Detecting and characterizing the highly divergent plastid genome of the nonphotosynthetic parasitic plant Hydnora visseri (Hydnoraceae)

Julia Naumann, Joshua P. Der, Eric K. Wafula, Samuel S. Jones, Sarah T. Wagner, Loren A. Honaas, Paula E. Ralph, Jay F. Bolin, Erika Maass, Christoph Neinhuis, Stefan Wanke, Claude W. De Pamphilis

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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 1,400x coverage for the plastome, whereas the mitochondrial genome is covered at 40x and the nuclear genome at 2 x. 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. Afour-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.

Original languageEnglish (US)
Pages (from-to)345-363
Number of pages19
JournalGenome biology and evolution
Volume8
Issue number2
DOIs
StatePublished - Jan 1 2016

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All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

Cite this

Naumann, J., Der, J. P., Wafula, E. K., Jones, S. S., Wagner, S. T., Honaas, L. A., Ralph, P. E., Bolin, J. F., Maass, E., Neinhuis, C., Wanke, S., & De Pamphilis, C. W. (2016). Detecting and characterizing the highly divergent plastid genome of the nonphotosynthetic parasitic plant Hydnora visseri (Hydnoraceae). Genome biology and evolution, 8(2), 345-363. https://doi.org/10.1093/gbe/evv256