Chromophyte algae differ fundamentally from plants in possessing chloroplasts that contain chlorophyll c and that have a more complex bounding-membrane topology. Although chromophytes are known to be evolutionary chimaeras of a red alga and a non-photosynthetic host, which gave rise to their exceptional membrane complexity, their cell biology is poorly understood. Cryptomonads are the only chromophytes that still retain the enslaved red algal nucleus as a minute nucleomorph. Here we report complete sequences for all three nucleomorph chromosomes from the cryptomonad Guillardia theta. This tiny 551-kilobase eukaryotic genome is the most gene-dense known, with only 17 diminutive spliceosomal introns and 44 overlapping genes. Marked evolutionary compaction hundreds of millions of years ago eliminated nearly all the nucleomorph genes for metabolic functions, but left 30 for chloroplast-located proteins. To allow expression of these proteins, nucleomorphs retain hundreds of genetic-housekeeping genes. Nucleomorph DNA replication and periplastid protein synthesis require the import of many nuclear gene products across endoplasmic reticulum and periplastid membranes. The chromosomes have centromeres, but possibly only one loop domain, offering a means for studying eukaryotic chromosome replication, segregation and evolution.

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In eukaryotes, DNA is exchanged between endosymbiosis-derived compartments (mitochondria and chloroplasts) and the nucleus. Organelle-to-nucleus DNA transfer involves repair of double-stranded breaks by nonhomologous end-joining, and resulted during early organelle evolution in massive relocation of organelle genes to the nucleus. A large fraction of the products of the nuclear genes so acquired are retargeted to their ancestral compartment; many others now function in new subcellular locations. Almost all present-day nuclear transfers of mitochondrial or plastid DNA give rise to noncoding sequences, dubbed nuclear mitochondrial DNAs (NUMTs) and nuclear plastid DNAs (NUPTs). Some of these sequences were recruited as exons, thus introducing new coding sequences into preexisting nuclear genes by a novel mechanism. In organisms derived from secondary or tertiary endosymbiosis, serial gene transfers involving nucleus-to-nucleus migration of DNA have also occurred. Intercompartmental DNA transfer therefore represents a significant driving force for gene and genome evolution, relocating and refashioning genes and contributing to genetic diversity.

Background: The holoparasitic plant genus Cuscuta comprises species with photosynthetic capacity and functional chloroplasts as well as achlorophyllous and intermediate forms with restricted photosynthetic activity and degenerated chloroplasts. Previous data indicated significant differences with respect to the plastid genome coding capacity in different Cuscuta species that could correlate with their photosynthetic activity. In order to shed light on the molecular changes accompanying the parasitic lifestyle, we sequenced the plastid chromosomes of the two species Cuscuta reflexa and Cuscuta gronovii. Both species are capable of performing photosynthesis, albeit with varying efficiencies. Together with the plastid genome of Epifagus virginiana, an achlorophyllous parasitic plant whose plastid genome has been sequenced, these species represent a series of progression towards total dependency on the host plant, ranging from reduced levels of photosynthesis in C. reflexa to a restricted photosynthetic activity and degenerated chloroplasts in C. gronovii to an achlorophyllous state in E. virginiana.