The chromosome-level genome sequence and karyotypic evolution of Megadenia pygmaea (Brassicaceae).

Brassicaceae Qinghai-Tibet Plateau descending dysploidy genome assembly karyotype and chromosome evolution

Journal

Molecular ecology resources
ISSN: 1755-0998
Titre abrégé: Mol Ecol Resour
Pays: England
ID NLM: 101465604

Informations de publication

Date de publication:
Apr 2021
Historique:
received: 28 06 2020
revised: 23 10 2020
accepted: 30 10 2020
pubmed: 6 11 2020
medline: 18 8 2021
entrez: 5 11 2020
Statut: ppublish

Résumé

Karyotypic changes in chromosome number and structure are drivers in the divergent evolution of diverse plant species and lineages. This study aimed to reveal the origins of the unique karyotype (2n = 12) and phylogenetic relationships of the genus Megadenia (Brassicaceae). A high-quality chromosome-scale genome was assembled for Megadenia pygmaea using Nanopore long reads and high-throughput chromosome conformation capture (Hi-C). The assembled genome is 215.2 Mb and is anchored on six pseudochromosomes. We annotated a total of 25,607 high-confidence protein-coding genes and corroborated the phylogenetic affinity of Megadenia with the Brassicaceae expanded lineage II, containing numerous agricultural crops. We dated the divergence of Megadenia from its closest relatives to 27.04 (19.11-36.60) million years ago. A reconstruction of the chromosomal composition of the species was performed based on the de novo assembled genome and comparative chromosome painting analysis. The karyotype structure of M. pygmaea is very similar to the previously inferred proto-Calepineae karyotype (PCK; n = 7) of the lineage II. However, an end-to-end translocation between two ancestral chromosomes reduced the chromosome number from n = 7 to n = 6 in Megadenia. Our reference genome provides fundamental information for karyotypic evolution and evolutionary study of this genus.

Identifiants

pubmed: 33151630
doi: 10.1111/1755-0998.13291
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

871-879

Subventions

Organisme : National Natural Science Foundation of China
ID : 41771055
Organisme : National Natural Science Foundation of China
ID : 31700323
Organisme : National Key Research and Development program
ID : 2017YFC0505203
Organisme : Central European Institute of Technology (CEITEC) 2020 project
ID : LQ1601

Informations de copyright

© 2020 John Wiley & Sons Ltd.

