Chromosome-level baobab genome illuminates its evolutionary trajectory and environmental adaptation
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články
PubMed
39396056
PubMed Central
PMC11470940
DOI
10.1038/s41467-024-53157-w
PII: 10.1038/s41467-024-53157-w
Knihovny.cz E-zdroje
- MeSH
- chromozomy rostlin * genetika MeSH
- fylogeneze MeSH
- fyziologická adaptace genetika MeSH
- genom rostlinný * MeSH
- molekulární evoluce * MeSH
- retroelementy genetika MeSH
- stromy genetika MeSH
- tok genů MeSH
- transpozibilní elementy DNA genetika MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Madagaskar MeSH
- Názvy látek
- retroelementy MeSH
- transpozibilní elementy DNA MeSH
Baobab (Adansonia digitata) is a long-lived tree endemic to Africa with economic, ecological, and cultural importance, yet its genomic features are underexplored. Here, we report a chromosome-level reference genome anchored to 42 chromosomes for A. digitata, alongside draft assemblies for a sibling tree, two trees from distinct locations in Africa, and A. za from Madagascar. The baobab genome is uniquely rich in DNA transposons, which make up 33%, while LTR retrotransposons account for 10%. A. digitata experienced whole genome multiplication (WGM) around 30 million years ago (MYA), followed by a second WGM event 3-11 MYA, likely linked to autotetraploidy. Resequencing of 25 trees identify three subpopulations, with gene flow across West Africa distinct from East Africa. Gene enrichment and fixation index (Fst) analyses show baobab retained multiple circadian, flowering, and light-responsive genes, which likely support longevity through the UV RESISTANCE LOCUS 8 (UVR8) pathway. In sum, we provide genomic resources and insights for baobab breeding and conservation.
Department of Botany Faculty of Science Charles University Prague Czech Republic
Department of Botany University of Wisconsin Madison Madison WI USA
Missouri Botanical Garden Science and Conservation Division St Louis MO USA
School of Life Sciences University of Nottingham Nottingham UK
Zobrazit více v PubMed
Gibb, H. A. R. & Beckingham, C. F. The Travels of Ibn Battuta, AD1325–1354 (Routledge, 2017).
Baum, D. A. A systematic revision of Adansonia (Bombacaceae). Ann. Mo. Bot. Gard.82, 440–470 (1995).
Asogwa, I. S., Ibrahim, A. N. & Agbaka, J. I. African baobab: its role in enhancing nutrition, health, and the environment. Trees For. People3, 100043 (2021).
Silva, V. M., Putti, F. F., White, P. J. & Reis, A. R. D. Phytic acid accumulation in plants: biosynthesis pathway regulation and role in human diet. Plant Physiol. Biochem.164, 132–146 (2021). PubMed
Research and Markets. Baobab powder - global strategic business report. https://www.researchandmarkets.com/reports/5029822/baobab-powder-global-strategic-business-report (2024).
Offiah, V. O. & Falade, K. O. Potentials of baobab in food systems. Appl. Food Res.3, 100299 (2023).
Patrut, A. et al. The demise of the largest and oldest African baobabs. Nat. Plants4, 423–426 (2018). PubMed
Gebauer, J. et al. Africa’s wooden elephant: the baobab tree (Adansonia digitata L.) in Sudan and Kenya: a review. Genet. Resour. Crop Evol.63, 377–399 (2016).
Venter, S. M. & Witkowski, E. T. F. Where are the young baobabs? Factors affecting regeneration of Adansonia digitata L. in a communally managed region of southern Africa. J. Arid Environ.92, 1–13 (2013).
Venter, S. M. et al. Baobabs (Adansonia digitata L.) are self-incompatible and ‘male’ trees can produce fruit if hand-pollinated. S. Afr. J. Bot.109, 263–268 (2017).
Karimi, N. et al. Evidence for hawkmoth pollination in the chiropterophilous African baobab (Adansonia digitata). Biotropica54, 113–124 (2022).
Start, A. N. Pollination of the baobab (Adansonia digitata L.) by the fruit bat Rousettus aegyptiacus E. Geoffroy. Afr. J. Ecol.10, 71–72 (1972).
Taylor, P. J., Vise, C., Krishnamoorthy, M. A., Kingston, T. & Venter, S. Citizen science confirms the rarity of fruit bat pollination of baobab (Adansonia digitata) flowers in Southern Africa. Diversity12, 106 (2020).
Coe, M. J. & Isaac, F. M. Pollination of the baobab (Adansonia digitata L.) by the lesser bush baby (Galago crassicaudatus E. Geoffroy). East Afr. Wildl. J.3, 123–124 (1965).
