Centrosomes and Not-Coding DNA during the Emergence and Evolution of Bilaterally Symmetric Complex Organs: Computational Models — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
Centrosomes and Not-Coding DNA during the Emergence and Evolution of Bilaterally Symmetric Complex Organs: Computational Models
Department of Biophysics, MFR Bioengineering, Milano, Italy
1 Department of Biophysics, MFR Bioengineering, Milano, Italy
The origin of complex biological symmetric structures has long been a subject of interest and debate. How new sophisticated structures arise, perfectly meshed together, and added to preexisting organs without breaking their anatomy and physiology remains challenging. A mystery is how endless amounts of new bilaterally symmetric organs have arisen in an infinite number of species: bilateral symmetry requires two different pathways for arranging and driving cells in symmetric locations in the left and right halves of the organism. It is unsustainable that two different genetic codes, independent of each other and assembled by chance, have simultaneously arisen for every organ in millions of different species. Many findings have evidenced that DNA tandem repeats and centrosomes are involved in morphogenesis, suggesting they have played a role in the evolution of shapes. This paper introduces computational simulations to test and ascertain whether DNA tandem repeats and centrosomes can manage and accelerate the evolution of complex organs and bilaterally symmetric structures. The present study follows an interdisciplinary perspective that combines biology and computational modeling to understand cellular behavior across species, underlying the similarity between programming and cellular procedures. The integration of programming codes, tandem repeats, centrioles, and centrosomes provides a potential framework for investigating fundamental biological processes.
Laland, K., Uller, T., Feldman, M., Sterelny, K., Müller, G.B., Moczek, A., et al . (2014) Does Evolutionary Theory Need a Rethink? Nature , 514, 161-164. https://doi.org/10.1038/514161a
Andersen, J.S., Wilkinson, C.J., Mayor, T., Mortensen, P., Nigg, E.A. and Mann, M. (2003) Proteomic Characterization of the Human Centrosome by Protein Correlation Profiling. Nature , 426, 570-574. https://doi.org/10.1038/nature02166
Myers, P. (2007) Tandem Repeats and Morphological Variation. Nature Education , 1, 1.
Ostrander, E.A. (2007) Genetics and the Shape of Dogs. American Scientist , 95, 406. https://doi.org/10.1511/2007.67.406
Fondon, J.W. and Garner, H.R. (2004) Molecular Origins of Rapid and Continuous Morphological Evolution. Proceedings of the National Academy of Sciences of the United States of America , 101, 18058-18063. https://doi.org/10.1073/pnas.0408118101
Sears, K.E., Goswami, A., Flynn, J.J. and Niswander, L.A. (2007) The Correlated Evolution of runx2 Tandem Repeats, Transcriptional Activity, and Facial Length in Carnivora. Evolution & Development , 9, 555-565. https://doi.org/10.1111/j.1525-142x.2007.00196.x
Balzano, E., Pelliccia, F. and Giunta, S. (2021) Genome (In)stability at Tandem Repeats. Seminars in Cell & Developmental Biology , 113, 97-112. https://doi.org/10.1016/j.semcdb.2020.10.003
Wahls, W.P., Wallace, L.J. and Moore, P.D. (1990) Hypervariable Minisatellite DNA Is a Hotspot for Homologous Recombination in Human Cells. Cell , 60, 95-103. https://doi.org/10.1016/0092-8674(90)90719-u
