Skip to main content

Insights into Germline Development and Differentiation in Molluscs and Reptiles: The Use of Molecular Markers in the Study of Non-model Animals

  • Chapter
  • First Online:
Evo-Devo: Non-model Species in Cell and Developmental Biology

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 68))

Abstract

When shifting research focus from model to non-model species, many differences in the working approach should be taken into account and usually methodological modifications are required because of the lack of genetics/genomics and developmental information for the vast majority of organisms. This lack of data accounts for the largely incomplete understanding of how the two components—genes and developmental programs—are intermingled in the process of evolution. A deeper level of knowledge was reached for a few model animals, making it possible to understand some of the processes that guide developmental changes during evolutionary time. However, it is often difficult to transfer the obtained information to other, even closely related, animals. In this chapter, we present and discuss some examples, such as the choice of molecular markers to be used to characterize differentiation and developmental processes. The chosen examples pertain to the study of germline in molluscs, reptiles, and other non-model animals.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 189.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alié A, Hayashi T, Sugimura I, Manuel M, Sugano W et al (2015) The ancestral gene repertoire of animal stem cells. Proc Natl Acad Sci USA 112:E7093–E7100

    PubMed  Google Scholar 

  • Allen JF (1996) Separate sexes and the mitochondrial theory of ageing. J Theor Biol 180:135–140

    Article  CAS  PubMed  Google Scholar 

  • Amikura R, Kashikawa M, Nakamura A, Kobayashi S (2001) Presence of mitochondria-type ribosomes outside mitochondria in germ plasm of Drosophila embryos. Proc Natl Acad Sci USA 98:9133–9138

    Article  CAS  PubMed  Google Scholar 

  • Amikura R, Sato K, Kobayashi S (2005) Role of mitochondrial ribosome-dependent translation in germline formation in Drosophila embryos. Mech Dev 122:1087–1093

    Article  CAS  PubMed  Google Scholar 

  • Andreuccetti P, Taddei C, Filosa S (1978) Intercellular bridges between follicle cells and oocyte during the differentiation of follicular epithelium in Lacerta sicula. J Cell Sci 33:341–350

    CAS  PubMed  Google Scholar 

  • Bachvarova RF, Masi T, Drum M, Parker N, Mason K et al (2004) Gene expression in the axolotl germ line: Axdazl, Axvh, Axoct-4, and Axkit. Dev Dyn 231:871–880

    Article  CAS  PubMed  Google Scholar 

  • Bachvarova RF, Crother BI, Johnson AD (2009a) Evolution of germ cell development in tetrapods: comparison of urodeles and amniotes. Evol Dev 11:603–609

    Article  PubMed  Google Scholar 

  • Bachvarova RF, Crother BI, Manova K, Chatfield J et al (2009b) Expression of Dazl and Vasa in turtle embryos and ovaries: evidence for inductive specification of germ cells. Evol Dev 11:525–534

    Article  CAS  PubMed  Google Scholar 

  • Bilinski SM, Kloc M, Tworzydlo W (2017) Selection of mitochondria in female germline cells: is Balbiani body implicated in this process? J Assist Reprod Genet 34:1405–1412

    Article  PubMed  PubMed Central  Google Scholar 

  • Blackler AW (1958) Contribution to the study of germ-cells in the anura. J Embryol Exp Morphol 6:491–503

    CAS  PubMed  Google Scholar 

  • Bounoure L (1934) Recherches sur la lignée germinale chez la grenouille rousse aux premiers stades du développement. Ann Sci Nat 17:67–248

    Google Scholar 

  • Braat AK, Speksnijder JE, Zivkovic D (1999) Germ line development in fishes. Int J Dev Biol 43:745–760

    CAS  PubMed  Google Scholar 

  • Cao L, Kenchington E, Zouros E (2004) Differential segregation patterns of sperm mitochondria in embryos of the blue mussel (Mytilus edulis). Genetics 166:883–894

    Article  PubMed  PubMed Central  Google Scholar 

  • Cherif-Feildel M, Kellner K, Goux D, Elie N, Adeline B, Lelong C, Heude Berthelin C (2018) Morphological and molecular criteria allow the identification of putative germ stem cells in a lophotrochozoan, the Pacific oyster Crassostrea gigas. Histochem Cell Biol 151(5):419–433. https://doi.org/10.1007/s00418-018-1740-3

    Article  PubMed  CAS  Google Scholar 

  • Chiquoine AD (1954) The identification, origin, and migration of the primordial germ cells in the mouse embryo. Anat Rec 118:135–146

