CHAPTER SIX
Apical Meristems
The term apical meristem refers to a group of meri-
stematic cells at the apex of shoot and root that by cell
division lay the foundation of the primary plant body.
As indicated in Chapter 5, meristems are composed
of initials, which perpetuate the meristems, and their
derivatives. Also the derivatives usually divide and
produce one or more generations of cells before the
cytologic changes, denoting differentiation of specific
cells and tissues, occur near the tip of the shoot or root.
The divisions continue at all levels where such changes
are already discernible. Therefore growth, in the sense
of cell division, is not limited to the very tip of shoot
or root but extends to levels considerably removed
from the region usually called the apical meristem. In
fact the divisions some distance from the apex are more
abundant than at the apex (Buvat, 1952). In the shoot
a more intensive meristematic activity is observed at
levels where new leaves are initiated than at the tip,
and during the elongation of the stem, cell division
extends several internodes below the apical meristem
(Sachs, 1965). The change from apical meristem to
adult primary tissues is gradual and involves the inter-
grading of the phenomena of cell division, cell enlarge-
Esau’s Plant Anatomy, Third Edition, By Ray F. Evert.
Copyright © 2006 John Wiley & Sons, Inc.
ment, and cell differentiation, so one cannot restrict the
term meristem to the apex of shoot and root. The parts
of shoot and root where future tissues and organs are
already partly determined but where cell division and
cell enlargement are still in progress are also
meristematic.
The profuse and inconsistent terminology in the
voluminous literature on apical meristems (Wardlaw,
1957; Clowes, 1961; Cutter, 1965; Gifford and Corson,
1971; Medford, 1992; Lyndon, 1998) reflects the com-
plexity of the subject matter. Most commonly the term
apical meristem is used in a wider sense than merely the
initials and their immediate derivatives; it also includes
variable lengths of shoot and root proximal to the apex.
Shoot apex and root apex often are employed as
synonyms of apical meristem, although a distinction is
sometimes made between the shoot apical meristem
and the shoot apex: the apical meristem denotes only
the part of the shoot lying distal to the youngest leaf
primordium, whereas the shoot apex includes the apical
meristem together with the subapical region bearing
young leaf primordia (Cutter, 1965). When determina-
tions of the dimensions of apices of shoots are made,
133
134 | Esau’s Plant Anatomy, Third Edition

only the part above the youngest leaf primordium, or
the youngest node, is measured.
When it is important to differentiate the least deter-
mined part of the apical meristem the term promeri-
stem or protomeristem (Jackson, 1953) is used: it
refers to the initials and their most recent derivatives,
which exhibit no evidence of tissue differentiation and
are presumed to be in the same physiological state as
the initials (Sussex and Steeves, 1967; Steeves and
Sussex, 1989). Johnson and Tolbert’s (1960) metameri-
stem refers to the same group of cells as the promeri-
stem (protomeristem). They define it specifically as “the
central part of the shoot apex which maintains itself,
contributes to the growth and organization of the apex,
but exhibits little or no evidence of tissue separation.”
Thus this least determined part of the apical meristem
corresponds to the general area termed the central zone
in shoot apices (see below). The promeristem of Clowes
(1961), on the other hand, includes only the initials.
❙ EVOLUTION OF THE CONCEPT OF APICAL ORGANIZATION
Apical Meristems Originally Were Envisioned as
Having a Single Initial Cell
Following Wolff’s (1759) recognition of the shoot apex
as an undeveloped region from which growth of the
plant proceeded and the discovery of a single, morpho-
logically distinct initial cell at the apex of seedless vas-
cular plants, the idea developed that such cells exist in
seed plants as well. The apical cell (Fig. 6.1) was inter-
preted as a consistent structural and functional unit
of apical meristems governing the whole process of
growth (the apical-cell theory). Subsequent research-
ers refuted the assumption of a universal occurrence of
single apical cells and replaced it by a concept of inde-
pendent origin of different parts of the plant body.
The Apical-Cell Theory Was Superseded by the
Histogen Theory
The histogen theory was developed by Hanstein (1868,
1870) on the basis of extensive studies of angiosperm
shoot apices and embryos. According to this theory the
main body of the plant arises not from superficial cells
but from a massive meristem of considerable depth com-
prising three parts, the histogens, which may be dis-
tinguished by their origin and course of development.
The outermost part, the dermatogen (from the Greek
words meaning skin and to bring forth), is the precursor
of the epidermis; the second, the periblem (from the
Greek, clothing), gives rise to the cortex; the third, the
plerome (from the Greek, that which fills), constitutes
the inner mass of the axis. The dermatogen, each layer

