Skip to main content
SpringerLink
Log in

The first homosporous lycophyte genome revealed the association between the recent dynamic accumulation of LTR-RTs and genome size variation

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The contrasting genome size between homosporous and heterosporous plants is fascinating. Different from the heterosporous seed plants and mainly homosporous ferns, the lycophytes are either heterosporous (Isoetales and Selaginellales) or homosporous (Lycopodiales). Many lycophytes are the resource plants of Huperzine A (HupA) which is invaluable for treating Alzheimer’s disease. For the seed-free vascular plants, several high-quality genomes of heterosporous Selaginella, homosporous ferns (maidenhair fern, monkey spider tree fern), and heterosporous ferns (Azolla) have been published and provided important insights into the origin and evolution of early land plants. However, the homosporous lycophyte genome has not been decoded. Here, we assembled the first homosporous lycophyte genome and conducted comparative genomic analyses by applying a reformed pipeline for filtering out non-plant sequences. The obtained genome size of Lycopodium clavatum is 2.30 Gb, distinguished in more than 85% repetitive elements of which 62% is long terminal repeat (LTR). This study disclosed a high birth rate and a low death rate of the LTR-RTs in homosporous lycophytes, but the opposite occurs in heterosporous lycophytes. we propose that the recent activity of LTR-RT is responsible for the immense genome size variation between homosporous and heterosporous lycophytes. By combing Ks analysis with a phylogenetic approach, we discovered two whole genome duplications (WGD). Morover, we identified all the five recognized key enzymes for the HupA biosynthetic pathway in the L. clavatum genome, but found this pathway incomplete in other major lineages of land plants. Overall, this study is of great importance for the medicinal utilization of lycophytes and the decoded genome data will be a key cornerstone to elucidate the evolution and biology of early vascular land plants.

Key message

The first homosporous lycophyte genome of Lycopodium clavatum.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig.5

Similar content being viewed by others

Data availability

The whole genome sequence data reported in this paper have been deposited in the Genome Warehouse in National Genomics Data Center (Chen et al. 2021a, b; CNCB-NGDC Members and Partners 2022), Beijing Institute of Genomics, Chinese Academy of Sciences / China National Center for Bioinformation, under accession number GWHBJYW00000000 that is publicly accessible at https://ngdc.cncb.ac.cn/gwh. And the gene annotations are available at https://figshare.com/articles/dataset/Lycopodium_clavatum_genome_annotation/20493417.

References

  • Ainge GD, Lorimer SD, Gerard PJ, Ruf LD (2002) Insecticidal activity of huperzine A from the New Zealand clubmoss, Lycopodium varium. J Agric Food Chem 50:491–494

    Article  CAS  PubMed  Google Scholar 

  • Baniaga AE, Barker MS (2019) Nuclear genome size is positively correlated with median LTR-RT insertion time in fern and lycophyte genomes. American Fern Journal 109:248–266

    Article  Google Scholar 

  • Banks JA, Nishiyama T, Hasebe M, Bowman JL, Gribskov M, dePamphilis C et al (2011) The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332:960–963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bao Z, Eddy SR (2002) Automated de novo identification of repeat sequence families in sequenced genomes. Genome Res 12:1269–1276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barba-Montoya J, Dos RM, Schneider H, Donoghue PCJ, Yang Z (2018) Constraining uncertainty in the timescale of angiosperm evolution and the veracity of a Cretaceous Terrestrial Revolution. New Phytol 218:819–834

    Article  PubMed  PubMed Central  Google Scholar 

  • Barker MS, Wolf PG (2010) Unfurling fern biology in the genomics age. Bioscience 60:177–185

    Article  Google Scholar 

  • Bateman, R.M. (1996) An overview of lycophyte phylogeny. In Pteridology in Perspective (Camus J.M., Gibby M. and Johns R.J. eds). London: Royal Botanic Gardens, Kew, pp. 405–415.

  • Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Birney E, Clamp M, Durbin R (2004) GeneWise and genomewise. Genome Res 14:988–995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59–60

    Article  CAS  PubMed  Google Scholar 

  • Bunsupa S, Hanada K, Maruyama A, Aoyagi K, Kana K, Ueno H et al (2016) Molecular evolution and functional characterization of a bifunctional decarboxylase involved in lycopodium alkaloid biosynthesis. Plant Physiol 171:2432–2444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen M, Ma Y, Wu S, Zheng X, Kang H, Sang J et al (2021a) Genome Warehouse: a public repository housing genome-scale data. Genomics Proteomics Bioinformatics 19:584–589

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen S, Zhang M, Wang J, Zhang X (2021b) Original plant and research progress of the medicinal plant Huperzia javanica. Guihaia 41:1794–1809

