Chromosome-level genome assembly of Indian mangrove (Ceriops tagal) revealed a genome-wide duplication event predating the divergence of Rhizophoraceae mangrove species.


Journal

The plant genome
ISSN: 1940-3372
Titre abrégé: Plant Genome
Pays: United States
ID NLM: 101273919

Informations de publication

Date de publication:
09 2022
Historique:
received: 20 01 2022
accepted: 30 03 2022
pubmed: 25 5 2022
medline: 20 9 2022
entrez: 24 5 2022
Statut: ppublish

Résumé

Mangrove ecosystems are unique, highly diverse, provide benefits to humans, and aid in coastal protection. The Indian mangrove, or spurred mangrove, [Ceriops tagal (Perr.) C. B. Rob.] is a member of the Rhizophoraceae family and is commonly found along the intertidal zones in tropical regions in Southeast Asia, southern Asia, and Africa. Here, we present the first high-quality reference genome assembly of the Ceriops species. A preliminary draft assembly, generated from the 10× Genomics linked-read library, was scaffolded using the proximity ligation chromatin contact mapping technique (Hi-C) to obtain a chromosome-scale assembly of 231,919,005 bases with an N50 length of 11,408,429 bases. The benchmarking universal single-copy orthologs (BUSCO) analysis revealed that C. tagal gene predictions recovered 95.8% of the highly conserved orthologs. Phylogenetic analyses suggested that C. tagal diverged from the last common ancestor of flat-leaf spurred mangrove [C. decandra (Griff.) Ding Hou] and C. zippeliana Blume ∼10.4 million yr ago (MYA), and the last common ancestor of genera Ceriops, Kandelia, and Rhizophora diverged from that of genus Bruguiera ∼49.4 MYA. In addition, our analysis of the transversion rate at fourfold-degenerate sites from orthologous gene pairs provided evidence supporting a recent whole-genome duplication in C. tagal. The STRUCTURE and principal component analyses illustrated that C. tagal individuals investigated in this study were the admixture of two subpopulations, the genetic background of which was influenced primarily by location. The availability of genomic and transcriptomic resources and biodiversity data reported in this work will be useful for future studies that may shed light on adaptive evolutions of mangrove species.

Identifiants

pubmed: 35608212
doi: 10.1002/tpg2.20217
doi:

Substances chimiques

Chromatin 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

e20217

Informations de copyright

© 2022 The Authors. The Plant Genome published by Wiley Periodicals LLC on behalf of Crop Science Society of America.

