Detecting and Characterizing the Highly Divergent Plastid Genome of the Nonphotosynthetic Parasitic PlantHydnora visseri(Hydnoraceae)

Abstract

Plastid genomes of photosynthetic flowering plants are usually highly conserved in both structure and gene content. However, the plastomes of parasitic and mycoheterotrophic plants may be released from selective constraint due to the reduction or loss of photosynthetic ability. Here we present the greatly reduced and highly divergent, yet functional, plastome of the nonphotosynthetic holoparasite Hydnora visseri (Hydnoraceae, Piperales). The plastome is 27 kb in length, with 24 genes encoding ribosomal proteins, ribosomal RNAs, tRNAs, and a few nonbioenergetic genes, but no genes related to photosynthesis. The inverted repeat and the small single copy region are only approximately 1.5 kb, and intergenic regions have been drastically reduced. Despite extreme reduction, gene order and orientation are highly similar to the plastome of Piper cenocladum, a related photosynthetic plant in Piperales. Gene sequences in Hydnora are highly divergent and several complementary approaches using the highest possible sensitivity were required for identification and annotation of this plastome. Active transcription is detected for all of the protein-coding genes in the plastid genome, and one of two introns is appropriately spliced out of rps12 transcripts. The whole-genome shotgun read depth is 1,400× coverage for the plastome, whereas the mitochondrial genome is covered at 40× and the nuclear genome at 2×. Despite the extreme reduction of the genome and high sequence divergence, the presence of syntenic, long transcriptionally active open-reading frames with distant similarity to other plastid genomes and a high plastome stoichiometry relative to the mitochondrial and nuclear genomes suggests that the plastome remains functional in H. visseri. A four-stage model of gene reduction, including the potential for complete plastome loss, is proposed to account for the range of plastid genomes in nonphotosynthetic plants.

Limited mitogenomic degradation in response to a parasitic lifestyle in Orobanchaceae

“…Plastomes in the holoparasitic species of Orobanchaceae are also heavily degraded2391011, most extensively in Conopholis americana whose plastome is only 46 kb in size with just 21 intact protein-coding genes. Similar levels of degradation were found in the plastomes of other holoparasites in Cynomoriaceae and Hydnoraceae1213. Even greater genomic reduction was reported in Pilostyles (Apodanthaceae), whose plastomes are reduced to just 11–15 kb and may contain only five or six functional genes14.…”

Dense infraspecific sampling reveals rapid and independent trajectories of plastome degradation in a heterotrophic orchid complex

“…only genes with essential functions remain in the plastome (i.e. ‘stationary phase’ sensu Naumann et al ., ). These two scenarios could happen together: ‘punctuational’ stages of gene loss, with each stage of stasis representing a new, temporary equilibrium with higher mutation rates.…”

“…These include overall decreases in genome size, decreases in GC content, increasing frequency of rearrangements, accumulation of indels, losses of introns, etc. (Wicke et al ., , , ; Barrett & Davis, ; Barrett et al ., ; Naumann et al ., ; reviewed in Graham et al ., ).…”

The Plastid Genome of Polytoma uvella Is the Largest Known among Colorless Algae and Plants and Reflects Contrasting Evolutionary Paths to Nonphotosynthetic Lifestyles

“…To the best of our knowledge, this is the first example of a nonphotosynthetic plant or alga having a bigger plastid genome than its closest known photosynthetic relative(s). If anything, previous work has proven that the forfeiting of photosynthesis almost always results in a reduction of plastid genome size (Yan et al, 2015;Naumann et al, 2016). To put this in perspective, the P. uvella ptDNA is at least 6 times larger than that of Helicosporidium sp.…”