    Google Scholar 

  • Chen H, Fang Y, Zwaenepoel A, Huang S, Van de Peer Y, Li Z (2023) Revisiting ancient polyploidy in leptosporangiate ferns. New Phytol 237:1405–1417

    Article  CAS  PubMed  Google Scholar 

  • CNCB-NGDC Members & Partners (2022) Database resources of the national genomics data center, China national center for bioinformation in 2022. Nucleic Acids Res 50:D27-38

    Article  Google Scholar 

  • Ellinghaus D, Kurtz S, Willhoeft U (2008) LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics 9:18

    Article  PubMed  PubMed Central  Google Scholar 

  • Emms DM, Kelly S (2019) OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol 20:238

    Article  PubMed  PubMed Central  Google Scholar 

  • Fang Y, Qin X, Liao Q, Du R, Luo X, Zhou Q et al (2022) The genome of homosporous maidenhair fern sheds light on the euphyllophyte evolution and defences. Nature Plants 8:1024–1037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feschotte C, Jiang N, Wessler SR (2002) Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3:329–341

    Article  CAS  PubMed  Google Scholar 

  • Flynn JM, Hubley R, Goubert C, Rosen J, Clark AG, Feschotte C et al (2020) RepeatModeler2 for automated genomic discovery of transposable element families. Proc Natl Acad Sci USA 117:9451–9457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao L, Su YJ, Wang T (2010) Plastid genome sequencing, comparative genomics, and phylogenomics: current status and prospects. J Syst Evol 48:77–93

    Article  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I et al (2013) Trinity: reconstructing a full-length transcriptome without a genome from RNA-seq data. Nat Biotechnol 29:644

    Article  Google Scholar 

  • Griffiths-Jones S, Grocock RJ, Van Dongen S, Bateman A, Enright AJ (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34:D140-144

    Article  CAS  PubMed  Google Scholar 

  • Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith RK Jr, Hannick LI et al (2003) Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res 31:5654–5666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haas BJ, Salzberg SL, Zhu W, Pertea M, Allen JE, Orvis J et al (2008) Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biol 9:R7

    Article  PubMed  PubMed Central  Google Scholar 

  • Hanson L, Leitch IJ (2002) DNA amounts for five pteridophyte species fill phylogenetic gaps in C-value data. Bot J Linn Soc 140:169–173

    Article  Google Scholar 

  • Haufler CH (1987) Electrophoresis is modifying our concepts of evolution in homosporous pteridophytes. Am J Bot 74:953–966

    Article  Google Scholar 

  • Horn K, Franke T, Unterseher M, Schnittler M, Beenken L (2013) Morphological and molecular analyses of fungal endophytes of achlorophyllous gametophytes of Diphasiastrum alpinum (Lycopodiaceae). Am J Bot 100:2158–2174

    Article  PubMed  Google Scholar 

  • Huang CH, Qi X, Chen D, Qi J, Ma H (2020) Recurrent genome duplication events likely contributed to both the ancient and recent rise of ferns. J Integr Plant Biol 62:433–455

    Article  PubMed  Google Scholar 

  • Jiao Y, Li J, Tang H, Paterson AH (2014) Integrated syntenic and phylogenomic analyses reveal an ancient genome duplication in monocots. Plant Cell 26:2792–2802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang X, Liu C, Shen P, Hu L, Lin R, Ling J et al (2019) Genomic characterization provides new insights into the biosynthesis of the secondary metabolite huperzine a in the endophyte Colletotrichum gloeosporioides Cg01. Front Microbiol 9:3237

    Article  PubMed  PubMed Central  Google Scholar 

  • Keilwagen J, Hartung F, Grau J (2019) GeMoMa: Homology-based gene prediction utilizing intron position conservation and RNA-seq data. Methods Mol Biol 1962:161–177

    Article  CAS  PubMed  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klekowski E, Baker H (1966) Evolutionary significance of polyploidy in the pteridophyta. Science 153:305–307

    Article  PubMed  Google Scholar 

  • Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH, Phillippy AM (2017) Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res 27:722–736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Korf I (2004) Gene finding in novel genomes. BMC Bioinformatics 5:59

    Article  PubMed  PubMed Central  Google Scholar 

  • Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35:4453–4455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuo LY, Li FW (2019) A roadmap for fern genome sequencing. American Fern Journal 109:212–223

    Article  Google Scholar 

  • Lang D, Ullrich KK, Murat F, Fuchs J, Jenkins J, Haas FB et al (2018) The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution. Plant J 93:515–533

