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PPR Proteins in Plant Growth and Development

Pentatricopeptide repeat (PPR) proteins are characterized by the presence of tandem arrays of a degenerate 35-amino-acid repeat motif, PPR motif. Based on the types of motif and their arrangement, PPR proteins are divided into two classes, P and PLS. P-class proteins only contain canonical P-motifs with 35 amino acids, whereas PLS-class proteins consist of P-, L- (35 or 36 amino acids), and S- (31 or 32 amino acids) motifs forming tandemly repeated PLS triplets. 

  • PPR protein
  • cytoplasmic male sterility
  • seed development

1. Introduction

Pentatricopeptide repeat (PPR) proteins are characterized by the presence of tandem arrays of a degenerate 35-amino-acid repeat motif, PPR motif [1]. Based on the types of motif and their arrangement, PPR proteins are divided into two classes, P and PLS. P-class proteins only contain canonical P-motifs with 35 amino acids, whereas PLS-class proteins consist of P-, L- (35 or 36 amino acids), and S- (31 or 32 amino acids) motifs forming tandemly repeated PLS triplets [2]. Many of the PLS-class proteins are carboxyl terminally extended with highly conserved E, E+, or DYW domains. Thus, PLS-class proteins can be further divided into PLS, E, E+, and DYW subclasses according to the domains identified in carboxyl terminal [3].
PPR proteins are sequence-specific RNA-binding proteins that are mostly localized to mitochondria and/or chloroplasts, where they are involved in RNA post-transcriptional processing [4] (Figure 1A). In general, the P-class PPR proteins mediate diverse aspects of RNA processing in plant organelles, while the PLS-class PPR proteins mainly function in RNA editing [5]. Mutations in these PPR protein-coding genes lead to the dysfunction of mitochondria and/or chloroplasts, thereby resulting in growth retardation, pollen abortion, and seed development defects in plants [4], indicating the important roles of PPR proteins in plant growth and development (Figure 1B).
Figure 1. The functions of PPR proteins in plants. (A) The molecular functions of PPR proteins in plant mitochondria and chloroplasts. PPR proteins are encoded by nuclear genes, translated in the cytoplasm, and then imported into mitochondrion or chloroplast to mediate multiple steps of RNA processing. (B) The main growing and developmental phenotypes of plant mutants of PPR protein-coding genes.

2. Functions of PPR Proteins in Cytoplasmic Male Sterility

Cytoplasmic male sterility (CMS) is a maternally inherited trait that presents a defect in the production of viable pollen. CMS is widespread in higher plants, and has been widely used in the production of hybrid seeds and utilization of heterosis in many crop species [6][7]. Plant CMS is usually caused by mutations, rearrangements, or recombinations of mitochondrial DNA, and in many instances, male fertility can be restored specifically by restorer-of-fertility (Rf) genes in the nuclear genome [8][9]. To date, more than ten Rf genes have been cloned and functionally characterized in various crop species, and the majority of them were found to encode PPR protein, including Rf1a [10]Rf1b [11]Rf3 [12]Rf4 [13]Rf5 [14]Rf6 [15] in rice; Rfo [16]PPR-B [17]RsRf3-4 [18]Rfk1 [19] in radish; Rf1 [20]Rf2 [21] in sorghum; Rfp [22]Rfn [23] in rapeseed; Rf-PPR592 [24] in petunia; BrRfp1 [25] in Chinese cabbage; and Rfm1 [26] in barley. With the exception of the sorghum Rf1 [20] and the barely Rfm1 [26], the PPR-type Rf genes encode PPR proteins belonging to P class.
