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The meso-octoploid Heliophila variabilis genome sheds a new light on the impact of polyploidization and diploidization on the diversity of the Cape flora

. 2023 Oct ; 116 (2) : 446-466. [epub] 20230726

Language English Country Great Britain, England Media print-electronic

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

Although the South African Cape flora is one of the most remarkable biodiversity hotspots, its high diversity has not been associated with polyploidy. Here, we report the chromosome-scale genome assembly of an ephemeral cruciferous species Heliophila variabilis (~334 Mb, n = 11) adapted to South African semiarid biomes. Two pairs of differently fractionated subgenomes suggest an allo-octoploid origin of the genome at least 12 million years ago. The ancestral octoploid Heliophila genome (2n = 8x = ~60) has probably originated through hybridization between two allotetraploids (2n = 4x = ~30) formed by distant, intertribal, hybridization. Rediploidization of the ancestral genome was marked by extensive reorganization of parental subgenomes, genome downsizing, and speciation events in the genus Heliophila. We found evidence for loss-of-function changes in genes associated with leaf development and early flowering, and over-retention and sub/neofunctionalization of genes involved in pathogen response and chemical defense. The genomic resources of H. variabilis will help elucidate the role of polyploidization and genome diploidization in plant adaptation to hot arid environments and origin of the Cape flora. The sequenced H. variabilis represents the first chromosome-scale genome assembly of a meso-octoploid representative of the mustard family.

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Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology, 215, 403-410.

Arabidopsis Genome Initiative. (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796-815.

Bailey, T.L. & Elkan, C. (1994) Fitting a mixture model by expectation maximization to discover motifs in bipolymers. Proceedings - International Conference on Intelligent Systems for Molecular Biology, 2, 28-36.

Bennetzen, J.L. (2002) Mechanisms and rates of genome expansion and contraction in flowering plants. Genetica, 115, 29-36.

Birchler, J.A. & Veitia, R.A. (2012) Gene balance hypothesis: connecting issues of dosage sensitivity across biological disciplines. Proceedings of the National Academy of Sciences, 109, 14746-14753.

Birchler, J.A. & Yang, H. (2022) The multiple fates of gene duplications: deletion, hypofunctionalization, subfunctionalization, neofunctionalization, dosage balance constraints, and neutral variation. The Plant Cell, 34, 2466-2474.

Boratyn, G.M., Camacho, C., Cooper, P.S., Coulouris, G., Fong, A., Ma, N. et al. (2013) BLAST: a more efficient report with usability improvements. Nucleic Acids Research, 41, W29-W33.

Burns, R., Mandáková, T., Gunis, J., Soto-Jiménez, L.M., Liu, C., Lysak, M.A. et al. (2021) Gradual evolution of allopolyploidy in Arabidopsis suecica. Nature Ecology & Evolution, 5, 1367-1381.

Calle García, J., Guadagno, A., Paytuvi-Gallart, A., Saera-Vila, A., Amoroso, C.G., D'Esposito, D. et al. (2022) PRGdb 4.0: an updated database dedicated to genes involved in plant disease resistance process. Nucleic Acids Research, 50, D1483-D1490.

Capella-Gutiérrez, S., Silla-Martínez, J.M. & Gabaldón, T. (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics, 25, 1972-1973.

Chalhoub, B., Denoeud, F., Liu, S., Parkin, I.A., Tang, H., Wang, X. et al. (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science, 345, 950-953.

Chang, J., Duong, T.A., Schoeman, C., Ma, X., Roodt, D., Barker, N. et al. (2023) The genome of the king protea, Protea cynaroides. The Plant Journal, 113, 262-276.

Cheng, F., Wu, J., Cai, X., Liang, J., Freeling, M. & Wang, X. (2018) Gene retention, fractionation and subgenome differences in polyploid plants. Nature Plants, 4, 258-268.

Cheng, F., Wu, J., Fang, L. & Wang, X. (2012) Syntenic gene analysis between Brassica rapa and other Brassicaceae species. Frontiers in Plant Science, 3, 198.

