{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T06:42:39Z","timestamp":1792651359723,"version":"4.5.0"},"reference-count":40,"publisher":"Oxford University Press (OUP)","issue":"7","license":[{"start":{"date-parts":[[2017,7,1]],"date-time":"2017-07-01T00:00:00Z","timestamp":1498867200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2017,7,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>The aquatic planorbid snail Biomphalaria glabrata is one of the most intensively-studied mollusks due to its role in the transmission of schistosomiasis. Its 916 Mb genome has recently been sequenced and annotated, but it remains poorly assembled. Here, we used targeted capture markers to map over 10,000 B. glabrata scaffolds in a linkage cross of 94 F1 offspring, generating 24 linkage groups (LGs). We added additional scaffolds to these LGs based on linkage disequilibrium (LD) analysis of targeted capture and whole-genome sequences of 96 unrelated snails. Our final linkage map consists of 18,613 scaffolds comprising 515 Mb, representing 56% of the genome and 75% of genic and nonrepetitive regions. There are 18 large (&amp;gt; 10 Mb) LGs, likely representing the expected 18 haploid chromosomes, and &amp;gt; 50% of the genome has been assigned to LGs of at least 17 Mb. Comparisons with other gastropod genomes reveal patterns of synteny and chromosomal rearrangements. Linkage relationships of key immune-relevant genes may help clarify snail\u2013schistosome interactions. By focusing on linkage among genic and nonrepetitive regions, we have generated a useful resource for associating snail phenotypes with causal genes, even in the absence of a complete genome assembly. A similar approach could potentially improve numerous poorly-assembled genomes in other taxa. This map will facilitate future work on this host of a serious human parasite.<\/jats:p>","DOI":"10.1534\/g3.117.041319","type":"journal-article","created":{"date-parts":[[2017,5,20]],"date-time":"2017-05-20T01:00:29Z","timestamp":1495242029000},"page":"2353-2361","source":"Crossref","is-referenced-by-count":20,"title":["A Targeted Capture Linkage Map Anchors the Genome of the Schistosomiasis Vector Snail, <i>Biomphalaria glabrata<\/i>"],"prefix":"10.1093","volume":"7","author":[{"given":"Jacob A","family":"Tennessen","sequence":"first","affiliation":[{"name":"Department of Integrative Biology, Oregon State University, Corvallis, Oregon 97331"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephanie R","family":"Bollmann","sequence":"additional","affiliation":[{"name":"Department of Integrative Biology, Oregon State University, Corvallis, Oregon 97331"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael S","family":"Blouin","sequence":"additional","affiliation":[{"name":"Department of Integrative Biology, Oregon State University, Corvallis, Oregon 97331"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2017,7,1]]},"reference":[{"key":"2021042013014636200_bib1","doi-asserted-by":"crossref","first-page":"15451","DOI":"10.1038\/ncomms15451","article-title":"Whole genome analysis of a schistosomiasis-transmitting freshwater snail.","volume":"8","author":"Adema","year":"2017","journal-title":"Nat. Commun."},{"key":"2021042013014636200_bib2","doi-asserted-by":"crossref","first-page":"e0005362","DOI":"10.1371\/journal.pntd.0005362","article-title":"Schistosome infectivity in the snail, Biomphalaria glabrata, is partially dependent on the expression of Grctm6, a Guadeloupe Resistance Complex protein.","volume":"11","author":"Allan","year":"2017","journal-title":"PLoS Negl. Trop. Dis."},{"key":"2021042013014636200_bib3","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.cbpb.2015.04.011","article-title":"p63 gene structure in the phylum mollusca.","volume":"186","author":"Bari\u010devi\u0107","year":"2015","journal-title":"Comp. Biochem. Physiol. B Biochem. Mol. Biol."},{"key":"2021042013014636200_bib4","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.molbiopara.2009.01.005","article-title":"Successful parasitism of vector snail Biomphalaria glabrata by the human blood fluke (trematode) Schistosoma mansoni: a 2009 assessment.","volume":"165","author":"Bayne","year":"2009","journal-title":"Mol. Biochem. Parasitol."