Genome defense against integrated organellar DNA fragments from plastids into plant nuclear genomes through DNA methylation

Abstract

Nuclear genomes are always faced with the modification of themselves by insertions and integrations of foreign DNAs and intrinsic parasites such as transposable elements. There is also substantial number of integrations from symbiotic organellar genomes to their host nuclear genomes. Such integration might have acted as a beneficial mutation during the evolution of symbiosis, while most of them have more or less deleterious effects on the stability of current genomes. Here we report the pattern of DNA substitution and methylation on organellar DNA fragments integrated from plastid into plant nuclear genomes. The genome analyses of 17 plants show homology–dependent DNA substitution bias. A certain number of these sequences are DNA methylated in the nuclear genome. The intensity of DNA methylation also decays according to the increase of relative evolutionary times after being integrated into nuclear genomes. The methylome data of epigenetic mutants shows that the DNA methylation of organellar DNA fragments in nuclear genomes are mainly dependent on the methylation maintenance machinery, while other mechanisms may also affect on the DNA methylation level. The DNA methylation on organellar DNA fragments may contribute to maintaining the genome stability and evolutionary dynamics of symbiotic organellar and their host’s genomes.

Nuclear Integrants of Organellar DNA Contribute to Genome Structure and Evolution in Plants

“…In fact, it has been revealed that a considerable number of NUPTs are methylated, and the DNA methylation intensity and level decrease over evolutionary time. The DNA methylation-modified NUPTs may maintain the stability of plant nuclear genomes against the insertion of organellar DNA sequences and play an important role in the symbiosis of nuclear and organelle genomes [51]. Further methylome data analysis of epigenetic mutants in Arabidopsis and rice show that organellar DNA sequences are methylated mainly via the maintenance methylation machinery, involving DDM1, CMT3, CMT2, and SUVH4/KYP.…”

“…The mutation patterns of NUPTs of a number of plant species show biased mutations of cytosine (C) → thymime (T) on one DNA strand, and guanine (G) → adenine (A) substitutions on the opposite strand [4,33,38,51]. These biased substitutions might be due to the hypermethylation of cytosine residues with subsequent deamination [52].…”

“…Such sequences could result in nuclear genome instability, and the nuclear genome can initiate defense mechanisms [49,50]. A recent report showed that DNA methylation might play an important role in this process [51]. Future studies on DNA methylation and heterochromatization of organellar DNA insertions may improve our understanding of the organellar DNA integrants involved in dynamic genome evolution.…”

Genomic Variation between PRSV Resistant Transgenic SunUp and Its Progenitor Cultivar Sunset

“…Non-homologous end joining of double-strand break repair (NHEJ-DSB repair) are suggested to be the integration mechanism as any other foreign sequences [18]. Recent evidence reveals that DNA methylation plays a pivotal role in regulating norgDNA, which may contribute to maintaining the genome stability and evolutionary dynamics of organellar and nuclear genomes [19]. NUPTs were shown to have integration preferences, simultaneous integration [20] and strong bias for nucleotide substitutions from C/G to T/A correlating with the time of integration [19].…”

“…Recent evidence reveals that DNA methylation plays a pivotal role in regulating norgDNA, which may contribute to maintaining the genome stability and evolutionary dynamics of organellar and nuclear genomes [19]. NUPTs were shown to have integration preferences, simultaneous integration [20] and strong bias for nucleotide substitutions from C/G to T/A correlating with the time of integration [19]. It is intriguing that in Suzuki's study [7] all six genomic DNA segments flanking three inserts in 'SunUp' were nuclear organelle sequences.…”