Clark, J.W. & Donoghue, P.C. (2017) Constraining the timing of whole genome duplication in plant evolutionary history. Proceedings of the Royal Society B: Biological Sciences, 284, 20170912.

De Beer, A. & Vivier, M.A. (2011) Four plant defensins from an indigenous South African Brassicaceae species display divergent activities against two test pathogens despite high sequence similarity in the encoding genes. BMC Research Notes, 4, 1-19.

Deamer, D., Akeson, M. & Branton, D. (2016) Three decades of nanopore sequencing. Nature Biotechnology, 34, 518-524.

Debernardi, J.M., Mecchia, M.A., Vercruyssen, L., Smaczniak, C., Kaufmann, K., Inze, D. et al. (2014) Post-transcriptional control of GRF transcription factors by microRNA miR396 and GIF co-activator affects leaf size and longevity. The Plant Journal, 79, 413-426.

Derelle, R., Philippe, H. & Colbourne, J.K. (2020) Broccoli: combining phylogenetic and network analyses for orthology assignment. Molecular Biology and Evolution, 37, 3389-3396.

Devos, K.M., Brown, J.K. & Bennetzen, J.L. (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Research, 12, 1075-1079.

Dogan, M., Pouch, M., Mandáková, T., Hloušková, P., Guo, X., Winter, P. et al. (2021) Evolution of tandem repeats is mirroring post-polyploid cladogenesis in Heliophila (Brassicaceae). Frontiers in Plant Science, 11, 607893.

Doležel, J., Greilhuber, J. & Suda, J. (2007) Estimation of nuclear DNA content in plants using flow cytometry. Nature Protocols, 2, 2233-2244.

Dudchenko, O., Batra, S.S., Omer, A.D., Nyquist, S.K., Hoeger, M., Durand, N.C. et al. (2017) De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science, 356, 92-95.

Durand, N.C., Shamim, M.S., Machol, I., Rao, S.S., Huntley, M.H., Lander, E.S. et al. (2016) Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Systems, 3, 95-98.

Edger, P.P., Poorten, T.J., VanBuren, R., Hardigan, M.A., Colle, M., McKain, M.R. et al. (2019) Origin and evolution of the octoploid strawberry genome. Nature Genetics, 51, 541-547.

Feschotte, C., Jiang, N. & Wessler, S.R. (2002) Plant transposable elements: where genetics meets genomics. Nature Reviews Genetics, 3, 329-341.

Garsmeur, O., Schnable, J.C., Almeida, A., Jourda, C., D'Hont, A. & Freeling, M. (2014) Two evolutionarily distinct classes of paleopolyploidy. Molecular Biology and Evolution, 31, 448-454.

Geiser, C., Mandáková, T., Arrigo, N., Lysak, M.A. & Parisod, C. (2016) Repeated whole-genome duplication, karyotype reshuffling, and biased retention of stress-responding genes in buckler mustard. The Plant Cell, 28, 17-27.

Goldblatt, P. & Manning, J.C. (2002) Plant diversity of the Cape region of southern Africa. Annals of the Missouri Botanical Garden, 89, 281-302.

Gonzalez, N., Vanhaeren, H. & Inzé, D. (2012) Leaf size control: complex coordination of cell division and expansion. Trends in Plant Science, 17, 332-340.

Gordon, S.P., Levy, J.J. & Vogel, J.P. (2019) Polycracker, a robust method for the unsupervised partitioning of polyploid subgenomes by signatures of repetitive DNA evolution. BMC Genomics, 20, 1-14.

Grover, C.E. & Wendel, J.F. (2010) Recent insights into mechanisms of genome size change in plants. Journal of Botany, 2010, 1-8.

Guo, X., Mandáková, T., Trachtová, K., Özüdoğru, B., Liu, J. & Lysak, M.A. (2021) Linked by ancestral bonds: multiple whole-genome duplications and reticulate evolution in a Brassicaceae tribe. Molecular Biology and Evolution, 38, 1695-1714.

