Chromosome-scale genome assembly of the autoalloenneaploid Arundo donax

Mengmeng Ren , Fupeng Liu , Xiaohong Han , Daohong Wu , Hai Peng

Grassland Research ›› 2024, Vol. 3 ›› Issue (3) : 230 -242.

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Grassland Research ›› 2024, Vol. 3 ›› Issue (3) : 230 -242. DOI: 10.1002/glr2.12091
RESEARCH ARTICLE

Chromosome-scale genome assembly of the autoalloenneaploid Arundo donax

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Abstract

Background: Arundo donax L. has great potential as an energy crop due to its high biomass yield and broad adaptability, while lack of a reference genome is a hindrance to genetic improvement efforts for this species.

Methods: Genome assembly of A. donax was conducted by utilizing PacBio SMRT sequencing and high-throughput chromosome conformation capture technology, with further analysis exploring the plant’s ploidy, whole-genome duplication event, and evolutionary history through comparative genomics.

Results: The genome assembly of A. donax consists of 1.30 Gb with a contig N50 size of 33.15 Mb. A total of 74 403 gene models were identified, with over 90% of genes being functionally annotated. Karyotype and synteny analyses revealed that A. donax is an autoalloenneaploid (3n = 9x = 108) and has experienced significant gene family expansion and two whole-genome duplication events during its evolutionary history. Furthermore, utilizing the genome assembly, a variety of salinity stress-related genes were uncovered through the analysis of public RNA-seq data.

Conclusions: This study presents the initial chromosome-scale genome assembly of A. donax, which will advance genetic comprehension and support the genetic enhancement of this important energy crop.

Keywords

Arundo donax / autoallopolyploid / comparative genomics / genome assembly

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Mengmeng Ren, Fupeng Liu, Xiaohong Han, Daohong Wu, Hai Peng. Chromosome-scale genome assembly of the autoalloenneaploid Arundo donax. Grassland Research, 2024, 3(3): 230-242 DOI:10.1002/glr2.12091

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References

[1]

Ahmad, R., Liow, P. S., Spencer, D. F., & Jasieniuk, M. (2008). Molecular evidence for a single genetic clone of invasive Arundo donax in the United States. Aquatic Botany, 88(2), 113–120.

[2]

Angelini, L. G., Ceccarini, L., & Bonari, E. (2005). Biomass yield and energy balance of giant reed (Arundo donax L.) cropped in central Italy as related to different management practices. European Journal of Agronomy, 22, 375–389.

[3]

Angelini, L. G., Ceccarini, L., Nasso, N., & Bonari, E. (2009). Comparison of Arundo donax L. and Miscanthus × giganteus in a long-term field experiment in central Italy: Analysis of productive characteristics and energy balance. Biomass & Bioenergy, 33(4), 635–643.

[4]

Bayani, J., & Squire, J. A. (2004). Fluorescence in situ hybridization (FISH). Current Protocols in Cell Biology, 3(1), 22–24.

[5]

Benson, G. (1999). Tandem repeats finder: A program to analyze DNA sequences. Nucleic Acids Research, 27(2), 573–580.

[6]

Bucci, A., Cassani, E., Landoni, M., Cantaluppi, E., & Pilu, R. (2013). Analysis of chromosome number and speculations on the origin of Arundo donax L. (Giant Reed). Cytology and Genetics, 47(4), 237–241.

[7]

Burton, J. N., Adey, A., Patwardhan, R. P., Qiu, R., Kitzman, J. O., & Shendure, J. (2013). Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nature Biotechnology, 31, 1119–1125.

[8]

Chen, C., Wu, Y., Li, J., Wang, X., Zeng, Z., Xu, J., Liu, Y., Feng, J., Chen, H., He, Y., & Xia, R. (2023). TBtools-II: A “one for all, all for one” bioinformatics platform for biological big-data mining. Molecular Plant, 16(11), 1733–1742.

[9]

Chen, H., Zeng, Y., Yang, Y., Huang, L., Tang, B., Zhang, H., Hao, F., Liu, W., Li, Y., Liu, Y., Zhang, X., Zhang, R., Zhang, Y., Li, Y., Wang, K., He, H., Wang, Z., Fan, G., Yang, H., … Qiu, Q. (2020). Allele-aware chromosome-level genome assembly and efficient transgene-free genome editing for the autotetraploid cultivated alfalfa. Nature Communications, 11(1), 2494.

[10]

Chen, N. S. (2004). Using RepeatMasker to identify repetitive elements in genomic sequences. Current Protocols in Bioinformatics, 4, 10.

[11]

Chen, S., Zhou, Y., Chen, Y., & Gu, J. (2018). fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34(17), i884–i890.