Ruiz-Ruano, F.J., López-León, M.D., Cabrero, J. and Camacho, J.P.M. (2016) High-throughput Analysis of the Satellitome Illuminates Satellite DNA Evolution. Scientific Reports , 6, Article No. 28333. https://doi.org/10.1038/srep28333
Cacheux, L., Ponger, L., Gerbault-Seureau, M., Richard, F.A. and Escudé, C. (2016) Diversity and Distribution of α Satellite DNA in the Genome of an Old World Monkey: Cercopithecus solatus . BMC Genomics , 17, Article No. 916. https://doi.org/10.1186/s12864-016-3246-5
Ahmad, S.F., Singchat, W., Jehangir, M., Suntronpong, A., Panthum, T., Malaivijitnond, S., et al . (2020) Dark Matter of Primate Genomes: Satellite DNA Repeats and Their Evolutionary Dynamics. Cells , 9, Article 2714. https://doi.org/10.3390/cells9122714
Ma, S., Skarica, M., Li, Q., Xu, C., Risgaard, R.D., Tebbenkamp, A.T.N., et al . (2022) Molecular and Cellular Evolution of the Primate Dorsolateral Prefrontal Cortex. Science , 377, eabo7257. https://doi.org/10.1126/science.abo7257
Sun, F., Fleurdépine, S., Bousquet-Antonelli, C., Caetano-Anollés, G. and Deragon, J. (2007) Common Evolutionary Trends for SINE RNA Structures. Trends in Genetics , 23, 26-33. https://doi.org/10.1016/j.tig.2006.11.005
Malgrange, B. and Nguyen, L. (2022) Scaling Brain Neurogenesis across Evolution. Science , 377, 1155-1156. https://doi.org/10.1126/science.ade4388
Regolini, M.F.G. (2024) DNA Tandem Repeats as Iterable Objects to Count Cell Divisions: A Computational Model. Advances in Bioscience and Biotechnology , 15, 207-234. https://doi.org/10.4236/abb.2024.154015
Brown, R.E. and Freudenreich, C.H. (2021) Structure-forming Repeats and Their Impact on Genome Stability. Current Opinion in Genetics & Development , 67, 41-51. https://doi.org/10.1016/j.gde.2020.10.006
Shi, G., Pang, Q., Lin, Z., Zhang, X. and Huang, K. (2024) Repetitive Sequence Stability in Embryonic Stem Cells. International Journal of Molecular Sciences , 25, Article 8819. https://doi.org/10.3390/ijms25168819
Schaper, E., Gascuel, O. and Anisimova, M. (2014) Deep Conservation of Human Protein Tandem Repeats within the Eukaryotes. Molecular Biology and Evolution , 31, 1132-1148. https://doi.org/10.1093/molbev/msu062
Fedorov, A.N., Fedorova, L.V., Grechko, V.V., Ryabinin, D.M., Sheremet’eva, V.A., Bannikova, A.A., et al . (1999) Variable and Invariable DNA Repeat Characters Revealed by Taxonprint Approach Are Useful for Molecular Systematics. Journal of Molecular Evolution , 48, 69-76. https://doi.org/10.1007/pl00006446
Satir, P. (2016) Chirality of the Cytoskeleton in the Origins of Cellular Asymmetry. Philosophical Transactions of the Royal Society B : Biological Sciences , 371, Article ID: 20150408. https://doi.org/10.1098/rstb.2015.0408
Basquin, C., Ershov, D., Gaudin, N., Vu, H.T., Louis, B., Papon, J., et al . (2019) Emergence of a Bilaterally Symmetric Pattern from Chiral Components in the Planarian Epidermis. Developmental Cell , 51, 516-525.e5. https://doi.org/10.1016/j.devcel.2019.10.021
Rahman, T., Peters, F.D. and Wan, L.Q. (2024) Biomechanical Modeling of Cell Chirality and Symmetry Breaking of Biological Systems. Mechanobiology in Medicine , 2, Article ID: 100038. https://doi.org/10.1016/j.mbm.2024.100038
Marshall, W.F. (2012) Centriole Asymmetry Determines Algal Cell Geometry. Current Opinion in Plant Biology , 15, 632-637. https://doi.org/10.1016/j.pbi.2012.09.011
Regolini, M. (2014) Centrosome, Cell Geometry and Tissue Topology. The Biological 3D Reference System of Metazoa. International Journal of Current Research , 6, 9685-9689.
