Evolutionary roles of polyploidization-derived structural variations in the phenotypic diversification of Panax species.

Panax diploidization phenotypic novelty polyploidization structural variation triterpenoid saponin

Journal

Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478

Informations de publication

Date de publication:
09 2023
Historique:
revised: 10 07 2023
received: 01 02 2023
accepted: 19 07 2023
medline: 6 9 2023
pubmed: 1 8 2023
entrez: 1 8 2023
Statut: ppublish

Résumé

Genomic structural variations (SVs) are widespread in plant and animal genomes and play important roles in phenotypic novelty and species adaptation. Frequent whole genome duplications followed by (re)diploidizations have resulted in high diversity of genome architecture among extant species. In this study, we identified abundant genomic SVs in the Panax genus that are hypothesized to have occurred through during the repeated polyploidizations/(re)diploidizations. Our genome-wide comparisons demonstrated that although these polyploidization-derived SVs have evolved at distinct evolutionary stages, a large number of SV-intersecting genes showed enrichment in functionally important pathways related to secondary metabolites, photosynthesis and basic cellular activities. In line with these observations, our metabolic analyses of these Panax species revealed high diversity of primary and secondary metabolites both at the tissue and interspecific levels. In particular, genomic SVs identified at ginsenoside biosynthesis genes, including copy number variation and large fragment deletion, appear to have played important roles in the evolution and diversification of ginsenosides. A further herbivore deterrence experiment demonstrated that, as major triterpenoidal saponins found exclusively in Panax, ginsenosides provide protection against insect herbivores. Our study provides new insights on how polyploidization-derived SVs have contributed to phenotypic novelty and plant adaptation.

Identifiants

pubmed: 37525516
doi: 10.1111/mec.17088
doi:

Substances chimiques

Ginsenosides 0
Saponins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4999-5012

Informations de copyright

© 2023 John Wiley & Sons Ltd.

