The Protistan Cell Surface

296 Pages·1994·20.693 MB·English

by  H. R. Preisig, O. R. Anderson, J. O. Corliss, Ø. Moestrup (auth.), Dr. Richard Wetherbee, Dr. Jeremy D. Pickett-Heaps, Dr. Robert A. Andersen (eds.)

R. Wetherbee, R. A. Andersen,
and J. D. Pickett-Heaps (eds.)
The Protistan
Cell Surface
Springer-Verlag Wien New York
Dr. Richard Wetherbee
Dr. Jeremy D. Pickett-Heaps
School of Botany
University of Melbourne
Parkville, Victoria, Australia
Dr. Robert A. Andersen
Provasoli-Guillard Center for Culture of Marine Phytoplankton
Bigelow Laboratory for Ocean Sciences
West Boothbay Harbor, Maine, U.S.A.
This work is subject to copyright.
All rights are reserved, whether the whole or part of the material is concerned, specifically those of translation, reprinting, re-use of illustrations,
broadcasting, reproduction by photocopying machine or similar means, and storage in data banks.
© 1994 Springer-VerlaglWien
Softcover reprint of the hardcover 1st edition 1994
Printed on acid-free and chlorine-free bleached paper
With 566 Figures
Library of Congress Cataloging-in-Publication Data
The protistan cell surface / R. Wetherbee, R. A. Andersen, and J. D.
Pickett-Heaps, eds.
p. cm.
Includes bibliographical references.
ISBN-13: 978-3-7091-9380-8
I. Protista. 2. Cell membrances. 3. Fungal cell walls.
I. Wetherbee, R. (Richard). II. Andersen, Robert A. (Robert
Althur). III. Pickett-Heaps. Jeremy D.
QR74.5.P76 1994 94-33622
576'.14-dc20
Special Edition of "'Protoplasma", Vol. 181, 1994
ISBN-13: 978-3-7091-9380-8 e-ISBN-13: 978-3-7091-9378-5
DOL: 10.1007/978-3-7091-9378-5
Preface
The protists represent an immensely diverse group of in terminology are cited and recommended for change
organisms comprised of algae, fungi and protozoa. His (e.g., the common and inconsistent use of the terms
torically studied in isolation within the specialized dis "periplast" and "theca"). The remaining contributions
ciplines ofphycology, mycology and protozoology, re to this book represent the proceedings of two symposia,
spectively, recent phylogenetic analyses by a variety of entitled "The Cell Surface in Protistan Taxonomy and
techniques, most notably ultrastructural and gene se Systematics" and "The Structure, Development and
quence comparisons, have shown these classical sep Function of Protistan Cell Surfaces", or were solicited
arations to be artificial. In the search for true phylo by the editors to fill obvious gaps in the symposia
genetic classifications, the need for a common vocab program. Both the Task Force and the Symposia met
ulary that reflects the relationship between protists, at the Phycological Society of America meetings held
rather than the field of study that produced the terms, in conjunction with the AIBS at Iowa State University
is imperative. This communal vocabulary will allow in August of 1993. Despite the efforts of the editors,
modern protistologists to identify and compare ho not all of the contributors to the symposia were able
mologous structures and to break down the historical to produce their required written papers. These pro
barriers between disciplines. To help address this prob ceedings therefore have some obvious gaps, most no
lem, a number of Task Forces were formed in 1987 to tably in the coverage of protistan cell walls (fungal and
help create a common vocabulary for the Protists as a algal) and the organic coverings of many protistan
whole. The history of the origin and function of Task groups (e.g., the periplast, pellicle, and theca).
Forces is discussed in the Preface to the report of the We are grateful to Dr. James Rodman and the Sys
Task Force on the Cytoskeleton, which was published tematic Biology Program of the National Science
both as an issue of the international journal "Proto Foundation of the U.S.A. for funding both the Task
plasma" (Vol. 164) and subsequently as a book by Force and the Symposia that lead to this book (NSF
Springer-Verlag: Melkonian, M., Andersen, R. A., grant DEB-9304086). We are also grateful to Dr. Ran
Schnepf, E. (eds.), The Cytoskeleton of Flagellate and dall Alberte and the Office for Naval Research (U.S.A.)
