Reconstructing cell lineage trees with genomic barcoding: approaches and applications

Zizhang Li; Wenjing Yang; Peng Wu; Yuyan Shan; Xiaoyu Zhang; Feng Chen; Junnan Yang; Jian-Rong Yang

doi:10.1016/j.jgg.2023.05.011

Volume 51 Issue 1

Jan. 2024

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Article Navigation > Journal of Genetics and Genomics > 2024 > 51(1): 35-47

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Reconstructing cell lineage trees with genomic barcoding: approaches and applications

doi: 10.1016/j.jgg.2023.05.011

a. Advanced Medical Technology Center, The First Affiliated Hospital, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, Guangdong 510080, China;
b. Department of Genetics and Biomedical Informatics, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, Guangdong 510080, China;
c. Key Laboratory of Tropical Disease Control, Ministry of Education, Sun Yat-sen University, Guangzhou, Guangdong 510080, China

Funds:

This work was supported by the National Key Research and Development Program of China (2021YFF1200904 and 2021YFA1302500 to J.-R. Y.), the National Natural Science Foundation of China (32122022 and 31871320 to J.-R. Y.), and by Science and Technology Planning Project of Guangdong Province, China (2014A030304053 to X. Z.).

Received Date: 2023-02-03
Accepted Date: 2023-05-20
Rev Recd Date: 2023-05-19
Publish Date: 2023-06-01

Abstract

Abstract

In multicellular organisms, developmental history of cell divisions and functional annotation of terminal cells can be organized into a cell lineage tree (CLT). The reconstruction of the CLT has long been a major goal in developmental biology and other related fields. Recent technological advancements, especially those in editable genomic barcodes and single-cell high-throughput sequencing, have sparked a new wave of experimental methods for reconstructing CLTs. Here we review the existing experimental approaches to the reconstruction of CLT, which are broadly categorized as either image-based or DNA barcode-based methods. In addition, we present a summary of the related literature based on the biological insight provided by the obtained CLTs. Moreover, we discuss the challenges that will arise as more and better CLT data become available in the near future. Genomic barcoding-based CLT reconstructions and analyses, due to their wide applicability and high scalability, offer the potential for novel biological discoveries, especially those related to general and systemic properties of the developmental process.
- Cell lineage tree,
- Developmental regulation,
- Biotechnology,
- Computational biology

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References

Alemany, A., Florescu, M., Baron, C.S., Peterson-Maduro, J.,van Oudenaarden, A., 2018. Whole-organism clone tracing using single-cell sequencing. Nature 556, 108-112.

Anderson, D.J., Pauler, F.M., McKenna, A., Shendure, J., Hippenmeyer, S.,Horwitz, M.S., 2022. Simultaneous brain cell type and lineage determined by scRNA-seq reveals stereotyped cortical development. Cell Syst. 13, 438-453.

Arendt, D., Bertucci, P.Y., Achim, K.,Musser, J.M., 2019. Evolution of neuronal types and families. Curr. Opin. Neurobiol. 56, 144-152.

Arendt, D., Musser, J.M., Baker, C.V.H., Bergman, A., Cepko, C., Erwin, D.H., Pavlicev, M., Schlosser, G., Widder, S., Laubichler, M.D., et al., 2016. The origin and evolution of cell types. Nat. Rev. Genet. 17, 744-757.

Aviv, R., Teichmann, S.A., Lander, E.S., Ido, A., Christophe, B., Ewan, B., Bernd, B., Campbell, P., Piero, C.,Menna, C., 2017. The human cell atlas. Elife 6, e27041.

Azevedo, R.B., Lohaus, R., Braun, V., Gumbel, M., Umamaheshwar, M., Agapow, P.M., Houthoofd, W., Platzer, U., Borgonie, G., Meinzer, H.P., et al., 2005. The simplicity of metazoan cell lineages. Nature 433, 152-156.

Barker, N.,Clevers, H., 2010a. Lineage tracing in the intestinal epithelium. Curr Protoc Stem Cell Biol Chapter 5, Unit5A 4.

