Comparisons of complete mitochondrial genomes of the parasites and their hosts found that closely related species evolved dramatically different genome architectures through distinct mechanisms: one lineage accumulated large amounts of host-derived DNA, whereas another expanded through the proliferation of repetitive sequences with limited contribution from foreign DNA.
Abstract
Horizontal gene transfer (HGT) drives organellar evolution, particularly in parasitic plants where host connections facilitate extensive DNA exchange. However, how these processes intersect with cellular machinery to reshape mitogenomic architecture remains poorly understood. Here, we investigate the mechanisms governing structural plasticity and asymmetric host-DNA integration in the extreme holoparasitic family Rafflesiaceae. By performing a comprehensive comparative analysis across all three extant genera (Sapria, Rhizanthes, and Rafflesia) and their Tetrastigma host lineage, we discovered extraordinary mitogenome size divergence, ranging from the expanded 824-kb genome of Sapria (40 circular chromosomes) to the streamlined 282-kb genome of Rhizanthes (35 circular chromosomes). Strikingly, these closely related genera display a total lack of chromosomal synteny, which we link to the ancestral loss of key recombination surveillance genes (RECX, ODB1). Furthermore, while all three genera strictly conserve an identical core of 30 protein-coding genes, host-derived HGT is highly asymmetric, ranging from minimal in Rhizanthes to 60% in Sapria. In Sapria, foreign tracts are sequestered into 15 predominantly non-coding circular chromosomes, a structural arrangement that aligns with the circle-mediated HGT model validated in other holoparasites. Collectively, these parallel patterns across phylogenetically distant lineages demonstrate that sorting and maintaining foreign DNA in autonomous circular blocks is a convergent architectural outcome of massive host-to-parasite genetic transfers. SIGNIFICANCE STATEMENT Horizontal gene transfer is widespread in the nuclear genome of the parasitic plant family Rafflesiaceae, but its contribution to mitochondrial genome evolution has been assessed through the analyses of a limited number of genes. By comparing complete mitochondrial genomes of the parasites and their hosts, we found that closely related species evolved dramatically different genome architectures through distinct mechanisms: one lineage accumulated large amounts of host-derived DNA, whereas another expanded through the proliferation of repetitive sequences with limited contribution from foreign DNA. These findings show that different evolutionary processes can generate profoundly divergent mitochondrial genomes even among closely related parasitic plants.
New methodologies were examined, including genome scanning, advanced assembly tools such as GetOrganelle, and multispecies merger phylogenetic reconstruction, highlighting the necessity of multi-genome integration, the application of pan-plastome methodologies, and the expanding possibilities of chloroplast synthetic biology and genome editing to improve agriculture.
Shaima Mahfood Ebrahim Abdulrahman, M. Karaismailoğlu· Bartın University Internatio...· 0 citations
It is demonstrated that homologous recombination, genome plasticity, and lineage-specific diversification are major drivers of adaptation, ecological fitness, and pathogenic evolution in this emerging phytopathogen P. jejuense across diverse hosts and geographic regions.
Dario Arizala, S. Dobhal, Gamze Boluk et al.· bioRxiv· 0 citations
Paramecium bursaria maintains a stable endosymbiosis with green algae, yet the evolutionary consequences of this association remain unclear. Here, we screened the host genome for algal-derived horizontally transferred genes (HTGs) using a lineage-aware workflow designed to detect horizontal gene transfer (HGT) between two defined lineages. We identified 16 candidate HTGs, including four putative newly transferred genes and 12 homologous transferred genes, most of which were functionally associated with redox homeostasis and metabolism. Five HTGs showed symbiosis-dependent expression. RNAi knockdown of GH32s and SATs reduced host proliferation, total cell area, and motility, while GH32s knockdown also reduced endosymbiont load. Duplication patterns suggest that most transfers may have occurred after the P. bursaria lineage diverged from the sampled Paramecium species but before its lineage-specific whole-genome duplication (WGD). The HTGs also showed host-associated shifts in GC content and gene length, while representative HTGs retained conserved domains and functional motifs. Together, our results support algae-to-host HGT in P. bursaria and suggest that some transferred genes may contribute to metabolic integration during endosymbiosis.
