{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,10]],"date-time":"2026-10-10T23:18:21Z","timestamp":1791674301567,"version":"4.3.4"},"update-to":[{"DOI":"10.1371\/journal.ppat.1013706","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2025,11,24]],"date-time":"2025-11-24T00:00:00Z","timestamp":1763942400000}}],"reference-count":100,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2025,11,18]],"date-time":"2025-11-18T00:00:00Z","timestamp":1763424000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["2203286"],"award-info":[{"award-number":["2203286"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003246","name":"Nederlandse Organisatie voor Wetenschappelijk Onderzoek","doi-asserted-by":"publisher","award":["VENI grant 17282"],"award-info":[{"award-number":["VENI grant 17282"]}],"id":[{"id":"10.13039\/501100003246","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"<jats:p>\n                    Root-knot nematodes (\n                    <jats:italic>Meloidogyne spp.)<\/jats:italic>\n                    are among the most destructive agricultural pests that cause significant yield losses across a wide range of crops.\n                    <jats:italic>Meloidogyne hapla<\/jats:italic>\n                    is a valuable model for studying root-knot nematodes due to its parasitic diversity, small diploid genome, and a reproductive strategy that facilitates genetic analysis. Here, we report the most contiguous genome assembly to date for any plant-parasitic nematode built using PacBio HiFi, Oxford Nanopore, Illumina, and Hi-C sequencing. Genetic linkage analysis of F2 populations derived from crosses between\n                    <jats:italic>M. hapla<\/jats:italic>\n                    strains validated the assembly but also revealed anomalies indicating chromosome structure differences between parental isolates such as fissions, fusions, and rearrangements. Strikingly, we identified sharply delimited zones with extraordinarily high recombination on most chromosomes. Notably, several of these high recombination zones were significantly enriched for genes encoding secreted proteins, many of which contribute to parasitism. These findings suggest that meiotic recombination facilitates effector diversification and offer insight into how these parasites diversify their effector protein repertoire to change or expand their extraordinary host range. We further report the discovery of a novel 16-nucleotide tandem repeat and lack of canonical telomere repeats at chromosome ends. The localization of this 16-nt repeat at chromosome ends highlights a potentially divergent mechanism of chromosome-end maintenance in this nematode group. Overall, our study integrates high-resolution structural genomics, genetic mapping, and functional inference to uncover links between genome architecture, recombination landscapes, and host\u2013parasite interactions.\n                  <\/jats:p>","DOI":"10.1371\/journal.ppat.1013706","type":"journal-article","created":{"date-parts":[[2025,11,18]],"date-time":"2025-11-18T18:34:16Z","timestamp":1763490856000},"page":"e1013706","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":5,"title":["High-resolution genome assembly and linkage mapping in Meloidogyne hapla reveal non-canonical telomere repeats and recombination hotspots associated with effector proteins"],"prefix":"10.1371","volume":"21","author":[{"given":"Pallavi","family":"Shakya","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Muhammad I.","family":"Maulana","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Etienne G. J.","family":"Danchin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M. Laurens","family":"Voogt","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stefan J. S.","family":"van de Ruitenbeek","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jacinta","family":"Gimeno","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adam P.","family":"Taranto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alison C.","family":"Blundell","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Evelin","family":"Despot-Slade","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nevenka","family":"Me\u0161trovi\u0107","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana Zotta","family":"Mota","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dadong","family":"Dai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Valerie M.","family":"Williamson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark