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Proc Natl Acad Sci U S A. 2019 Jan 15;116(3):934-943. doi: 10.1073/pnas.1816822116. Epub 2018 Dec 31.

Novel genetic code and record-setting AT-richness in the highly reduced plastid genome of the holoparasitic plant Balanophora.

Author information

1
Department of Earth and Life Sciences, University of Taipei, 100 Taipei, Taiwan.
2
Department of Biology, Pennsylvania State University, University Park, PA 16802.
3
Institute of Molecular Evolutionary Genetics, Pennsylvania State University, University Park, PA 16802.
4
Department of Biological Sciences, Western Michigan University, Kalamazoo, MI 49008.
5
Department of Biological Sciences, Wayne State University, Detroit, MI 48202.
6
Graduate Program in Plant Biology, Pennsylvania State University, University Park, PA 16802.
7
Department of Biology, Indiana University, Bloomington, IN 47405.
8
Institute of Ecology and Evolutionary Biology, National Taiwan University, 106 Taipei, Taiwan.
9
Department of Biology, Indiana University, Bloomington, IN 47405; jpalmer@indiana.edu cwd3@psu.edu.
10
Department of Biology, Pennsylvania State University, University Park, PA 16802; jpalmer@indiana.edu cwd3@psu.edu.

Abstract

Plastid genomes (plastomes) vary enormously in size and gene content among the many lineages of nonphotosynthetic plants, but key lineages remain unexplored. We therefore investigated plastome sequence and expression in the holoparasitic and morphologically bizarre Balanophoraceae. The two Balanophora plastomes examined are remarkable, exhibiting features rarely if ever seen before in plastomes or in any other genomes. At 15.5 kb in size and with only 19 genes, they are among the most reduced plastomes known. They have no tRNA genes for protein synthesis, a trait found in only three other plastid lineages, and thus Balanophora plastids must import all tRNAs needed for translation. Balanophora plastomes are exceptionally compact, with numerous overlapping genes, highly reduced spacers, loss of all cis-spliced introns, and shrunken protein genes. With A+T contents of 87.8% and 88.4%, the Balanophora genomes are the most AT-rich genomes known save for a single mitochondrial genome that is merely bloated with AT-rich spacer DNA. Most plastid protein genes in Balanophora consist of ≥90% AT, with several between 95% and 98% AT, resulting in the most biased codon usage in any genome described to date. A potential consequence of its radical compositional evolution is the novel genetic code used by Balanophora plastids, in which TAG has been reassigned from stop to tryptophan. Despite its many exceptional properties, the Balanophora plastome must be functional because all examined genes are transcribed, its only intron is correctly trans-spliced, and its protein genes, although highly divergent, are evolving under various degrees of selective constraint.

KEYWORDS:

AT-biased base composition; genetic code change; genome reduction; overlapping genes; parasitic plants

PMID:
30598433
PMCID:
PMC6338844
[Available on 2019-07-15]
DOI:
10.1073/pnas.1816822116

Conflict of interest statement

Conflict of interest statement: E.K.W. and C.W.d. are coauthors on a 2018 paper with reviewer I.D.S. This paper had 42 authors with E.K.W., C.W.d., and I.D.S. all middle authors. E.K.W. and C.W.d. had no significant interaction with I.D.S. on the project or paper.

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