[en] BACKGROUND: Cassava is an important food crop in tropical and sub-tropical regions worldwide. In Africa, cassava production is widely affected by cassava mosaic disease (CMD), which is caused by the African cassava mosaic geminivirus that is transmitted by whiteflies. Cassava breeders often use a single locus, CMD2, for introducing CMD resistance into susceptible cultivars. The CMD2 locus has been genetically mapped to a 10-Mbp region, but its organization and genes as well as their functions are unknown. RESULTS: We report haplotype-resolved de novo assemblies and annotations of the genomes for the African cassava cultivar TME (tropical Manihot esculenta), which is the origin of CMD2, and the CMD-susceptible cultivar 60444. The assemblies provide phased haplotype information for over 80% of the genomes. Haplotype comparison identified novel features previously hidden in collapsed and fragmented cassava genomes, including thousands of allelic variants, inter-haplotype diversity in coding regions, and patterns of diversification through allele-specific expression. Reconstruction of the CMD2 locus revealed a highly complex region with nearly identical gene sets but limited microsynteny between the two cultivars. CONCLUSIONS: The genome maps of the CMD2 locus in both 60444 and TME3, together with the newly annotated genes, will help the identification of the causal genetic basis of CMD2 resistance to geminiviruses. Our de novo cassava genome assemblies will also facilitate genetic mapping approaches to narrow the large CMD2 region to a few candidate genes for better informed strategies to develop robust geminivirus resistance in susceptible cassava cultivars.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Kuon, Joel-E.
Qi, Weihong
Schläpfer, Pascal
Hirsch-Hoffmann, Matthias
von Bieberstein, Philipp Rogalla
Patrignani, Andrea
Poveda, Lucy
Grob, Stefan
Keller, Miyako
Shimizu-Inatsugi, Rie
Grossniklaus, Ueli
Vanderschuren, Hervé ; Université de Liège - ULiège > Département GxABT > Plant Sciences
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Bibliography
Parmar A, Sturm B, Hensel O. Crops that feed the world: production and improvement of cassava for food, feed, and industrial uses. Food Secur. 2017;9:907-27.
Balat M, Balat H. Recent trends in global production and utilization of bio-ethanol fuel. Appl Energy. 2009;86:2273-82.
Ceballos H, Iglesias CA, Pérez JC, Dixon AGO. Cassava breeding: opportunities and challenges. Plant Mol Biol. 2004;56:503-16.
Ceballos H, Pérez JC, Joaqui Barandica O, Lenis JI, Morante N, Calle F, et al. Cassava breeding I: the value of breeding value. Front Plant Sci. 2016;7:1-12.
Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S. Geminiviruses: masters at redirecting and reprogramming plant processes. Nat Rev Microbiol. 2013;11:777-88.
McCallum EJ, Anjanappa RB, Gruissem W. Tackling agriculturally relevant diseases in the staple crop cassava (Manihot esculenta). Curr Opin Plant Biol. 2017;38:50-8.
Legg JP, Thresh JM. Cassava mosaic virus disease in East Africa: a dynamic disease in a changing environment. Virus Res. 2000;71:135-49.
Legg JP, Owor B, Sseruwagi P, Ndunguru J. Cassava mosaic virus disease in east and central Africa: epidemiology and management of a regional pandemic. Adv Virus Res. 2006;67:355-418.
Rey C, Vanderschuren H. Cassava mosaic and brown streak diseases: current perspectives and beyond. Annu Rev Virol. 2017;4:429-52.
de Ronde D, Butterbach P, Kormelink R. Dominant resistance against plant viruses. Front Plant Sci. 2014;5:307.
Lapidot M, Karniel U, Gelbart D, Fogel D, Evenor D, Kutsher Y, et al. A novel route controlling begomovirus resistance by the messenger RNA surveillance factor pelota. PLoS Genet. 2015;11:1-19.
Verlaan MG, Hutton SF, Ibrahem RM, Kormelink R, Visser RGF, Scott JW, et al. The tomato yellow leaf curl virus resistance genes Ty-1 and Ty-3 are allelic and code for DFDGD-class RNA-dependent RNA polymerases. PLoS Genet. 2013;9:e1003399.
Yamaguchi H, Ohnishi J, Saito A, Ohyama A, Nunome T, Miyatake K, et al. An NB-LRR gene, TYNBS1, is responsible for resistance mediated by the Ty-2 Begomovirus resistance locus of tomato. Theor Appl Genet. 2018;131:1345-62.
Okogbenin E, Egesi CN, Olasanmi B, Ogundapo O, Kahya S, Hurtado P, et al. Molecular marker analysis and validation of resistance to cassava mosaic disease in elite cassava genotypes in Nigeria. Crop Sci. 2012;52:2576-86.
