Unique territorial and compartmental organization of chromosomes in the holocentric silkmoth

preprint OA: closed
Full text JSON View at publisher

Abstract

Abstract The hallmarks of chromosome organization in multicellular eukaryotes are chromosome territories (CT), chromatin compartments, and insulated domains, including topologically associated domains (TADs). Yet, most of these elements of chromosome organization are derived from analyses of a limited set of model organisms, while large eukaryotic groups, including insects, remain mostly unexplored. Here we combine Hi-C, biophysical modeling, and microscopy to characterize the 3D genome architecture of the silkmoth, Bombyx mori. In contrast to other eukaryotes, B. mori chromosomes form highly separated territories. Similar to other eukaryotes, B. mori chromosomes segregate into active A and inactive B compartments, yet unlike in vertebrate systems, contacts between euchromatic A regions appear to be a strong driver of compartmentalization. Remarkably, we also identify a third compartment, called secluded “S,” with a unique contact pattern. Each S region shows prominent short-range self-contacts and is remarkably devoid of contacts with the rest of the chromosome, including other S regions. Compartment S hosts a unique combination of genetic and epigenetic features, localizes towards the periphery of CTs, and shows developmental plasticity. Biophysical modeling reveals that the formation of such secluded domains requires highly localized loop extrusion within them, along with a low level of extrusion in A and B. Our Hi-C data supports predicted genome-wide and localized extrusion. Such a broad, non-uniform distribution of extruders has not been seen in other organisms. Overall, our analyses support loop extrusion in insects and highlight the evolutionary plasticity of 3D genome organization, driven by a new combination of known processes.
Full text 19,574 characters · extracted from preprint-html · click to expand
Unique territorial and compartmental organization of chromosomes in the holocentric silkmoth | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Article Unique territorial and compartmental organization of chromosomes in the holocentric silkmoth Ines Drinnenberg, Jose Gil, Emily Navarette, Leah Rosin, Neil Chowdhury, and 6 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-4732646/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract The hallmarks of chromosome organization in multicellular eukaryotes are chromosome territories (CT), chromatin compartments, and insulated domains, including topologically associated domains (TADs). Yet, most of these elements of chromosome organization are derived from analyses of a limited set of model organisms, while large eukaryotic groups, including insects, remain mostly unexplored. Here we combine Hi-C, biophysical modeling, and microscopy to characterize the 3D genome architecture of the silkmoth, Bombyx mori. In contrast to other eukaryotes, B. mori chromosomes form highly separated territories. Similar to other eukaryotes, B. mori chromosomes segregate into active A and inactive B compartments, yet unlike in vertebrate systems, contacts between euchromatic A regions appear to be a strong driver of compartmentalization. Remarkably, we also identify a third compartment, called secluded “S,” with a unique contact pattern. Each S region shows prominent short-range self-contacts and is remarkably devoid of contacts with the rest of the chromosome, including other S regions. Compartment S hosts a unique combination of genetic and epigenetic features, localizes towards the periphery of CTs, and shows developmental plasticity. Biophysical modeling reveals that the formation of such secluded domains requires highly localized loop extrusion within them, along with a low level of extrusion in A and B. Our Hi-C data supports predicted genome-wide and localized extrusion. Such a broad, non-uniform distribution of extruders has not been seen in other organisms. Overall, our analyses support loop extrusion in insects and highlight the evolutionary plasticity of 3D genome organization, driven by a new combination of known processes. Biological sciences/Molecular biology/Chromatin/Chromatin structure Biological sciences/Evolution Full Text Additional Declarations There is NO Competing Interest. Supplementary Files FiguresSxTablesS1S2S12S13MM.pdf TableS3GenesintheScompartment.xlsx TableS4HomeoboxandPcGinBmoriv4.xlsx TableS5Bmoriv4base.txt TableS6Bmoriv4basegenesnoTE.txt TableS7Bmoriv4tRNA.xlsx TableS8Bmoriv4basenolowTEpositions.txt TableS9Bmoriv4basesimplerepeats.txt TableS10Bmoriv4invisiblebySR100seq.txt