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. 2022;2450:27–48. doi: 10.1007/978-1-0716-2172-1_2

Studying Regeneration in Ascidians: An Historical Overview.

Virginia Vanni, Loriano Ballarin, Fabio Gasparini, Anna Peronato, Lucia Manni
PMCID: PMC9761513  PMID: 35359301

Abstract

Ascidians are sessile tunicates, that is, marine animals belonging to the phylum Chordata and considered the sister group of vertebrates. They are widespread in all the seas, constituting abundant communities in various ecosystems. Among chordates, only tunicates are able to reproduce asexually, forming colonies. The high regenerative potentialities enabling tunicates to regenerate damaged body parts, or the whole body, represent a peculiarity of this taxon. Here we review the methodological approaches used in more than a century of biological studies to induce regeneration in both solitary and colonial species. For solitary species, we refer to the regeneration of single organs or body parts (e.g., siphon, brain, gonad, tunic, viscera). For colonial species, we review a plethora of experiments regarding the surgical manipulation of colonies, the regeneration of isolated colonial entities, such as single buds in the tunic, or part of tunic and its circulatory system.

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References

  1. Jeffery WR (2018) Regeneration and aging in the tunicate Ciona intestinalis. In: Conn’s handbook of models for human aging, second Edi. Elsevier Inc., Amsterdam, pp 521–531
  2. Manni L, Anselmi C, Cima F, Gasparini F, Voskoboynik A, Martini M, Peronato A, Burighel P, Zaniolo G, Ballarin L (2019) Sixty years of experimental studies on the blastogenesis of the colonial tunicate Botryllus schlosseri. Dev Biol 448:293–308. https://doi.org/10.1016/j.ydbio.2018.09.009 doi: 10.1016/j.ydbio.2018.09.009. [DOI] [PubMed]
  3. Carnevali MDC, Burighel P (2010) Regeneration in echinoderms and ascidians. In: Encyclopedia of life sciences. John Wiley & Sons, Ltd, Chichester
  4. Tiozzo S, Brown FD, De Tomaso AW (2008) Regeneration and stem cells in ascidians. In: Stem Cells: From Hydra to Man. Springer, Dordrecht, pp 95–112
  5. Voskoboynik A, Simon-Blecher N, Soen Y, Rinkevich B, De Tomaso AW, Ishizuka KJ, Weissman IL (2007) Striving for normality: whole body regeneration through a series of abnormal generations. FASEB J 21:1335–1344. https://doi.org/10.1096/fj.06-7337com doi: 10.1096/fj.06-7337com. [DOI] [PubMed]
  6. Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968. https://doi.org/10.1038/nature04336 doi: 10.1038/nature04336. [DOI] [PubMed]
  7. Delsuc F, Philippe H, Tsagkogeorga G, Simion P, Tilak M, Turon X, López-legentil S, Piette J, Lemaire P, Douzery EJP (2018) A phylogenomic framework and timescale for comparative studies of tunicates. BMC Biol 16(1):39 doi: 10.1186/s12915-018-0499-2. [DOI] [PMC free article] [PubMed]
  8. Alvarado AS, Tsonis PA (2006) Bridging the regeneration gap: genetic insights from diverse animal models. Nat Rev Genet 7:873–884. https://doi.org/10.1038/nrg1923 doi: 10.1038/nrg1923. [DOI] [PubMed]
  9. Seifert AW, Muneoka K (2018) The blastema and epimorphic regeneration in mammals. Dev Biol 433:190–199. https://doi.org/10.1016/j.ydbio.2017.08.007 doi: 10.1016/j.ydbio.2017.08.007. [DOI] [PMC free article] [PubMed]
  10. Alié A, Hiebert LS, Scelzo M, Tiozzo S (2020) The eventful history of nonembryonic development in tunicates. J Exp Zool Part B Mol Dev Evol 336(3):250–266. https://doi.org/10.1002/jez.b.22940 doi: 10.1002/jez.b.22940. [DOI] [PubMed]