Références

Ahmad, M., Ghaffar, A., & Rafiq, M. (2013). Host plants of leaf worm, Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) in Pakistan. Asian Journal of Agriculture and Biology, 1, 23-28.
Almarri, M. A., Bergstrom, A., Prado-Martinez, J., Yang, F., Fu, B., Dunham, A. S., & Xue, Y. (2020). Population structure, stratification, and introgression of human structural variation. Cell, 182(1), 189-199. https://doi.org/10.1016/j.cell.2020.05.024
Alonge, M., Wang, X., Benoit, M., Soyk, S., Pereira, L., Zhang, L., & Lippman, Z. B. (2020). Major impacts of widespread structural variation on gene expression and crop improvement in tomato. Cell, 182(1), 145-161.e123. https://doi.org/10.1016/j.cell.2020.05.021
Altschul, S., Gish, W., Miller, W., Myers, E., & Lipman, D. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(2), 403-410. https://doi.org/10.1016/s0022-2836(05)80360-2
Anderson, J. E., Kantar, M. B., Kono, T. Y., Fu, F., Stec, A. O., Song, Q., & Stupar, R. M. (2014). A roadmap for functional structural variants in the soybean genome. G3 (Bethesda), 4(7), 1307-1318. https://doi.org/10.1534/g3.114.011551
Armstrong, J., Hickey, G., Diekhans, M., Fiddes, I. T., Novak, A. M., Deran, A., & Paten, B. (2020). Progressive cactus is a multiple-genome aligner for the thousand-genome era. Nature, 587(7833), 246-251. https://doi.org/10.1038/s41586-020-2871-y
Baker, M. (2012). Structural variation: The genome's hidden architecture. Nature Methods, 9(2), 133-137. https://doi.org/10.1038/nmeth.1858
Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic - A flexible trimmer for Illumina sequence data. Bioinformatics, 30(15), 2114-2120. https://doi.org/10.1093/bioinformatics/btu170
Cai, X., Chang, L., Zhang, T., Chen, H., Zhang, L., Lin, R., & Wang, X. (2021). Impacts of allopolyploidization and structural variation on intraspecific diversification in Brassica rapa. Genome Biology, 22(1), 166. https://doi.org/10.1186/s13059-021-02383-2
Cai, Y., Cai, X., Wang, Q., Wang, P., Zhang, Y., Cai, C., & Liu, F. (2020). Genome sequencing of the Australian wild diploid species Gossypium australe highlights disease resistance and delayed gland morphogenesis. Plant Biotechnology Journal, 18(3), 814-828. https://doi.org/10.1111/pbi.13249
Campy, W. H., & Tax, S. (1960). Evolution after Darwin. Aibs Bulletin, 10(5), 42.
Carroll, S. B. (2008). Evo-devo and an expanding evolutionary synthesis: A genetic theory of morphological evolution. Cell, 134(1), 25-36. https://doi.org/10.1016/j.cell.2008.06.030
Chawla, H. S., Lee, H., Gabur, I., Vollrath, P., Tamilselvan-Nattar-Amutha, S., Obermeier, C., & Snowdon, R. J. (2021). Long-read sequencing reveals widespread intragenic structural variants in a recent allopolyploid crop plant. Plant Biotechnology Journal, 19(2), 240-250. https://doi.org/10.1111/pbi.13456
Chen, H., & Boutros, P. C. (2011). VennDiagram: A package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinformatics, 12, 35.
Chen, W., Balan, P., & Popovich, D. G. (2020a). Comparison of ginsenoside components of various tissues of New Zealand forest-grown Asian ginseng (Panax ginseng) and American ginseng (Panax quinquefolium L.). Biomolecules, 10(3), 1-17. https://doi.org/10.3390/biom10030372
Chen, W., Balan, P., & Popovich, D. G. (2020b). Ginsenosides analysis of New Zealand-grown forest Panax ginseng by LC-QTOF-MS/MS. Journal of Ginseng Research, 44(4), 552-562. https://doi.org/10.1016/j.jgr.2019.04.007
De Coster, W., D'Hert, S., Schultz, D. T., Cruts, M., & Van Broeckhoven, C. (2018). NanoPack: Visualizing and processing long-read sequencing data. Bioinformatics, 34(15), 2666-2669. https://doi.org/10.1093/bioinformatics/bty149
