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Stable Chloroplast: Myth or Reality?

Chloroplasts principally encode the photosynthetic machinery in Viridiplantae. It has long been accepted that in photosynthetic plants chloroplast genomic structure is uniquely stable. The first chloroplast genomes sequenced supported this view, with the only major structural rearrangements being identified between the Poales and the Poaceae. Recently, additional chloroplast genomes across all plant lineages have been sequenced. Our novel bioinformatics methodology allows whole chloroplast alignments, at the micro, gene and at macro scales. The current study includes 110 chloroplast genomes covering 280MY of plant evolution. Our results at the micro level demonstrate that short nucleotide repeats are uncommon, whereas, large scale repeats (50-300nt) are distributed throughout the genome of all lineages. However, the duplication in each event is lineage specific and is not repeated. These unique insertion and deletion events, point towards a constant chromosomal churn, which contradicts the existing perception of a stable chloroplast. At the gene level there have been specific gene losses that characterise new plant lineages as noted in the five events separating early dicots from the Poaceae. At macro levels, when plants become non-photosynthetic, we observed massive rearrangements in the chloroplast genome (eg. Petrosavia). Even when chloroplast function is essential there is a tendency for large regions to be inverted around tRNA genes (eg. Poaceae, Piper, Dioscorea.). We further noted the complete loss of the IRb region from chloroplasts in the wheat lineage.
This large scale, multigenome, study allows us to demonstrate that the chloroplast is a dynamic genome, rather than being static and stable as perceived in the traditional, erroneous view. The chloroplast is derived from an ancestral cyanobacterial genome and still retains it plasticity. This means that lineages can have profoundly different clock rates of plastid evolution. Here, we demonstrate alterations in every examined chloroplast genome, at all scales, proving that the stable chloroplast is a myth.