BofanicalJournal of the I.inncan Socie!v (1981), 83: 199 212. With 3' figures
Terminology and classification of stomata
and stornatal development-a critical survey
HANNE RASMUSSEN
Institute of Plant Anatomy &3 Cytology, University of Copenhagen, Solvgade 83,
DK 1307 Copenhagen K , Denmark
Acccpttd for publication May 1981
The literature on terminology of stomata and stomatal development is reviewed and the terminology
rationalized. The classification of developmental types and of the developing cells should not be
combined with the morphological classification of mature stornatal complexes. The cells involved in
the development should be distinguished on the basis of their origin and position in the developing
stornatal complex, and not on the basis of their future form and appearance. It is unsound to
distinguish any kind ofcell only on the basis ofa presumed future division by which it is replaced by its
two daughter cells.
Development ofstomata begins with the formation of a stornatal meristemoid by an unequal division
of a protodermal cell. A meristemoid may divide unequally to produce a new meristemoid and a
mesogene cell. Stomata1 meristemoids eventually function as guard-cell mother-cells. The adjective
perigene is restricted to those cells that have arisen by divisions of protodermal cells surrounding the
future stoma. The undivided cells surrounding protodermal cells should be termed agene cells, and not
neighbouring cells, a term which should be restricted to morphological terminology.
KEY WORDS:-meristemoid -- mesogene cell - neighbouring cell
stornatal development - subsidiary cell - terminology.
-
perigene cell
-
stomata
-
CONTENTS
Introduction . . . . .
Terminology . . . . .
Discussion. . . . . .
The combined terminology
. . . .
Protoderm
The meristemoid . . .
The surrounding cells . .
Thestoma
. . . .
Reservations . . . .
Acknowledgements. . . .
References. . . . . .
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199
200
202
202
20'3
204
208
210
211
211
211
INTRODUCTION
Stomata in plants are generally considered homologous structures. Therefore
the comparative study of stomata and stomatal development is meaningful, and a
consistent and universal terminology is needed to facilitate the comparison.
0024-4074/81/070199+ 14 $02.00/0
199
01981 The Linnean Society of London
200
H. RASMUSSEN
The history of the terminology of stomata and the recent discussions and
suggestions to alterations illustrate a progression towards a more generalized
terminology. The progress in the study of stomatal ontogeny in the last few decades
has revealed a variation pattern much more diverse than previously imagined, and
has made necessary an elaborate terminology. A suggestion for a complete
terminology for stomata according to their ontogeny was presented by Pant
(1965), who based his system on the terminology for gymnosperms created by
Florin ( 1931, 1933). Pant’s system was later extended by Stevens & Martin ( 1978).
There is increasing acceptance of their basic concepts, although some problems
remain unsettled, especially regarding the distinction between this terminology
and the traditional morphological terminology describing mature stomata
(Metcalfe & Chalk, 1950; Van Cotthem, 1970; IVilkinson, 1979). The definition
of the initial point of stomatal development has also been discussed, most recently
by Payne (1979).
A review of the literature on stomatal terminology especially with respect to the
ontogenetic terminology, reveals intended and unintended changes of definitions,
some of which may be a source of confusion when new observations are to be
compared with previous results. These changes and their consequences for the
terminology will be assessed in the following pages.
TERMINOLOGY
The terminology recommended here is based on considerations of previous
literature and on my own observations of stomatal development, especially in
Liliiflorae. The basic ideas stem from discussions on terminology with Dr D. F.
Cutler (see also Cutler, 1978).
Existing concepts are used and the terminology of these precisely defined, with
the aim that the terminology should be widely applicable. The morphological
description of the mature stomatal complex and the description of its development
should be separate, and no term should have a dual connotation.
The MORPHOLOGICAL TERMINOLOGY includes the term SUBSIDIARY CELL for
epidermal cells adjacent to the stoma, and which differ from other epidermal cells,
and the term NEIGHBOURING CELL for epidermal cells adjacent to the stoma, but
which are morphologically indistinguishable from other epidermal cells. IYhen
these terms are used, no consideration is given to the origin of the cells. (This is in
accordance with Fryns-Claessens & Van Cotthem, 1973.)