Du, X., Huang, G., He, S., Yang, Z., Sun, G., Ma, X., & Li, F. (2018). Resequencing of 243 diploid cotton accessions based on an updated a genome identifies the genetic basis of key agronomic traits. Nature Genetics, 50(6), 796-802. https://doi.org/10.1038/s41588-018-0116-x
Ducat, D. C., & Silver, P. A. (2012). Improving carbon fixation pathways. Current Opinion in Chemical Biology, 16(3-4), 337-344. https://doi.org/10.1016/j.cbpa.2012.05.002
Edger, P. P., Heidel-Fischer, H. M., Bekaert, M., Rota, J., Glockner, G., Platts, A. E., & Wheat, C. W. (2015). The butterfly plant arms-race escalated by gene and genome duplications. Proceedings of the National Academy of Sciences of the United States of America, 112(27), 8362-8366. https://doi.org/10.1073/pnas.1503926112
Feng, S., Stiller, J., Deng, Y., Armstrong, J., Fang, Q., Reeve, A. H., & Zhang, G. (2020). Dense sampling of bird diversity increases power of comparative genomics. Nature, 587(7833), 252-257. https://doi.org/10.1038/s41586-020-2873-9
Franceschi, V. R., Krokene, P., Christiansen, E., & Krekling, T. (2005). Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytologist, 167(2), 353-375. https://doi.org/10.1111/j.1469-8137.2005.01436.x
Francis, G., Kerem, Z., Makkar, H. P., & Becker, K. (2002). The biological action of saponins in animal systems: A review. British Journal of Nutrition, 88(6), 587-605. https://doi.org/10.1079/BJN2002725
Fuentes, R. R., Chebotarov, D., Duitama, J., Smith, S., De la Hoz, J. F., Mohiyuddin, M., & Alexandrov, N. (2019). Structural variants in 3000 rice genomes. Genome Research, 29(5), 870-880. https://doi.org/10.1101/gr.241240.118
Hartmann, T. (2007). From waste products to ecochemicals: Fifty years research of plant secondary metabolism. Phytochemistry, 68(22-24), 2831-2846. https://doi.org/10.1016/j.phytochem.2007.09.017
He, Y., Luo, X., Zhou, B., Hu, T., Meng, X., Audano, P. A., & Su, B. (2019). Long-read assembly of the Chinese rhesus macaque genome and identification of ape-specific structural variants. Nature Communications, 10(1), 4233. https://doi.org/10.1038/s41467-019-12174-w
Hegde, M. L., Hazra, T. K., & Mitra, S. (2008). Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells. Cell Research, 18(1), 27-47. https://doi.org/10.1038/cr.2008.8
Hickey, G., Paten, B., Earl, D., Zerbino, D., & Haussler, D. (2013). HAL: A hierarchical format for storing and analyzing multiple genome alignments. Bioinformatics, 29(10), 1341-1342. https://doi.org/10.1093/bioinformatics/btt128
Huang, A. C., Jiang, T., Liu, Y. X., Bai, Y. C., Reed, J., Qu, B., Goossens, A., Nützmann, H. W., Bai, Y., & Osbourn, A. (2019). A specialized metabolic network selectively modulates Arabidopsis root microbiota. Science, 364(6440), eaau6389. https://doi.org/10.1126/science.aau6389
Huang, S. H., Xian, J. D., Kong, S. Z., Li, Y. C., Xie, J. H., Lin, J., & Su, Z. R. (2014). Insecticidal activity of pogostone against Spodoptera litura and Spodoptera exigua (Lepidoptera: Noctuidae). Pest Management Science, 70(3), 510-516. https://doi.org/10.1002/ps.3635
Jiang, Z., Tu, L., Yang, W., Zhang, Y., Hu, T., Ma, B., & Gao, W. (2021). The chromosome-level reference genome assembly for Panax notoginseng and insights into ginsenoside biosynthesis. Plant Communications, 2(1), 100113. https://doi.org/10.1016/j.xplc.2020.100113
Jiao, Y., Wickett, N. J., Ayyampalayam, S., Chanderbali, A. S., Landherr, L., Ralph, P. E., & de Pamphilis, C. W. (2011). Ancestral polyploidy in seed plants and angiosperms. Nature, 473(7345), 97-100. https://doi.org/10.1038/nature09916