  11. Burighel P, Cloney RA (1997) Urochordata: Ascidiacea. Microsc Anat Invertebr Vol 15 Hemichordata. Chaetognatha, Invertebr chordates 15:221–347
  12. Selys-Longchamps M (1915) Autotomie et régénération des viscères chez Polycarpa tenera Lacaze et Delage. C R Acad Sci Paris 160:566–569
  13. Shenkar N, Gordon T (2015) Gut-spilling in chordates: evisceration in the tropical ascidian Polycarpa mytiligera. Sci Rep 5:9614. https://doi.org/10.1038/srep09614 doi: 10.1038/srep09614. [DOI] [PMC free article] [PubMed]
  14. Gordon T, Upadhyay AK, Manni L, Huchon D, Shenkar N (2021) And then there were three…: extreme regeneration ability of the solitary chordate Polycarpa mytiligera. Front Cell Dev Biol 9:652466. https://doi.org/10.3389/fcell.2021.652466 doi: 10.3389/fcell.2021.652466. [DOI] [PMC free article] [PubMed]
  15. Voskoboynik A, Weissman IL (2015) Botryllus schlosseri, an emerging model for the study of aging, stem cells, and mechanisms of regeneration. Invertebr Reprod Dev 59:33–38. https://doi.org/10.1080/07924259.2014.944673 doi: 10.1080/07924259.2014.944673. [DOI] [PMC free article] [PubMed]
  16. Schultze LS (1899) Die Regeneration Des Ganglions Von Ciona intestinalis L. und. Jena Z f Naturwiss 33:263–344
  17. Schultze LS (1900) Die Regeneration des Ganglions von Ciona intestinalis L. und über das Verhältnis der Regeneration und Knospung zur Keimblätterlehre. Jena Z Med Naturwiss 33:263–344
  18. Hirschler J (1914) Über die Restitutions-und Involutionsvoränge bei operierten Exemplaren von Ciona intestinalis Flem. (Teil I) nebst Bemurkungen über den Wert des Negativen für das Potenzproblem. Arch Mikrosk Anat 85:205–227
  19. Fol A (1908) Note sur la régénération de la tunique chez les Tuniciers. Bull Soc Zool Fr 33:79–81
  20. Azéma M (1927) Sur le role des prolongements vasculaires au cours de la régénération de la tunique chez Ascidiella aspersa. Bull Soc Zool Fr 52:549–557
  21. Brien P (1930) Régénération naturelle et expérimentale chez les Clavelinidae. Ann la Société R Zool Belgique 61:20–112
  22. Brien P (1932) L’heteromorphose chez les Tuniciers. La regeneration bithoracique et monothoracique des fragments oesophagiens de Clavelina lepadiformis (Muller). Bull la Cl des Sci Académie R Belgique 18:975–1005
  23. Peres JM (1948) Recherches sur la genese et la regeneration de la tunique chez Ciona intestinalis L. Bull Inst Oceanogr Monaco 145:1–12
  24. Wagers AJ, Christensen JL, Weissman IL (2002) Cell fate determination from stem cells. Gene Ther 9:606 doi: 10.1038/sj.gt.3301717. [DOI] [PubMed]
  25. Deviney EM (1934) The behavior of isolated pieces of ascidian (Perophora viridis) stolon as compared with ordinary budding. J Elisha Mitchell Sci Soc 49:185–224
  26. Berrill NJ (1951) Regeneration and budding in tunicates. Biol Rev 26:456–475. https://doi.org/10.1111/j.1469-185X.1951.tb01207.x doi: 10.1111/j.1469-185X.1951.tb01207.x. [DOI]
  27. Mj W (1958) Regeneration of buds in Botryllus. Biol Bull 115:147–152. https://doi.org/10.2307/1539101 doi: 10.2307/1539101. [DOI]
  28. Wermel J (1930) Über den Einfluss der Regeneration und Überernährung auf die Siphonenlänge bei Ciona Intestinalis L. - Ein Beitrag zu Kammerers Experimenten. Wilhelm Roux Arch Entwickl Mech Org 122:22–47. https://doi.org/10.1007/BF00576964 doi: 10.1007/BF00576964. [DOI] [PubMed]
  29. Whittaker JR (1975) Siphon regeneration in Ciona. Nature 255:224–225. https://doi.org/10.1038/255224a0 doi: 10.1038/255224a0. [DOI] [PubMed]
  30. Sutton MF (1953) The regeneration of the siphon of Ciona intestinalis. J Mar Biol Ass UK 32:249–268