Olivier, B.G., Rohwer, J.M. and Hofmeyr, J.S. (2002) Modelling Cellular Processes With Python and Scipy. Molecular Biology Reports , 29, 249-254. https://doi.org/10.1023/a:1020346417223
Tomás, H. (2011) Boolean Modeling of Biochemical Networks. The Open Bioinformatics Journal , 5, 16-25. https://doi.org/10.2174/1875036201105010016
Chiang, C., Ohashi, M. and Tang, Y. (2023) Deciphering Chemical Logic of Fungal Natural Product Biosynthesis through Heterologous Expression and Genome Mining. Natural Product Reports , 40, 89-127. https://doi.org/10.1039/d2np00050d
Boniolo, G., D’Agostino, M., Piazza, M. and Pulcini, G. (2021) Molecular Biology Meets Logic: Context-Sensitiveness in Focus. Foundations of Science , 28, 307-325. https://doi.org/10.1007/s10699-021-09789-y
Gaudin, N., Martin Gil, P., Boumendjel, M., Ershov, D., Pioche-Durieu, C., Bouix, M., et al . (2022) Evolutionary Conservation of Centriole Rotational Asymmetry in the Human Centrosome. eLife , 11, e72382. https://doi.org/10.7554/elife.72382
Burmeister, A.R. (2015) Horizontal Gene Transfer: Figure 1. Evolution , Medicine , and Public Health , 2015, 193-194. https://doi.org/10.1093/emph/eov018
Avni, E. and Snir, S. (2020) A New Phylogenomic Approach for Quantifying Horizontal Gene Transfer Trends in Prokaryotes. Scientific Reports , 10, Article No. 12425. https://doi.org/10.1038/s41598-020-62446-5
Shabbir, M.A.B., Hao, H., Shabbir, M.Z., Wu, Q., Sattar, A. and Yuan, Z. (2016) Bacteria vs. Bacteriophages: Parallel Evolution of Immune Arsenals. Frontiers in Microbiology , 7, Article 1292. https://doi.org/10.3389/fmicb.2016.01292
Pray, L. (2008) DNA Replication and Causes of Mutation. Nature Education , 1, 214.
Katsonis, P., Koire, A., Wilson, S.J., Hsu, T., Lua, R.C., Wilkins, A.D., et al . (2014) Single Nucleotide Variations: Biological Impact and Theoretical Interpretation. Protein Science , 23, 1650-1666. https://doi.org/10.1002/pro.2552
Barton, R.A. and Venditti, C. (2014) Rapid Evolution of the Cerebellum in Humans and Other Great Apes. Current Biology , 24, 2440-2444. https://doi.org/10.1016/j.cub.2014.08.056
Zhuang, X., Shao, Y., Chen, C., Zhou, L., Yao, Y., Cooper, D.N., et al . (2024) Divergent Evolutionary Rates of Primate Brain Regions as Revealed by Genomics and Transcriptomics. Genome Biology and Evolution , 16, evae023. https://doi.org/10.1093/gbe/evae023
Fan, H. and Chu, J. (2007) A Brief Review of Short Tandem Repeat Mutation. Genomics , Proteomics & Bioinformatics , 5, 7-14. https://doi.org/10.1016/s1672-0229(07)60009-6
Gemayel, R., Cho, J., Boeynaems, S. and Verstrepen, K.J. (2012) Beyond Junk-Variable Tandem Repeats as Facilitators of Rapid Evolution of Regulatory and Coding Sequences. Genes , 3, 461-480. https://doi.org/10.3390/genes3030461
Dogan, M., Pouch, M., Mandáková, T., Hloušková, P., Guo, X., Winter, P., et al . (2022) Corrigendum: Evolution of Tandem Repeats Is Mirroring Post-Polyploid Cladogenesis in Heliophila (Brassicaceae). Frontiers in Plant Science , 13, Article 1054800. https://doi.org/10.3389/fpls.2022.1054800
Beauregard, A., Curcio, M.J. and Belfort, M. (2008) The Take and Give between Retrotransposable Elements and Their Hosts. Annual Review of Genetics , 42, 587-617. https://doi.org/10.1146/annurev.genet.42.110807.091549
Vassetzky, N.S. and Kramerov, D.A. (2012) SINEBase: A Database and Tool for SINE Analysis. Nucleic Acids Research , 41, D83-D89. https://doi.org/10.1093/nar/gks1263
Ishak, C.A. and De Carvalho, D.D. (2020) Reactivation of Endogenous Retroelements in Cancer Development and Therapy. Annual Review of Cancer Biology , 4, 159-176. https://doi.org/10.1146/annurev-cancerbio-030419-033525
Sharma, A., Wolfgruber, T.K. and Presting, G.G. (2013) Tandem Repeats Derived from Centromeric Retrotransposons. BMC Genomics , 14, Article No. 142. https://doi.org/10.1186/1471-2164-14-142
