Biology of Coenocytes
to "Coenocytes Research Group"
Kataoka D. Sc.,
of Biomolecular Sciences,
Graduate School of Life Sciences,
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?
are very large and easy to handle, and hence used for experimental materials
for electrophysiological and cell physiological studies.
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.
giant nucleus contains more than1,000 copies of genome. These giant nuclei
divide amitotically, and the internodal cell eventually lacks the ability
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.
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
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
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).
it was microtubular bundle that translocated the nuclei. During interphase
every nucleus had a long microtubule bundle at its head(Fig. 5) (11,
(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
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.
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:
or Motomura, Taizo: e-mail:firstname.lastname@example.org
Also, please look at homepages of the members of
the Coenocytes Research Group
H. 1975. Phototropism in Vaucheria geminata II. The mechanism
of bending and
Plant Cell Physiol. 16:439-448
H. 1980. Handbook of Phycological Methods III. Developmental &
(ed. Gantt, E. ), Cambridge Univ. Press. Cambridge. pp. 205-218
H. 1981a. Expansion of Vaucheria
cell apex caused by blue or red light.
Cell Physiol. 22:583-595
H. 1981b. Orientation movement of chloroplasts. In Photomovements.(Hikari
Hannou, In Japanese) , Furuya, M. ed.pp. 206-241. Kyoritsu Shuppan,
H. 1982. Colchicine-induced expansion
of Vaucheria cell apex. Alteration
from isotropic to transversally anisotropic growth. Bot. Mag. Tokyo
H. 1990. Negative phototropism
of Vaucheria terrestris regulated by
calcium II. Inhibition by Ca2+-channel blockers and mimesis by A23187.
Physiol. 31: 933-940
H.1991. Tropisms. In Responses
to Environment. (Kankyo Outoh, in Japanese) (ed.
T.) pp. 64-84. Asakura Shuppan, Tokyo
Y., Kataoka, H., Masuda, Y., Nagai, R. 1995. Dynamic changes in
cytoskeleton during the high-fluence rate response of the Mougeotia
H. 1999. Photosignaling
in Phototropsm and Branch of Vaucheria. In Photosignal
(In Japanese) eds. Hasunuma, K., Kimura,
N.,Tokunaga, S., pp. 80-88. Springer Verlag, Tokyo.
H. 2001. Phototaxis and phototropism.
In Responses to Environment. Asakura
Physiology Series 5. (Kankyo Outoh, in Japanese) (ed. Terashima, I.)
. pp. 17-39.Asakura
F., Hishinuma, T., Kataoka , H. 2001. Blue light-induced branching
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
H., Schopfer, P. 1992. Pflanzenphysiologie 4 Auflage.
Takahashi, F., Yamaguchi , K., Hishinuma, T., Kataoka, H.
(2003) Mitosis and
wave propagataion in the coenocytic alga, Vaucheria terrestris
sensu Goetz. J. Plant Res. 116:381-388
Yamagishi, T., Hishinuma, T., Kataoka, H. (2003) Bicarbonate enhances
division of the giant nuclei of sporophytes
in Bryopsis plumosa. J Plant Res. 116:295-300.
Yamagishi, T., Hishinuma, T., Kataoka, H. (2004) Nuclear reprogramming
Bryopsis plumosa: nuclei
of gametophytic protoplast synthesize proteins characteristic of sporophyte
by cell fusion with sporophytic protoplast. Planta 219:253-260