Mitochondrial genomes of two parasitic Cuscuta species lack clear evidence of horizontal gene transfer and retain unusually fragmented ccmFC genes

Abstract

Background: The intimate association between parasitic plants and their hosts favours the exchange of genetic material, potentially leading to horizontal gene transfer (HGT) between plants. With the recent publication of several parasitic plant nuclear genomes, there has been considerable focus on such non-sexual exchange of genes. To enhance the picture on HGT events in a widely distributed parasitic genus, Cuscuta (dodders), we assembled and analyzed the organellar genomes of two recently sequenced species, C. australis and C. campestris, making this the first account of complete mitochondrial genomes (mitogenomes) for this genus.

Results: The mitogenomes are 265,696 and 275,898 bp in length and contain a typical set of mitochondrial genes, with 10 missing or pseudogenized genes often lost from angiosperm mitogenomes. Each mitogenome also possesses a structurally unusual ccmF_C gene, which exhibits splitting of one exon and a shift to trans-splicing of its intron. Based on phylogenetic analysis of mitochondrial genes from across angiosperms and similarity-based searches, there is little to no indication of HGT into the Cuscuta mitogenomes. A few candidate regions for plastome-to-mitogenome transfer were identified, with one suggestive of possible HGT.

Conclusions: The lack of HGT is surprising given examples from the nuclear genomes, and may be due in part to the relatively small size of the Cuscuta mitogenomes, limiting the capacity to integrate foreign sequences.

Keywords: Chloroplast; Dodder; Intracellular transfer; Mitogenome.

Fig. 1

Linear representations of mitogenomes of Cuscuta australis and C. campestris. The assembly of C. australis consists of eight contigs (divided by gaps), while that of C. campestris is represented as a single circle. Pseudogenes are indicated with a capital psi (Ψ). Fragmented genes have “_frag” at the end of their labels. Transcription is to the right above the lines, and to the left below the lines

Fig. 2

Schematic of ccmF_C gene structure in Cuscuta australis and its close relative Ipomoea nil compared to typical structure in angiosperms. Transcriptomic reads from both species are mapped to three DNA sequences with high similarity to ccmF_C from Cuscuta australis and three from Ipomoea nil. Red lines indicate mismatches in the mapped RNA reads and correspond to putative RNA editing sites. Light grey lines connect read pairs, while solid black lines indicate a break in a single read. Group II intron domains are denoted with Roman numerals. *The third domain in Cuscuta may not fold properly given its sequence divergence

Fig. 3

Maximum likelihood cladogram based on concatenation of all known mitochondrial genes present in Cuscuta together with representatives from angiosperm orders with fully assembled mitogenomes. Orders are indicated at the right along with the outgroup gymnosperms, and the location of Cuscuta is highlighted in yellow. Bootstrap support of 60% or greater is shown above branches. The sequence for Bupleurum falcatum (NC_035962.1) is likely misidentified