Terms such as ‘paracytic’, ‘anisocytic’, ‘tetracytic’, will be applied to the mature
stomatal complex according to purely morphological criteria. (Thisis in accordance
with Van Cotthem, 1970, 1971 ; Wilkinson, 1979.)
The ONTOGENETIC TERMINOLOGY includes the terms ‘meristemoid’, ‘mesogene
cell’, ‘perigene cell’, and ‘agene cell’. The terms are applied according to the origin
of the cells and their position during development. Hence, the term MERISTEMOID is
used for a cell formed by an unequal division of a protodermal cell (see Fig. 2,
lower row). It is a cell of meristematic properties and appearance; if a stomatal
meristemoid, it will give rise to the guard-cell mother-cell directly or after further
divisions. A meristemoid of higher order may be produced by an unequal division
of the meristemoid. (This is in accordance with Fryns-Claessens & Van Cotthem,
1973.) The term MESOGENE CELL is used for any cell derived by division of a
meristemoid (that is not itself a meristemoid) before the meristemoid divides into
TERMINOLOGY O F STOMATAL DEVELOPMENT
20 I
the two guard cells (See Fig. 2, lower row). (This is in accordance with Pant,
1965.) Daughter cells of a divided mesogene cell are mesogene cells. The term
PERIGENE CELL is used for any daughter cell formed by one or more divisions in a
protodermal cell adjacent to the guard-cell mother-cell (see Fig. 2, lower row).
Divisions forming the perigene cells are not connected with normal meristematic
activity, but are clearly related to the presence of meristemoids. (No special
properties will be ascribed to such dividing protodermal cells by their
terminology.) Daughter cells of a divided perigene cell are perigene cells. The
perigene cell is broadly equivalent to the perigene subsidiary cell defined by
Stevens & Martin, 1978; see Discussion, ‘The surrounding cells’),
Any protodermal cell, adjacent to the guard-cell mother-cell and which remains
in this position without dividing is here called a n AGENE CELL. This term is not
defined as precisely as those for the mesogene and perigene cells, because the
‘agene cell’ cannot be distinguished from other protodermal cells on the basis of its
descent, and can be identified only towards the end ofstomatal development when
it is apparent that it will not give rise to perigene cells. However, it is convenient to
be able to refer to this kind of cell, as in the scheme below. The ‘agene cell’, as
introduced here, is equivalent to the neighbouring cell in an ontogenetic context as
defined by Stevens & Martin (1978).
As defined above, the meristemoid constitutes a general concept which can be
used elsewhere, for example in the description of developing trichomes. The
4
...,”’
1 1
-+
Figure 1. Representation ofdevelopmental types according to definitions of Stevens & Martin (1978).
The meristemoid and its derivatives are indicated by stippling, the proximal perigene cells by hatched
cell walls towards their sister cells. ( I ) The meristemoid divides to form two guard-cells (agenous). ( 2 )
Perigene cells are formed, incompletely surrounding the meristemoid = the guard-cell mother-cell
(hemiperigenous).(3)Perigenecellsare formedaround the meristemoid = theguard-cellmother-cell, on
all sides (euperigenous). (4) One or more mesogene cells are formed by the meristemoid, incompletely
surrounding the guard-cell mother-cell (hemimesogenous). (5)Both the mesogene and perigene cells are
formed , incompletely surrounding the guard-cell mother-cell (hemimesoperigenous). (6) Perigene and
mesogene cells completely surround the guard-cell mother-cell (eumesoperigenous). (7)Mesogene cells
completely surround the guard-cell mother-cell (eumesogenous).
202
H. RASMUSSEN
surrounding cells are at present distinguished only in studies of stomatal
development and are defined in relatior-, only to the developing stomatal
merist emoid.