TableS11p50D224hAHmRNATPM.xlsx TableS14p50D224hBmoriv440kbcompAmerge.txt TableS15p50D224hBmoriv440kbcompBmerge.txt TableS16p50D224hBmoriv440kbcompSmerge.txt Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-4732646","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":333584546,"identity":"05d34f51-9539-4af8-a86f-598ae1c8b464","order_by":0,"name":"Ines Drinnenberg","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAABBElEQVRIie3PMUvDQBTA8VeETIldn1zArxAIXBGk+SpPDuISaCFQOhQJFOJXuMFvUXAuFM7l6JypCAXnA0Gcil6SoQ5XOwref3gvgfy4C4DP9wcL+hnadWHH0A7q93nkqupIu387qyPJuntxkku23BiY7eIRW6r9dL4br140N69zwJHDBLHKEbZlePOk7lOpS/Gsi1SSBozXDoIFh0FNYdIUnEU1Cd6EKdzV8ICuv8DJu+nI5INFBxKptOQA6CYFYH9KwKKKxglaUp0iOUfaWpJzJhUR6rwEUugk11LsjZlRljTijU0XlA0fN6vB5+LWSdro6Pn7Sm0nwc+y8z/1+Xy+/9IX1I1NcWcx/ekAAAAASUVORK5CYII=","orcid":"https://orcid.org/0000-0002-9649-0352","institution":"Institut Curie","correspondingAuthor":true,"prefix":"","firstName":"Ines","middleName":"","lastName":"Drinnenberg","suffix":""},{"id":333584547,"identity":"f3c3f504-1338-4f80-a53a-3436e26cb6a4","order_by":1,"name":"Jose Gil","email":"","orcid":"","institution":"Institut Curie","correspondingAuthor":false,"prefix":"","firstName":"Jose","middleName":"","lastName":"Gil","suffix":""},{"id":333584548,"identity":"1a01409b-c0b3-417a-8357-405b64fd6a2e","order_by":2,"name":"Emily Navarette","email":"","orcid":"","institution":"Massachusetts Institute of Technology","correspondingAuthor":false,"prefix":"","firstName":"Emily","middleName":"","lastName":"Navarette","suffix":""},{"id":333584549,"identity":"1f842227-d049-42dc-ab44-1b9b799f451f","order_by":3,"name":"Leah Rosin","email":"","orcid":"","institution":"National Institutes of Health","correspondingAuthor":false,"prefix":"","firstName":"Leah","middleName":"","lastName":"Rosin","suffix":""},{"id":333584550,"identity":"031d328b-9706-4de6-b206-7aae90b833b5","order_by":4,"name":"Neil Chowdhury","email":"","orcid":"","institution":"Massachusetts Institute of Technology","correspondingAuthor":false,"prefix":"","firstName":"Neil","middleName":"","lastName":"Chowdhury","suffix":""},{"id":333584551,"identity":"76e84855-536c-450f-8ef6-760bb900ddc4","order_by":5,"name":"Sameer Abraham","email":"","orcid":"","institution":"Massachusetts Institute of Technology","correspondingAuthor":false,"prefix":"","firstName":"Sameer","middleName":"","lastName":"Abraham","suffix":""},{"id":333584552,"identity":"7ad2ab03-f1ff-4801-928f-0084d0a4a05c","order_by":6,"name":"Gaetan Cornilleau","email":"","orcid":"","institution":"Institut Curie","correspondingAuthor":false,"prefix":"","firstName":"Gaetan","middleName":"","lastName":"Cornilleau","suffix":""},{"id":333584553,"identity":"506d2d08-d093-408d-8fce-7ff44e8c9297","order_by":7,"name":"Elissa Lei","email":"","orcid":"","institution":"National Institutes of Health","correspondingAuthor":false,"prefix":"","firstName":"Elissa","middleName":"","lastName":"Lei","suffix":""},{"id":333584554,"identity":"5e743524-2444-4b55-a09f-b1560d3a4a89","order_by":8,"name":"Julien Mozziconacci","email":"","orcid":"https://orcid.org/0000-0001-5652-0302","institution":"UMPC","correspondingAuthor":false,"prefix":"","firstName":"Julien","middleName":"","lastName":"Mozziconacci","suffix":""},{"id":333584555,"identity":"cd57efe9-d25d-4a03-b614-95a8f50c00e5","order_by":9,"name":"Leonid Mirny","email":"","orcid":"https://orcid.org/0000-0002-0785-5410","institution":"MIT","correspondingAuthor":false,"prefix":"","firstName":"Leonid","middleName":"","lastName":"Mirny","suffix":""},{"id":333584556,"identity":"a49c9e04-c6a9-42a2-ae6c-f21444561f10","order_by":10,"name":"Heloise Muller","email":"","orcid":"","institution":"Institut Curie","correspondingAuthor":false,"prefix":"","firstName":"Heloise","middleName":"","lastName":"Muller","suffix":""}],"badges":[],"createdAt":"2024-07-12 21:35:14","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-4732646/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-4732646/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":86525511,"identity":"514b7143-1488-482f-afe8-81bcacb9a219","added_by":"auto","created_at":"2025-07-11 15:48:33","extension":"pdf","order_by":1,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":6130314,"visible":true,"origin":"","legend":"","description":"","filename":"Giletalmainnumbered.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4732646/v1_covered_087f9ad8-085a-483b-8545-335eec27f7a7.pdf"},{"id":61464088,"identity":"ff4b6b63-6245-45b2-82d1-7645cdcf62b6","added_by":"auto","created_at":"2024-07-31 05:23:44","extension":"pdf","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":36402601,"visible":true,"origin":"","legend":"","description":"","filename":"FiguresSxTablesS1S2S12S13MM.