Rickettsial DNA and a trans-splicing rRNA group I intron in the unorthodox mitogenome of the fern Haplopteris ensiformis

Abstract

Plant mitochondrial genomes can be complex owing to highly recombinant structures, lack of gene syntenies, heavy RNA editing and invasion of chloroplast, nuclear or even foreign DNA by horizontal gene transfer (HGT). Leptosporangiate ferns remained the last major plant clade without an assembled mitogenome, likely owing to a demanding combination of the above. We here present both organelle genomes now for Haplopteris ensiformis. More than 1,400 events of C-to-U RNA editing and over 500 events of reverse U-to-C edits affect its organelle transcriptomes. The Haplopteris mtDNA is gene-rich, lacking only the ccm gene suite present in ancestral land plant mitogenomes, but is highly unorthodox, indicating extraordinary recombinogenic activity. Although eleven group II introns known in disrupted trans-splicing states in seed plants exist in conventional cis-arrangements, a particularly complex structure is found for the mitochondrial rrnL gene, which is split into two parts needing reassembly on RNA level by a trans-splicing group I intron. Aside from ca. 80 chloroplast DNA inserts that complicated the mitogenome assembly, the Haplopteris mtDNA features as an idiosyncrasy 30 variably degenerated protein coding regions from Rickettiales bacteria indicative of heavy bacterial HGT on top of tRNA genes of chlamydial origin.

Beyond a PPR-RNA recognition code: Many aspects matter for the multi-targeting properties of RNA editing factor PPR56

“…10B). At present, cox3eU290SF cannot be identified as a candidate editing site in moss mtDNAs but is confirmed as an RNA editing site in the mitochondria of the lycophytes Isoetes engelmannii [39] and Selaginella moellendorffii [40] and in the fern Haplopteris ensiformis [41].…”

PMAT: an efficient plant mitogenome assembly toolkit using low-coverage HiFi sequencing data

“…The L. japonicum mitogenome was annotated to contain 83 genes, including 34 PCGs, 6 rRNAs, and 43 tRNAs ( Supplementary Data Table S2 ). Some plant core mitochondrial PCGs ( atp8 , ccmB , ccmC , ccmFc , ccmFn , matR , and nad7 ) could not be detected in the L. japonicum mitogenome, which is a very common phenomenon [ 47 , 48 ].…”

Beyond a PPR-RNA recognition code: Many aspects matter for the multi-targeting properties of RNA editing factor PPR56

“…coli RNA editing assay setup allows to test such a hypothesis quickly and we accordingly exchanged the T at the potential editing position of the Physcomitrium mtDNA sequence into a C. Whereas we could not detect editing of cox3eU290SF when routinely cloned as a single target inserted downstream of the PPR protein coding region, we observed an editing efficiency of 93% when cloned in tandem downstream of nad4eU272SL ( Fig 10B ). At present, cox3eU290SF cannot be identified as a candidate editing site in moss mtDNAs but is confirmed as an RNA editing site in the mitochondria of the lycophytes Isoetes engelmannii [ 52 ] and Selaginella moellendorffii [ 53 ] and in the fern Haplopteris ensiformis [ 54 ].…”