Ciliate Protists, Springer-Verlag, Wi en New York for providing additional funds in support of the Editors
(1991). and the Symposia. This is the second Task Force to
The nature of the protistan cell surface is as diverse as report, and several others (e.g., on mitosis/cytokinesis:
the terminology that has evolved to describe the various paleobiology) are scheduled to meet and report in the
surface components. This terminology is defined and near future. The common goal of each Task Force is
discussed in the report of the Task Force on the Pro the same, to promote and enhance the study of pro
tistan Cell Surface chaired by Dr. Hans Preisig. The tistan biology through a common terminology and a
Task Force members were representative of mycology better understanding of the interwoven evolutionary
(Dr. M. J. Powell and Dr. R. W. Roberson), phycology relationships of algae, fungi, and protozoa.
(Dr. O. Moestrup and Dr. R. Wetherbee), and pro
tozoology (Dr. O. R. Anderson and Dr. J. O. Corliss).
Although the Task Force made no attempt to dictate R. Wetherbee, R. A. Andersen, and
a common vocabulary, several obvious discrepancies J. D. Pickett-Heaps
Contents
Preisig, H. R., Anderson, O. R., Corliss, J. 0., Moestrup, 0., Powell, Martha J., Roberson, R. W., Wetherbee,
R.: Terminology and nomenclature of protist cell surface structures .................................... .
Preisig, H. R.: Siliceous structures and silicification in flagellated protists .................................... 29
Schmid, Anna-Maria M.: Aspects of morphogenesis and function of diatom cell walls with implications for
taxonomy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
Anderson, O. R.: Cytoplasmic origin and surface deposition of siliceous structures in Sarcodina............ 61
Faber, W., Jr., Preisig, H. R.: Calcified structures and calcification in protists .............................. 78
Brett, S. J., Perasso, L., Wetherbee, R.: Structure and development of the cryptomonad periplast: a review 106
Powell, Martha J.: Production and modifications of extracellular structures during development of chytri-
diomycetes .................................................................................................. 123
Burr, A. W., Beakes, G. W.: Characterization of zoospore and cyst surface structure in saprophytic and fish
pathogenic Saprolegnia species (oomycete fungal protists) ................................................ 142
Kugrens, P., Lee, R. E., Corliss, J. 0.: Ultrastructure, biogenesis, and functions of extrusive organelles in
selected non-ciliate protists ................................................................................. 164
Russell, D. G.: Biology of the Leishmania surface: with particular reference to the surface proteinase, gp 63 191
Braun, E. J., Howard, R. J.: Adhesion of fungal spores and germlings to host plant surfaces... . .......... 202
Hardham, A. R., Cahill, D. M., Cope, M., Gabor, B. K., Gubler, F., Hyde, G. J.: Cell surface antigens of
Phytophthora spores: biological and taxonomic characterization .......................................... 213
Becker, B., Marin, B., Melkonian, M.: Structure, composition, and biogenesis of prasinophyte cell coverings 233
Woessner, J. P., Goodenough, Ursula W.: Volvocine cell walls and their constituent glycoproteins: an evo-
lutionary perspective ........................................................................................ 245
Lavau, S., Wetherbee, R.: Structure and development of the scale case of Mallomonas adamas (Synurophyceae) 259
Pickett-Heaps, J., Carpenter, Jocelyn, Koutoulis. A.: Valve and seta (spine) morphogenesis in the centric
diatom Chaetoceros peruvianus Brightwell ................................................................. 269
Fazio, M. J., Marrs, J. A., Bouck, G. B.: Protein kinases in protists ......................................... 283
Protoplasma (1994) 181: 1-28
PROTOPLASMA
© Springer-Verlag 1994
Terminology and nomenclature of protist cell surface structures
H. R. Preisig1, *, O. R. Anderson2, J. O. Corliss3, 0. Moestrup\ Martha J. Powells, R. W. Roberson6,
and R. Wetherbee 7
1 Institute of Systematic Botany, University of Zurich, Zurich, 2 Department of Biological Oceanography, Lamont-Doherty Earth Observatory,
Columbia University, Palisades, New York, 3 Albuquerque, New Mexico, 4 Botanical Institute, Department of Mycology and Phycology,
University of Copenhagen, Copenhagen, 5 Department of Botany, Miami University, Oxford, Ohio, 6 Department of Botany, Arizona State
University, Tempe, Arizona, and 7 School of Botany, University of Melbourne, Parkville, Victoria
Received September 28, 1993
Accepted January 2, 1994
Summary. The use of a precise terminology is important to the clature of the Cytoskeletal Elements in Protists", An
unambiguous exchange of information in the multidisciplinary area dersen et al. 1991).
of protistology. In this paper we attempt to establish clear definitions,
The task of defining cell surface features for protists
give illustrations, and comment on the different terms used for cell
is complex for several reasons:
surface structures of protists and related organisms.