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4732646/v1/f5584c0a4bb3ea7bf6021eae.pdf"},{"id":61464003,"identity":"cf987e26-d59e-49a7-958a-9d9a30940d6c","added_by":"auto","created_at":"2024-07-31 05:23:43","extension":"xlsx","order_by":2,"title":"","display":"","copyAsset":false,"role":"supplement","size":58395,"visible":true,"origin":"","legend":"","description":"","filename":"TableS3GenesintheScompartment.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-4732646/v1/9f6f1698292b3be0f75daf42.xlsx"},{"id":61464791,"identity":"79e01dce-e071-4bb3-bfee-dfeb355d47c5","added_by":"auto","created_at":"2024-07-31 05:31:43","extension":"xlsx","order_by":3,"title":"","display":"","copyAsset":false,"role":"supplement","size":38255,"visible":true,"origin":"","legend":"","description":"","filename":"TableS4HomeoboxandPcGinBmoriv4.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-4732646/v1/553d84d51be24a355924196f.xlsx"},{"id":61464094,"identity":"2858292d-6f5d-4028-be72-a82ffe7c1018","added_by":"auto","created_at":"2024-07-31 05:23:44","extension":"txt","order_by":4,"title":"","display":"","copyAsset":false,"role":"supplement","size":34318537,"visible":true,"origin":"","legend":"","description":"","filename":"TableS5Bmoriv4base.txt","url":"https://assets-eu.researchsquare.com/files/rs-4732646/v1/b9b428b296122684b14c3460.txt"},{"id":61464007,"identity":"e622cf42-bc27-4cda-8d16-e34a8751b7ba","added_by":"auto","created_at":"2024-07-31 05:23:43","extension":"txt","order_by":5,"title":"","display":"","copyAsset":false,"role":"supplement","size":686197,"visible":true,"origin":"","legend":"","description":"","filename":"TableS6Bmoriv4basegenesnoTE.txt","url":"https://assets-eu.researchsquare.com/files/rs-4732646/v1/8f53bf85b5b0b3d53b3eb92d.txt"},{"id":61464002,"identity":"caa88882-9730-414f-90ad-01659f452cd6","added_by":"auto","created_at":"2024-07-31 05:23:43","extension":"xlsx","order_by":6,"title":"","display":"","copyAsset":false,"role":"supplement","size":51891,"visible":true,"origin":"","legend":"","description":"","filename":"TableS7Bmoriv4tRNA.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-4732646/v1/0e26d1476421349c93ca36f7.xlsx"},{"id":61464041,"identity":"b498b5d5-fe2c-4813-9d7b-ac41126878e9","added_by":"auto","created_at":"2024-07-31 05:23:44","extension":"txt","order_by":7,"title":"","display":"","copyAsset":false,"role":"supplement","size":18049453,"visible":true,"origin":"","legend":"","description":"","filename":"TableS8Bmoriv4basenolowTEpositions.txt","url":"https://assets-eu.researchsquare.com/files/rs-4732646/v1/6790c0c9aec0e10c7ccb9897.txt"},{"id":61464016,"identity":"033b22c2-8aff-4d50-b03f-d2912c9b53d9","added_by":"auto","created_at":"2024-07-31 05:23:43","extension":"txt","order_by":8,"title":"","display":"","copyAsset":false,"role":"supplement","size":17266651,"visible":true,"origin":"","legend":"","description":"","filename":"TableS9Bmoriv4basesimplerepeats.txt","url":"https://assets-eu.researchsquare.com/files/rs-4732646/v1/6b2ebd68e523d824eac1f322.txt"},{"id":61464055,"identity":"96538e7d-b54b-46ba-92d8-00629735bcca","added_by":"auto","created_at":"2024-07-31 05:23:44","extension":"txt","order_by":9,"title":"","display":"","copyAsset":false,"role":"supplement","size":10466782,"visible":true,"origin":"","legend":"","description":"","filename":"TableS10Bmoriv4invisiblebySR100seq.txt","url":"https://assets-eu.researchsquare.com/files/rs-4732646/v1/fde39e09ec8120b25562dcba.txt"},{"id":61464008,"identity":"12cf3085-8855-46f4-89f5-a3daa03c96a5","added_by":"auto","created_at":"2024-07-31 05:23:43","extension":"xlsx","order_by":10,"title":"","display":"","copyAsset":false,"role":"supplement","size":1126549,"visible":true,"origin":"","legend":"","description":"","filename":"TableS11p50D224hAHmRNATPM.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-4732646/v1/18f1244e2d9408a2956f0695.xlsx"},{"id":61464792,"identity":"b1f80235-439d-4bbc-95f1-938373a5bfe8","added_by":"auto","created_at":"2024-07-31 05:31:43","extension":"txt","order_by":11,"title":"","display":"","copyAsset":false,"role":"supplement","size":31397,"visible":true,"origin":"","legend":"","description":"","filename":"TableS14p50D224hBmoriv440kbcompAmerge.txt","url":"https://assets-eu.researchsquare.com/files/rs-4732646/v1/4017516f1600325e3e20d318.txt"},{"id":61464006,"identity":"303d209b-3780-4e33-8ee8-fcdffa7d0ef5","added_by":"auto","created_at":"2024-07-31 05:23:43","extension":"txt","order_by":12,"title":"","display":"","copyAsset":false,"role":"supplement","size":31447,"visible":true,"origin":"","legend":"","description":"","filename":"TableS15p50D224hBmoriv440kbcompBmerge.txt","url":"https://assets-eu.researchsquare.com/files/rs-4732646/v1/e013a465075cb5c3c5055fe0.txt"},{"id":61464005,"identity":"6e5676f3-c6fe-4b37-9839-d834d885a785","added_by":"auto","created_at":"2024-07-31 