Cron, G. V. et al. One African baobab species or two? Synonymy of Adansonia kilima and A. digitata. Taxon65, 1037–1049 (2016).
Patrut, A. et al. Radiocarbon dating of two old African baobabs from India. PLoS ONE15, e0227352 (2020). PubMed PMC
Swanepoel, C. M. Notes and records baobab phenology and growth in the Zambezi Valley, Zimbabwe. Afr. J. Ecol.31, 84–86 (1993).
Kitony, J. K. Nested association mapping population in crops: current status and future prospects. J. Crop Sci. Biotechnol.26, 1–12 (2022).
Levin, D. A. The Role of Chromosomal Change in Plant Evolution (Oxford Univ. Press, Oxford, 2002).
Wickens, G. E. The Baobabs: Pachycauls of Africa, Madagascar and Australia (Springer Science & Business Media, 2008).
Chan, E. K. F. et al. Human origins in a southern African palaeo-wetland and first migrations. Nature575, 185–189 (2019). PubMed
Sanchez, A. C., Osborne, P. E. & Haq, N. Climate change and the African baobab (Adansonia digitata L.): the need for better conservation strategies. Afr. J. Ecol.49, 234–245 (2011).
Woods, S., O’Neill, K. & Pirro, S. The complete genome sequence of (Malvaceae, Malvales), the African baobab. Biodivers. Genomes10.56179/001c.72789 (2023). PubMed PMC
Wan, J.-N. et al. The rise of baobab trees in Madagascar. Nature629, 1091–1099 (2024). PubMed PMC
Islam-Faridi, N., Sakhanokho, H. F. & Dana Nelson, C. New chromosome number and cyto-molecular characterization of the African Baobab (Adansonia digitata L.) - ‘The Tree of Life’. Sci. Rep.10, 13174 (2020). PubMed PMC
Costa, L., Oliveira, Á., Carvalho-Sobrinho, J. & Souza, G. Comparative cytomolecular analyses reveal karyotype variability related to biogeographic and species richness patterns in Bombacoideae (Malvaceae). Plant Syst. Evol.303, 1131–1144 (2017).
Baum, D. A. & Oginuma, K. A review of chromosome numbers in Bombacaceae with new counts for Adansonia. Taxon43, 1 (1994).
Pettigrew FRS, J. D. et al. Morphology, ploidy and molecular phylogenetics reveal a new diploid species from Africa in the baobab genus Adansonia (Malvaceae: Bombacoideae). Taxon61, 1240–1250 (2012).
Bennett, M. D. & Leitch, I. J. Nuclear DNA amounts in angiosperms: targets, trends and tomorrow. Ann. Bot.107, 467–590 (2011). PubMed PMC
Henniges, M. C. et al. The plant DNA C-values database: a one-stop shop for plant genome size data. Methods Mol. Biol.2703, 111–122 (2023). PubMed
Leong Pock Tsy, J.-M. et al. Nuclear microsatellite variation in Malagasy baobabs (Adansonia, Bombacoideae, Malvaceae) reveals past hybridization and introgression. Ann. Bot.112, 1759–1773 (2013). PubMed PMC
Sun, H. et al. Chromosome-scale and haplotype-resolved genome assembly of a tetraploid potato cultivar. Nat. Genet.54, 342–348 (2022). PubMed PMC
Aklilu, B. B. et al. Functional diversification of replication protein A paralogs and telomere length maintenance in Arabidopsis. Genetics215, 989–1002 (2020). PubMed PMC
Aklilu, B. B., Soderquist, R. S. & Culligan, K. M. Genetic analysis of the replication protein A large subunit family in Arabidopsis reveals unique and overlapping roles in DNA repair, meiosis and DNA replication. Nucleic Acids Res.42, 3104–3118 (2014). PubMed PMC
Ishibashi, T. et al. Two types of replication protein A in seed plants. FEBS J.272, 3270–3281 (2005). PubMed
Takashi, Y., Kobayashi, Y., Tanaka, K. & Tamura, K. Arabidopsis replication protein A 70a is required for DNA damage response and telomere length homeostasis. Plant Cell Physiol.50, 1965–1976 (2009). PubMed
Colt, K. et al. Telomere length in plants estimated with long read sequencing. Preprint at bioRxiv10.1101/2024.03.27.586973 (2024).
