Plastome convergence across parasitic lineages: genome reduction, extreme AT bias, and functional persistence in the endoparasitic Mitrastemonaceae

The loss of photosynthesis triggers extreme plastid genome (ptDNA) decay, including complete genome loss. Of the multiple transitions to heterotrophy among angiosperms, the ptDNA status remains poorly defined in lineages such as the endophytic Mitrastemonaceae (Ericales). Adopting a super-panplastome perspective, we characterized genomic variation across Mitrastemon individuals, assembling two complete circular ptDNAs and re-evaluating all available genomic resources for the genus. Our results reveal a highly minimized ptDNA (18–26 kb) with extreme AT content (>77%) and loss of the typical quadripartite architecture. Despite the absence of the quadripartite genomic arrangement containing inverted repeats, the Mitrastemon super-panplastome exhibits remarkable structural stability and collinearity among individuals. The reduced suite of 26 genes, which includes accD, infA, clpP, ycf1, ycf2, and the essential tetrapyrrole precursor trnE−UUC, exhibit elevated substitution rates. Evolutionary rate analyses (dN/dS) demonstrate that while several genes show signs of relaxed selection, the core ribosomal suite remains under strong purifying selection (ω<1), confirming the organelle's functional status. Furthermore, transcriptomic analysis identified a nearly complete set of nuclear-encoded DNA-RRR genes, with the notable exception of the MUTS2 surveillance system. The convergent loss of these homologs in Mitrastemon and other holoparasitic lineages may be linked to the shared structural instability and mutational bias . Our findings demonstrate that despite extreme genome compaction, accelerated substitution rates, and severe AT-bias, the Mitrastemon super-panplastome remains quite stable, providing a definitive genomic framework for understanding plastid evolution within the endoparasitic Mitrastemonaceae.