Kalisz, S., & Kramer, E. M. (2008). Variation and constraint in plant evolution and development. Heredity (Edinb), 100(2), 171-177. https://doi.org/10.1038/sj.hdy.6800939
Kang, K., Yue, L., Xia, X., Liu, K., & Zhang, W. (2019). Comparative metabolomics analysis of different resistant rice varieties in response to the brown planthopper Nilaparvata lugens Hemiptera: Delphacidae. Metabolomics, 15(4), 62. https://doi.org/10.1007/s11306-019-1523-4
Kim, D., Langmead, B., & Salzberg, S. L. (2015). HISAT: A fast spliced aligner with low memory requirements. Nature Methods, 12(4), 357-360. https://doi.org/10.1038/nmeth.3317
Kim, N. H., Jayakodi, M., Lee, S. C., Choi, B. S., Jang, W., Lee, J., & Yang, T. J. (2018). Genome and evolution of the shade-requiring medicinal herb Panax ginseng. Plant Biotechnology Journal, 16(11), 1904-1917. https://doi.org/10.1111/pbi.12926
Kochan, E., Szymczyk, P., Kuzma, L., Szymanska, G., Wajs-Bonikowska, A., Bonikowski, R., & Sienkiewicz, M. (2018). The increase of triterpene Saponin production induced by trans-Anethole in hairy root cultures of Panax quinquefolium. Molecules, 23(10), 2674. https://doi.org/10.3390/molecules23102674
Kolde, R. (2012). Pheatmap: Pretty heatmaps. R Package Version 1.0.12. https://CRAN.R-project.org/package=heatmap
LaSalle, J. M., Powell, W. T., & Yasui, D. H. (2013). Epigenetic layers and players underlying neurodevelopment. Trends in Neurosciences, 36(8), 460-470. https://doi.org/10.1016/j.tins.2013.05.001
Levis, N. A., & Pfennig, D. W. (2020). Plasticity-led evolution: A survey of developmental mechanisms and empirical tests. Evolution & Development, 22(1-2), 71-87. https://doi.org/10.1111/ede.12309
Li, H. (2018). Minimap2: Pairwise alignment for nucleotide sequences. Bioinformatics, 34(18), 3094-3100. https://doi.org/10.1093/bioinformatics/bty191
Li, M. R., Ding, N., Lu, T., Zhao, J., Wang, Z. H., Jiang, P., & Li, L. F. (2021). Evolutionary contribution of duplicated genes to genome evolution in the ginseng species complex. Genome Biology and Evolution, 13(5), evab051. https://doi.org/10.1093/gbe/evab051
Lilue, J., Doran, A. G., Fiddes, I. T., Abrudan, M., Armstrong, J., Bennett, R., & Keane, T. M. (2018). Sixteen diverse laboratory mouse reference genomes define strain-specific haplotypes and novel functional loci. Nature Genetics, 50(11), 1574-1583. https://doi.org/10.1038/s41588-018-0223-8
Loll-Krippleber, R., & Brown, G. W. (2017). P-body proteins regulate transcriptional rewiring to promote DNA replication stress resistance. Nature Communications, 8(1), 558. https://doi.org/10.1038/s41467-017-00632-2
Love, M. I., Huber, W., & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15(12), 550. https://doi.org/10.1186/s13059-014-0550-8
Ma, X. Q., Liang, X. M., Xu, Q., Zhang, X. Z., & Xiao, H. B. (2005). Identification of ginsenosides in roots of Panax ginseng by HPLC-APCI/MS. Phytochemical Analysis, 16(3), 181-187. https://doi.org/10.1002/pca.842
Ma, Y., Min, L., Wang, M., Wang, C., Zhao, Y., Li, Y., & Zhang, X. (2018). Disrupted genome methylation in response to high temperature has distinct affects on microspore abortion and anther indehiscence. The Plant Cell, 30(7), 1387-1403. https://doi.org/10.1105/tpc.18.00074
Macel, M., Visschers, I. G. S., Peters, J. L., Kappers, I. F., de Vos, R. C. H., & van Dam, N. M. (2019). Metabolomics of thrips resistance in pepper (capsicum spp.) reveals monomer and dimer acyclic diterpene glycosides as potential chemical defenses. Journal of Chemical Ecology, 45(5-6), 490-501. https://doi.org/10.1007/s10886-019-01074-4