Behjati, S., Huch, M., van Boxtel, R., Karthaus, W., Wedge, D.C., Tamuri, A.U., Martincorena, I., Petljak, M., Alexandrov, L.B., Gundem, G., et al., 2014. Genome sequencing of normal cells reveals developmental lineages and mutational processes. Nature 513, 422-425.

Biben, C., Weber, T., Potts, K., Choi, J., Miles, D., Carmagnac, A., Sargeant, T., de Graaf, C., Fennell, K.,Farley, A., 2023. In vivo clonal tracking reveals evidence of haemangioblast and haematomesoblast contribution to yolk sac haematopoiesis. Nat. Commun. 14, 41.

Biddy, B.A., Kong, W., Kamimoto, K., Guo, C., Waye, S.E., Sun, T.,Morris, S.A., 2018. Single-cell mapping of lineage and identity in direct reprogramming. Nature 564, 219-224.

Bowling, S., Sritharan, D., Osorio, F.G., Nguyen, M., Cheung, P., Rodriguez-Fraticelli, A., Patel, S., Yuan, W.C., Fujiwara, Y., Li, B.E., et al., 2020. An engineered CRISPR-Cas9 mouse line for simultaneous readout of lineage histories and gene expression profiles in single cells. Cell 181, 1410-1422. e1427.

Briggs, J.A., Weinreb, C., Wagner, D.E., Megason, S., Peshkin, L., Kirschner, M.W.,Klein, A.M., 2018. The dynamics of gene expression in vertebrate embryogenesis at single-cell resolution. Science 360, eaar5780.

Brunet, T., Fischer, A.H., Steinmetz, P.R., Lauri, A., Bertucci, P.,Arendt, D., 2016. The evolutionary origin of bilaterian smooth and striated myocytes. Elife 5.

Burrell, R.A., McGranahan, N., Bartek, J.,Swanton, C., 2013. The causes and consequences of genetic heterogeneity in cancer evolution. Nature 501, 338-345.

Cao, J., Packer, J.S., Ramani, V., Cusanovich, D.A., Huynh, C., Daza, R., Qiu, X., Lee, C., Furlan, S.N., Steemers, F.J., et al., 2017. Comprehensive single-cell transcriptional profiling of a multicellular organism. Science 357, 661-667.

Cao, J., Spielmann, M., Qiu, X., Huang, X., Ibrahim, D.M., Hill, A.J., Zhang, F., Mundlos, S., Christiansen, L., Steemers, F.J., et al., 2019. The single-cell transcriptional landscape of mammalian organogenesis. Nature 566, 496-502.

Casasent, A.K., Schalck, A., Gao, R., Sei, E., Long, A., Pangburn, W., Casasent, T., Meric-Bernstam, F., Edgerton, M.E.,Navin, N.E., 2018. Multiclonal invasion in breast tumors identified by topographic single cell sequencing. Cell 172, 205-217 e212.

Chan, M.M., Smith, Z.D., Grosswendt, S., Kretzmer, H., Norman, T.M., Adamson, B., Jost, M., Quinn, J.J., Yang, D., Jones, M.G., et al., 2019. Molecular recording of mammalian embryogenesis. Nature 570, 77-82.

Chang, H.H., Hemberg, M., Barahona, M., Ingber, D.E.,Huang, S., 2008. Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 453, 544-547.

Chen, C., Liao, Y.,Peng, G., 2022a. Connecting past and present: single-cell lineage tracing. Protein Cell 13, 790-807.

Chen, F., Li, Z., Zhang, X., Wu, P., Yang, W., Yang, J., Chen, X.,Yang, J.R., 2023. Phylogenetic comparative analysis of single-cell transcriptomes reveals constrained accumulation of gene expression heterogeneity during clonal expansion. Mol. Biol. Evol. 40, msad113.

Chen, H., Liu, S., Padula, S., Lesman, D., Griswold, K., Lin, A., Zhao, T., Marshall, J.L.,Chen, F., 2020. Efficient, continuous mutagenesis in human cells using a pseudo-random DNA editor. Nat. Biotechnol. 38, 165-168.

