Chromosome evolution and the genetic basis of agronomically important traits in greater yam
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, Research Support, U.S. Gov't, Non-P.H.S., Research Support, N.I.H., Extramural, práce podpořená grantem
Grantová podpora
S10 OD018174
NIH HHS - United States
BB/M004155/1
Biotechnology and Biological Sciences Research Council - United Kingdom
PubMed
35422045
PubMed Central
PMC9010478
DOI
10.1038/s41467-022-29114-w
PII: 10.1038/s41467-022-29114-w
Knihovny.cz E-zdroje
- MeSH
- chromozomy MeSH
- Dioscorea * genetika MeSH
- hlízy rostlin MeSH
- lidé MeSH
- lokus kvantitativního znaku genetika MeSH
- šlechtění rostlin MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, N.I.H., Extramural MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
The nutrient-rich tubers of the greater yam, Dioscorea alata L., provide food and income security for millions of people around the world. Despite its global importance, however, greater yam remains an orphan crop. Here, we address this resource gap by presenting a highly contiguous chromosome-scale genome assembly of D. alata combined with a dense genetic map derived from African breeding populations. The genome sequence reveals an ancient allotetraploidization in the Dioscorea lineage, followed by extensive genome-wide reorganization. Using the genomic tools, we find quantitative trait loci for resistance to anthracnose, a damaging fungal pathogen of yam, and several tuber quality traits. Genomic analysis of breeding lines reveals both extensive inbreeding as well as regions of extensive heterozygosity that may represent interspecific introgression during domestication. These tools and insights will enable yam breeders to unlock the potential of this staple crop and take full advantage of its adaptability to varied environments.
African Orphan Crops Consortium Nairobi Kenya
Agricultural Research Council Biotechnology Platform Pretoria South Africa
Chan Zuckerberg BioHub 499 Illinois St San Francisco CA 94158 USA
Cornell University Ithaca NY 14850 USA
Department of Biology University of Copenhagen Copenhagen Denmark
Department of Molecular and Cell Biology University of California Berkeley CA 94720 USA
DOE Joint Genome Institute Berkeley CA USA
Innovative Genomics Institute Berkeley CA USA
International Institute of Tropical Agriculture PMB 5320 Oyo Road Ibadan Nigeria
International Trade Center Accra Ghana
James Hutton Institute Dundee UK
National Root Crops Research Institute Umudike Nigeria
Okinawa Institute of Science and Technology Onna Okinawa Japan
School of Life Sciences University of Dundee Dundee UK
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Mignouna, H. D., Abang, M. M. & Asiedu, R. In Genomics of Tropical Crop Plants (eds. Moore, P. H. & Ming, R.) 549–570 (Springer New York, 2008).
Lebot, V. Tropical Root and Tuber Crops, 2nd edn. (CABI, 2019).
Coursey, D. G. Yams. An account of the nature, origins, cultivation and utilisation of the useful members of the Dioscoreaceae (Longmans, Green and Co. Ltd, London, 1968).
Zannou A, et al. Yam and cowpea diversity management by farmers in the Guinea-Sudan transition zone of Benin. NJAS Wagening. J. Life Sci. 2004;52:393–420. doi: 10.1016/S1573-5214(04)80023-X. DOI
Obidiegwu JE, Akpabio EM. The geography of yam cultivation in southern Nigeria: exploring its social meanings and cultural functions. J. Ethn. Foods. 2017;4:28–35. doi: 10.1016/j.jef.2017.02.004. DOI
Power RC, Güldemann T, Crowther A, Boivin N. Asian crop dispersal in Africa and late Holocene human adaptation to tropical environments. J. World Prehistory. 2019;32:353–392. doi: 10.1007/s10963-019-09136-x. DOI
Hahn, S. K. Yams. In Evolution of crop plants (eds. Smartt, J. & Simmonds, N. W.) 112–120 (Wiley-Blackwell, 1995).