The stomatal complex at the end of the development is described as follows (in
accordance with Stevens & Martin, 1978, corresponding numbers in Fig. 1 are
indicated in brackets) :
agenous (1)
euperigenous (3)
eumesogenous (7)
hemiperigenous (2)
hemimesogenous (4)
eumesoperigenous ( 6 )
hemimesoperigenous ( 5 )
- surrounded
- surrounded
- surrounded
- surrounded
- surrounded
- surrounded
- surrounded
solely by agene cells
solely by perigene cells
solely by mesogene cells
by agene and perigene cells
by agene and mesogene cells
by perigene and mesogene cells
by agene, perigene and mesogene cells
Every possible combination of the three kinds of surrounding cells is
accommodated in this scheme.
The stomata can further be described by the angle formed by the wall between
the guard cells and the wall of the preceding cell division as parameristic ( O O ) ,
diameristic (go”), and anomomeristic (any other angle) (Payne, 1979).
Other ontogenetic terms which are not used here, have been defined for certain
cells solely by virtue of their daughter cells. One example is the ‘subsidiary
meristemoid’ (Stevens & Martin, 1978). The unsoundness of using such terms is
discussed below.
DISCUSSION
The combined terminology
Stomata1 development proceeds as a characteristic sequence of cell divisions in
the protoderm followed by the growth and differentiation of the cells constituting
the mature stomatal complex. Different initial developments of the stomatal
complexes may, by later growth, attain a similar mature appearance; similar
initial developments of the stomatal complexes, do not necessarily lead to a similar
adult form.
The developing stomatal complex can be classified according to the divisions
taking place in the first stage of development. The cells constituting the developing
complex at any stage can be defined on their derivation and position. This
classification, referring to the occurrence of certain cell divisions, has a limited
number of well-defined classes which can be designated by accurate, mutually
exclusive terms.
There is a long tradition for classifying mature stomatal complexes on
morphological criteria. T o the four classical terms ‘anomocytic’, ‘anisocytic’,
‘paracytic’, and ‘diacytic’ (Metcalfe & Chalk, 1950), several have been added (a
survey is given by Van Cotthem, 1970, 1971 ; Wilkinson, 1979). It is a matter of
judgement how many terms are needed to describe the more or less continuous
range of variation in the structure of mature stomatal complexes. The application
of a certain term depends on the subjective recognition of the structural
differentiation of the surrounding cells in relation to the other epidermal cells.
Hence, the individual terms cannot be mutually exclusive.
TERMINOLOGY OF STOMATAL DEVELOPMENT
203
A complex terminology has been created to combine ontogenetic and
morphological description of the stomatal apparatus (Fryns-Claessens & Van
Cotthem, 1973; Stevens & Martin, 1978). This combined terminology is based
on two presumptions. The first is that all cells surrounding the stoma, having gone
through a similar development, will show a similar structural differentiation at
maturity. The second is that all surrounding cells deviating in structure from other
epidermal cells at maturity must have participated in the development of the
stomatal complex. Our present knowledge does not support these two statements.
It has been pointed out on several occasions (Pant, 1965; Paliwal, 1969;
Tomlinson, 1969) that several developmental pathways may result in the
formation of indistinguishable mature stomatal complexes and that similar
sequences of cell divisions may result in quite different structural patterns at
maturity. The development of the stomatal complex and its appearance at
maturity can therefore be considered as independent characters.
Fryns-Claessens & Van Cotthem (1973) suggested 26 combined terms in the
form ‘paramesogenous’, ‘anisomesoperigenous’, etc. (with unnumbered
subdivisions) in a system which still includes only the combinations of character
states already known, anticipating that future results would increase the system.
Stevens & Martin (1978) raised the number of ontogenetic terms for the stomatal
complex from the three recognized by Fryns-Claessens & Van Cotthem to seven.
Although well-founded and advantageous to ontogenetic studies, such a change
potentially increases the number of combined terms to more than fifty.
Ontogenetic studies require living plant material, but morphological studies can
be done on herbarium specimens. As a result, the structure of mature stomata has
often been described without reference to the ontogeny. The structure of the
mature stomatal complex provides a character of a certain taxonomic importance.