Chen, S., Luo, Y., Gao, H., Li, F., Chen, Y., Li, J., You, R., Hao, M., Bian, H.,Xi, X., 2022b. hECA: the cell-centric assembly of a cell atlas. iScience 25, 104318.

Chen, S., Luo, Y., Gao, H., Li, F., Li, J., Chen, Y., You, R., Lv, H., Hua, K., Jiang, R., et al., 2022c. Toward a unified information framework for cell atlas assembly. Natl. Sci. Rev. 9, nwab179.

Choi, J., Chen, W., Minkina, A., Chardon, F.M., Suiter, C.C., Regalado, S.G., Domcke, S., Hamazaki, N., Lee, C.,Martin, B., 2022. A time-resolved, multi-symbol molecular recorder via sequential genome editing. Nature 608, 98-107.

Chow, K.K., Budde, M.W., Granados, A.A., Cabrera, M., Yoon, S., Cho, S., Huang, T.H., Koulena, N., Frieda, K.L., Cai, L., et al., 2021. Imaging cell lineage with a synthetic digital recording system. Science 372.

Doyle, J.J., 2022. Cell types as species: exploring a metaphor. Front. Plant Sci. 13, 868565.

Du, Z., Santella, A., He, F., Shah, P.K., Kamikawa, Y.,Bao, Z., 2015. The regulatory landscape of lineage differentiation in a metazoan embryo. Dev. Cell 34, 592-607.

Du, Z., Santella, A., He, F., Tiongson, M.,Bao, Z., 2014. De novo inference of systems-level mechanistic models of development from live-imaging-based phenotype analysis. Cell 156, 359-372.

Elowitz, M.B., Levine, A.J., Siggia, E.D.,Swain, P.S., 2002. Stochastic gene expression in a single cell. Science 297, 1183-1186.

Evrony, G.D., Cai, X., Lee, E., Hills, L.B., Elhosary, P.C., Lehmann, H.S., Parker, J.J., Atabay, K.D., Gilmore, E.C., Poduri, A., et al., 2012. Single-neuron sequencing analysis of L1 retrotransposition and somatic mutation in the human brain. Cell 151, 483-496.

Eyler, C.E., Matsunaga, H., Hovestadt, V., Vantine, S.J., van Galen, P.,Bernstein, B.E., 2020. Single-cell lineage analysis reveals genetic and epigenetic interplay in glioblastoma drug resistance. Genome Biol. 21, 174.

Fang, W., Bell, C.M., Sapirstein, A., Asami, S., Leeper, K., Zack, D.J., Ji, H.,Kalhor, R., 2022. Quantitative fate mapping: a general framework for analyzing progenitor state dynamics via retrospective lineage barcoding. Cell 185, 4604-4620 e4632.

Farrell, J.A., Wang, Y., Riesenfeld, S.J., Shekhar, K., Regev, A.,Schier, A.F., 2018. Single-cell reconstruction of developmental trajectories during zebrafish embryogenesis. Science 360.

Frieda, K.L., Linton, J.M., Hormoz, S., Choi, J., Chow, K.K., Singer, Z.S., Budde, M.W., Elowitz, M.B.,Cai, L., 2017. Synthetic recording and in situ readout of lineage information in single cells. Nature 541, 107-111.

Frumkin, D., Wasserstrom, A., Kaplan, S., Feige, U.,Shapiro, E., 2005. Genomic variability within an organism exposes its cell lineage tree. PLoS Comput. Biol. 1, e50.

Gong, W., Granados, A.A., Hu, J., Jones, M.G., Raz, O., Salvador-Martinez, I., Zhang, H., Chow, K.K., Kwak, I.Y., Retkute, R., et al., 2021. Benchmarked approaches for reconstruction of in vitro cell lineages and in silico models of C. elegans and M. musculus developmental trees. Cell Syst. 12, 810-826 e814.

Gould, S.J.,Subramani, S., 1988. Firefly luciferase as a tool in molecular and cell biology. Anal. Biochem. 175, 5-13.

Griffiths, J.A., Scialdone, A.,Marioni, J.C., 2018. Using single-cell genomics to understand developmental processes and cell fate decisions. Mol. Syst. Biol. 14, e8046.

