The Mitochondrial Genome of the Holoparasitic Plant Thonningia sanguinea Provides Insights into the Evolution of the Multichromosomal Structure

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

  • Shuaixi Zhou - , Sun Yat-Sen University (Author)
  • Neng Wei - , CAS - Wuhan Institute of Botany (Author)
  • Matthias Jost - , Chair of Botany (Author)
  • Stefan Wanke - , Chair of Botany (Author)
  • Mathew Rees - , University of Edinburgh, Royal Botanic Garden Edinburgh (Author)
  • Ying Liu - , Sun Yat-Sen University (Author)
  • Renchao Zhou - , Sun Yat-Sen University (Author)

Abstract

Multichromosomal mitochondrial genome (mitogenome) structures have repeatedly evolved in many lineages of angiosperms. However, the underlying mechanism remains unclear. The mitogenomes of three genera of Balanophoraceae, namely Lophophytum, Ombrophytum, and Rhopalocnemis, have already been sequenced and assembled, all showing a highly multichromosomal structure, albeit with different genome and chromosome sizes. It is expected that characterization of additional lineages of this family may expand the knowledge of mitogenome diversity and provide insights into the evolution of the plant mitogenome structure and size. Here, we assembled and characterized the mitogenome of Thonningia sanguinea, which, together with Balanophora, forms a clade sister to the clade comprising Lophophytum, Ombrophytum, and Rhopalocnemis. The mitogenome of T. sanguinea possesses a multichromosomal structure of 18 circular chromosomes of 8.7-19.2 kb, with a total size of 246,247†bp. There are very limited shared regions and poor chromosomal correspondence between T. sanguinea and other Balanophoraceae species, suggesting frequent rearrangements and rapid sequence turnover. Numerous medium- and small-sized repeats were identified in the T. sanguinea mitogenome; however, no repeat-mediated recombination was detected, which was verified by Illumina reads mapping and PCR experiments. Intraspecific mitogenome variations in T. sanguinea are mostly insertions and deletions, some of which can lead to degradation of perfect repeats in one or two accessions. Based on the mitogenome features of T. sanguinea, we propose a mechanism to explain the evolution of a multichromosomal mitogenome from a master circle, which involves mutation in organellar DNA replication, recombination and repair genes, decrease of recombination, and repeat degradation.

Details

Original languageEnglish
Article numberevad155
Number of pages13
JournalGenome biology and evolution
Volume15
Issue number9
Early online date21 Aug 2023
Publication statusPublished - Sept 2023
Peer-reviewedYes

External IDs

PubMed 37603455

Keywords

ASJC Scopus subject areas

Keywords

  • DNA-RRR genes, holoparasites, master circle, mitogenome, parasitic plants, recombination