    Article  CAS  PubMed  Google Scholar 

  • Chuva de Sousa Lopes SM, Roelen BA (2010) On the formation of germ cells: the good, the bad and the ugly. Differentiation 79:131–140

    Article  PubMed  CAS  Google Scholar 

  • Cinalli RM, Rangan P, Lehmann R (2008) Germ cells are forever. Cell 132:559–562

    Article  CAS  PubMed  Google Scholar 

  • Cogswell AT, Kenchington ELR, Zouros E (2006) Segregation of sperm mitochondria in two- and four-cell embryos of the blue mussel Mytilus edulis: implications for the mechanism of doubly uniparental inheritance of mitochondrial DNA. Genome 49:799–807

    Article  CAS  PubMed  Google Scholar 

  • Cox RT, Spradling AC (2003) A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development 130:1579–1590

    Article  CAS  PubMed  Google Scholar 

  • Davidson EH (2001) Genomic regulatory systems: development and evolution. Academic, San Diego

    Google Scholar 

  • De Felici M (2010) Germ stem cells in the mammalian adult ovary: considerations by a fan of the primordial germ cells. Mol Hum Reprod 16:632–636

    Article  PubMed  CAS  Google Scholar 

  • de Paula WBM, Agip A-NA, Missirlis F, Ashworth R, Vizcay-Barrena G, Lucas CH, Allen JF (2013) Female and male gamete mitochondria are distinct and complementary in transcription, structure, and genome function. Genome Biol Evol 5:196–1977

    Article  CAS  Google Scholar 

  • de Sousa Lopes SM, Hayashi K, Surani MA (2007) Proximal visceral endoderm and extraembryonic ectoderm regulate the formation of primordial germ cell precursors. BMC Dev Biol 7:140–148

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Devauchelle N (1990) Sexual development and maturity of Tapes philippinarum, chapter 3. In: Tapes philippinarum, biologia e sperimentazione. Ente Sviluppo Agricolo Veneto (ESAV), Regione Veneto

    Google Scholar 

  • Ding D, Whittaker KL, Lipshitz HD (1994) Mitochondrially encoded 16S large ribosomal RNA is concentrated in the posterior polar plasm of early Drosophila embryos but is not required for pole cell formation. Dev Biol 163:503–515

    Article  CAS  PubMed  Google Scholar 

  • Eddy EM (1975) Germ plasm and the differentiation of the germ cell line. Int Rev Cytol 43:229–280

    Article  CAS  PubMed  Google Scholar 

  • Ernoult-Lange M, Bénard M, Kress M, Weil D (2012) P-bodies and mitochondria: which place in RNA interference? Biochimie 94:1572e1577

    Article  CAS  Google Scholar 

  • Eulalio A, Behm-Ansmant I, Izaurralde E (2007) P bodies: at the crossroads of post-transcriptional pathways. Nat Rev Mol Cell Biol 8:9–22

    Article  CAS  PubMed  Google Scholar 

  • Ewen-Campen B, Schwager EE, Extavour CGM (2010) The molecular machinery of germ line specification. Mol Reprod Dev 77:3–18

    Article  CAS  PubMed  Google Scholar 

  • Extavour CGM (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884

    Article  CAS  PubMed  Google Scholar 

  • Extavour CGM (2007) Evolution of the bilaterian germ line: lineage origin and modulation of specification mechanisms. Integr Comp Biol 47:770–785

    Article  PubMed  Google Scholar 

  • Extavour CGM (2008) Urbisexuality: the evolution of bilaterian germ cell specification and reproductive systems. In: Minelli A, Fusco G (eds) Evolving pathways: key themes in evolutionary developmental biology. Cambridge University Press, Cambridge, pp 321–342

    Chapter  Google Scholar 

  • Extavour C, Akam ME (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884

    Article  CAS  PubMed  Google Scholar 

  • Fabioux C, Corporeau C, Quillien V, Favrel P, Huvet A (2009) In vivo RNA interference in oyster—vasa silencing inhibits germ cell development. FEBS J 276:2566–2573

    Article  CAS  PubMed  Google Scholar 

  • Fierro-Constaín L, Schenkelaars Q, Gazave E, Haguenauer A, Rocher C, Ereskovsky A, Borchiellini C, Renard E (2017) The conservation of the germline multipotency program, from sponges to vertebrates: a stepping stone to understanding the somatic and germline origins. Genome Biol Evol 9:474–488

    PubMed  PubMed Central  Google Scholar 

  • Filosa S (1973) Biological and cytological aspect of the ovarian cycle in Lacerta sicula Raf. Mon Zool Ital 7:151–165

    Google Scholar 

  • Filosa S, Taddei C, Andreuccetti P (1979) The differentation and proliferation of follicle cells during oocyte growth in Lacerta sicula. J Embryol Exp Morphol 54:5–15