Members of P-class PPR proteins mostly function in various post-transcriptional process of organellar RNAs, such as RNA splicing, RNA stabilization, RNA cleavage, and translation [4][5]. Proteins encoded by Rf genes usually target mitochondria and act as fertility restorers by suppressing the production of mitochondrial CMS-inducing proteins [6][11]; however, the exact molecular mechanisms underlying fertility restoration by RF proteins is presently unclear. The PPR-type RF proteins have been proposed to rescue fertility by regulating the expression of CMS-conferring genes through the similar molecular mechanisms as that of other PPR proteins. In most of the CMS systems, PPR-type RF proteins bind to the mitochondrial CMS-conferring transcripts and promote their cleavage or degradation [27]. For example, rice RF1A and RF1B proteins, respectively encoded by Rf1a and Rf1b genes, have been considered to restore CMS by processing mitochondrial orf79 transcript via different mechanisms. RF1A directly binds to and cleaves the atp6-orf79 transcript at the intercistronic region, whereas RF1B promotes the rapid degradation of the atp6-orf79 transcript [10][11]. The protein encoded by rice Rf4 gene was reported to suppress WA352-mediated male sterility by reducing WA352 transcript levels [13]. Two rice RF proteins, Rfp and Rfn, are involved in transcript cleavage of orf224 and orf222, respectively [22][23].
In some CMS systems, PPR-type RF proteins restore the male fertility by impeding the translation or post-translational processing of mitochondrial CMS-inducing proteins. Studies on radish PPR-B revealed that PPR-B protein does not function through cleavage or degradation of the orf138 mRNA, but rather block its translation by inhibiting either the association with or the progression of mitochondrial ribosomes on the orf138 mRNA [17]. Similarly, rice RF3 protein does not affect the abundance of WA352 transcript but suppresses the accumulation of WA352 protein [12]. In addition, Rf1 from sorghum and Rfm1 from barely encode PPR proteins belonging to PLS class. As PLS-class PPR proteins almost exclusively play a role in RNA editing, it is possible that sorghum Rf1 and barely Rfm1 restore pollen fertility by editing S-orf transcripts or other target RNAs [8][26].
CMS was not only an ideal model system to study the interaction between mitochondrial and nuclear genomes but also a useful genetic tool for breeding to exploit hybrid vigor in crops [27]. Although PPR proteins are involved in the restoration of male fertility, functions of most PPR proteins are still obscure. Therefore, exploring the functions of PPR proteins will contribute to understanding the CMS mechanism and improving molecular breeding in crops.

3. Functions of PPR Proteins in Seed Development

In angiosperm plants, seed development starts with double fertilization of egg and central cells with two sperm cells, which leads to the formation of a diploid embryo and a triploid endosperm, and develops into mature seeds comprising three structures: maternal coat, embryo, and endosperm [28]. Development of embryo and endosperm is well correlated and regulated by numerous distinct proteins involved in many important physiological processes [29], including cell growth, RNA transcription and post-transcriptional processing, etc.
In recent years, more and more genetic and biochemical studies have shown that PPR proteins play important roles in seed development of higher plants, and loss-of-function of these PPR proteins usually leads to defects in embryogenesis and/or endosperm development [4][30]. According to the phenotypic expression, seed mutants can be divided into four major classes: empty pericarp (emp), embryo specific (emb), defective kernel (dek), and small kernel (smk). A detailed summary of the maize and Arabidopsis seed mutants caused by the functional defects of PPR proteins is provided in Table 1.
Table 1. Selected functionally characterized PPR proteins essential for seed development in maize and Arabidopsis.