Whittemore, K., Vera, E., Martínez-Nevado, E., Sanpera, C. & Blasco, M. A. Telomere shortening rate predicts species life span. Proc. Natl Acad. Sci. USA116, 15122–15127 (2019). PubMed PMC
Han, Y. et al. Chromosome-level genome assembly of Welwitschia mirabilis, a unique Namib Desert species. Mol. Ecol. Resour.22, 391–403 (2022). PubMed
Wan, T. et al. The Welwitschia genome reveals a unique biology underpinning extreme longevity in deserts. Nat. Commun.12, 4247 (2021). PubMed PMC
Patrut, A. et al. AMS radiocarbon dating of large Za baobabs (Adansonia za) of Madagascar. PLoS ONE11, e0146977 (2016). PubMed PMC
Scott, A. D., Stenz, N. W. M., Ingvarsson, P. K. & Baum, D. A. Whole genome duplication in coast redwood (Sequoia sempervirens) and its implications for explaining the rarity of polyploidy in conifers. N. Phytol.211, 186–193 (2016). PubMed
Ernst, E. et al. The genomes and epigenomes of aquatic plants (Lemnaceae) promote triploid hybridization and clonal reproduction. Preprint at bioRxiv10.1101/2023.08.02.551673 (2023).
VanBuren, R. et al. Exceptional subgenome stability and functional divergence in the allotetraploid Ethiopian cereal teff. Nat. Commun.11, 884 (2020). PubMed PMC
Bell, C. G. et al. DNA methylation aging clocks: challenges and recommendations. Genome Biol.20, 249 (2019). PubMed PMC
Wilkinson, G. S. et al. DNA methylation predicts age and provides insight into exceptional longevity of bats. Nat. Commun.12, 1615 (2021). PubMed PMC
Mira, S., Pirredda, M., Martín-Sánchez, M., Marchessi, J. E. & Martín, C. DNA methylation and integrity in aged seeds and regenerated plants. Seed Sci. Res.30, 92–100 (2020).
Gallego-Bartolomé, J. DNA methylation in plants: mechanisms and tools for targeted manipulation. N. Phytol.227, 38–44 (2020). PubMed
Naish, M. et al. The genetic and epigenetic landscape of the centromeres. Science374, eabi7489 (2021). PubMed PMC
Niederhuth, C. E. et al. Widespread natural variation of DNA methylation within angiosperms. Genome Biol.17, 194 (2016). PubMed PMC
Michael, T. P. Plant genome size variation: bloating and purging DNA. Brief. Funct. Genom.13, 308–317 (2014). PubMed
Comai, L., Maheshwari, S. & Marimuthu, M. P. A. Plant centromeres. Curr. Opin. Plant Biol.36, 158–167 (2017). PubMed
Tilbrook, K. et al. The UVR8 UV-B photoreceptor: perception, signaling and response. Arabidopsis Book11, e0164 (2013). PubMed PMC
Tossi, V. E. et al. Beyond Arabidopsis: differential UV-B response mediated by UVR8 in diverse species. Front. Plant Sci.10, 780 (2019). PubMed PMC
Liu, W. et al. Phosphorylation of Arabidopsis UVR8 photoreceptor modulates protein interactions and responses to UV-B radiation. Nat. Commun.15, 1221 (2024). PubMed PMC
Jenkins, G. I. The UV-B photoreceptor UVR8: from structure to physiology. Plant Cell26, 21–37 (2014). PubMed PMC
Bourbousse, C., Barneche, F. & Laloi, C. Plant chromatin catches the sun. Front. Plant Sci.10, 1728 (2019). PubMed PMC
Amborella Genome Project. The Amborella genome and the evolution of flowering plants. Science342, 1241089 (2013). PubMed
Jaillon, O. et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature449, 463–467 (2007). PubMed
Karimi, N. et al. Reticulate evolution helps explain apparent homoplasy in floral biology and pollination in baobabs (Adansonia; Bombacoideae; Malvaceae). Syst. Biol.69, 462–478 (2020). PubMed
Wang, M. et al. Comparative genome analyses highlight transposon-mediated genome expansion and the evolutionary architecture of 3D genomic folding in cotton. Mol. Biol. Evol.38, 3621–3636 (2021). PubMed PMC
Conover, J. L. et al. A Malvaceae mystery: a mallow maelstrom of genome multiplications and maybe misleading methods? J. Integr. Plant Biol.61, 12–31 (2019). PubMed
Argout, X. et al. The genome of Theobroma cacao. Nat. Genet.43, 101–108 (2010). PubMed
Wang, X. et al. Comparative genomic de-convolution of the cotton genome revealed a decaploid ancestor and widespread chromosomal fractionation. N. Phytol.209, 1252–1263 (2016). PubMed
Paterson, A. H. et al. Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature492, 423–427 (2012). PubMed
Sun, P. et al. Subgenome-aware analyses reveal the genomic consequences of ancient allopolyploid hybridizations throughout the cotton family. Proc. Natl Acad. Sci. USA121, e2313921121 (2024). PubMed PMC