G.","family":"Sterken","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7503-4318","authenticated-orcid":true,"given":"Shahid","family":"Siddique","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2025,11,18]]},"reference":[{"issue":"3","key":"ppat.1013706.ref001","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1163\/156854101750413270","article-title":"Biodiversity in helminths and nematodes as a field of study: 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Croll","year":"2015","journal-title":"Genetics"},{"issue":"2","key":"ppat.1013706.ref064","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1111\/mpp.12524","article-title":"High-resolution mapping of the recombination landscape of the phytopathogen Fusarium graminearum suggests two-speed genome evolution","volume":"19","author":"B Laurent","year":"2018","journal-title":"Mol Plant Pathol"},{"issue":"6674","key":"ppat.1013706.ref065","doi-asserted-by":"crossref","DOI":"10.1126\/science.adh2531","article-title":"Meiotic DNA breaks drive multifaceted mutagenesis in the human germ line","volume":"382","author":"R Hinch","year":"2023","journal-title":"Science"},{"issue":"10","key":"ppat.1013706.ref066","doi-asserted-by":"crossref","first-page":"2844","DOI":"10.1093\/gbe\/evx201","article-title":"Comparative Genomics of Apomictic Root-Knot Nematodes: Hybridization, Ploidy, and Dynamic Genome Change","volume":"9","author":"A Szitenberg","year":"2017","journal-title":"Genome Biol 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Mar\u00e7ais","year":"2011","journal-title":"Bioinformatics"},{"issue":"1","key":"ppat.1013706.ref070","doi-asserted-by":"crossref","first-page":"1432","DOI":"10.1038\/s41467-020-14998-3","article-title":"GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes","volume":"11","author":"TR Ranallo-Benavidez","year":"2020","journal-title":"Nat Commun"},{"issue":"2","key":"ppat.1013706.ref071","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1038\/s41592-020-01056-5","article-title":"Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm","volume":"18","author":"H Cheng","year":"2021","journal-title":"Nat Methods"},{"issue":"5","key":"ppat.1013706.ref072","doi-asserted-by":"crossref","first-page":"722","DOI":"10.1101\/gr.215087.116","article-title":"Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation","volume":"27","author":"S Koren","year":"2017","journal-title":"Genome Res"},{"issue":"11","key":"ppat.1013706.ref073","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0112963","article-title":"Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement","volume":"9","author":"BJ Walker","year":"2014","journal-title":"PLoS One"},{"issue":"4","key":"ppat.1013706.ref074","doi-asserted-by":"crossref","first-page":"1361","DOI":"10.1534\/g3.119.400908","article-title":"BlobToolKit - interactive quality assessment of genome assemblies","volume":"10","author":"R Challis","year":"2020","journal-title":"G3 (Bethesda)"},{"issue":"24","key":"ppat.1013706.ref075","doi-asserted-by":"crossref","first-page":"2818","DOI":"10.1093\/bioinformatics\/btn548","article-title":"Aggressive assembly of pyrosequencing reads with mates","volume":"24","author":"JR Miller","year":"2008","journal-title":"Bioinformatics"},{"issue":"1","key":"ppat.1013706.ref076","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1186\/s13059-020-02134-9","article-title":"Merqury: reference-free quality, completeness, and phasing assessment for genome assemblies","volume":"21","author":"A Rhie","year":"2020","journal-title":"Genome Biol"},{"issue":"4","key":"ppat.1013706.ref077","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1038\/s41592-021-01101-x","article-title":"Sensitive protein alignments at tree-of-life scale using DIAMOND","volume":"18","author":"B Buchfink","year":"2021","journal-title":"Nat Methods"},{"key":"ppat.1013706.ref078","unstructured":"Griffin S. 2023. Available from: https:\/\/github.com\/sogriffin98\/Contamination_of_Genomes_using_BlobToolKit"},{"key":"ppat.1013706.ref079","article-title":"Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:1303.3997.","author":"H Li","year":"2013","journal-title":"arXiv"},{"issue":"18","key":"ppat.1013706.ref080","doi-asserted-by":"crossref","first-page":"3094","DOI":"10.1093\/bioinformatics\/bty191","article-title":"Minimap2: pairwise alignment for nucleotide sequences","volume":"34","author":"H Li","year":"2018","journal-title":"Bioinformatics"},{"issue":"1","key":"ppat.1013706.ref081","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.cels.2016.07.002","article-title":"Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments","volume":"3","author":"NC