As a resistant plant fragment, the cuticle, with imprints of the mature stomata, is
important as a means of identifying Recent and fossil plants. However, the
combined terminology cannot be used in these cases because it implies a
knowledge of the development.
The fact that no exact demarcation can be drawn between growing stage and
maturity evidently underlies the efforts of combining the ontogenetic and
morphological terminology. However, the entire process of development will be
satisfactorily circumscribed if one term is used to describe the cell divisions
involved and another term is used to describe the mature state.
It seems advisable to avoid the combined terminology, because it is unnecessary
and cumbersome, and because of the questionable value of combining two
fundamentally different classifications.
If the combined terminology is rejected, the classification of surrounding cells
becomes much simplified, and a means of describing mature structures without
knowledge of the development is maintained.
Protodenn
The protoderm is described as the meristem of the epidermis (e.g. Fahn,
1974). The protoderm cells form by division of the epidermal layers. The transition
from a protodermal to an epidermal cell involves a cessation ofmitotic activity and
a structural differentiation. Strictly speaking, the cells surrounding the developing
Patel 1978
b
PrOtOd.-rm c e l l s
.
5-residual
k Nelqhbourlng
protoderm
Ne'qhbourinq
Cell
D
cell
k
R e s i d u a l protoderm
19,9
Termlnoloqy
accepted h e r e
k
Protoderm cells
D
MerlStemoid
'
PcotOderm cells
D
.
Mesoqene cell
b
Mesoqene cell
Merrstemoid
b
nesoqene Cell
b
Perlqene cells
M e n e Cell
Contact Cell5
~dpc'vatlYes Of
neighhour Inq cells
cell
6
P e r i q e n e cells
g
per,gene cells
stomata should in many cases be called young epidermal cells rather than
protodermal cells. However, the term protodermal cells has been used rather
liberally in papers on stornatal development for the young stages of future
epidermal cells, whether still in meristematic activity or not. This established usage
will be retained here, restricting the term epidermal cells to the more or less fully
differentiated cell.
The different usage of various terms in some important'papers on this subject is
shown schematically in Fig. 2, and is discussed below.
The meristmoid
It is now generally accepted that stornatal development is initiated by a n
unequal, anticlinal division of a protodermal cell (Fryns-Claessens & Van
Cotthem, 1973; Stevens & Martin, 1978; Payne, 1979).
Some exceptions have been described from sporophytes of mosses (Campbell,
1895; Cavers, 191 1 ; Paton 1951), from Psilotum and Tmesipteris (Pant & Khare,
1971), Cyras and Ginkgo (Pant & Mehra, 1964) and in conifers (Florin, 1931). I n
these cases a protodermal cell is claimed to divide only once to produce the guard
cells directly. However, Maroti ( 1966) demonstrated unequal divisions in both
Psilotum nudum and Tmesipteris elongata. The records of such exceptions could
TERMINOLOGY OF STOMATAL DEVELOPMENT
205
therefore be erroneous resulting from a f i l u r e to observe a previous unequal
division, an opinion held by Fryns-Claessens & Van Cotthem (1973)and by Payne
( 1979).
O n the other hand, Florin (1931 : 54) explicitly noted that such an unequal
division did not occur in the numerous conifers studied by him. O n this basis he
segregated three fundamental types of stornatal development, of which the last
two were already known from other plant groups:
The protodermal cell destined for stornatal development (called
‘Urmutterzelle’) becomes the guard-cell mother-cell directly. (This was later
(Florin, 1933 : 14) called ‘haplocheilic’ development.)
The guard-cell mother-cell is formed by a single unequal division of the
‘Urm u t terzelle’.
The guard-cell mother-cell is formed after preceding divisions of the
‘Urmutterzelle’. (The ‘syndetocheilic’ development (Florin, 1933) would fall in
this category.)