Gui, Q., Deng, S., Zhou, Z., Cao, W., Zhang, X., Shi, W., Cai, X., Jiang, W., Cui, Z., Hu, Z., et al., 2021. Transcriptome analysis in yeast reveals the externality of position effects. Mol. Biol. Evol. 38, 3294-3307.

Han, X., Wang, R., Zhou, Y., Fei, L., Sun, H., Lai, S., Saadatpour, A., Zhou, Z., Chen, H., Ye, F., et al., 2018. Mapping the mouse cell atlas by Microwell-seq. Cell 173, 1307.

He, Z., Maynard, A., Jain, A., Gerber, T., Petri, R., Lin, H.-C., Santel, M., Ly, K., Dupre, J.-S.,Sidow, L., 2022. Lineage recording in human cerebral organoids. Nat. Methods 19, 90-99.

He, L., Pu, W., Liu, X., Zhang, Z., Han, M., Li, Y., Huang, X., Han, X., Li, Y., Liu, K., et al., 2021. Proliferation tracing reveals regional hepatocyte generation in liver homeostasis and repair. Science 371, eabc4346.

Hormoz, S., Singer, Z.S., Linton, J.M., Antebi, Y.E., Shraiman, B.I.,Elowitz, M.B., 2016. Inferring cell-state transition dynamics from lineage trees and endpoint single-cell measurements. Cell Syst. 3, 419-433 e418.

HuBMAP Consortium, 2019. The human body at cellular resolution: the NIH Human Biomolecular Atlas Program. Nature 574, 187-192.

Humphreys, B.D.,DiRocco, D.P., 2014a. Lineage-tracing methods and the kidney. Kidney Int. 86, 481-488.

Hurley, K., Ding, J., Villacorta-Martin, C., Herriges, M.J., Jacob, A., Vedaie, M., Alysandratos, K.D., Sun, Y.L., Lin, C.,Werder, R.B., 2020. Reconstructed single-cell fate trajectories define lineage plasticity windows during differentiation of human PSC-derived distal lung progenitors. Cell Stem Cell 26, 593-608. e598.

Hwang, B., Lee, W., Yum, S.-Y., Jeon, Y., Cho, N., Jang, G.,Bang, D., 2019. Lineage tracing using a Cas9-deaminase barcoding system targeting endogenous L1 elements. Nat. Commun. 10, 1-9.

Lander, E.S., Linton, L.M., Birren, B., Nusbaum, C., Zody, M.C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W., et al., 2001. Initial sequencing and analysis of the human genome. Nature 409, 860-921.

Jindal, K., Adil, M.T., Yamaguchi, N., Yang, X., Wang, H.C., Kamimoto, K., Rivera-Gonzalez, G.C.,Morris, S.A., 2022. Multiomic single-cell lineage tracing to dissect fate-specific gene regulatory programs. bioRxiv, 2022.2010. 2023.512790.

Kalhor, R., Kalhor, K., Mejia, L., Leeper, K., Graveline, A., Mali, P.,Church, G.M., 2018. Developmental barcoding of whole mouse via homing CRISPR. Science 361, eaat9804.

Karras, P., Bordeu, I., Pozniak, J., Nowosad, A., Pazzi, C., Van Raemdonck, N., Landeloos, E., Van Herck, Y., Pedri, D., Bervoets, G., et al., 2022. A cellular hierarchy in melanoma uncouples growth and metastasis. Nature 610, 190-198.

Kimmerling, R.J., Lee Szeto, G., Li, J.W., Genshaft, A.S., Kazer, S.W., Payer, K.R., de Riba Borrajo, J., Blainey, P.C., Irvine, D.J., Shalek, A.K., et al., 2016. A microfluidic platform enabling single-cell RNA-seq of multigenerational lineages. Nat. Commun. 7, 10220.

Klein, A.M., Mazutis, L., Akartuna, I., Tallapragada, N., Veres, A., Li, V., Peshkin, L., Weitz, D.A.,Kirschner, M.W., 2015. Droplet barcoding for single-cell transcriptomics applied to embryonic stem cells. Cell 161, 1187-1201.

