INTRODUCTION

The most dominant  polysaccharide  of  the  cell wall  is
cellulose. The universal distribution of this natural polymer
among  prokaryotic  and  eukaryotic  organisms  attests  to  its
ancient evolutionary  history.  Not  only  is  cellulose  found
among photosynthetic and protistan cells,  it is present in
animals such as the Ascidians  (Wardrop,  1970).  Furthermore,
levels of elevated cellulose synthesis have been suggested in
humans with the disease scleroderma (Hall, et al, 1960).

The algae have been prominent organisms of  study among
eukaryotic  organisms  because  of  their  great  diversity  of
structure and cellular  organization.  Chloroplast morphology
(Gibbs, 1981), organization of the mitotic apparatus (Pickett-
Heaps, 1972), cell wall structure and composition  (Preston,
1974),  flagellar apparatus  (Stewart and Mattox,  1978),  and
reproduction have provided a wealth of information on algal
phylogeny  (Stewart  and  Mattox,  1982);  however,  very  few
studies  have  concentrated  on  evolutionary  and  phylogenetic
aspects of cell walls,  let alone cellulose, mainly because
the cellulose synthases had never been observed or isolated.

In  1976,  the  first  successful  application  of  freeze
fracture demonstrated the structure of a cellulose synthase
complex in Oocystis apiculata (Brown and Montezinos, 1976).
These  membrane   associated   structures,   called   terminal
synthesizing complexes (=TCs), were found at the growing tip
of  microfibril  impressions  on  the  E-fracture  face  of  the
plasma membrane. Earlier, Roelofsen (1958) had predicted that
an organized terminal enzyme complex would be found; however,
the shape and geometry could not be predicted at that time.

In 1964, Preston proposed the ordered granule hypothesis
for the cellulose synthase complex.  This study was based on
observations  of  remnants  of  organized  particle  subunits
associated with the innermost wall  of Chaetomorpha.  During
this time, the freeze fracture technique was becoming widely
used,  and  organized  particle  complexes  were  found  in  the
plasma membranes, particularly abundant in yeasts  (Moor and
Muhlethaler,  1963).  Thus,  a  logical  extension  of  the
possibility of such an organization could be made for the
cellulose synthesizing complex.  Interestingly, TCs were not
observed in cells which had been chemically fixed or treated
with glycerol or cryoprotectants. The breakthrough in finding
TCs came when Brown and Montezinos demonstrated that rapid
direct freezing of living cells yielded organized particle
structures associated with the tips of microfibrils.

Since 1976, TCs have been found in more than 14 algal
genera, and presently, a  distinct pattern of TC structure is
beginning to emerge which provides  some  insight  into  the
substantial  diversity  of  cellulose  microfibril  synthesis
among the algae.  In this  presentation,  the  fundamental TC
diversity  among  the  algae  will  be  described.  Because  TC
variation is the greatest among the algae, it also provides
hints  at  the  relationship  between  TC  organization  and
microfibril  shape,  molecular weight of the  cellulose,  and
crystallization.  Phylogenetic  relationships  based  on  TC
structure  can  be  correlated  with  other  structural  and
biochemical evidence. This presentation will conclude with a
proposed evolutionary history of cellulose biogenesis.

TERMINAL COMPLEX DIVERSITY

So far,  only two basic  forms  of  TCs  have  been  found
among eukaryotic cells. The linear TC was first discovered in
Oocystis and is present among most members of the Ulvophyceae
(Hotchkiss  and Brown,  1989)  (Fig  1).  The  rosette  TC  was
reported  simultaneously  by  Mueller  and  Brown  (1980)  and
Giddings, et a], (1980).  Earlier, Mueller,  et al  (1976)  had
observed a globular component of the TC  on  the E-fracture
face  of  the  plasma  membrane  in  corn  roots.  Subsequent
examination of the P-fracture face revealed a rosette of 6
symmetrically organized particle subunits (Fig 2).

Unlike that in the corn root, the rosette TC found in
Micrasterias  frequently  is  organized  in  ordered  arrays,
especially during secondary wall formation (Giddings, et al,
1980). Furthermore, the rosette subunits have been shown to
span  both  layers  of  the  bimolecular  leaflet.  Since  these
first reports, rosette TC's have been found in a variety of
organisms, ranging from the land plants to Chara (McLean and
Juniper, 1986) and Nitella (Hotchkiss and Brown, 1987).