In the terminology system set up by Pant (1965)’ the first two groups were
united, neglecting the difference between them, and in the later modification of the
system by Fryns-Claessens & Van Cotthem (1973) the occurrence of the first of
Florin’s groups was questioned (see below and Fig. 3 ) . Fresh studies of stornatal
development of mosses and gymnosperms are needed to settle the matter.
Nevertheless, an unequal division of a protodermal cell initiates stornatal
development in a wide range of ferns and angiosperms, and this feature ofstornatal
development is possibly universal.
The unequal division of the protodermal cell results in two cells with quite
different properties. One cell, usually the larger (and in monocotyledons the
proximal one with respect to the basal leaf meristem) is vacuolated and looks much
like the protodermal cells. The other cell, often delimited by a curved wall from its
sister cell, is usually markedly smaller and characterized by a denser cytoplasm, a
stronger stainability, and a nuclear dimension which is significantly different from
that of the protodermal cells. This cell develops into the guard-cell mother-cell
either directly or after subsequent divisions, and is called a ‘meristemoid’ by many
recent workers (Fryns-Claessens & Van Cotthem, 1973; Tomlinson, 1974; Stevens
& Martin, 1978), (Fig. 2). However, Biinning (1956) used the same term with a
much wider connotation to include every cell outside the meristem with ability to
divide, viz. any epidermal cells dividing and any further dividing derivatives. In
accordance with this, Pant (1965) defined the meristemoid as “a protoderm cell
whose first division or closely following consecutive divisions ultimately lead to the
formation of the guard cells . . . , and such segments of the meristemoid which
retain the capacity for further division”.
Pate1 (1978) favoured the term ‘residual protoderm cell’ for all cells outside the
meristematic region with ability to divide (the cells leading to stornatal formation
were termed ‘S-residual protoderm cells’). In this category were included
protodermal cells adjacent to the guard-cell mother-cell, which may in some cases
divide unequally to form perigene cells.
Recently, Payne (1979) suggested that the term meristemoid should be applied
as by Pant (1965) to the protodermal cell that by divisions leads to guard cell
formation. This application refers to the cell generation immediately preceding
that for which Fryns-Claessens & Van Cotthem (1973) used the term (Fig. 2).
13
TERMINOLOGY OF STOMATAL DEVELOPMENT
207
leads to guard cell formation, the other daughter cell being treated as an ordinary
protodermal cell. Tomlinson (1974) and Stevens & Martin (1978) agreed with this
view.
Payne (1979) also agreed with Fryns-Claessens & Van Cotthem (1973) in
assuming that an unequal division defines the start of stomatal development
without exceptions. However, since he defined the meristemoid as the protodermal
cell which is going to divide unequally, there would in his opinion always be at
least one cell besides the guard cells derived from the meristemoid and the
perigenous type of development would then never occur (Fig. 3 ) . Payne supported
his use of the term meristemoid in this sense by stating that “. . . any protodermal
cell that divides otherwise [not equally] is already committed to a particular
developmental pathway. Indeed, it seems obvious that a cell that divides
unequally with walls of unusual configuration or orientation and with derivative
cells that contain cytoplasmic allotments that exhibit differential staining, is a
specialized cell”.
It is possible, that the unequally dividing protodermal cells are specialized long
before that crucial division takes place, but this has not been demonstrated by any
difference in their structure as seen in light or electron microscopy (Galatis &
Mitrakos, 1979). O n the other hand, the results of Bunning & Sagromsky (1948)
show that external factors can increase the density of stomata during development,
so it may well be that every protodermal cell is capable of dividing unequally.
External factors and interaction between adjacent cells may then be supposed to
determine how many of them are recruited to this particular developmental
pathway. Summarizing the present evidence concerning this question, Sachs
(1978 : 70) concluded: “These facts do not indicate the presence of any pattern of
signal distribution which precedes the differentiation of the stomata”. If this
hypothesis is correct there is no theoretical reason for distinguishing such
protodermal cells from others before the unequal division is initiated. This
distinction is not justified on practical grounds either. \.Vhen a cell divides, it is
replaced by its two daughter cells. If a certain kind of cell is distinguished only on
the basis of the daughter cells it may produce, it is impossible to identify before it is
about to end its existence as a cell. These considerations also serve as a n argument
against the use of the term ‘subsidiary meristemoid’ coined by Stevens & Martin
(1978) for the protodermal cells adjacent to the guard-cell mother-cell which are
going to divide to form perigene cells, and against any other special designation of
these cells as, for example Patel (1978), mentioned above (see Fig. 2).
