Abstract
The plastid DNA (ptDNA) replication is initiated by primases, which synthesize RNA primers; following the synthesis of DNA fragments, primers must be removed before ligation. However, the enzymes and mechanisms underlying this process are poorly understood. Here we cloned a gene from maize that encodes a plastid-localized and Mn2+-dependent 5′–3′ exonuclease (designated PEN1) responsible for this process. The pen1 seeds show development and filling defects that intensify across generations. PEN1 cleaves the RNA primers, allowing for the complete excision of ribonucleotides. We reconstituted the plastid RNA primer removal processes in vitro. We also determined the crystal structure of the PEN1–dsDNA binary complex and explained the structural mechanism of the 5′ to 3′ exonuclease activity. Mutation of Pen1 resulted in the accumulation of ptDNA breaks, thereby compromising plastid function. These studies fill a critical gap that has long existed in the understanding of ptDNA replication.
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Data availability
Sequence data from this work can be found in the NCBI (https://www.ncbi.nlm.nih.gov/) under the following accession numbers: Pen1 (Zm00001d047988), LIG1 (Zm00001d032632), LIG4 (Zm00001d002390), LIG6 (Zm00001d043835), PolA (Zm00001D026402), Pol1B (Zm00001d024423), AtRNH1C (AT1G24090), SGT1 (Zm00001d044172) and B73 plastid genome (NC_001666.2). The BSA-seq data generated in this study have been deposited in the NCBI database and are publicly accessible with the accession code Bio Project PRJNA1177240. The RNA-seq data generated in this study have been deposited in the NCBI database and are publicly accessible with accession code Bio Project: PRJNA1191067. The DIP-seq data generated in this study have been deposited in the NCBI database and are publicly accessible with the accession code Bio Project: PRJNA1188804. The DEtail-seq data generated in this study have been deposited in the NCBI database and are publicly accessible with accession code Bio Project: PRJNA1187259. The model of PEN1–Mn and PEN1–DNA have been deposited in the Protein Data Bank (http://www.rcsb.org) under the accession numbers 9L56 and 9L55, respectively. Source data are provided with this paper.
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Acknowledgements
We thank J. Long from the Chinese Academy of Sciences (CAS) Center for Excellence in Molecular Plant Sciences for his advice on the project. We thank X. Zhu and X. Mao from the CAS Center for Excellence in Molecular Plant Sciences for their technical support in the false-coloured image. We thank W. Cai, L. Liu, Z. Zhang, X. Gao, N. Xu, L. Xu, S. Wang and J. Li (CAS Center for Excellence in Molecular Plant Sciences) for their technical support. We thank the staff at beamline BL10U2 of Shanghai Synchrotron Radiation Facility for their support in crystal data collection. We thank X. Zeng from Northeast Agricultural University for his assistance in cultivating genetic material. This research was supported by the National Science and Technology Major Project of the Ministry of Science and Technology of China (2022YFF1003302 to Y.W.), the National Natural Science Foundation of China (32430074 and 32525007 to Y.W. and 32425006 to Y.Z.), THE XPLORER PRIZE, NEW CORNERSTONE SCIENCE FOUNDATION (to Y.W.), Shanghai Academy of Natural Sciences (to Y.W.) and Postdoctoral Fellowship Program of CPSF (GZB20240745 to X.H.).
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Y.W., Y.Z., W.W. and X.H. designed the research. Y.W., Y.Z. and X.H. supervised the project. X.H., Q.X., Y.H., H.S., Q.W., Y.S., J.W., Y.C. and H.W. contributed to gene cloning, genotype analysis and phenotype analysis. X.H. contributed to microscope imaging, immunoblotting analysis, DIP-seq, slot blot, DEtail-seq, fluorescence immunostaining, the nuclease activity assay and protein purification. G.S. contributed to protein purification, crystallization, diffraction data collection and structure determination. J.F. and X.W. contributed to bioinformatics analysis. Y.W., Y.Z., W.W., X.H. and G.S. analysed the data and drafted and edited the manuscript.
