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Novel Genetic Code and Record-Setting AT-Richness in the Highly Reduced Plastid Genome of the Holoparasitic Plant Balanophora

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Novel Genetic Code and Record-Setting AT-Richness in the Highly Reduced Plastid Genome of the Holoparasitic Plant Balanophora Novel genetic code and record-setting AT-richness in the highly reduced plastid genome of the holoparasitic plant Balanophora Huei-Jiun Sua,b,c, Todd J. Barkmand, Weilong Haoe, Samuel S. Jonesf, Julia Naumannb,c,1, Elizabeth Skippingtong,2, Eric K. Wafulab,c, Jer-Ming Huh, Jeffrey D. Palmerg,3, and Claude W. dePamphilisb,c,f,3 aDepartment of Earth and Life Sciences, University of Taipei, 100 Taipei, Taiwan; bDepartment of Biology, Pennsylvania State University, University Park, PA 16802; cInstitute of Molecular Evolutionary Genetics, Pennsylvania State University, University Park, PA 16802; dDepartment of Biological Sciences, Western Michigan University, Kalamazoo, MI 49008; eDepartment of Biological Sciences, Wayne State University, Detroit, MI 48202; fGraduate Program in Plant Biology, Pennsylvania State University, University Park, PA 16802; gDepartment of Biology, Indiana University, Bloomington, IN 47405; and hInstitute of Ecology and Evolutionary Biology, National Taiwan University, 106 Taipei, Taiwan Contributed by Jeffrey D. Palmer, November 27, 2018 (sent for review October 2, 2018; reviewed by Ian D. Small, David Roy Smith, and Kenneth H. Wolfe) Plastid genomes (plastomes) vary enormously in size and gene contain 112 or 113 different genes, and are 35–40% G+C (12). In content among the many lineages of nonphotosynthetic plants, but sharp contrast, the much smaller number (∼60) of sequenced key lineages remain unexplored. We therefore investigated plas- plastomes of nonphotosynthetic angiosperms vary substantially in tome sequence and expression in the holoparasitic and morpholog- size (11–157 kb), gene content (5–101 genes), and GC base ically bizarre Balanophoraceae. The two Balanophora plastomes composition (23–40%) (13, 14). Many, if not all, plastid genes examined are remarkable, exhibiting features rarely if ever seen encoding proteins involved in photosynthesis, ATP synthesis, and before in plastomes or in any other genomes. At 15.5 kb in size transcription have been lost or become pseudogenes in most ex- and with only 19 genes, they are among the most reduced plastomes amined nonphotosynthetic plants (13, 14). The great majority of known. They have no tRNA genes for protein synthesis, a trait found the intact plastid genes retained by these nonphotosynthetic plants in only three other plastid lineages, and thus Balanophora plastids function solely in protein synthesis; these genes include, depend- must import all tRNAs needed for translation. Balanophora plas- ing on the plastome, 2–21 ribosomal protein genes, 2–4rRNA tomes are exceptionally compact, with numerous overlapping genes, genes, and 0–30 tRNA genes (13, 14). As opposed to the sup- highly reduced spacers, loss of all cis-spliced introns, and shrunken porting process of gene expression, plastomes of photosynthetic protein genes. With A+T contents of 87.8% and 88.4%, the Balano- and nonphotosynthetic angiosperms contain only one to four phora genomes are the most AT-rich genomes known save for a single mitochondrial genome that is merely bloated with AT-rich Significance spacer DNA. Most plastid protein genes in Balanophora consist of ≥90% AT, with several between 95% and 98% AT, resulting in Many groups of flowering plants have become parasites and the most biased codon usage in any genome described to date. A have lost the capacity to carry out photosynthesis. The plastid potential consequence of its radical compositional evolution is the genomes of these parasitic plants are often highly reduced in novel genetic code used by Balanophora plastids, in which TAG has size and gene content and are divergent in other ways too. been reassigned from stop to tryptophan. Despite its many excep- Here we report, to our knowledge, unprecedented levels and tional properties, the Balanophora plastome must be functional be- novel types of plastid-genome divergence in the bizarre, cause all examined genes are transcribed, its only intron is correctly mushroom-like parasitic plant Balanophora. The miniaturized trans-spliced, and its protein genes, although highly divergent, are plastid genome in Balanophora is exceptionally streamlined, evolving under various degrees of selective constraint. has evolved a novel genetic code, and possesses the most A+T- rich protein-coding genes known. These findings extend our parasitic plants | AT-biased base composition | genome reduction | understanding of the lower limits of genome complexity and genetic code change | overlapping genes offer exciting opportunities to explore the mutational and se- lective forces that drive radical genome evolution. arasitic plants, which penetrate their host plant tissues to Pform a vascular connection to acquire water, carbohydrates, Author contributions: H.-J.S., J.D.P., and C.W.d. designed research; H.-J.S. and S.S.J. per- and mineral nutrients, have arisen at least 12 times during angio- formed research; T.J.B. and J.