Unraveling the embryonic fate map through the mechanical signature of cells and their trajectories

Unraveling the embryonic fate map through the mechanical signature of cells and their trajectories | 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 Help Center Sign In Submit a Preprint Cite Share Download PDF Article Unraveling the embryonic fate map through the mechanical signature of cells and their trajectories David Pastor-Escuredo, Benoit Lombardot, Thierry Savy, Adeline Adeline Boyreau, and 7 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-333921/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 Digital cell lineages reconstructed from 3D+time imaging data of the developing zebrafish embryo are used to uncover mechanical cues and their role in morphogenesis. A continuous approximation of cell displacements obtained from cell lineages is used to assess tissue deformation during gastrulation. At this stage, embryonic tissues display multi-scale compressible fluid-like properties. The deformation rate at the mesoscopic level of the cell’s immediate surroundings appears noisy, in both space and time. The patterns identified by clustering the cells, according to the cumulative deformation rate along their trajectory throughout gastrulation, lead to a robust, ordered and coherent biomechanical map. The timing and amplitude of the biomechanical deformations provide a measurement of the phenotypic variability in small cohorts of specimens. We show that the biomechanical map matches the embryonic fate map of the zebrafish presumptive forebrain, in both wild type and Nodal pathway mutants ( zoep tz57/tz57 ), where it reveals the biomechanical defects that lead to cyclopia.. The comparison of biomechanical patterns and the expression pattern of a transgenic reporter for the transcription factor goosecoid (gsc) , supports the hypothesis that embryonic cells acquire, at an early developmental stage, a biomechanical signature that contributes to defining their fate. Biophysics Bioinformatics Developmental Biology embryo morphogenesis mechanical cues digital cell lineages tissue deformation biomechanical signature Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Figure 6 Full Text Due to technical limitations, full-text HTML conversion of this manuscript could not be completed. However, the latest manuscript can be downloaded and accessed as a PDF. Additional Declarations There is NO Competing Interest. Supplementary Files PastorEscuredoetalSupInformationNatComms.docx Supp material 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 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-333921","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":16848461,"identity":"cfb5f4b8-4fd6-4c18-b48e-b59883e92422","order_by":0,"name":"David 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08:51:44","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-333921/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-333921/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":7027026,"identity":"869306d5-6338-4fb1-8d23-ab8985e7ba50","added_by":"auto","created_at":"2021-03-16 20:07:17","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":167943,"visible":true,"origin":"","legend":"Construction of the biomechanical map from the reconstructed cell lineage (A, B, C) WT specimen wt1 imaged live between 6 and 12 hpf, animal pole (AP) view, 3D rendering with the Mov-IT software. Scale bar 50 µm. (A) 3D+time microscopy imaging of zebrafish embryos, nuclear staining (green), snapshots at 8, 10 and 12 hpf indicated top right. Insets schematize the imaged volume and the xy field of view. (B) Regularized displacement field (see Methods, Supplementary Fig. 2). Colormap for the speed intensity from 0 (dark blue) to 2 (white) µm/sec. (C) Left Panel: 3D rendering of the original cell tracking; right panel: trajectories completed using the regularized velocity field. Each cell nucleus approximate center is represented by a cube, the cell trajectory for the next 5 time steps is represented by a line. (D) Schematics of a typical cell distribution in 2D (top-left panel); deformation patterns quantified with the IDG tensor, instantaneous descriptors