Références

Ball, M. C. (1988). Ecophysiology of mangroves. Trees, 2, 129-142. https://doi.org/10.1007/BF00196018
Botstein, D., White, R. L., Skolnick, M., & Davis, R. W. (1980). Construction of a genetic linkage map in man using restriction fragment length polymorphisms. American Journal of Human Genetics, 32, 314-331.
Bradbury, P. J., Zhang, Z., Kroon, D. E., Casstevens, T. M., Ramdoss, Y., & Buckler, E. S. (2007). TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics, 23, 2633-2635. https://doi.org/10.1093/bioinformatics/btm308
Capella-Gutierrez, S., Silla-Martinez, J. M., & Gabaldon, T. (2009). trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics, 25, 1972-1973. https://doi.org/10.1093/bioinformatics/btp348
Chan, A. P., Crabtree, J., Zhao, Q., Lorenzi, H., Orvis, J., Puiu, D., Melake-Berhan, A., Jones, K. M., Redman, J., Chen, G., Cahoon, E. B., Gedil, M., Stanke, M., Haas, , B. J., Wortman, J. R., Fraser-Liggett, C. M., Ravel, J., & Rabinowicz, P. D. (2010). Draft genome sequence of the oilseed species Ricinus communis. Nature Biotechnology, 28, 951-956. https://doi.org/10.1038/nbt.1674
Chen, Y., Yang, Y., Li, J., Jin, Y., Liu, Q., & Zhang, Y. (2019). The complete chloroplast genome sequence of a medicinal mangrove tree Ceriops tagal and its phylogenetic analysis. Mitochondrial DNA Part B, 4, 267-268. https://doi.org/10.1080/23802359.2018.1541714
Darriba, D., Posada, D., Kozlov, A. M., Stamatakis, A., Morel, B., & Flouri, T. (2020). ModelTest-NG: A new and scalable tool for the selection of DNA and protein evolutionary models. Molecular Biology and Evolution, 37, 291-294. https://doi.org/10.1093/molbev/msz189
Davis, C. C., Webb, C. O., Wurdack, K. J., Jaramillo, C. A., & Donoghue, M. J. (2005). Explosive radiation of Malpighiales supports a mid-cretaceous origin of modern tropical rain forests. The American Naturalist, 165, E36-E65. https://doi.org/10.1086/428296
Dolezel, J. (2005). Plant DNA flow cytometry and estimation of nuclear genome size. Annals of Botany, 95, 99-110. https://doi.org/10.1093/aob/mci005
Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792-1797. https://doi.org/10.1093/nar/gkh340
Falush, D., Stephens, M., & Pritchard, J. K. (2003). Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics, 164, 1567-1587. https://doi.org/10.1093/genetics/164.4.1567
Feng, X., Li, G., Xu, S., Wu, W., Chen, Q., Shao, S., Liu, M., Wang, N., Zhong, C., He, Z., & Shi, S. (2021). Genomic insights into molecular adaptation to intertidal environments in the mangrove Aegiceras corniculatum. New Phytologist, 231, 2346-2358. https://doi.org/10.1111/nph.17551
Friis, G., Vizueta, J., Smith, , E. G., Nelson, D. R., Khraiwesh, B., Qudeimat, E., Salehi-Ashtiani, K., Ortega, A., Marshell, A., Duarte, C. M., & Burt, J. A. (2021). A high-quality genome assembly and annotation of the gray mangrove, Avicennia marina. G3 Genes|Genomes|Genetics, 11, jkaa025. https://doi.org/10.1093/g3journal/jkaa025
Ge, X.-J., & Sun, M. (2001). Population genetic structure of Ceriops tagal (Rhizophoraceae) in Thailand and China. Wetlands Ecology and Management, 9, 213-219. https://doi.org/10.1023/A:1011156707160
Giri, C., Ochieng, E., Tieszen, L. L., Zhu, Z., Singh, A., Loveland, T., Masek, J., & Duke, N. (2011). Status and distribution of mangrove forests of the world using earth observation satellite data. Global Ecology and Biogeography, 20, 154-159. https://doi.org/10.1111/j.1466-8238.2010.00584.x
Graham, A. (2006). Paleobotanical evidence and molecular data in reconstructing the historical phytogeography of Rhizophoraceae. Annals of the Missouri Botanical Garden, 93, 325-334. https://doi.org/10.3417/0026-6493(2006)93%5b325:PEAMDI%5d2.0.CO;2
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, R7. https://doi.org/10.1186/gb-2008-9-1-r7
He, Z., Xu, S., Zhang, Z., Guo, W., Lyu, H., Zhong, C., Boufford, D. E., Duke, N. C., & Shi, S. (2020). Convergent adaptation of the genomes of woody plants at the land-sea interface. National Science Review, 7, 978-993. https://doi.org/10.1093/nsr/nwaa027
Hoff, K. J., Lange, S., Lomsadze, A., Borodovsky, M., & Stanke, M. (2016). BRAKER1: Unsupervised RNA-seq-based genome annotation with GeneMark-ET and AUGUSTUS. Bioinformatics, 32, 767-769. https://doi.org/10.1093/bioinformatics/btv661
Hoff, K. J., Lomsadze, A., Borodovsky, M., & Stanke, M. (2019). Whole-genome annotation with BRAKER. In M. Kollmar (Ed.), Gene prediction. Methods in molecular biology(Vol. 1962, pp. 65-95). Humana. https://doi.org/10.1007/978-1-4939-9173-0_5
Hu, M.-J., Sun, W.-H., Tsai, W.-C., Xiang, S., Lai, X.-K., Chen, D.-Q., Liu, X.-D., Wang, Y.-F., Le, Y.-X., Chen, S.-M., Zhang, D.-Y., Yu, X., Hu, W.-Q., Zhou, Z., Chen, Y.-Q., Zou, S.-Q., & Liu, Z.-J. (2020). Chromosome-scale assembly of the Kandelia obovata genome. Horticulture Research, 7, 75. https://doi.org/10.1038/s41438-020-0300-x
