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.

Conservation of Plastid Sequences in the Plant Nuclear Genome for Millions of Years Facilitates Endosymbiotic Evolution

“…After activation in the nucleus, two functional copies will exist in different cellular compartments, and if they are functionally equivalent, then the silencing of one or the other will depend upon chance mutations (Martin and Herrmann, 1998;Adams et al, 1999) and thus will favor the retention of the chloroplastic copy. This is due to the presence of a higher substitution rate in the nucleus compared to the chloroplast genome (Wolfe et al, 1987), the organization of chloroplast genes in operons, the mainly uniparental inheritance of plastids, and the rarity of fusion of plastids (Wicke et al, 2011). However, if a successfully activated chloroplast gene loses its function in the nucleus, many subsequent nupt integrations and activations remain possible.…”

The dynamic history of plastid genomes in the Campanulaceae sensu lato is unique among angiosperms

“…2) and ycf2 (still of unknown function)] were incorporated before the origin of land plants (3). The characteristic plastome architecture of land plants ( Fig.…”

YCF1: A Green TIC: Response to the de Vries et al. Commentary

“…Decades of chloroplast genome research have revealed that chloroplast-encoded genes are frequently divided into exons and introns and, in some cases, may contain a RNA (transcript) editing site or a transsplicing site where two different transcripts derived from two distinct regions of a chloroplast genome are spliced and fused to form a full-length mRNA (Glanz and Kü ck, 2009;Stern et al, 2010;Wicke et al, 2011;Takenaka et al, 2013 ). Ribosomal frameshifting also occurs in chloroplasts (Kohl and Bock, 2009).…”

“…The elucidation of an alternative TIC system may offer insight into the origin of the ycf1 gene, which has long been believed to have appeared suddenly in the chloroplast genomes of Chlorophyta (Wicke et al, 2011). It can be reasonably hypothesized that a simpler ancestral-type TIC system, retained in Glaucophyta as well as Rhodophyta, also served as a prototype of the major photosynthetic-type green TIC complex containing Ycf1.…”