Species Subcellular
Localization
Mutant
Phenotype
Protein
Name
PPR
Class
Function(s) References
Maize Mitochondrion dek DEK2 P RNA splicing, nad1 intron 1 [31]
Mitochondrion dek DEK10 PLS RNA editing, nad3-61, 62, and cox2-550 [32]
Mitochondrion dek DEK35 P RNA splicing, nad4 intron 1 [33]
Mitochondrion dek DEK36 PLS RNA editing, atp4-59, nad7-383, and ccmFN-302 [34]
Mitochondrion dek DEK37 P RNA splicing, nad2 intron 1 [35]
Mitochondrion dek DEK39 PLS RNA editing, nad3-247 and nad3-275 [36]
Mitochondrion dek DEK40 PLS RNA editing, cox3-314, nad2-26, and nad5-1916 [37]
Mitochondrion dek DEK41/
DEK43
P RNA splicing, nad4 intron 1 and 3 [38][39]
Mitochondrion dek DEK46 PLS RNA editing, D5-C22 of nad7 intron 3 and 4 [40]
Mitochondrion dek DEK53 PLS RNA editing, multiples sites [41]
Mitochondrion dek DEK55 PLS RNA splicing, nad4 intron 1 and 3;RNA editing, multiple sites [42]
Mitochondrion dek DEK605 PLS RNA editing, nad1-608 [43]
Mitochondrion smk SMK1 PLS RNA editing, nad7-836 [44]
Mitochondrion smk SMK4 PLS RNA editing, cox1-1489 [45]
Mitochondrion smk SMK6 PLS RNA editing, nad1-740, nad4L-110, nad7-739, and mttB-138, 139 [46]
Mitochondrion smk ZmSMK9 P RNA splicing, nad5 intron 1 and 4 [47]
Mitochondrion smk PPR2263 PLS RNA editing, nad5-1550 and cob-908 [48]
Mitochondrion smk MPPR6 P Translation, rps3 mRNA [49]
Mitochondrion dek/smk PPR20 P RNA splicing, nad2 intron 3 [50]
Mitochondrion smk PPR78 P RNA stabilization, nad5 mature mRNA [51]
Mitochondrion emp EMP4 P Expression of mitochondrial transcripts [52]
Mitochondrion emp EMP5 PLS RNA editing, multiple sites [53]
Mitochondrion emp EMP7 PLS RNA editing, ccmFN-1553 [54]
Mitochondrion emp EMP8 P RNA splicing, nad1 intron 4, nad2 intron 1, and nad4 intron 1 [55]
Mitochondrion emp EMP9 PLS RNA editing, ccmB-43 and rps4-335 [56]
Mitochondrion emp EMP10 P RNA splicing, nad2 intron 1 [57]
Mitochondrion emp EMP11 P RNA splicing, nad1 intron 1, 2, 3, and 4 [58]
Mitochondrion emp EMP12 P RNA splicing, nad2 intron 1, 2, and 4 [59]
Chloroplast smk qKW9 PLS RNA editing, NdhB-246 [60]
Mitochondrion emp EMP16 P RNA splicing, nad2 intron 4 [61]
Mitochondrion emp EMP17 PLS RNA editing, ccmFC-799 and nad2-677 [62]
Mitochondrion emp EMP18 PLS RNA editing, atp6-635 and cox2-449 [63]
Mitochondrion emp EMP21 PLS RNA editing, multiple sites [64]
Mitochondrion emp EMP32 P RNA splicing, nad7 intron 2 [65]
Mitochondrion emp EMP602 P RNA splicing, nad4 intron 1 and 3 [66]
Mitochondrion emp EMP603 P RNA splicing, nad1 intron 2 [67]
Mitochondrion emp PPR14 P RNA splicing, nad2 intron 3, nad7 intron 1 and 2 [68]
Mitochondrion emp PPR18 P RNA splicing, nad4 intron 1 [69]
Mitochondrion emp PPR27 PLS RNA editing, multiple sites [70]
Mitochondrion emp PPR101 P RNA splicing, nad5 intron 1 and 2 [71]
Mitochondrion emp PPR231 P RNA splicing, nad5 intron 1, 2, 3 and nad2 intron 3 [71]
Mitochondrion emp PPR-SMR1 P RNA splicing, multiple introns [72]
Chloroplast emb PPR8522 P RNA transcription, nearly all chloroplast-encoded genes [73]
Chloroplast emb EMB-7L P RNA splicing, multiple introns [74]
Arabidopsis Mitochondrion dek OTP43 P RNA splicing, nad1 intron 1 [75]
Mitochondrion smk PPR19 P RNA stabilization, nad1 mature mRNA [76]
Mitochondrion emp BLX PLS RNA editing, multiple sites; RNA splicing, nad1 intron 4 and nad2 intron 1 [77]
Chloroplast emb AtPPR2 P RNA translation [78]
Chloroplast emb ECD2 P RNA splicing, ndhAycf3 intron 1, rps12 intron 2 and clpp intron 2 [79]
Chloroplast emb EMB2654 P RNA splicing, rps12 intron 1 [80]
Mitochondrion emb EMB2794 P RNA splicing, nad2 intron 2 [81]
