Biology subjects

Roulet, M. E.

Publications and source records attributed to Roulet, M. E..

3 recordsLinked to original sources

bioRxiv2026

Plastome convergence across heterotrophic plant lineages: genome reduction, extreme AT bias, high substitution rates, 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 panplastome perspective, we characterized genomic variation across Mitrastemon yamamotoi 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 stabilizing inverted repeats, the Mitrastemon 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 the core ribosomal suite remains under strong purifying selection ({omega}<1), confirming the organelles 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 another holoparasitic lineage 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 panplastome remains quite stable, providing a definitive genomic framework for understanding plastid evolution within the endoparasitic Mitrastemonaceae.

evolutionary biology↗

bioRxiv2025

A structural solution to functional HGT: Gene chimerism bypasses mitochondrial expression barriers in parasitic plants

Horizontal Gene Transfer (HGT) in plant mitochondria is frequent, yet acquired genes are rarely functional due to expression barriers. The holoparasitic plant Lophophytum mirabile (Balanophoraceae) is an exceptional case, having functionally replaced numerous native mitochondrial genes with host-derived xenologs. This system provides a unique opportunity to investigate the mechanisms of functional HGT assimilation. Here, we assembled mitochondrial genomes of the sister species L. pyramidale and their mimosoid hosts and analyzed expression data from both holoparasites. We show that this extensive functional integration occurred without the co-transfer of nuclear regulatory factors; Lophophytum relies entirely on its pre-existing, native machinery. Our results demonstrate that the primary mechanism enabling Lophophytum to overcome the transcription barrier is structural: most functional xenologs are chimeric and retain native 5' regions that likely place foreign coding sequences under the control of a recognizable native promoter. This structural solution is complemented by post-transcriptional flexibility, as the RNA editing machinery efficiently processes novel host-specific sites. However, functional replacement appears biased towards genes with inherently low editing requirements and no introns, highlighting a strong selective filter. Taken together, our results show that functional integration is driven by a combination of structural integration and the flexibility of the native regulatory system.

genomics↗

bioRxiv2025

Circle-Mediated HGT shapes the multichromosomal mitochondrial genome of the endoparasite Mitrastemon yamamotoi

Horizontal gene transfer (HGT), a well-established driver of genome evolution in prokaryotes, was historically considered rare in plants. However, accumulating genomic evidence supports its occurrence in angiosperms, impacting both nuclear and mitochondrial genomes, particularly in parasitic species that establish vascular connections with their hosts. Despite the increasing recognition of HGT in a few clades of parasitic plants (e.g., Balanophoraceae, Rafflesiaceae, and Cynomoriaceae), the underlying mechanisms and evolutionary consequences of these transfers are still not fully understood. Mitrastemon yamamotoi, a holoparasitic endoparasite in the order Ericales, invades the roots of host trees in the Fagaceae family, creating favorable conditions for HGT. In this study, we assembled for the first time the mtDNA of Mitrastemon, revealing a multipartite structure consisting of 51 circular-mapping chromosomes. Phylogenetic and comparative genomic analyses uncovered extensive HGT from Fagaceae hosts, affecting both coding and non-coding regions. Notably, more than 60% of the Mitrastemon mtDNA is of foreign origin, and seven chromosomes are entirely foreign, with structural signatures in the donor mtDNA consistent with the recently proposed circle-mediated HGT model. Additionally, we detected six protein-coding genes of foreign origin and one chimeric gene. Remarkably, a foreign atp1 gene has replaced the missing native copy and represents a rare event of functional HGT in plant mitochondria. These results position Mitrastemon as a valuable model for studying mtDNA evolution and deepening our understanding of the HGT process. Our findings expand the range of lineages in which circle-mediated HGT has been documented, suggesting it is a more widespread and fundamental mode of mitochondrial HGT in plants. Significant StatementParasitic plants form intimate connections with their hosts, but how these interactions influence genome evolution remains poorly understood. Our study shows that Mitrastemon yamamotoi has acquired over 60% of its mitochondrial DNA from its host through horizontal gene transfer, including entire foreign chromosomes. These findings provide strong support for a recently proposed mechanism, circle-mediated HGT, and suggest that this process may be a more widespread driver of mitochondrial genome evolution in flowering plants.

evolutionary biology↗