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DNA maintenance in plastids and mitochondria of plants

View Article: PubMed Central

ABSTRACT

The DNA molecules in plastids and mitochondria of plants have been studied for over 40 years. Here, we review the data on the circular or linear form, replication, repair, and persistence of the organellar DNA (orgDNA) in plants. The bacterial origin of orgDNA appears to have profoundly influenced ideas about the properties of chromosomal DNA molecules in these organelles to the point of dismissing data inconsistent with ideas from the 1970s. When found at all, circular genome-sized molecules comprise a few percent of orgDNA. In cells active in orgDNA replication, most orgDNA is found as linear and branched-linear forms larger than the size of the genome, likely a consequence of a virus-like DNA replication mechanism. In contrast to the stable chromosomal DNA molecules in bacteria and the plant nucleus, the molecular integrity of orgDNA declines during leaf development at a rate that varies among plant species. This decline is attributed to degradation of damaged-but-not-repaired molecules, with a proposed repair cost-saving benefit most evident in grasses. All orgDNA maintenance activities are proposed to occur on the nucleoid tethered to organellar membranes by developmentally-regulated proteins.

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Single-strand annealing mechanism for plastid DNA replication. This single-strand annealing (SSA), recombination-dependent replication model for ptDNA is based on a replication mechanism for herpes virus DNA (Weller and Sawitzke, 2014). (1) A 3′-overhang is generated by 5′-to-3′ exonuclease digestion at the end of a unit-genome-sized monomer. A single-strand annealing protein (SSAP) binds to a 3′-overhang. (2) Annealing of the 3′-overhang of Molecule 1 to a homologous single-strand gap in another ptDNA molecule (Molecule 2). (3) Replication is initiated by priming at the 3′-end, assembly of the replisome, and formation of a replication fork, leading to a branched-linear structure. A similar model with the same or analogous proteins applies to the replication of mtDNA in plants. We propose that replication occurs only with ptDNA attached to the nucleoid-on-membrane using single-strand end-binding proteins. Although we propose that Whirly proteins serve attachment and SSAP functions, other single-strand-binding proteins, such as the OSB and RecA families, may also participate in ptDNA replication. Other replication and recombination mechanisms have been described (Cox, 2007; Marechal and Brisson, 2010; Weller and Sawitzke, 2014; Morrical, 2015).
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Figure 3: Single-strand annealing mechanism for plastid DNA replication. This single-strand annealing (SSA), recombination-dependent replication model for ptDNA is based on a replication mechanism for herpes virus DNA (Weller and Sawitzke, 2014). (1) A 3′-overhang is generated by 5′-to-3′ exonuclease digestion at the end of a unit-genome-sized monomer. A single-strand annealing protein (SSAP) binds to a 3′-overhang. (2) Annealing of the 3′-overhang of Molecule 1 to a homologous single-strand gap in another ptDNA molecule (Molecule 2). (3) Replication is initiated by priming at the 3′-end, assembly of the replisome, and formation of a replication fork, leading to a branched-linear structure. A similar model with the same or analogous proteins applies to the replication of mtDNA in plants. We propose that replication occurs only with ptDNA attached to the nucleoid-on-membrane using single-strand end-binding proteins. Although we propose that Whirly proteins serve attachment and SSAP functions, other single-strand-binding proteins, such as the OSB and RecA families, may also participate in ptDNA replication. Other replication and recombination mechanisms have been described (Cox, 2007; Marechal and Brisson, 2010; Weller and Sawitzke, 2014; Morrical, 2015).