[12]

Chen, Z., Debernardi, J. M., Dubcovsky, J., & Gallavotti, A. (2022). Recent advances in crop transformation technologies. Nature Plants, 8(12), 1343–1351.

[13]

Cheng, H., Concepcion, G. T., Feng, X., Zhang, H., & Li, H. (2021). Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nature Methods, 18(2), 170–175.

[14]

Christopher, J., & Abraham, A. (1971). Studies on the cytology and phylogeny of South Indian grasses I. Subfamilies Bambusoideae, Oryzoideae, Arundinoideae and Festucoideae. Cytologia, 36, 579–594.

[15]

Clevering, O. A., & Lissner, J. (2000). Erratum to “Taxonomy, chromosome numbers, clonal diversity and population dynamics of Phragmites australis”. Aquatic Botany, 66, 249–250.

[16]

Corno, L., Pilu, R., & Adani, F. (2014). Arundo donax L.: A non-food crop for bioenergy and bio-compound production. Biotechnology Advances, 32(8), 1535–1549.

[17]

Danecek, P., & McCarthy, S. A. (2017). BCFtools/csq: Haplotype-aware variant consequences. Bioinformatics, 33(13), 2037–2039.

[18]

Danelli, T., Laura, M., Savona, M., Landoni, M., Adani, F., & Pilu, R. (2020). Genetic improvement of Arundo donax L.: Opportunities and challenges. Plants, 9(11), 1584.

[19]

Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013). STAR: Ultrafast universal RNA-seq aligner. Bioinformatics, 29(1), 15–21.

[20]

Ellinghaus, D., Kurtz, S., & Willhoeft, U. (2008). LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics, 9, 18.

[21]

Evangelistella, C., Valentini, A., Ludovisi, R., Firrincieli, A., Fabbrini, F., Scalabrin, S., Cattonaro, F., Morgante, M., Mugnozza, G. S., Keurentjes, J. J. B., & Harfouche, A. (2017). De novo assembly, functional annotation, and analysis of the giant reed (Arundo donax L.) leaf transcriptome provide tools for the development of a biofuel feedstock. Biotechnology for Biofuels, 10(1), 138.

[22]

Fu, Y., Poli, M., Sablok, G., Wang, B., Liang, Y., La Porta, N., Velikova, V., Loreto, F., Li, M., & Varotto, C. (2016). Dissection of early transcriptional responses to water stress in Arundo donax L. by unigene-based RNA-seq. Biotechnology for Biofuels, 9, 54.

[23]

Guan, D., McCarthy, S. A., Wood, J., Howe, K., Wang, Y., & Durbin, R. (2020). Identifying and removing haplotypic duplication in primary genome assemblies. Bioinformatics, 36(9), 2896–2898.

[24]

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.

[25]

Haddadchi, A., Gross, C. L., & Fatemi, M. (2013). The expansion of sterile Arundo donax (Poaceae) in southeastern Australia is accompanied by genotypic variation. Aquatic Botany, 104, 153–161.

[26]

Han, Y., & Wessler, S. R. (2010). MITE-Hunter: A program for discovering miniature inverted-repeat transposable elements from genomic sequences. Nucleic Acids Research, 38, e199.

[27]

Hunter, A. W. S. (1934). A karyosystematic investigation in the Gramineae. Canadian Journal of Research, 11(2), 213–241.

[28]

Jámbor, A., & Török, Á. (2019). The economics of Arundo donax—A systematic literature review. Sustainability, 11, 4225.

[29]

Jia, K. H., Wang, Z. X., Wang, L., Li, G. Y., Zhang, W., Wang, X. L., Xu, F. J., Jiao, S. Q., Zhou, S. S., Liu, H., Ma, Y., Bi, G., Zhao, W., El-Kassaby, Y. A., Porth, I., Li, G., Zhang, R. G., & Mao, J. F. (2022). SubPhaser: A robust allopolyploid subgenome phasing method based on subgenome-specific k-mers. New Phytologist, 235(2), 801–809.

[30]

Jiang, J. (2019). Fluorescence in situ hybridization in plants: Recent developments and future applications. Chromosome Research, 27(3), 153–165.

[31]

Jike, W., Li, M., Zadra, N., Barbaro, E., Sablok, G., Bertorelle, G., Rota-Stabelli, O., & Varotto, C. (2020). Phylogenomic proof of recurrent demipolyploidization and evolutionary stalling of the “Triploid Bridge” in Arundo (Poaceae). International Journal of Molecular Sciences, 21(15), 5247.

[32]

Keilwagen, J., Wenk, M., Erickson, J. L., Schattat, M. H., Grau, J., & Hartung, F. (2016). Using intron position conservation for homology-based gene prediction. Nucleic Acids Research, 44, e89.

[33]

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(8), 907–915.