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Extended data
Extended Data Fig. 1 Mutation Pen1 impaired the plant development.
a, Statistical analysis of plant height of B73 and pen1F2 at the heading stage (n = 40 biological replicates, two-tailed Student’s t-tests). The lower and upper whiskers indicate the minimum and maximum values, respectively. The upper boundary, middle line and lower boundary of the box indicate the 75th percentile, median and 25th percentile, respectively. Statistical testing was performed using an unpaired two-tailed t-test. b, Confocal laser scanning microscopy of chlorophyll autofluorescence in leaves depicted in magenta. A representative image is displayed for B73 (left) and pen1F2 (right, etiolated region). The regions marked with dashed white lines are shown in Fig. 1h. Scale bars: 20 μm. c, Statistical analysis of the chloroplast number for B73 and pen1F2. Four cells/leaf were measured (n = 6, biological replicates, two-tailed Student’s t-tests). The lower and upper whiskers indicate the minimum and maximum values, respectively. The upper boundary, middle line and lower boundary of the box indicate the 75th percentile, median and 25th percentile, respectively. Statistical testing was performed using an unpaired two-tailed t-test.
Extended Data Fig. 2 Genetic validation of Pen1.
a, Mapping-by-sequencing of pen1 (Top: SNP-index of the mutant-segregated pool; middle: SNP-index of the WT-segregated pool; bottom: the difference in SNP-index values between the two pools). The purple lines indicate the 99% confidence interval, and the orange lines indicate the 95% confidence interval. The red line indicates the ΔSNP-index values. b,c, RT-qPCR analysis of Pen1 expression pattern during various stages of seed development and the maternal tissue. Data are presented as individual values and means ± SD (n = 3, biological replicates). d, Construction of CRISPR/Cas9-mediated Pen1 knockout lines in the C01 inbred line genetic background. Two sgRNAs that specifically target Pen1 were designed, resulting in the identification of three allelic mutants: pen1CR-1, pen1CR-2, and pen1CR-3. e, Immunoblotting analysis of PEN1 in 14-DAP endosperms of C01, pen1cr-1, pen1cr-2 and pen1cr-3. ACTIN was used as an internal control. Three replicates, consistent results. f, Plant phenotypes of the segregated homozygous mutants from self-pollinated pen1CR-1/+, pen1CR-2/+, and pen1CR-3/+ ears. Scale bars: 25 cm. g, Ear phenotypes of the self-pollinated pen1CR-1/+, pen1CR-2/+, and pen1CR-3/+. The white arrows indicate the segregated homozygous mutant kernels. Scale bars: 1 cm. h, The allelic test of pen1 and other alleles. From panels 1 to 3, the pen1/+ ears were pollinated by pen1CR-1/+, pen1CR-2/+, and pen1CR-3/+, respectively. The white arrows indicate the segregated homozygous mutant seeds. From panels 4 to 6, the pen1F3 ears were pollinated by pen1CR-1/+, pen1CR-2/+, and pen1CR-3/+, respectively. Scale bars: 1 cm.
Extended Data Fig. 3 PEN1 encodes a typical 5′-3′ exonuclease.
a, Chromatogram from size exclusion chromatography and SDS-PAGE analysis of PEN1. M represents the protein Marker. Three replicates, consistent results. b,c, Cleavage activity of PEN1 on 30-nt ssDNA substrates in the presence of different metal ions. Various concentrations of Mg2+ and Mn2+ ranging from 0 mM to 10 mM were used for the analysis. M, molecular Marker (values indicate the number of nucleotides). The green stars represent the /6FAMdT/ modification. Reactions were terminated at 15 min and analyzed on a high-resolution denaturing polyacrylamide gel. Three replicates, consistent results. d, Cleavage activity of PEN1 on 30-nt ssDNA substrates with P-S modifications at different sites from 5′ to 3′ end. The sites of the P-S modifications were indicated in the substrate diagram. M, molecular Marker (values indicate the number of nucleotides). The green stars represent the /6FAMdT/ modification. Reactions were terminated at 15 min and analyzed on a high-resolution denaturing polyacrylamide gel. Three replicates, consistent results.
