Skip to main content
Log in

Cleavage, incomplete inversion, and cytoplasmic bridges in Gonium pectorale (Volvocales, Chlorophyta)

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Multicellularity arose several times in evolution of eukaryotes. The volvocine algae have full range of colonial organization from unicellular to colonies, and thus these algae are well-known models for examining the evolution and mechanisms of multicellularity. Gonium pectorale is a multicellular species of Volvocales and is thought to be one of the first small colonial organisms among the volvocine algae. In these algae, a cytoplasmic bridge is one of the key traits that arose during the evolution of multicellularity. Here, we observed the inversion process and the cytoplasmic bridges in G. pectorale using time-lapse, fluorescence, and electron microscopy. The cytoplasmic bridges were located in the middle region of the cell in 2-, 4-, 8-, and 16-celled stages and in inversion stages. However, there were no cytoplasmic bridges in the mature adult stage. Cytoplasmic bridges and cortical microtubules in G. pectorale suggest that a mechanism of kinesin-microtubule machinery similar to that in other volvocine algae is responsible for inversion in this species.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bisalputra T, Stein JR (1966) The development of cytoplasmic bridges in Volvox aureus. Can J Bot 44:1697–1702

    Article  Google Scholar 

  • Deason TR, Darden WH, Ely S (1969) The development of sperm packets of the M5 strain of Volvox aureus. J Ultrastruct Res 26:85–94

    Article  PubMed  CAS  Google Scholar 

  • Fulton AB (1978) Colonial development in Pandorina morum. II. Colony morphogenesis and formation of the extracellular matrix. Dev Biol 64:236–251

    Article  PubMed  CAS  Google Scholar 

  • Gerisch G (1959) Die Zelldifferenzierung bei Pleodorina californica Shaw und die Organisation der Phytomonadinekolonien. Arch Protistenkd 104:292–358

    Google Scholar 

  • Green KJ, Kirk DL (1981) Cleavage patterns, cell lineages, and development of a cytoplasmic bridge system in Volvox embryos. J Cell Biol 91:743–755. doi:10.1083/jcb.91.3.743

    Article  PubMed  CAS  Google Scholar 

  • Green KJ, Viamontes GI, Kirk DL (1981) Mechanism of formation, ultrastructure, and function of the cytoplasmic bridge system during morphogenesis in Volvox. J Cell Biol 91:756–769. doi:10.1083/jcb.91.3.756

    Article  PubMed  CAS  Google Scholar 

  • Greuel BT, Floyd GL (1985) Development of the flagellar apparatus and flagellar orientation in the colonial green alga Gonium pectorale (Volvocales). J Phycol 21:358–371

    Article  Google Scholar 

  • Hallmann A (2006) Morphogenesis in the family Volvocaceae: different tactics for turning an embryo right-side out. Protist 157:445–461. doi:10.1016/j.protis.2006.05.010

    Article  PubMed  Google Scholar 

  • Hallmann A (2011) Evolution of reproductive development in the volvocine algae. Sex Plant Reprod 24:97–112. doi:10.1007/s00497-010-0158-4

    Article  PubMed  CAS  Google Scholar 

  • Harper RA (1912) The structure and development of the colony in Gonium. Trans Am Microsc Soc 31:65–83

    Article  Google Scholar 

  • Harris DO, Starr RC (1969) Life history and physiology of reproduction of Platydorina caudata Kofoid. Arch Protistenkd 111:138–155

    Google Scholar 

  • Hartmann M (1924) Üeber die Veränderung der Koloniebildung von Eudorina elegans und Gonium pectorale unter dem Einfluss äuβerer Bedingungen. Mitt.der Untersuchungen über die Morphologie und Physiologie des Formwechsels der Phytomonadinen (Volvocales). Arch Protistenkd 49:375–395

    Google Scholar 

  • Herron MD, Michod RE (2008) Evolution of complexity in the volvocine algae: transitions in individuality through Darwin’s eye. Evolution 62(2):436–451. doi:10.1111/j.1558-5646.2007.00304.x

    Article  PubMed  Google Scholar 

  • Hoops HJ, Nishii I, Kirk DL (2005) Cytoplasmic bridges in Volvox and its relatives. In: Baluska F, Volkmann D, Barlow PW (eds) Cell–cell channels. Eurekah.com, Georgetown, TX, pp 1–20

    Google Scholar 

  • Iida H, Nishii I, Inouye I (2011) Embryogenesis and cell positioning in Platydorina caudata (Volvocaceae, Chlorophyta). Phycologia 50:530–540. doi:10.2216/10-80.1

    Article  Google Scholar 

  • Kelland JL (1977) Inversion in Volvox (Chlorophyceae). J Phycol 13:373–378. doi:10.1111/j.1529-8817.1977.tb00614.x

    Google Scholar 

  • Kirk DL (1998) Volvox: molecular-genetic origins of multicellularity and cellular differentiation. Developmental and cell biology series. Cambridge University Press, Cambridge

    Google Scholar 

  • Kirk DL (2005) A twelve-step program for evolving multicellularity and a division of labor. BioEssays 27:299–310. doi:10.1002/bies.20197