Sartie A, Asiedu R. Segregation of vegetative and reproductive traits associated with tuber yield and quality in water yam (Dioscorea alata L.) Afr. J. Biotechnol. 2014;13:2807–2818. doi: 10.5897/AJB2014.13839. DOI
Muzac-Tucker I, Asemota HN, Ahmad MH. Biochemical composition and storage of Jamaican yams (Dioscorea sp) J. Sci. Food Agric. 1993;62:219–224. doi: 10.1002/jsfa.2740620303. DOI
Obidiegwu JE, Lyons JB, Chilaka CA. The Dioscorea genus (yam)-an appraisal of nutritional and therapeutic potentials. Foods. 2020;9:1304. doi: 10.3390/foods9091304. PubMed DOI PMC
Darkwa K, Olasanmi B, Asiedu R, Asfaw A. Review of empirical and emerging breeding methods and tools for yam (Dioscorea spp.) improvement: status and prospects. Plant Breed. 2020;139:474–497. doi: 10.1111/pbr.12783. DOI
Malapa R, Arnau G, Noyer JL, Lebot V. Genetic diversity of the greater yam (Dioscorea alata L.) and relatedness to D. nummularia Lam. and D. transversa Br. as revealed with AFLP markers. Genet. Resour. Crop Evol. 2005;52:919–929. doi: 10.1007/s10722-003-6122-5. DOI
Arnau G, Nemorin A, Maledon E, Abraham K. Revision of ploidy status of Dioscorea alata L. (Dioscoreaceae) by cytogenetic and microsatellite segregation analysis. Theor. Appl. Genet. 2009;118:1239–1249. doi: 10.1007/s00122-009-0977-6. PubMed DOI
Arnau, G. et al. Yams. In Root and Tuber Crops (ed. Bradshaw, J. E.) 127–148 (Springer New York, 2010).
Winch JE, Newhook FJ, Jackson GVH, Cole JS. Studies of Colletotrichum gloeosporioides disease on yam, Dioscorea alata, in Solomon Islands. Plant Pathol. 1984;33:467–477. doi: 10.1111/j.1365-3059.1984.tb02870.x. DOI
Nwankiti AO, Okpala EU, Odurukwe SO. Effect of planting dates on the incidence and severity of anthracnose/blotch disease complex of Dioscorea alata L., caused by Colletotrichum gloeosporioides Penz., and subsequent effects on the yield. Beitr. Trop. Landwirtsch. Veterinarmed. 1984;22:288–292.
Mignucci JS, Hepperly PR, Green J, Torres-López R, Figueroa LA. Yam protection II. Anthracnose, yield, and profit of monocultures and interplantings. J. Agric. Univ. Puerto Rico. 1988;72:179–189. doi: 10.46429/jaupr.v72i2.7836. DOI
Abang MM, Winter S, Mignouna HD, Green KR, Asiedu R. Molecular taxonomic, epidemiological and population genetic approaches to understanding yam anthracnose disease. Afr. J. Biotechnol. 2003;2:486–496. doi: 10.5897/AJB2003.000-1098. DOI
Egesi CN, Odu BO, Ogunyemi S, Asiedu R, Hughes J. Evaluation of water yam (Dioscorea alata L.) germplasm for reaction to yam anthracnose and virus diseases and their effect on yield. J. Phytopathol. 2007;155:536–543. doi: 10.1111/j.1439-0434.2007.01273.x. DOI
Lebot V, Abraham K, Kaoh J, Rogers C, Molisalé T. Development of anthracnose resistant hybrids of the Greater Yam (Dioscorea alata L.) and interspecific hybrids with D. nummularia Lam. Genet. Resour. Crop Evol. 2019;66:871–883. doi: 10.1007/s10722-019-00756-y. DOI
Sugihara, Y. et al. Genome analyses reveal the hybrid origin of the staple crop white Guinea yam (Dioscorea rotundata). Proc. Natl Acad. Sci. USA10.1073/pnas.2015830117 (2020). PubMed PMC
Cheng J, et al. The origin and evolution of the diosgenin biosynthetic pathway in yam. Plant Commun. 2021;2:100079. doi: 10.1016/j.xplc.2020.100079. PubMed DOI PMC