The meristemoid, as defined by Fryns-Claessens & Van Cotthem (1973) is
certainly committed to a particular developmental pathway. Such meristemoids
can be identified by their origin and position and must be supposed to have
important features in common in different plant groups. Hence, they constitute a
convenient starting point for any description of stomatal development in which the
unequal division of a protodermal cell is involved.
The sister cell of the meristemoid can be regarded as the same as any
surrounding protodermal cell. No inconsistency arises since it behaves exactly like
other protodermal cells during the maturation of the stomatal complex. The fact
that this sister cell may undergo an unequal division and give rise to another
meristemoid indicates that its potentiality compared with other protodermal cells
is unaltered as in Trochodendron (Bondeson, 1952), Vigna (Galatis & Mitrakos,
1979), and some Orchidaceae (H. Rasmussen, unpublished data).
208
H. RASMUSSEN
The surrounding cells
In morphological studies of the mature epidermis, the cells surrounding the
stoma at maturity are traditionally referred to as subsidiary cells if structurally
modified (Metcalfe & Chalk, 1950) and as neighbouring cells if not differing
markedly from the rest of the epidermal cells (Pant, 1965; Fryns-Claessens & Van
Cotthem, 1973).
In the ontogenetic studies by Florin (1933), the surrounding cells are
distinguished by their derivation (Fig. 2). Florin’s German terms are here cited
unchanged. A “mesogene Yebenzelle” is produced by a division of the
“Urmut terzelle” prior to its division into guard cells. “perigene Nebenzellen” are
protodermal cells surrounding the guard-cell mother-cell or comprise the proximal
products of divisions of such cells, in which case the distal products are termed
“perigene Kranzzellen”. If surrounded by one or more mesogene cells the stornatal
complex is ‘syndetocheilic’, otherwise it is ‘haplocheilic’. This terminology was
modified by Pant ( 1965). The mesogene and perigene cells correspond to those of
Florin, but the stornatal complex is described as ‘mesogenous’, when wholly
surrounded by mesogene cells, ‘perigenous’, when all surrounding cells are
perigene, and ‘mesoperigenous’ if cells of both origins surround the stoma.
Following Pant (1965) the monocotyledons to which he refers would possess at
least one mesogene cell because of the initiating unequal division, and thus be
mesoperigenous. However, they were placed in the perigenous category
apparently neglecting the first mesogene cell produced by the meristemoid (Figs 2,
3).
A similar terminology was adopted by Fryns-Claessens & Van Cotthem (1973),
but, with their definition of the meristemoid, the surrounding cells of these
monocotyledons were all truly perigene. It was implied both by Pant (1965) and
by Fryns-Claessens & Van Cotthem (1973) that at maturity both kinds of
surrounding cells could either be indistinguishable from other epidermal cells, in
which case they comprise ‘neighbouring cells’, or be structurally distinct from the
other epidermal cells, comprising ‘subsidiary cells’.
Tomlinson (1974) also restricted the term ‘subsidiary cells’ for cells in mature
stornatal complexes in morphological description. Neighbouring cells in his sense,
are cells adjacent to the meristemoid when it is initiated (Fig. 2). This means that a
neighbouring cell defined this way may differentiate into a subsidiary cell later on.
