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Review
, 20 (19)

Plant DNA Polymerases

Affiliations
Review

Plant DNA Polymerases

Jose-Antonio Pedroza-Garcia et al. Int J Mol Sci.

Abstract

Maintenance of genome integrity is a key process in all organisms. DNA polymerases (Pols) are central players in this process as they are in charge of the faithful reproduction of the genetic information, as well as of DNA repair. Interestingly, all eukaryotes possess a large repertoire of polymerases. Three protein complexes, DNA Pol α, δ, and ε, are in charge of nuclear DNA replication. These enzymes have the fidelity and processivity required to replicate long DNA sequences, but DNA lesions can block their progression. Consequently, eukaryotic genomes also encode a variable number of specialized polymerases (between five and 16 depending on the organism) that are involved in the replication of damaged DNA, DNA repair, and organellar DNA replication. This diversity of enzymes likely stems from their ability to bypass specific types of lesions. In the past 10-15 years, our knowledge regarding plant DNA polymerases dramatically increased. In this review, we discuss these recent findings and compare acquired knowledge in plants to data obtained in other eukaryotes. We also discuss the emerging links between genome and epigenome replication.

Keywords: DNA repair; DNA replication.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Hyphomorphic alleles of replicative DNA polymerases (Pols) in Arabidopsis thaliana. On all panels, orange boxes represent exons, and the black line represents introns and regulatory sequences. Below the gene structure, the schematic organization of the corresponding protein is shown. (A) The AtPOL2A gene also known as TIL1/ABO4/ESD7 is annotated to be 18,039 bp, with 48 exons, accounting for an open reading frame of 6818 bp. The til1-4 plants contain two G-to-A mutations: one at position 3927 (counting from the first ATG) in exon 12 and one at position 5005 in intron 14. The former mutation changes a conserved Gly (position 472) into Arg [37]. The abo4-1 mutation changes Gly (position 534) to Arg (G to A in position 4171 counting from the first putative ATG, in the 13th exon). The abo4-2 Salk transfer DNA (T-DNA) insertion line (SALK 0963441) was also found to be viable: in the abo4-2 mutant, the T-DNA is inserted at position 3972 (in the 12th intron), counting from the first putative ATG of the genomic coding sequence [39]. In the mutant, messenger RNAs (mRNAs) lacking exons 12 and 13 (represented in yellow) are produced [50]. The esd7-1 mutation consists of a guanine-to-adenine transition in the 26th exon, which substitutes Gly (G) with Arg (R) at amino-acid position 992, a residue located in the catalytic domain [52]. (B) Structure of the POLA1/ICU2 gene and corresponding protein. The POLA1 gene is 2806 bp long and encodes a 1499-amino-acid (a.a.) protein. The icu2-1 mutant harbors a point mutation in a C/T transition in the 24th exon, at nucleotide position 6762 from the initiation codon, which substitutes Arg (R) with Cys (C) at amino-acid position 1273 [38]. The polα mutation consists of a guanine-to-adenine transition in position 5996 counting from the first putative ATG within the 20th exon, which substitutes Gly (G) with Arg (R) at amino-acid position 1135, a residue in the catalytic domain [41]. (C) Structure of the POLD1 gene and corresponding protein. The POLD1 gene is 7255 bp long and encodes a protein of 1112 amino acids. The gis5 mutation is located within the polymerase domain in the 18th exon causing a C-to-T transition which leads to an Ala 707 Val substitution [40]. (D) Structure of the POLD2 gene and corresponding protein. The gene is 2876 bp long and encodes a 441 amino-acid protein. The pold2-1 mutation changes G to A at position 1170 counting from the first putative ATG, and the mutated nucleotide is located at a splicing site between the fifth intron and the sixth exon [48].
Figure 1
Figure 1
Hyphomorphic alleles of replicative DNA polymerases (Pols) in Arabidopsis thaliana. On all panels, orange boxes represent exons, and the black line represents introns and regulatory sequences. Below the gene structure, the schematic organization of the corresponding protein is shown. (A) The AtPOL2A gene also known as TIL1/ABO4/ESD7 is annotated to be 18,039 bp, with 48 exons, accounting for an open reading frame of 6818 bp. The til1-4 plants contain two G-to-A mutations: one at position 3927 (counting from the first ATG) in exon 12 and one at position 5005 in intron 14. The former mutation changes a conserved Gly (position 472) into Arg [37]. The abo4-1 mutation changes Gly (position 534) to Arg (G to A in position 4171 counting from the first putative ATG, in the 13th exon). The abo4-2 Salk transfer DNA (T-DNA) insertion line (SALK 0963441) was also found to be viable: in the abo4-2 mutant, the T-DNA is inserted at position 3972 (in the 12th intron), counting from the first putative ATG of the genomic coding sequence [39]. In the mutant, messenger RNAs (mRNAs) lacking exons 12 and 13 (represented in yellow) are produced [50]. The esd7-1 mutation consists of a guanine-to-adenine transition in the 26th exon, which substitutes Gly (G) with Arg (R) at amino-acid position 992, a residue located in the catalytic domain [52]. (B) Structure of the POLA1/ICU2 gene and corresponding protein. The POLA1 gene is 2806 bp long and encodes a 1499-amino-acid (a.a.) protein. The icu2-1 mutant harbors a point mutation in a C/T transition in the 24th exon, at nucleotide position 6762 from the initiation codon, which substitutes Arg (R) with Cys (C) at amino-acid position 1273 [38]. The polα mutation consists of a guanine-to-adenine transition in position 5996 counting from the first putative ATG within the 20th exon, which substitutes Gly (G) with Arg (R) at amino-acid position 1135, a residue in the catalytic domain [41]. (C) Structure of the POLD1 gene and corresponding protein. The POLD1 gene is 7255 bp long and encodes a protein of 1112 amino acids. The gis5 mutation is located within the polymerase domain in the 18th exon causing a C-to-T transition which leads to an Ala 707 Val substitution [40]. (D) Structure of the POLD2 gene and corresponding protein. The gene is 2876 bp long and encodes a 441 amino-acid protein. The pold2-1 mutation changes G to A at position 1170 counting from the first putative ATG, and the mutated nucleotide is located at a splicing site between the fifth intron and the sixth exon [48].
Figure 2
Figure 2
Model for Pol ε function in plant DNA damage repair (DDR). Pol ε may be directly involved in replicative stress sensing upstream of ATR to trigger checkpoint activation via the two SOG1-dependent and independent pathways, allowing the expression of genes involved in cell-cycle arrest, DNA repair, and nucleotide biosynthesis. In parallel, WEE1 contributes to arrest the cell cycle. The activation of all these mechanisms ultimately leads to fork stabilization and completion of DNA replication and cell survival [49,50].
Figure 3
Figure 3
Roles of replicative DNA polymerases in the maintenance of epigenetic information. In addition to replicating DNA, the three plant replicative DNA Pols are involved in the replication of chromatin marks. (A) During DNA replication, chromatin is disrupted ahead of the replication fork, and the epigenetic information must be restored behind the fork, in order for chromatin marks to be inherited through DNA replication. (B) Hypomorphic mutants for replicative DNA polymerases showing early flowering caused by de-repression of flowering genes, due to defects in the maintenance of the inhibitory histone marks H3K27me for mutants of three polymerases [38,39,40,41,43,48,52,53]. In addition, loss of Pol δ mutants also affects the active H3K4me mark [40].

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