Biology of Coenocytes

Invitation to "Coenocytes Research Group"　　

　

Hironao Kataoka D. Sc.,

Assoc. Prof.,Department of Biomolecular Sciences,
Graduate School of Life Sciences,
Tohoku University

 kataoka@ige.tohoku.ac.jp
　A cell is the unit of life, as in a tiny space separated from external space by a thin closed membrane system, all necessary apparata for life are equipped and a single nucleus spatially and temporally controls all the functions of life (12).   We have believed that the uninuclear organization and principal functions of a cell, such as DNA replication, protein biosynthesis and respiraion, should almost be the same in mammals and tall trees. However, is this always true for all living things? Or, is it only a naiive oversimplification?
　We know, on the otherhand, that there is alternative cellular organization, called coenocyte or apocyte in which a cell (to call "cell" may not be appropriate: sometimes, called acellular structure) contains many nuclei. There are various kinds of coenocytes, widely spreading among phylogenetic branches. Are the celular mechanisms of coenocytes also the same as in the ordinary uninuclear cells? Some coenocytes are very large and easy to handle, and hence used for experimental materials for electrophysiological and cell physiological studies.

　Coenocytic cells can be classified into several groups in term of theirposition and status in the individuals (Fig. 1).
a: Xanthophycean alga (Chromista, Stramenopiles), Vaucheria and Zygomycetous fungus, Phycomyces, Oomycetes, etc. are coenocytic throughout their cell cycles, except when they are mechanically injured or at the formation of sex organs or zoosporangiophores.
b: Slime molds, such as Physarum polycepharum . are conocytic only in a limited phase of life cycle. Marine green algae Bryopsis, Caulerpa, Acetabularia, etc. are well known large coenocytes. But their diploid (2n) sporophytes, as well as their gametes and zoosopores are nuninuclear cells.
c: Internodal cells of Chara (Charophyte) are giant coenocytes, whereas their node cells are ordinary uninuclear cells. Since the Chara internodal cells reach 0. 5 mm in diameter and 20 cm in length, they have been suitable materials in cell physiology. Differentiation of sex organs and new internodal cells are only from these node cells. The internodal cell contains numerous giant nuclei which are circulated in the large cell by the protoplasmic streaming.


Fig. 1. Various types of coenocytes.

　Each giant nucleus contains more than1,000 copies of genome. These giant nuclei divide amitotically, and the internodal cell eventually lacks the ability of differentiation.
d: Cladophora spp. (also Aegagropira linnaei = Marimo), Acrosiphonia (green algae) , and Griffithsia(red algae) are consist of sausage-shaped coenocytic tubes (Fig. 1). The common characteristics which lead coenocytic organization is that cytokinesis does not follow mitotic nuclear division.
　Following questions are, however, heretofore asked: How is the coenocytic status maintained? Have their Genes for cytokinesis been lost or disfunctioned?
　New questions also arise: Is there any causal relationship between being a coenocyte and being a giant cell? Is coenocytic organization ecologically more profitable? How are the internuclear distances regulated? Which nucleus or a group of nuclei does take leadership in nuclear division and cell cycle rotation? How is the signal for nuclear division transmitted to others in the different region? Are individual nuclei taking part different functions, such as CPUs in a parallel-task computer? Does the function of the nuclei (gene expression) depend on the site of residence? And so on.
　We don'tstill have any answer to these questions. However, we are finding some interesting features and functions which are specific to coenocytes, through detailed observation of cytoskeletons and nuclear movement.

　We recently found an admirable function of Vaucheria in photo-cytomorphogenesis, which is only possible in coenocytes. The body of Vaucheria (V. terrestris sensu G嗾z =V. frigida) consists of a sparsely branched coenocytic tube of 50-70 ｵm in diameter(Fig. 2). Tips of the branches exhibit typical tip growth andpositive- as well as negative phototropism. Vaucheria has thus been very useful material for the photoresponses of tip-growing cells (1-10).
　When a narrow region of the cell was irradiated with blue light(400- 500 nm) of moderate intensity, a new growth center was induced at the center of the irraidated region 4 h (at the earliest) after the onset of light. The initiated growth center then bulged out and developed as a new branch (Fig. 3). Only blue light is effective and yellow-red light is completely inert. This is an experimentally induced branching. But, the similar thing must occurs in natural habitats: Vaucheria grows as a mat on wet soil near the stream. In fall, the mat would be shaded by fallen leaves. In the shaded region no photosyntehsis would take place. The ability to form a branch from the opening would have been evolutionary and ecologically profitable trait.
　 Thus, study of the photocytomorpho-genetic response is very important in photobiology and cell physiology.