05:23:43","extension":"txt","order_by":13,"title":"","display":"","copyAsset":false,"role":"supplement","size":12159,"visible":true,"origin":"","legend":"","description":"","filename":"TableS16p50D224hBmoriv440kbcompSmerge.txt","url":"https://assets-eu.researchsquare.com/files/rs-4732646/v1/37dc9118bf770a72d9ebf88d.txt"}],"financialInterests":"There is \u003cb\u003eNO\u003c/b\u003e Competing Interest.","formattedTitle":"Unique territorial and compartmental organization of chromosomes in the holocentric silkmoth","fulltext":[],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":false,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":true,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":true,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":true,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"","lastPublishedDoi":"10.21203/rs.3.rs-4732646/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4732646/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"The hallmarks of chromosome organization in multicellular eukaryotes are chromosome territories (CT), chromatin compartments, and insulated domains, including topologically associated domains (TADs). Yet, most of these elements of chromosome organization are derived from analyses of a limited set of model organisms, while large eukaryotic groups, including insects, remain mostly unexplored. Here we combine Hi-C, biophysical modeling, and microscopy to characterize the 3D genome architecture of the silkmoth, Bombyx mori. In contrast to other eukaryotes, B. mori chromosomes form highly separated territories. Similar to other eukaryotes, B. mori chromosomes segregate into active A and inactive B compartments, yet unlike in vertebrate systems, contacts between euchromatic A regions appear to be a strong driver of compartmentalization. Remarkably, we also identify a third compartment, called secluded “S,” with a unique contact pattern. Each S region shows prominent short-range self-contacts and is remarkably devoid of contacts with the rest of the chromosome, including other S regions. Compartment S hosts a unique combination of genetic and epigenetic features, localizes towards the periphery of CTs, and shows developmental plasticity. Biophysical modeling reveals that the formation of such secluded domains requires highly localized loop extrusion within them, along with a low level of extrusion in A and B. Our Hi-C data supports predicted genome-wide and localized extrusion. Such a broad, non-uniform distribution of extruders has not been seen in other organisms. Overall, our analyses support loop extrusion in insects and highlight the evolutionary plasticity of 3D genome organization, driven by a new combination of known processes.","manuscriptTitle":"Unique territorial and compartmental organization of chromosomes in the holocentric silkmoth","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-07-31 05:23:38","doi":"10.21203/rs.3.rs-4732646/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"00b43498-bffa-49c9-8b5a-82501bd7ba16","owner":[],"postedDate":"July 31st, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[{"id":35323789,"name":"Biological sciences/Molecular biology/Chromatin/Chromatin structure"},{"id":35323790,"name":"Biological sciences/Evolution"}],"tags":[],"updatedAt":"2025-07-11T15:40:22+00:00","versionOfRecord":[],"versionCreatedAt":"2024-07-31 05:23:38","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-4732646","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-4732646","identity":"rs-4732646","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}

Text is read by the "Ask this paper" AI Q&A widget below. Extraction quality varies by source — PMC NXML preserves structure cleanly, OA-HTML may include some navigation residue, and OA-PDF can have broken hyphenation. The publisher copy (via DOI) is the canonical version.

My notes (saved in your browser only)

Ask this paper AI returns verbatim quotes from the full text · source: preprint-html

Answers must be backed by verbatim quotes from this paper's full text. Hallucinated quotes are dropped automatically; if no verbatim passage answers the question, we say so. How this works

Citation neighborhood (no data yet)

We don't have any in-corpus citations linked to this paper yet. This is a recent paper (2024) — citers typically take a year or two to land, and the OpenAlex reference graph may still be filling in.

Source provenance

europepmc
last seen: 2026-05-20T01:45:00.602351+00:00