derivatives

A B

apical cells

leaf
primordium

C D

Equisetum shoot Pteridium rhizome

FIGURE 6.1
Shoot apices with apical cells. A, B, two forms of the apical cell, pyramidal, or four-sided, (A) and lenticular, or three-
sided, (B). Cells are cut off from three faces of the pyramidal cell, from two in the lenticular. In both A and B a deriva-
tive cell is shown attached to the right side of the apical cell. C, D, apical cells in longitudinal sections of shoot (C)
and rhizome (D). In C, apical cells in leaf primordia; one of these (left) is dividing. Subdivided derivatives—
merophytes—of the apical cell are indicated by slightly thicker walls. (C, D, ×230. A, B, adapted from Schüepp, 1926.
www.schweizerbart.de)

of the periblem, and the plerome begin with one or
several initials distributed in superposed tiers in the
most distal part of the apical meristem.
Hanstein’s “dermatogen” is not equivalent to Haber-
landt’s (1914) “protoderm.” Haberlandt’s protoderm
refers to the outermost layer of the apical meristem
regardless of whether this layer arises from independent
initials or not, and regardless of whether it gives rise to
the epidermis or to some subepidermal tissue as well.
In many apices the epidermis does originate from an
independent layer in the apical meristem; in such apices
the protoderm and dermatogen may coincide. The
periblem and plerome in the sense of Hanstein are dis-
cernible in many roots but are seldom delimited in
shoots. Thus the subdivision into dermatogen, periblem,
and plerome has no universal application. But the fatal
flaw of Hanstein’s histogen theory is its presumption
that the destinies of the different regions of the plant
body are determined by the discrete origin of these
regions in the apical meristem.
The Tunica-Corpus Concept of Apical Organization
Applies Largely to Angiosperms
The apical-cell and histogen theories were developed
with reference to both root and shoot apices. The third
theory of apical structure, the tunica-corpus theory
of A. Schmidt (1924), was an outcome of observations
on angiosperm shoot apices. It states that the initial
region of the apical meristem consists of (1) the tunica,
one or more peripheral layers of cells that divide in
planes perpendicular to the surface of the meristem
(anticlinal divisions), and (2) the corpus, a body of cells
several layers deep in which the cells divide in various
planes (Fig. 6.2). Thus, whereas the corpus adds bulk
to the apical meristem by increase in volume, the one
or more layers of tunica maintain their continuity over
anticlinal division
initial layer of corpus
leaf primordium
FIGURE 6.2
Shoot apex of Pisum (pea). Cellular details in A, interpretative diagram in B. The pith meristem does not show typical
rib-meristem form of growth. (From Esau, 1977.)
Apical Meristems | 135
the enlarging mass by surface growth. Each layer of
tunica arises from a small group of separate initials, and
the corpus has its own initials located beneath those of
the tunica. In other words, the number of tiers of initials
is equal to the number of tunica layers plus one, the tier
of corpus initials. In contrast to the histogen theory,
the tunica-corpus theory does not imply any relation
between the configuration of cells at the apex and
histogenesis below the apex. Although the epidermis
usually arises from the outermost layer of tunica, which
thus coincides with Hanstein’s dermatogen, the underly-
ing tissues may have their origin in the tunica or corpus
or both, depending on the plant species and the number
of tunica layers.
As more plants came to be examined, the tunica-
corpus concept underwent some modifications, espe-
cially with regard to the strictness of the defi nition of
the tunica. According to one view, tunica should include
only those layers that never show any periclinal divi-
sions in the median position, that is, above the level of
origin of leaf primordia (Jentsch, 1957). If the apex
contains additional parallel layers that periodically
divide periclinally, these layers are assigned to the
corpus and the latter is characterized as being stratified
(Sussex, 1955; Tolbert and Johnson, 1966). Other
workers treat the tunica more loosely and describe it as
fluctuating in number of layers: one or more of the inner
layers of the tunica may divide periclinally and thus
become part of the corpus (Clowes, 1961). Because of
the differing usage of the term tunica, its usefulness in
accurately describing growth relations at the shoot apex
was questioned by Popham (1951), who proposed the
term mantle to include “all layers at the summit of the
apex in which anticlinal divisions are sufficiently
frequent to result in the perpetuation of definite cell