Shao, L. et al. High-quality genomes of Bombax ceiba and Ceiba pentandra provide insights into the evolution of Malvaceae species and differences in their natural fiber development. Plant Commun.5, 100832 (2024). PubMed PMC
Cheng, F. et al. Gene retention, fractionation and subgenome differences in polyploid plants. Nat. Plants4, 258–268 (2018). PubMed
Raju, S. K. K. Gene dosage balance immediately following whole-genome duplication in Arabidopsis. Plant cell32, 1344–1345 (2020). PubMed PMC
Michael, T. P. Core circadian clock and light signaling genes brought into genetic linkage across the green lineage. Plant Physiol.190, 1037–1056 (2022). PubMed PMC
Lou, P. et al. Preferential retention of circadian clock genes during diploidization following whole genome triplication in Brassica rapa. Plant Cell24, 2415–2426 (2012). PubMed PMC
Wickell, D. et al. Underwater CAM photosynthesis elucidated by Isoetes genome. Nat. Commun.12, 6348 (2021). PubMed PMC
Yang, X. et al. The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism. Nat. Commun.8, 1–15 (2017). PubMed PMC
Wai, C. M. et al. Time of day and network reprogramming during drought induced CAM photosynthesis in Sedum album. PLoS Genet.15, e1008209 (2019). PubMed PMC
Ming, R. et al. The pineapple genome and the evolution of CAM photosynthesis. Nat. Genet.47, 1435–1442 (2015). PubMed PMC
Greenham, K. et al. Geographic variation of plant circadian clock function in natural and agricultural settings. J. Biol. Rhythms32, 26–34 (2017). PubMed
Condamine, F. L., Silvestro, D., Koppelhus, E. B. & Antonelli, A. The rise of angiosperms pushed conifers to decline during global cooling. Proc. Natl Acad. Sci. USA117, 28867–28875 (2020). PubMed PMC
Soltis, P. S., Folk, R. A. & Soltis, D. E. Darwin review: angiosperm phylogeny and evolutionary radiations. Proc. R. Soc. B.286, 20190099 (2019).
Chetty, A., Glennon, K. L., Venter, S. M., Cron, G. V. & Witkowski, E. T. F. Reproductive ecology of the African baobab: floral features differ among individuals with different fruit production. Ecol. Manag.489, 119077 (2021).
Li, H. & Ralph, P. Local PCA shows how the effect of population structure differs along the genome. Genetics211, 289–304 (2019). PubMed PMC
Wild, S. Africa’s majestic baobab trees are mysteriously dying. Nature558, 529–529 (2018). PubMed
Birchler, J. A. & Veitia, R. A. Gene balance hypothesis: connecting issues of dosage sensitivity across biological disciplines. Proc. Natl Acad. Sci. USA109, 14746–14753 (2012). PubMed PMC
Feng, X. et al. Genomic evidence for rediploidization and adaptive evolution following the whole-genome triplication. Nat. Commun.15, 1635 (2024). PubMed PMC
Marshall, C. M., Thompson, V. L., Creux, N. M. & Harmer, S. L. The circadian clock controls temporal and spatial patterns of floral development in sunflower. eLife12, e80984 (2023). PubMed PMC
Fenske, M. P., Nguyen, L. P., Horn, E. K., Riffell, J. A. & Imaizumi, T. Circadian clocks of both plants and pollinators influence flower seeking behavior of the pollinator hawkmoth Manduca sexta. Sci. Rep.8, 2842 (2018). PubMed PMC
Garsmeur, O. et al. Two evolutionarily distinct classes of paleopolyploidy. Mol. Biol. Evol.31, 448–454 (2014). PubMed
Fehér, B. et al. Functional interaction of the circadian clock and UV RESISTANCE LOCUS 8-controlled UV-B signaling pathways in Arabidopsis thaliana. Plant J.67, 37–48 (2011). PubMed
Monnahan, P. et al. Pervasive population genomic consequences of genome duplication in Arabidopsis arenosa. Nat. Ecol. Evol.3, 457–468 (2019). PubMed
Bloch, G., Bar-Shai, N., Cytter, Y. & Green, R. Time is honey: circadian clocks of bees and flowers and how their interactions may influence ecological communities. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372, 20160256 (2017). PubMed PMC
Fenske, M. P. & Imaizumi, T. Circadian rhythms in floral scent emission. Front. Plant Sci.7, 462 (2016). PubMed PMC
Klein, S. J. & O’Neill, R. J. Transposable elements: genome innovation, chromosome diversity, and centromere conflict. Chromosome Res.26, 5–23 (2018). PubMed PMC
Korbo, A. et al. Comparison of East and West African populations of baobab (Adansonia digitata L.). Agrofor. Syst.85, 505–518 (2011).
