Plastome convergence across endoparasitic plant lineages: genome reduction, high AT bias, elevated substitution rates, and functional persistence in Mitrastemon yamamotoi.

Abstract

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.