    CAS  PubMed  Google Scholar 

  • Franz JK, Gall L, Williams MA, Picheral B, Franke WW (1983) Intermediate-size filaments in a germ cell: expression of cytokeratins in oocytes and eggs of the frog Xenopus. Proc Natl Acad Sci U S A 80(20):6254–6258

    Article  CAS  Google Scholar 

  • Fujiwara Y, Komiya T, Kawabata H, Sato M, Fujimoto H et al (1994) Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. Proc Natl Acad Sci USA 91:12258–12262

    Article  CAS  PubMed  Google Scholar 

  • Funayama N (2010) The stem cell system in demosponges: insights into the origin of somatic stem cells. Dev Growth Differ 52:1–14

    Article  CAS  PubMed  Google Scholar 

  • Ghiselli F, Milani L, Passamonti M (2011) Strict sex-specific mtDNA segregation in the germline of the DUI species Venerupis philippinarum (Bivalvia Veneridae). Mol Biol Evol 28:949–961

    Article  CAS  PubMed  Google Scholar 

  • Ghiselli F, Milani L, Chang PL, Hedgecock D, Davis JP et al (2012) De novo assembly of the Manila clam Ruditapes philippinarum transcriptome provides new insights into expression bias, mitochondrial doubly uniparental inheritance and sex determination. Mol Biol Evol 29:771–786

    Article  CAS  PubMed  Google Scholar 

  • Ghiselli F, Breton S, Milani L (2018) Mitochondrial activity in gametes and uniparental inheritance—a comment on ‘What can we infer about the origin of sex in early eukaryotes?’. Philos Trans R Soc Lond B Biol Sci 373:20170147

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gomperts M, Garcia-Castro M, Wylie C, Heasman J (1994) Interactions between primordial germ cells play a role in their migration in mouse embryos. Development 120:135–141

    CAS  PubMed  Google Scholar 

  • Gribbins KM (2011) Reptilian spermatogenesis. A histological and ultrastructural perspective. Spermatogenesis 1:250–269

    Article  PubMed  PubMed Central  Google Scholar 

  • Gusman A, Lecomte S, Stewart DT, Passamonti M, Breton S (2016) Pursuing the quest for better understanding the taxonomic distribution of the system of doubly uniparental inheritance of mtDNA. PeerJ 4:e2760

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gustafson EA, Wessel GM (2010) Vasa genes: emerging roles in the germ line and in multipotent cells. BioEssays 32:626–637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hejnol A (2010) A twist in time—the evolution of spiral cleavage in the light of animal phylogeny. Integr Comp Biol 50:695–706

    Article  PubMed  Google Scholar 

  • Herpin A, Rohr S, Riedel D, Kluever N, Raz E et al (2007) Specification of primordial germ cells in medaka (Oryzias latipes). BMC Dev Biol 7:3

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang L, Mollet S, Souquere S, Le Roy F, Ernoult-Lange M et al (2011) Mitochondria associate with P-bodies and modulate MicroRNA-mediated RNA interference. J Biol Chem 286:24219–24230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubert J (1985) Origin and development of oocytes. In: Gans C, Billet F, Maderson PFA (eds) Biology of the Reptilia: development A, vol 14. Wiley, New York, pp 42–74

    Google Scholar 

  • Iida T, Kobayashi S (1998) Essential role of mitochondrially encoded large rRNA for germ-line formation in Drosophila embryos. Proc Natl Acad Sci USA 95:11274–11278

    Article  CAS  PubMed  Google Scholar 

  • Ikenishi K, Tanaka TS (1997) The cause of the decreased number of primordial germ cells in albino Xenopus resides not in the micro-environment but in the presumptive PGC. Dev Growth Differ 39:345–349

    Article  CAS  PubMed  Google Scholar 

  • Ikenishi K, Kotani M, Tanabe K (1974) Ultrastructural changes associated with UV irradiation in the “germinal plasm” of Xenopus laevis. Dev Biol 36:155–168

    Article  CAS  PubMed  Google Scholar 

  • Isaeva VV, Reunov AA (2001) Germ plasm and germ-line cell determination: the role of mitochondria. Russ J Mar Biol 27:S8–S14

    Article  Google Scholar 

  • Johnson AD, Drum M, Bachvarova RF, Masi T, White ME et al (2003) Evolution of predetermined germ cells in vertebrate embryos: implications for macroevolution. Evol Dev 5:414–431

    Article  PubMed  Google Scholar 

  • Johnson AD, Richardson E, Bachvarova RF, Crother BI (2011) Evolution of the germ line-soma relationship in vertebrate embryos. Reproduction 141:291–300