For a more detailed elaboration of the distribution of
TC's  among  eukaryotic  cells,  consult  the  report  of  Brown
(1985). Since this publication, TCs have been found in other
organisms and will briefly described. In 1987, Hotchkiss and
Brown described a solitary rosette TC in Nitella translucens
(Hotchkiss   and   Brown,   1987).   This   TC   is   virtually
indistinguishable from that of land plants,  in addition,  a
solitary- rosette TC has been observed in Chara  (McLean and
Juniper, 1986).

Only in the Zygnematales has an ordered consolidation
of TC's been found, and among one member, Mougeotia, the TCs
are exclusively solitary (Hotchkiss et al 1989 ).  Thus,  the
consolidation  of  rosette TCs  appears  to have been a more
recent  event  (Hotchkiss  and  Brown,   1989a).  When  wall
composition  is  taken  into  consideration,   the  evidence
strongly supports that the Charophyceae is the phylogenetic
line which may have given rise to the vascular plants.

Another interesting and different TC structure recently
was found in the xanthophycean genus, Vaucheria  (Mizuta et
al,  1989).  Overall,  the  TC  is  linear,  but  the  subunit
arrangement within the TC is in the form of unique diagonal
rows (Fig 3).

THE EVOLUTION OF THE TC AND CELLULOSE BIOGENESIS

Based on TC ultrastructure and cellulose organization,
it  is  possible  to  construct  a  phylogenetic  pathway  for
cellulose biogenesis  (Fig 4).  Although  somewhat premature,
this treatment gives several important and interesting clues
to the subject of eukaryotic cellular evolution. Clearly, the
algae  as a group have been pivotal in the diversification of
cellulose  microfibril   assembly   as   exemplified  by   the
diversity of TC  and microfibril morphology.

Prokaryotic Cellulose

The evolution of cellulose among prokaryotic cells will
first be considered. The fact that cellulose assembly occurs
among two widely divergent prokaryotic groups suggests that
this   process   must   have   been   an   ancient   one.   The
investigations of Woese have  shed much  light on bacterial
evolution. Using homologous sequences in rRNA,  it has been
possible  to unambiguously examine  and measure phylogenetic
relationships among the bacteria (Woese, 1987).

The  genus,  Sarcina  is  a  gram  +  bacterium  and  is
considered primitive among the eubacteria. Sarcina also is an
obligate anaerobe. Cellulose synthesis in Sarcina was first
described by Canale-Parola et al (1961). We have also studied
cellulose   synthesis   in   Sarcina   (Roberts   and   Brown,
unpublished data) and have come to the conclusion supporting
Canale-Parola et al that only the cellulose II polymorph is
synthesized.  The  exact  site  of  cellulose  synthesis  is
unknown;   however,   membrane   fractions   of   Sarcina   can
synthesize cellulose II in vitro (Lin, Roberts, and Brown,
unpublished data).

Among  the  purple  bacteria,   only  the  cellulose  I
polymorph  is  synthesized  (one  exception  is  a  mutation  in
Acetobacter  giving  rise  to  cellulose  II  synthesis,  see
Roberts  et  al,  1989).  The  site  of  cellulose  microfibril
synthesis  is  a  linear  row  of  particles  parallel  to  the
longitudinal axis of the cell  (Brown et al,  1976). On the
surface of the LPS  layer  of  the  cell  envelope  is  a pore
complex  through  which  fibrils  are  extruded.  The  enzyme
complex is located in the cytoplasmic membrane  (Bureau and
Brown, 1987).- Groups of three or more particles are required
to   assemble   subfibrils   which   consolidate   to   form   a
microfibril tangential to the cell surface (Haigler et al,
1980). Microfibrils unite  to  form  bundles which,  in  turn,
group  to  assemble  ribbons.  The  ribbons  are  visible  with
darkfield microscopy, and the progress of cellulose synthesis
can be directly monitored using time lapse video microscopy
(Brown  and  Santos,  unpublished  observations;  Brown  and
Colpitts, 1978; Lin and Brown, 1989).