Extended Data Fig. 4 Characterization of different DNA Ligases, Pol1A and Pol1B.
a,b,c, Subcellular localization of LIG4-GFP, LIG6-GFP, and LIG1-GFP in N.benthamiana leaf epidermal cells. Chl, chlorophyll autofluorescence (magenta). DAPI was used to stain the nucleus. Scale bars: 10 μm. More than six replicates, consistent results. d, High-resolution image of LIG1-TDT in the chloroplast. DAPI was used to stain the nucleus and chloroplast nucleoids. The PEN1-GFP was used for co-localization analysis. Scale bars: 2 μm. More than six replicates, consistent results. e, Purity analysis of LIG1 (253-909aa), Pol1A (257-1052aa), and Pol1B (245-1039aa). SDS-PAGE analysis of the LIG1, Pol1A, and Pol1B. M represents the protein molecular Marker. Three replicates, consistent results. f, Subcellular localization of Pol1A-GFP in N.benthamiana leaf epidermal cells. Scale bars: 10 μm. More than six replicates, consistent results. g, High-resolution image of Pol1A-TDT in the chloroplast. The PEN1-GFP was used for co-localization analysis. Scale bars: 2 μm. More than six replicates, consistent results. h, Subcellular localization of Pol1B-GFP in N.benthamiana leaf epidermal cells. Scale bars: 10 μm. More than six replicates, consistent results. i, High-resolution image of Pol1B-TDT in the chloroplast. The PEN1-GFP was used for co-localization analysis. Scale bars: 2 μm. More than six replicates, consistent results. j, Phylogeny of plastid Pol1A and Pol1B homologs in representative plant taxa. The simplified phylogenetic tree illustrates the relationships among plant species from which Pol1A and Pol1B homologs were identified. Given the high protein similarity between Pol1A and Pol1B, only Pol1A was selected for phylogenetic analysis.
Extended Data Fig. 5 The strand-displacement activity analysis of the Pol1A and Pol1B.
a, Schematic of the linear gapped substrates used in strand-displacement assays, with the resulting products depicted in each corresponding diagram. The magenta lines indicate the ribonucleotides. The green star represents the /6FAMdT/ modification. To prevent end-binding by the Pol1A and Pol1B, all the unlabeled ends were blocked by the streptavidin. The black balls represent the streptavidin modification. b, Coupled primer extension and ligation mediated by Pol1A, Pol1B, and LIG1. The displaced primer is 5 nt longer than the template strand, so the ligated product (65 nt) can be distinguished from the displaced product (60 nt), which is the same size as the template strand. The black balls represent the streptavidin modification. M, molecular Marker (values indicate the number of nucleotides). The green stars represent the /6FAMdT/ modification. Reactions were terminated at 15 min and analyzed on a high-resolution denaturing polyacrylamide gel. Three replicates, consistent results.
Extended Data Fig. 6 Overall structure of PEN1-Mn and comparison of the catalytic centers of PEN1-Mn and PEN1D249A-Mg-dsDNA.