Haas, B.J., Delcher, A.L., Mount, S.M., Wortman, J.R., Smith, R.K., Jr., Hannick, L.I. et al. (2003) Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Research, 31, 5654-5666.

Haas, B.J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P.D., Bowden, J. et al. (2013) De novo transcript sequence reconstruction from RNA-seq using the trinity platform for reference generation and analysis. Nature Protocols, 8, 1494-1512.

Haas, B.J., Salzberg, S.L., Zhu, W., Pertea, M., Allen, J.E., Orvis, J. et al. (2008) Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biology, 9, 1-22.

Hao, Y., Mabry, M.E., Edger, P.P., Freeling, M., Zheng, C., Jin, L. et al. (2021) The contributions from the progenitor genomes of the mesopolyploid Brassiceae are evolutionarily distinct but functionally compatible. Genome Research, 31, 799-810.

Hendriks, K.P., Kiefer, C., Al-Shehbaz, I.A., Bailey, C.D., Hooft Van Huysduynen, A., Nikolov, L.A. et al. (2022) Global phylogeny of the Brassicaceae provides important insights into gene discordance. bioRxiv 2022-09. https://doi.org/10.1101/2022.09.01.506188

Hoang, D.T., Chernomor, O., Von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2018) UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35, 518-522.

Hofstatter, P.G., Thangavel, G., Lux, T., Neumann, P., Vondrak, T., Novak, P. et al. (2022) Repeat-based holocentromeres influence genome architecture and karyotype evolution. Cell, 185, 3153-3168.

Hohmann, N., Wolf, E.M., Lysak, M.A. & Koch, M.A. (2015) A time-calibrated road map of Brassicaceae species radiation and evolutionary history. The Plant Cell, 27, 2770-2784.

Hopper, S.D., Silveira, F.A. & Fiedler, P.L. (2016) Biodiversity hotspots and Ocbil theory. Plant and Soil, 403, 167-216.

Horiguchi, G., Kim, G.T. & Tsukaya, H. (2005) The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. The Plant Journal, 43, 68-78.

Hu, B., Jin, J., Guo, A.Y., Zhang, H., Luo, J. & Gao, G. (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics, 31, 1296-1297.

Hu, Q., Ma, Y., Mandáková, T., Shi, S., Chen, C., Sun, P. et al. (2021) Genome evolution of the psammophyte Pugionium for desert adaptation and further speciation. Proceedings of the National Academy of Sciences, 118, e2025711118.

Huang, X. & Dixit, V.M. (2016) Drugging the undruggables: exploring the ubiquitin system for drug development. Cell Research, 26, 484-498.

International Wheat Genome Sequencing Consortium (IWGSC), Appels, R., Eversole, K., Stein, N., Feuillet, C., Keller, B. et al. (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science, 361, eaar7191.

Jaillon, O., Aury, J., Noel, B., Policriti, A., Clepet, C., Casagrande, A. et al. (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature, 449, 463-467.

Jiao, Y., Wickett, N.J., Ayyampalayam, S., Chanderbali, A.S., Landherr, L., Ralph, P.E. et al. (2011) Ancestral polyploidy in seed plants and angiosperms. Nature, 473, 97-100.

Kagale, S., Robinson, S.J., Nixon, J., Xiao, R., Huebert, T., Condie, J. et al. (2014) Polyploid evolution of the Brassicaceae during the Cenozoic era. The Plant Cell, 26, 2777-2791.

Kamal, N., Tsardakas Renhuldt, N., Bentzer, J., Gundlach, H., Haberer, G., Juhász, A. et al. (2022) The mosaic oat genome gives insights into a uniquely healthy cereal crop. Nature, 606, 113-119.

Katoh, K., Misawa, K., Kuma, K.I. & Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30, 3059-3066.

Kidwell, M.G. (2002) Transposable elements and the evolution of genome size in eukaryotes. Genetica, 115, 49-63.

Kim, D., Langmead, B. & Salzberg, S.L. (2015) HISAT: a fast spliced aligner with low memory requirements. Nature Methods, 12, 357-360.