Merot, C., Oomen, R. A., Tigano, A., & Wellenreuther, M. (2020). A roadmap for understanding the evolutionary significance of structural genomic variation. Trends in Ecology & Evolution, 35(7), 561-572. https://doi.org/10.1016/j.tree.2020.03.002
Muller, G. B., & Wagner, G. P. (1991). Novelty in evolution: Restructuring the concept. Annual Review of Ecology and Systematics, 22, 229-256.
Murat, F., Armero, A., Pont, C., Klopp, C., & Salse, J. (2017). Reconstructing the genome of the most recent common ancestor of flowering plants. Nature Genetics, 49(4), 490-496. https://doi.org/10.1038/ng.3813
Peng, R., Xu, Y., Tian, S., Unver, T., Liu, Z., Zhou, Z., & Liu, F. (2022). Evolutionary divergence of duplicated genomes in newly described allotetraploid cottons. Proceedings of the National Academy of Sciences of the United States of America, 119(39), e2208496119. https://doi.org/10.1073/pnas.2208496119
Pertea, M., Pertea, G. M., Antonescu, C. M., Chang, T. C., Mendell, J. T., & Salzberg, S. L. (2015). StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature Biotechnology, 33(3), 290-295. https://doi.org/10.1038/nbt.3122
Pespeni, M. H., Oliver, T. A., Manier, M. K., & Palumbi, S. R. (2010). Restriction site tiling analysis: Accurate discovery and quantitative genotyping of genome-wide polymorphisms using nucleotide arrays. Genome Biology, 11(4), R44. https://doi.org/10.1186/gb-2010-11-4-r44
Piao, X., Zhang, H., Kang, J. P., Yang, D. U., Li, Y., Pang, S., Jin, Y., Yang, D. C., & Wang, Y. (2020). Advances in saponin diversity of Panax ginseng. Molecules, 25, 3452. https://doi.org/10.3390/molecules25153452
Puddu, F., Herzog, M., Selivanova, A., Wang, S., Zhu, J., Klein-Lavi, S., & Jackson, S. P. (2019). Genome architecture and stability in the Saccharomyces cerevisiae knockout collection. Nature, 573(7774), 416-420. https://doi.org/10.1038/s41586-019-1549-9
Qin, P., Lu, H., Du, H., Wang, H., Chen, W., Chen, Z., & Li, S. (2021). Pan-genome analysis of 33 genetically diverse rice accessions reveals hidden genomic variations. Cell, 184(13), 3542-3558. https://doi.org/10.1016/j.cell.2021.04.046
R Core Team. (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org/
Robinson, J. T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E. S., Getz, G., & Mesirov, J. P. (2011). Integrative genomics viewer. Nature Biotechnology, 29(1), 24-26. https://doi.org/10.1038/nbt.1754
Saintenac, C., Jiang, D., & Akhunov, E. D. (2011). Targeted analysis of nucleotide and copy number variation by exon capture in allotetraploid wheat genome. Genome Biology, 12(9), R88. https://doi.org/10.1186/gb-2011-12-9-r88
Salmon, M., Thimmappa, R. B., Minto, R. E., Melton, R. E., Hughes, R. K., O'Maille, P. E., & Osbourn, A. (2016). A conserved amino acid residue critical for product and substrate specificity in plant triterpene synthases. Proceedings of the National Academy of Sciences of the United States of America, 113(30), E4407-E4414. https://doi.org/10.1073/pnas.1605509113
Saxena, R. K., Edwards, D., & Varshney, R. K. (2014). Structural variations in plant genomes. Briefings in Functional Genomics, 13(4), 296-307. https://doi.org/10.1093/bfgp/elu016
Sebastian, S., Zachary, L., Sedlazeck, F. J., Jiménez-Gómez, J. M., Alonge, M., Hutton, S. F., Van Eck, J., & Schatz, M. C. (2019). Duplication of a domestication locus neutralized a cryptic variant that caused a breeding barrier in tomato. Nature Plants, 5(5), 471-479. https://doi.org/10.1038/s41477-019-0422-z