Durand","year":"2016","journal-title":"Cell Syst"},{"issue":"6333","key":"ppat.1013706.ref082","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1126\/science.aal3327","article-title":"De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds","volume":"356","author":"O Dudchenko","year":"2017","journal-title":"Science"},{"issue":"17","key":"ppat.1013706.ref083","doi-asserted-by":"crossref","first-page":"9451","DOI":"10.1073\/pnas.1921046117","article-title":"RepeatModeler2 for automated genomic discovery of transposable element families","volume":"117","author":"JM Flynn","year":"2020","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ppat.1013706.ref084","volume-title":"RepeatMasker Open-4.0","author":"AFA Smit","year":"2021"},{"issue":"1","key":"ppat.1013706.ref085","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1186\/s12864-023-09212-9","article-title":"Long read isoform sequencing reveals hidden transcriptional complexity between cattle subspecies","volume":"24","author":"Y Ren","year":"2023","journal-title":"BMC Genomics"},{"key":"ppat.1013706.ref086","article-title":"BRAKER3: Fully automated genome annotation using RNA-seq and protein evidence with GeneMark-ETP, AUGUSTUS and TSEBRA","author":"L Gabriel","year":"2024","journal-title":"bioRxiv"},{"issue":"12","key":"ppat.1013706.ref087","doi-asserted-by":"crossref","first-page":"5825","DOI":"10.1093\/molbev\/msab293","article-title":"eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale","volume":"38","author":"CP Cantalapiedra","year":"2021","journal-title":"Mol Biol Evol"},{"issue":"9","key":"ppat.1013706.ref088","doi-asserted-by":"crossref","first-page":"1236","DOI":"10.1093\/bioinformatics\/btu031","article-title":"InterProScan 5: genome-scale protein function classification","volume":"30","author":"P Jones","year":"2014","journal-title":"Bioinformatics"},{"issue":"3","key":"ppat.1013706.ref089","doi-asserted-by":"crossref","DOI":"10.18637\/jss.v058.i03","article-title":"changepoint: AnRPackage for Changepoint Analysis","volume":"58","author":"R Killick","year":"2014","journal-title":"J Stat Soft"},{"issue":"6","key":"ppat.1013706.ref090","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1093\/bioinformatics\/btq033","article-title":"BEDTools: a flexible suite of utilities for comparing genomic features","volume":"26","author":"AR Quinlan","year":"2010","journal-title":"Bioinformatics"},{"issue":"1","key":"ppat.1013706.ref091","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1186\/s13059-019-1832-y","article-title":"OrthoFinder: phylogenetic orthology inference for comparative genomics","volume":"20","author":"DM Emms","year":"2019","journal-title":"Genome Biol"},{"key":"ppat.1013706.ref092","doi-asserted-by":"crossref","DOI":"10.1093\/nar\/gkad328","article-title":"dbCAN3: automated carbohydrate-active enzyme and substrate annotation","volume":"51","author":"J Zheng","year":"2023","journal-title":"Nucleic Acids Res"},{"issue":"11","key":"ppat.1013706.ref093","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1010686","article-title":"AvP: A software package for automatic phylogenetic detection of candidate horizontal gene transfers","volume":"18","author":"GD Koutsovoulos","year":"2022","journal-title":"PLoS Comput Biol"},{"issue":"2","key":"ppat.1013706.ref094","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/j.ympev.2012.08.023","article-title":"MITOS: improved de novo metazoan mitochondrial genome annotation","volume":"69","author":"M Bernt","year":"2013","journal-title":"Mol Phylogenet Evol"},{"issue":"1","key":"ppat.1013706.ref095","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1186\/s12859-023-05385-y","article-title":"MitoHiFi: a python pipeline for mitochondrial genome assembly from PacBio high fidelity reads","volume":"24","author":"Darwin Tree of Life Consortium","year":"2023","journal-title":"BMC Bioinformatics"},{"issue":"11","key":"ppat.1013706.ref096","doi-asserted-by":"crossref","DOI":"10.1093\/nar\/gkz173","article-title":"MitoZ: a toolkit for animal mitochondrial genome assembly, annotation and visualization","volume":"47","author":"G Meng","year":"2019","journal-title":"Nucleic Acids Res"},{"issue":"16","key":"ppat.1013706.ref097","doi-asserted-by":"crossref","first-page":"9077","DOI":"10.1093\/nar\/gkab688","article-title":"tRNAscan-SE 2.0: improved detection and functional classification of transfer RNA genes","volume":"49","author":"PP Chan","year":"2021","journal-title":"Nucleic Acids 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