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PremisePhylogenetic trees of bryophytes provide important evolutionary context for land plants. However, published inferences of overall embryophyte relationships vary considerably. We performed phylogenomic analyses of bryophytes and relatives using both mitochondrial and plastid gene sets, and investigated bryophyte plastome evolution. MethodsWe employed diverse likelihood‐based analyses to infer large‐scale bryophyte phylogeny for mitochondrial and plastid data sets. We tested for changes in purifying selection in plastid genes of a mycoheterotrophic liverwort (Aneura mirabilis) and a putatively mycoheterotrophic moss (Buxbaumia), and compared 15 bryophyte plastomes for major structural rearrangements. ResultsOverall land‐plant relationships conflict across analyses, generally weakly. However, an underlying (unrooted) four‐taxon tree is consistent across most analyses and published studies. Despite gene coverage patchiness, relationships within mosses, liverworts, and hornworts are largely congruent with previous studies, with plastid results generally better supported. Exclusion ofRNAedit sites restores cases of unexpected non‐monophyly to monophyly forTakakiaand two hornwort genera. Relaxed purifying selection affects multiple plastid genes in mycoheterotrophicAneurabut notBuxbaumia. Plastid genome structure is nearly invariant across bryophytes, but thetufA locus, presumed lost in embryophytes, is unexpectedly retained in several mosses. ConclusionsA common unrooted tree underlies embryophyte phylogeny, [(liverworts, mosses), (hornworts, vascular plants)]; rooting inconsistency across studies likely reflects substantial distance to algal outgroups. Analyses combining genomic and transcriptomic data may be misled locally for heavilyRNA‐edited taxa. TheBuxbaumiaplastome lacks hallmarks of relaxed selection found in mycoheterotrophicAneura. Autotrophic bryophyte plastomes, includingBuxbaumia, hardly vary in overall structure.
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Evolution of Whirly1 in the angiosperms: sequence, splicing, and expression in a clade of early transitional mycoheterotrophic orchids
The plastid-targeted transcription factorWhirly1(WHY1) has been implicated in chloroplast biogenesis, plastid genome stability, and fungal defense response, which together represent characteristics of interest for the study of autotrophic losses across the angiosperms. While gene loss in the plastid and nuclear genomes has been well studied in mycoheterotrophic plants, the evolution of the molecular mechanisms impacting genome stability is completely unknown. Here, we characterize the evolution ofWHY1in four early transitional mycoheterotrophic orchid species in the genusCorallorhizaby synthesizing the results of phylogenetic, transcriptomic, and comparative genomic analyses withWHY1genomic sequences sampled from 21 orders of angiosperms. We found an increased number of non-canonicalWHY1isoforms assembled from all but the greenestCorallorhizaspecies, including intron retention in some isoforms. WithinCorallorhiza, phylotranscriptomic analyses revealed the presence of tissue-specific differential expression ofWHY1in only the most photosynthetically capable species and a coincident increase in the number of non-canonicalWHY1isoforms assembled from fully mycoheterotrophic species. Gene- and codon-level tests ofWHY1selective regimes did not infer significant signal of either relaxed selection or episodic diversifying selection inCorallorhizabut did so for relaxed selection in the late-stage full mycoheterotrophic orchidsEpipogium aphyllumandGastrodia elata. Additionally, nucleotide substitutions that most likely impact the function ofWHY1, such as nonsense mutations, were only observed in late-stage mycoheterotrophs. We propose that our findings suggest that splicing and expression changes may precede the selective shifts we inferred for late-stage mycoheterotrophic species, which therefore does not support a primary role forWHY1in the transition to mycoheterotrophy in the Orchidaceae. Taken together, this study provides the most comprehensive view ofWHY1evolution across the angiosperms to date.
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- Award ID(s):
- 2117043
- PAR ID:
- 10571873
- Publisher / Repository:
- Fronteirs in Plant Science
- Date Published:
- Journal Name:
- Frontiers in Plant Science
- Volume:
- 15
- ISSN:
- 1664-462X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fpls.2024.1241515