Huang, X., Adams, M. D., Zhou, H., & Kerlavage, A. R. (1997). A tool for analyzing and annotating genomic sequences. Genomics, 46, 37-45. https://doi.org/10.1006/geno.1997.4984
Kim, D., Paggi, J. M., Park, C., Bennett, C., & Salzberg, S. L. (2019). Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nature Biotechnology, 37, 907-915. https://doi.org/10.1038/s41587-019-0201-4
Kriventseva, E. V., Tegenfeldt, F., Petty, T. J., Waterhouse, R. M., Simão, F. A., Pozdnyakov, I. A., Ioannidis, P., & Zdobnov, E. M. (2015). OrthoDB v8: Update of the hierarchical catalog of orthologs and the underlying free software. Nucleic Acids Res., 43, D250-256. https://doi.org/10.1093/nar/gku1220
Liu, K., & Muse, S. V. (2005). PowerMarker: An integrated analysis environment for genetic marker analysis. Bioinformatics, 21, 2128-2129. https://doi.org/10.1093/bioinformatics/bti282
Loureiro, J., Rodriguez, E., Dolezel, J., & Santos, C. (2007). Two new nuclear isolation buffers for plant DNA flow cytometry: A test with 37 species. Annals of Botany, 100, 875-888. https://doi.org/10.1093/aob/mcm152
Lyu, H., He, Z., Wu, C.-I., & Shi, S. (2018). Convergent adaptive evolution in marginal environments: Unloading transposable elements as a common strategy among mangrove genomes. New Phytologist, 217, 428-438. https://doi.org/10.1111/nph.14784
Ma, D., Guo, Z., Ding, Q., Zhao, Z., Shen, Z., Wei, M., Gao, C., Zhang, L., Li, H., Zhang, S., Li, J., Zhu, X., & Zheng, H.-L. (2021). Chromosome-level assembly of the mangrove plant Aegiceras corniculatum genome generated through Illumina, PacBio and Hi-C sequencing technologies. Molecular Ecology Resources, 21, 1593-1607. https://doi.org/10.1111/1755-0998.13347
Miryeganeh, M., Marlétaz, F., Gavriouchkina, D., & Saze, H. (2022). De novo genome assembly and in natura epigenomics reveal salinity-induced DNA methylation in the mangrove tree Bruguiera gymnorhiza. New Phytologist, 233, 2094-2110. https://doi.org/10.1111/nph.17738
Muller, J. (1981). Fossil pollen records of extant angiosperms. The Botanical Review, 47, 1. https://doi.org/10.1007/BF02860537
Natarajan, P., Murugesan, A. K., Govindan, G., Gopalakrishnan, A., Kumar, R., Duraisamy, P., Balaji, R., Tanuja Shyamli, P. S., Parida, A. K., & Parani, M. (2021). A reference-grade genome identifies salt-tolerance genes from the salt-secreting mangrove species Avicennia marina. Communications Biology, 4, 851. https://doi.org/10.1038/s42003-021-02384-8
Nyanga, C. (2020). The role of mangroves forests in decarbonizing the atmosphere. In Bartoli, M., Frediani, M., & Rosi, L. (Eds.), Carbon-based material for environmental protection and remediation. IntechOpen. https://doi.org/10.5772/intechopen.92249
Paradis, E., Claude, J., & Strimmer, K. (2004). APE: Analyses of phylogenetics and evolution in R language. Bioinformatics, 20, 289-290. https://doi.org/10.1093/bioinformatics/btg412
Parida, A. K., & Jha, B. (2010). Salt tolerance mechanisms in mangroves: A review. Trees, 24, 199-217. https://doi.org/10.1007/s00468-010-0417-x
Paul, S., Bag, S. K., Das, S., Harvill, E. T., & Dutta, C. (2008). Molecular signature of hypersaline adaptation: Insights from genome and proteome composition of halophilic prokaryotes. Genome Biology, 9, R70. https://doi.org/10.1186/gb-2008-9-4-r70
Pootakham, W., Naktang, C., Sonthirod, C., Kongkachana, W., Yoocha, T., Jomchai, N., Maknual, C., Chumriang, P., Pravinvongvuthi, T., & Tangphatsornruang, S. (2022a). De novo reference assembly of the upriver orange mangrove (Bruguiera sexangula) genome. Genome Biology and Evolution, 14, evac025. https://doi.org/10.1093/gbe/evac025
Pootakham, W., Nawae, W., Naktang, C., Sonthirod, C., Yoocha, T., Kongkachana, W., Sangsrakru, D., Jomchai, N., U-Thoomporn, S., Somta, P., Laosatit, K., & Tangphatsornruang, S. (2021a). A chromosome-scale assembly of the black gram (Vigna mungo) genome. Molecular Ecology Resources, 21, 238-250. https://doi.org/10.1111/1755-0998.13243
Pootakham, W., Sonthirod, C., Naktang, C., Kongkachana, W., Sangsrakru, D., U-thoomporn, S., Maknual, C., Meepol, W., Promchoo, W., Maprasop, P., Phormsin, N., & Tangphatsornruang, S. (2022b). A chromosome-scale reference genome assembly of yellow mangrove (Bruguiera parviflora) reveals a whole genome duplication event associated with the Rhizophoraceae lineage. Molecular Ecology Resources, https://doi.org/10.1111/1755-0998.13587
Pootakham, W., Sonthirod, C., Naktang, C., Kongkachana, W., U-Thoomporn, S., Phetchawang, P., Maknual, C., Jiumjamrassil, D., Pravinvongvuthi, T., & Tangphatsornruang, S. (2022c). A de novo reference assembly of the yellow mangrove Ceriops zippeliana genome. G3 Genes|Genomes|Genetics, 12, jkac025. https://doi.org/10.1093/g3journal/jkac025