Paço, A., Freitas, R. and Vieira-da-Silva, A. (2019) Conversion of DNA Sequences: From a Transposable Element to a Tandem Repeat or to a Gene. Genes , 10, Article 1014. https://doi.org/10.3390/genes10121014
Wang, W. and Kirkness, E.F. (2005) Short Interspersed Elements (SINEs) Are a Major Source of Canine Genomic Diversity. Genome Research , 15, 1798-1808. https://doi.org/10.1101/gr.3765505
Böhne, A., Brunet, F., Galiana-Arnoux, D., Schultheis, C. and Volff, J. (2008) Transposable Elements as Drivers of Genomic and Biological Diversity in Vertebrates. Chromosome Research , 16, 203-215. https://doi.org/10.1007/s10577-007-1202-6
Zhang, Y., Hu, N., Xu, J. and Wang, Z. (2023) DNA Logic Programming: From Concept to Construction. VIEW , 5, Article ID: 20230062. https://doi.org/10.1002/viw.20230062
Black, E.M. and Giunta, S. (2018) Repetitive Fragile Sites: Centromere Satellite DNA as a Source of Genome Instability in Human Diseases. Genes , 9, Article 615. https://doi.org/10.3390/genes9120615
Ahmed, M. and Liang, P. (2012) Transposable Elements Are a Significant Contributor to Tandem Repeats in the Human Genome. Comparative and Functional Genomics , 2012, Article ID: 947089. https://doi.org/10.1155/2012/947089
Zattera, M.L. and Bruschi, D.P. (2022) Transposable Elements as a Source of Novel Repetitive DNA in the Eukaryote Genome. Cells , 11, Article 3373. https://doi.org/10.3390/cells11213373
McGurk, M.P. and Barbash, D.A. (2018) Double Insertion of Transposable Elements Provides a Substrate for the Evolution of Satellite DNA. Genome Research , 28, 714-725. https://doi.org/10.1101/gr.231472.117
Guichard, P., Hachet, V., Majubu, N., Neves, A., Demurtas, D., Olieric, N., et al . (2013) Native Architecture of the Centriole Proximal Region Reveals Features Underlying Its 9-Fold Radial Symmetry. Current Biology , 23, 1620-1628. https://doi.org/10.1016/j.cub.2013.06.061
Ferreira, R.R., Pakula, G., Klaeyle, L., Fukui, H., Vilfan, A., Supatto, W., et al . (2018) Chiral Cilia Orientation in the Left-Right Organizer. Cell Reports , 25, 2008-2016.e4. https://doi.org/10.1016/j.celrep.2018.10.069
Regolini, M. (2019) The Centrosome as a Geometry Organizer. In: Kloc, M., Ed., The Golgi Apparatus and Centriole , Springer, 253-276. https://doi.org/10.1007/978-3-030-23173-6_11
Laporte, M. (2024) Time-Series Reconstruction of the Molecular Architecture of hu-Man Centriole Assembly. Cell , 187, 2158-2174.e19.
LeGuennec, M., Klena, N., Aeschlimann, G., Hamel, V. and Guichard, P. (2021) Overview of the Centriole Architecture. Current Opinion in Structural Biology , 66, 58-65. https://doi.org/10.1016/j.sbi.2020.09.015
Nazarov, S., Bezler, A., Hatzopoulos, G.N., Nemčíková Villímová, V., Demurtas, D., Le Guennec, M., et al . (2020) Novel Features of Centriole Polarity and Cartwheel Stacking Revealed by Cryo-Tomography. The EMBO Journal , 39, e106249. https://doi.org/10.15252/embj.2020106249
Woglar, A., Pierron, M., Schneider, F.Z., Jha, K., Busso, C. and Gönczy, P. (2022) Molecular Architecture of the C . elegans Centriole. PLOS Biology , 20, e3001784. https://doi.org/10.1371/journal.pbio.3001784
Fishman, E.L., Jo, K., Nguyen, Q.P.H., Kong, D., Royfman, R., Cekic, A.R., et al . (2018) Author Correction: A Novel Atypical Sperm Centriole Is Functional during Human Fertilization. Nature Communications , 9, Article No. 2800. https://doi.org/10.1038/s41467-018-05324-z
Avidor-Reiss, T. (2018) Rapid Evolution of Sperm Produces Diverse Centriole Structures That Reveal the Most Rudimentary Structure Needed for Function. Cells , 7, Article 67. https://doi.org/10.3390/cells7070067
Regolini, M. (2015) Centrosome RNA: A Molecular Basis for Non-Equivalence of Triplets in Centrioles and Centrosomes. Molecular Biology , 4, Article ID: 1000125.