layers”; the mantle overarches a body of cells called the
core. The term corpus was avoided.
two-layered tunica
corpus
pith meristem
A B
136 | Esau’s Plant Anatomy, Third Edition
The Shoot Apices of Most Gymnosperms and
Angiosperms Show a Cytohistological Zonation
The tunica-corpus concept, which was developed with
reference to angiosperm shoot apices, proved to be
largely unsuitable for the characterization of the apical
meristem of gymnosperms (Foster, 1938, 1941; Johnson,
1951; Gifford and Corson, 1971; Cecich, 1980). With few
exceptions (Gnetum, Ephedra, and several species of
conifers) the gymnosperms do not show a tunica-corpus
organization in the shoot apex; that is, they do not have
stable surface layers dividing only anticlinally. The outer-
most layer of the apical meristem undergoes periclinal
and anticlinal divisions and contributes cells to the
peripheral and interior tissues of the shoot. The surface
cells located in a median position in the apical meristem
are interpreted as initials. Studies of gymnosperm apices
led to the recognition of a zonation—termed a cytohis-
tological zonation—based not only on planes of divi-
sion but also on cytologic and histologic differentiation
and the degree of meristematic activity of the compo-
nent cell complexes (Fig. 6.3). Similar zonations, super-
imposed on a tunica-corpus organization, have since
been observed in most angiosperms (Clowes, 1961;
Gifford and Corson, 1971).
The cytologic zones that may be recognized in shoot
apical meristems vary in degree of differentiation and
in details of grouping of cells. The zonation may be suc-
cinctly characterized by dividing the apical meristem
into a central zone and two zones derived from it. One
of these, the rib zone, or rib (pith) meristem, appears
directly below the central zone and is centrally located
in the apex. It usually becomes the pith after additional
meristematic activity has occurred. The other, the
peripheral zone, or peripheral meristem, encircles
the other zones. The peripheral zone typically is the
most meristematic of all three zones and has the densest
protoplasts and the smallest cell dimensions. It may be
described as a eumeristem. Leaf primordia and the
procambium arise here, as well as the cortical ground
tissue. In species with a tunica-corpus organization, the
central zone corresponds to the corpus and the
portion(s) of the tunica layer(s) overlying the corpus.
❙ INQUIRIES INTO THE IDENTITY OF APICAL INITIALS
The next development in the interpretation of the shoot
apical meristem resulted from the efforts of French
cytologists (Buvat, 1955a; Nougarède, 1967). Meriste-
matic activity drew the chief attention of this work.
Counts of mitoses, and cytological, histochemical, and
ultrastructural studies served to formulate the theory
that after the apical structure is organized in the embryo,
the central zone of cells becomes the waiting meristem
(Fig. 6.4; méristème d’attente). The méristème d’attente
stays in a quiescent state until the reproductive stage is
peripheral apical initials
zone
central
mother cells
transitional
zone
rib meristem
A
central mother cells
initial layer
transitional
zone
peripheral
zone
rib meristem
B
FIGURE 6.3
Shoot tip of Pinus strobus in longitudinal view. Cellular
details in A, interpretative diagram in B. Apical initials
contribute cells to the surface layer by anticlinal divi-
sions and to the central mother-cell zone by periclinal
divisions. The mother-cell zone (cells with nuclei) con-
tributes cells to the transitional zone composed of
actively dividing cells arranged in a series radiating from
the mother-cell zone. Products of these divisions form
the rib meristem and the subsurface layers of the periph-
eral zone. (A, ×139. A, as drawn from a slide by A. R.
Spurr; B, from Esau, 1977.)
reached and meristematic activity is resumed in the
distal cells. During the vegetative stage, meristematic
activity is centered in the initiating ring (anneau
initial), corresponding to the peripheral zone, and in
the medullary (pith) meristem (méristème medul-
laire). The concept of the inactive central zone in the
apical meristem was extended from the shoots of angio-
sperms to those of gymnosperms (Camefort, 1956; who
called the central zone “zone apicale”) and the seedless
vascular plants (Buvat, 1955b), and to roots (Buvat and
Genevès, 1951; Buvat and Liard, 1953). The concept was
later somewhat modified in that variations in degree of
inactivity of the central zone in relation to the size of
the apex and its stage of development came to be
recognized (Catesson, 1953; Lance, 1957; Loiseau, 1959).
With regard to root apices, the occurrence of an inactive
 Apical Meristems | 137