indicated top right of each panel: expansion (P \u003e 0), compression (P \u003c 0), simple shear (bottom left panel) and pure shear (bottom middle panel) (Qd), rotation (D \u003e 0). (E) Schematic representation of the computation of instantaneous and cumulative descriptors from the IDG tensor field. Eulerian compression descriptor P(Trajs) at each time step along the cell trajectory. Lagrangian compression descriptor ∆Vtini (Trajs) is calculated from an initial time point tini. Colormap: from compression (red) to expansion (blue). (F) Schematic representation of instantaneous (left panel) and cumulative (right panel) Lagrangian Biomechanical Profiles (LPBs) for a selection of cells and their trajectories between 8 (tini) to 14 hpf. Colormap: from compression (red) to expansion (blue). (G) Overview of the two-step clustering strategy that leads to the identification of Langrangian biomechanical domains. First, Lagrangian Biomechanical Profiles (LPBs) displayed in (F) are split into 3 main clusters called CLBPs (dark grey, brown, light grey). Second, CLBPs are used to classify trajectories and label cells accordingly (red, magenta, green and yellow).µm","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-333921/v1/2a30e4491a6ffd2fa9d39b59.png"},{"id":7027027,"identity":"95c46b59-c2e0-489c-ad42-a68f47b7e9a7","added_by":"auto","created_at":"2021-03-16 20:07:17","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":590665,"visible":true,"origin":"","legend":"wt and zoeptz57/tz57 biomechanical landmarks of gastrulation Comparison between a wild-type embryo wt1 (columns 1 and 3) and a zoeptz57/tz57 mutant embryo oep1 (columns 2 and 4). Time point (7, 8, 9, 10, 11 and 12 hpf) indicated to right. Descriptor indicated top left of each pair (wt1 and oep1) of panels. Velocity field (νTR) colormap from from dark (zero speed) to white (2 µm/sec). P colormap goes from compression (red) to neutral (grey) to expansion (blue). Qd colormap from dark (no distortion) to bright (maximum distortion). Comparison at 9 hpf (top-left panel) features velocity field (up) and P (down). Rotation discriminant D colormap from blue (no rotation) to green-yellow (maximum rotation observed). Scale bar 50 µm.","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-333921/v1/e49962df430d66a7ee2413cd.png"},{"id":7027611,"identity":"f952dc91-5d3f-4e35-8dbb-4b19ef83d9c8","added_by":"auto","created_at":"2021-03-16 20:10:17","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":548134,"visible":true,"origin":"","legend":"Cumulative descriptors of wt development Comparison between Eulerian and Lagrangian descriptors for wild-type embryo wt1. Time points (9, 10, 11 and 12 hpf) indicated top right of each panel. 6 sub-panels per time point with descriptor indicated top left. Similar display in the 4 panels with Eulerian descriptors (PQd, , D) left column in each subpanel and Lagrangian descriptors (ΔV, Δγ1 and Δα) on the right. Eulerian descriptors, same colormap as in Figure 2: P colormap from compression (red) to neutral (grey) to expansion (blue); Qd from dark (no distortion) to bright (maximum distortion); D colormap goes from blue (no rotation) to green-yellow (maximum rotation). Lagrangian descriptors: ΔV colormap from compression (red) to neutral (grey) to expansion (blue); Δγ1 colormap from dark (no distortion) to bright (maximum distortion); Δα colormap from blue (no rotation) to green-yellow (maximum rotation). Scale bar 50 µm.","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-333921/v1/599da6755d0af6e411a01af5.png"},{"id":7027859,"identity":"38c8e267-539b-4c46-b365-5188b94c760b","added_by":"auto","created_at":"2021-03-16 20:13:17","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":1407809,"visible":true,"origin":"","legend":"Quantitative comparison of Lagrangian Biomechanical Profiles (LBPs) in a cohort of zebrafish embryos (A, B) Comparison of the LBPs’ mean (line) and variance (shaded area), calculated for selected cell populations (selection at the tail bud stage, Supplementary Fig. 8, Supplementary Movie 22), hypoblast (red) and epiblast (blue) in embryos wt1-wt5 (row 1 to 5 respectively). (A) Instantaneous LBPs. Time in hpf. The vertical