Pootakham, W., Sonthirod, C., Naktang, C., Nawae, W., Yoocha, T., Kongkachana, W., Sangsrakru, D., Jomchai, N., U-Thoomporn, S., Sheedy, J. R., Buaboocha, J., Mekiyanon, S., & Tangphatsornruang, S. (2021b). De novo assemblies of Luffa acutangula and Luffa cylindrica genomes reveal an expansion associated with substantial accumulation of transposable elements. Molecular Ecology Resources, 21, 212-225. https://doi.org/10.1111/1755-0998.13240
Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945-959. https://doi.org/10.1093/genetics/155.2.945
Putnam, N. H., O'Connell, B. L., Stites, J. C., Rice, B. J., Blanchette, M., Calef, R., Troll, C. J., Fields, A., Hartley, P. D., Sugnet, C. W., Haussler, D., Rokhsar, D. S., & Green, R. E. (2016). Chromosome-scale shotgun assembly using an in vitro method for long-range linkage. Genome Research, 26, 342-350. https://doi.org/10.1101/gr.193474.115
R Core Team (2016). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
Rothschild, L. J., & Mancinelli, R. L. (2001). Life in extreme environments. Nature, 409, 1092-1101. https://doi.org/10.1038/35059215
Ruang-Areerate, P., Yoocha, T., Kongkachana, W., Phetchawang, P., Maknual, C., Meepol, W., Jiumjamrassil, D., Pootakham, W., & Tangphatsornruang, S. (2022). Comparative analysis and phylogenetic relationships of Ceriops Species (Rhizophoraceae) and Avicennia lanata (Acanthaceae): Insight into the chloroplast genome evolution between middle and seaward zones of mangrove forests. Biology, 11, 383. https://doi.org/10.3390/biology11030383
Shearman, J. R., Naktang, C., Sonthirod, C., Kongkachana, W., U-thoomporn, S., Jomchai, N., Maknual, C., Yamprasai, S., Promchoo, W., Ruang-areerate, P., Pootakham, W., & Tangphatsornruang, S. (2022). Assembly of a hybrid mangrove, Bruguiera hainesii, and its two ancestral contributors, Bruguiera cylindrica and Bruguiera gymnorhiza. Genomics, https://doi.org/10.1016/j.ygeno.2022.110382
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. https://doi.org/10.1093/bioinformatics/btv351
Stamatakis, A. (2006). RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688-2690. https://doi.org/10.1093/bioinformatics/btl446
Stanke, M., Steinkamp, R., Waack, S., & Morgenstern, B. (2004). AUGUSTUS: A web server for gene finding in eukaryotes. Nucleic Acids Research, 32, W309-W312. https://doi.org/10.1093/nar/gkh379
Tomlinson, P. B. (2016). The botany of mangroves (2nd ed.). Cambridge University Press.
Tuskan, G. A., Difazio, S., Jansson, S., Bohlmann, J., Grigoriev, I., Hellsten, U., Putnam, N., Ralph, S., Rombauts, S., Salamov, A., Schein, J., Sterck, L., Aerts, A., Bhalerao, R. R., Bhalerao, R. P., Blaudez, D., Boerjan, W., Brun, A., Brunner, A., … Rokhsar, D. (2006). The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science, 313, 1596-1604. https://doi.org/10.1126/science.1128691
Villanueva, R. A. M., & Chen, Z. J. (2019). ggplot2: Elegant Graphics for Data Analysis (2nd ed.). Measurement: Interdisciplinary Research and Perspectives, 17, 160-167. https://doi.org/10.1080/15366367.2019.1565254
Vurture, G. W., Sedlazeck, F. J., Nattestad, M., Underwood, C. J., Fang, H., Gurtowski, J., & Schatz, M. C. (2017). GenomeScope: Fast reference-free genome profiling from short reads. Bioinformatics, 33, 2202-2204. https://doi.org/10.1093/bioinformatics/btx153
Wu, T. D., & Watanabe, C. K. (2005). GMAP: A genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics, 21, 1859-1875. https://doi.org/10.1093/bioinformatics/bti310
Xi, Z., Ruhfel, B. R., Schaefer, H., Amorim, A. M., Sugumaran, M., Wurdack, K. J., Endress, P. K., Matthews, M. L., Stevens, P. F., Mathews, S., & Davis, C. C. (2012). Phylogenomics and a posteriori data partitioning resolve the Cretaceous angiosperm radiation Malpighiales. Proceedings of the National Academy of Sciences, 109, 17519-17524. https://doi.org/10.1073/pnas.1205818109
Xu, S., He, Z., Zhang, Z., Guo, Z., Guo, W., Lyu, H., Li, J., Yang, M., Du, Z., Huang, Y., Zhou, R., Zhong, C., Boufford, D. E., Lerdau, M., Wu, C.-I., Duke, N. C., & Shi, S. (2017). The origin, diversification and adaptation of a major mangrove clade (Rhizophoreae) revealed by whole-genome sequencing. National Science Review, 4, 721-734. https://doi.org/10.1093/nsr/nwx065
Yamanaka, T., Miyama, M., & Tada, Y. (2009). Transcriptome profiling of the mangrove plant Bruguiera gymnorhiza and identification of salt tolerance genes by Agrobacterium functional screening. Biotechnology, and Biochemistry, 73, 304-310. https://doi.org/10.1271/bbb.80513
Yang, Z. (2007). PAML 4: Phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24, 1586-1591. https://doi.org/10.1093/molbev/msm088

