Li-Yaung Kuo
Alexandre Salino
Thaís Elias Almeida- 1Institute of Molecular & Cellular Biology, National Tsing Hua University, Hsinchu, Taiwan
- 2Programa de Pós-Graduação em Biologia Vegetal, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
- 3Universidade Federal de Pernambuco, Departamento de Botânica, Centro de Biociências, Recife, PE, Brazil
Editorial on the Research Topic
Biology, systematics, and evolution of ferns and lycophytes in the omics era, volume II
Ferns and lycophytes represent the earliest-diverging lineages among extant vascular plants and occupy critical positions in bridging knowledge gaps of land plant evolution (Pryer et al., 2001; Marchant et al., 2022). However, genomic research and understanding of these groups remain limited, largely due to their enormous genome sizes and limited economic interest (Kuo and Li, 2019). Partly as a result, model-organism-scale surveys in ferns and lycophytes have progressed slowly, delaying broader biological insights (Marchant et al., 2022). Nonetheless, recent advances in sequencing technologies have boosted the generation of phylogenomics, transcriptomics, and metagenomics data, among others, which are increasingly integrated into multi-omics approaches. These developments are helping to overcome the traditional limitations of working with non-model plants like most ferns and lycophytes, significantly advancing our understanding of their evolutionary biology. Through such multi-omics approaches, genomics and expression profiles of ferns and lycophytes can now be readily generated to investigate their biological processes in different tissues, developmental stages, and responses to various biotic/abiotic factors (e.g., Li et al., 2018, 2023; Peng et al., 2024). This enables us to study the unique and intriguing aspects of fern and lycophyte evolution, further clarifying both known and unresolved questions about land plant evolution, as covered by the articles in this Research Topic.
Allopolyploidy, a prevalent mode of speciation in ferns and one that may occur more frequently in these plants compared to their sister lineages (Wood et al., 2009; Barker et al., 2016), offers unique insights into genome evolution. Phegopteris decursive-pinnata Fée (Thelypteridaceae), an allotetraploid fern species derived from diploid ancestors of P. koreana B.Y.Sun & C.H.Kim and P. taiwaniana T.Fujiw., along with their artificially produced diploid F1 hybrids, has served as the model by Katayama et al. to investigate subgenome dominance at the transcriptional level. Comparative transcriptomics revealed homeolog expression bias in some genes, with a slight bias favoring the taiwaniana-subgenome dominance. Furthermore, comparisons between the diploid F1 hybrids and the naturally evolving allotetraploid suggest that the observed expression differences in the latter might have emerged during its evolutionary establishment (Katayama et al.). These significant findings highlight that, along the allopolyploid speciation pathway, heterozygosity in ferns can become not only stably fixed at the genomic level but also strongly maintained at the level of gene expression.
RNA editing is an intriguing aspect of molecular evolution that commonly occurs in the organellar genomes of ferns and lycophytes (Takenaka et al., 2013; Fauskee et al., 2025). Their mitochondrial and plastid transcripts exhibit some of the highest known levels of RNA editing among land plants, including frequent C-to-U and U-to-C post-transcriptional modifications. These RNA edits occur predominantly in protein-coding sequences (CDS), where they can restore the function of essential genes, effectively acting as correctors of underlying DNA mutations. In Isoetes, an aquatic lycophyte lineage, Pereira et al. assembled organellar genomes and transcriptomes from multiple species. The authors compared genetic divergence within the genus by examining both DNA polymorphisms and post-transcriptional variation, i.e., at the RNA and amino acid levels. Their findings revealed a notable degree of evolutionary conservatism in RNA edits dating back to the deepest divergences of extant species. At the amino acid level, these edits often increased the hydrophobicity of organellar proteins. Also, RNA editing introduces additional genetic diversity into the transcriptome, particularly evident in mitochondrial CDS genes.
Organellar phylogenomics has also proven instrumental in clarifying the evolutionary relationships of the enigmatic plant lineages (Wicke and Schneeweiss, 2015). By assembling complete plastomes and mitogenomes, Kuo et al. reconstructed a robust phylogenomic framework encompassing all genera in the fern family Ophioglossaceae, including Rhizoglossum C.Presl, which was sampled phylogenetically for the first time. Importantly, this phylogenomic tree of Ophioglossaceae resolved long-standing controversies of relationships at the subfamily level, better aligning with their morphology and genome size evolution. On these phylogenomic bases, the authors further examined putative horizontal and intracellular gene transfers (HGT and IGT) in these organellar genomes. One of their interesting findings is prevalent HGT in Ophioglossaceae mitogenomes, with mtHGTs originating predominantly from mitogenomes of other fern lineages and angiosperm lineages containing root parasites. Phylogenies of MORFFO, Mobile Open Reading Frames in Fern Organelles, in their study also revealed HGT-like or even IGT-like patterns.