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Barker MS (2020) Inferring putative ancient whole-genome duplications in the 1000 Plants (1KP) initiative: access to gene family phylogenies and age distributions. Gigascience 9:giaa004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Richard D (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N et al (2009) The sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Li J, Wang S, Jing Y, Wang L, Zhou S (2013) A modified CTAB protocol for plant DNA extraction. Chinese Journal of Botany 48:72–78

    Article  Google Scholar 

  • Li FW, Brouwer P, Carretero-Paulet L, Cheng S, de Vries J, Delaux PM et al (2018) Fern genomes elucidate land plant evolution and cyanobacterial symbioses. Nature Plants 4:460–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, B., Shi, Y., Yuan, J., Galaxy, Y., Zhang, H., Li, N. et al. (2013) Estimation of genomic characteristics by analyzing k-mer frequency in de novo genome projects. arXiv.

  • Loman, T. (2017) A novel method for predicting ribosomal RNA genes in prokaryotic genomes. http://lup.lub.lu.se/student-papers/record/8914064.

  • Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo H, Li Y, Sun C, Wu Q, Song J, Sun Y et al (2010a) Comparison of 454-ESTs from Huperzia serrata and Phlegmariurus carinatus reveals putative genes involved in lycopodium alkaloid biosynthesis and developmental regulation. BMC Plant Biol 10:1

    Article  Google Scholar 

  • Luo H, Sun C, Li Y, Wu Q, Song J, Wang D et al (2010b) Analysis of expressed sequence tags from the Huperzia serrata leaf for gene discovery in the areas of secondary metabolite biosynthesis and development regulation. Physiol Plant 139:1–2

    Article  CAS  PubMed  Google Scholar 

  • Lyu H, He Z, Wu CI, Shi S (2018) Convergent adaptive evolution in marginal environments: unloading transposable elements as a common strategy among mangrove genomes. New Phytol 217:428–438

    Article  CAS  PubMed  Google Scholar 

  • Marchant DB, Sessa EB, Wolf PG, Heo K, Barbazuk WB, Soltis PS et al (2019) The C-Fern (Ceratopteris richardii) genome: insights into plant genome evolution with the first partial homosporous fern genome assembly. Sci Rep 9:18181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marchant DB, Chen G, Cai S, Chen F, Schafran P, Jenkins J et al (2022) Dynamic genome evolution in a model fern. Nature Plants 8:1038–1051

    Article  PubMed  PubMed Central  Google Scholar 

  • Nakazato, T., Barker, M.S., Rieseberg, L.H. & Gastony, G.J. (2008) Evolution of the nuclear genome of ferns and lycophytes. In Biology and evolution of ferns and lycophytes (Ranker T.A. & Haufler C.H. eds.). Cambridge: Cambridge University Press, pp. 175–198.

  • Nawrocki EP, Eddy SR (2013) Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29:2933–2935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426

    CAS  PubMed  Google Scholar 

  • One Thousand Plant Transcriptomes Initiative (2019) One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574:679–685

    Article  CAS  Google Scholar 

  • Ou S, Jiang N (2018) LTR_retriever: A highly accurate and sensitive program for identification of long terminal repeat retrotransposons. Plant Physiol 176:1410–1422

    Article  CAS  PubMed  Google Scholar 

  • Ou S, Chen J, Jiang N (2018) Assessing genome assembly quality using the LTR Assembly Index (LAI). Nucleic Acids Res 46:e126

    PubMed  PubMed Central  Google Scholar 

  • Parra G, Bradnam K, Korf I (2007) CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23:1061–1067

    Article  CAS  PubMed  Google Scholar 

  • Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33:290–295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Price AL, Jones NC, Pevzner PA (2005) De novo identification of repeat families in large genomes. Bioinformatics 21:351–358

    Article  Google Scholar 

  • Qiao X, Li Q, Yin H, Qi K, Li L, Wang R et al (2019) Gene duplication and evolution in recurring polyploidization-diploidization cycles in plants. Genome Biol 20:38

    Article  PubMed  PubMed Central  Google Scholar 

  • Roach MJ, Schmidt SA, Borneman AR (2018) Purge Haplotigs: Allelic contig reassignment for third-gen diploid genome assemblies. BMC Bioinformatics 19:460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sahidan N, Choo CY, Latiff A, Jaman R (2012) Variations of huperzine A content in Lycopodiaceae species from tropics. Chin J Nat Med 10:125–128

    Article  CAS  Google Scholar 

  • Schneider H, Smith AR, Pryer KM (2009) Is morphology really at odds with molecules in estimating fern phylogeny? Syst Bot 34:455–475

