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Genome-wide analysis of the core DNA replication machinery in the higher plants Arabidopsis and rice - PubMed

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Genome-wide analysis of the core DNA replication machinery in the higher plants Arabidopsis and rice

Randall W Shultz et al. Plant Physiol. 2007 Aug.

Abstract

Core DNA replication proteins mediate the initiation, elongation, and Okazaki fragment maturation functions of DNA replication. Although this process is generally conserved in eukaryotes, important differences in the molecular architecture of the DNA replication machine and the function of individual subunits have been reported in various model systems. We have combined genome-wide bioinformatic analyses of Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa) with published experimental data to provide a comprehensive view of the core DNA replication machinery in plants. Many components identified in this analysis have not been studied previously in plant systems, including the GINS (go ichi ni san) complex (PSF1, PSF2, PSF3, and SLD5), MCM8, MCM9, MCM10, NOC3, POLA2, POLA3, POLA4, POLD3, POLD4, and RNASEH2. Our results indicate that the core DNA replication machinery from plants is more similar to vertebrates than single-celled yeasts (Saccharomyces cerevisiae), suggesting that animal models may be more relevant to plant systems. However, we also uncovered some important differences between plants and vertebrate machinery. For example, we did not identify geminin or RNASEH1 genes in plants. Our analyses also indicate that plants may be unique among eukaryotes in that they have multiple copies of numerous core DNA replication genes. This finding raises the question of whether specialized functions have evolved in some cases. This analysis establishes that the core DNA replication machinery is highly conserved across plant species and displays many features in common with other eukaryotes and some characteristics that are unique to plants.

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Figures

Figure 1.
Figure 1.

Model depicting the core eukaryotic DNA replication machinery from initiation through Okazaki fragment maturation. A, Components of the preinitiation complex. DNA bound ORC recruits NOC3, CDC6, and CDT1 in early G1. Reiterative loading of 10 to 40 MCM complexes forms a licensed origin. After MCM loading is complete, CDC6 and CDT1 dissociate from the origin. B, At the G1/S transition a subset of licensed origins transition to an initiation complex. The precise order of events is not clear and may vary between systems. CDC45, TOPBP1, and MCM8-10 contribute to GINS complex loading, DNA unwinding, and recruitment of the polymerases. C, Components of the active DNA replication fork. MCM2-7, CDC45, and GINS unwind the duplex DNA. Leading strand synthesis is accomplished primarily by POLE. GINS increases the processivity of POLE. On the lagging strand, RPA stabilizes ssDNA, POLA lays down a short RNA/DNA primer and then is replaced by POLD, which completes the Okazaki fragment. RFC loads PCNA, which increases the processivity of POLD. The precise role of MCM8-10 in this process is not clear. D, The dominant mechanism of Okazaki fragment maturation requires FEN1 to cleave the RNA/DNA flap, resulting in a nick that is sealed by LIG1.

Figure 2.
Figure 2.

Multiple sequence alignments of plant ORC6 and GINS complex proteins. A, ORC6. B, PSF1. C, PSF2. D, PSF3. E, SLD5. For all sections, protein sequences from the indicated plant species were aligned using the Clustal W algorithm. Black shading indicates identical residues in all aligned sequences. Gray shading denotes residues with similar chemical properties that are conserved in >50% of sequences aligned. Similar chemical properties of amino acid residues were defined as follows: DE, Acidic; AGILV, aliphatic; NQ, amide; FWY, aromatic; RHK, basic; ST, hydroxyl; CM, sulphur. Plant sequences were also aligned with proteins from other eukaryotes. Ascomycota includes sequences from yeast and Schizosaccharomyces pombe. Vertebrata includes Homo sapeins, Danio rerio, X. laevis, and Gallus gallus. An x indicates residues that are identical in all sequences from plants and the specified group. An o denotes residues with similar chemical properties that are conserved in >50% of plant sequences and 100% of sequences from the specified group. The plant species are designated as Ac, Ananas comosus; Af, Aquilegia formosa × Aquilegia pubescens; At, Arabidopsis; Bn, Brassica napus; Br, B. rapa; Cs, Citrus sinensis; Ee, Euphorbia esula; Ga, Gossypium arboreum; Gm, G. max; Gr, Gossypium raimondii; Ha, Helianthus annus; Ht, Helianthus petiolaris; Hv, Hordeum vulgare; In, Ipomoea nil; Lc, Lotus corniculatus; Ls, Lactuca serriola; Lv, Lactuca virosa; Mt, Medicago truncatula; Nt, N. tabacum; Os, O. sativa; Pg, Picea glauca; Ps, Picea sitchensis; Pt, Populus trichocarpa; Pta, Pinus taeda; Sa, Senecio aethnensis; Sb, Sorghum bicolor; Sch, Solanum chacoense; So, Saccharum officinarum; St, Solanum tuberosum; Ta, Triticum aestivum; Zm, Z mays.