    Article  CAS  PubMed  Google Scholar 

  • Johnstone O, Lasko P (2004) Interaction with eIF5B is essential for Vasa function during development. Development 131:4167–4178

    Article  CAS  PubMed  Google Scholar 

  • Juliano C, Wessel G (2010) Versatile germline genes. Science 329:640–641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Juliano CE, Swartz SZ, Wessel GM (2010) A conserved germline multipotency program. Development 137:4113–4126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kemp A (1982) The embryological development of the Queensland lungfish, Neoceratodus forsteri (krefft). Mem Queensl Mus 20:553–598

    Google Scholar 

  • Kitauchi T, Saito T, Motomura T, Arai K, Yamaha E (2012) Distribution and function of germ plasm in cytoplasmic fragments from centrifuged eggs of the goldfish, Carassius auratus. J Appl Ichthyol 28:998–1005

    Article  Google Scholar 

  • Kloc M, Larabell C, Pui-Yee Chan A, Etkin LD (1998) Contribution of METRO pathway localized molecules to the organization of the germ cell lineage. Mech Dev 75:81–93

    Article  CAS  PubMed  Google Scholar 

  • Kloc M, Zearfoss NR, Etkin LD (2002) Mechanisms of subcellular mRNA localization. Cell 108:533–544

    Article  CAS  PubMed  Google Scholar 

  • Kloc M, Bilinski S, Etkin LD (2004) The Balbiani body and germ cell determinants: 150 years later. Curr Top Dev Biol 59:1–36

    Article  CAS  PubMed  Google Scholar 

  • Kloc M, Jaglarz M, Dougherty M, Stewart MD, Nel-Themaat L et al (2008) Mouse early oocytes are transiently polar: three-dimensional and ultrastructural analysis. Exp Cell Res 314:3245–3254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi S, Amikura R, Okada M (1993) Presence of mitochondrial large ribosomal RNA outside mitochondria in germ plasm of Drosophila melanogaster. Science 260:1521–1524

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi S, Amikura R, Mukai M (1998) Localization of mitochondrial RNA in germ plasm of Xenopus embryos. Curr Biol 8:1117–1120

    Article  CAS  PubMed  Google Scholar 

  • Kotaja N, Sassone-Corsi P (2007) The chromatoid body: a germ-cell-specific RNA-processing centre. Nat Rev Mol Cell Biol 8:85–90

    Article  CAS  PubMed  Google Scholar 

  • Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Takamatsu K, Chuma S et al (2010) MVH in piRNA processing and gene silencing of retrotransposons. Genes Dev 24:887–892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lasko P (2013) The DEAD-box helicase Vasa: evidence for a multiplicity of functions in RNA processes and developmental biology. Biochim Biophys Acta 1829:810–816

    Article  CAS  PubMed  Google Scholar 

  • Lasko PF, Ashburner M (1990) Posterior localization of Vasa protein correlates with, but is not sufficient for, pole cell development. Genes Dev 4:905–921

    Article  CAS  PubMed  Google Scholar 

  • Lavial F, Acloque H, Bachelard E, Nieto A, Samarut J et al (2009) Ectopic expression of Cvh (Vasa, Chicken homologue) mediates the reprogramming of chicken embryonic stem cells to a germ cell fate. Dev Biol 330:73–82

    Article  CAS  PubMed  Google Scholar 

  • Lawson KA, Hage WJ (1994) Clonal analysis of the origin of primordial germ cells in the mouse. Ciba Found Symp 182:68–84

    CAS  PubMed  Google Scholar 

  • Lawson KA, Dunn NR, Roelen BAJ, Zeinstra LM, Davis AM et al (1999) Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev 13:424–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leclère L, Jager M, Barreau C, Chang P, Le Guyader H et al (2012) Maternally localized germ plasm mRNAs and germ cell/stem cell formation in the cnidarian Clytia. Dev Biol 364:236–248

    Article  PubMed  CAS  Google Scholar 

  • Leitch HG, Blair K, Mansfield W, Ayetey H, Humphreys P, Nichols J, Surani MA, Smith A (2010) Embryonic germ cells from mice and rats exhibit properties consistent with a generic pluripotent ground state. Development 137:2279–2287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Zhang P, Wu X, Zhu X, Xu H (2017) A novel dynamic expression of vasa in male germ cells during spermatogenesis in the Chinese soft-shell turtle (Pelidiscus sinensis). J Exp Zool B Mol Dev Evol 328:230–239

