Chromosome-level genome assemblies from two sandalwood species provide insights into the evolution of the Santalales.
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
01 06 2023
01 06 2023
Historique:
received:
18
05
2022
accepted:
25
05
2023
medline:
5
6
2023
pubmed:
2
6
2023
entrez:
1
6
2023
Statut:
epublish
Résumé
Sandalwood is one of the most expensive woods in the world and is well known for its long-lasting and distinctive aroma. In our study, chromosome-level genome assemblies for two sandalwood species (Santalum album and Santalum yasi) were constructed by integrating NGS short reads, RNA-seq, and Hi-C libraries with PacBio HiFi long reads. The S. album and S. yasi genomes were both assembled into 10 pseudochromosomes with a length of 229.59 Mb and 232.64 Mb, containing 21,673 and 22,816 predicted genes and a repeat content of 28.93% and 29.54% of the total genomes, respectively. Further analyses resolved a Santalum-specific whole-genome triplication event after divergence from ancestors of the Santalales lineage Malania, yet due to dramatic differences in transposon content, the Santalum genomes were only one-sixth the size of the Malania oleifera genome. Examination of RNA-seq data revealed a suite of genes that are differentially expressed in haustoria and might be involved in host hemiparasite interactions. The two genomes presented here not only provide an important comparative dataset for studying genome evolution in early diverging eudicots and hemiparasitic plants but will also hasten the application of conservation genomics for a lineage of trees recovering from decades of overexploitation.
Identifiants
pubmed: 37264116
doi: 10.1038/s42003-023-04980-2
pii: 10.1038/s42003-023-04980-2
pmc: PMC10235099
doi:
Substances chimiques
Sesquiterpenes
0
Banques de données
figshare
['10.6084/m9.figshare.22877087']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
587Commentaires et corrections
Type : ErratumIn
Informations de copyright
© 2023. The Author(s).
Références
Harbaugh, D. T. & Baldwin, B. G. Phylogeny and biogeography of the sandalwoods (Santalum, Santalaceace): repeated dispersals throughout the Pacific. Am. J. Bot. 94, 1028–1040 (2007).
pubmed: 21636472
doi: 10.3732/ajb.94.6.1028
Scartezzini, P. & Speroni, E. Review on some plants of Indian traditional medicine with antioxidant activity. J. Ethnopharmacol. 71, 23–43 (2000).
pubmed: 10904144
doi: 10.1016/S0378-8741(00)00213-0
Kim, T. H. et al. New antitumor sesquiterpenoids from Santalum album of Indian origin. Tetrahedron 62, 6981–6989 (2006).
doi: 10.1016/j.tet.2006.04.072
Kumar, A. N. A., Joshi, G. & Ram, H. Y. M. Sandalwood: history, uses, present status and the future. Curr. Sci. 103, 1408–1416 (2012).
Radomiljac, A. M., McComb, J. A., Pate, J. S. & Tennakoon, K. U. Xylem transfer of organic solutes in Santalum album L. (Indian sandalwood) in association with legume and non-legume hosts. Ann. Bot. 82, 675–682 (1998).
doi: 10.1006/anbo.1998.0741
Ouyang, Y., Zhang, X. H., Chen, Y. L., da Silva, J. A. T. & Ma, G. H. Growth, photosynthesis and haustorial development of semiparasitic Santalum album L. penetrating into roots of three hosts: a comparative study. Trees 30, 317–328 (2016).
doi: 10.1007/s00468-015-1303-3
Das, S., Ray, S., Dey, S. & Dasgupta, S. Optimisation of sucrose, inorganic nitrogen and abscisic acid levels for Santalum album L. somatic embryo production in suspension culture. Process Biochem. 37, 51–56 (2001).
doi: 10.1016/S0032-9592(01)00168-6
Bottin, L. & Bouvet, J.-M. Chemical variability of sandalwood populations in New Caledonia. In Proc. Regional Workshop on Sandalwood Research, Development and Extension in the Pacific Islands and Asia, 81–85 (2005).