    Article  PubMed  Google Scholar 

  • Kirk DL, Kirk MM (1983) Protein synthetic patterns during the asexual life cycle of Volvox carteri. Dev Biol 96:493–506. doi:10.1016/0012-1606(83)90186-0

    Article  PubMed  CAS  Google Scholar 

  • Kirk DL, Nishii I (2001) Volvox carteri as a model for studying the genetic and cytological control of morphogenesis. Dev Growth Differ 43:621–631

    Article  PubMed  CAS  Google Scholar 

  • Kirk DL, Viamontes GI, Green KJ, Bryant JL Jr (1982) Integrated morphogenetic behavior of cell sheets: Volvox as a model. In: Subtelny S, Green PB (eds) Developmental order: Its Origin and Regulation. Alan R. Liss, New York, pp 247–274

    Google Scholar 

  • Lang NJ (1963) Electron microscopy of the Volvocaceae and Astrephomaneceae. Am J Bot 50:280–300

    Article  Google Scholar 

  • Marchant HJ (1977) Colony formation and inversion in the green alga Eudorina elegans. Protoplasma 93:325–339

    Article  Google Scholar 

  • Meyer A (1896) Die Plasmaverbindung und die Membranen von Volvox. Bot Zeitg 54:187–217

    Google Scholar 

  • Nishii I, Ogihara S (1999) Actomyosin contraction of the posterior hemisphere is required for inversion of the Volvox embryo. Development 126:2117–2127

    PubMed  CAS  Google Scholar 

  • Nishii I, Ogihara S, Kirk DL (2003) A kinesin, InvA, plays an essential role in Volvox morphogenesis. Cell 113:743–753. doi:10.1016/S0092-8674(03)00431-8

    Article  PubMed  CAS  Google Scholar 

  • Nozaki H (2003) Origin and evolution of the genera Pleodorina and Volvox (Volvocales). Biologia (Bratislava) 58:425–431

    CAS  Google Scholar 

  • Pickett-Heaps JD (1970) Some ultrastructural features of Volvox, with particular reference to the phenomenon of inversion. Planta 90:174–190

    Article  Google Scholar 

  • Pocock MA (1933) Volvox in South Africa. Ann S Afr Mus 16:523–646

    Google Scholar 

  • Pocock MA (1955) Studies in North American Volvocales. I. The genus Gonium. Madroño 13:49–64

    Google Scholar 

  • Stein JR (1958) A morphologic and genetic study of Gonium pectorale. Am J Bot 45:664–672

    Article  Google Scholar 

  • Stein JR (1965) On cytoplasmic strands in Gonium pectorale (Volvocales). J Phycol 1:1–5. doi:10.1111/j.1529-8817.1965.tb04547.x

    Article  Google Scholar 

  • Taft CE (1940) Asexual and sexual reproduction in Platydorina caudata Kofoid. Trans Am Microsc Soc 59:1–11

    Article  Google Scholar 

  • Taylor MG, Floyd GL, Hoops HJ (1985) Development of the flagellar apparatus and flagellar position in the colonial green alga Platydorina caudata (Chlorophyceae). J Phycol 21:533–546

    Article  Google Scholar 

  • Viamontes GI, Kirk DL (1977) Cell shape changes and the mechanism of inversion in Volvox. J Cell Biol 75:719–730

    Article  PubMed  CAS  Google Scholar 

  • Viamontes GI, Fochtmann LJ, Kirk DL (1979) Morphogenesis in Volvox: analysis of critical variables. Cell 17:537–550. doi:10.1016/0092-8674(79)90262-9

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Drs Ken-ichiro Ishida and Shinichi Miyamura (University of Tsukuba) for valuable advice during this research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hitoshi Iida.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10265_2013_553_MOESM1_ESM.avi

Supplementary Figure S1. Microscopic time-lapse video of inversion in G. pectorale: Embryogenesis from 4-celled embryo to mature 8-celled colonies. (AVI 2179 kb)

10265_2013_553_MOESM2_ESM.tif

Supplementary Figure S2. a Merged image of DIC, microtubules (green), and EtBr-stained nuclei (red) corresponding to Fig. 5d-f. b, c Microtubules of the posterior region of the embryo are shown along the z-axis. Note that few cortical microtubules are localized in the posterior region of each cell. (TIFF 953 kb)

10265_2013_553_MOESM3_ESM.tif

Supplementary Figure S3. Simplified schematic tree of the volvocine algae based on the phylogenetic analysis of Herron and Michod (2008). Black branches indicate multicellular species. Arrowhead indicates acquisition of cytoplasmic bridges in embryos. Double arrowhead indicates acquisition of complete inversion. Note that the genus Gonium is a member of the basal clade within Volvocales and incomplete inversion arose independently in the Gonium lineage. (TIFF 345 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Iida, H., Ota, S. & Inouye, I. Cleavage, incomplete inversion, and cytoplasmic bridges in Gonium pectorale (Volvocales, Chlorophyta). J Plant Res 126, 699–707 (2013). https://doi.org/10.1007/s10265-013-0553-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-013-0553-7

Keywords

Navigation