In Rhizobium and Agrobacterium,  the  sites  of  cellulose
assembly   are   similar;    however,    fewer    microfibrils
consolidate. Only a floe of cellulose is produced, while in
Acetobacter,  a  thick  leathery  membrane  or  pellicle  is
synthesized.  The  function of  cellulose  biosynthesis  in
-Acetobacter is_ unknown. Acetobacter xylinum is an obligate
aerobe. Therefore the buoyancy of its cellulose could provide
an aerobic environment for cells active in cellulose
synthesis (Schramm and Hestrin, 1954). Why Acetobacter would
divert large pools of metabolic substrate into cellulose is
unknown; however, cellulose could serve as a reserve pool for
metabolism.  Unfortunately,  extensive  cellulase activity  has
not   been   found;   yet,   degradation   of   non-crystalline
carboxymethylcellulose   can   occur   (Brown   and   White,
unpublished observations).

Fundamental   research   investigations   of   cellulose
biogenesis  in  Acetobacter  have  yielded  perhaps  the  most
extensive evidence for the molecular mechanisms  of cellulose
assembly.  Cellulose  has  now  been  synthesized  in  vitro
(Glaser, 1958); a specific activator for cellulose synthesis
has  been  found  (Ross  et al,  1985),  the  in  vitro  product
characterized morphologically (Lin et al, 1985), the in vitro
crystalline polymorph deduced (Bureau and Brown, 1987), the
cellular site of the synthase localized  (Bureau and Brown,
1987), the cellulose synthase purified (Lin and Brown, 1989,),
and gene cloning for the purified enzyme  initiated  (Saxena
and Brown, 1989).

Cellulose synthesis among the blue green algae has been
mentioned  only  once  in  the  literature,  and  conclusive
evidence for this is lacking (Frey-Wyssling, 1976). According
to Woese (1987), the cyanobacteria emerged from the distance
matrix phylogenetic tree of the eubacteria almost from the
same region as the gram + bacteria and also  close  to  the
purple bacteria. Thus, it is clear that cellulose biogenesis
must have been an ancient process during the  evolution  of
life on earth.

With the accumulating evidence of cellulose biogenesis
among  prokaryotes,  the  evolution  of  cellulose  among  this
group  can  now  be  addressed.  The  cellulose  II  polymorph
appears  to  be  primitive.  This  polymorph  is  the  more
thermodynamically stable form with an additional inter-chain
H-bond  formed per  glucose residue.  Cellulose  II  can  form
spontaneously from solution when cellulose is solubilized by
such   agents   as   DMSO/paraformaldehyde   or   cupraammonium
reagents  (Blackwell  et  al,  1986).  On  the  other  hand,
cellulose I is a metastable polymorph, presumably
assembled only by living organisms. Therefore, cellulose I is
more  advanced,  requiring  additional  mechanisms  for  chain
orientation and positioning to achieve the metastable state.

The  first  cellulose  producer  probably  had  its  glucan
synthase randomly organized in association with the membrane
(Fig 5). Under these primitive conditions, only cellulose II
could bioynthesized in vivo. Thus, in Sarcina, glucan chains
appear to be randomly positioned over the cell surface in an
amorphous array. Sarcina is an excellent example of an extant
organism which lacks mechanisms to consolidate and organize
the  glucan  synthase  complex  to  induce  ordered  microfibril
assembly  and  aggregation  into  bundles  and  ribbons  of
cellulose 1. On the other hand, the purple bacteria evolved
the   mechanisms   to   order   glucan   chains   into   various
conformations  leading  to  a  diversity   of   cellulose   I
microfibril assembly. Because of abundant evidence suggesting
that the purple bacteria are more advanced (Woese, 1987), it
follows that cellulose I assembly is more advanced. A logical
extension of this evolutionary advancement is to consider the
evolution of cellulose among the eukaryotes. Did these cells
obtain genes for cellulose synthesis from the eubacteria? If
so, what are the likely candidates? It is obvious that if the
mitochondria of eukaryotes came from the purple bacteria, did
they  also  transfer  the  genes  for  organized  cellulose  I
synthesis? This is  an  intriguing question,  one which must
await cloning and sequencing of the genes for the cellulose
synthases.

Eukaryotic Cellulose

We shall now consider one of the greatest mysteries in
biology- the origin of cellulose synthesis among eukaryotic
cells. The possibility that the genes for cellulose synthesis
may have come from the purple bacteria has been alluded to.
What was the first eukaryotic organism to have received the
cellulose synthase gene? An examination of phylogenetic trees
indicates  that  among  the  extant  primitive  eukaryotes,
cellulose is found among one group, namely, the cellular
slime molds. Cellulose I of low crystallinity has been found
in  Dictyostelium  (Roberts  and  Brown,   unpublished  data).
Because Dictyostelium is non-photosynthetic, it seems highly
unlikely that it could have received the genes for cellulose
synthesis  from a photosynthetic prokaryotic progenitor.  It
seems  attractive,  therefore,  that  the  purple  bacteria  may
have donated these complexes.

