Preview

Vavilov Journal of Genetics and Breeding

Advanced search

Flax transposons: unraveling their impact on domestication and agronomic trait variation

https://doi.org/10.18699/vjgb-25-131

Abstract

Flax is an important agricultural crop with multifunctional uses. Diversified breeding for oil content in seeds and fiber in stems has led to the emergence of two morphotypes – fiber flax and oilseed flax. Previously, using single nucleotide polymorphisms (SNPs), we characterized the genetic diversity of 306 flax samples from the collection of the Russian Federal Research Center for Bast Crops. However, larger structural variations, such as mobile genetic elements, also play a significant role in shaping agronomically important plant traits and can be used for further flax improvement. Here, we used the same flax collection to predict sites of new transposon insertions and to assess the role of such insertions in the formation of agronomically important traits, as well as in the process of flax domestication. We discovered 588,480 new transposon insertion sites not present in the reference flax genome (NCBI assembly ASM22429v2), the majority of which were attributed to retrotransposons of the Copia and Gypsy superfamilies, while among DNA transposons, insertion sites of the MULE-MuDR, hAT, and CMC-EnSpm superfamilies were most common. Unlike SNPs, which were significantly more numerous in oilseed flax than in fiber flax, we did not find such a substantial difference in the number of insertions of different transposon families per plant among samples of different morphotypes. Analysis of genomic regions affected by recent breeding efforts revealed a total of 61 candidate regions, of which 18 regions overlapped with QTLs associated with important agronomic traits. Interestingly, 5 regions of reduced genetic diversity in kryazhs and cultivars compared to landraces were also identified as regions of reduced diversity when using single nucleotide polymorphisms as markers. A genomewide association study (GWAS) identified 50 TE insertions associated with different phenotypic traits, with many associations confirmed by multiple models or detected in data from multiple years. Thus, transposon insertion sites are an important source of genetic diversity in flax, alongside single nucleotide polymorphisms, making them suitable for further crop improvement in breeding.

About the Authors

M. A. Duk
Ioffe Institute of the Russian Academy of Sciences,
Russian Federation

St. Petersburg



V. A. Stanin
Peter the Great St. Petersburg Polytechnic University
Russian Federation

St. Petersburg



A. A. Kanapin
Peter the Great St. Petersburg Polytechnic University
Russian Federation

St. Petersburg



A. A. Samsonova
Peter the Great St. Petersburg Polytechnic University
Russian Federation

St. Petersburg



T. A. Rozhmina
Federal Research Center for Bast Fiber Crops
Russian Federation

Torzhok



M. G. Samsonova
Peter the Great St. Petersburg Polytechnic University
Russian Federation

St. Petersburg



References

1. Alexander D.H., Novembre J., Lange K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 2009;19(9):16551664. doi 10.1101/gr.094052.109

2. Bourque G., Burns K.H., Gehring M., Gorbunova V., Seluanov A., Hammell M., Imbeault М., Izsvák Z., Levin H.L., Macfarlan T.S., Mager D.L., Feschotte C. Ten things you should know about transposable elements. Genome Biol. 2018;19(1):199. doi 10.1186/s13059-018-1577-z

3. Breitenbach H.H., Wenig M., Wittek F., Jordá L., Maldonado-Alconada A.M., Sarioglu H., Colby T., Knappe C., Bichlmeier M., Pabst E., Mackey D., Parker J.E., Vlot A.C. Contrasting roles of the apoplastic aspartyl protease APOPLASTIC, ENHANCED DISEASE SUSCEPTIBILITY1-DEPENDENT1 and LEGUME LECTIN-LIKE PROTEIN1 in Arabidopsis systemic acquired resistance. Plant Physiol. 2014;165(2):791-809. doi 10.1104/pp.114.239665

4. Danecek P., Auton A., Abecasis G., Albers C.A., Banks E., DePristo M.A., Handsaker R.E., Lunter G., Marth G.T., Sherry S.T., McVean G., Durbin R.; 1000 Genomes Project Analysis Group. The variant call format and VCFtools. Bioinformatics. 2011;27(15):2156-2158. doi 10.1093/bioinformatics/btr330

5. Duk M., Kanapin A., Rozhmina T., Bankin M., Surkova S., Samsonova A., Samsonova M. The genetic landscape of fiber flax. Front Plant Sci. 2021;12:764612. doi 10.3389/fpls.2021.764612

6. Duk M.A., Kanapin A.A., Samsonova A.A., Bankin M.P., Samsonova М.G. The IIIVmrMLM method uncovers new genetic variants associated with resistance to Fusarium wilt in flax. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov J Genet Breed. 2025;29(3): 380-391. doi 10.18699/vjgb-25-41

7. Flutre T., Duprat E., Feuillet C., Quesneville H. Considering transposable element diversification in de novo annotation approaches. PloS One. 2011;6(1):e16526. doi 10.1371/journal.pone.0016526

8. Geldner N., Anders N., Wolters H., Keicher J., Kornberger W., Muller P., Delbarre A., Ueda T., Nakano A, Jürgens G. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell. 2003;112(2):219-230. doi 10.1016/s0092-8674(03)00003-5

9. Goudenhooft C., Bourmaud A., Baley C. Flax (Linum usitatissimum L.) fibers for composite reinforcement: exploring the link between plant growth, cell walls development, and fiber properties. Front Plant Sci. 2019;10:411. doi 10.3389/fpls.2019.00411