    Article  CAS  PubMed  Google Scholar 

  • Liang L, Diehl-Jones W, Lasko PF (1994) Localization of vasa protein to the Drosophila pole plasm is independent of its RNA-binding and helicase activities. Development 120:1201–1211

    CAS  PubMed  Google Scholar 

  • Linder P, Fuller-Pace FV (2013) Looking back on the birth of DEAD-box RNA helicases. Biochim Biophys Acta 1829:750–755

    Article  CAS  PubMed  Google Scholar 

  • Lyons DC, Perry KJ, Lesoway MP, Henry JQ (2012) Cleavage pattern and fate map of the mesentoblast, 4d, in the gastropod Crepidula: a hallmark of spiralian development. EvoDevo 3:21

    Article  PubMed  PubMed Central  Google Scholar 

  • MacAskill AF, Kittler JT (2009) Control of mitochondrial transport and localization in neurons. Trends Cell Biol 20:102–112

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Juárez A, López-Luna MA, Porras-Gómez TJ, Moreno-Mendoza N (2018) Expression of the Sox9, Foxl2, Vasa, and TRPV4 genes in the ovaries and testes of the Morelet’s crocodile, Crocodylus moreletii. J Exp Zool B Mol Dev Evol 330:148–164

    Article  PubMed  CAS  Google Scholar 

  • Matsui Y, Zsebo K, Hogan BL (1992) Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell 70:841–847

    Article  CAS  PubMed  Google Scholar 

  • Maurizii MG, Taddei C (1996) Immunolocalization of cytoskeletal proteins in the previtellogenic ovarian follicle of the lizard Podarcis sicula. Cell Tissue Res 284:489–493

    Article  CAS  PubMed  Google Scholar 

  • Maurizii MG, Taddei C (2012) Microtubules organization and nucleation in the differentiating ovarian follicle of the lizard Podarcis sicula. J Morphol 273:1089–1095

    Article  CAS  PubMed  Google Scholar 

  • Maurizii MG, Saverino O, Taddei C (1997) Cytokeratin cytoskeleton in the differentiating ovarian follicle of the lizard Podarcis sicula Raf. Mol Reprod Dev 48:536–542

    Article  CAS  PubMed  Google Scholar 

  • Maurizii MG, Alibardi L, Taddei C (2000) Organization and characterization of the keratin cytoskeleton in the previtellogenic ovarian follicle of the lizard Podarcis sicula Raf. Mol Reprod Dev 57:159–166

    Article  CAS  PubMed  Google Scholar 

  • Maurizii MG, Alibardi L, Taddei C (2004) α-Tubulin and acetylated α-tubulin during ovarian follicle differentiation in the lizard Podarcis sicula Raf. J Exp Zool A Comp Exp Biol 301:532–541

    Article  PubMed  CAS  Google Scholar 

  • Maurizii MG, Cavaliere V, Gamberi C, Lasko P, Gargiulo G et al (2009) Vasa protein is localized in the germ cells and in the oocyte-associated pyriform follicle cells during early oogenesis in the lizard Podarcis sicula. Dev Genes Evol 219:361–367

    Article  PubMed  Google Scholar 

  • Mikedis MM, Downs KM (2014) Mouse primordial germ cells: a reappraisal. Int Rev Cell Mol Biol 309:1–57

    Article  CAS  PubMed  Google Scholar 

  • Milani L (2015) Mitochondrial membrane potential: a trait involved in organelle inheritance? Biol Lett 11:20150732

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Milani L, Ghiselli F (2015) Mitochondrial activity in gametes and transmission of viable mtDNA. Biol Direct 10:22

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Milani L, Maurizii MG (2014a) Differentiating male germ cells during spermatogenesis of a reptile. Mol Reprod Dev 81:777

    Article  CAS  Google Scholar 

  • Milani L, Maurizii MG (2014b) First evidence of Vasa expression in differentiating male germ cells of a reptile. Mol Reprod Dev 81:390

    Article  CAS  Google Scholar 

  • Milani L, Maurizii MG (2015) Vasa expression in spermatogenic cells during the reproductive-cycle phases of Podarcis sicula (Reptilia, Lacertidae). J Exp Zool B Mol Dev Evol 324:424–434

    Article  CAS  PubMed  Google Scholar 

  • Milani L, Ghiselli F, Maurizii MG, Passamonti M (2011) Doubly uniparental inheritance of mitochondria as a model system for studying germ line formation. PLoS One 6:e28194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milani L, Ghiselli F, Passamonti M (2012) Sex-linked mitochondrial behavior during early embryo development in Ruditapes philippinarum (Bivalvia Veneridae) a species with the Doubly Uniparental Inheritance (DUI) of mitochondria. J Exp Zool B Mol Dev Evol 318:182–189