Dictyostelium TCs are unlike any  so far  found among
eukaryotic cells. They appear to consist of linear arrays of
single  particles  (Fig.  4'  (Mizuta  and  Brown,  unpublished
results). These arrays are somewhat similar to those found in
Acetobacter.  Thus,  among  eukaryotic  organisms,  the  linear
arrangement   of   single   rows   of  particle   subunits (arrows)   in
Dictyostelium appears to be primitive. This is also supported
by the low crystallinity of cellulose I from this organism.

Certain  fungi,  among  them,  the  Oomycetes,  synthesize
cellulose. Yet, nothing is known of TC structure among the
fungi. This is a major research area which needs  immediate
attention. One could predict, however, that if Vaucheria is
closely related to Saprolegnia,  the unique  linear TC with
diagonal rows (Mizuta and Brown, 1989) might be found in the
latter.

Why many of the fungi opted for chitin as the major
wall polymer is an interesting sidelight to the question of
the evolution of cellulose synthesis. Some of the fungi are
almost as  primitive as Dictyostelium,  yet  there  is  scant
knowledge of chitin synthesis among primitive eukaryotes, let
alone  the  eubacteria and  archaebacteria.  Perhaps  nutrition
may have played a role in the more efficient utilization of
strong  polymers.  Since  chitin  walled  organisms  may  have
required more nitrogen, the energy budget would be greater.
Thus, to synthesize a polymer of cellulose would represent a
selective  advantage  from  a  nutritional  point  of  view
(Duchesne and Larson, 1989).

THE  EVOLUTION  OF  CELLULOSE  SYNTHESIS  AMONG  PHOTOSYNTHETIC
EUKARYOTES

At this  junction,  the algae  certainly  have  played  a
diversified role, for it is here that the greatest variety of
TCs and cellulose structure is found among the algae (Fig 6).
Gunderson et al, 1987) have suggested on the basis of 18S
rRNA sequences that a cellulose  producing  oomycete,  Achlya
bisexual is, is closely related to Ochromonas danica, a chitin
producer.  Perhaps  the  fungi  and  chromophytes  appeared  at
roughly the same time.

The recent studies of  Pearasso et al,  1989)  have shed
some light on the origin of the algae. On the basis of 28S
cytoplasmic rRNA homology,  they  found that  three  distinct
groups    emerged   late   among    eukaryotes:    rhodophytes,
chromophytes,   and   chlorophytes.   A  late  occurrence   of
eukaryotic   photosynthetic   symbiosis   was   implied.   The
conserved rosette/linear TCs among the algae  suggests  that
the synthase may have come from the more primitive fungi or
Dictyostelium,  rather  than  through  the chloroplast.  Again,
this  implies  that  even  earlier,  the  ancient  eukaryotic
mitochondrion may  have  contained  the  genes  for  cellulose
synthase.

Could the cellulose synthase of the Rhodophyta have come
from the cyanobacteria? This question cannot be answered
until  we  have  more  data  on  the  presence  and  physical
characteristics of cellulose among the cyanobacteria. If only
cellulose II is present among the cyanobacteria, it would be
difficult  to  imagine an  independent  evolutionary  event  to
organize the TC to allow it to produce cellulose I which is
found among the Rhodophyta. If, however, Nostoc is found to
produce  cellulose  I  in  vivo,  the  hypothesis  that  the
cyanobacteria  could  have  been  the  progenitors  of  the
Rhodophyta, would be strengthened. It should be apparent that
these  questions  cannot  really  be  answered,   let  alone
seriously considered, until we have sequence information on
the cellulose synthase;  yet these questions do  need  to  be
placed  before  the  scientific  community  now  so  that  the
blueprint for solving this great mystery can be expedited.