10. Helbaek H. Domestication of food plants in the Old World. Joint efforts by botanists and archeologists illuminate the obscure history of plant domestication. Science. 1959;130(3372):365-372. doi 10.1126/science.130.3372.365

11. Kanapin A., Rozhmina T., Bankin M., Surkova S., Duk M., Osyagina E., Samsonova M. Genetic determinants of fiber-associated traits in flax identified by Omics data integration. Int J Mol Sci. 2022;23(23):14536. doi 10.3390/ijms232314536

12. Karim S., Lundh D., Holmström K.O., Mandal A., Pirhonen M. Structural and functional characterization of AtPTR3, a stress-induced peptide transporter of Arabidopsis. J Mol Model. 2005;11(3):226236. doi 10.1007/s00894-005-0257-6

13. Lin S.H., Kuo H.F., Canivenc G., Lin C.S., Lepetit M., Hsu P.K., Tillard P., Lin H.L., Wang Y.Y., Tsai C.B., Gojon A., Tsay Y.F. Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport. Plant Cell. 2008;20(9):2514-2528. doi 10.1105/tpc.108.060244

14. Liscum E., Reed J.W. Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol. 2002;49(3-4):387-400. doi 10.1023/A:1015255030047

15. Meyer A., Eskandari S., Grallath S., Rentsch D. AtGAT1, a high affinity transporter for γ-aminobutyric acid in Arabidopsis thaliana. J Biol Chem. 2006;281(11):7197-7204. doi 10.1074/jbc.M510766200

16. Mhiri C., Borges F., Grandbastien M.-A. Specificities and dynamics of transposable elements in land plants. Biology. 2022;11(4):488. doi 10.3390/biology11040488

17. Niu X.M., Xu Y.C., Li Z.W., Bian Y.T., Hou X.H., Chen J.F., Zou Y.P., Jiang J., Wu Q., Ge S., Balasubramanian S., Guo Y.L. Transposable elements drive rapid phenotypic variation in Capsella rubella. Proc Natl Acad Sci USA. 2019;116(14):6908-6913. doi 10.1073/pnas.1811498116

18. Pulido M., Casacuberta J.M. Transposable element evolution in plant genome ecosystems. Curr Opin Plant Biol. 2023;75:102418. doi 10.1016/j.pbi.2023.102418

19. Quesneville H. Twenty years of transposable element analysis in the Arabidopsis thaliana genome. Mob DNA. 2020;11:28. doi 10.1186/s13100-020-00223-x

20. Schrader L., Schmitz J. The impact of transposable elements in adaptive evolution. Mol Ecol. 2019;28(6):1537-1549. doi 10.1111/mec.14794

21. Stanin V.A., Duk М.A., Kanapin А.A., Samsonova А.A., Surkova S.Y., Samsonova М.G. Chickpea diversity driven by transposon insertion polymorphism. Vavilovskii Zhurnal Genetiki i Selek tsii = Vavilov J Genet Breed. 2025;29(1):61-71. doi 10.18699/vjgb-25-08

22. Takemoto K., Ebine K., Askani J.C., Krüger F., Gonzalez Z.A., Ito E., Goh T., Schumacher K., Nakano A., Ueda T. Distinct sets of tethering complexes, SNARE complexes, and Rab GTPases mediate membrane fusion at the vacuole in Arabidopsis. Proc Natl Acad Sci USA. 2018;115(10):E2457-E2466. doi 10.1073/pnas.1717839115

23. Veiseth S.V., Rahman M.A., Yap K.L., Fischer A., Egge-Jacobsen W., Reuter G., Zhou M.M., Aalen R.B., Thorstensen T. The SUVR4 histone lysine methyltransferase binds ubiquitin and converts H3K9me1 to H3K9me3 on transposon chromatin in Arabidopsis. PLoS Genet. 2011;7(3):e1001325. doi 10.1371/journal.pgen.1001325

24. Wang J., Zhang Z. GAPIT version 3: boosting power and accuracy for genomic association and prediction. Genom Proteom Bioinform. 2021;19(4):629-640. doi 10.1016/j.gpb.2021.08.005

25. Xu T., Lee K., Gu L., Kim J.I., Kang H. Functional characterization of a plastid-specific ribosomal protein PSRP2 in Arabidopsis thaliana under abiotic stress conditions. Plant Physiol Biochem. 2013; 73:405-411. doi 10.1016/j.plaphy.2013.10.027

26. Yanofsky M.F., Ma H., Bowman J.L., Drews G.N., Feldmann K.A., Meyerowitz E.M. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature. 1990;346(6279):35-39. doi 10.1038/346035a0

27. You F., Cloutier S. Mapping quantitative trait loci onto chromosomescale pseudomolecules in flax. Methods Protoc. 2020;3(2):28. doi 10.3390/mps3020028

28. Yu G. Using ggtree to visualize data on tree-like structures. Curr Protoc

29. Bioinform. 2020;69(1):e96. doi 10.1002/cpbi.96

30. Yu T., Huang X., Dou S., Tang X., Luo S., Theurkauf W.E., Lu J., Weng Z. A benchmark and an algorithm for detecting germline transposon insertions and measuring de novo transposon insertion frequencies. Nucleic Acids Res. 2021;49(8):e44. doi 10.1093/nar/gkab010


Review

Views: 30

JATS XML


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 2500-3259 (Online)