Sedlazeck, F. J., Rescheneder, P., Smolka, M., Fang, H., Nattestad, M., von Haeseler, A., & Schatz, M. C. (2018). Accurate detection of complex structural variations using single-molecule sequencing. Nature Methods, 15(6), 461-468. https://doi.org/10.1038/s41592-018-0001-7
Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., & Ideker, T. (2003). Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Research, 13(11), 2498-2504. https://doi.org/10.1101/gr.1239303
Shi, F. X., Li, M. R., Li, Y. L., Jiang, P., Zhang, C., Pan, Y. Z., & Li, L. F. (2015). The impacts of polyploidy, geographic and ecological isolations on the diversification of Panax (Araliaceae). BMC Plant Biology, 15, 297. https://doi.org/10.1186/s12870-015-0669-0
Song, J. M., Guan, Z., Hu, J., Guo, C., Yang, Z., Wang, S., & Guo, L. (2020). Eight high-quality genomes reveal pan-genome architecture and ecotype differentiation of Brassica napus. Nature Plants, 6(1), 34-45. https://doi.org/10.1038/s41477-019-0577-7
Van Dooren, T. J. M., Silveira, A. B., Gilbault, E., Jimenez-Gomez, J. M., Martin, A., Bach, L., & Colot, V. (2020). Mild drought in the vegetative stage induces phenotypic, gene expression, and DNA methylation plasticity in Arabidopsis but no transgenerational effects. Journal of Experimental Botany, 71(12), 3588-3602. https://doi.org/10.1093/jxb/eraa132
Walden, N., German, D. A., Wolf, E. M., Kiefer, M., Rigault, P., Huang, X. C., & Koch, M. A. (2020). Nested whole-genome duplications coincide with diversification and high morphological disparity in Brassicaceae. Nature Communications, 11(1), 3795. https://doi.org/10.1038/s41467-020-17605-7
Wang, Y., Zhang, H., Ri, H. C., An, Z., Wang, X., Zhou, J. N., & Li, Y. (2022). Deletion and tandem duplications of biosynthetic genes drive the diversity of triterpenoids in Aralia elata. Nature Communications, 13(1), 2224. https://doi.org/10.1038/s41467-022-29908-y
Wang, Z. H., Wang, X. F., Lu, T., Li, M. R., Jiang, P., Zhao, J., & Li, L. F. (2022). Reshuffling of the ancestral core-eudicot genome shaped chromatin topology and epigenetic modification in Panax. Nature Communications, 13(1), 1902. https://doi.org/10.1038/s41467-022-29561-5
Wei, G., Yang, F., Wei, F., Zhang, L., Gao, Y., Qian, J., & Chen, S. (2020). Metabolomes and transcriptomes revealed the saponin distribution in root tissues of Panax quinquefolius and Panax notoginseng. Journal of Ginseng Research, 44(6), 757-769. https://doi.org/10.1016/j.jgr.2019.05.009
Weissensteiner, M. H., Bunikis, I., Catalán, A., Francoijs, K.-J., Knief, U., Heim, W., & Wolf, J. B. W. (2020). Discovery and population genomics of structural variation in a songbird genus. Nature Communications, 11(1), 3403. https://doi.org/10.1038/s41467-020-17195-4
Wendel, J. F. (2000). Genome evolution in polyploids. Plant Molecular Biology, 42(1), 225-249.
Wendel, J. F., Jackson, S. A., Meyers, B. C., & Wing, R. A. (2016). Evolution of plant genome architecture. Genome Biology, 17, 37. https://doi.org/10.1186/s13059-016-0908-1
Wick, R. R., Judd, L. M., & Holt, K. E. (2019). Performance of neural network basecalling tools for Oxford Nanopore sequencing. Genome Biology, 20, 129. https://doi.org/10.1186/s13059-019-1727-y
Wickham, H. (2009). Ggplot2: Elegant graphics for data analysis. Springer Nature. https://doi.org/10.1007/978-3-319-24277-4
Yang, W. Y., Zheng, Y., Bahn, S. C., Pan, X. Q., Li, M. Y., Vu, H. S., & Wang, X. M. (2012). The patatin-containing phospholipase a pPLAIIalpha modulates oxylipin formation and water loss in Arabidopsis thaliana. Molecular Plant, 5(2), 452-460. https://doi.org/10.1093/mp/ssr118