The origin of cellulose synthesis among the major algal
groups is still a major mystery. Consider that cellulose is
known   among   the   Pyrrophyta,   the   Chrysophycease,   the
Xanthophyceae, the Phaeophyta, and the Chlorophyta  (Fig 6).
Did each of these major groups receive a cellulose synthase
independently,  possibly  from  pro-chloroplast  capture?  The
diversity of TC structure among these groups might suggest
multiple independent captures, yet only the purple bacteria
are known to synthesize cellulose I, the same polymorph found
among the great diversity of algae  (with the exception  of
Halicystis,   Sisson,   1938;   Roberts   and   Brown,   1989,
unpublished data). This argues in favor of a single capture
of the cellulose synthase very early in eukaryotic evolution,
possibly through the  purple bacteria donation  of  the pro-
mitochondrial apparatus. This implies that the organizational
machinery for glucan chain assembly  into  the  cellulose  I
polymorph  may  have  also  been  introduced  early  through
transfer   to   an   ancient   eukaryotic    progenitor.   Then,
Dictyostelium may be an example of one of the most ancient
surviving groups which received the cellulose synthase from a
prokaryotic progenitor. These are provocative questions, but
ones which cannot be answered with certainty at present.

 Fig   5.   Possible   evolutionary   pathways   of   cellulose
biogenesis,  showing the relationship of the algae to early
life.

CONCLUSIONS

Cellulose synthase is an ancient molecule as evidenced
by its ubiquity among prokaryotic and eukaryotic organisms. It
therefore must have served an important early function in the
origin of life on earth.  The most advanced eukaryotic land
plants  have  the  rosette  cellulose  synthase  TC.  Advanced
members  of  the Charophyta  have  the rosette TC,  an  so  do
members of the Zygnemetales. At present, all pieces to the
puzzle are not in place. Critically important algae need to
be investigated for their TC structure to provide more direct
confirming data for the rosette TC in land plant evolution.
These  include Coleochaetae,  members  of  the Trentepholiales
(Cephaleuros),   the  Klebsormidiales   (Klebshormidium),   the
Chlorokybales   (Chlorokybus),  and  other  members  of  the
Zygnematales ( Zygnema, Netrium) .

The  concept  of  symbiotic  capture  of  the  cellulose
synthase in eukaryotic cells needs more study  (Fig 7). Did
the cellulose synthase come from a mitochondrial progenitor
(through the purple bacteria)? Did  it originate through  a
chloroplast   progenitor   (from   the   cyanobacteria,   pro-
chlorophyta, or pro-chromophyta)? Did the cellulose synthase
transfer directly from the prokaryote chromosome or plasmid?
Perhaps one or more symbiotic captures occurred, giving rise
the the diversity of TC morphology and microfibril diversity.

The known diversity of cellulose microfibril structure,
degree of polymerization,  and crystallinity,  suggests that
secondary modifications to the primary glucan synthase must
have  occurred.  Perhaps  even  the  regulation  of  cellulose
synthase  activity  has  been  modified,  although  cellulose
synthase activity appears largely constitutive. The diversity
of  fibrillar polymers  other  than  cellulose among the algae
supports  an  extremely  diverse  evolution  in  cell  wall
structure, possibly reflecting the wide range of environments
for survival.

Algae  have  served as  excellent model  systems  in  the
quest for understanding cellulose biogenesis. Not only do the
algae synthesize diverse forms off cellulose, they offer an
uncompromising approach for cytological observation,  coupled
with a potential for isolation, cloning, and sequencing of
the genes involved in cellulose biogenesis. The coming decade
will see great advances in cellulose biogenesis research.

ACKNOWLEDGMENTS

Appreciation  is  expressed  to  Richard  Santos  for  his
unfailing loyalty and support throughout the past 19 years.
Also, my former and present graduate students, post-doctoral
fellows,  and visitors  to the  lab  deserve  recognition  for
their contributions to this research. I thank Inger Johansen
for preparing this manuscript. This research was supported by
the  National  Science  Foundation,  The  Johnson  &  Johnson
Centennial Chair Endowment, and funds from the University of
Texas at Austin.

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Professor Dr. WOLFGANG WIESSNER
Professor DAVID G. ROBINSON
Pflanzenphysiologisches Institut der Universitat
Untere Karspiile 2
3400 Gottingen, FRG
Professor RICHARD C. STARR, Ph. D.
The University of Texas at Austin
Austin, TX 78712, USA

ISBN 3-540-52496-7 Springer-Verlag Berlin Heidelberg New York
ISBN 0-387-52496-7 Springer-Verlag New York Berlin Heidelberg
 

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