Références

Arnegard, M. E., McGee, M. D., Matthews, B., Marchinko, K. B., Conte, G. L., Kabir, S. M.,Bedford, N., Bergek, S., Frank Chan, Y., Jones, F. C., Kingsley, D. M., Peichel, C. L., & Schluter, D. (2014). Genetics of ecological divergence during speciation. Nature, 511(7509), 307-311.
Artyukova, E. V., Kozyrenko, M. M., Boltenkov, E. V., & Gorovoy, P. G. (2014). One or three species in Megadenia (Brassicaceae): Insight from molecular studies. Genetica, 142(4), 337-350. https://doi.org/10.1007/s10709-014-9778-1
Bairoch, A., & Apweiler, R. (2000). The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Research, 28(1), 45-48. https://doi.org/10.1093/nar/28.1.45
Beilstein, M. A., Al-Shehbaz, I. A., Mathews, S., & Kellogg, E. A. (2008). Brassicaceae phylogeny inferred from phytochrome A and ndhF sequence data: Tribes and trichomes revisited. American Journal of Botany, 95(10), 1307-1327.
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
Cheng, F., Wu, J., & Wang, X. (2014). Genome triplication drove the diversification of Brassica plants. Horticulture Research, 1(1), 1-8. https://doi.org/10.1038/hortres.2014.24
Conesa, A., Götz, S., García-Gómez, J. M., Terol, J., Talón, M., & Robles, M. (2005). Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21(18), 3674-3676. https://doi.org/10.1093/bioinformatics/bti610
De Bie, T., Cristianini, N., Demuth, J. P., & Hahn, M. W. (2006). CAFE: A computational tool for the study of gene family evolution. Bioinformatics, 22(10), 1269-1271. https://doi.org/10.1093/bioinformatics/btl097
Dorofeyev, V. I. (2004). System of family Cruciferae B. Juss.(Brassicaceae Burnett). Turczaninowia, 7(3), 43-52.
Dudchenko, O., Batra, S. S., Omer, A. D., Nyquist, S. K., Hoeger, M., Durand, N. C., & Aiden, A. P. (2017). De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science, 356(6333), 92-95.
Dudchenko, O., Shamim, M. S., Batra, S., Durand, N. C., Musial, N. T., Mostofa, R., Stamenova, E. (2018). The Juicebox Assembly Tools module facilitates de novo assembly of mammalian genomes with chromosome-length scaffolds for under $1000. Biorxiv, 254797.
Durand, N. C., Robinson, J. T., Shamim, M. S., Machol, I., Mesirov, J. P., Lander, E. S., & Aiden, E. L. (2016). Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Systems, 3(1), 99-101. https://doi.org/10.1016/j.cels.2015.07.012
Durand, N. C., Shamim, M. S., Machol, I., Rao, S. S. P., Huntley, M. H., Lander, E. S., & Aiden, E. L. (2016). Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Systems, 3(1), 95-98. https://doi.org/10.1016/j.cels.2016.07.002
Ellinghaus, D., Kurtz, S., & Willhoeft, U. (2008). LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics, 9(1), 18. https://doi.org/10.1186/1471-2105-9-18
Emms, D. M. (2018). STAG: Species Tree Inference from All Genes. BioRxiv, 267914.
Emms, D. M., & Kelly, S. (2019). OrthoFinder: Phylogenetic orthology inference for comparative genomics. Genome Biology, 20(1). https://doi.org/10.1186/s13059-019-1832-y
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(1), 17-27. https://doi.org/10.1105/tpc.15.00791
German, D. A., & Al-Shehbaz, I. A. (2008). Five additional tribes (Aphragmeae, Biscutelleae, Calepineae, Conringieae, and Erysimeae) in the Brassicaceae (Cruciferae). Harvard Papers in Botany, 13(1), 165-170. https://doi.org/10.3100/1043-4534(2008)13[165:FATABC]2.0.CO;2
Guo, X., Liu, J., Hao, G., Zhang, L., Mao, K., Wang, X., Zhang, D., Ma, T., Hu, Q., Al-Shehbaz, I. A., & Koch, M. A. (2017). Plastome phylogeny and early diversification of Brassicaceae. BMC Genomics, 18(1), 176. https://doi.org/10.1186/s12864-017-3555-3
Haas, B. J., Delcher, A. L., Mount, S. M., Wortman, J. R., Smith, R. K. Jr, Hannick, L. I., & Town, C. D. (2003). Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Research, 31(19), 5654-5666. https://doi.org/10.1093/nar/gkg770
Haas, B. J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P. D., Bowden, J., Couger, M. B., Eccles, D., Li, B. O., Lieber, M., MacManes, M. D., Ott, M., Orvis, J., Pochet, N., Strozzi, F., Weeks, N., Westerman, R., William, T., Dewey, C. N., … Regev, A. (2013). De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocols, 8(8), 1494. https://doi.org/10.1038/nprot.2013.084