Keywords: Protists; Algae; Fungi; Protozoa; Cell surface structures; (1) The limits of this kingdom (if it is indeed a single
Terminology; Nomenclature. assemblage; see Corliss 1993) are not clear, and the
"Kingdom Protista" most likely encompasses a para
Introduction
phyletic assemblage of eukaryotic organisms with rel
Cell surface structures are scientifically important for atively simple body structure (i.e., no highly differen
a number of reasons including species identification, tiated tissues, multicellular organs, or complex em
cell structural support and protection, evidence of cel bryological development). We have been inclusive in
lular biosynthetic activity and stages of development, the organisms considered and have incorporated terms
as well as cell-cell interactions and antigenic properties which apply to all taxa of algae, protozoa and fungi.
of the cell. The reason for this strategy is that "lower" organisms
The terminology used to describe cell surface structures in the Kingdoms Plantae, Animalia, and Fungi inter
of protists is sometimes confusing. This is mainly be grade into Protista. For example recent molecular se
cause protists have traditionally been studied by work quence studies (Bowman et al. 1992, Wainright et al.
ers from different disciplines of biology (mycology, 1993) support the view that chytridiomycetes, with pro
phycology, protozoology), in which special vocabular genitor and close phylogenetic affinities with higher
ies have been developed and used over scores of years. fungi, are also phylogenetically related to protozoa
In order to assist the flow of information amongst the such as choanoflagellates. The term fungal-protists re
different scientific fields, to address the terminological fers to the "lower" plasmodial and zoosporic "fungi",
problems and to provide definitions of terms used in that are organisms resembling fungi but which are phy
protistology, a "Task Force" has been established with logenetically diverse, including those with affinities to
expertise in all three protistological disciplines (for Chromista (Cavalier-Smith 1986; labyrinthulids,
background and rationale of the Task Force concept, thraustochytrids, plasmodiophoromycetes, hyphochy
see a previous account on "Terminology and Nomen- triomycetes, oomycetes) and to fungi (chytridiomy
cetes). In preparing this glossary, we have unanimously
• Correspondence and reprints: Institut fiir Systematische Botanik,
adopted a "protist perspective" in order to demonstrate
Universitat Ziirich, Zollikerstrasse 107, CH-8008 Ziirich, Switzer
land. the need today to bridge the lamentable gap between
2 H. R. Preisig et al.: Terminology and nomenclature of protist cell surface structures
the conventionally separate fields of mycology, phy cially appear to be and because they may contain non
cology and protozoology. living material, we have included them (e.g., alveoli,
(2) Widely used terms may not always apply to ho amphiesma). Plasma membrane, cortex, epiplasm and
mologous structures. Common structures, such as cell pellicle are main constituents of the outer layers of the
walls and stalks, probably arose and evolved indepen living cytoplasm and have also been included, but oth
dently many times among organisms, and a single term erwise living cell-surface structures and appendages
applies to analogous structures in different protists, just have been omitted from direct consideration, even
as wings do in animals. Cell surface features are highly though they do protrude or extend from the surface of
adaptive, and chances of similarity of form due to sim the protist in some cases (e.g., cilia, flagella, hapto
ilar selective pressures are great. It is beyond the scope nemata, pseudopodia, tentacles, undulating mem
of this effort to suppose or propose homologies, but branes, etc.). Extrusive organelles have also been ex
hopefully the terms listed will suggest structures present cluded here (see Kugrens etal. 1994).
in diverse groups of protists which can be explored for (5) There is a multiplicity of terms used in protisto
potential homologies and as indicators of phylogenetic logical literature with reference to components of cell
relationships and organellar evolution. surface structures, but in this account we limited our
(3) As it is difficult to resolve homologous versus anal selves to major components and not all their "parts".
