In vivo stabilization of endogenous chloroplast RNAs by customized artificial pentatricopeptide repeat proteins [J]. Nucleic Acids Res, 2021, 49(10): 5985-5997.
[88]	Kwok van der Giezen F, Honkanen S, Colas des Francs-Small C, et al. Applications of synthetic pentatricopeptide repeat proteins [J]. Plant Cell Physiol, 2024, 65(4): 503-515.
[89]	McDowell R, Small I, Bond CS. Synthetic PPR proteins as tools for sequence-specific targeting of RNA [J]. Methods, 2022, 208: 19-26.
[90]	Bernath-Levin K, Schmidberger J, Honkanen S, et al. Cofactor-independent RNA editing by a synthetic S-type PPR protein [J]. Synth Biol, 2021, 7(1): ysab034.
[91]	Zhang MY, Zhao YQ, Meng Y, et al. PPR proteins in the tea plant (Camellia sinensis) and their potential roles in the leaf color changes [J]. Sci Hortic, 2022, 293: 110745.
[92]	Zehrmann A, Härtel B, Glass F, et al. Selective Homo- and heteromer interactions between the multiple organellar RNA editing factor (MORF) proteins in Arabidopsis thaliana [J]. J Biol Chem, 2015, 290(10): 6445-6456.
[93]	Shi XW, Castandet B, Germain A, et al. ORRM5, an RNA recognition motif-containing protein, has a unique effect on mitochondrial RNA editing [J]. J Exp Bot, 2017, 68(11): 2833-2847.
[94]	Shi XW, Germain A, Hanson MR, et al. RNA recognition motif-containing protein ORRM4 broadly affects mitochondrial RNA editing and impacts plant development and flowering [J]. Plant Physiol, 2016, 170(1): 294-309.
[95]	Sun T, Shi XW, Friso G, et al. A zinc finger motif-containing protein is essential for chloroplast RNA editing [J]. PLoS Genet, 2015, 11(3): e1005028.
[96]	Sandoval R, Boyd RD, Kiszter AN, et al. Stable native RIP9 complexes associate with C-to-U RNA editing activity, PPRs, RIPs, OZ1, ORRM1 and ISE2 [J]. Plant J, 2019, 99(6): 1116-1126.
[97]	Wu J, Wang Y, Chen HD, et al. Solid-like condensation of MORF8 inhibits RNA editing under heat stress in Arabidopsis [J]. Nat Commun, 2025, 16(1): 2789.