dashed black line indicates the onset of epiblast compression chosen as the initial time (tini). (B) LBPs cumulated from (tini) for the next 6 hours, mean (line) and variance (shaded area). The 5 plots are aligned in time at tini. Hypoblast was not analyzed in embryo wt2 as it was not present at tini because of the embryo position in the field of view.","description":"","filename":"Figure4v3.png","url":"https://assets-eu.researchsquare.com/files/rs-333921/v1/1bbe389f4fe7f737123fa4b4.png"},{"id":7027613,"identity":"09342a3a-5a36-4938-9cd0-00f96c016b6f","added_by":"auto","created_at":"2021-03-16 20:10:18","extension":"png","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":3177764,"visible":true,"origin":"","legend":"Order and coherence of the Lagrangian biomechanical map in normal and oep mutant embryos (A) Mean (m) for each of the three LBP clusters (number of clusters identified as optimal, Supplementary Fig. 10-12) defined the CLBPs for each Lagrangian descriptor (e.g. ∆Vm1 to ∆Vm3, , etc) for the wild type embryo (top row) and the mutant (bottom row); arbitrary color code to distinguish the different CLBPs. For ∆V, values higher than 1 mean expansion and bellow 1 compression. For Δγ1 and Δγ2, the value range goes from no distortion (0) to maximum of distortion (3). For Δα, the value represents the angle of rotation between 0º and 360º. (B) Snapshots of the Lagangian biomechanical map built for wt1 and oep1 embryos, cells at tini = 8 hpf were selected in Mov-IT and labeled according to their Lagrangian biomechanical signature; the corresponding color code was propagated along the cell lineage; different time points indicated top right. At 8 and 12 hpf, unlabeled nuclei in blue. At 10 and 13 hpf, labeled nuclear centers are displayed together with the membrane raw data (3D rendering in blue), upper sections were removed down to 65 µm below the embryo surface. Scale bar 50 µm. First row: wt1 embryo, four clusters identified at tini = 8 hpf (Supplementary Movie 23-26). Second row: oep1 embryo, three clusters identified at tini = 8 hpf.","description":"","filename":"Figure5v3sb.png","url":"https://assets-eu.researchsquare.com/files/rs-333921/v1/944bd4c5d3383409333a051f.png"},{"id":7027610,"identity":"fea61be0-ec8b-47d3-96b9-1764d770c8bc","added_by":"auto","created_at":"2021-03-16 20:10:17","extension":"png","order_by":6,"title":"Figure 6","display":"","copyAsset":false,"role":"figure","size":1376244,"visible":true,"origin":"","legend":"The gsc gene expression domain matches a biomechanical field wt6 embryo from the transgenic line gsc:egfp (Methods) imaged from 8 to 13 hpf. (A) Quantification of gsc reporter expression at the single cell level (Methods, Supplementary Table 1) and clustering of cell populations according to the reporter expression level using k-means clustering (k=3 green -gscm1-, light blue -gscm2- and magenta -gscm3- for the mean expression level in each cluster). (B) Average value of nuclear staining intensity along cell trajectories for each of the clusters identified in (A): nucm1, nucm2 and nucm3. (C) Average value of the gsc reporter expression after being corrected by the nuclear staining intensity (gscNm1, gscNm2 and gscNm3). (D, E) Visualization of the Lagrangian Biomechanical Maps with the Mov-IT software. Cells at 8 hpf are labelled according to their cluster and the color propagated along the cell lineage. Scale bar 50 µm. (D) Spatial organization of the three gsc expression clusters (green -gscm1-, light blue -gscm2- and magenta -gscm3). Snapshots at 8 and 10 hpf indicated top right. (E) Lagrangian Biomechanical Map for wt6 computed and displayed as for wt1 and oep1 in Figure 5B (tini = 8 hpf). Snapshots at 8 hpf and 10 hpf indicated top right","description":"","filename":"Figure6v5sb.png","url":"https://assets-eu.researchsquare.com/files/rs-333921/v1/967e2a0d7de305acf0f3d268.png"},{"id":13607869,"identity":"0b4ecd3a-ae11-43cf-9e6e-61dc4694de59","added_by":"auto","created_at":"2021-09-17 06:13:54","extension":"pdf","order_by":1,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1129533,"visible":true,"origin":"","legend":"Article