Mentions: A SSA mechanism has been described for HSV DNA that can generate concatemers, initiate DNA synthesis, and produce branched replicative forms (Weller and Sawitzke, 2014). We propose an analogous SSA mechanism for plant orgDNA (Figure 3): (1) 5′-to-3′ exonuclease digestion of a double-stranded DNA (dsDNA) end to create a 3′ single-strand overhang; (2) binding of a single-strand annealing protein (SSAP) to this single-stranded DNA (ssDNA) region; and (3) either annealing to a homologous DNA region of another 3′-overhang end to form a concatemer or annealing of the 3′-overhang to a ssDNA gap to form a branched structure that can prime DNA synthesis and create a replication fork. ICP8 has been identified as the SSAP in HSV and possesses helix-destabilizing activity (to unwind duplex DNA), binds non-specifically to ssDNA, promotes annealing of homologous ssDNA sequences, and forms thin helical filaments and oligomeric rings in the presence of ssDNA. Is there a plastid (and mitochondrial) protein with similar characteristics to function as a SSAP? Among the organellar DNA-binding proteins that have been identified thus far (Dickey et al., 2013; Moriyama and Sato, 2014), we suggest that the Whirly family of single-strand binding proteins are good candidates to fulfill this role. Although initially implicated in the regulation of nuclear transcription and maintenance of nuclear telomeres, localization to plastids has been demonstrated for Why1 and Why3 and to mitochondria for Why2 (Marechal and Brisson, 2010). The Whirlies are DNA-binding proteins that have a higher binding affinity for ssDNA (with no sequence specificity) than dsDNA, but do promote unwinding of the ends of dsDNA (Cappadocia et al., 2010). The Whirlies form tetramers on short stretches of ssDNA and filaments on long stretches of ssDNA by cooperative binding of hexamers-of-tetramers (24-mers; Cappadocia et al., 2012). Thus Whirlies share many characteristics with ICP8 of HSV. Studies of whirly mutants have shown rearrangements of orgDNA likely facilitated by microhomology-mediated recombination (MHMR; Cappadocia et al., 2010; Zampini et al., 2015) and indicated that these proteins are important for maintaining organellar genome stability (Marechal and Brisson, 2010). We suggest that the filamentous Whirly-ssDNA structure ensures proper alignment of a strand-annealing end with its homologous target region and prevents MHMR as proposed for non-homologous end-joining whereby filament-forming proteins help align ends during double-strand break repair (Reid et al., 2015).