Nucleus emb GRP23 P RNA transcription [82]
Mitochondrion emb MID1 P RNA splicing, nad2 intron 1 [83]
Chloroplast emb PMD3 P RNA splicing, trnAndhB, and clpP-1 [84]
Most PPR proteins identified to date are targeted to mitochondria and/or chloroplasts [4]. The disruption of PPR proteins localized to chloroplasts usually results in the emb mutants that are defective in embryogenesis, but relatively normal in endosperm development. For instance, PPR8522 [73] and EMB-7L [74] in maize and GRP23 [82] in Arabidopsis are necessary for embryogenesis, and their mutations lead to arrested embryo development at the transition stage, resulting in an embryo-lethal phenotype. For mitochondrion-targeted PPR proteins, their disruptions mostly cause diverse seed development mutants, including smkdek, and emp, with different degrees of defects in embryo and endosperm. The loss-of-function of SMK1 [44], SMK4 [45], SMK6 [46], ZmSMK9 [47], PPR2263 [48], and MPPR6 [49] in maize and PPR19 [76] in Arabidopsis arrests both embryo and endosperm development, resulting in smk phenotypes. Some characterized mitochondrion-targeted PPR proteins, such as DEK2 [31], DEK10 [32], DEK35 [33], DEK36 [34], DEK37 [35], DEK39 [36], DEK40 [37], DEK41/43 [38][39], DEK46 [40], and DEK53 [41] in maize, are necessary for seed development, and their disruptions result in dek mutants with arrested development of both the embryo and endosperm at an early stage. Meanwhile, many PPR proteins are targeted to mitochondria and function in development of both embryo and endosperm, and mutations in their encoding genes arrest embryo and endosperm development at early stages and even result in embryo lethality. For example, Emp5 encodes a mitochondrion-targeted DYW-type PPR protein, the emp5 mutants exhibit abortion of embryo and endosperm development at early stages in maize [53]. Loss-of-function of the mitochondrial P-type PPR protein EMP10 severely disturbs embryo and endosperm development, resulting in empty pericarp or papery seeds in maize [57]. Additionally, the P-type protein PPR5 was recently identified as a regulator required for endosperm development in rice, the ppr5 mutants develop small starch grains [85].

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  51. Zhang, Y.F.; Suzuki, M.; Sun, F.; Tan, B.C. The mitochondrion-targeted PENTATRICOPEPTIDE REPEAT78 protein is required for nad5 mature mRNA stability and seed development in maize. Mol. Plant 2017, 10, 1321–1333.
  52. Gutierrez-Marcos, J.F.; Dal Pra, M.; Giulini, A.; Costa, L.M.; Gavazzi, G.; Cordelier, S.; Sellam, O.; Tatout, C.; Paul, W.; Perez, P.; et al. Empty pericarp4 encodes a mitochondrion-targeted pentatricopeptide repeat protein necessary for seed development and plant growth in maize. Plant Cell 2007, 19, 196–210.
  53. Liu, Y.J.; Xiu, Z.H.; Meeley, R.; Tan, B.C. Empty pericarp5 encodes a pentatricopeptide repeat protein that is required for mitochondrial RNA editing and seed development in maize. Plant Cell 2013, 25, 868–883.
  54. Sun, F.; Wang, X.M.; Bonnard, G.; Shen, Y.; Xiu, Z.H.; Li, X.J.; Gao, D.H.; Zhang, Z.H.; Tan, B.C. Empty pericarp7 encodes a mitochondrial E-subgroup pentatricopeptide repeat protein that is required for ccmFN editing, mitochondrial function and seed development in maize. Plant J. 2015, 84, 283–295.
  55. Sun, F.; Zhang, X.Y.; Shen, Y.; Wang, H.C.; Liu, R.; Wang, X.M.; Gao, D.H.; Yang, Y.Z.; Liu, Y.W.; Tan, B.C. The pentatricopeptide repeat protein EMPTY PERICARP8 is required for the splicing of three mitochondrial introns and seed development in maize. Plant J. 2018, 95, 919–932.