Mignouna H, et al. A genetic linkage map of water yam (Dioscorea alata L.) based on AFLP markers and QTL analysis for anthracnose resistance. Theor. Appl. Genet. 2002;105:726–735. doi: 10.1007/s00122-002-0912-6. PubMed DOI
Petro D, Onyeka TJ, Etienne S, Rubens S. An intraspecific genetic map of water yam (Dioscorea alata L.) based on AFLP markers and QTL analysis for anthracnose resistance. Euphytica. 2011;179:405–416. doi: 10.1007/s10681-010-0338-1. DOI
Bhattacharjee R, et al. An EST-SSR based genetic linkage map and identification of QTLs for anthracnose disease resistance in water yam (Dioscorea alata L.) PLoS ONE. 2018;13:e0197717. doi: 10.1371/journal.pone.0197717. PubMed DOI PMC
Cormier F, et al. A reference high-density genetic map of greater yam (Dioscorea alata L.) Theor. Appl. Genet. 2019;132:1733–1744. doi: 10.1007/s00122-019-03311-6. PubMed DOI PMC
Mignouna HD, Abang MM, Green KR, Asiedu R. Inheritance of resistance in water yam (Dioscorea alata) to anthracnose (Colletotrichum gloeosporioides) Theor. Appl. Genet. 2001;103:52–55. doi: 10.1007/s001220000531. DOI
Cowan CR, Carlton PM, Cande WZ. The polar arrangement of telomeres in interphase and meiosis. Rabl Organ. Bouquet Plant Physiol. 2001;125:532–538. PubMed PMC
Mascher M, et al. A chromosome conformation capture ordered sequence of the barley genome. Nature. 2017;544:427–433. doi: 10.1038/nature22043. PubMed DOI
Muller H, Gil J, Jr, Drinnenberg IA. The impact of centromeres on spatial genome architecture. Trends Genet. 2019;35:565–578. doi: 10.1016/j.tig.2019.05.003. PubMed DOI
Waterhouse RM, et al. BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol. Biol. Evol. 2018;35:543–548. doi: 10.1093/molbev/msx319. PubMed DOI PMC
Kriventseva EV, et al. OrthoDB v10: Sampling the diversity of animal, plant, fungal, protist, bacterial and viral genomes for evolutionary and functional annotations of orthologs. Nucleic Acids Res. 2019;47:D807–D811. doi: 10.1093/nar/gky1053. PubMed DOI PMC
Dong P, et al. 3D chromatin architecture of large plant genomes determined by local A/B compartments. Mol. Plant. 2017;10:1497–1509. doi: 10.1016/j.molp.2017.11.005. PubMed DOI
Siadjeu C, Pucker B, Viehöver P, Albach DC, Weisshaar B. High contiguity de novo genome sequence assembly of trifoliate yam (Dioscorea dumetorum) using long read sequencing. Genes. 2020;11:274. doi: 10.3390/genes11030274. PubMed DOI PMC
Chellappan BV, et al. High quality draft genome of Arogyapacha (Trichopus zeylanicus), an important medicinal plant endemic to western Ghats of India. G3 Genes Genomes Genet. 2019;9:2395–2404. PubMed PMC
Scarcelli N, Daïnou O, Agbangla C, Tostain S, Pham J-L. Segregation patterns of isozyme loci and microsatellite markers show the diploidy of African yam Dioscorea rotundata (2n = 40) Theor. Appl. Genet. 2005;111:226–232. doi: 10.1007/s00122-005-2003-y. PubMed DOI
Tamiru M, et al. Genome sequencing of the staple food crop white Guinea yam enables the development of a molecular marker for sex determination. BMC Biol. 2017;15:86. doi: 10.1186/s12915-017-0419-x. PubMed DOI PMC
Huang X, Guo H. Karyotype of different ploidy Dioscorea zingiberensis CH Wright. J. Trop. Subtrop. Bot. 2012;20:256–262.