Liao, N. et al. Chromosome-level genome assembly of bunching onion illuminates genome evolution and flavor formation in Allium crops. Nat. Commun.13, 6690 (2022). PubMed PMC
Budhlakoti, N. et al. Genomic selection: a tool for accelerating the efficiency of molecular breeding for development of climate-resilient crops. Front. Genet.13, 832153 (2022). PubMed PMC
Lutz, K. A., Wang, W., Zdepski, A. & Michael, T. P. Isolation and analysis of high quality nuclear DNA with reduced organellar DNA for plant genome sequencing and resequencing. BMC Biotechnol.11, 54 (2011). PubMed PMC
Kolmogorov, M., Yuan, J., Lin, Y. & Pevzner, P. A. Assembly of long, error-prone reads using repeat graphs. Nat. Biotechnol.37, 540–546 (2019). PubMed
Vaser, R., Sović, I., Nagarajan, N. & Šikić, M. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res.27, 737–746 (2017). PubMed PMC
Walker, B. J. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE9, e112963 (2014). PubMed PMC
Manni, M., Berkeley, M. R., Seppey, M., Simão, F. A. & Zdobnov, E. M. BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol. Biol. Evol.38, 4647–4654 (2021). PubMed PMC
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). PubMed PMC
Weiß, C. L., Pais, M., Cano, L. M., Kamoun, S. & Burbano, H. A. nQuire: a statistical framework for ploidy estimation using next generation sequencing. BMC Bioinforma.19, 122 (2018). PubMed PMC
Ou, S. et al. Author correction: Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline. Genome Biol.23, 76 (2022). PubMed PMC
Benson, G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res.27, 573–580 (1999). PubMed PMC
Cantalapiedra, C. P., Hernández-Plaza, A., Letunic, I., Bork, P. & Huerta-Cepas, J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol. Biol. Evol.38, 5825–5829 (2021). PubMed PMC
Lynch, R. C. et al. Domesticated cannabinoid synthases amid a wild mosaic cannabis pangenome. Preprint at bioRxiv10.1101/2024.05.21.595196 (2024).
Cossu, R. M., Buti, M., Giordani, T., Natali, L. & Cavallini, A. A computational study of the dynamics of LTR retrotransposons in the Populus trichocarpa genome. Tree Genet. Genomes8, 61–75 (2011).
Emms, D. M. & Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol.20, 238 (2019). PubMed PMC
Goodstein, D. M. et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res.40, D1178–D1186 (2012). PubMed PMC
Mendes, F. K., Vanderpool, D., Fulton, B. & Hahn, M. W. CAFE 5 models variation in evolutionary rates among gene families. Bioinformatics36, 5516–5518 (2021). PubMed
Padgitt-Cobb, L. K., Pitra, N. J., Matthews, P. D., Henning, J. A. & Hendrix, D. A. An improved assembly of the ‘Cascade’ hop (Humulus lupulus) genome uncovers signatures of molecular evolution and refines time of divergence estimates for the Cannabaceae family. Hortic. Res10, uhac281 (2023). PubMed PMC
Goel, M., Sun, H., Jiao, W.-B. & Schneeberger, K. SyRI: finding genomic rearrangements and local sequence differences from whole-genome assemblies. Genome Biol.20, 277 (2019). PubMed PMC
Gaut, B. S., Morton, B. R., McCaig, B. C. & Clegg, M. T. Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc. Natl Acad. Sci. USA93, 10274–10279 (1996). PubMed PMC
Klopfenstein, D. V. et al. GOATOOLS: a Python library for gene ontology analyses. Sci. Rep.8, 10872 (2018). PubMed PMC
Supek, F., Bošnjak, M., Škunca, N. & Šmuc, T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE6, e21800 (2011). PubMed PMC
Kitony, J. K. et al. Chromosome-level baobab genome illuminates its evolutionary trajectory and environmental adaptation. Figshare, 10.6084/m9.figshare.26039878 (2024). PubMed PMC