-M.H. contributed new reagents/analytic tools; H.-J.S., T.J.B., ∼ W.H., S.S.J., J.N., E.S., E.K.W., J.D.P., and C.W.d. analyzed data; and H.-J.S., T.J.B., J.D.P., sperm evolution (1, 2). Although 90% of parasitic angiosperms and C.W.d. wrote the paper. are hemiparasites, ranging from fully to minimally photosynthetic, Reviewers: I.D.S., University of Western Australia; D.R.S., University of Western Ontario; 10 groups of parasitic angiosperms contain holoparasites, i.e., and K.H.W., University College Dublin. completely nonphotosynthetic plants. Mycoheterotrophs, the term Conflict of interest statement: E.K.W. and C.W.d. are coauthors on a 2018 paper with used for nonphotosynthetic plants that parasitize fungi, have arisen reviewer I.D.S. This paper had 42 authors with E.K.W., C.W.d., and I.D.S. all middle au- in 10 angiosperm families (3). The many independent lineages of thors. E.K.W. and C.W.d. had no significant interaction with I.D.S. on the project or paper. holoparasitic and mycoheterotrophic angiosperms provide numer- Published under the PNAS license. ous test cases to explore the limits and potential outcomes of plastid Data deposition: The sequences reported in this paper have been deposited in the Gen- – genome (plastome) reduction in heterotrophic plants and the ex- Bank database (accession nos. KX784265, KX784266, and MK144465 MK144474). 1Present address: Department of Biology, Institute for Botany, University for Technology tent to which parallel evolution of gene content occurs. Indeed, Dresden, D-01062 Dresden, Germany. these many independent transitions from autotrophy to heterotro- 2Present address: Department of Bioinformatics and Computational Biology, Genentech, phy show sufficiently similar trends in plastid gene evolution that South San Francisco, CA 94080. several similar models have been erected proposing the progressive 3To whom correspondence may be addressed. Email: [email protected] or cwd3@psu. loss and diversification of different classes of plastid genes (4–9). edu. The >2,000 sequenced plastomes of photosynthetic angio- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. sperms (10) are highly conserved in size, gene content, and base 1073/pnas.1816822116/-/DCSupplemental. composition; the great majority are 135–165 kb in size (11), Published online December 31, 2018. 934–943 | PNAS | January 15, 2019 | vol. 116 | no. 3 www.pnas.org/cgi/doi/10.1073/pnas.1816822116 Downloaded by guest on September 25, 2021 protein genes thought to be involved in core plastid processes records for AT-richness and codon-usage bias, and are excep- other than photosynthesis and ATP synthesis. One or more of tionally compact, with many overlapping and/or shrunken genes. these few genes, plus the dual-functional trnEgene(15,16),are presumed to serve as the driving force—the raison d’être (15–17)— Results for retention of the plastome in nonphotosynthetic angiosperms, as Size, Gene Content, and Synteny of Balanophora Plastomes. We well as retention of the hundreds of mostly nuclear genes required obtained circular plastome assemblies of 15,505 bp for Balano- for its replication, repair, recombination, and expression (18). phora laxiflora (Fig. 2) and 15,507 bp for Balanophora reflexa The smallest angiosperm plastome described to date belongs to (GenBank accession nos. KX784265 and KX784266, respectively). the endoparasite Pilostyles aethiopica; this 11-kb genome contains The near identity in size of the two Balanophora plastomes is the only five identified genes, only one of which does not function in fortuitous result of the accumulation of many indels in each ge- protein synthesis (19). In Rafflesia lagascae, another endoparasitic nome that happen to virtually balance out in aggregate length; holoparasite, the plastome is thought to have been lost entirely indeed, all but 2 of their 19 genes differ in length (SI Appendix, (20), although the possibility that an extremely small and di- Table S1). The Balanophora genomes are the smallest known vergent plastome escaped detection cannot be ruled out (9, 19). plastomes except for the 11.3- and 15.2-kb genomes of two hol- Extreme plastome reduction has also occurred in several lineages oparasitic species of Pilostyles (19) and the 12.8-kb genome of the of mycoheterotrophic plants (13), most notably in Sciaphila thai- mycoheterotroph S. thaidanica (21). danica, whose 13-kb genome is stuffed with 20 genes as a result of The two Balanophora plastomes have an identical and highly severe compaction pressure (21), and Thismia tentaculata,whose reduced set of 19 putatively functional genes, consisting of three rRNA genes (rrn16, rrn23, rrn4.5), one tRNA gene (trnE), 11 ribo- 16-kb genome contains only 12 genes (22). somal protein genes (rps2, rps3, rps4, rps7, rps11, rps12, rps14, rps18, Of the various parasitic and mycoheterotrophic lineages of an- rps19, rpl2, rpl14), and four protein genes of varying or unknown giosperms for which no plastome sequences are available, the function (accD, clpP, ycf1, ycf2; Fig. 2 and SI Appendix,Fig.S1A). holoparasitic Balanophoraceae are one of the most biologically No traces of any photosynthetic, ATP synthase, RNA polymerase, interesting.
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