Can Green Algal Plastid Genome Size Be Explained by DNA Repair Mechanisms?

Abstract

A major finding in organelle biology over the past decade is that land plant mitochondrial genomes, which are the largest among eukaryotes, can have a “Jekyll and Hyde” mutational pattern: low for synonymous sites, high for intergenic ones. This has led to the theory that double-strand breaks (DSBs) in the intergenic DNA of plant mitogenomes are repaired by inaccurate mechanisms, such as break-induced replication, which can result in large insertions and, thus, could explain why these genomes are so prone to expansion. But how universal is this theory? Can it apply to other giant organelle DNAs, such as the massive plastid DNAs (ptDNAs) of chlamydomonadalean green algae? Indeed, it can. Analysis of the expanded plastomes from two distinct isolates of the unicellular chlamydomonadalean Chlorosarcinopsis eremi uncovered exceptionally low rates of synonymous substitution in the coding regions but high substitution rates, including frequent indels, in the noncoding ptDNA, mirroring the trend from land plant mitogenomes. Remarkably, nearly all of the substitutions and indels identified in the noncoding ptDNA of C. eremi occur adjacent to or within short inverted palindromic repeats, suggesting that these elements are mutational hotspots. Building upon earlier studies, I propose that these palindromic repeats are predisposed to DSBs and that error-prone repair of these breaks is contributing to genomic expansion. Short palindromic repeats are a common theme among bloated plastomes, including the largest one on record, meaning that these data could have wide-reaching implications for our understanding of ptDNA expansion.