Haas, B. J., Salzberg, S. L., Zhu, W., Pertea, M., Allen, J. E., Orvis, J., White, O., Buell, C. R., & Wortman, J. R. (2008). Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biology, 9(1), R7. https://doi.org/10.1186/gb-2008-9-1-r7
Hedges, S. B., Dudley, J., & Kumar, S. (2006). TimeTree: A public knowledge-base of divergence times among organisms. Bioinformatics, 22(23), 2971-2972. https://doi.org/10.1093/bioinformatics/btl505
Huang, C.-H., Sun, R., Hu, Y. I., Zeng, L., Zhang, N., Cai, L., Zhang, Q., Koch, M. A., Al-Shehbaz, I., Edger, P. P., Pires, J. C., Tan, D.-Y., Zhong, Y., & Ma, H. (2016). Resolution of brassicaceae phylogeny using nuclear genes uncovers nested radiations and supports convergent morphological evolution. Molecular Biology and Evolution, 33(2), 394-412. https://doi.org/10.1093/molbev/msv226
Kanehisa, M., Goto, S., Sato, Y., Furumichi, M., & Tanabe, M. (2012). KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Research, 40(D1), D109-D114. https://doi.org/10.1093/nar/gkr988
Kang, M., Wu, H., Yang, Q., Huang, L. I., Hu, Q., Ma, T., Li, Z., & Liu, J. (2020). A chromosome-scale genome assembly of Isatis indigotica, an important medicinal plant used in traditional Chinese medicine. Horticulture Research, 7(1), 1-10. https://doi.org/10.1038/s41438-020-0240-5
Kang, Y. J., Kim, S. K., Kim, M. Y., Lestari, P., Kim, K. H., Ha, B.-K., Jun, T. H., Hwang, W. J., Lee, T., Lee, J., Shim, S., Yoon, M. Y., Jang, Y. E., Han, K. S., Taeprayoon, P., Yoon, N. A., Somta, P., Tanya, P., Kim, K. S., … Lee, S.-H. (2014). Genome sequence of mungbean and insights into evolution within Vigna species. Nature Communications, 5, 5443. https://doi.org/10.1038/ncomms6443
Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772-780. https://doi.org/10.1093/molbev/mst010
Kiefer, M., Schmickl, R., German, D. A., Mandáková, T., Lysak, M. A., Al-Shehbaz, I. A., Franzke, A., Mummenhoff, K., Stamatakis, A., & Koch, M. A. (2014). BrassiBase: Introduction to a novel knowledge database on Brassicaceae evolution. Plant and Cell Physiology, 55(1), e3. https://doi.org/10.1093/pcp/pct158
Koren, S., Walenz, B. P., Berlin, K., Miller, J. R., Bergman, N. H., & Phillippy, A. M. (2017). Canu: Scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Research, 27(5), 722-736.
Lv, H., Fang, Z., Yang, L., Zhang, Y., & Wang, Y. (2020). An update on the arsenal: Mining resistance genes for disease management of Brassica crops in the genomic era. Horticulture Research, 7(1), 1-18.
Lysak, M. A. (2014). Live and let die: Centromere loss during evolution of plant chromosomes. New Phytologist, 203(4), 1082-1089.
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.
Majoros, W. H., Pertea, M., & Salzberg, S. L. (2004). TigrScan and GlimmerHMM: Two open source ab initio eukaryotic gene-finders. Bioinformatics, 20(16), 2878-2879.
Mandáková, T., Guo, X., Özüdoğru, B., Mummenhoff, K., & Lysak, M. A. (2018). Hybridization-facilitated genome merger and repeated chromosome fusion after 8 million years. Plant Journal, 96(4), 748-760.
Mandáková, T., & Lysak, M. A. (2008). Chromosomal phylogeny and karyotype evolution in x= 7 crucifer species (Brassicaceae). The Plant Cell, 20(10), 2559-2570.
Mandáková, T., & Lysak, M. A. (2016a). Painting of Arabidopsis chromosomes with chromosome-specific BAC clones. Current Protocols in Plant Biology, 1(2), 359-371.
Mandáková, T., & Lysak, M. A. (2016b). Chromosome preparation for cytogenetic analyses in Arabidopsis. Current Protocols in Plant BiologyPlant Biology, 1(1), 43-51.
Mandáková, T., & Lysak, M. A. (2018). Post-polyploid diploidization and diversification through dysploid changes. Current Opinion in Plant Biology, 42, 55-65.
Marçais, G., & Kingsford, C. (2011). A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics, 27(6), 764-770.
Nikolov, L. A., Shushkov, P., Nevado, B., Gan, X., Al-Shehbaz, I. A., Filatov, D., Bailey, C. D., & Tsiantis, M. (2019). Resolving the backbone of the Brassicaceae phylogeny for investigating trait diversity. New Phytologist, 222(3), 1638-1651. https://doi.org/10.1111/nph.15732
Ossowski, S., Schneeberger, K., Lucas-Lledó, J. I., Warthmann, N., Clark, R. M., Shaw, R. G., & Lynch, M. (2010). The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science, 327(5961), 92-94.