TABLE 6.1 ■ Cell Doubling Time (Mean Cell

Generation Time) at the Summit and on the Flanks of
Vegetative Shoot Apical Meristems of Angiosperms

Cell Doubling Time (h)

Species Summit c Flanksd

ma Trifolium repens 108 69
Pisum (probably P. sativum) 69 28
Pisum (main apex) 49 31
ai ai Pisum (axillary bud, initiated) 127 65
Pisum (axillary bud, released) 40 33
Oryza (rice) 86 11
Rudbeckia bicolor >40 30
Solanum (potato) 117 74
Datura stramonium 76 36
Coleus blumei 250 130
Sinapis alba 288 157
Chrysanthemuma 144 50
mm Chrysanthemumb 102 32
FIGURE 6.4 Chrysanthemum 139 48
Chrysanthemum segetum 140 54
Diagram of a shoot apex of Cheiranthus cheiri inter-
Helianthus annuus 83 37
preted according to the méristème d’attente concept.
Details: ai, anneau initial; ma, méristème d’attente; mm, Source: From Lyndon, 1998.
méristème medullaire. (After Buvat, 1955a. © Masson, a
photon flux = 70 μmol/m2 .
Paris.)
b
photon flux = 200 μmol/m2 .
c
Or central zone.
d
Or peripheral zone.
center in the meristem found confirmation in many
studies, resulting in the development of the concept of
quiescent center by Clowes (1961).
The revision of the concept of apical initials by viding evidence for one to three initials in each layer
the French workers served as a considerable stimulant (Stewart and Dermen, 1970, 1979; Zagórska-Marek and
for further research on apical meristems (Cutter, 1965; Turzańska, 2000; Korn, 2001).
Nougarède, 1967; Gifford and Corson, 1971). Counts of The relation between the initials and the immediate
mitoses in different regions of the shoot apex, feeding derivatives in the apical meristem is flexible. A cell func-
root tips with radiolabeled compounds to detect the tions as an initial not because of any inherent properties
location and synthesis of DNA, RNA, and protein, histo- but because of its position. (See the similar concept of
chemical tests, experimental manipulations, and tracing initials in the vascular cambium, Chapter 12.) At the
of cell patterns in fi xed and living shoot apices provided time of division of an initial it is impossible to predict
data that, in essence, corroborated the postulate of the which of the two daughter cells will “inherit” the initial
relative infrequency of mitotic activity in the central function and which will become the derivative. It is also
zone (Table 6.1) (Davis et al., 1979; Lyndon, 1976, known that a given initial may be replaced by a cell that
1998). through prior history would be classified as a derivative
Recognition of the relative infrequency of mitotic of an initial (Soma and Ball, 1964; Ball, 1972; Ruth et al.,
activity in the central zone has not led to an abandon- 1985; Hara, 1995; Zagórska-Marek and Turzańska,
ment of the concept that the most distal cells are the 2000).
true initials and the ultimate source of all body cells in Inasmuch as no cells are permanent initials, Newman
the shoot. Considering the geometry of the apex, one (1965) maintained that in order to understand structure
can deduce a priori that in view of the exponential and functioning of a meristem, a distinction must be
growth of the derivatives of the apical meristem, a few made between the “continuing meristematic residue”—
divisions in the distalmost cells would result in the that is, the source of cellular structure that functions as
