Extreme plastomes in holoparasitic Balanophoraceae are not the norm

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

  • Woorin Kim - , TUD Dresden University of Technology (Author)
  • Thea Lautenschläger - , Chair of Botany, TUD Dresden University of Technology, University of Hamburg (Author)
  • Jay F. Bolin - , Catawba College (Author)
  • Mathew Rees - , University of Edinburgh, Royal Botanic Garden Edinburgh (Author)
  • Albertina Nzuzi - , Instituto Nacional da Biodiversidade e Conservação (Author)
  • Renchao Zhou - , Sun Yat-Sen University (Author)
  • Stefan Wanke - , Chair of Botany, TUD Dresden University of Technology, Universidad Nacional Autónoma de México (Author)
  • Matthias Jost - , Chair of Plant Cell and Molecular Biology, TUD Dresden University of Technology (Author)

Abstract

Background: Balanophoraceae plastomes are known for their highly condensed and re-arranged nature alongside the most extreme nucleotide compositional bias known to date, culminating in two independent reconfigurations of their genetic code. Currently, a large portion of the Balanophoraceae diversity remains unexplored, hindering, among others, evolutionary pattern recognition. Here, we explored newly sequenced plastomes of Sarcophyte sanguinea and Thonningia sanguinea. The reconstructed plastomes were analyzed using various methods of comparative genomics based on a representative taxon sampling. Results: Sarcophyte, recovered sister to the other sampled Balanophoraceae s. str., has plastomes up to 50% larger than those currently published. Its gene set contains five genes lost in any other species, including matK. Five cis-spliced introns are maintained. In contrast, the Thonningia plastome is similarly reduced to published Balanophoraceae and retains only a single cis-spliced intron. Its protein-coding genes show a more biased codon usage compared to Sarcophyte, with an accumulation of in-frame TAG stop codons. Structural plastome comparison revealed multiple, previously unknown, structural rearrangements within Balanophoraceae. Conclusions: For the “minimal plastomes” of Thonningia, we propose a genetic code change identical to sister genus Balanophora. Sarcophyte however differs drastically from our current understanding on Balanophoraceae plastomes. With a less-extreme nucleotide composition, there is no evidence for an altered genetic code. Using comparative genomics, we identified a hotspot for plastome reconfiguration in Balanophoraceae. Based on previously published and newly identified structural reconfigurations, we propose an updated model of evolutionary plastome trajectories for Balanophoraceae, illustrating a much greater plastome diversity than previously known.

Details

Original languageEnglish
Article number330
JournalBMC genomics
Volume24
Issue number1
Publication statusPublished - Dec 2023
Peer-reviewedYes

External IDs

PubMed 37322447

Keywords

ASJC Scopus subject areas

Keywords

  • Genetic code change, Heterotrophic lifestyle, MatK gene, Nucleotide compositional bias, Plastome condensation, Santalales