Lamesch P, et al. The Arabidopsis Information Resource (TAIR): Improved gene annotation and new tools. Nucleic Acids Res. 2012;40:D1202–D1210. doi: 10.1093/nar/gkr1090. PubMed DOI PMC
Baquar SR. Chromosome behaviour in Nigerian yams (Dioscorea) Genetica. 1980;54:1–9. doi: 10.1007/BF00122401. DOI
One Thousand Plant Transcriptomes Initiative. One thousand plant transcriptomes and the phylogenomics of green plants. Nature574, 679–685 (2019). PubMed PMC
Ren R, et al. Widespread whole genome duplications contribute to genome complexity and species diversity in angiosperms. Mol. Plant. 2018;11:414–428. doi: 10.1016/j.molp.2018.01.002. PubMed DOI
Vanneste K, Baele G, Maere S, Van de Peer Y. Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous–Paleogene boundary. Genome Res. 2014;24:1334–1347. doi: 10.1101/gr.168997.113. PubMed DOI PMC
Schubert I, Lysak MA. Interpretation of karyotype evolution should consider chromosome structural constraints. Trends Genet. 2011;27:207–216. doi: 10.1016/j.tig.2011.03.004. PubMed DOI
Garsmeur O, et al. Two evolutionarily distinct classes of paleopolyploidy. Mol. Biol. Evol. 2014;31:448–454. doi: 10.1093/molbev/mst230. PubMed DOI
Shi T, et al. Distinct expression and methylation patterns for genes with different fates following a single whole-genome duplication in flowering plants. Mol. Biol. Evol. 2020;37:2394–2413. doi: 10.1093/molbev/msaa105. PubMed DOI PMC
Langham RJ, et al. Genomic duplication, fractionation and the origin of regulatory novelty. Genetics. 2004;166:935–945. doi: 10.1093/genetics/166.2.935. PubMed DOI PMC
Cheng F, et al. Gene retention, fractionation and subgenome differences in polyploid plants. Nat. Plants. 2018;4:258–268. doi: 10.1038/s41477-018-0136-7. PubMed DOI
Edger PP, McKain MR, Bird KA, VanBuren R. Subgenome assignment in allopolyploids: challenges and future directions. Curr. Opin. Plant Biol. 2018;42:76–80. doi: 10.1016/j.pbi.2018.03.006. PubMed DOI
Jiao Y, Li J, Tang H, Paterson AH. Integrated syntenic and phylogenomic analyses reveal an ancient genome duplication in monocots. Plant Cell. 2014;26:2792–2802. doi: 10.1105/tpc.114.127597. PubMed DOI PMC
Ming R, et al. The pineapple genome and the evolution of CAM photosynthesis. Nat. Genet. 2015;47:1435–1442. doi: 10.1038/ng.3435. PubMed DOI PMC
Singh R, et al. Oil palm genome sequence reveals divergence of interfertile species in Old and New worlds. Nature. 2013;500:335–339. doi: 10.1038/nature12309. PubMed DOI PMC
Harkess A, et al. The asparagus genome sheds light on the origin and evolution of a young Y chromosome. Nat. Commun. 2017;8:1279. doi: 10.1038/s41467-017-01064-8. PubMed DOI PMC
Wang W, et al. The Spirodela polyrhiza genome reveals insights into its neotenous reduction fast growth and aquatic lifestyle. Nat. Commun. 2014;5:3311. doi: 10.1038/ncomms4311. PubMed DOI PMC
Egesi CN, Onyeka TJ, Asiedu R. Severity of anthracnose and virus diseases of water yam (Dioscorea alata L.) In Nigeria I: effects of yam genotype and date of planting. Crop Prot. 2007;26:1259–1265. doi: 10.1016/j.cropro.2006.10.025. DOI
Ron M, Avni A. The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell. 2004;16:1604–1615. doi: 10.1105/tpc.022475. PubMed DOI PMC
Eulgem T, et al. EDM2 is required for RPP7-dependent disease resistance in Arabidopsis and affects RPP7 transcript levels. Plant J. 2007;49:829–839. doi: 10.1111/j.1365-313X.2006.02999.x. PubMed DOI
Tsuchiya T, Eulgem T. EMSY-like genes are required for full RPP7-mediated race-specific immunity and basal defense in Arabidopsis. Mol. Plant. Microbe Interact. 2011;24:1573–1581. doi: 10.1094/MPMI-05-11-0123. PubMed DOI
Song J, et al. Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. Proc. Natl Acad. Sci. USA. 2003;100:9128–9133. doi: 10.1073/pnas.1533501100. PubMed DOI PMC
Tang D, Ade J, Frye CA, Innes RW. Regulation of plant defense responses in Arabidopsis by EDR2, a PH and START domain-containing protein. Plant J. 2005;44:245–257. doi: 10.1111/j.1365-313X.2005.02523.x. PubMed DOI PMC
Vorwerk S, et al. EDR2 negatively regulates salicylic acid-based defenses and cell death during powdery mildew infections of Arabidopsis thaliana. BMC Plant Biol. 2007;7:35. doi: 10.1186/1471-2229-7-35. PubMed DOI PMC
Agre PA, et al. Identification of QTLs controlling resistance to anthracnose disease in water yam (Dioscorea alata) Genes. 2022;13:1–15. doi: 10.3390/genes13020347. PubMed DOI PMC