Auteurs

Wirulda Pootakham (W)

National Omics Center, National Science and Technology Development Agency (NSTDA), Pathum Thani, Thailand.

Chaiwat Naktang (C)

National Omics Center, National Science and Technology Development Agency (NSTDA), Pathum Thani, Thailand.

Chutima Sonthirod (C)

National Omics Center, National Science and Technology Development Agency (NSTDA), Pathum Thani, Thailand.

Wasitthee Kongkachana (W)

National Omics Center, National Science and Technology Development Agency (NSTDA), Pathum Thani, Thailand.

Nattapol Narong (N)

National Omics Center, National Science and Technology Development Agency (NSTDA), Pathum Thani, Thailand.

Duangjai Sangsrakru (D)

National Omics Center, National Science and Technology Development Agency (NSTDA), Pathum Thani, Thailand.

Chatree Maknual (C)

Dep. of Marine and Coastal Resources, 120 The Government Complex, Chaengwatthana Rd., Thung Song Hong, Bangkok, 10210, Thailand.

Darunee Jiumjamrassil (D)

Dep. of Marine and Coastal Resources, 120 The Government Complex, Chaengwatthana Rd., Thung Song Hong, Bangkok, 10210, Thailand.

Pranom Chumriang (P)

Dep. of Marine and Coastal Resources, 120 The Government Complex, Chaengwatthana Rd., Thung Song Hong, Bangkok, 10210, Thailand.

Sithichoke Tangphatsornruang (S)

National Omics Center, National Science and Technology Development Agency (NSTDA), Pathum Thani, Thailand.

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