    Article  Google Scholar 

  • Schuettpelz E, Schneider H, Smith AR, Hovenkamp P, Prado J, Rouhan G et al (2016) A community-derived classification for extant lycophytes and ferns. J Syst Evol 54:563–603

    Article  Google Scholar 

  • Seppey M, Manni M, Zdobnov EM (2019) BUSCO: Assessing genome assembly and annotation completeness. Methods Mol Biol 1962:227–245

    Article  CAS  PubMed  Google Scholar 

  • Sessa EB, Der JP (2016) Evolutionary genomics of ferns and lycophytes. Adv Bot Res 78:215–254

    Article  Google Scholar 

  • She R, Chu JS, Wang K, Pei J, Chen N (2009) GenBlastA: enabling BLAST to identify homologous gene sequences. Genome Res 19:143–149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shu S, Zhao X, Wang W, Zhang G, Cosoveanu A, Ahn Y et al (2014) Identification of a novel endophytic fungus from Huperzia serrata which produces huperzine A. World J Microbiol Biotechnol 30:3101–3109

    Article  CAS  PubMed  Google Scholar 

  • Simao FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–3212

    Article  CAS  PubMed  Google Scholar 

  • Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B (2006) AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res 34:W435-439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su J, Yang M (2015) Huperzine A production by Paecilomyces tenuis YS-13, an endophytic fungus isolated from Huperzia serrata. Nat Prod Res 29:1035–1041

    Article  CAS  PubMed  Google Scholar 

  • Sun JY, Morita H, Chen G, Noguchi H, Abe I (2012) Molecular cloning and characterization of copper amine oxidase from Huperzia serrata. Bioorg Med Chem Lett 22:5784–5790

    Article  CAS  PubMed  Google Scholar 

  • Szövényi P, Gunadi A, Li FW (2021) Charting the genomic landscape of seed-free plants. Nature Plants 7:554–565

    Article  PubMed  Google Scholar 

  • Tang XC, Han YF, Chen XP, Zhu XD (1986) Effects of huperzine A on learning and the retrieval process of discrimination performance in rats. Acta Pharmacol Sin 7:507

    CAS  Google Scholar 

  • Tang XC, De Sarno P, Sugaya K, Giacobini E (1989) Effect of huperzine A, a new cholinesterase inhibitor, on the central cholinergic system of the rat. J Neurosci Res 24:276–285

    Article  CAS  PubMed  Google Scholar 

  • Tang S, Lomsadze A, Borodovsky M (2015) Identification of protein coding regions in RNA transcripts. Nucleic Acids Res 43:e78

    Article  PubMed  PubMed Central  Google Scholar 

  • Tarailo-Graovac M, Chen N (2009) Using RepeatMasker to identify repetitive elements in genomic sequences. Curr Protoc Bioinformatics 4:10

    Google Scholar 

  • U’Ren JM, Lutzoni F, Miadlikowska J, Laetsch AD, Arnold AE (2012) Host and geographic structure of endophytic and endolichenic fungi at a continental scale. Am J Bot 99:898–914

    Article  PubMed  Google Scholar 

  • VanBuren R, Wai CM, Ou S, Pardo J, Bryant D, Jiang N et al (2018) Extreme haplotype variation in the desiccation-tolerant clubmoss Selaginella lepidophylla. Nat Commun 9:13

    Article  PubMed  PubMed Central  Google Scholar 

  • Wagner WH, Wagner FS (1979) Polyploidy in pteridophytes. Basic Life Sci 13:199–214

    PubMed  Google Scholar 

  • Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S et al (2014) Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9:e112963

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Zeng QG, Zhang ZB, Yan RM, Wang LY, Zhu D (2011) Isolation and characterization of endophytic huperzine A-producing fungi from Huperzia serrata. J Ind Microbiol Biotechnol 38:1267–1278

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Sun P, Li Y, Liu Y, Yang N, Yu J et al (2018) An overlooked paleotetraploidization in cucurbitaceae. Mol Biol Evol 35:16–26

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Zheng Z, Li Y, Hu H, Wang Z, Du X et al (2021) Which factors contribute most to genome size variation within angiosperms? Ecol Evol 11:2660–2668

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang FG, Wang AH, Bai CK, Jin DM, Nie LY, Harris AJ et al (2022) Genome size evolution of the extant lycophytes and ferns. Plant Diversity 44:141–152

    Article  PubMed  PubMed Central  Google Scholar 

  • Wanibuchi K, Zhang P, Abe T, Morita H, Kohno T, Chen G et al (2007) An acridone-producing novel multifunctional type III polyketide synthase from Huperzia serrata. FEBS J 274:1073–1082