Axelrod, J.D. (2020) Planar Cell Polarity Signaling in the Development of Left-Right Asymmetry. Current Opinion in Cell Biology , 62, 61-69. https://doi.org/10.1016/j.ceb.2019.09.002
Conceição, I.C., Long, A.D., Gruber, J.D. and Beldade, P. (2011) Genomic Sequence around Butterfly Wing Development Genes: Annotation and Comparative Analysis. PLOS ONE , 6, e23778. https://doi.org/10.1371/journal.pone.0023778
Jiggins, C.D., Wallbank, R.W.R. and Hanly, J.J. (2017) Waiting in the Wings: What Can We Learn about Gene Co-Option from the Diversification of Butterfly Wing Patterns? Philosophical Transactions of the Royal Society B : Biological Sciences , 372, 20150485. https://doi.org/10.1098/rstb.2015.0485
Mazo-Vargas, A., Langmüller, A.M., Wilder, A., van der Burg, K.R.L., Lewis, J.J., Messer, P.W., et al . (2022) Deep Cis-Regulatory Homology of the Butterfly Wing Pattern Ground Plan. Science , 378, 304-308. https://doi.org/10.1126/science.abi9407
Lower, S.S., McGurk, M.P., Clark, A.G. and Barbash, D.A. (2018) Satellite DNA Evolution: Old Ideas, New Approaches. Current Opinion in Genetics & Development , 49, 70-78. https://doi.org/10.1016/j.gde.2018.03.003
Durrant, M.G., Perry, N.T., Pai, J.J., Jangid, A.R., Athukoralage, J.S., Hiraizumi, M., et al . (2024) Bridge RNAs Direct Programmable Recombination of Target and Donor DNA. Nature , 630, 984-993. https://doi.org/10.1038/s41586-024-07552-4
Finnerty, J.R. (2003) The Origins of Axial Patterning in the Metazoa: How Old Is Bi-Lateral Symmetry? The International Journal of Developmental Biology , 47, 523-529.
Brown, N.A. and Wolpert, L. (1990) The Development of Handedness in Left/Right Asymmetry. Development , 109, 1-9. https://doi.org/10.1242/dev.109.1.1
Abouchar, L., Petkova, M.D., Steinhardt, C.R. and Gregor, T. (2014) Fly Wing Vein Patterns Have Spatial Reproducibility of a Single Cell. Journal of the Royal Society Interface , 11, Article ID: 20140443. https://doi.org/10.1098/rsif.2014.0443
Gopalakrishnan, J., Guichard, P., Smith, A.H., Schwarz, H., Agard, D.A., Marco, S., et al . (2010) Self-Assembling SAS-6 Multimer Is a Core Centriole Building Block. Journal of Biological Chemistry , 285, 8759-8770. https://doi.org/10.1074/jbc.m109.092627
Ford, J., Stansfeld, P. and Vakonakis, I. (2017) Coupling Form and Function: How the Oligomerisation Symmetry of the SAS-6 Protein Contributes to the Architecture of Centriole Organelles. Symmetry , 9, Article 74. https://doi.org/10.3390/sym9050074
Beisson, J. and Jerka‐Dziadosz, M. (1999) Polarities of the Centriolar Structure: Morphogenetic Consequences. Biology of the Cell , 91, 367-378. https://doi.org/10.1111/j.1768-322x.1999.tb01094.x
Bengueddach, H., Lemullois, M., Aubusson-Fleury, A. and Koll, F. (2017) Basal Body Positioning and Anchoring in the Multiciliated Cell Paramecium tetraurelia : Roles of OFD1 and VFL3. Cilia , 6, Article No. 6. https://doi.org/10.1186/s13630-017-0050-z
Geimer, S. and Melkonian, M. (2004) The Ultrastructure of The Chlamydomonas reinhardtii Basal Apparatus: Identification of an Early Marker of Radial Asymmetry Inherent in the Basal Body. Journal of Cell Science , 117, 2663-2674. https://doi.org/10.1242/jcs.01120
Pearson, C.G. and Winey, M. (2009) Basal Body Assembly in Ciliates: The Power of Numbers. Traffic , 10, 461-471. https://doi.org/10.1111/j.1600-0854.2009.00885.x
Regolini, M. (2019) Centrosome: Is It a Geometric, Noise Resistant, 3D Interface That Translates Morphogenetic Signals into Precise Locations in the Cell? Italian Journal of Anatomy and Embryology , 118, 19-66.