propagation of any distinctive genome characteristic of initials—and the “general meristem,” a region of elabo-
these cells through large populations of cells. As noted ration. Emergence of new cells from the continuing
earlier, the tunica-corpus theory postulated the pres- meristematic residue is a very slow, continuous process
ence of a small group of initials in each layer of the of long duration, whereas the passage of cells in the
apical meristem. Clonal analyses are often cited as pro- general meristem is a very rapid, continuous process of
138 | Esau’s Plant Anatomy, Third Edition
only short duration. This concept is used in Newman’s
classification of apical meristems designed for all groups
of vascular plants: (1) monopodial, as in ferns—the
residue is in the superficial layer and any kind of division
contributes to growth in length and breadth; (2)
simplex, as in gymnosperms—the residue is in a single,
superficial layer and both anticlinal and periclinal divi-
sions are needed for bulk growth; (3) duplex, as in
angiosperms—the residue occurs in at least two surface
layers with two contrasting modes of growth, anticlinal
divisions near the surface and divisions in at least two
planes deeper in the apical meristem.
❙ VEGETATIVE SHOOT APEX
The vegetative shoot apex is a dynamic structure that
in addition to adding cells to the primary plant body,
repetitively produces units, or modules, called phyto-
meres (Fig. 6.5). Each phytomere consists of a node,
apical meristem
leaf primordia
bud primordia
leaf
node
phytomere
internode
axillary bud
FIGURE 6.5
Diagram of a longitudinal section of a eudicot shoot tip.
Activity of the apical meristem, which repetitively pro-
duces leaf and bud primordia, results in a succession of
repeated units called phytomeres. Each phytomere con-
sists of a node, its attached leaf, the internode below
that leaf, and the bud at the base of the internode. The
boundaries of the phytomeres are indicated by the
dashed lines. Note that the internodes are increasing in
length the farther they are from the apical meristem.
Internodal elongation accounts for most of the increase
in length of the stem.
with its attached leaf, a subjacent internode, and a bud
at the base of the internode. The bud is located in the
axil of the leaf of the next lower phytomere and may
develop into a lateral shoot. In seed plants the apical
meristem of the first shoot is organized in the embryo
before or after the appearance of the cotyledon or coty-
ledons (Saint-Côme, 1966; Nougarède, 1967; Gregory
and Romberger, 1972).
Vegetative shoot apices vary in shape, size, cytologic
zonation, and meristematic activity (Fig. 6.6). The shoot
apices of conifers are commonly relatively narrow and
conical in form; in Ginkgo and in the cycads they are
rather broad and flat. The apical meristem of some
monocots (grasses, Elodea) and eudicots (Hippuris) is
sa
pr
A
sa
pr
B
FIGURE 6.6
Distinctive forms of shoot apices (sa): flat or slightly
concave in Drimys (A) and conical but inserted on
broad base bearing leaf primordia in Washingtonia
palm (B). Longitudinal sections. The large cavities in
the Drimys shoot apex are oil cells. Other detail: pr,
procambium. (A, ×90; B, ×19. A, slide by Ernest M.
Gifford; B, from Ball, 1941.)