Fig. 2. Actively growing apex of Vaucheria terrestris sensu Goetz

Fig. 3. Schematic diagram of the blue-light-induced branching and redistribution of nuclei.

　We found that the accumulation of nuclei was indispensable for this blue light-induced branching. The accumulation of chloroplasts which starts immediately and completed 1 h after the onset of light was by itself not sufficient (Fig. 4) (9-10). The nuclear accumulation started 30- 40 min after the onset of light. Not only nuclei, but also protoplasm, which also included chlorplasts rushed into the lighted region.
　Density of nuclei in the irradiated region reached 200% of that in the adjacent dark region by 5 h. The increase in number of nuclei was never due to induction of nuclear division in the lighted region. This was performed by careful observation with many specimen fixed at intervals of 10 min.
　Accumulation of protoplasm continued and after 3 h the central vacuole was occasionally teared off. Then, about 4 h after the onset of blue light, cell wall at the center of the irradiated region was softend, and a bulge developed to an actively growing branchlet.


Fig. 4. Bluelight-induced branching in Vaucheria.

　
Fig. 5. Microtubule bundle extends from centrosome of a nucleus. From Takahashi et al.(2001) Plant Cell Physiol. 42:274-285 and from unpublished photograph (taken by Fumio Takahashi).

　Surprizingly, it was microtubular bundle that translocated the nuclei. During interphase every nucleus had a long microtubule bundle at its head(Fig. 5) (11, 12). Centrosome (including centrioles) serves as an MTOC (12). Additional 2 (or 3?) short microtubule bundles are extending backward from the centrosome region. Observing the movement of nuclei under optical microscope (DIC optics), we confirmed that the frontal microtubule bundles pulled nuclei in longitudinal direction. If the microtubule bundles are destroyed, nuclei are not accumulated, and hence no branch is induced (11). We are now intending to identify the microtubule associated motor protein and to elucidate the motor mechanism.
　Nuclear accumulation is probaly necessary for producing cellulytic enzymes, ion channel proteins and deliver exocytotic vesicles to the presumptive site of branching. It is not known yet that the accumulated nuclei themselves are the site of blue light reception and that only in those nuclei new expression of genes start. By the way, the present results also suggest that the nuclear control for the morphogenesis is rather a short range, as is the case in uninuclear fern protonema cell.
　Now, let's compare the Vaucheria system with morphogenesis of multicullular plants. In multicellular plants morphogenesis always requires a local cell division(13). If a high nuclear density is principally necessary for creating a new shape, all multicellular plants must inevitably use nuclear- and cell division. In coenocytic cells, however, the high nuclear density can be achieved by gathering nuclei into desired locus without waiting for the next mitosis. Only coenocytic cells can adopt this principle. But we don't know yet, whether this is also the case in coenocytic algae other than Vaucheria.
　Then, what on earth the roles of individual nuclei in the coenocytic cell? Is the coenocytic organization, monarchy, anarchy, feudalismic, or republic? what is necessary for maintaining coenocytic organization other than deletion of prevention of cytokinesis? Such exciting questions lead us to a new subdiscipline, CELL ECOLOGY. Recently, we have found in Vaucheria that the nuclear division started mainly at the growing apex and the phase of the mitotis propgated from tip to the base as a mitotic wave (14). In a narrow region (about 200 µm in length) the mitosis occur synchrounously. Probably, the mitotic wave is driven via the production of cyclin- like proteins by the dividing nuclei. This may indicate that the nuclein the apical growing region plays a role as the leaders in the coenocytic continuum. ヾimilar　internucleus communication in a coenocytic cell can be observed in the green alga, Bryopsis plumosa (15,16) aritificially fused protoplasts between gametophyte and sporophyte.