  31. Gordon T, Manni L, Shenkar N (2019) Regeneration ability in four stolidobranch ascidians: ecological and evolutionary implications. J Exp Mar Bio Ecol 519:151184. https://doi.org/10.1016/j.jembe.2019.151184 doi: 10.1016/j.jembe.2019.151184. [DOI]
  32. Jeffery WR (2015) Distal regeneration involves the age dependent activity of branchial sac stem cells in the ascidian Ciona intestinalis. Regeneration 2:1–18. https://doi.org/10.1002/reg2.26 doi: 10.1002/reg2.26. [DOI] [PMC free article] [PubMed]
  33. Jeffery WR (2015) Closing the wounds: one hundred and twenty-five years of regenerative biology in the ascidian Ciona intestinalis. Genesis 53:48–65. https://doi.org/10.1002/dvg.22799 doi: 10.1002/dvg.22799. [DOI] [PMC free article] [PubMed]
  34. Brunetti R, Gissi C, Pennati R, Caicci F, Gasparini F, Manni L (2015) Morphological evidence that the molecularly determined Ciona intestinalis type a and type B are different species: Ciona robusta and Ciona intestinalis. J Zool Syst Evol Res 53:186–193. https://doi.org/10.1111/jzs.12101 doi: 10.1111/jzs.12101. [DOI]
  35. Giard A (1872) Recherches sur les Ascidies composées. Arch zool exp 1:566 ff
  36. Driesch H (1902) Über ein neues harmonisch-äquipotentielles System und über solche Systeme überhaupt. Arch Entwickleungsmechanik der Org 14:227–246. https://doi.org/10.1007/BF02162038 doi: 10.1007/BF02162038. [DOI]
  37. Della Valle P (1914) Studii sui rapporti fra differenziazione e rigenerazione - 3. Lo sviluppo di segmenti isolati di stolone di Clavelina di lunghezza diversa e di calibro eguale. Boll della Soc di Nat Napoli 27:195–237
  38. Della Valle P (1915) Studii sui rapporti fra differenziazione e rigenerazione - 4. Le restituzioni dei cespugli di ramificazioni stoloniali di Clavelina. Boll della Soc dei Nat Napoli 28:49–82
  39. Huxley JS (1921) Studies in dedifferentiation. II. Dedifferentiation and resorption in Perophora. J Cell Sci 65(260):643–697
  40. Goldin A (1948) Regeneration in Perophora viridis. Biol Bull 94:184–193. https://doi.org/10.2307/1538246 doi: 10.2307/1538246. [DOI] [PubMed]
  41. Savigny JC (1816) Recherches anatomiques sur les ascidies composées et sur les ascidies simples - Système de la classe des Ascidies. In: Mémoires sur les Animaux sans Vertèbres, vol 2. G. Dufour, Paris, pp 1–229
  42. Bancroft FW (1903) Aestivation of Botrylloides gascoi Della Valle. Mark Anniv, vol 147–166. H. Holt, New York
  43. Herdman EC (1925) Botryllus. Trans Liverp Biol Soc Proc 39:201–236
  44. Oka H, Watanabe H (1957) Vascular budding, a new type of budding in Botryllus. Biol Bull 112:225–240. https://doi.org/10.2307/1539200 doi: 10.2307/1539200. [DOI]
  45. Sunanaga T, Saito Y, Kawamura K (2006) Postembryonic epigenesis of vasa-positive germ cells from aggregated hemoblasts in the colonial ascidian, Botryllus primigenus. Develop Growth Differ 48:87–100. https://doi.org/10.1111/j.1440-169X.2006.00849.x doi: 10.1111/j.1440-169X.2006.00849.x. [DOI] [PubMed]
  46. Sunanaga T, Satoh M, Kawamura K (2008) The role of Nanos homologue in gametogenesis and blastogenesis with special reference to male germ cell formation in the colonial ascidian, Botryllus primigenus. Dev Biol 324:31–40. https://doi.org/10.1016/j.ydbio.2008.08.023 doi: 10.1016/j.ydbio.2008.08.023. [DOI] [PubMed]
  47. Sunanaga T, Inubushi H, Kawamura K (2010) Piwi -expressing hemoblasts serve as germline stem cells during postembryonic germ cell specification in colonial ascidian, Botryllus primigenus. Dev Growth Differ 52:603–614. https://doi.org/10.1111/j.1440-169X.2010.01196.x doi: 10.1111/j.1440-169X.2010.01196.x. [DOI] [PubMed]