Kim, J.H., Choi, D. & Kende, H. (2003) The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. The Plant Journal, 36, 94-104.

Kim, J.H. & Lee, B.H. (2006) GROWTH-REGULATING FACTOR4 of Arabidopsis thaliana is required for development of leaves, cotyledons, and shoot apical meristem. Journal of Plant Biology, 49, 463-468.

Li, H. & Durbin, R. (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754-1760.

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

Li, Z., Defoort, J., Tasdighian, S., Maere, S., Van de Peer, Y. & De Smet, R. (2016) Gene duplicability of core genes is highly consistent across all angiosperms. The Plant Cell, 28, 326-344.

Liao, Y., Smyth, G.K. & Shi, W. (2014) FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics, 30, 923-930.

Lieberman-Aiden, E., Van Berkum, N.L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A. et al. (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science, 326, 289-293.

Lomsadze, A., Burns, P.D. & Borodovsky, M. (2014) Integration of mapped RNA-Seq reads into automatic training of eukaryotic gene finding algorithm. Nucleic Acids Research, 42, e119.

Lysak, M.A., Cheung, K., Kitschke, M. & Bures, P. (2007) Ancestral chromosomal blocks are triplicated in Brassiceae species with varying chromosome number and genome size. Plant Physiology, 145, 402-410.

Lysak, M.A., Koch, M.A., Beaulieu, J.M., Meister, A. & Leitch, I.J. (2009) The dynamic ups and downs of genome size evolution in Brassicaceae. Molecular Biology and Evolution, 26, 85-98.

Lysak, M.A., Mandáková, T. & Schranz, M.E. (2016) Comparative paleogenomics of crucifers: ancestral genomic blocks revisited. Current Opinion in Plant Biology, 30, 108-115.

Mandáková, T., Li, Z., Barker, M.S. & Lysak, M.A. (2017) Diverse genome organization following 13 independent mesopolyploid events in Brassicaceae contrasts with convergent patterns of gene retention. The Plant Journal, 91(1), 3-21.

Mandáková, T. & Lysak, M.A. (2008) Chromosomal phylogeny and karyotype evolution in x= 7 crucifer species (Brassicaceae). The Plant Cell, 20, 2559-2570.

Mandáková, T. & Lysak, M.A. (2018) Post-polyploid diploidization and diversification through dysploid changes. Current Opinion in Plant Biology, 42, 55-65.

Mandáková, T., Mummenhoff, K., Al-Shehbaz, I.A., Mucina, L., Mühlhausen, A. & Lysak, M.A. (2012) Wholegenome triplication and species radiation in the southern African tribe Heliophileae (Brassicaceae). Taxon, 61, 989-1000.

Marçais, G. & Kingsford, C. (2011) A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics, 27, 764-770.

Marchler-Bauer, A. & Bryant, S.H. (2004) CD-search: protein domain annotations on the fly. Nucleic Acids Research, 32, W327-W331.

Marchler-Bauer, A., Lu, S., Anderson, J.B., Chitsaz, F., Derbyshire, M.K., DeWeese-Scott, C. et al. (2010) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Research, 39, D225-D229.

McWhite, C.D., Papoulas, O., Drew, K., Cox, R.M., June, V., Dong, O.X. et al. (2020) A pan-plant protein complex map reveals deep conservation and novel assemblies. Cell, 181, 460-474.

Mittermeier, R.A., Myers, N., Thomsen, J.B., Da Fonseca, G.A. & Olivieri, S. (1998) Biodiversity hotspots and major tropical wilderness areas: approaches to setting conservation priorities. Conservation Biology, 12, 516-520.

Mummenhoff, K., Al-Shehbaz, I.A., Bakker, F.T., Linder, H.P. & Mühlhausen, A. (2005) Phylogeny, morphological evolution, and speciation of endemic Brassicaceae genera in the Cape flora of southern Africa. Annals of the Missouri Botanical Garden, 92, 400-424.