[34]

Kokot, M., Długosz, M., & Deorowicz, S. (2017). KMC 3: Counting and manipulating k-mer statistics. Bioinformatics, 33(17), 2759–2761.

[35]

Kovaka, S., Zimin, A. V., Pertea, G. M., Razaghi, R., Salzberg, S. L., & Pertea, M. (2019). Transcriptome assembly from long-read RNA-seq alignments with StringTie2. Genome Biology, 20(1), 278.

[36]

Lagesen, K., Hallin, P., Rødland, E. A., Stærfeldt, H. H., Rognes, T., & Ussery, D. W. (2007). RNAmmer: Consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Research, 35(9), 3100–3108.

[37]

Langmead, B., & Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4), 357–359.

[38]

Li, H., & Durbin, R. (2010). Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics, 26(5), 589–595.

[39]

Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., & Durbin, R. (2009). The sequence Alignment/Map format and SAMtools. Bioinformatics, 25(16), 2078–2079.

[40]

Liao, Y., Smyth, G. K., & Shi, W. (2014). featureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics, 30(7), 923–930.

[41]

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.

[42]

Lowe, T. M., & Eddy, S. R. (1997). tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research, 25(5), 955–964.

[43]

Malone, J. M., Virtue, J. G., Williams, C., & Preston, C. (2017). Genetic diversity of giant reed (Arundo donax) in Australia. Weed Biology and Management, 17, 17–28.

[44]

Mariani, C., Cabrini, R., Danin, A., Piffanelli, P., Fricano, A., Gomarasca, S., Dicandilo, M., Grassi, F., & Soave, C. (2010). Origin, diffusion and reproduction of the giant reed (Arundo donax L.): A promising weedy energy crop. Annals of Applied Biology, 157(2), 191–202.

[45]

Mario, S., & Burkhard, M. (2005). AUGUSTUS: A web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Research, 33(Suppl. 2), W465–W467.

[46]

Mirza, N., Mahmood, Q., Pervez, A., Ahmad, R., Farooq, R., Shah, M. M., & Azim, M. R. (2010). Phytoremediation potential of Arundo donax in arsenic-contaminated synthetic wastewater. Bioresource Technology, 101, 5815–5819.

[47]

Mirza, N., Pervez, A., Mahmood, Q., Shah, M. M., & Shafqat, M. N. (2011). Ecological restoration of arsenic contaminated soil by Arundo donax L. Ecological Engineering, 37(12), 1949–1956.

[48]

Murashige, T., & Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiologia Plantarum, 15, 473–497.

[49]

Nackley, L. L., & Kim, S. H. (2015). A salt on the bioenergy and biological invasions debate: Salinity tolerance of the invasive biomass feedstock Arundo donax. Global Change Biology Bioenergy, 7, 752–762.

[50]

Nassi o Di Nasso, N., Roncucci, N., & Bonari, E. (2013). Seasonal dynamics of aboveground and belowground biomass and nutrient accumulation and remobilization in giant reed (Arundo donax L.): A three-year study on marginal land. Bioenergy Research, 6(2), 725–736.

[51]

Nawrocki, E. P., & Eddy, S. R. (2013). Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics, 29(22), 2933–2935.

[52]

Ou, S., Chen, J., & Jiang, N. (2018). Assessing genome assembly quality using the LTR Assembly Index (LAI). Nucleic Acids Research, 46(21), 126.

[53]

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.

[54]

Papazoglou, E. G., Karantounias, G. A., Vemmos, S. N., & Bouranis, D. L. (2005). Photosynthesis and growth responses of giant reed (Arundo donax L.) to the heavy metals Cd and Ni. Environment International, 31(2), 243–249.

[55]

Parra, G., Bradnam, K., & Korf, I. (2007). CEGMA: A pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics, 23(9), 1061–1067.

[56]

Patz, J. A., Frumkin, H., Holloway, T., Vimont, D. J., & Haines, A. (2014). Climate change: Challenges and opportunities for global health. Journal of the American Medical Association, 312(5), 1565–1580.

[57]

Peng, Y., Yan, H., Guo, L., Deng, C., Wang, C., Wang, Y., Kang, L., Zhou, P., Yu, K., Dong, X., Liu, X., Sun, Z., Peng, Y., Zhao, J., Deng, D., Xu, Y., Li, Y., Jiang, Q., Li, Y., … Ren, C. (2022). Reference genome assemblies reveal the origin and evolution of allohexaploid oat. Nature Genetics, 54(8), 1248–1258.

[58]

Pilu, R., Manca, A., & Landoni, M. (2013). Arundo donax as an energy crop: Pros and cons of the utilization of this perennial plant. Maydica, 58(1), 54–59.

[59]

Pizzolongo, P. (1962). Osservazioni cariologichec su Arundo donax e Arundo plinii. Annuali Botany, 27, 173–187.