Konno, N., Kijima, Y., Watano, K., Ishiguro, S., Ono, K., Tanaka, M., Mori, H., Masuyama, N., Pratt, D., Ideker, T., et al., 2022. Deep distributed computing to reconstruct extremely large lineage trees. Nat. Biotechnol. 40, 566-575.

Kruglyak, L.,Nickerson, D.A., 2001. Variation is the spice of life. Nat. Genet. 27, 234-236.

Kwon, G.S., Viotti, M.,Hadjantonakis, A.K., 2008. The endoderm of the mouse embryo arises by dynamic widespread intercalation of embryonic and extraembryonic lineages. Dev. Cell 15, 509-520.

La Manno, G., Soldatov, R., Zeisel, A., Braun, E., Hochgerner, H., Petukhov, V., Lidschreiber, K., Kastriti, M.E., Lonnerberg, P.,Furlan, A., 2018. RNA velocity of single cells. Nature 560, 494-498.

Lee-Six, H., Obro, N.F., Shepherd, M.S., Grossmann, S., Dawson, K., Belmonte, M., Osborne, R.J., Huntly, B.J.P., Martincorena, I., Anderson, E., et al., 2018. Population dynamics of normal human blood inferred from somatic mutations. Nature 561, 473-478.

Li, L., Bowling, S., Yu, Q., McGeary, S.E., Alcedo, K., Lemke, B., Ferreira, M., Klein, A.M., Wang, S.-W.,Camargo, F., 2023. A mouse model with high clonal barcode diversity for joint lineage, transcriptomic, and epigenomic profiling in single cells. bioRxiv, 2023.2001. 2029.526062.

Liu, K., Deng, S., Ye, C., Yao, Z., Wang, J., Gong, H., Liu, L.,He, X., 2021. Mapping single-cell-resolution cell phylogeny reveals cell population dynamics during organ development. Nat. Methods 18, 1506-1514.

Ludwig, L.S., Lareau, C.A., Ulirsch, J.C., Christian, E., Muus, C., Li, L.H., Pelka, K., Ge, W., Oren, Y., Brack, A., et al., 2019. Lineage tracing in humans enabled by mitochondrial mutations and single-cell genomics. Cell 176, 1325-1339 e1322.

Luo, T., He, X.,Xing, K., 2016. Lineage analysis by microsatellite loci deep sequencing in mice. Mol. Reprod. Dev. 83, 387-391.

Maienschein, J., 1978. Cell lineage, ancestral reminiscence, and the biogenetic law. J. Hist. Biol., 129-158.

Marques, S., van Bruggen, D., Vanichkina, D.P., Floriddia, E.M., Munguba, H., Varemo, L., Giacomello, S., Falcao, A.M., Meijer, M., Bjorklund, A.K., et al., 2018. Transcriptional convergence of oligodendrocyte lineage progenitors during development. Dev. Cell 46, 504-517 e507.

Masuyama, N., Konno, N.,Yachie, N., 2022. Molecular recorders to track cellular events. Science 377, 469-470.

Masuyama, N., Mori, H.,Yachie, N., 2019. DNA barcodes evolve for high-resolution cell lineage tracing. Curr. Opin. Chem. Biol. 52, 63-71.

McKenna, A., Findlay, G.M., Gagnon, J.A., Horwitz, M.S., Schier, A.F.,Shendure, J., 2016. Whole-organism lineage tracing by combinatorial and cumulative genome editing. Science 353, aaf7907.

Moon, K.R., Stanley III, J.S., Burkhardt, D., van Dijk, D., Wolf, G.,Krishnaswamy, S., 2018. Manifold learning-based methods for analyzing single-cell RNA-sequencing data. Curr. Opin. Syst. Biol. 7, 36-46.

Murray, J.I., Boyle, T.J., Preston, E., Vafeados, D., Mericle, B., Weisdepp, P., Zhao, Z., Bao, Z., Boeck, M.,Waterston, R.H., 2012. Multidimensional regulation of gene expression in the C. elegans embryo. Genome Res. 22, 1282-1294.