Martin FW, Ruberte R. Polyphenol of Dioscorea alata (yam) tubers associated with oxidative browning. J. Agric. Food Chem. 1976;24:67–70. doi: 10.1021/jf60203a039. DOI
Akissoe N, Mestres C, Hounhouigan J, Nago M. Biochemical origin of browning during the processing of fresh Yam (Dioscorea spp.) into dried product. J. Agric. Food Chem. 2005;53:2552–2557. doi: 10.1021/jf040265n. PubMed DOI
Jia G-L, Shi J-Y, Song Z-H, Li F-D. Prevention of enzymatic browning of Chinese yam (Dioscorea spp.) using electrolyzed oxidizing water. J. Food Sci. 2015;80:C718–C728. doi: 10.1111/1750-3841.12820. PubMed DOI
Goenaga RJ, Irizarry H. Accumulation and partitioning of dry matter in water yam. Agron. J. 1994;86:1083–1087. doi: 10.2134/agronj1994.00021962008600060029x. DOI
Gatarira C, et al. Genome-wide association analysis for tuber dry matter and oxidative browning in water yam (Dioscorea alata L.) Plants. 2020;9:969. doi: 10.3390/plants9080969. PubMed DOI PMC
Narina SS, et al. Generation and analysis of expressed sequence tags (ESTs) for marker development in yam (Dioscorea alata L.) BMC Genomics. 2011;12:100. doi: 10.1186/1471-2164-12-100. PubMed DOI PMC
Saski CA, Bhattacharjee R, Scheffler BE, Asiedu R. Genomic resources for water yam (Dioscorea alata L.): Analyses of EST-sequences, de novo sequencing and GBS libraries. PLoS ONE. 2015;10:e0134031. doi: 10.1371/journal.pone.0134031. PubMed DOI PMC
Bredeson JV, et al. Sequencing wild and cultivated cassava and related species reveals extensive interspecific hybridization and genetic diversity. Nat. Biotechnol. 2016;34:562–570. doi: 10.1038/nbt.3535. PubMed DOI
Wu GA, et al. Genomics of the origin and evolution of Citrus. Nature. 2018;554:311–316. doi: 10.1038/nature25447. PubMed DOI
Wolfe MD, et al. Historical introgressions from a wild relative of modern cassava improved important traits and may be under balancing selection. Genetics. 2019;213:1237–1253. doi: 10.1534/genetics.119.302757. PubMed DOI PMC
Sharif BM, et al. Genome-wide genotyping elucidates the geographical diversification and dispersal of the polyploid and clonally propagated yam (Dioscorea alata) Ann. Bot. 2020;126:1029–1038. doi: 10.1093/aob/mcaa122. PubMed DOI PMC
Alonge M, et al. Major impacts of widespread structural variation on gene expression and crop improvement in tomato. Cell. 2020;182:145–161.e23. doi: 10.1016/j.cell.2020.05.021. PubMed DOI PMC
Todesco, M. et al. Massive haplotypes underlie ecotypic differentiation in sunflowers. Nature10.1038/s41586-020-2467-6 (2020). PubMed
Ihediohanm NC, Onuegbu NC, Peter-Ikec AI, Ojimba NC. A comparative study and determination of Glycemic Indices of three yam cultivars (Dioscorea rotundata, Dioscorea alata and Dioscorea domentorum) Pak. J. Nutr. 2012;11:547–552. doi: 10.3923/pjn.2012.547.552. DOI
Oko AO, Famurewa AC. Estimation of nutritional and starch characteristics of Dioscorea alata (water yam) varieties commonly cultivated in the South-Eastern Nigeria. Br. J. Appl. Sci. Technol. 2014;6:145–152. doi: 10.9734/BJAST/2015/14095. DOI
Doležel J, Sgorbati S, Lucretti S. Comparison of three DNA fluorochromes for flow cytometric estimation of nuclear DNA content in plants. Physiol. Plant. 1992;85:625–631. doi: 10.1111/j.1399-3054.1992.tb04764.x. DOI
Lieberman-Aiden E, et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science. 2009;326:289–293. doi: 10.1126/science.1181369. PubMed DOI PMC
Koren S, et al. Canu: Scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 2017;27:722–736. doi: 10.1101/gr.215087.116. PubMed DOI PMC
Durand NC, et al. Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Syst. 2016;3:99–101. doi: 10.1016/j.cels.2015.07.012. PubMed DOI PMC
Dudchenko, O., Shamim, M. S., Batra, S. S. & Durand, N. C. The Juicebox Assembly Tools module facilitates de novo assembly of mammalian genomes with chromosome-length scaffolds for under $1000. Biorxiv. https://www.biorxiv.org/content/10.1101/254797v1 (2018). DOI
Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics. 2011;27:578–579. doi: 10.1093/bioinformatics/btq683. PubMed DOI
Dudchenko O, et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science. 2017;356:92–95. doi: 10.1126/science.aal3327. PubMed DOI PMC
Chin C-S, et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods. 2013;10:563–569. doi: 10.1038/nmeth.2474. PubMed DOI
Garrison, E. & Marth, G. Haplotype-based variant detection from short-read sequencing. arXiv. https://arxiv.org/abs/1207.3907 (2012).