},{"key":"2021042013014636200_bib5","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1016\/j.ymeth.2012.05.001","article-title":"Hi-C: a comprehensive technique to capture the conformation of genomes.","volume":"58","author":"Belton","year":"2012","journal-title":"Methods"},{"key":"2021042013014636200_bib6","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.ijpara.2012.10.020","article-title":"Three genes involved in the oxidative burst are closely linked in the genome of the snail, Biomphalaria glabrata.","volume":"43","author":"Blouin","year":"2013","journal-title":"Int. J. Parasitol."},{"key":"2021042013014636200_bib7","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: a flexible trimmer for Illumina sequence data.","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"2021042013014636200_bib8","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1186\/1471-2164-15-617","article-title":"Efficient linkage mapping using exome capture and extreme QTL in schistosome parasites.","volume":"15","author":"Chevalier","year":"2014","journal-title":"BMC Genomics"},{"key":"2021042013014636200_bib9","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.tree.2013.09.008","article-title":"Genome sequencing and population genomics in non-model organisms.","volume":"29","author":"Ellegren","year":"2014","journal-title":"Trends Ecol. Evol."},{"key":"2021042013014636200_bib10","doi-asserted-by":"crossref","first-page":"e1003216","DOI":"10.1371\/journal.ppat.1003216","article-title":"Biomphalysin, a new \u03b2 pore-forming toxin involved in Biomphalaria glabrata immune defense against Schistosoma mansoni.","volume":"9","author":"Galinier","year":"2013","journal-title":"PLoS Pathog."},{"key":"2021042013014636200_bib11","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.molbiopara.2006.02.009","article-title":"Biomphalaria glabrata cytosolic copper\/zinc superoxide dismutase (SOD1) gene: association of SOD1 alleles with resistance\/susceptibility to Schistosoma mansoni.","volume":"147","author":"Goodall","year":"2006","journal-title":"Mol. Biochem. Parasitol."},{"key":"2021042013014636200_bib12","doi-asserted-by":"crossref","first-page":"e1591","DOI":"10.1371\/journal.pntd.0001591","article-title":"A somatically diversified defense factor, FREP3, is a determinant of snail resistance to schistosome infection.","volume":"6","author":"Hanington","year":"2012","journal-title":"PLoS Negl. Trop. Dis."},{"key":"2021042013014636200_bib13","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1186\/s12864-017-3511-2","article-title":"Exome QTL-seq maps monogenic locus and QTLs in barley.","volume":"18","author":"Hisano","year":"2017","journal-title":"BMC Genomics"},{"key":"2021042013014636200_bib14","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1016\/j.ijpara.2013.03.007","article-title":"Identification and characterization of functional expressed sequence tags-derived simple sequence repeats (eSSR) markers for genetic linkage mapping of Schistosoma mansoni juvenile resistance and susceptibility loci in Biomphalaria glabrata.","volume":"43","author":"Ittiprasert","year":"2013","journal-title":"Int. J. Parasitol."},{"key":"2021042013014636200_bib15","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1111\/mec.13304","article-title":"Targeted capture in evolutionary and ecological genomics.","volume":"25","author":"Jones","year":"2016","journal-title":"Mol. Ecol."},{"key":"2021042013014636200_bib16","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.actatropica.2009.11.012","article-title":"Parasites and poverty: the case of schistosomiasis.","volume":"113","author":"King","year":"2010","journal-title":"Acta Trop."