Musser, J.M.,Wagner, G.P., 2015. Character trees from transcriptome data: origin and individuation of morphological characters and the so-called “species signal”. J. Exp. Zool. B Mol. Dev. Evol. 324, 588-604.

Nakashima, S., Sughiyama, Y.,Kobayashi, T.J., 2020. Lineage EM algorithm for inferring latent states from cellular lineage trees. Bioinformatics 36, 2829-2838.

Nik-Zainal, S., Van Loo, P., Wedge, D.C., Alexandrov, L.B., Greenman, C.D., Lau, K.W., Raine, K., Jones, D., Marshall, J., Ramakrishna, M., et al., 2012. The life history of 21 breast cancers. Cell 149, 994-1007.

Ouardini, K., Lopez, R., Jones, M.G., Prillo, S., Zhang, R., Jordan, M.I.,Yosef, N., 2021. Reconstructing unobserved cellular states from paired single-cell lineage tracing and transcriptomics data. bioRxiv, 2021.2005.2028.446021.

Panina, Y., Karagiannis, P., Kurtz, A., Stacey, G.N.,Fujibuchi, W., 2020. Human Cell Atlas and cell-type authentication for regenerative medicine. Exp. Mol. Med. 52, 1443-1451.

Patel, S.H., Christodoulou, C., Weinreb, C., Yu, Q., da Rocha, E.L., Pepe-Mooney, B.J., Bowling, S., Li, L., Osorio, F.G.,Daley, G.Q., 2022. Lifelong multilineage contribution by embryonic-born blood progenitors. Nature 606, 747-753.

Pei, W., Feyerabend, T.B., Rossler, J., Wang, X., Postrach, D., Busch, K., Rode, I., Klapproth, K., Dietlein, N., Quedenau, C., et al., 2017. Polylox barcoding reveals haematopoietic stem cell fates realized in vivo. Nature 548, 456-460.

Perli, S.D., Cui, C.H.,Lu, T.K., 2016. Continuous genetic recording with self-targeting CRISPR-Cas in human cells. Science 353, aag0511.

Prados, A., Onder, L., Cheng, H.W., Morbe, U., Lutge, M., Gil-Cruz, C., Perez-Shibayama, C., Koliaraki, V., Ludewig, B.,Kollias, G., 2021. Fibroblastic reticular cell lineage convergence in Peyer's patches governs intestinal immunity. Nat. Immunol. 22, 510-519.

Quinn, J.J., Jones, M.G., Okimoto, R.A., Nanjo, S., Chan, M.M., Yosef, N., Bivona, T.G.,Weissman, J.S., 2021. Single-cell lineages reveal the rates, routes, and drivers of metastasis in cancer xenografts. Science 371, eabc1944.

Raj, B., Wagner, D.E., McKenna, A., Pandey, S., Klein, A.M., Shendure, J., Gagnon, J.A.,Schier, A.F., 2018. Simultaneous single-cell profiling of lineages and cell types in the vertebrate brain. Nat. Biotechnol. 36, 442-450.

Reizel, Y., Chapal-Ilani, N., Adar, R., Itzkovitz, S., Elbaz, J., Maruvka, Y.E., Segev, E., Shlush, L.I., Dekel, N.,Shapiro, E., 2011. Colon stem cell and crypt dynamics exposed by cell lineage reconstruction. PLoS Genet. 7, e1002192.

Reizel, Y., Itzkovitz, S., Adar, R., Elbaz, J., Jinich, A., Chapal-Ilani, N., Maruvka, Y.E., Nevo, N., Marx, Z., Horovitz, I., et al., 2012. Cell lineage analysis of the mammalian female germline. PLoS Genet. 8, e1002477.

Rodrigo-Torres, D., Affo, S., Coll, M., Morales-Ibanez, O., Millan, C., Blaya, D., Alvarez-Guaita, A., Rentero, C., Lozano, J.J., Maestro, M.A., et al., 2014. The biliary epithelium gives rise to liver progenitor cells. Hepatology 60, 1367-1377.

Salipante, S.J.,Horwitz, M.S., 2006. Phylogenetic fate mapping. Proc. Natl. Acad. Sci. U. S. A. 103, 5448-5453.