Bredeson, J. V. et al. Chromosome evolution and the genetic basis of agronomically important traits in greater yam. Dryad. Dataset. 10.6078/D1DQ54 (2021). PubMed PMC
International Cassava Genetic Map Consortium (ICGMC High-resolution linkage map and chromosome-scale genome assembly for cassava (Manihot esculenta Crantz) from 10 populations. G3 Genes Genomes Genet. 2015;5:133–144. PubMed PMC
Danecek P, et al. The Variant Call Format and VCFtools. Bioinformatics. 2011;27:2156–2158. doi: 10.1093/bioinformatics/btr330. PubMed DOI PMC
Whalen, A., Gorjanc, G. & Hickey, J. M. AlphaFamImpute: High accuracy imputation in full-sib families from genotype-by-sequencing data. Bioinformatics10.1093/bioinformatics/btaa499 (2020). PubMed PMC
Van Ooijen, J. W. JoinMap 4: Software for the calculation of genetic linkage maps in experimental populations of diploid species (Plant Research International BV and Kayazma BV, 2006).
Van Ooijen JW. Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet. Res. 2011;93:343–349. doi: 10.1017/S0016672311000279. PubMed DOI
Endelman JB, Plomion C. LPmerge: An R package for merging genetic maps by linear programming. Bioinformatics. 2014;30:1623–1624. doi: 10.1093/bioinformatics/btu091. PubMed DOI
Parker MT, et al. Nanopore direct RNA sequencing maps the complexity of Arabidopsis mRNA processing and m6A modification. Elife. 2020;9:e49658. doi: 10.7554/eLife.49658. PubMed DOI PMC
Hackl T, Hedrich R, Schultz J, Förster F. proovread: Large-scale high-accuracy PacBio correction through iterative short read consensus. Bioinformatics. 2014;30:3004–3011. doi: 10.1093/bioinformatics/btu392. PubMed DOI PMC
Li H. Minimap2: Pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34:3094–3100. doi: 10.1093/bioinformatics/bty191. PubMed DOI PMC
Lovell JT, et al. The genomic landscape of molecular responses to natural drought stress in Panicum hallii. Nat. Commun. 2018;9:5213. doi: 10.1038/s41467-018-07669-x. PubMed DOI PMC
Wu Z-G, et al. Transciptome analysis reveals flavonoid biosynthesis regulation and simple sequence repeats in yam (Dioscorea alata L.) tubers. BMC Genomics. 2015;16:346. doi: 10.1186/s12864-015-1547-8. PubMed DOI PMC
Sarah G, et al. A large set of 26 new reference transcriptomes dedicated to comparative population genomics in crops and wild relatives. Mol. Ecol. Resour. 2017;17:565–580. doi: 10.1111/1755-0998.12587. PubMed DOI
Haas BJ, et al. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 2003;31:5654–5666. doi: 10.1093/nar/gkg770. PubMed DOI PMC
Shu, S., Rokhsar, D., Goodstein, D., Hayes, D. & Mitros, T. JGI Plant Genomics Gene Annotation Pipeline. https://www.osti.gov/biblio/1241222 (2014).