},{"key":"2021042013014636200_bib17","doi-asserted-by":"crossref","first-page":"1561","DOI":"10.1016\/S0140-6736(05)66457-4","article-title":"Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis.","volume":"365","author":"King","year":"2005","journal-title":"Lancet"},{"key":"2021042013014636200_bib18","doi-asserted-by":"crossref","first-page":"1510","DOI":"10.1073\/pnas.96.4.1510","article-title":"The identification of markers segregating with resistance to Schistosoma mansoni infection in the snail Biomphalaria glabrata.","volume":"96","author":"Knight","year":"1999","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2021042013014636200_bib19","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1016\/j.ijpara.2013.11.004","article-title":"Resistance of Biomphalaria glabrata 13\u201316\u2013R1 snails to Schistosoma mansoni PR1 is a function of haemocyte abundance and constitutive levels of specific transcripts in haemocytes.","volume":"44","author":"Larson","year":"2014","journal-title":"Int. J. Parasitol."},{"key":"2021042013014636200_bib20","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/S0378-1119(01)00444-9","article-title":"Structure of two FREP genes that combine IgSF and fibrinogen domains, with comments on diversity of the FREP gene family in the snail Biomphalaria glabrata.","volume":"269","author":"L\u00e9onard","year":"2001","journal-title":"Gene"},{"key":"2021042013014636200_bib21","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.1093\/bioinformatics\/btp324","article-title":"Fast and accurate short read alignment with Burrows-Wheeler Transform.","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"2021042013014636200_bib22","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","article-title":"The Sequence Alignment\/Map (SAM) format and SAMtools.","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"2021042013014636200_bib23","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1111\/j.2007.0018-0661.02000.x","article-title":"OneMap: software for genetic mapping in outcrossing species.","volume":"144","author":"Margarido","year":"2007","journal-title":"Hereditas"},{"key":"2021042013014636200_bib24","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1016\/j.dci.2004.10.002","article-title":"Gene discovery and expression analysis of immune-relevant genes from Biomphalaria glabrata hemocytes.","volume":"29","author":"Mitta","year":"2005","journal-title":"Dev. Comp. Immunol."},{"key":"2021042013014636200_bib25","doi-asserted-by":"crossref","first-page":"526","DOI":"10.2307\/3273814","article-title":"The establishment of a strain of Australorbis glabratus which combines albinism and high susceptibility to infection with Schistosoma mansoni.","volume":"41","author":"Newton","year":"1955","journal-title":"J. Parasitol."},{"key":"2021042013014636200_bib26","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1038\/nrg3908","article-title":"Genetic linkage analysis in the age of whole-genome sequencing.","volume":"16","author":"Ott","year":"2015","journal-title":"Nat. Rev. Genet."},{"key":"2021042013014636200_bib27","doi-asserted-by":"crossref","first-page":"e0168665","DOI":"10.1371\/journal.pone.0168665","article-title":"The planorbid snail Biomphalaria glabrata expresses a hemocyanin-like sequence in the albumen gland.","volume":"11","author":"Pe\u00f1a","year":"2016","journal-title":"PLoS One"},{"key":"2021042013014636200_bib28","doi-asserted-by":"crossref","first-page":"e1005513","DOI":"10.1371\/journal.ppat.1005513","article-title":"A novel roll-like receptor (TLR) influences compatibility between the gastropod Biomphalaria glabrata, and the digenean trematode Schistosoma mansoni.","volume":"12","author":"Pila","year":"2016","journal-title":"PLoS Pathog."},{"key":"2021042013014636200_bib29","doi-asserted-by":"crossref","first-page":"5305","DOI":"10.1073\/pnas.1521239113","article-title":"Endogenous growth factor stimulation of hemocyte proliferation induces resistance to Schistosoma mansoni challenge in the snail host.","volume":"113","author":"Pila","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2021042013014636200_bib30","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1016\/j.gpb.2015.08.002","article-title":"PacBio sequencing and its applications.","volume":"13","author":"Rhoads","year":"2015","journal-title":"Genomics Proteomics Bioinformatics"},{"key":"2021042013014636200_bib31","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1038\/nature11696","article-title":"Insights into bilaterian evolution from three spiralian genomes.","volume":"493","author":"Simakov","year":"2013","journal-title":"Nature"},{"key":"2021042013014636200_bib32","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1093\/molbev\/msh252","article-title":"Disentangling the effects of demography and selection in human history.","volume":"22","author":"Stajich","year":"2005","journal-title":"Mol. Biol. Evol."