ogous functions for structures defined with the same For example, we dealt with "frustule" of diatoms, but
term among protists, the situation is even more per not with subparts of this structure such as mantle, girdle
plexing when terms also apply to structures produced bands, labiate processes, etc.
by other eukaryotes, as well as prokaryotes. We have
tried to identify these possible confusions, and again Literature citations have not been included in the def
emphasize that the same term may in practice be used initions because so many are possible. A great number
for analogous and unrelated structures. of pertinent citations can be found in accompanying
(4) Deciding the limits of extracellular material be papers in this volume and in the following references
comes difficult when demarcations are not certain and to major sources of protistological glossaries embracing
when material may have the superficial appearance of appropriate mycological, phycological, and protozo-
extracellular material. In the strictest sense some terms 010gica1 terms (overviews that naturally go beyond our
included in our list are not actually non-living com own coverage restricted to cell surface structures): Al
ponents of the cell surface, but because they superfi- exopoulos and Mims (1979), Anderson (1988), Berner
Abbreviations used in all legends: BF (bright field microscopy), DIC (Nomarski differential interference contrast microscopy), FM (fluorescence
microscopy), PC (phase contrast microscopy), SEM (scanning electron microscopy), TEM (transmission electron microscopy)
Fig. I. Adhesions. Extracellular adhesions (A) released from the germ tube (GT) of a germling of Entophlyctis variabilis (Chytridiomycetes).
High pressure cryofixed and freeze substituted material, TEM, x 25,000
Figs. 2 and 3. Adhesion pad
Fig. 2. Oomycete cystospore (S) attached to the surface of a glass coverslip at the site indicated with the arrow and germinating with a germ
tube (GT). The arrow denotes the location of the adhesion pad, which is not visible with DIC but is detected with staining, as seen in Fig. 3.
DIC, x 1,250
Fig.3. Binding pattern of fluorescein isothiocyanate labelled-wheat germ agglutinin lectin to N-acetylglucosamine sugar residues within
extracellular material on oomycete cystospore. The arrow points out the adhesion pad which adheres the cystospore to the glass cover slip.
Although cystospore walls do not bind the lectin, sheath material coating germ tube surfaces does. FM, x 1,250
Fig. 4. Amphiesma. Transverse section through the cell surface of the dinoflagellate Katodiniurn rotundaturn showing the amphiesma consisting
of the plasma membrane (PM) and underlying flattened amphiesmal vesicles (= alveolar sacs) (AS). A thin plate (P) is visible within the
vesicle. Groups of microtubules (Mt) are situated beneath the vesicles; Sc body scales. TEM, x 45,000
Fig. 5. Appressorium ring. Basidiospore (Bs). of Gyrnnosporangiurn juniper-virginianae (Basidiomycetes). Note the appressorium (A) and the
appressorium ring (AR). DIC, x 1,250
Figs. 6 and 7. Auxospore wall
Fig. 6. Siliceous scale from the auxospore wall of the diatom Melosira nurnrnuloides. TEM, x 10,000 (courtesy of R. M. Crawford)
Fig. 7. Auxospore pair of the diatom Rhoicosphenia curvata showing the numerous siliceous bands (perizonium) of the secondary auxospore
wall. The arrow points out the initial epivalve developing within the perizonium. SEM, x 10,000 (courtesy of D. G. Mann)
H. R. Preisig et al.: Terminology and nomenclature of protist cell surface structures 3
(1993), Bold and Wynne (1985), Grell (1973), Harrison (hence the suffix of the name) for some taxa (see Corliss
and Corliss (1991), Hawksworth et al. (1983), Lee et al. 1993).
(1985), Margulis etal. (1990, 1993), Moore-Landecker The terms are arranged in alphabetical order and are
(1990), Olive (1975), Ross etal. (1979), Sleigh (1989), not organized around a theme (such as function or
van den Hoek et al. (1994). spatial relationships), as one might expect. Thus, we
For the taxa of higher rank we have generally used assume cross-references will be easier to find in the text.
vernacular names. In most cases the taxonomic com Furthermore, functional or other groupings of terms
position of the group will be clear to the reader; there could be out-of-date at any point in the near future if
is debate concerning the most correct scientific name additional functions or relationships were discovered
for some taxa and the hierarchical level of classification necessitating reassignment. For cross-references the ab-
4 H. R. Preisig et al.: Tenninology and nomenclature of protist cell surface structures
breviation q.v. ("quo vide") has been used. Also note pads determines the overall morphology of the colony.
that some "lesser" synonyms have not been defined An adhesion disc made of denticles (ring) immediately
independently but entered with a notation to see the beneath the pellicle (q.v.) occurs in the ciliate Tricho
chosen "major" synonym (e.g., for "acellular stalk" dina. See also, Adhesions, Holdfast adhesion, Plaque,
see "stalk"). Stalk.