Figure 2.
Figure 2.

Multiple sequence alignments of plant ORC6 and GINS complex proteins. A, ORC6. B, PSF1. C, PSF2. D, PSF3. E, SLD5. For all sections, protein sequences from the indicated plant species were aligned using the Clustal W algorithm. Black shading indicates identical residues in all aligned sequences. Gray shading denotes residues with similar chemical properties that are conserved in >50% of sequences aligned. Similar chemical properties of amino acid residues were defined as follows: DE, Acidic; AGILV, aliphatic; NQ, amide; FWY, aromatic; RHK, basic; ST, hydroxyl; CM, sulphur. Plant sequences were also aligned with proteins from other eukaryotes. Ascomycota includes sequences from yeast and Schizosaccharomyces pombe. Vertebrata includes Homo sapeins, Danio rerio, X. laevis, and Gallus gallus. An x indicates residues that are identical in all sequences from plants and the specified group. An o denotes residues with similar chemical properties that are conserved in >50% of plant sequences and 100% of sequences from the specified group. The plant species are designated as Ac, Ananas comosus; Af, Aquilegia formosa × Aquilegia pubescens; At, Arabidopsis; Bn, Brassica napus; Br, B. rapa; Cs, Citrus sinensis; Ee, Euphorbia esula; Ga, Gossypium arboreum; Gm, G. max; Gr, Gossypium raimondii; Ha, Helianthus annus; Ht, Helianthus petiolaris; Hv, Hordeum vulgare; In, Ipomoea nil; Lc, Lotus corniculatus; Ls, Lactuca serriola; Lv, Lactuca virosa; Mt, Medicago truncatula; Nt, N. tabacum; Os, O. sativa; Pg, Picea glauca; Ps, Picea sitchensis; Pt, Populus trichocarpa; Pta, Pinus taeda; Sa, Senecio aethnensis; Sb, Sorghum bicolor; Sch, Solanum chacoense; So, Saccharum officinarum; St, Solanum tuberosum; Ta, Triticum aestivum; Zm, Z mays.

Figure 2.
Figure 2.

Multiple sequence alignments of plant ORC6 and GINS complex proteins. A, ORC6. B, PSF1. C, PSF2. D, PSF3. E, SLD5. For all sections, protein sequences from the indicated plant species were aligned using the Clustal W algorithm. Black shading indicates identical residues in all aligned sequences. Gray shading denotes residues with similar chemical properties that are conserved in >50% of sequences aligned. Similar chemical properties of amino acid residues were defined as follows: DE, Acidic; AGILV, aliphatic; NQ, amide; FWY, aromatic; RHK, basic; ST, hydroxyl; CM, sulphur. Plant sequences were also aligned with proteins from other eukaryotes. Ascomycota includes sequences from yeast and Schizosaccharomyces pombe. Vertebrata includes Homo sapeins, Danio rerio, X. laevis, and Gallus gallus. An x indicates residues that are identical in all sequences from plants and the specified group. An o denotes residues with similar chemical properties that are conserved in >50% of plant sequences and 100% of sequences from the specified group. The plant species are designated as Ac, Ananas comosus; Af, Aquilegia formosa × Aquilegia pubescens; At, Arabidopsis; Bn, Brassica napus; Br, B. rapa; Cs, Citrus sinensis; Ee, Euphorbia esula; Ga, Gossypium arboreum; Gm, G. max; Gr, Gossypium raimondii; Ha, Helianthus annus; Ht, Helianthus petiolaris; Hv, Hordeum vulgare; In, Ipomoea nil; Lc, Lotus corniculatus; Ls, Lactuca serriola; Lv, Lactuca virosa; Mt, Medicago truncatula; Nt, N. tabacum; Os, O. sativa; Pg, Picea glauca; Ps, Picea sitchensis; Pt, Populus trichocarpa; Pta, Pinus taeda; Sa, Senecio aethnensis; Sb, Sorghum bicolor; Sch, Solanum chacoense; So, Saccharum officinarum; St, Solanum tuberosum; Ta, Triticum aestivum; Zm, Z mays.

Figure 3.
Figure 3.

Phylogenetic analysis of eukaryotic GINS complex proteins. Protein sequences were aligned with ClustalW using the Gonnet scoring matrix in MEGA. A single tree containing all of the sequences was constructed by the neighbor-joining method, and was split manually into four subtrees (A–D) for visualization. Bootstrap values from 5,000 iterations are shown at each node. Species abbreviations are the same as in Figure 2.

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