[60]

Reid, W. V., Ali, M. K., & Field, C. B. (2020). The future of bioenergy. Global Change Biology, 26(1), 274–286.

[61]

Sablok, G., Fu, Y., Bobbio, V., Laura, M., Rotino, G. L., Bagnaresi, P., Allavena, A., Velikova, V., Viola, R., Loreto, F., Li, M., & Varotto, C. (2014). Fuelling genetic and metabolic exploration of C3 bioenergy crops through the first reference transcriptome of Arundo donax L. Plant Biotechnology Journal, 12, 554–567.

[62]

Sánchez, E., Scordia, D., Lino, G., Arias, C., Cosentino, S. L., & Nogués, S. (2015). Salinity and water stress effects on biomass production in different Arundo donax L. clones. Bioenergy Research, 8(4), 1461–1479.

[63]

Servant, N., Varoquaux, N., Lajoie, B. R., Viara, E., Chen, C. J., Vert, J. P., Heard, E., Dekker, J., & Barillot, E. (2015). HiC-Pro: An optimized and flexible pipeline for Hi-C data processing. Genome Biology, 16, 259.

[64]

Sicilia, A., Santoro, D. F., Testa, G., Cosentino, S. L., & Piero, A. R. L. (2020). Transcriptional response of giant reed (Arundo donax L.) low ecotype to long-term salt stress by unigene-based RNAseq. Phytochemistry, 177, 112436.

[65]

Sicilia, A., Testa, G., Santoro, D. F., Cosentino, S. L., & Lo Piero, A. R. (2019). RNASeq analysis of giant cane reveals the leaf transcriptome dynamics under long-term salt stress. BMC Plant Biology, 19(1), 355.

[66]

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(19), 3210–3212.

[67]

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.

[68]

Sun, H., Jiao, W. B., Krause, K., Campoy, J. A., Goel, M., Folz-Donahue, K., Kukat, C., Huettel, B., & Schneeberger, K. (2022). Chromosome-scale and haplotype-resolved genome assembly of a tetraploid potato cultivar. Nature Genetics, 54(3), 342–348.

[69]

Sun, J., Lu, F., Luo, Y., Bie, L., Xu, L., & Wang, Y. (2023). OrthoVenn3: An integrated platform for exploring and visualizing orthologous data across genomes. Nucleic Acids Research, 51(W1), W397–W403.

[70]

Sun, P., Jiao, B., Yang, Y., Shan, L., Li, T., Li, X., Xi, Z., Wang, X., & Liu, J. (2022). WGDI: A user-friendly toolkit for evolutionary analyses of whole-genome duplications and ancestral karyotypes. Molecular Plant, 15(12), 1841–1851.

[71]

Tang, Y., Xie, J. S., & Geng, S. (2010). Marginal land-based biomass energy production in China. Journal of Integrative Plant Biology, 52(1), 112–121.

[72]

Tarin, D., Pepper, A. E., Goolsby, J. A., Moran, P. J., Arquieta, A. C., Kirk, A. E., & Manhart, J. R. (2013). Microsatellites uncover multiple introductions of clonal giant reed (Arundo donax). Invasive Plant Science & Management, 6(3), 328–338.

[73]

Wang, X., Wang, J., Jin, D., Guo, H., Lee, T. H., Liu, T., & Paterson, A. H. (2015). Genome alignment spanning major poaceae lineages reveals heterogeneous evolutionary rates and alters inferred dates for key evolutionary events. Molecular Plant, 8(6), 885–898.

[74]

Wang, X., & Wang, L. (2016). GMATA: An integrated software package for genome-scale SSR mining, marker development and viewing. Frontiers in Plant Science, 7(7), 1350.

[75]

Wang, Y., Yu, J., Jiang, M., Lei, W., Zhang, X., & Tang, H. (2023). Sequencing and assembly of polyploid genomes. Methods in Molecular Biology, 2545, 429–458.

[76]

Xu, Z., & Wang, H. (2010). LTR_FINDER: An efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Research, 35(Web Server issue), W265–W268.

[77]

Zdobnov, E. M., & Apweiler, R. (2001). InterProScan—An integration platform for the signature-recognition methods in InterPro. Bioinformatics, 17(9), 847–848.

[78]

Zhang, C., Yang, Z., Tang, D., Zhu, Y., Wang, P., Li, D., Zhu, G., Xiong, X., Shang, Y., Li, C., & Huang, S. (2021). Genome design of hybrid potato. Cell, 184(15), 3873–3883.e12.

[79]

Zhang, J., Li, Y., Zhang, C., & Jing, Y. (2008). Adsorption of malachite green from aqueous solution onto carbon prepared from Arundo donax root. Journal of Hazardous Materials, 150(3), 774–782.

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