Neighbouring cells can divide, producing derivatives of which some will border the
future guard cells, the ‘contact cells’. Neighbouring and contact cells equal the
perigene cells of Pant (1965) and Fryns-Claessens & Van Cotthem (1973). This
terminology was coined with special reference to monocotyledons and did not
contain a term for mesogene cells, which had then only just been described for the
first time in monocotyledons in two orchids (LVilliams, 1975, cited as “in
preparation” in Tomlinson, 1974). As mesogene cells have since been shown to
occur quite normally in certain orchid groups (Williams, 1979; Rasmussen, 1981)
and in other monocotyledon families as well (Howard, 1980; Rasmussen,
unpublished data) monocotyledon stomata seem to be more similar to those of
dicotyledons than could previously be assumed, and so a similar terminology must
be preferred.
Pate1 (1978) followed the definitions of Tomlinson (1974) with respect to
surrounding cells, but taking into account examples with mesogene as well as
t
TERMINOLOGY OF STOMATAL DEVELOPMENT
209
perigene cells. The possibility of distinguishing the two categories of cells was
questioned, as both were originally derived from protodermal cells. However, even
the illustrations (Patel, 1978, Figs 1, 2, 3, respectively) demonstrate that such a
distinction is in fact possible (although the theoretical significance of this
distinction is still to be determined).
Paliwal (1969) proposed the terms ‘Sahodar Sah Koshika’ and ‘Sah Koshika’
derived from Sanskrit, referring to the mesogene and perigene cells of Pant ( 1965),
respectively. These terms as well as other Sanskrit terms designating stomatal
complexes have not gained international recognition because they covered
concepts for which other terms were already in use and probably also because this
ancient language is unfamiliar to most people.
Stevens & Martin (1978) elaborated the terminology of Pant (1965) and FrynsClaessens & Van Cotthem (1973) for the surrounding cells during development,
but combined these terms with terms previously used in morphological
descriptions. Their definitions follow. ‘Subsidiary cells’ are “related
ontogenetically to their associated guard cells and are derived de novo from either
the stomatal meristemoid or protodermal cells adjacent to the stomatal
meristemoids and, at maturity, are generally morphologically distinct from other
epidermal cells”. In consequence, the mesogene cells of Pant ( 1965) were termed
‘mesogene subsidiary cells’ (Fig. 2), while the ‘perigene subsidiary cells’ were
defined as derived by division of surrounding protodermal cells.‘Neighbouring
cells’ are “protodermal cells” which represent “direct products of the leaf
meristem, which lie immediately adjacent to a stomatal meristemoid and which
mature in this position without undergoing any cell divisions so that, at maturity,
they are morphologically indistinguishable from other epidermal cells except for
their contact with the guard cell complex”. Neighbouring cells in this sense
comprise the surrounding cells not dividing during stomatal development, and
together with the perigene subsidiary cells they correspond to the perigene cell
concept as defined by Pant (1965).
In an ontogenetic classification which is intended to express the pattern of cell
divisions, it is appropriate to make a distinction between the surrounding cells
which are derived by divisions of protodermal cells and those which are not.
However, the fact that in Stevens & Martin (1978) definitions are on both
ontogenetic and morphological criteria presents a theoretical as well as a practical
problem. Mesogene and perigene cells not structurally modified at maturity do
exist and epidermal cells adjacent to the guard cells may be structurally modified
compared with other epidermal cells. In such cases the two requirements of the
definitions quoted above are not fulfilled at the same time, and the cells are not
possible to classify. The problem is easily overcome if the definitions are restricted
to the ontogenetic criteria, and if the terms subsidiary and neighbouring cells are
reinstated in their previous, morphological sense (Pant, 1965 ; Fryns-Claessens &
Van Cotthem, 1973). The neighbouring cells as defined by Stevens & Martin
could, by analogy with their terminology for stomatal complexes, be called ‘agene
cells’, a new term which is proposed in this paper. I define the perigene cell as any
daughter cell ofa divided cell adjacent to the guard-cell mother-cell. The definition
refers to divisions occurring only in relation to the developing stoma and not to
those related to general activity of the leaf meristem.