Slater GSC, Birney E. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics. 2005;6:31. doi: 10.1186/1471-2105-6-31. PubMed DOI PMC
Schmutz J, et al. Genome sequence of the palaeopolyploid soybean. Nature. 2010;463:178–183. doi: 10.1038/nature08670. PubMed DOI
McCormick RF, et al. The Sorghum bicolor reference genome: Improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization. Plant J. 2018;93:338–354. doi: 10.1111/tpj.13781. PubMed DOI
Ouyang S, et al. The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res. 2007;35:D883–D887. doi: 10.1093/nar/gkl976. PubMed DOI PMC
Mamidi S, et al. A genome resource for green millet Setaria viridis enables discovery of agronomically valuable loci. Nat. Biotechnol. 2020;38:1203–1210. doi: 10.1038/s41587-020-0681-2. PubMed DOI PMC
Amborella Genome Project. The Amborella genome and the evolution of flowering plants. Science. 2013;342:1241089. doi: 10.1126/science.1241089. PubMed DOI
Olsen JL, et al. The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature. 2016;530:331–335. doi: 10.1038/nature16548. PubMed DOI
D’Hont A, et al. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature. 2012;488:213–217. doi: 10.1038/nature11241. PubMed DOI
The French–Italian Public Consortium for Grapevine Genome Characterization. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature. 2007;449:463–467. doi: 10.1038/nature06148. PubMed DOI
Goodstein DM, et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2012;40:D1178–D1186. doi: 10.1093/nar/gkr944. PubMed DOI PMC
UniProt Consortium, T. UniProt: The universal protein knowledgebase. Nucleic Acids Res. 2018;46:2699. doi: 10.1093/nar/gky092. PubMed DOI PMC
Salamov AA, Solovyev VV. Ab initio gene finding in Drosophila genomic DNA. Genome Res. 2000;10:516–522. doi: 10.1101/gr.10.4.516. PubMed DOI PMC
Hoff KJ, Lange S, Lomsadze A, Borodovsky M, Stanke M. BRAKER1: Unsupervised RNA-seq-based genome annotation with GeneMark-ET and AUGUSTUS. Bioinformatics. 2016;32:767–769. doi: 10.1093/bioinformatics/btv661. PubMed DOI PMC
Jones P, et al. InterProScan 5: Genome-scale protein function classification. Bioinformatics. 2014;30:1236–1240. doi: 10.1093/bioinformatics/btu031. PubMed DOI PMC
Smit, A. F. A., Hubley, R. & Green, P. RepeatMasker Open-4.0. https://www.repeatmasker.org/ (2013–2015).
Smit, A. F. A. & Hubley, R. RepeatModeler Open-1.0. https://www.repeatmasker.org/ (2008–2015).
Bao W, Kojima KK, Kohany O. Repbase Update, a database of repetitive elements in eukaryotic genomes. Mob. DNA. 2015;6:11. doi: 10.1186/s13100-015-0041-9. PubMed DOI PMC
Emms DM, Kelly S. OrthoFinder: Phylogenetic orthology inference for comparative genomics. Genome Biol. 2019;20:238. doi: 10.1186/s13059-019-1832-y. PubMed DOI PMC
Costa M-CD, et al. A footprint of desiccation tolerance in the genome of Xerophyta viscosa. Nat. Plants. 2017;3:17038. doi: 10.1038/nplants.2017.38. PubMed DOI
Zhang G-Q, et al. The Apostasia genome and the evolution of orchids. Nature. 2017;549:379–383. doi: 10.1038/nature23897. PubMed DOI PMC
Zhang G-Q, et al. The Dendrobium catenatum Lindl. genome sequence provides insights into polysaccharide synthase, floral development and adaptive evolution. Sci. Rep. 2016;6:19029. doi: 10.1038/srep19029. PubMed DOI PMC
Al-Mssallem IS, et al. Genome sequence of the date palm Phoenix dactylifera L. Nat. Commun. 2013;4:2274. doi: 10.1038/ncomms3274. PubMed DOI PMC
Kawahara Y, et al. Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice. 2013;6:4. doi: 10.1186/1939-8433-6-4. PubMed DOI PMC
Jiao Y, et al. Improved maize reference genome with single-molecule technologies. Nature. 2017;546:524–527. doi: 10.1038/nature22971. PubMed DOI PMC
Michael TP, et al. Comprehensive definition of genome features in Spirodela polyrhiza by high-depth physical mapping and short-read DNA sequencing strategies. Plant J. 2017;89:617–635. doi: 10.1111/tpj.13400. PubMed DOI
Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000;408:796–815. doi: 10.1038/35048692. PubMed DOI
Xu L, et al. OrthoVenn2: A web server for whole-genome comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res. 2019;47:W52–W58. doi: 10.1093/nar/gkz333. PubMed DOI PMC
Varoquaux N, et al. Accurate identification of centromere locations in yeast genomes using Hi-C. Nucleic Acids Res. 2015;43:5331–5339. doi: 10.1093/nar/gkv424. PubMed DOI PMC
R Core Team. R: A language and environment for statistical computing. (Foundation for Statistical Computing, 2013).