    Article  CAS  PubMed  Google Scholar 

  • Milani L, Ghiselli F, Guerra D, Breton S, Passamonti M (2013) A comparative analysis of mitochondrial ORFans: new clues on their origin and role in species with doubly uniparental inheritance of mitochondria. Genome Biol Evol 5:1408–1434

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Milani L, Ghiselli F, Maurizii MG, Nuzhdin SV, Passamonti M (2014) Paternally transmitted mitochondria express a new gene of potential viral origin. Genome Biol Evol 6:391–405

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Milani L, Maurizii MG, Pecci A, Ghiselli F, Passamonti M (2015a) Localization and dynamics of primordial germ cells in the bivalve species Ruditapes philippinarum. Mol Reprod Dev 82:406–407

    Article  CAS  PubMed  Google Scholar 

  • Milani L, Ghiselli F, Pecci A, Maurizii MG, Passamonti M (2015b) The expression of a novel mitochondrially-encoded gene in gonadic precursors may drive paternal inheritance of mitochondria. PLoS One 10:e0137468

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Milani L, Ghiselli F, Passamonti M (2016) Mitochondrial selfish elements and the evolution of biological novelties. Curr Zool 62:687–697

    Article  PubMed  PubMed Central  Google Scholar 

  • Milani L, Pecci A, Cifaldi C, Maurizii MG (2017a) PL10 DEAD-box protein is expressed during germ cell differentiation in the reptile Podarcis sicula (family Lacertidae). J Exp Zool B Mol Dev Evol 328:433–448

    Article  CAS  PubMed  Google Scholar 

  • Milani L, Pecci A, Ghiselli F, Passamonti M, Bettini S, Franceschini V, Maurizii MG (2017b) VASA expression suggests shared germ line dynamics in bivalve molluscs. Histochem Cell Biol 148:157–171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milani L, Pecci A, Ghiselli F, Passamonti M, Lazzari M, Franceschini V, Maurizii MG (2018) Germ cell line during the seasonal sexual rest of clams: finding niches of cells for gonad renewal. Histochem Cell Biol 149:105–110

    Article  CAS  PubMed  Google Scholar 

  • Minelli A, Fusco G (2008) Evolving Pathways. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Mishra P, Chan DC (2014) Mitochondrial dynamics and inheritance during cell division, development and disease. Nat Rev Mol Cell Biol 15:634–646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monteiro A, Podlaha O (2009) Wings, horns, and butterfly eyespots: how do complex traits evolve? PLoS Biol 7:e37

    Article  PubMed  CAS  Google Scholar 

  • Motta CM, Castriota Scanderberg M, Filosa S, Andreuccetti P (1995) Role of pyriform cells during the growth of oocytes in the lizard Podarcis sicula. J Exp Zool 273:247–256

    Article  Google Scholar 

  • Muller WA, Teo R, Frank U (2004) Totipotent migratory stem cells in a hydroid. Dev Biol 275:215–224

    Article  PubMed  CAS  Google Scholar 

  • Nagamori I, Cruickshank VA, Sassone-Corsi P (2011) Regulation of an RNA granule during spermatogenesis: acetylation of MVH in the chromatoid body of germ cells. J Cell Sci 124:4346–4355

    Article  CAS  PubMed  Google Scholar 

  • Newmark PA, Wang Y, Chong T (2008) Germ cell specification and regeneration in planarians. Cold Spring Harb Symp Quant Biol 73:573–581

    Article  CAS  PubMed  Google Scholar 

  • Nieuwkoop PD, Sutasurya LA (1979) Primordial germ cells in chordates. Cambridge University Press, Cambridge

    Google Scholar 

  • Noce T, Okamoto-Ito S, Tsunekawa N (2001) Vasa homolog genes in mammalian germ cell development. Cell Struct Funct 26:131–136

    Article  CAS  PubMed  Google Scholar 

  • Obata M, Komaru A (2005) Specific location of sperm mitochondria in mussel Mytilus galloprovincialis zygotes stained by MitoTracker. Develop Growth Differ 47:255–263

    Article  Google Scholar 

  • Ogawa M, Amikura R, Akasaka K, Kinoshita T, Kobayashi S, Shimada H (1999) Asymmetrical distribution of mitochondrial rRNA into small micromeres of sea urchin embryos. Zool Sci 16:445–451

    Article  CAS  Google Scholar 

  • Ohinata Y, Payer B, O’Carroll D, Ancelin K, Ono Y et al (2005) Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436:207–213

    Article  CAS  PubMed  Google Scholar 

  • Parvinen M (2005) The chromatoid body in spermatogenesis. Int J Androl 28:189–201