Akano O, Dixon O, Barrera E, Fregene M. Genetic mapping of a dominant gene conferring resistance to cassava mosaic disease. Tag Theor Appl Genet Theor Und Angew Genet. 2002;105:521-5.
Rabbi IY, Hamblin MT, Kumar PL, Gedil M a., Ikpan AS, Jannink JL, et al. High-resolution mapping of resistance to cassava mosaic geminiviruses in cassava using genotyping-by-sequencing and its implications for breeding. Virus Res 2014;186:87-96.
Fondong VN. The search for resistance to cassava mosaic geminiviruses: how much we have accomplished, and what lies ahead. Front Plant Sci. 2017;8:1-19.
Beyene G, Chauhan RD, Wagaba H, Moll T, Alicai T, Miano D, et al. Loss of CMD2-mediated resistance to cassava mosaic disease in plants regenerated through somatic embryogenesis. Mol Plant Pathol. 2016;17:1095-110.
Bredeson JV, Lyons JB, Prochnik SE, Wu GA, Ha CM, Edsinger-Gonzales E, et al. Sequencing wild and cultivated cassava and related species reveals extensive interspecific hybridization and genetic diversity. Nat Biotechnol. 2016;34:562-70.
Wang W, Feng B, Xiao J, Xia Z, Zhou X, Li P, et al. Cassava genome from a wild ancestor to cultivated varieties. Nat Commun. 2014;5:5110.
Prochnik S, Marri PR, Desany B, Rabinowicz PD, Kodira C, Mohiuddin M, et al. The cassava genome: current progress, future directions. Trop Plant Biol. 2012;5:88-94.
Wolfe MD, Rabbi IY, Egesi C, Hamblin M, Kawuki R, Kulakow P, et al. Genome-wide association and prediction reveals the genetic architecture of cassava mosaic disease resistance and prospects for rapid genetic improvement. Plant Genome. 2016;9:1-13.
Kayondo SI, Del Carpio DP, Lozano R, Ozimati A, Wolfe M, Baguma Y, et al. Genome-wide association mapping and genomic prediction for CBSD resistance in Manihot esculenta. Sci Rep. 2018;8:1-11.
Masumba EA, Kapinga F, Mkamilo G, Salum K, Kulembeka H, Rounsley S, et al. QTL associated with resistance to cassava brown streak and cassava mosaic diseases in a bi-parental cross of two Tanzanian farmer varieties, Namikonga and Albert. Theor Appl Genet. 2017;130:2069-90.
Wilson MC, Mutka AM, Hummel AW, Berry J, Chauhan RD, Vijayaraghavan A, et al. Gene expression atlas for the food security crop cassava. New Phytol. 2017;213:1632-41.
Amuge T, Berger DK, Katari MS, Myburg AA, Goldman SL, Ferguson ME. A time series transcriptome analysis of cassava (Manihot esculenta Crantz) varieties challenged with Ugandan cassava brown streak virus. Sci Rep. 2017;7:1-21.
Wang H, Beyene G, Zhai J, Feng S, Fahlgren N, Taylor NJ, et al. CG gene body DNA methylation changes and evolution of duplicated genes in cassava. Proc Natl Acad Sci. 2015;112:13729-34.
Sedlazeck FJ, Lee H, Darby CA, Schatz MC. Piercing the dark matter: bioinformatics of long-range sequencing and mapping. Nat Rev Genet. 2018;19:329-46.
Staňková H, Hastie AR, Chan S, Vrána J, Tulpová Z, Kubaláková M, et al. BioNano genome mapping of individual chromosomes supports physical mapping and sequence assembly in complex plant genomes. Plant Biotechnol J. 2016;14:1523-31.
Bickhart DM, Rosen BD, Koren S, Sayre BL, Hastie AR, Chan S, et al. Single-molecule sequencing and chromatin conformation capture enable de novo reference assembly of the domestic goat genome. Nat Genet. 2017;49:643-50.
Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science. 2009;326:289-93.
(ICGMC) ICGMC. High-resolution linkage map and chromosome-scale genome assembly for cassava (Manihot esculenta Crantz) from ten populations. G3. 2015;5:133-44.
Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH, Phillippy AM. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 2017;27:722-36.
Chin C-S, Peluso P, Sedlazeck FJ, Nattestad M, Concepcion GT, Clum A, et al. Phased diploid genome assembly with single-molecule real-time sequencing. Nat Methods. 2016;13:1050.
Berlin K, Koren S, Chin C-S, Drake JP, Landolin JM, Phillippy AM. Assembling large genomes with single-molecule sequencing and locality-sensitive hashing. Nat Biotechnol. 2015;33:623-30.
