Abstract
The chloroplast genomes of many algae and almost all land plants carry two identical copies of a large inverted repeat (IR) sequence that can pair for flip-flop recombination and undergo expansion/contraction. Although the IR has been lost multiple times during the evolution of the green algae, the underlying mechanisms are still largely unknown. A recent comparison of IR-lacking and IR-containing chloroplast genomes of chlorophytes from the Ulvophyceae (Ulotrichales) suggested that differential elimination of genes from the IR copies might lead to IR loss. To gain deeper insights into the evolutionary history of the chloroplast genome in the Ulvophyceae, we analyzed the genomes of Ignatius tetrasporus and Pseudocharacium americanum (Ignatiales, an order not previously sampled), Dangemannia microcystis (Oltmannsiellopsidales), Pseudoneochloris marina (Ulvales) and also Chamaetrichon capsulatum and Trichosarcina mucosa (Ulotrichales). Our comparison of these six chloroplast genomes with those previously reported for nine ulvophyceans revealed unsuspected variability. All newly examined genomes feature an IR, but remarkably, the copies of the IR present in the Ignatiales, Pseudoneochloris, and Chamaetrichon diverge in sequence, with the tRNA genes from the rRNA operon missing in one IR copy. The implications of this unprecedented finding for the mechanism of IR loss and flip-flop recombination are discussed.
Highlights
Descendants from cyanobacteria, the chloroplasts of photosynthetic eukaryotes possess their own genome that encodes components necessary for replication and expression as well as for diverse functions of the chloroplasts[1, 2]
The chloroplast genome sequences of the six newly sampled taxa were assembled as circular-mapping molecules, with sizes ranging from 135 kb to 239 kb (Table 1 and Supplementary Figs S1–S6)
All six genomes contain more than one copy of a sequence that encodes the genes making up the rRNA operon; this sequence is designated hereafter as the inverted repeat (IR) even though the copies differ in both size and sequence in four of the taxa: the two representatives of the Ignatiales (Ignatius and Pseudocharacium), the ulvalean Pseudoneochloris and the ulotrichalean Chamaetrichon (Table 1 and Fig. 1a)
Summary
Descendants from cyanobacteria, the chloroplasts (plastids) of photosynthetic eukaryotes possess their own genome that encodes components necessary for replication and expression as well as for diverse functions of the chloroplasts[1, 2]. Despite frequent variations in IR/SC boundaries, the overall quadripartite structure shows a high degree of conservation in land plants, as shown by the retention of similar gene contents in the large and small SC regions (LSC and SSC regions) of different taxa and the absence of the IR in only a few lineages (e.g. gymnosperms, legumes, Erodium)[3, 14]. A more recent study in which gene orders of the IR-lacking genome of the ulvophycean green alga Gloeotilopsis planctonica (Ulotrichales) and the IR-containing genome of Pseudendoclonium akinetum (Ulotrichales) were compared led to the hypothesis that IR loss might occur through differential elimination of the gene sequences making up the rRNA operon in the two IR copies[31]. Identifying ulvophycean genomes carrying IR copies with differing gene content would provide strong support for this hypothesis
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