Finally, the interplay between lycophytes and their symbiotic fungi is emerging as a vital yet largely unexplored subject in the coevolution of land plants. Lin et al. applied metabarcoding strategies to investigate the phyllosphere mycobiome across various aboveground tissues of the Lycopodiaceae species Huperzia asiatica (Ching) N.Shrestha & X.C.Zhang, which produces significant amounts of Huperzine A (HupA), a pharmacologically important alkaloid that may require co-synthesis with fungal partners. For comparison, the mycobiome of a non-HupA-producing Lycopodiaceae species, Diphasiastrum complanatum (L.) Holub, was also analyzed. Their findings, which contrasted HupA concentrations across tissues with the corresponding mycobiomes, reveal that members of certain fungal genera are closely associated with HupA biosynthesis. This study underscores the potential of lycophyte–fungus interactions and their symbiotic coevolution in producing secondary metabolites. Importantly, the discovery of such frontier natural products can be greatly facilitated by integrative, multi-omics approaches.
Together, these studies collectively advance our understanding of fern and lycophyte biology, systematics, and evolution across omics data. They reveal unique evolutionary processes in ferns and lycophytes and offer new frameworks for studying plant diversification, genomic signatures, and symbiosis. As foundational members of the vascular plant lineage, these groups hold untapped potential for answering long-standing evolutionary questions and exploring novel biochemical pathways.
Author contributions
LK: Conceptualization, Writing – original draft, Writing – review & editing. AS: Conceptualization, Writing – original draft, Writing – review & editing. TA: Conceptualization, Writing – original draft, Writing – review & editing.
Acknowledgments
We would like to thank the reviewers, authors, editorial team, and the Specialty Chief Editor for their collective effort in making this Research Topic possible.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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The author(s) declare that no Generative AI was used in the creation of this manuscript.
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References
Barker, M. S., Arrigo, N., Baniaga, A. E., Li, Z., and Levin, D. A. (2016). On the relative abundance of autopolyploids and allopolyploids. New Phytol. 210, 391–398. doi: 10.1111/nph.13698
Fauskee, B., Kuo, L.-Y., Heath, T., Xie, P.-J., and Pryer, K. (2025). Comparative phylogenetic analyses of RNA editing in fern plastomes. New Phytol. doi: 10.1111/nph.70244
Kuo, L.-Y. and Li, F.-W. (2019). A roadmap for fern genome sequencing. Am. Fern J. 109, 212–223. doi: 10.1640/0002-8444-109.3.212
Li, F. W., Brouwer, P., Carretero-Paulet, L., Cheng, S., de Vries, J., Delaux, P.-M., et al. (2018). Fern genomes elucidate land plant evolution and cyanobacterial symbioses. Nat. Plants 4, 460–472. doi: 10.1038/s41477-018-0188-8
Li, C., Wenjie, H., Xiaoxu, H., Guohua, Z., Wenyang, Z., Weijun, H., et al. (2023). Diel dynamics of multi-omics in elkhorn fern provide new insights into weak CAM photosynthesis. Plant Commun. 4, 100594. doi: 10.1016/j.xplc.2023.100594
Marchant, D. B., Chen, G., Cai, S., Chen, F., Schafran, P., Jenkins, J., et al. (2022). Dynamic genome evolution in a model fern. Nat. Plants 8, 1038–1051. doi: 10.1038/s41477-022-01226-7
Peng, Y., Wang, Z., Li, M., Wang, T., and Su, Y. (2024). Characterization and analysis of multi-organ full-length transcriptomes in Sphaeropteris brunoniana and Alsophila latebrosa highlight secondary metabolism and chloroplast RNA editing pattern of tree ferns. BMC Plants Bio. 24, 73. doi: 10.1186/s12870-024-04746-w
Pryer, K. M., Smith, A. R., Cranfill, R., Hunt, J. S., Wolf, P. G., Sipes, S. D., et al. (2001). Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409, 618–622. doi: 10.1038/35054555
Takenaka, M., Zehrmann, A., Verbitskiy, D., Härtel, B., and Brennicke, A. (2013). RNA editing in plants and its evolution. Annu. Rev. Genet. 47, 335–352. doi: 10.1146/annurev-genet-111212-133519
Wicke, S. and Schneeweiss, G. M. (2015). “Next-generation organellar genomics: Potentials and pitfalls of high-throughput technologies for molecular evolutionary studies and plant systematics,” in Next-Generation Sequencing in Plant Systematics. Eds. Hörandl, E. and Appelhans, M. S. (International Association for Plant Taxonomy (IAPT, Hessen), 9–50. doi: 10.14630/000002
Keywords: allopolyploidy, ferns, lycophytes, multi-omics, organellar phylogenomics, RNA editing
Citation: Kuo L-Y, Salino A and Almeida TE (2025) Editorial: Biology, systematics, and evolution of ferns and lycophytes in the omics era, volume II. Front. Plant Sci. 16:1629348. doi: 10.3389/fpls.2025.1629348
Received: 15 May 2025; Accepted: 30 June 2025;
Published: 15 July 2025.
Edited and Reviewed by:
Germinal Rouhan, Muséum National d’Histoire Naturelle, FranceCopyright © 2025 Kuo, Salino and Almeida. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Thaís Elias Almeida, dGhhaXMuZWxpYXNAdWZwZS5icg==