    Article  PubMed  Google Scholar 

  • Pepling ME, Wilhelm JE, O’Hara AL, Gephardt GW, Spradling AC (2007) Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body. Proc Natl Acad Sci USA 104:187–192

    Article  CAS  PubMed  Google Scholar 

  • Punzi E, Milani L, Ghiselli F, Passamonti M (2018) Lose it or keep it: (how bivalves can provide) insights into mitochondrial inheritance mechanisms. J Exp Zool B Mol Dev Evol 330:41–51

    Article  PubMed  Google Scholar 

  • Rayon T, Menchero S, Nieto A, Xenopoulos P, Crespo M et al (2014) Notch and hippo converge on Cdx2 to specify the trophectoderm lineage in the mouse blastocyst. Dev Cell 30:410–422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reunov A (2006) Structures related to the germ plasm in mouse. Zygote 14:231–238

    Article  PubMed  Google Scholar 

  • Reunov AA, Reunova YA (2015) In mouse oocytes the mitochondrion-originated germinal body-like structures accumulate mouse Vasa homologue (MVH) protein. Zygote 23:501–506

    Article  CAS  PubMed  Google Scholar 

  • Reunov A, Isaeva V, Au D, Wu R (2000) Nuage constituents arising from mitochondria: is it possible? Develop Growth Differ 42:139–143

    Article  CAS  Google Scholar 

  • Reunov A, Alexandrova Y, Reunova Y, Komkova A, Milani L (2019) Germ plasm provides clues on meiosis: the concerted action of germ plasm granules and mitochondria in gametogenesis of the clam Ruditapes philippinarum. Zygote 27(1):25–35. https://doi.org/10.1017/S0967199418000588

    Article  CAS  PubMed  Google Scholar 

  • Rink JC (2013) Stem cell systems and regeneration in planaria. Dev Genes Evol 223:67–84

    Article  PubMed  Google Scholar 

  • Saffman EE, Lasko P (1999) Germline development in vertebrates and invertebrates. CMLS 55:1141–1163

    Article  CAS  PubMed  Google Scholar 

  • Saito T, Psenicka M, Goto R, Adachi S, Inoue K et al (2014) The origin and migration of primordial germ cells in sturgeons. PLoS One 9:e86861

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Seki Y, Hayashi K, Itoh K, Mizugaki M, Saitou M et al (2005) Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev Biol 278:440–458

    Article  CAS  PubMed  Google Scholar 

  • Scholtz G (2008) On comparisons and causes in evolutionary developmental biology. In: Minelli A, Fusco G (eds) Evolving pathways: key themes in evolutionary developmental biology. Cambridge University Press, Cambridge, pp 144–159

    Chapter  Google Scholar 

  • Shukalyuk AI, Isaeva VV (2012) Molecular and sub-cellular gametogenic machinery of stem and germline cells across metazoa. In: Najman S (ed) Current frontiers and perspectives in cell biology. InTech, Rijeka. ISBN: 978-953-51-0544-2

    Google Scholar 

  • Solana J (2013) Closing the circle of germline and stem cells: the primordial stem cell hypothesis. Evodevo 4:2

    Article  PubMed  PubMed Central  Google Scholar 

  • Solana J, Kao D, Mihaylova Y, Jaber-Hijazi F, Malla S et al (2012) Defining the molecular profile of planarian pluripotent stem cells using a combinatorial RNA-seq, RNA interference and irradiation approach. Genome Biol 13:R19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sutasurya LA, Nieuwkoop PD (1974) The induction of the primordial germ cells in the urodeles. Wilhelm Roux Arch Entwickl Mech Org 175:199–220

    Article  Google Scholar 

  • Swartz SZ, Wessel GM (2015) Germ line versus soma in the transition from egg to embryo. Curr Top Dev Biol 113:149–190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tada H, Mochii M, Orii H, Watanabe K (2012) Ectopic formation of primordial germ cells by transplantation of the germ plasm: direct evidence for germ cell determinant in Xenopus. Dev Biol 371:86–93

    Article  CAS  PubMed  Google Scholar 

  • Tam PP, Zhou SX (1996) The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. Dev Biol 178:124–132

    Article  CAS  PubMed  Google Scholar 

  • Tanaka SS, Toyooka Y, Akasu R, Katoh-Fukui Y, Nakahara Y et al (2000) The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev 14:841–853

    CAS  PubMed  PubMed Central  Google Scholar 

  • Toyooka Y, Tsunekawa N, Takahashi Y, Matsui Y, Satoh M et al (2000) Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech Dev 93:139–149