Small KS, Brudno M, Hill MM, Sidow A. A haplome alignment and reference sequence of the highly polymorphic Ciona savignyi genome. Genome Biol. 2007;8:R41.
Vinson JP, Jaffe DB, O'Neill K, Karlsson EK, Stange-Thomann N, Anderson S, et al. Assembly of polymorphic genomes: algorithms and application to Ciona savignyi. Genome Res. 2005;15:1127-35.
Roach MJ, Schmidt SA, Borneman AR. Purge Haplotigs: allelic contig reassignment for third-gen diploid genome assemblies. BMC Bioinformatics. 2018;19:460.
Rival L, McKey D. Domestication and diversity in Manioc (Manihot esculenta Crantz ssp. esculenta, Euphorbiaceae). Curr Anthropol. 2008;49:1119-28.
Lam ET, Hastie A, Lin C, Ehrlich D, Das SK, Austin MD, et al. Genome mapping on nanochannel arrays for structural variation analysis and sequence assembly. Nat Biotechnol. 2012;30:771-6.
Wolfe MD, Kulakow P, Rabbi IY, Jannink J-L. Marker-based estimates reveal significant non-additive effects in clonally propagated cassava (Manihot esculenta): implications for the prediction of total genetic value and the selection of varieties. G3. 2016;6:3497-506.
Wu TD, Watanabe CK. GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics. 2005;21:1859-75.
Rojas MC, Pérez JC, Ceballos H, Baena D, Morante N, Calle F. Analysis of inbreeding depression in eight S1 cassava families. Crop Sci. 2009;49:543-8.
Ramu P, Esuma W, Kawuki R, Rabbi IY, Egesi C, Bredeson JV, et al. Cassava haplotype map highlights fixation of deleterious mutations during clonal propagation. Nat Genet. 2017;49:1-7.
Sémon M, Wolfe KH. Consequences of genome duplication. Curr Opin Genet Dev. 2007;17:505-12.
Reyes-Chin-Wo S, Wang Z, Yang X, Kozik A, Arikit S, Song C, et al. Genome assembly with in vitro proximity ligation data and whole-genome triplication in lettuce. Nat Commun. 2017;8:14953.
Edger PP, Poorten TJ, VanBuren R, Hardigan MA, Colle M, McKain MR, et al. Origin and evolution of the octoploid strawberry genome. Nat Genet. 2019;51:541-7.
Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet. 2007;8:272-85.
VanBuren R, Bryant D, Edger PP, Tang H, Burgess D, Challabathula D, et al. Single-molecule sequencing of the desiccation-tolerant grass Oropetium thomaeum. Nature. 2015;527:508-11.
Daccord N, Celton J-M, Linsmith G, Becker C, Choisne N, Schijlen E, et al. High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat Genet. 2017;49:1099-106.
Mascher M, Gundlach H, Himmelbach A, Beier S, Twardziok SO, Wicker T, et al. A chromosome conformation capture ordered sequence of the barley genome. Nature. 2017;544:1-43.
Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, et al. The Sorghum bicolor genome and the diversification of grasses. Nature. 2009;457:551-6.
Jarvis DE, Ho YS, Lightfoot DJ, Schmöckel SM, Li B, Borm TJA, et al. The genome of Chenopodium quinoa. Nature. 2017;542:1-6.
Li L, Stoeckert CJJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003;13:2178-89.
Schläpfer P, Zhang P, Wang C, Kim T, Banf M, Chae L, et al. Genome-wide prediction of metabolic enzymes, pathways, and gene clusters in plants. Plant Physiol. 2017;173:2041-59.
Gene Ontology Consortium. The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res. 2004;32:258D-261.
Chen G, Pan H, Xie W, Wang S, Wu Q, Fang Y, et al. Virus infection of a weed increases vector attraction to and vector fitness on the weed. Sci Rep. 2013;3:1-6.
Kong L, Li S, Liao Q, Zhang Y, Sun R, Zhu X, et al. Oleanolic acid and ursolic acid: novel hepatitis C virus antivirals that inhibit NS5B activity. Antivir Res. 2013;98:44-53.
Ashour A, El-Sharkawy S, Amer M, Abdel Bar F, Katakura Y, Miyamoto T, et al. Rational design and synthesis of topoisomerase i and II inhibitors based on oleanolic acid moiety for new anti-cancer drugs. Bioorganic Med Chem. 2014;22:211-20.
Patil BL, Fauquet CM. Cassava mosaic geminiviruses: actual knowledge and perspectives. Mol Plant Pathol. 2009;10:685-701.