Ou, S., & Jiang, N. (2018). LTR_retriever: A highly accurate and sensitive program for identification of long terminal repeat retrotransposons. Plant Physiology, 176(2), 1410-1422. https://doi.org/10.1104/pp.17.01310
Price, M. N., Dehal, P. S., & Arkin, A. P. (2010). FastTree 2 - Approximately maximum-likelihood trees for large alignments. PLoS One, 5(3). https://doi.org/10.1371/journal.pone.0009490
Price, A. L., Jones, N. C., & Pevzner, P. A. (2005). De novo identification of repeat families in large genomes. Bioinformatics, 21, i351-i358.
Ranallo-Benavidez, T. R., Jaron, K. S., & Schatz, M. C. (2020). GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nature Communications, 11(1), 1-10.
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(11), 535-542. https://doi.org/10.1016/j.tplants.2006.09.002
Slater, G. S. C., & Birney, E. (2005). Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics, 6.
Stanke, M., Steinkamp, R., Waack, S., & Morgenstern, B. (2004). AUGUSTUS: A web server for gene finding in eukaryotes. Nucleic Acids Research, 32(suppl_2), W309-W312. https://doi.org/10.1093/nar/gkh379
Stebbins, G. L. (1971). Chromosomal evolution in higher plants. Edward Arnold Ltd.
Sun, H., Ding, J., Piednoël, M., & Schneeberger, K. (2018). findGSE: Estimating genome size variation within human and Arabidopsis using k-mer frequencies. Bioinformatics, 34(4), 550-557. https://doi.org/10.1093/bioinformatics/btx637
Tarailo-Graovac, M., & Chen, N. (2009). Using RepeatMasker to identify repetitive elements in genomic sequences. Current Protocols in Bioinformatics, 25(1), 4-10. https://doi.org/10.1002/0471250953.bi0410s25
van Berkum, N. L., Lieberman-Aiden, E., Williams, L., Imakaev, M., Gnirke, A., Mirny, L. A., Dekker, J., & Lander, E. S. (2010). Hi-C: A method to study the three-dimensional architecture of genomes. Journal of Visualized Experiments, 39, 1-7. https://doi.org/10.3791/1869
Walker, B. J., Abeel, T., Shea, T., Priest, M., Abouelliel, A., Sakthikumar, S., Cuomo, C. A., Zeng, Q., Wortman, J., Young, S. K., & Earl, A. M. (2014). Pilon: An integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One, 9(11). https://doi.org/10.1371/journal.pone.0112963
Wang, Y., Tang, H., DeBarry, J. D., Tan, X., Li, J., Wang, X., Lee, T.-H., Jin, H., Marler, B., Guo, H., Kissinger, J. C., & Paterson, A. H. (2012). MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Research, 40(7), e49. https://doi.org/10.1093/nar/gkr1293
Xu, Z., & Wang, H. (2007). LTR_FINDER: An efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Research, 35(suppl_2), W265-W268. https://doi.org/10.1093/nar/gkm286
Zdobnov, E. M., & Apweiler, R. (2001). InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics, 17(9), 847-848. https://doi.org/10.1093/bioinformatics/17.9.847
Zhang, L., Cai, X. U., Wu, J., Liu, M., Grob, S., Cheng, F., Liang, J., Cai, C., Liu, Z., Liu, B. O., Wang, F., Li, S., Liu, F., Li, X., Cheng, L., Yang, W., Li, M.-H., Grossniklaus, U., Zheng, H., & Wang, X. (2018). Improved Brassica rapa reference genome by single-molecule sequencing and chromosome conformation capture technologies. Horticulture Research, 5(1), 1-11. https://doi.org/10.1038/s41438-018-0071-9
Zhou, T. Y. (2001). Brassicaceae. Flora of China, 8, 1-193.

Auteurs

Wenjie Yang (W)

Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.

Lei Zhang (L)

Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.

Terezie Mandáková (T)

Central European Institute of Technology (CEITEC), Masaryk University, Brno, Czech Republic.

Li Huang (L)

Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.

Ting Li (T)

Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.

Jiebei Jiang (J)

Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.

Yongzhi Yang (Y)

State Key Laboratory of Grassland AgroEcosystem, Institute of Innovation Ecology, Lanzhou University, Lanzhou, China.

Martin A Lysak (MA)

Central European Institute of Technology (CEITEC), Masaryk University, Brno, Czech Republic.

Jianquan Liu (J)

Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.
State Key Laboratory of Grassland AgroEcosystem, Institute of Innovation Ecology, Lanzhou University, Lanzhou, China.

Quanjun Hu (Q)

Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.

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