We hope that this account serves to identify specific
terminological problems and to suggest specific solu Adhesion plaque, see Adhesion pad.
tions that will be acceptable to the scientific commu
nity. Alveoli
Definition: Membrane-bounded flattened vesicles or
Results
sacs underlying the plasma membrane (q.v.) in certain
One hundred terms (including 34 synonyms) are dealt protists, most notably, the (majority of the) ciliates,
with below. the dinoflagellates [where they are called "amphiesmal
vesicles" (q.v.)], some sporozoan (apicomplexan) par
Acellular stalk, see Stalk. asitic protists, and possibly the glaucophyte algal pro
tists (Figs. 4 and 17).
Adhesions Comments: A single alveolar vesicle is also known as
Definition: Morphologically and chemically diverse a "lacuna", and the entire system in ciliates has been
classes of compounds which function in attachment of called a "lacunar system" in older literature. In more
cells to substrates or hosts (Fig. 1). recent usage, it is called pellicular alveoli. A similar
Comments: Distributions of adhesions at the cell sur system found in the Sporozoa is known as "inner mem
face range from adhesive junctions to the entire cell brane complex". In some actinopods (e.g., radiolaria)
surface. Symphoriontic ciliated protozoa, for example, an organic capsular wall (q.v.) surrounding the central
attach to host carapaces with stalks (q.v.) that have cell mass is deposited within lacunae resembling alveoli.
adhesive bases. Fine pseudopodia in amoeboid protists The flattened peripheral cisternae underlying the
that adhere closely to the substratum are categorized plasma membrane of oomycete zoospores may well
as adhesive. See also, Adhesion pad, Holdfast adhesion, deserve consideration as a kind of alveoli. In diatoms,
Holdfast organelle. the term alveoli is used for elongated chambers of the
valve (q.v.) opening to the inside of the cell by a large
Adhesion pad opening and with a perforate outer layer. See Conclu
Definition: A type of extracellular matrix (q.v.) which sions and recommendations; see also, Cortex, Epi
spreads at the cell or spore substrate interface, binding plasm, Pellicle.
the two surfaces together (Figs. 2 and 3).
Comments: "Adhesion pad", "adhesion plaque", "mu Amphiesma
cous pad" and "spore tip mucilage" are used as syn Definition: Term describing the plasma membrane
onyms. The polarized distribution of this material dis (q.v.) and the underlying flattened vesicles of dinofla
tinguishes it from an extracellular matrix or sheath gellates (amphiesmal vesicles = "thecal vesicles")
(q.v.). Among oomycetes it attaches encysting zoo which in some species contain plates (= thecal plates).
spores to a host or substrate; among pennate diatoms In certain naked dinoflagellates the amphiesmal vesi
it denotes distinct, localized regions of polysaccharide cles appear to be without plate-like structures (Fig. 4).
adhering cells together into colonies; among pedinellid Comments: Apparently the same system of vesicles un
flagellates (such as Apedinella) it is a surface associated derneath the plasma membrane occurs in ciliates, some
structure that spine-scales attach to. Adhesion pads apicomplexans, glaucophytes, and perhaps other pro
may have diverse origins including: (1) discharge from tists (see Alveoli), but the term amphiesma is presently
pre-existing organelles such as K-bodies as oomycete restricted to dinoflagellates.
zoospores are induced to encyst and (2) selective se
cretion of polysaccharide from localized pores on the Amphiesmal vesicles, see Amphiesma.
frustule (q.v.) surface of diatoms. Adhesion pads of
diatoms are a specialized part of the non-silicified, or Appressorium ring
ganic casing and maintain connections between daugh Definition: Extracellular matrix (q.v.) in an o-ring like
ter cells following division. The exact position of these arrangement through which the penetration peg from
H. R. Preisig et al.: Terminology and nomenclature of protist cell surface structures 5
the appressorium of some pathogenic fungi, such as is a dynamic structure for grasping and ingesting food
rust fungi, passes just prior to entering host cells particles, including filamentous algae in some species.