Lei Yang, De-Yu Wei, Yuan Li et al.· Molecular Phylogenetics and...· 0 citations
In heterotrophic plants, the loss of photosynthesis is often associated with plastid genome (ptDNA) reduction, although the extent of genome decay varies widely among lineages and may culminate in complete genome loss. Of the multiple transitions to heterotrophy among angiosperms, the ptDNA status remains poorly defined in lineages such as the endoparasitic Mitrastemonaceae (Ericales). Adopting a panplastome perspective, we characterized genomic variation across Mitrastemon yamamotoi individuals, assembling two complete circular ptDNAs and re-evaluating all available genomic resources for the species. Our results reveal a highly minimized ptDNA (18-26 kb) with elevated AT content (>77%) and loss of the typical quadripartite architecture. The M. yamamotoi panplastome exhibits remarkable structural stability and collinearity among individuals. The reduced plastid gene set comprises 26 genes, including accD, infA, clpP, ycf1, ycf2, and the essential tetrapyrrole precursor trnE-UUC. Root-to-tip substitution-rate analyses of 13 conserved protein-coding genes revealed elevated synonymous and nonsynonymous substitution rates in M. yamamotoi relative to photosynthetic angiosperms. However, dN/dS analyses showed that the retained protein-coding genes evolve under purifying selection (ω < 1), indicating persistent functional constraint. Furthermore, transcriptomic analysis identified a nearly complete set of nuclear-encoded plastid-targeted DNA-RRR factors, with the notable exception of the MUTS2 surveillance system and two photolyases. The convergent loss of MUTS2 homologs in M. yamamotoi and holoparasitic Balanophoraceae may be linked to shared plastome features (genome compaction, accelerated substitution rates, and severe AT bias). In contrast, the shared loss of the photolyases CRY3 and UVR3 likely results from relaxed selection pressure associated with an underground lifestyle. Deciphering the M. yamamotoi panplastome provides a definitive genomic framework for understanding plastid evolution within the endoparasitic Mitrastemonaceae.
Maria Emilia Roulet, L. Gatica-Soria, L. E. Garcia et al.· Annals of Botany· 0 citations
The olive family (Oleaceae) comprises numerous species of economic, horticultural, and medicinal importance. Despite its significance, the evolutionary history of this complex family remains enigmatic. Here, we generated a high-quality haplotype-resolved genome of Forsythia suspensa, a distylous species that occupies a key phylogenetic position in Oleaceae. The two haplotypes exhibit significant allelic divergence with potential allele-specific regulation. We reconstructed the polyploidization history of Oleaceae by confirming and precisely dating a shared whole-genome triplication (WGT) and an independent whole-genome duplication (WGD) event. We revealed a complex reticulate evolution that gave rise to the tribe Oleeae: an initial hybridization between Forsythieae (♂) and Jasmineae (♀), a subsequent backcrossing event, and a final WGD. We identified a novel tandemly duplicated pectin methylesterase inhibitor (PMEI) gene cluster that regulates filament length and pollen size via restricting cell elongation in the long-styled morph. Dosage augmentation via stepwise cluster formation (0.99-3.83 Mya) may contribute to maintaining stamen traits of the long-styled morph. These FsPMEIs are co-expressed with many cell wall-related genes, suggesting a functional link in cell wall modification. Our study reveals the reticulate evolution in Oleaceae and a novel gene cluster controlling stamen development in F. suspensa, provides valuable haplotype-resolved genomic resources for heterostylous species, offering novel framework and molecular pathways to understand plant adaptive evolution.
Quanling Zhang, Ezi Zhao, Xiaomin Fu et al.· Plant Physiology· 0 citations