The evolution of the plastid chromosome in land plants: gene content, gene order, gene function

Abstract

This review bridges functional and evolutionary aspects of plastid chromosome architecture in land plants and their putative ancestors. We provide an overview on the structure and composition of the plastid genome of land plants as well as the functions of its genes in an explicit phylogenetic and evolutionary context. We will discuss the architecture of land plant plastid chromosomes, including gene content and synteny across land plants. Moreover, we will explore the functions and roles of plastid encoded genes in metabolism and their evolutionary importance regarding gene retention and conservation. We suggest that the slow mode at which the plastome typically evolves is likely to be influenced by a combination of different molecular mechanisms. These include the organization of plastid genes in operons, the usually uniparental mode of plastid inheritance, the activity of highly effective repair mechanisms as well as the rarity of plastid fusion. Nevertheless, structurally rearranged plastomes can be found in several unrelated lineages (e.g. ferns, Pinaceae, multiple angiosperm families). Rearrangements and gene losses seem to correlate with an unusual mode of plastid transmission, abundance of repeats, or a heterotrophic lifestyle (parasites or myco-heterotrophs). While only a few functional gene gains and more frequent gene losses have been inferred for land plants, the plastid Ndh complex is one example of multiple independent gene losses and will be discussed in detail. Patterns of ndh-gene loss and functional analyses indicate that these losses are usually found in plant groups with a certain degree of heterotrophy, might rendering plastid encoded Ndh1 subunits dispensable.

Fig. 1

Evolution of plastid gene content in land plants. Events of gene losses in Embryophytes, as well as gains and duplication of protein coding genes in green plant lineages are depicted along the branches/nodes of the Plant Tree of Life (Palmer et al. ; Qiu et al. ; Zhong et al. 2010). The putatively ancestral gene content, as reflected in Marchantia and derived from parsimony analysis after Maul et al. (2002), is given at the first land plant node. Gene losses during the evolution of land plants are indicated by red arrows (those occurring before the emergence of Embryophytes are not considered here); a green arrow indicates the evolution of a novel gene prior to the transition to land; blue arrows refer to gene duplications. Changes in the content of transfer RNAs are not considered here (refer to Gao et al. for review). A detailed summary of gene losses during the evolution of angiosperms is provided by Jansen et al. (2007) and Magee et al. (2010). Although chl-subunits are still present in some gymnosperm plastomes, multiple losses and pseudogenizations indicate a functional transfer to the nuclear genome. As chl genes have been lost entirely from angiosperm plastomes, functional chl-gene transfer might have already occurred in a common ancestor

Fig. 2

Synteny of land plant plastid chromosomes. The plastid chromosomes are shown in linearized form illustrating relative gene synteny. Genes are depicted by boxes colored according to their relevant functional class (see legend). Genes encoded by the leading strand (+ strand) or by the lagging strand (- strand) are shown above or below the grey chromosome bar, respectively. Lengths of boxes do not reflect lengths of genes, but are artificially increased to aid legibility (consequently, overlapping genes on ± strand do not indicate overlapping reading frames). Lines from selected genes/gene-regions mentioned above the first chromosome bar roughly indicate genes clusters that have been reorganizated during land plant evolution. Not all regions that underwent genomic relocations prior or during land plant evolution are depicted here. The chromosome bars are colored gray to highlight the positions of the two large Inverted Repeat regions (IR_A/IR_B) and are connected by gray lines between the different lineages. Gray lines are discontinued once to indicate loss of the large inverted repeat in Pinus. Drawn with GenomePixelizer (Kozik et al. 2002) using genome annotations deposited in public sequence databases. Refer to the text for genome references and original publications.]