  48. Milkman R, Byrne S (1961) Recent observations on Botryllus schlosseri. Biol Bull 121:376
  49. Milkman R (1967) Genetic and developmental studies on Botryllus schlosseri. Biol Bull 132:229–243. https://doi.org/10.2307/1539891 doi: 10.2307/1539891. [DOI] [PubMed]
  50. Sabbadin A, Zaniolo G, Majone F (1975) Determination of polarity and bilateral asymmetry in palleal and vascular buds of the ascidian Botryllus schlosseri. Dev Biol 46:79–87. https://doi.org/10.1016/0012-1606(75)90088-3 doi: 10.1016/0012-1606(75)90088-3. [DOI] [PubMed]
  51. Ricci L, Cabrera F, Lotito S, Tiozzo S (2016) Redeployment of germ layers related TFs shows regionalized expression during two non-embryonic developments. Dev Biol 416:235–248. https://doi.org/10.1016/j.ydbio.2016.05.016 doi: 10.1016/j.ydbio.2016.05.016. [DOI] [PubMed]
  52. Kassmer SH, Langenbacher AD, De Tomaso AW (2020) Integrin-alpha-6+ candidate stem cells are responsible for whole body regeneration in the invertebrate chordate Botrylloides diegensis. Nat Commun 11:4435. https://doi.org/10.1038/s41467-020-18288-w doi: 10.1038/s41467-020-18288-w. [DOI] [PMC free article] [PubMed]
  53. Rosner A, Kravchenko O, Rinkevich B (2019) IAP genes partake weighty roles in the astogeny and whole body regeneration in the colonial urochordate Botryllus schlosseri. Dev Biol 448:320–341. https://doi.org/10.1016/j.ydbio.2018.10.015 doi: 10.1016/j.ydbio.2018.10.015. [DOI] [PubMed]
  54. Majone F (1977) Regeneration of isolated bud fragments of Botryllus schlosseri. Acta Embryol Exp (Palermo):11–19 [PubMed]
  55. Ries E (1937) Untersuchungen Über den Zelltod II - Das Verhalten differenzierter und undifferenzierter Zellen bei der Regeneration, Reduktion und Knospung von Clavelina lepadiformis. Wilhelm Roux Arch Entwickl Mech Org 137:327–362. https://doi.org/10.1007/BF00593065 doi: 10.1007/BF00593065. [DOI] [PubMed]
  56. Scelzo M, Alié A, Pagnotta S, Lejeune C, Henry P, Gilletta L, Hiebert LS, Mastrototaro F, Tiozzo S (2019) Novel budding mode in Polyandrocarpa zorritensis: a model for comparative studies on asexual development and whole body regeneration. EvoDevo 10:7. https://doi.org/10.1186/s13227-019-0121-x doi: 10.1186/s13227-019-0121-x. [DOI] [PMC free article] [PubMed]
  57. Sabbadin A (1956) Effetti dell’estirpazione delle gemme sulla durata del ciclo vitale in Botryllus schlosseri (pallas). Bolletino di Zool 23:331–342. https://doi.org/10.1080/11250005609439244 doi: 10.1080/11250005609439244. [DOI]
  58. Sabbadin A (1958) Analisi sperimentale dello sviluppo delle colonie di Botryllus schlosseri (Pallas) [Ascidiacea]. Arch Ital Anat Embriol 58:177–221 [PubMed]
  59. Brien P (1933) Regeneration thoracique chez Archiascidia neapolitana (Julin) Structure du Système nerveux central. Bull Biol Fr Belg 67:100–124
  60. Kawamura K, Hashimoto K, Nakauchi M (1995) Development of irradiated tunicate buds: is cell division cycle required for morphallaxis? Develop Growth Differ 37:487–496. https://doi.org/10.1046/j.1440-169X.1995.t01-4-00003.x doi: 10.1046/j.1440-169X.1995.t01-4-00003.x. [DOI] [PubMed]
  61. Kaneko N, Katsuyama Y, Kawamura K, Fujiwara S (2010) Regeneration of the gut requires retinoic acid in the budding ascidian Polyandrocarpa misakiensis. Develop Growth Differ 52:457–468. https://doi.org/10.1111/j.1440-169X.2010.01184.x doi: 10.1111/j.1440-169X.2010.01184.x. [DOI] [PubMed]
  62. Tiozzo S, Voskoboynik A, Brown FD, De Tomaso AW (2008) A conserved role of the VEGF pathway in angiogenesis of an ectodermally-derived vasculature. Dev Biol 315:243–255. https://doi.org/10.1016/j.ydbio.2007.12.035 doi: 10.1016/j.ydbio.2007.12.035. [DOI] [PMC free article] [PubMed]