  56. Yang, Y.Z.; Ding, S.; Wang, H.C.; Sun, F.; Huang, W.L.; Song, S.; Xu, C.H.; Tan, B.C. The pentatricopeptide repeat protein EMP9 is required for mitochondrial ccmB and rps4 transcript editing, mitochondrial complex biogenesis and seed development in maize. New Phytol. 2017, 214, 782–795.
  57. Cai, M.J.; Li, S.Z.; Sun, F.; Sun, Q.; Zhao, H.L.; Ren, X.M.; Zhao, Y.X.; Tan, B.C.; Zhang, Z.X.; Qiu, F.Z. Emp10 encodes a mitochondrial PPR protein that affects the cis-splicing of nad2 intron 1 and seed development in maize. Plant J. 2017, 91, 132–144.
  58. Ren, X.M.; Pan, Z.Y.; Zhao, H.L.; Zhao, J.L.; Cai, M.J.; Li, J.; Zhang, Z.X.; Qiu, F.Z. EMPTY PERICARP11 serves as a factor for splicing of mitochondrial nad1 intron and is required to ensure proper seed development in maize. J. Exp. Bot. 2017, 68, 4571–4581.
  59. Sun, F.; Xiu, Z.H.; Jiang, R.C.; Liu, Y.W.; Zhang, X.Y.; Yang, Y.Z.; Li, X.J.; Zhang, X.; Wang, Y.; Tan, B.C. The mitochondrial pentatricopeptide repeat protein EMP12 is involved in the splicing of three nad2 introns and seed development in maize. J. Exp. Bot. 2019, 70, 963–972.
  60. Huang, J.; Lu, G.; Liu, L.; Raihan, M.S.; Xu, J.T.; Jian, L.M.; Zhao, L.X.; Tran, T.M.; Zhang, Q.H.; Liu, J.; et al. The kernel size-related quantitative trait locus qKW9 encodes a pentatricopeptide repeat protein that affects photosynthesis and grain filling. Plant Physiol. 2020, 183, 1696–1709.
  61. Xiu, Z.H.; Sun, F.; Shen, Y.; Zhang, X.Y.; Jiang, R.C.; Bonnard, G.; Zhang, J.H.; Tan, B.C. EMPTY PERICARP16 is required for mitochondrial nad2 intron 4 cis-splicing, complex I assembly and seed development in maize. Plant J. 2016, 85, 507–519.
  62. Wang, Y.; Liu, X.Y.; Huang, Z.Q.; Li, Y.Y.; Yang, Y.Z.; Sayyed, A.; Sun, F.; Gu, Z.Q.; Wang, X.M.; Tan, B.C. PPR-DYW protein EMP17 is required for mitochondrial RNA editing, complex III biogenesis, and seed development in maize. Front. Plant Sci. 2021, 12, 693272.
  63. Li, X.L.; Huang, W.L.; Yang, H.H.; Jiang, R.C.; Sun, F.; Wang, H.C.; Zhao, J.; Xu, C.H.; Tan, B.C. EMP18 functions in mitochondrial atp6 and cox2 transcript editing and is essential to seed development in maize. New Phytol. 2019, 221, 896–907.
  64. Wang, Y.; Liu, X.Y.; Yang, Y.Z.; Huang, J.; Sun, F.; Lin, J.S.; Gu, Z.Q.; Sayyed, A.; Xu, C.H.; Tan, B.C. Empty Pericarp21 encodes a novel PPR-DYW protein that is required for mitochondrial RNA editing at multiple sites, complexes I and V biogenesis, and seed development in maize. PLoS Genet. 2019, 15, e1008305.
  65. Yang, Y.Z.; Ding, S.; Liu, X.Y.; Tang, J.J.; Wang, Y.; Sun, F.; Xu, C.H.; Tan, B.C. EMP32 is required for the cis-splicing of nad7 intron 2 and seed development in maize. RNA Biol. 2021, 18, 499–509.