File","description":"","filename":"PastorEscuredoNatCommfullarticle.pdf","url":"https://assets-eu.researchsquare.com/files/rs-333921/v1_covered.pdf"},{"id":7028037,"identity":"33af4fd2-5cde-432f-aba5-4b423785b8a2","added_by":"auto","created_at":"2021-03-16 20:16:21","extension":"pdf","order_by":1,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":414491,"visible":true,"origin":"","legend":"Article File","description":"","filename":"PastorEscuredoNatCommfullarticle.pdf","url":"https://assets-eu.researchsquare.com/files/rs-333921/v1_stamped.pdf"},{"id":7027615,"identity":"9497199d-e0b8-4136-b402-74a828204d86","added_by":"auto","created_at":"2021-03-16 20:10:18","extension":"docx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":66830229,"visible":true,"origin":"","legend":"Supp material","description":"","filename":"PastorEscuredoetalSupInformationNatComms.docx","url":"https://assets-eu.researchsquare.com/files/rs-333921/v1/3414f77fae5592131fd01478.docx"}],"financialInterests":"There is \u003cb\u003eNO\u003c/b\u003e Competing Interest.","formattedTitle":"Unraveling the embryonic fate map through the mechanical signature of cells and their trajectories","fulltext":[{"header":"Full Text","content":"Due to technical limitations, full-text HTML conversion of this manuscript could not be completed. However, the latest manuscript can be downloaded and \u003ca href='/article/rs-333921/latest.pdf' target='_blank'\u003e accessed as a PDF.\u003c/a\u003e"}],"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":false,"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":"embryo morphogenesis, mechanical cues, digital cell lineages, tissue deformation, biomechanical signature","lastPublishedDoi":"10.21203/rs.3.rs-333921/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-333921/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eDigital cell lineages reconstructed from 3D+time imaging data of the developing zebrafish embryo are used to uncover mechanical cues and their role in morphogenesis. A continuous approximation of cell displacements obtained from cell lineages is used to assess tissue deformation during gastrulation. At this stage, embryonic tissues display multi-scale compressible fluid-like properties. The deformation rate at the mesoscopic level of the cell’s immediate surroundings appears noisy, in both space and time. The patterns identified by clustering the cells, according to the cumulative deformation rate along their trajectory throughout gastrulation, lead to a robust, ordered and coherent biomechanical map. The timing and amplitude of the biomechanical deformations provide a measurement of the phenotypic variability in small cohorts of specimens. We show that the biomechanical map matches the embryonic fate map of the zebrafish presumptive forebrain, in both wild type and Nodal pathway mutants (\u003cem\u003ezoep\u003c/em\u003e\u003csup\u003e\u003cem\u003etz57/tz57\u003c/em\u003e\u003c/sup\u003e), where it reveals the biomechanical defects that lead to cyclopia.. The comparison of biomechanical patterns and the expression pattern of a transgenic reporter for the transcription factor \u003cem\u003egoosecoid (gsc)\u003c/em\u003e, supports the hypothesis that embryonic cells acquire, at an early developmental stage, a biomechanical signature that contributes to defining their fate.\u003c/p\u003e","manuscriptTitle":"Unraveling the embryonic fate map through the mechanical signature of cells and their trajectories","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2021-03-16 20:07:15","doi":"10.21203/rs.3.rs-333921/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":"a3290550-2fd3-4820-a38b-48fad807e942","owner":[],"postedDate":"March 16th, 2021","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[{"id":3017522,"name":"Biophysics"},{"id":3017523,"name":"Bioinformatics"},{"id":3017524,"name":"Developmental Biology"}],"tags":[],"updatedAt":"2021-05-17T10:31:30+00:00","versionOfRecord":[],"versionCreatedAt":"2021-03-16 20:07:15","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-333921","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-333921","identity":"rs-333921","version":["v1"]},"buildId":"GqpaHPwrfC8PjnIFayRh5","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}