Yang, Z., Ge, X., Yang, Z., Qin, W., Sun, G., Wang, Z., & Li, F. (2019). Extensive intraspecific gene order and gene structural variations in upland cotton cultivars. Nature Communications, 10(1), 2989. https://doi.org/10.1038/s41467-019-10820-x
Yang, Z., Liu, G., Zhang, G., Yan, J., Dong, Y., Lu, Y., & Yang, S. (2021). The chromosome-scale high-quality genome assembly of Panax notoginseng provides insight into dencichine biosynthesis. Plant Biotechnology Journal, 19(5), 869-871. https://doi.org/10.1111/pbi.13558
Yin, X., Yang, D., Zhao, Y., Yang, X., Zhou, Z., Sun, X., & Yang, Y. (2022). Differences in pseudogene evolution contributed to the contrasting flavors of turnip and Chiifu, two Brassica rapa subspecies. Plant Communications, 100427, 100427. https://doi.org/10.1016/j.xplc.2022.100427
Yu, X., Xiao, J., Chen, S., Yu, Y., Ma, J., Lin, Y., & Liu, R. (2020). Metabolite signatures of diverse Camellia sinensis tea populations. Nature Communications, 11(1), 5586. https://doi.org/10.1038/s41467-020-19441-1
Yuan, W., Luo, X., Li, Z., Yang, W., Wang, Y., Liu, R., & He, Y. (2016). A cis cold memory element and a trans epigenome reader mediate Polycomb silencing of FLC by vernalization in Arabidopsis. Nature Genetics, 48(12), 1527-1534. https://doi.org/10.1038/ng.3712
Zhang, D., Li, W., Chen, Z. J., Wei, F. G., Liu, Y. L., & Gao, L. Z. (2020). SMRT- and Illumina-based RNA-seq analyses unveil the ginsinoside biosynthesis and transcriptomic complexity in Panax notoginseng. Scientific Reports, 10(1), 15310. https://doi.org/10.1038/s41598-020-72291-1
Zhang, Y., Du, L., Xu, R., Cui, R., Hao, J., Sun, C., & Li, Y. (2015). Transcription factors SOD7/NGAL2 and DPA4/NGAL3 act redundantly to regulate seed size by directly repressing KLU expression in Arabidopsis thaliana. The Plant Cell, 27(3), 620-632. https://doi.org/10.1105/tpc.114.135368
Zhang, Y. X., Niu, Y. Q., Wang, X. F., Wang, Z. H., Wang, M. L., Yang, J., & Li, L. F. (2022). Phenotypic and transcriptomic responses of the shade-grown species Panax ginseng to variable light conditions. Annals of Botany, 130, 749-762. https://doi.org/10.1093/aob/mcac105
Zhong, S., Joung, J. G., Zheng, Y., Chen, Y. R., Liu, B., Shao, Y., Xiang, J. Z., Fei, Z., & Giovannoni, J. J. (2011). High-throughput illumina strand-specific RNA sequencing library preparation. Cold Spring Harbor Protocols, 2011(8), 940-949. https://doi.org/10.1101/pdb.prot5652
Zhou, M., Yang, G., Sun, G., Guo, Z., Gong, X., & Pan, Y. (2020). Resolving complicated relationships of the Panax bipinnatifidus complex in southwestern China by RAD-seq data. Molecular Phylogenetics and Evolution, 149, 106851. https://doi.org/10.1016/j.ympev.2020.106851

Auteurs

Yu-Xin Zhang (YX)

Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Sciences, Fudan University, Shanghai, China.

Xin-Feng Wang (XF)

Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Sciences, Fudan University, Shanghai, China.

Yu-Qian Niu (YQ)

Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Sciences, Fudan University, Shanghai, China.

Yu-Guo Wang (YG)

Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Sciences, Fudan University, Shanghai, China.

Wen-Ju Zhang (WJ)

Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Sciences, Fudan University, Shanghai, China.

Zhi-Ping Song (ZP)

Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Sciences, Fudan University, Shanghai, China.

Ji Yang (J)

Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Sciences, Fudan University, Shanghai, China.

Lin-Feng Li (LF)

Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Sciences, Fudan University, Shanghai, China.

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