    Article  CAS  PubMed  Google Scholar 

  • Wendel JF, Jackson SA, Meyers BC, Wing RA (2016) Evolution of plant genome architecture. Genome Biol 17:37

    Article  PubMed  PubMed Central  Google Scholar 

  • Wickell D, Kuo LY, Yang HP, Ashok AD, Irisarri I, Dadras A et al (2021) Underwater CAM photosynthesis elucidated by Isoetes genome. Nat Commun 12:6348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolf PG, Sessa EB, Marchant DB, Li FW, Rothfels CJ, Sigel EM et al (2015) An exploration into fern genome space. Genome Biol Evol 7:2533–2544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia ZQ, Wei ZY, Shen H, Shua JP, Wang T, Gu YF et al (2022) Lycophyte transcriptomes reveal two whole-genome duplications in Lycopodiaceae: Insights into the polyploidization of Phlegmariurus. Plant Diversity 44:262–270

    Article  PubMed  Google Scholar 

  • Xu Z, Wang H (2007) LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res 35:W265-268

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu BF, Lei L, Zhu X, Zhou XC, Zhou YQ, Xiao YL (2017) Identification and characterization of L-lysine decarboxylase from Huperzia serrata and its role in the metabolic pathway of lycopodium alkaloid. Phytochemistry 136:23–30

    Article  CAS  PubMed  Google Scholar 

  • Xu Z, Xin T, Bartels D, Li Y, Gu W, Yao H et al (2018) Genome analysis of the ancient tracheophyte Selaginella tamariscina reveals evolutionary features relevant to the acquisition of desiccation tolerance. Mol Plant 11:983–994

    Article  CAS  PubMed  Google Scholar 

  • Yang MQ, You WJ, Wu SW, Fan Z, Xu BF, Zhu ML et al (2017) Global transcriptome analysis of Huperzia serrata and identification of critical genes involved in the biosynthesis of huperzine A. BMC Genomics 18:245

    Article  PubMed  PubMed Central  Google Scholar 

  • Zedek F, Smerda J, Smarda P, Bureš P (2010) Correlated evolution of LTR retrotransposons and genome size in the genus Eleocharis. BMC Plant Biol 10:265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang FF, Wang MZ, Zheng YX, Liu HY, Zhang XQ, Wu SS (2015) Isolation and characterzation of endophytic huperzine A-producing fungi from Phlegmariurus phlegmaria. Microbiology 84:701–709

    Article  CAS  Google Scholar 

  • Zhang J, Fu XX, Li RQ, Zhao X, Liu Y, Li MH et al (2020) The hornwort genome and early land plant evolution. Nature Plants 6:107–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank two anonymous reviewers for their helpful remarks. This work was supported by the National Natural Science Foundation of China (Grant No.32170233, Grant No.32270248), and the Youth Innovation Promotion Association CAS (Grant No.2021075). We thank Fan Chun-Xue, Xiang Zi-Yu, and Xie Yang-Qin for providing technical assistance and suggestions for data analyses.

Author information

Author notes

  1. Ji-Gao Yu and Jun-Yong Tang have been contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, The Chinese Academy of Sciences, Beijing, 100093, China

    Ji-Gao Yu, Jun-Yong Tang, Ran Wei, Mei-Fang Lan, Rui-Chen Xiang, Xian-Chun Zhang & Qiao-Ping Xiang

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Ji-Gao Yu, Jun-Yong Tang & Mei-Fang Lan

  3. China National Botanical Garden, Beijing, China

    Ji-Gao Yu, Jun-Yong Tang, Ran Wei, Mei-Fang Lan, Xian-Chun Zhang & Qiao-Ping Xiang

Authors
  1. Ji-Gao Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun-Yong Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ran Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mei-Fang Lan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rui-Chen Xiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xian-Chun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Qiao-Ping Xiang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

XQP and ZXC conceived the project, designed the experiments, and revised the manuscript. YJG and TJY wrote the manuscript. YJG and LMF analyzed the data. YJG developed the Pipeline for Post-assembly Decontamination. YJG and TJY finalized the Figures and Tables. WR and XRC assisted in writing and editing. All authors have read and approved the manuscript.

Corresponding authors

Correspondence to Xian-Chun Zhang or Qiao-Ping Xiang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest associated with this work.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLS 9132 KB)

Supplementary file2 (PDF 6493 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, JG., Tang, JY., Wei, R. et al. The first homosporous lycophyte genome revealed the association between the recent dynamic accumulation of LTR-RTs and genome size variation. Plant Mol Biol 112, 325–340 (2023). https://doi.org/10.1007/s11103-023-01366-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-023-01366-0

Keywords

Search

Navigation