Regolini, M. (2019) Centriole Enantiomerism: Unexpected Information from Mice and Fish. Italian Journal of Anatomy and Embryology , 123, 232-240.
Fu, J., Hagan, I.M. and Glover, D.M. (2015) The Centrosome and Its Duplication Cycle. Cold Spring Harbor Perspectives in Biology , 7, a015800. https://doi.org/10.1101/cshperspect.a015800
Abe, M., Takahashi, H. and Kuroda, R. (2014) Spiral Cleavages Determine the Left-Right Body Plan by Regulating Nodal Pathway in Monomorphic Gastropods, Physa acuta . The International Journal of Developmental Biology , 58, 513-520. https://doi.org/10.1387/ijdb.140087rk
Martín-Durán, J.M. and Marlétaz, F. (2020) Unravelling Spiral Cleavage. Development , 147, dev181081. https://doi.org/10.1242/dev.181081
Ito, K.K., Watanabe, K. and Kitagawa, D. (2020) The Emerging Role of ncRNAs and RNA-Binding Proteins in Mitotic Apparatus Formation. Non-Coding RNA , 6, Article 13. https://doi.org/10.3390/ncrna6010013
Ishigaki, Y., Nakamura, Y., Tatsuno, T., Hashimoto, M., Iwabuchi, K. and Tomosugi, N. (2013) RNA-binding Protein RBM8A (Y14) and MAGOH Localize to Centrosome in Human A549 Cells. Histochemistry and Cell Biology , 141, 101-109. https://doi.org/10.1007/s00418-013-1135-4
Kantsadi, A.L., Hatzopoulos, G.N., Gönczy, P. and Vakonakis, I. (2022) Structures of SAS-6 Coiled Coil Hold Implications for the Polarity of the Centriolar Cartwheel. Structure , 30, 671-684.e5. https://doi.org/10.1016/j.str.2022.02.005
Gupta, A. and Kitagawa, D. (2018) Ultrastructural Diversity between Centrioles of Eukaryotes. The Journal of Biochemistry , 164, 1-8. https://doi.org/10.1093/jb/mvy031
Alliegro, M.C. and Alliegro, M.A. (2008) Centrosomal RNA Correlates with Intron-Poor Nuclear Genes in Spisula Oocytes. Proceedings of the National Academy of Sciences of the United States of America , 105, 6993-6997. https://doi.org/10.1073/pnas.0802293105
Alliegro, M.C., Alliegro, M.A. and Palazzo, R.E. (2006) Centrosome-Associated RNA in Surf Clam Oocytes. Proceedings of the National Academy of Sciences of the United States of America , 103, 9034-9038. https://doi.org/10.1073/pnas.0602859103
Chichinadze, K., Lazarashvili, A. and Tkemaladze, J. (2012) RNA in Centrosomes: Structure and Possible Functions. Protoplasma , 250, 397-405. https://doi.org/10.1007/s00709-012-0422-6
Barvitenko, N., Lawen, A., Aslam, M., Pantaleo, A., Saldanha, C., Skverchinskaya, E., et al . (2018) Integration of Intracellular Signaling: Biological Analogues of Wires, Processors and Memories Organized by a Centrosome 3D Reference System. Biosystems , 173, 191-206. https://doi.org/10.1016/j.biosystems.2018.08.007
Fry, A.M., Sampson, J., Shak, C. and Shackleton, S. (2017) Recent Advances in Pericentriolar Material Organization: Ordered Layers and Scaffolding Gels. F 1000 Research , 6, Article 1622. https://doi.org/10.12688/f1000research.11652.1
Panda, S., Setia, M., Kaur, N., Shepal, V., Arora, V., Singh, D.K., et al . (2018) Noncoding RNA Ginir Functions as an Oncogene by Associating with Centrosomal Proteins. PLOS Biology , 16, e2004204. https://doi.org/10.1371/journal.pbio.2004204
Beisson, J. and Sonneborn, T.M. (1965) Cytoplasmic Inheritance of the Organization of the Cell Cortex in Paramecium Aurelia. Proceedings of the National Academy of Sciences of the United States of America , 53, 275-282. https://doi.org/10.1073/pnas.53.2.275