Salipante, S.J., Kas, A., McMonagle, E.,Horwitz, M.S., 2010. Phylogenetic analysis of developmental and postnatal mouse cell lineages. Evol. Dev. 12, 84-94.

Salvador-Martinez, I., Grillo, M., Averof, M.,Telford, M.J., 2019. Is it possible to reconstruct an accurate cell lineage using CRISPR recorders? Elife 8, e40292.

Sankaran, V.G., Weissman, J.S.,Zon, L.I., 2022. Cellular barcoding to decipher clonal dynamics in disease. Science 378, eabm5874.

Santella, A., Kovacevic, I., Herndon, L.A., Hall, D.H., Du, Z.,Bao, Z., 2016. Digital development: a database of cell lineage differentiation in C. elegans with lineage phenotypes, cell-specific gene functions and a multiscale model. Nucleic Acids Res. 44, D781-D785.

Serbedzija, G.N., Bronner-Fraser, M.,Fraser, S.E., 1989. A vital dye analysis of the timing and pathways of avian trunk neural crest cell migration. Development 106, 809-816.

Siebert, S., Farrell, J.A., Cazet, J.F., Abeykoon, Y., Primack, A.S., Schnitzler, C.E.,Juliano, C.E., 2019. Stem cell differentiation trajectories in Hydra resolved at single-cell resolution. Science 365, eaav9314.

Simeonov, K.P., Byrns, C.N., Clark, M.L., Norgard, R.J., Martin, B., Stanger, B.Z., Shendure, J., McKenna, A.,Lengner, C.J., 2021. Single-cell lineage tracing of metastatic cancer reveals selection of hybrid EMT states. Cancer Cell 39, 1150-1162 e1159.

Spanjaard, B., Hu, B., Mitic, N., Olivares-Chauvet, P., Janjuha, S., Ninov, N.,Junker, J.P., 2018. Simultaneous lineage tracing and cell-type identification using CRISPR-Cas9-induced genetic scars. Nat. Biotechnol. 36, 469-473.

Sulston, J.E., Schierenberg, E., White, J.G.,Thomson, J.N., 1983. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64-119.

Tabula Muris Consortium, 2018. Single-cell transcriptomics of 20 mouse organs creates a Tabula Muris. Nature 562, 367-372.

Tao, L., Raz, O., Marx, Z., Ghosh, M.S., Huber, S., Greindl-Junghans, J., Biezuner, T., Amir, S., Milo, L., Adar, R., et al., 2021. Retrospective cell lineage reconstruction in humans by using short tandem repeats. Cell Rep. Methods 1, None.

Tricou, T., Tannier, E.,de Vienne, D.M., 2022a. Ghost lineages can invalidate or even reverse findings regarding gene flow. PLoS Biol. 20, e3001776.

Tricou, T., Tannier, E.,de Vienne, D.M., 2022b. Ghost lineages highly influence the interpretation of introgression tests. Syst. Biol. 71, 1147-1158.

Van Egeren, D., Escabi, J., Nguyen, M., Liu, S., Reilly, C.R., Patel, S., Kamaz, B., Kalyva, M., DeAngelo, D.J., Galinsky, I., et al., 2021. Reconstructing the lineage histories and differentiation trajectories of individual cancer cells in myeloproliferative neoplasms. Cell Stem Cell 28, 514-523 e519.

VanHorn, S.,Morris, S.A., 2021. Next-Generation lineage tracing and fate mapping to interrogate development. Dev. Cell 56, 7-21.

Wagner, D.E.,Klein, A.M., 2020. Lineage tracing meets single-cell omics: opportunities and challenges. Nat. Rev. Genet. 21, 410-427.

Wagner, D.E., Weinreb, C., Collins, Z.M., Briggs, J.A., Megason, S.G.,Klein, A.M., 2018. Single-cell mapping of gene expression landscapes and lineage in the zebrafish embryo. Science 360, 981-987.

Walther, V.,Alison, M.R., 2016. Cell lineage tracing in human epithelial tissues using mitochondrial DNA mutations as clonal markers. Wiley Interdiscip. Rev. Dev. Biol. 5, 103-117.