  66. Ren, Z.J.; Fan, K.J.; Fang, T.; Zhang, J.J.; Yang, L.; Wang, J.H.; Wang, G.Y.; Liu, Y.J. Maize Empty pericarp602 encodes a P-type PPR protein that is essential for seed development. Plant Cell Physiol. 2019, 60, 1734–1746.
  67. Fan, K.J.; Ren, Z.J.; Zhang, X.F.; Liu, Y.; Fu, J.J.; Qi, C.L.; Tatar, W.; Rasmusson, A.G.; Wang, G.Y.; Liu, Y.J. The pentatricopeptide repeat protein EMP603 is required for the splicing of mitochondrial Nad1 intron 2 and seed development in maize. J. Exp. Bot. 2021, erab339.
  68. Wang, H.C.; Chen, Z.L.; Yang, Y.Z.; Sun, F.; Ding, S.; Li, X.L.; Xu, C.H.; Tan, B.C. PPR14 interacts with PPR-SMR1 and CRM protein Zm-mCSF1 to facilitate mitochondrial intron splicing in maize. Front. Plant Sci. 2020, 11, 732.
  69. Liu, R.; Cao, S.K.; Sayyed, A.; Xu, C.H.; Sun, F.; Wang, X.M.; Tan, B.C. The mitochondrial pentatricopeptide repeat protein PPR18 is required for the cis-splicing of nad4 intron 1 and essential to seed development in maize. Int. J. Mol. Sci. 2020, 21, 4047.
  70. Liu, R.; Cao, S.K.; Sayyed, A.; Yang, H.H.; Zhao, J.; Wang, X.M.; Jia, R.X.; Sun, F.; Tan, B.C. The DYW-subgroup pentatricopeptide repeat protein PPR27 functions on editing of multiple mitochondrial transcripts and interacts with ZmMORF1 in maize. J. Exp. Bot. 2020, 71, 5495–5505.
  71. Yang, H.H.; Xiu, Z.H.; Wang, L.; Cao, S.K.; Li, X.L.; Sun, F.; Tan, B.C. Two pentatricopeptide repeat proteins are required for the splicing of nad5 introns in maize. Front. Plant Sci. 2020, 11, 732.
  72. Chen, Z.L.; Wang, H.C.; Shen, J.Y.; Sun, F.; Wang, M.D.; Xu, C.H.; Tan, B.C. PPR-SMR1 is required for the splicing of multiple mitochondrial introns, interacts with Zm-mCSF1, and is essential for seed development in maize. J. Exp. Bot. 2019, 70, 5245–5258.
  73. Sosso, D.; Canut, M.; Gendrot, G.; Dedieu, A.; Chambrier, P.; Barkan, A.; Consonni, G.; Rogowsky, P.M. PPR8522 encodes a chloroplast-targeted pentatricopeptide repeat protein necessary for maize embryogenesis and vegetative development. J. Exp. Bot. 2012, 63, 5843–5857.
  74. Yuan, N.N.; Wang, J.C.; Zhou, Y.; An, D.; Xiao, Q.; Wang, W.Q.; Wu, Y.R. EMB-7L is required for embryogenesis and plant development in maize involved in RNA splicing of multiple chloroplast genes. Plant Sci. 2019, 287, 110203.
  75. De Longevialle, A.F.; Meyer, E.H.; Andres, C.; Taylor, N.L.; Lurin, C.; Millar, A.H.; Small, I.D. The pentatricopeptide repeat gene OTP43 is required for trans-splicing of the mitochondrial nad1 intron 1 in Arabidopsis thaliana. Plant Cell 2007, 19, 3256–3265.
  76. Lee, K.; Han, J.H.; Park, Y.I.; Colas des Francs-Small, C.; Small, I.; Kang, H. The mitochondrial pentatricopeptide repeat protein PPR19 is involved in the stabilization of NADH dehydrogenase 1 transcripts and is crucial for mitochondrial function and Arabidopsis thaliana development. New Phytol. 2017, 215, 202–216.