a, Sequence alignment of PEN1 with other homologous 5′-3′ exoribonucleases. The red dots represent the conserved aspartic acid residues at the catalytic center. (Ms, Mycobacterium smegmatis; Mt, Mycobacterium tuberculosis; T5 EXO, T5 phage D15 exonuclease; EcPol_N, Escherichia coli DNA polymerase 1 N terminal exonuclease domain (1-325)) b, The overall structure of PEN1-Mn. One asymmetric unit (ASU) contains two PEN1-Mn protomers. c, The superposition of PEN1-Mn protomer A and B (RMSD = 0.739) d, Chromatogram from size exclusion chromatography and SDS-PAGE analysis of PEN1D249A. M represents the protein Marker. Three replicates, consistent results. e, Cleavage activity of PEN1 and PEN1D249A on 30-nt ssDNA substrates. M, molecular markers (values indicate the number of nucleotides). The green stars represent the /6FAMdT/. Three replicates, consistent results. f, The comparison of the metal ions coordination network between PEN1-Mn (green) and PEN1D249A-Mg-dsDNA (blue). The superimposition reveals no differences in protein secondary structures (RMSD = 0.707 Å) but a slight location difference of metal ion (Mg1 vs Mn1) in the PEN1D249A-Mg-dsDNA compared with PEN1-Mn due to the D249A mutation. g, Details of the differences in the catalytic center of PEN1-Mn and PEN1D249A-Mg-dsDNA. The D249A mutation causes Mg(1) in the catalytic center to shift 3.6 Å towards D226, compared to Mn(1) in the PEN1-Mn structure. h,i, Simulated Fo-Fc map (contoured at 3.0) of the side chains of key residues and the metal ions within the catalytic center of PEN1-Mn and PEN1D249A-Mg-dsDNA.
Extended Data Fig. 7 Overall structure of PEN1D249A-Mg-dsDNA and the detailed interactions between PEN1 and dsDNA.
a, The overall structure of PEN1D249A-Mg-dsDNA. One ASU comprises two protomers (protomer A and protomer B colored by blue and salmon, respectively), which bind to the ends of the double-stranded DNA, respectively. b,The superposition of two protomers of PEN1D249A-Mg-dsDNA. No differences between the two PEN1 protomers in terms of overall structure and metal ion positioning. The dsDNA of protomer A extends into the catalytic center, whereas the dsDNA of protomer B is positioned near the entrance of the catalytic center. The 5′ phosphates of the cleavage strands bound to protomers A and B are labeled by red and yellow dots, respectively. c,d, The sequence, and 2Fo-Fc map (contoured at 1.8) of the F2 DNA used in PEN1D249A-Mg-dsDNA structure. The gray letters indicate nucleotides disordered in the structure. e,f, The simulated Fo-Fc map (contoured at 3.0) of DNA-contacting residues in the active center of the PEN1-protomer A. g, The simulated Fo-Fc map (contoured at 3.0) of distal DNA-contacting residues of the PEN1-protomer A. h, The comparison of the crystal structure of PEN1D249A-Mg-dsDNA structure (B-form dsDNA) with a structure model of PEN1D249A-DNA/RNA hybrid (A-form DNA-RNA hybrid). The structure model of PEN1D249A-DNA/RNA hybrid was made by the superimposition of the first 5′terminal three ribonucleotides of the RNA strand of a standard DNA-RND hybrid on the first 5′terminal three deoxyribonucleotides of the cleavage strand of the dsDNA in PEN1D249A-Mg-dsDNA structure. The structure comparison suggests that PEN1 can accommodate the 5′ terminal three ribonucleotides of the DNA-RNA hybrid in a similar way as for the 5′ terminal three deoxyribonucleotides of the dsDNA without steric clash with the A-form DNA-RNA hybrid.
Supplementary information
Supplementary Table 1
Primers used.
Supplementary Table 2
Oligonucleotide probes used.
Supplementary Table 3
Oligonucleotide probes annealing protocol.
Supplementary Table 4
Codon-optimized Pen1(amino acids 92–422) sequence.
Supplementary Table 5
Data collection and refinement statistics for PEN1-Mn and PEN1D249A–Mg–dsDNA.
Source data
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Huang, X., Shi, G., Xiao, Q. et al. PEN1 catalyses RNA primer removal during plastid DNA replication in maize. Nat. Plants 11, 1325–1338 (2025). https://doi.org/10.1038/s41477-025-02027-4
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DOI: https://doi.org/10.1038/s41477-025-02027-4