},{"key":"2021042013014636200_bib33","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1016\/S1473-3099(06)70521-7","article-title":"Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk.","volume":"6","author":"Steinmann","year":"2006","journal-title":"Lancet Infect. Dis."},{"key":"2021042013014636200_bib34","doi-asserted-by":"crossref","first-page":"1341","DOI":"10.1534\/g3.113.006288","article-title":"Targeted sequence capture provides insight into genome structure and genetics of male sterility in a gynodioecious diploid strawberry, Fragaria vesca ssp. bracteata (Rosaceae).","volume":"3","author":"Tennessen","year":"2013","journal-title":"G3"},{"key":"2021042013014636200_bib35","doi-asserted-by":"crossref","first-page":"3295","DOI":"10.1093\/gbe\/evu261","article-title":"Evolutionary origins and dynamics of octoploid strawberry subgenomes revealed by dense targeted capture linkage maps.","volume":"6","author":"Tennessen","year":"2014","journal-title":"Genome Biol. Evol."},{"key":"2021042013014636200_bib36","doi-asserted-by":"crossref","first-page":"e1005067","DOI":"10.1371\/journal.pgen.1005067","article-title":"Hyperdiverse gene cluster in snail host conveys resistance to human schistosome parasites.","volume":"11","author":"Tennessen","year":"2015","journal-title":"PLoS Genet."},{"key":"2021042013014636200_bib37","doi-asserted-by":"crossref","first-page":"e0004077","DOI":"10.1371\/journal.pntd.0004077","article-title":"Genome-wide scan and test of candidate genes in the snail Biomphalaria glabrata reveal new locus influencing resistance to Schistosoma mansoni.","volume":"9","author":"Tennessen","year":"2015","journal-title":"PLoS Negl. Trop. Dis."},{"key":"2021042013014636200_bib38","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1038\/sj.hdy.6800950","article-title":"Variation in genomic recombination rates among animal taxa and the case of social insects.","volume":"98","author":"Wilfert","year":"2007","journal-title":"Heredity"},{"key":"2021042013014636200_bib39","first-page":"20141739","article-title":"Phylogenomic analyses of deep gastropod relationships reject Orthogastropoda.","volume":"281","author":"Zapata","year":"2014","journal-title":"Proc. Biol. Sci."},{"key":"2021042013014636200_bib40","doi-asserted-by":"crossref","first-page":"1868","DOI":"10.1016\/j.molimm.2011.05.017","article-title":"Identification and characterization of five transcription factors that are associated with evolutionarily conserved immune signaling pathways in the schistosome-transmitting snail Biomphalaria glabrata.","volume":"48","author":"Zhang","year":"2011","journal-title":"Mol. Immunol."}],"container-title":["G3 Genes|Genomes|Genetics"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/g3journal\/article-pdf\/7\/7\/2353\/37145023\/g3journal2353.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/g3journal\/article-pdf\/7\/7\/2353\/37145023\/g3journal2353.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,4,21]],"date-time":"2021-04-21T00:41:30Z","timestamp":1618965690000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/g3journal\/article\/7\/7\/2353\/6053637"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,7,1]]},"references-count":40,"journal-issue":{"issue":"7","published-print":{"date-parts":[[2017,7,1]]}},"URL":"https:\/\/doi.org\/10.1534\/g3.117.041319","relation":{},"ISSN":["2160-1836"],"issn-type":[{"value":"2160-1836","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2017,7,1]]},"published":{"date-parts":[[2017,7,1]]}}}