Celedon, J. M. et al. Heartwood-specific transcriptome and metabolite signatures of tropical sandalwood (Santalum album) reveal the final step of (Z)-santalol fragrance biosynthesis. Plant J. 86, 289–299 (2016).
pubmed: 26991058
doi: 10.1111/tpj.13162
Yan, T., Chen, Y., Wang, Q., Shang, L. & Li, G. Identification of heartwood from different Santalaceae species by gas chromatography-mass spectrometer (GC-MS). China Wood Ind. 34, 48–51 (2016).
Zhang, Y. et al. Molecular cloning and functional analysis of 1-deoxy-D-xylulose 5-phosphate reductoisomerase from Santalum album. Genes 12, 626 (2021).
pubmed: 33922119
pmcid: 8143465
doi: 10.3390/genes12050626
Yan, H. et al. Genome-wide characterization, expression profile analysis of WRKY family genes in Santalum album and functional identification of their role in abiotic stress. Int. J. Mol. Sci. 20, 5676 (2019).
pubmed: 31766135
pmcid: 6888422
doi: 10.3390/ijms20225676
Zhang, X. et al. Identification and functional characterization of three new terpene synthase genes involved in chemical defense and abiotic stresses in Santalum album. BMC Plant Biol. 19, 115 (2019).
pubmed: 30922222
pmcid: 6437863
doi: 10.1186/s12870-019-1720-3
Robson, K. Prospects for high-value hardwood timber plantations in the dry tropics of Northern Australia. Aust. Forestry 69, 142–145 (2004).
Mahesh, H. B. et al. Multi-omics driven assembly and annotation of the sandalwood (Santalum album) genome. Plant Physiol. 176, 2772–2788 (2018).
pubmed: 29440596
pmcid: 5884603
doi: 10.1104/pp.17.01764
Dasgupta, M. G., Ulaganathan, K., Dev, S. A. & Balakrishnan, S. Draft genome of Santalum album L. provides genomic resources for accelerated trait improvement. Tree Genet. Genomes 15, 34 (2019).
doi: 10.1007/s11295-019-1334-9
Xu, C. Q. et al. Genome sequence of Malania oleifera, a tree with great value for nervonic acid production. Gigascience 8, giy164 (2019).
pubmed: 30689848
pmcid: 6377399
doi: 10.1093/gigascience/giy164
Wilhelm, M. & Wilhelm, F. X. Reverse transcription of retroviruses and LTR retrotransposons. Cell. Mol. Life Sci. 58, 1246–1262 (2001).
pubmed: 11577982
doi: 10.1007/PL00000937
Zhang, L. J. et al. The tartary buckwheat genome provides insights into rutin biosynthesis and abiotic stress tolerance. Mol. Plant 10, 1224–1237 (2017).
pubmed: 28866080
doi: 10.1016/j.molp.2017.08.013
Michael, T. P. Plant genome size variation: bloating and purging DNA. Brief. Funct. Genomics 13, 308–317 (2014).
pubmed: 24651721
doi: 10.1093/bfgp/elu005
Lee, S., Choi, S., Jeon, D., Kang, Y. & Kim, C. Evolutionary impact of whole genome duplication in Poaceae family. J. Crop Sci. Biotechnol. 23, 413–425 (2020).
doi: 10.1007/s12892-020-00049-2
Ichihashi, Y. et al. Transcriptomic and metabolomic reprogramming from roots to haustoria in the parasitic plant, Thesium chinense. Plant Cell Physiol. 59, 729–738 (2018).
doi: 10.1093/pcp/pcx200
Zhang, X. H. et al. RNA-Seq analysis identifies key genes associated with haustorial development in the root hemiparasite Santalum album. Front. Plant Sci. 6, 661 (2015).