Myers, N., Mittermeier, R.A., Mittermeier, C.G., Da Fonseca, G.A. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853-858.

Nguyen, L.T., Schmidt, H.A., Von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32, 268-274.

Nikolov, L.A., Shushkov, P., Nevado, B., Gan, X., Al-Shehbaz, I.A., Filatov, D. et al. (2019) Resolving the backbone of the Brassicaceae phylogeny for investigating trait diversity. New Phytologist, 222, 1638-1651.

Oberlander, K.C., Dreyer, L.L., Goldblatt, P., Suda, J. & Linder, H.P. (2016) Species-rich and polyploid-poor: insights into the evolutionary role of whole-genome duplication from the Cape flora biodiversity hotspot. American Journal of Botany, 103, 1336-1347.

Papp, B., Pal, C. & Hurst, L.D. (2003) Dosage sensitivity and the evolution of gene families in yeast. Nature, 424, 194-197.

Peppe, D.J., Cote, S.M., Deino, A.L., Fox, D.L., Kingston, J.D., Kinyanjui, R.N. et al. (2023) Oldest evidence of abundant C4 grasses and habitat heterogeneity in eastern Africa. Science, 380, 173-177.

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, 290-295.

Pompidor, N., Charron, C., Hervouet, C., Bocs, S., Droc, G., Rivallan, R. et al. (2021) Three founding ancestral genomes involved in the origin of sugarcane. Annals of Botany, 127, 827-840.

Qiao, X., Zhang, S. & Paterson, A.H. (2022) Pervasive genome duplications across the plant tree of life and their links to major evolutionary innovations and transitions. Computational and Structural Biotechnology Journal, 20, 3248-3256.

Robertson, F.M., Gundappa, M.K., Grammes, F., Hvidsten, T.R., Redmond, A.K., Lien, S. et al. (2017) Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification. Genome Biology, 18, 1-14.

Robinson, J.T., Turner, D., Durand, N.C., Thorvaldsdóttir, H., Mesirov, J.P. & Aiden, E.L. (2018) Juicebox. js provides a cloud-based visualization system for Hi-C data. Cell Systems, 6, 256-258.

Schaaper, W., Posthuma, G., Meloen, R., Plasman, H., Sijtsma, L., Van Amerongen, A. et al. (2001) Synthetic peptides derived from the β2−β3 loop of Raphanus sativus antifungal protein 2 that mimic the active site. The Journal of Peptide Research, 57, 409-418.

Schranz, M.E., Lysak, M.A. & Mitchell-Olds, T. (2006) The ABC's of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends in Plant Science, 11, 535-542.

Schranz, M.E., Mohammadin, S. & Edger, P.P. (2012) Ancient whole genome duplications, novelty and diversification: the WGD radiation lag-time model. Current Opinion in Plant Biology, 15, 147-153.

Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D. et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Research, 13, 2498-2504.

Shavrukov, Y., Kurishbayev, A., Jatayev, S., Shvidchenko, V., Zotova, L., Koekemoer, F. et al. (2017) Early flowering as a drought escape mechanism in plants: how can it aid wheat production? Frontiers in Plant Science, 8, 1950.

Simão, F.A., Waterhouse, R.M., Ioannidis, P., Kriventseva, E.V. & Zdobnov, E.M. (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics, 31, 3210-3212.

Stanke, M., Tzvetkova, A. & Morgenstern, B. (2006) AUGUSTUS at EGASP: using EST, protein and genomic alignments for improved gene prediction in the human genome. Genome Biology, 7, 1-8.

Stefanik, N., Bizan, J., Wilkens, A., Tarnawska-Glatt, K., Goto-Yamada, S., Strzałka, K. et al. (2020) NAI2 and TSA1 drive differentiation of constitutive and inducible ER body formation in Brassicaceae. Plant and Cell Physiology, 61, 722-734.

Sun, H., Wu, S., Zhang, G., Jiao, C., Guo, S., Ren, Y. et al. (2017) Karyotype stability and unbiased fractionation in the paleo-allotetraploid Cucurbita genomes. Molecular Plant, 10, 1293-1306.

