Unprecedented organelle genomic variations in morning glories reveal independent evolutionary scenarios of parasitic plants and the diversification of plant mitochondrial complexes

Abstract

Background The morning glories (Convolvulaceae) are distributed worldwide and produce economically important crops, medicinal herbs, and ornamentals. Members of this family are diverse in morphological characteristics and trophic modes, including the leafless parasitic Cuscuta (dodders). Organelle genomes were generally used for studying plant phylogeny and genomic variations. Notably, plastomes in parasitic plants always show non-canonical features, such as reduced size and accelerated rates. However, few organelle genomes of this group have been sequenced, hindering our understanding of their evolution, and dodder mitogenome in particular. Results We assembled 22 new mitogenomes and 12 new plastomes in Convolvulaceae. Alongside previously known ones, we totally analyzed organelle genomes of 23 species in the family. Our sampling includes 16 leafy autotrophic species and 7 leafless parasitic dodders, covering 8 of the 12 tribes. Both the plastid and mitochondrial genomes of these plants have encountered variations that were rarely observed in other angiosperms. All of the plastomes possessed atypical IR boundaries. Besides the gene and IR losses in dodders, some leafy species also showed gene and intron losses, duplications, structural variations, and insertions of foreign DNAs. The phylogeny reconstructed by plastid protein coding sequences confirmed the previous relationship of the tribes. However, the monophyly of ‘Merremieae’ and the sister group of Cuscuta remained uncertain. The mitogenome was significantly inflated in Cuscuta japonica, which has exceeded over 800 kb and integrated massive DNAs from other species. In other dodders, mitogenomes were maintained in small size, revealing divergent evolutionary strategies. Mutations unique to plants were detected in the mitochondrial gene ccmFc, which has broken into three fragments through gene fission and splicing shift. The unusual changes likely initially happened to the common ancestor of the family and were caused by a foreign insertion from rosids followed by double-strand breaks and imprecise DNA repairs. The coding regions of ccmFc expanded at both sides after the fission, which may have altered the protein structure. Conclusions Our family-scale analyses uncovered unusual scenarios for both organelle genomes in Convolvulaceae, especially in parasitic plants. The data provided valuable genetic resources for studying the evolution of Convolvulaceae and plant parasitism.

Mitochondrial Phylogenomics of Cuscuta (Convolvulaceae) Reveals a Potentially Functional Horizontal Gene Transfer from the Host

“…S1, Supplementary Material online). We also find that all Cuscuta we sampled possess fragmented ccmFc genes, in which exon 1 splits into two pieces, consistent with the observation in recent studies ( Anderson et al 2021 ; Lin et al 2022 ). Based on the phylogeny, each parasitic lineage is also grouped together with their autotrophic relatives with high support ( fig.…”

“… Anderson et al (2021) concluded that the apparent lack of mitochondrial HGT in Cuscuta may be due to the relatively small size of their mitogenomes, which limits the capacity to integrate foreign DNA. Supporting this notion is a recent finding of “HGT-like” sequences that have been reported within the mitogenome of C. japonica ( Lin et al 2022 ). In this species, belonging to subg.…”

“…In contrast, more recent studies found no evidence of HGT in mitochondrial genes of seven Cuscuta species across subg. Cuscuta , Grammica , and Monogynella ( Anderson et al 2021 ; Lin et al 2022 ). Grammica is the largest subgenus of Cuscuta , comprising about three-fourth of the species diversity of this genus, from which we included 23 samples, representing nearly all of its 15 sections ( supplementary material table S1, Supplementary Material online).…”

“…Cuscuta . However, none of its putatively horizontally transferred sequences were found in coding regions ( Lin et al 2022 ). Our finding indicates that although HGTs overall may be easier to happen in large mitogenomes, the HGTs of coding genes are still likely to be rare events within mitochondrial genomes of Cuscuta .…”

“…For example, two recent studies reported a lack of evidence for HGT in mitochondrial genomes of two closely related Cuscuta species from subg. Grammica ( Anderson et al 2021 ), and of seven species from three subgenera of Cuscuta except Pachystigma ( Lin et al 2022 ).…”