  77. Sun, Y.; Huang, J.Y.; Zhong, S.; Gu, H.Y.; He, S.; Qu, L.J. Novel DYW-type pentatricopeptide repeat (PPR) protein BLX controls mitochondrial RNA editing and splicing essential for early seed development of Arabidopsis. J. Genet. Genom. 2018, 45, 155–168.
  78. Lu, Y.Q.; Li, C.; Wang, H.; Chen, H.; Berg, H.; Xia, Y.J. AtPPR2, an Arabidopsis pentatricopeptide repeat protein, binds to plastid 23S rRNA and plays an important role in the first mitotic division during gametogenesis and in cell proliferation during embryogenesis. Plant J. 2011, 67, 13–25.
  79. Wang, X.W.; An, Y.Q.; Qi, Z.; Xiao, J.W. PPR protein early chloroplast development 2 is essential for chloroplast development at the early stage of Arabidopsis development. Plant Sci. 2021, 308, 110908.
  80. Aryamanesh, N.; Ruwe, H.; Sanglard, L.V.P.; Eshraghi, L.; Bussell, J.D.; Howell, K.A.; Small, I.; Colas des Francs-Small, C. The pentatricopeptide repeat protein EMB2654 is essential for trans-splicing of a chloroplast small ribosomal subunit transcript. Plant Physiol. 2017, 173, 1164–1176.
  81. Marchetti, F.; Cainzos, M.; Shevtsov, S.; Córdoba, J.P.; Sultan, L.D.; Brennicke, A.; Takenaka, M.; Pagnussat, G.; Ostersetzer-Biran, O.; Zabaleta, E. Mitochondrial pentatricopeptide repeat protein, EMB2794, plays a pivotal role in NADH dehydrogenase subunit nad2 mRNA maturation in Arabidopsis thaliana. Plant Cell Physiol. 2020, 61, 1080–1094.
  82. Ding, Y.H.; Liu, N.Y.; Tang, Z.S.; Liu, J.; Yang, W.C. Arabidopsis GLUTAMINE-RICH PROTEIN23 is essential for early embryogenesis and encodes a novel nuclear PPR motif protein that interacts with RNA polymerase II subunit III. Plant Cell 2006, 18, 815–830.
  83. Zhao, P.; Wang, F.; Li, N.; Shi, D.Q.; Yang, W.C. Pentatricopeptide repeat protein MID1 modulates nad2 intron 1 splicing and Arabidopsis development. Sci Rep. 2020, 10, 2008.
  84. Zhang, J.; Xiao, J.W.; Li, Y.Q.; Su, B.D.; Xu, H.M.; Shan, X.Y.; Song, C.W.; Xie, J.B.; Li, R.L. PDM3, a pentatricopeptide repeat-containing protein, affects chloroplast development. J. Exp. Bot. 2017, 68, 5615–5627.
  85. Zhang, L.; Qi, Y.Z.; Wu, M.M.; Zhao, L.; Zhao, Z.C.; Lei, C.L.; Hao, Y.Y.; Yu, X.W.; Sun, Y.L.; Zhang, X.; et al. Mitochondrion-targeted PENTATRICOPEPTIDE REPEAT5 is required for cis-splicing of nad4 intron 3 and endosperm development in rice. Crop J. 2021, 9, 282–296.
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    Li, X. PPR Proteins in Plant Growth and Development. Encyclopedia. Available online: https://encyclopedia.pub/entry/15530 (accessed on 25 June 2022).
    Li X. PPR Proteins in Plant Growth and Development. Encyclopedia. Available at: https://encyclopedia.pub/entry/15530. Accessed June 25, 2022.
    Li, Xiulan. "PPR Proteins in Plant Growth and Development," Encyclopedia, https://encyclopedia.pub/entry/15530 (accessed June 25, 2022).
    Li, X. (2021, October 29). PPR Proteins in Plant Growth and Development. In Encyclopedia. https://encyclopedia.pub/entry/15530
    Li, Xiulan. ''PPR Proteins in Plant Growth and Development.'' Encyclopedia. Web. 29 October, 2021.
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