Pant V, Gupta D, Choudhury NR, Malathi VG, Varma A, Mukherjee SK. Molecular characterization of the Rep protein of the blackgram isolate of Indian mungbean yellow mosaic virus. J Gen Virol. 2001;82:2559-67.
Bull SE, Briddon RW, Sserubombwe WS, Ngugi K, Markham PG, Stanley J, et al. Genetic diversity and phylogeography of cassava mosaic viruses in Kenya. J Gen Virol. 2006;87:3053-65.
Almagro L, Gómez Ros LV, Belchi-Navarro S, Bru R, Ros Barceló A, Pedreño MA. Class III peroxidases in plant defence reactions. J Exp Bot. 2009;60:377-90.
Dieng H, Satho T, Hassan AA, Aziz AT, Morales RE, Hamid SA, et al. Peroxidase activity after viral infection and whitefly infestation in juvenile and mature leaves of Solanum lycopersicum. J Phytopathol. 2011;159:707-12.
Yang P, Lüpken T, Habekuss A, Hensel G, Steuernagel B, Kilian B, et al. PROTEIN DISULFIDE ISOMERASE LIKE 5-1 is a susceptibility factor to plant viruses. Proc Natl Acad Sci USA. 2014;111:2104-9.
Mourrain P, Béclin C, Elmayan T, Feuerbach F, Godon C, Morel J-B, et al. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell. 2000;101:533-42.
Maine EM. A conserved mechanism for post-transcriptional gene silencing? Genome Biol. 2000;1:1018.1-4.
Glick E, Zrachya A, Levy Y, Mett A, Gidoni D, Belausov E, et al. Interaction with host SGS3 is required for suppression of RNA silencing by tomato yellow leaf curl virus V2 protein. Proc Natl Acad Sci USA. 2009;106:4571.
Horvath P, Barrangou R, Horvath P, Barrangou R. CRISPR/Cas, the immune system of bacteria and archaea. Source Sci New Ser. 2010;327:167-70.
Doyle JJ, Doyle JL. A rapid total DNA preparation procedure for fresh plant tissue. Focus (Madison). 1990;12:13-5.
Pendleton M, Sebra R, Pang AWC, Ummat A, Franzen O, Rausch T, et al. Assembly and diploid architecture of an individual human genome via single-molecule technologies. Nat Methods. 2015;12:780-6.
Chin C, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods. 2013;10:563-9.
Grob S, Grossniklaus U. Chromatin conformation capture-based analysis of nuclear architecture. In: Kovalchuk I, editor. Plant epigenetics: methods and protocols. Boston: Springer US; 2017. p. 15-32.
DOE-Joint Genome Institute. cassava WGS sequencing.2015. https://www.ncbi.nlm.nih.gov/sra/?term=SRX526747
Bolger AM, Lohse M, Usadel B. Genome analysis Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114-20.
Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:1754-60.
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078-9.
Okonechnikov K, Conesa A, Garcl F. Genome analysis Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data. Bioinformatics. 2015;2016(32):292-4.
Stanke M, Diekhans M, Baertsch R, Haussler D. Sequence analysis using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics. 2008;24:637-44.
Conesa A, Götz S, García-gómez JM, Terol J, Talón M, Genómica D, et al. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21:3674-6.
Lowe TM, Chan PP. tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res. 2016;44:54-7.
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15-21.
Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792-7.
Škuta C, Bartu°něk P, Svozil D. InCHlib-interactive cluster heatmap for web applications. J Cheminform. 2014;44:1-9.
Yuan Y, Bayer PE, Lee H, Edwards D. Sequence analysis runBNG: a software package for BioNano genomic analysis on the command line. Bioinformatics. 2017:1-3.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403-10.
Gentleman R, Carey V, Bates D, Bolstad B, Dettling M, Dudoit S, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004;5:R80.
Supek F, Bošnjak M, Škunca N, Šmuc T. Revigo summarizes and visualizes long lists of gene ontology terms. PLoS One. 2011;6.
Functional Genomics. Center Zurich. Cassava genomes assembled with single-molecule long reads, optical and Hi-C maps reveal narrow genetic diversity and mono-allelic expression. 2018. https://www.ncbi.nlm.nih.gov/bioproject/PRJEB27129
Kuon JE, Qi W, and Gruissem W. Cassava genomes assembled with single-molecule long reads, optical and Hi-C maps. 2018. https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA508471
DOE-Joint Genome Institute. cassava WGS sequencing.2015. https://www.ncbi.nlm.nih.gov/sra/?term=SRX1393211
Similar publications
Sorry the service is unavailable at the moment. Please try again later.
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.