　It is not always guaranteed that a phenomenon or a function found in Arabidopsis is also acting in other plants. Also, common senses in multicellular plants are not usually common sense in unicellular or coenocytic organisms. Also, the reason d'etre of coenocyte cannot be solved by the study of unicellular and multicellular organisms. Instead, from the study of coenocytes a quite new, heretofore overlooked important points on the mechanism of cell division could be found. We started to organize "coenocytes Research Group" a few years ago. Those who are interested in this group and/or hope to participate in the free discussion, please feel free to contact:

Kataoka, Hironao: e-mail: kataoka@ige.tohoku.ac.jp
or Motomura, Taizo: e-mail:motomura@bio.sci.hokudai.ac.jp

Also, please look at homepages of the members of the Coenocytes Research Group
Keiichi Yamamoto:http://bio.s.chiba-u.ac.jp/bio/physiology/yamamoto/yamamoto.html

References:

1) Kataoka, H. 1975. Phototropism in Vaucheria geminata II. The mechanism of bending and
  branching. Plant Cell Physiol. 16:439-448
2) Kataoka, H. 1980. Handbook of Phycological Methods III. Developmental & Cytological
  Methods. (ed. Gantt, E. ), Cambridge Univ. Press. Cambridge. pp. 205-218
3) Kataoka, H. 1981a. Expansion of Vaucheria cell apex caused by blue or red light.
  Plant Cell Physiol. 22:583-595
4）Kataoka, H. 1981b. Orientation movement of chloroplasts. In Photomovements.(Hikari
  Undou Hannou, In Japanese) , Furuya, M. ed.pp. 206-241. Kyoritsu Shuppan, Tokyo
5）Kataoka, H. 1982. Colchicine-induced expansion of Vaucheria cell apex. Alteration
  from isotropic to transversally anisotropic growth. Bot. Mag. Tokyo 95:317-330
6）Kataoka, H. 1990. Negative phototropism of Vaucheria terrestris regulated by　
  calcium II. Inhibition by Ca2+-channel blockers and mimesis by A23187. Plant Cell Physiol. 31: 933-940
7) Kataoka, H.1991. Tropisms. In Responses to Environment. (Kankyo Outoh, in Japanese) (ed.
  Shimmen, T.) pp. 64-84. Asakura Shuppan, Tokyo
8）Mineyuki, Y., Kataoka, H., Masuda, Y., Nagai, R. 1995. Dynamic changes in the
  actin cytoskeleton during the high-fluence rate response of the Mougeotia chloroplastProtoplasma 185: 222-229
9）Kataoka, H. 1999. Photosignaling in Phototropsm and Branch of Vaucheria. In Photosignal
  transductions. (In Japanese) eds. Hasunuma, K., Kimura, N.,Tokunaga, S., pp. 80-88. Springer Verlag, Tokyo.
10）Kataoka, H. 2001. Phototaxis and phototropism. In Responses to Environment. 　Asakura
  Plant Physiology Series 5. (Kankyo Outoh, in Japanese) (ed. Terashima, 　I.) . pp. 17-39.Asakura Shuppan, Tokyo
11）Takahashi, F., Hishinuma, T., Kataoka , H. 2001. Blue light-induced branching in 　
  Vaucheria. Requirement of nuclear accumulation in the irradiated region. Plant Cell Physiol. 　42:274-285
12 )　Ott, D. W. 1992. The Cytoskeleton of the Algae. Ed. By Menzel, D. M., pp. 255-272. CRC
  Press
13）Mohr, H., Schopfer, P. 1992. Pflanzenphysiologie 4 Auflage.
14) Takahashi, F., Yamaguchi , K., Hishinuma, T., Kataoka, H. (2003) Mitosis and 　
  mitotic wave propagataion in the coenocytic alga, Vaucheria terrestris sensu Goetz. 　J. Plant Res. 116:381-388
15) Yamagishi, T., Hishinuma, T., Kataoka, H. (2003) Bicarbonate enhances
  synchronous division of the giant nuclei of sporophytes in Bryopsis plumosa. J Plant Res. 116:295-300.
16) Yamagishi, T., Hishinuma, T., Kataoka, H. (2004) Nuclear reprogramming in
  Bryopsis plumosa: nuclei of gametophytic protoplast synthesize proteins characteristic of sporophyte by cell fusion with sporophytic protoplast. Planta 219:253-260

 

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