    Article  CAS  PubMed  Google Scholar 

  • Tsang TE, Khoo PL, Jamieson RV, Zhou SX, Ang SL et al (2001) The allocation and differentiation of mouse primordial germ cells. Int J Dev Biol 45:549–555

    CAS  PubMed  Google Scholar 

  • Tsunekawa N, Naito M, Sakai Y, Nishida T, Noce T (2000) Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells. Development 127:2741–2750

    CAS  PubMed  Google Scholar 

  • van Wolfswinkel JC (2014) Piwi and potency: PIWI proteins in animal stem cells and regeneration. Integr Comp Biol 54:700–713

    Article  PubMed  CAS  Google Scholar 

  • Venetis C, Theologidis I, Zouros E, Rodakis GC (2006) No evidence for presence of maternal mitochondrial DNA in the sperm of Mytilus galloprovincialis males. Proc Biol Sci 273:2483–2489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Venkatarama T, Lai F, Luo X, Zhou Y, Newman K et al (2010) Repression of zygotic gene expression in the Xenopus germline. Development 137:651–660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner G, Pavlicev M, Cheverud J (2007) The road to modularity. Nat Rev Genet 8:921–931

    Article  CAS  PubMed  Google Scholar 

  • Wessel GM (2016) Germ line mechanics—and unfinished business. Curr Top Dev Biol 117:553–566

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilding M, Carotenuto R, Infante V, Dale B, Marino M et al (2001) Confocal microscopy analysis of the activity of mitochondria contained within the ‘mitochondrial cloud’ during oogenesis in Xenopus laevis. Zygote 9:347–352

    Article  CAS  PubMed  Google Scholar 

  • Wilkins AS (2013) “The genetic tool-kit”: the life-history of an important metaphor, Chapter 1. In: Streelman JT (ed) Advances in evolutionary developmental biology. Wiley, Hoboken, pp 1–14

    Google Scholar 

  • Woodland HR (2016) The birth of animal development: multicellularity and the germline. Curr Top Dev Biol 117:609–630

    Article  PubMed  Google Scholar 

  • Wylie CC, Holwill S, O’Driscoll M, Snape A, Heasman J (1985) Germ plasm and germ cell determination in Xenopus laevis as studied by cell transplantation analysis. Cold Spring Harb Symp Quant Biol 50:37–43

    Article  CAS  PubMed  Google Scholar 

  • Yajima M, Wessel GM (2011) The multiple hats of Vasa: its functions in the germline and in cell cycle progression. Mol Reprod Dev 78:861–867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yajima M, Wessel GM (2015) Essential elements for translation: the germline factor Vasa functions broadly in somatic cells. Development 142:1960–1970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaji M, Seki Y, Kurimoto K, Yabuta Y, Yuasa M et al (2008) Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat Genet 40:1016–1022

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Aguero T, King ML (2015) The Xenopus maternal-to-zygotic transition from the perspective of the germline. Curr Top Dev Biol 113:271–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon C, Kawakami K, Hopkins N (1997) Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development 124:3157–3165

    CAS  PubMed  Google Scholar 

  • Zhang Y-Z, Ouyang Y-C, Hou Y, Schatten H, Chen D-Y et al (2008) Mitochondrial behavior during oogenesis in zebrafish: a confocal microscopy analysis. Develop Growth Differ 50:189–201

    Article  Google Scholar 

  • Zhou RR, Wang B, Wang J, Schatten H, Zhang YZ (2010) Is the mitochondrial cloud the selection machinery for preferentially transmitting wild-type mtDNA between generations? Rewinding Müller’s ratchet efficiently. Curr Genet 56:101–107

    Article  CAS  PubMed  Google Scholar 

  • Zouros E (2013) Biparental inheritance through uniparental transmission: the doubly uniparental inheritance (DUI) of mitochondrial DNA. Evol Biol 40:1–31

    Article  Google Scholar 

Download references

Acknowledgement

We are grateful to Waclaw Tworzydlo and Szczepan Bilinski for inviting this contribution and Malgorzata Kloc for commenting on the manuscript. This work was supported by the Italian Ministry of Education, University and Research MIUR-SIR Programme no. RBSI14G0P5 funded to L.M.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Liliana Milani .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Milani, L., Maurizii, M.G. (2019). Insights into Germline Development and Differentiation in Molluscs and Reptiles: The Use of Molecular Markers in the Study of Non-model Animals. In: Tworzydlo, W., Bilinski, S. (eds) Evo-Devo: Non-model Species in Cell and Developmental Biology. Results and Problems in Cell Differentiation, vol 68. Springer, Cham. https://doi.org/10.1007/978-3-030-23459-1_14

Download citation

Publish with us

Policies and ethics