  63. Braden BP, Taketa DA, Pierce JD, Kassmer S, Lewis DD, De Tomaso AW (2014) Vascular regeneration in a basal chordate is due to the presence of immobile, bi-functional cells. PLoS One 9:e95460. https://doi.org/10.1371/journal.pone.0095460 doi: 10.1371/journal.pone.0095460. [DOI] [PMC free article] [PubMed]
  64. Zaniolo G, Trentin P (1987) Regeneration of the tunic in the colonial ascidian, Botryllus schlosseri. Acta Embryol Morphol Exper 8:173–180
  65. Gasparini F, Burighel P, Manni L, Zaniolo G (2008) Vascular regeneration and angiogenic-like sprouting mechanism in a compound ascidian is similar to vertebrates. Evol Dev 10:591–605. https://doi.org/10.1111/j.1525-142X.2008.00274.x doi: 10.1111/j.1525-142X.2008.00274.x. [DOI] [PubMed]
  66. Bourchard-Madrelle C (1966) Régéneration de l’ovaire chez une ascidie simple Ciona intestinalis L. (Protochordé). Bull Soc Zool Fr 91:107–114
  67. Bollner T, Beesley PW, Thorndyke MC (1992) Pattern of substance P- and cholecystokinin-like immunoreactivity during regeneration of the neural complex in the ascidian Ciona intestinalis. J Comp Neurol 325:572–580 doi: 10.1002/cne.903250409. [DOI] [PubMed]
  68. Bollner T, Howalt S, Thorndyke MC, Beesley PW (1995) Regeneration and post-metamorphic development of the central nervous system in the protochordate Ciona intestinalis: a study with monoclonal antibodies. Cell Tissue Res 279:421–432. https://doi.org/10.1007/BF00318500 doi: 10.1007/BF00318500. [DOI] [PubMed]
  69. Dahlberg C, Auger H, Dupont S, Sasakura Y, Thorndyke M, Joly JS (2009) Refining the Ciona intestinalis model of central nervous system regeneration. PLoS One 4:e4458. https://doi.org/10.1371/journal.pone.0004458 doi: 10.1371/journal.pone.0004458. [DOI] [PMC free article] [PubMed]
  70. Medina BNSP, Santos de Abreu I, Cavalcante LA, Silva WAB, da Fonseca RN, Allodi S, de Barros CM (2015) 3-acetylpyridine-induced degeneration in the adult ascidian neural complex: reactive and regenerative changes in glia and blood cells. Dev Neurobiol 75:877–893. https://doi.org/10.1002/dneu.22255 doi: 10.1002/dneu.22255. [DOI] [PubMed]
  71. Rinkevich B, Shlemberg Z, Fishelson L (1995) Whole-body protochordate regeneration from totipotent blood cells. Proc Natl Acad Sci U S A 92:7695–7699. https://doi.org/10.1073/pnas.92.17.7695 doi: 10.1073/pnas.92.17.7695. [DOI] [PMC free article] [PubMed]
  72. Brown FD, Keeling EL, Le AD, Swalla BJ (2009) Whole body regeneration in a colonial ascidian, Botrylloides violaceus. J Exp Zool Part B Mol Dev Evol 312:885–900. https://doi.org/10.1002/jez.b.21303 doi: 10.1002/jez.b.21303. [DOI] [PubMed]
  73. Rinkevich Y, Paz G, Rinkevich B, Reshef R (2007) Systemic bud induction and retinoic acid signaling underlie whole body regeneration in the urochordate Botrylloides leachi. PLoS Biol 5:e71. https://doi.org/10.1371/journal.pbio.0050071 doi: 10.1371/journal.pbio.0050071. [DOI] [PMC free article] [PubMed]
  74. Rinkevich Y, Rosner A, Rabinowitz C, Lapidot Z, Moiseeva E, Rinkevich B (2010) Piwi positive cells that line the vasculature epithelium, underlie whole body regeneration in a basal chordate. Dev Biol 345:94–104. https://doi.org/10.1016/j.ydbio.2010.05.500 doi: 10.1016/j.ydbio.2010.05.500. [DOI] [PubMed]
  75. Ricci L, Chaurasia A, Lapébie P, Dru P, Helm RR, Copley RR, Tiozzo S (2016) Identification of differentially expressed genes from multipotent epithelia at the onset of an asexual development. Sci Rep 6:1–10. https://doi.org/10.1038/srep27357 doi: 10.1038/srep27357. [DOI] [PMC free article] [PubMed]