Tang, H., Woodhouse, M.R., Cheng, F., Schnable, J.C., Pedersen, B.S., Conant, G. et al. (2012) Altered patterns of fractionation and exon deletions in Brassica rapa support a two-step model of paleohexaploidy. Genetics, 190, 1563-1574.

Van de Peer, Y., Ashman, T.L., Soltis, P.S. & Soltis, D.E. (2021) Polyploidy: an evolutionary and ecological force in stressful times. The Plant Cell, 33, 11-26.

Van de Peer, Y., Mizrachi, E. & Marchal, K. (2017) The evolutionary significance of polyploidy. Nature Reviews Genetics, 18, 411-424.

Van Rooyen, M., Grobbelaar, N., Theron, G. & Van Rooyen, N. (1992) The ephemerals of Namaqualand: effect of germination date on development of three species. Journal of Arid Environments, 22, 51-66.

Van Santen, M. & Linder, H.P. (2020) The assembly of the Cape flora is consistent with an edaphic rather than climatic filter. Molecular Phylogenetics and Evolution, 142, 106645.

Vekemans, D., Proost, S., Vanneste, K., Coenen, H., Viaene, T., Ruelens, P. et al. (2012) Gamma paleohexaploidy in the stem lineage of core eudicots: significance for MADS-box gene and species diversification. Molecular Biology and Evolution, 29, 3793-3806.

Verboom, G.A., Archibald, J.K., Bakker, F.T., Bellstedt, D.U., Conrad, F., Dreyer, L.L. et al. (2009) Origin and diversification of the greater Cape flora: ancient species repository, hot-bed of recent radiation, or both? Molecular Phylogenetics and Evolution, 51, 44-53.

Walden, N., German, D.A., Wolf, E.M., Kiefer, M., Rigault, P., Huang, X.C. et al. (2020) Nested whole-genome duplications coincide with diversification and high morphological disparity in Brassicaceae. Nature Communications, 11, 3795.

Walker, B.J., 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.

Wang, D., Zhang, Y., Zhang, Z., Zhu, J. & Yu, J. (2010) KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics, Proteomics & Bioinformatics, 8, 77-80.

Wang, X., Wang, H., Wang, J., Sun, R., Wu, J., Liu, S. et al. (2011) The genome of the mesopolyploid crop species Brassica rapa. Nature Genetics, 43, 1035-1039.

Weiller, F., Moore, J.P., Young, P., Driouich, A. & Vivier, M.A. (2017) The Brassicaceae species Heliophila coronopifolia produces root border-like cells that protect the root tip and secrete defensin peptides. Annals of Botany, 119, 803-813.

Yu, G., Wang, L.G., Han, Y. & He, Q.Y. (2012) ClusterProfiler: an R package for comparing biological themes among gene clusters. Omics: A Journal of Integrative Biology, 16, 284-287.

Zhang, C., Scornavacca, C., Molloy, E.K. & Mirarab, S. (2020) ASTRAL-Pro: quartet-based species-tree inference despite paralogy. Molecular Biology and Evolution, 37, 3292-3307.

Zhang, J., Zhang, X., Tang, H., Zhang, Q., Hua, X., Ma, X. et al. (2018) Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Nature Genetics, 50, 1565-1573.

Zhang, X., Zhang, S., Zhao, Q., Ming, R. & Tang, H. (2019) Assembly of allele-aware, chromosomal-scale autopolyploid genomes based on Hi-C data. Nature Plants, 5, 833-845.

Zhang, Y., Zhang, L., Xiao, Q., Wu, C., Zhang, J., Xu, Q. et al. (2022) Two independent allohexaploidizations and genomic fractionation in Solanales. Frontiers in Plant Science, 13, 1001402.

Zhang, Z., Xiao, J., Wu, J., Zhang, H., Liu, G., Wang, X. et al. (2012) ParaAT: a parallel tool for constructing multiple protein-coding DNA alignments. Biochemical and Biophysical Research Communications, 419, 779-781.

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