Jones, C. G. et al. Sandalwood fragrance biosynthesis involves sesquiterpene synthases of both the terpene synthase (TPS)-a and TPS-b subfamilies, including santalene synthases. J. Biol. Chem. 286, 17445–17454 (2011).
pubmed: 21454632
pmcid: 3093818
doi: 10.1074/jbc.M111.231787
Diaz-Chavez, M. L. et al. Biosynthesis of sandalwood oil: Santalum album CYP76F cytochromes P450 produce santalols and bergamotol. PLoS ONE 8, e75053 (2013).
pubmed: 24324844
pmcid: 3854609
doi: 10.1371/journal.pone.0075053
Wei, C. L. et al. Draft genome sequence of Camellia sinensis var. sinensis provides insights into the evolution of the tea genome and tea quality. Proc. Natl Acad. Sci. USA 115, E4151–E4158 (2018).
pubmed: 29678829
pmcid: 5939082
doi: 10.1073/pnas.1719622115
Nowoshilow, S. et al. The axolotl genome and the evolution of key tissue formation regulators. Nature 554, 50 (2018).
pubmed: 29364872
doi: 10.1038/nature25458
The Angiosperm Phylogeny Group. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot. J. Linn. Soc. 181, 1–20 (2016).
doi: 10.1111/boj.12385
Qin, L. Y. et al. Insights into angiosperm evolution, floral development and chemical biosynthesis from the Aristolochia fimbriata genome. Nat. Plants 7, 1239 (2021).
pubmed: 34475528
pmcid: 8445822
doi: 10.1038/s41477-021-00990-2
Chanderbali, A. S. et al. Buxus and Tetracentron genomes help resolve eudicot genome history. Nat. Commun. 13, 643 (2022).
pubmed: 35110570
pmcid: 8810787
doi: 10.1038/s41467-022-28312-w
Escudero, M., Feliner, G. N., Pokorny, L., Spalink, D. & Viruel, J. Editorial: phylogenomic approaches to deal with particularly challenging plant lineages. Front. Plant Sci. 11, 591762 (2020).
pubmed: 33329657
pmcid: 7732580
doi: 10.3389/fpls.2020.591762
Birchler, J. A. & Yang, H. The multiple fates of gene duplications: deletion, hypofunctionalization, subfunctionalization, neofunctionalization, dosage balance constraints, and neutral variation. Plant Cell 34, 2466–2474 (2022).
pubmed: 35253876
pmcid: 9252495
doi: 10.1093/plcell/koac076
Devos, K. M., Brown, J. K. M. & Bennetzen, J. L. Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res. 12, 1075–1079 (2002).
pubmed: 12097344
pmcid: 186626
doi: 10.1101/gr.132102
Porebski, S., Bailey, L. G. & Baum, B. R. Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol. Biol. Rep. 15, 8–15 (1997).
doi: 10.1007/BF02772108
Zhu, X. Y. et al. Genome sequencing and analysis of Thraustochytriidae sp. SZU445 provides novel insights into the polyunsaturated fatty acid biosynthesis pathway. Mar. Drugs 18, 118 (2020).
pubmed: 32085426
pmcid: 7073664
doi: 10.3390/md18020118
Sun, X. P. et al. Phased diploid genome assemblies and pan-genomes provide insights into the genetic history of apple domestication. Nat. Genet. 52, 1423–1432 (2020).
pubmed: 33139952
pmcid: 7728601
doi: 10.1038/s41588-020-00723-9
Toni, L. S. et al. Optimization of phenol-chloroform RNA extraction. MethodsX 5, 599–608 (2018).
pubmed: 29984193
pmcid: 6031757
doi: 10.1016/j.mex.2018.05.011
Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357–360 (2015).
pubmed: 25751142
pmcid: 4655817
doi: 10.1038/nmeth.3317
Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
pubmed: 24227677
doi: 10.1093/bioinformatics/btt656
Ranallo-Benavidez, T.R., Jaron, K.S. & Schatz, M.C. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat. Commun. 11, 1432 (2020).
Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https://arxiv.org/abs/1303.3997 (2013).
Walker, B. J. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9, e112963 (2014).
pubmed: 25409509
pmcid: 4237348
doi: 10.1371/journal.pone.0112963
Simao, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015).
pubmed: 26059717
doi: 10.1093/bioinformatics/btv351
Ou, S. J. et al. Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline. Genome Biol. 20, 275 (2019).
pubmed: 31843001
pmcid: 6913007
doi: 10.1186/s13059-019-1905-y
Tarailo-Graovac, M. & Chen, N. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr. Protoc. Bioinformatics 4, 4.10 (2009).
Flynn, J. M. et al. RepeatModeler2 for automated genomic discovery of transposable element families. Proc. Natl Acad. Sci. USA 117, 9451–9457 (2020).
pubmed: 32300014
pmcid: 7196820
doi: 10.1073/pnas.1921046117
Benson, G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573–580 (1999).
pubmed: 9862982
pmcid: 148217
doi: 10.1093/nar/27.2.573
Kalvari, I. et al. Rfam 14: expanded coverage of metagenomic, viral and microRNA families. Nucleic Acids Res. 49, D192–D200 (2021).
pubmed: 33211869
doi: 10.1093/nar/gkaa1047
Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011).
pubmed: 21572440
pmcid: 3571712
doi: 10.1038/nbt.1883
Kim, D., Paggi, J. M., Park, C., Bennett, C. & Salzberg, S. L. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat. Biotechnol. 37, 907–915 (2019).
pubmed: 31375807
pmcid: 7605509
doi: 10.1038/s41587-019-0201-4
Kovaka, S. et al. Transcriptome assembly from long-read RNA-seq alignments with StringTie2. Genome Biol. 20, 278 (2019).
pubmed: 31842956
pmcid: 6912988
doi: 10.1186/s13059-019-1910-1
Kim, H. S. et al. Identification of xenobiotic biodegradation and metabolism-related genes in the copepod Tigriopus japonicus whole transcriptome analysis. Mar. Genomics 24, 207–208 (2015).
Stanke, M. et al. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 34, W435–W439 (2006).
pubmed: 16845043
pmcid: 1538822
doi: 10.1093/nar/gkl200
Majoros, W. H., Pertea, M. & Salzberg, S. L. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20, 2878–2879 (2004).
pubmed: 15145805
doi: 10.1093/bioinformatics/bth315
Haas, B. J. et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol. 9, R7 (2008).
pubmed: 18190707
pmcid: 2395244
doi: 10.1186/gb-2008-9-1-r7
Jones, P. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014).
pubmed: 24451626
pmcid: 3998142
doi: 10.1093/bioinformatics/btu031
Emms, D. M. & Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238 (2019).
pubmed: 31727128
pmcid: 6857279
doi: 10.1186/s13059-019-1832-y
Rozewicki, J., Li, S. L., Amada, K. M., Standley, D. M. & Katoh, K. MAFFT-DASH: integrated protein sequence and structural alignment. Nucleic Acids Res. 47, W5–W10 (2019).
pubmed: 31062021
pmcid: 6602451
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
pubmed: 24451623
pmcid: 3998144
doi: 10.1093/bioinformatics/btu033
De Bie, T., Cristianini, N., Demuth, J. P. & Hahn, M. W. CAFE: a computational tool for the study of gene family evolution. Bioinformatics 22, 1269–1271 (2006).
pubmed: 16543274
doi: 10.1093/bioinformatics/btl097
Zhang, C. F. et al. Asterid phylogenomics/phylotranscriptomics uncover morphological evolutionary histories and support phylogenetic placement for numerous whole-genome duplications. Mol. Biol. Evol. 37, 3188–3210 (2020).
pubmed: 32652014
doi: 10.1093/molbev/msaa160
Chen, C. et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol. Plant 13, 1194–1202 (2020).
pubmed: 32585190
doi: 10.1016/j.molp.2020.06.009