  76. Zondag LE, Rutherford K, Gemmell NJ, Wilson MJ (2016) Uncovering the pathways underlying whole body regeneration in a chordate model, Botrylloides leachi using de novo transcriptome analysis. BMC Genomics 17:114. https://doi.org/10.1186/s12864-016-2435-6 doi: 10.1186/s12864-016-2435-6. [DOI] [PMC free article] [PubMed]
  77. Zondag L, Clarke RM, Wilson MJ (2019) Histone deacetylase activity is required for Botrylloides leachii whole-body regeneration. J Exp Biol 222:jeb203620. https://doi.org/10.1242/jeb.203620 doi: 10.1242/jeb.203620. [DOI] [PubMed]
  78. Gasparini F, Caicci F, Rigon F, Zaniolo G, Manni L (2014) Testing an unusual in vivo vessel network model: a method to study angiogenesis in the colonial tunicate Botryllus schlosseri. Sci Rep 4:1–11. https://doi.org/10.1038/srep06460 doi: 10.1038/srep06460. [DOI] [PMC free article] [PubMed]
  79. Rinkevich B, Weissman IL (1987) The fate of Botryllus (Ascidiacea) larvae co-settled with parental colonies: beneficial or deleterious consequences? Biol Bull 173:474–488 doi: 10.2307/1541694. [DOI] [PubMed]
  80. Auger H, Sasakura Y, Joly J-S, Jeffery WR (2010) Regeneration of oral siphon pigment organs in the ascidian Ciona intestinalis. Dev Biol 339:374–389. https://doi.org/10.1016/j.ydbio.2009.12.040 doi: 10.1016/j.ydbio.2009.12.040. [DOI] [PMC free article] [PubMed]
  81. Jeffery WR (2015) Regeneration, stem cells, and aging in the tunicate Ciona: Insights from the Oral Siphon. Int Rev Cell Mol Biol 319:255–282 doi: 10.1016/bs.ircmb.2015.06.005. [DOI] [PubMed]
  82. Jeffery WR (2015) The tunicate Ciona: a model system for understanding the relationship between regeneration and aging. Invertebr Reprod Dev 59:17–22. https://doi.org/10.1080/07924259.2014.925515 doi: 10.1080/07924259.2014.925515. [DOI] [PMC free article] [PubMed]
  83. Hamada M, Goricki S, Byerly MS, Satoh N, Jeffery WR (2015) Evolution of the chordate regeneration blastema: differential gene expression and conserved role of notch signaling during siphon regeneration in the ascidian Ciona. Dev Biol 405:304–315. https://doi.org/10.1016/j.ydbio.2015.07.017 doi: 10.1016/j.ydbio.2015.07.017. [DOI] [PMC free article] [PubMed]
  84. Spina EJ, Guzman E, Zhou H, Kosik KS, Smith WC (2017) A microRNA-mRNA expression network during oral siphon regeneration in Ciona. Development 144:1787–1797. https://doi.org/10.1242/dev.144097 doi: 10.1242/dev.144097. [DOI] [PMC free article] [PubMed]
  85. Driesch H (1905) Skizzen zur Restitutionslehre. Arch Entwicklungsmechanik der Org 20:21–29. https://doi.org/10.1007/BF02162639 doi: 10.1007/BF02162639. [DOI]
  86. Driesch H (1902) Studien über das Regulationsvermögen der Organismen. Arch Entwicklungsmechanik der Org 14:532–538. https://doi.org/10.1007/bf02188502 doi: 10.1007/bf02188502. [DOI]
  87. Schultz E (1907) Über Reductionen - III. Die Reduction und Regeneration des abgeschnittenen Kiemenkorbes von Clavellina lepadiformis. Arch Entwicklungsmechanik der Org 24:503–523. https://doi.org/10.1007/BF02289889 doi: 10.1007/BF02289889. [DOI]
  88. Spek J (1927) Über die Winterknospenentwicklung, Regeneration und Reduktion bei Clavellina lepadiformis und die Bedeutung besonderer “omnipotenter” Zellelemente für diese Vorgänge. Wilhelm Roux’Archiv Entwicklungsmechanik der Org 111(119):172 doi: 10.1007/BF02080948. [DOI] [PubMed]
  89. Fischer I (1937) Über das Verhalten des stolonialen Gewebes der Ascidie Clavelina lepadiformis in vitro. Wilhelm Roux Arch Entwickl Mech Org 137:383–403. https://doi.org/10.1007/BF00593068 doi: 10.1007/BF00593068. [DOI] [PubMed]

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