DNA maintenance in plastids and mitochondria of plants
Single-strand annealing mechanism for plastid DNA replication. This single-strand annealing (SSA), recombination-dependent replication model for ptDNA is based on a replication mechanism for herpes virus DNA (Weller and Sawitzke, 2014). (1) A 3′-overhang is generated by 5′-to-3′ exonuclease digestion at the end of a unit-genome-sized monomer. A single-strand annealing protein (SSAP) binds to a 3′-overhang. (2) Annealing of the 3′-overhang of Molecule 1 to a homologous single-strand gap in another ptDNA molecule (Molecule 2). (3) Replication is initiated by priming at the 3′-end, assembly of the replisome, and formation of a replication fork, leading to a branched-linear structure. A similar model with the same or analogous proteins applies to the replication of mtDNA in plants. We propose that replication occurs only with ptDNA attached to the nucleoid-on-membrane using single-strand end-binding proteins. Although we propose that Whirly proteins serve attachment and SSAP functions, other single-strand-binding proteins, such as the OSB and RecA families, may also participate in ptDNA replication. Other replication and recombination mechanisms have been described (Cox, 2007; Marechal and Brisson, 2010; Weller and Sawitzke, 2014; Morrical, 2015).
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Figure 3: Single-strand annealing mechanism for plastid DNA replication. This single-strand annealing (SSA), recombination-dependent replication model for ptDNA is based on a replication mechanism for herpes virus DNA (Weller and Sawitzke, 2014). (1) A 3′-overhang is generated by 5′-to-3′ exonuclease digestion at the end of a unit-genome-sized monomer. A single-strand annealing protein (SSAP) binds to a 3′-overhang. (2) Annealing of the 3′-overhang of Molecule 1 to a homologous single-strand gap in another ptDNA molecule (Molecule 2). (3) Replication is initiated by priming at the 3′-end, assembly of the replisome, and formation of a replication fork, leading to a branched-linear structure. A similar model with the same or analogous proteins applies to the replication of mtDNA in plants. We propose that replication occurs only with ptDNA attached to the nucleoid-on-membrane using single-strand end-binding proteins. Although we propose that Whirly proteins serve attachment and SSAP functions, other single-strand-binding proteins, such as the OSB and RecA families, may also participate in ptDNA replication. Other replication and recombination mechanisms have been described (Cox, 2007; Marechal and Brisson, 2010; Weller and Sawitzke, 2014; Morrical, 2015).
Mentions: A SSA mechanism has been described for HSV DNA that can generate concatemers, initiate DNA synthesis, and produce branched replicative forms (Weller and Sawitzke, 2014). We propose an analogous SSA mechanism for plant orgDNA (Figure 3): (1) 5′-to-3′ exonuclease digestion of a double-stranded DNA (dsDNA) end to create a 3′ single-strand overhang; (2) binding of a single-strand annealing protein (SSAP) to this single-stranded DNA (ssDNA) region; and (3) either annealing to a homologous DNA region of another 3′-overhang end to form a concatemer or annealing of the 3′-overhang to a ssDNA gap to form a branched structure that can prime DNA synthesis and create a replication fork. ICP8 has been identified as the SSAP in HSV and possesses helix-destabilizing activity (to unwind duplex DNA), binds non-specifically to ssDNA, promotes annealing of homologous ssDNA sequences, and forms thin helical filaments and oligomeric rings in the presence of ssDNA. Is there a plastid (and mitochondrial) protein with similar characteristics to function as a SSAP? Among the organellar DNA-binding proteins that have been identified thus far (Dickey et al., 2013; Moriyama and Sato, 2014), we suggest that the Whirly family of single-strand binding proteins are good candidates to fulfill this role. Although initially implicated in the regulation of nuclear transcription and maintenance of nuclear telomeres, localization to plastids has been demonstrated for Why1 and Why3 and to mitochondria for Why2 (Marechal and Brisson, 2010). The Whirlies are DNA-binding proteins that have a higher binding affinity for ssDNA (with no sequence specificity) than dsDNA, but do promote unwinding of the ends of dsDNA (Cappadocia et al., 2010). The Whirlies form tetramers on short stretches of ssDNA and filaments on long stretches of ssDNA by cooperative binding of hexamers-of-tetramers (24-mers; Cappadocia et al., 2012). Thus Whirlies share many characteristics with ICP8 of HSV. Studies of whirly mutants have shown rearrangements of orgDNA likely facilitated by microhomology-mediated recombination (MHMR; Cappadocia et al., 2010; Zampini et al., 2015) and indicated that these proteins are important for maintaining organellar genome stability (Marechal and Brisson, 2010). We suggest that the filamentous Whirly-ssDNA structure ensures proper alignment of a strand-annealing end with its homologous target region and prevents MHMR as proposed for non-homologous end-joining whereby filament-forming proteins help align ends during double-strand break repair (Reid et al., 2015).

View Article: PubMed Central

ABSTRACT

The DNA molecules in plastids and mitochondria of plants have been studied for over 40 years. Here, we review the data on the circular or linear form, replication, repair, and persistence of the organellar DNA (orgDNA) in plants. The bacterial origin of orgDNA appears to have profoundly influenced ideas about the properties of chromosomal DNA molecules in these organelles to the point of dismissing data inconsistent with ideas from the 1970s. When found at all, circular genome-sized molecules comprise a few percent of orgDNA. In cells active in orgDNA replication, most orgDNA is found as linear and branched-linear forms larger than the size of the genome, likely a consequence of a virus-like DNA replication mechanism. In contrast to the stable chromosomal DNA molecules in bacteria and the plant nucleus, the molecular integrity of orgDNA declines during leaf development at a rate that varies among plant species. This decline is attributed to degradation of damaged-but-not-repaired molecules, with a proposed repair cost-saving benefit most evident in grasses. All orgDNA maintenance activities are proposed to occur on the nucleoid tethered to organellar membranes by developmentally-regulated proteins.

No MeSH data available.


Related in: MedlinePlus