Quinlan AR. BEDTools: The Swiss-army tool for genome feature analysis. Curr. Protoc. Bioinformatics. 2014;47:11.12.1–34. doi: 10.1002/0471250953.bi1112s47. PubMed DOI PMC
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J. Mol. Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI
Camacho C, et al. BLAST+: Architecture and applications. BMC Bioinformatics. 2009;10:421. doi: 10.1186/1471-2105-10-421. PubMed DOI PMC
Subramanian AR, Kaufmann M, Morgenstern B. DIALIGN-TX: Greedy and progressive approaches for segment-based multiple sequence alignment. Algorithms Mol. Biol. 2008;3:6. doi: 10.1186/1748-7188-3-6. PubMed DOI PMC
Charif, D. & Lobry, J. R. In Structural Approaches to Sequence Evolution: Molecules, Networks, Populations (eds. Bastolla, U., Porto, M., Roman, H. E. & Vendruscolo, M.) 207–232 (Springer Berlin Heidelberg, 2007).
Tang H, et al. Synteny and collinearity in plant genomes. Science. 2008;320:486–488. doi: 10.1126/science.1153917. PubMed DOI
Asfaw, A. Standard operating protocol for yam variety performance evaluation trial. Vol. 27 (IITA, Ibadan, Nigeria, 2016).
Green KR, Abang MM, Iloba C. A rapid bioassay for screening yam germplasm for response to anthracnose. Tropical Sci. 2000;40:132–138.
Nwadili CO, et al. Comparative reliability of screening parameters for anthracnose resistance in water yam (Dioscorea alata) Plant Dis. 2017;101:209–216. doi: 10.1094/PDIS-06-16-0924-RE. PubMed DOI
Tenorio Cavalcante PM, et al. The influence of microstructure on the performance of white porcelain stoneware. Ceram. Int. 2004;30:953–963. doi: 10.1016/j.ceramint.2003.11.002. DOI
Purcell S, et al. PLINK: A tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 2007;81:559–575. doi: 10.1086/519795. PubMed DOI PMC
Chang CC, et al. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience. 2015;4:7. doi: 10.1186/s13742-015-0047-8. PubMed DOI PMC
Browning BL. PRESTO: Rapid calculation of order statistic distributions and multiple-testing adjusted P-values via permutation for one and two-stage genetic association studies. BMC Bioinformatics. 2008;9:309. doi: 10.1186/1471-2105-9-309. PubMed DOI PMC
Broman, K. W. & Sen, S. A Guide to QTL mapping with R/qtl. Stat. Biol. Health10.1007/978-0-387-92125-9 (2009).
Aronesty E. Comparison of sequencing utility programs. The Open Bioinformatics Journal. 2013;7:1–8. doi: 10.2174/1875036201307010001. DOI
Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXivhttps://arxiv.org/abs/1303.3997 (2013).
Li H, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078–2079. doi: 10.1093/bioinformatics/btp352. PubMed DOI PMC
Poplin, R. et al. Scaling accurate genetic variant discovery to tens of thousands of samples. Cold Spring Harb. Lab.10.1101/201178 (2017).
Cingolani P, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly. 2012;6:80–92. doi: 10.4161/fly.19695. PubMed DOI PMC
Katoh K, Misawa K, Kuma K-I, Miyata T. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30:3059–3066. doi: 10.1093/nar/gkf436. PubMed DOI PMC
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC
Guindon S, et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010;59:307–321. doi: 10.1093/sysbio/syq010. PubMed DOI
Emms DM, Kelly S. STRIDE: Species Tree Root Inference from Gene Duplication Events. Mol. Biol. Evol. 2017;34:3267–3278. doi: 10.1093/molbev/msx259. PubMed DOI PMC
Emms, D. M. & Kelly, S. STAG: Species Tree Inference from All Genes. Cold Spring Harb. Lab.10.1101/267914 (2018).
Minh BQ, et al. IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 2020;37:1530–1534. doi: 10.1093/molbev/msaa015. PubMed DOI PMC
Rao SSP, et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell. 2014;159:1665–1680. doi: 10.1016/j.cell.2014.11.021. PubMed DOI PMC