Wang, K., Hou, L., Lu, Z., Wang, X., Zi, Z., Zhai, W., He, X., Curtis, C., Zhou, D.,Hu, Z., 2022a. Cell division history encodes directional information of fate transitions. 2022.2010.2006.511094.

Wang, S.W., Herriges, M.J., Hurley, K., Kotton, D.N.,Klein, A.M., 2022b. CoSpar identifies early cell fate biases from single-cell transcriptomic and lineage information. Nat. Biotechnol. 40, 1066-1074.

Wasserstrom, A., Frumkin, D., Adar, R., Itzkovitz, S., Stern, T., Kaplan, S., Shefer, G., Shur, I., Zangi, L., Reizel, Y., et al., 2008. Estimating cell depth from somatic mutations. PLoS Comput. Biol. 4, e1000058.

Weinreb, C.,Klein, A.M., 2020. Lineage reconstruction from clonal correlations. Proc. Natl. Acad. Sci. U. S. A. 117, 17041-17048.

Weinreb, C., Rodriguez-Fraticelli, A., Camargo, F.D.,Klein, A.M., 2020. Lineage tracing on transcriptional landscapes links state to fate during differentiation. Science 367, eaaw3381.

Weisblat, D.A., Sawyer, R.T.,Stent, G.S., 1978. Cell lineage analysis by intracellular injection of a tracer enzyme. Science 202, 1295-1298.

Whitman, C.O., 1878. The Embryology of Clepsine. JE Adlard.

Whitman, C.O., 1887. A contribution to the history of the germlayers in Clepsine. J. Morphol. 1, 105-182.

Williams, N., Lee, J., Mitchell, E., Moore, L., Baxter, E.J., Hewinson, J., Dawson, K.J., Menzies, A., Godfrey, A.L., Green, A.R., et al., 2022. Life histories of myeloproliferative neoplasms inferred from phylogenies. Nature 602, 162-168.

Woo, K.,Fraser, S.E., 1995. Order and coherence in the fate map of the zebrafish nervous system. Development 121, 2595-2609.

Yang, D., Jones, M.G., Naranjo, S., Rideout, W.M., 3rd, Min, K.H.J., Ho, R., Wu, W., Replogle, J.M., Page, J.L., Quinn, J.J., et al., 2022. Lineage tracing reveals the phylodynamics, plasticity, and paths of tumor evolution. Cell 185, 1905-1923 e1925.

Yang, J.R., Ruan, S.,Zhang, J., 2014. Determinative developmental cell lineages are robust to cell deaths. PLoS Genet. 10, e1004501.

Yao, Z., Liu, K., Deng, S.,He, X., 2021. An instantaneous coalescent method insensitive to population structure. J. Genet. Genomics 48, 219-224.

Ye, C., Chen, Z., Liu, Z., Wang, F.,He, X., 2020. Defining endogenous barcoding sites for CRISPR/Cas9-based cell lineage tracing in zebrafish. J. Genet. Genomics 47, 85-91.

Yuan, M., Yang, X., Lin, J., Cao, X., Chen, F., Zhang, X., Li, Z., Zheng, G., Wang, X., Chen, X., et al., 2020. Alignment of cell lineage trees elucidates genetic programs for the development and evolution of cell types. iScience 23, 101273.

Zhao, H., Huang, X., Liu, Z., Pu, W., Lv, Z., He, L., Li, Y., Zhou, Q., Lui, K.O.,Zhou, B., 2021. Pre-existing beta cells but not progenitors contribute to new beta cells in the adult pancreas. Nat. Metab. 3, 352-365.

Zheng, G.X., Terry, J.M., Belgrader, P., Ryvkin, P., Bent, Z.W., Wilson, R., Ziraldo, S.B., Wheeler, T.D., McDermott, G.P., Zhu, J., et al., 2017. Massively parallel digital transcriptional profiling of single cells. Nat. Commun. 8, 14049.

Zuckerkandl, E.,Pauling, L. 1965. Evolutionary divergence and convergence in proteins, in: Bryson, V., Vogel, H.J. (Eds.), Evolving Genes and Proteins. Academic Press, pp. 97-166.

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