(Fig. 5). See also, Lorica.
Comments: Believed to assist in attachment of appres
sorium to host cell and preventing dislodgement as host Bristle
colonization occurs.
Definition: Siliceous elongated structure that is tucked
under, and cemented to, the distal portion of a scale
Auxospore wall in the synurophyte genus Mallomonas (Fig. 9). The
Definition: The cell wall (q.v.) of a diatom auxospore term "bristle" is also widely used to describe diverse
(a cell resulting from sexual fusion or autogamy, or stiff hair-like appendages on cell walls and other sur
one formed purely by vegetative processes that swells faces (e.g., in some chlorococcalean algae). In ciliates
to maximum size) (Figs. 6 and 7). it is a common name for stiff cilia of several kinds and
Comments: The auxospore wall differs from that of the functions.
normal vegetative cell. Its primary wall consists of po Comments: The terms "bristle" and "spine" (q.v.) are
lysaccharide material, which in most centric diatoms sometimes used as synonyms (e.g., in ciliates). Bristles
contains overlapping siliceous scales (q.v.) (Fig. 6). of Mallomonas radiate outwards from the cell and may
Auxospores may also develop a secondary wall system change their position relative to the longitudinal axis
consisting of siliceous hoops or bands, collectively of the cell. They are streamlined when the cell is actively
termed the "perizonium" (in pennate diatoms) and swimming and positioned closer to 90° at rest. Movable
"properizonium" (in centric diatoms), respectively. bristle-like components, possibly homologous to bris
Unlike the perizonium, the properizonium is not sep tles of Mallomonas, also occur on the valve (q.v.) of
arated spatially from the primary auxospore wall, but the diatom Corethron. Euplotid ciliates have modified
is physically and developmentally continuous with it. cilia known as bristles on the dorsal surface; they may
The individual siliceous components of the perizonium be sensory.
(properizonium) resemble modified girdle bands, and
are secreted sequentially to create the secondary auxo Capillitium
spore wall. The new frustule (q. v.) of the enlarged initial
Definition: Sterile threads, which are often coiled and
cell is deposited within the perizonium (properi
bear ornamentation, intermixed with spores of fruiting
zonium), which then ruptures to release the cell (Fig. 7).
bodies of some Mycetozoa. Differentiated prior to
complete spore cleavage, these threads aid in spore
Basal disc dispersal (Fig. 10).
Definition: A general term describing the attachment Comments: Among higher fungi' the' term is not re
of the stalk (q.v.) (or occasionally the entire aboral stricted to extracellular material, but can describe spe
surface of the body) to a substrate in a wide range of cialized hyphae in frutifications such as those in puff
protists. balls. The term "elaters" is sometimes used for capil
Comments: See also, Hypothallus. litial strands that are short and unbranched.
Basket Capsular wall
Definition: (1) An enclosing structure composed of Definition: An organic wall in actinopods, especially
loosely arranged components [spicules, costae (q.v.), radiolaria, composed of closely spaced plates deposited
etc.] surrounding a cell as in some choanoflagellates within cytoplasmic lacunae or alveoli (q.v.) at the pe
and silicoflagellates (Fig. 8); (2) a type of complex scale riphery of the central, more dense cytoplasm (Figs. 11
(q.v.) on the surface of some flagellates; (3) the conical and 12). Cytoplasmic projections protrude through po
array of microtubules forming a feeding apparatus in res in the wall. In myxozoan spores, the polar capsular
nassulid-type ciliates. wall consists of two layers with varying sensitivities to
Comments: The feeding apparatus in nassulid-type cil chemical digestion which can be observed with trans
iates is also known as a "feeding basket", "cytopha mission electron microscopy; the inner electron-lucent
ryngeal basket", or "cyrtos" and is an intracellular layer resists alkaline hydrolysis and the outer electron
structure with the narrow end of the conical array of dense layer is digested with proteases.
microtubules pointed toward the interior of the cell. It Comments: The thickness and organization of the wall