Many authors-without
stating this precisely-have not included, in the
category of perigene cells, the distal product of a division parallel to the guard-cell
210
H. RASMUSSEN
mother-cell. For instance, the stomata of grasses are often described as having two
perigene cells (Fryns-Claessens & Van Cotthem, 1973) while as specified here they
have four. T h e distal perigene cells were called by Florin ‘perigene Kranzzellen’
(see Fig. 2) and they are also commonly designated as ‘encircling cells’. However,
when the surrounding cell has divided at right angles or obliquely to the side of the
guard-cell mother-cell, it would not be obvious which daughter cell is the perigene
cell when using the term in this more restricted sense.
In summary, on the basis of their ontogeny the three kinds of cells that may
surround the stoma by the end of development are: AGENE CELLS, PERIGENE CELLS
and MESOGENECELLS. They may be indistinguishable from ordinary epidermal cells
at maturity and are then referred to as NEIGHBOURING CELLS, or they may be
morphologically distinct and then constitute SUBSIDIARY CELLS.
Stevens & Martin (1978) coined seven terms to denote the whole stomatal
complex according to the derivation of the surrounding cells. These terms
encompass every possible combination of the three kinds of surrounding cells
mentioned above, and hence are universal. They are accepted here, see Fig. 1.
The stoma
When a mesogene cell is produced from a meristemoid, this always happens by
an unequal division. One daughter cell, usually the larger, is the mesogene cell,
while the smaller daughter cell takes over the meristemoid function. The process
may be repeated several times, in each case a mesogene cell and a new meristemoid
of increasing order being produced. The last division of the meristemoid is equal
and results in the two guard cells. The meristemoid can usually be recognized by
its shape prior to this division and can then be distinguished as the guard-cell
moth er-cell.
The guard cells and the pore between them constitute the ‘stoma’. This is the
generally accepted usage ofthis term (Metcalfe & Chalk, 1950: xiv; Van Cotthem,
1970 : 235; Wilkinson, 1979 : 97). The stomatal complex in a morphological
context consists of the stoma and its neighbouring and subsidiary cells, whatever
the origin of these cells. In an ontogenetic context the stomatal complex is the
stoma surrounded by ontogenetically related (mesogene and perigene) cells and by
undivided protodermal (agene) cells. It should be emphasized that the stomatal
complex may not comprise exactly the same group of cells in the two contexts, but
the approach chosen in each case will appear from the descriptive terms attached,
namely, a ‘hemiperigenous stomatal complex’ versus an ‘anomocytic stomatal
complex’.
The stomatal complex is commonly referred to simply as the stoma, for example,
papers describing stomatal development in fact usually deal with the development
of stomatal complexes. This inaccuracy is of established usage and, as noted by
Pant ( 1965), rarely the cause of any misunderstanding. The exact meaning should
be specified by the available terms in the cases where doubt could arise.
The division of the guard-cell mother-cell which determines the position of the
stomatal pore may be classified according to the angle of the partitioning wall
relative to that of the immediately preceding cell division. Pant (1965) introduced
the terms Tetracentron-type, Plagiogyria-type and Ranunculus-type referring to an
angle of 0”, 90” and any other, respectively. This terminology was improved by
TERMINOLOGY O F STOMATAL DEVELOPMENT
21 1
Payne ( 1979) who proposed the more informative terms parameristic, diameristic
and anomomeristic, respectively.
Reservations
There are limits to how much information it is feasible for a system of
terminology to contain. A gain in the level of information may easily lead to a loss
in utility. The ontogenetic terminology system recommended here does not
describe the number, form and position of the cells forming part of the stomatal
complex. Some of this information may be found in the morphological
terminology. A full description of stomatal development should also account for
the mature condition.
The system of terminology outlined here is based on the widely occurring
unequal division of a protodermal cell as a starting point, as in Fryns-Claessens &
Van Cotthem (1973) and Stevens & Martin (1978). It does not take into account
the old records from mosses and gymnosperms of a stomatal development devoid of
any unequal division. It should be possible to coin terms for this special kind of
development, if it proves necessary, without fundamental changes in the
terminology .
ACKNOWLEDGEMENTS
I am gratefiil to L. Bolt Jsrgensen and R. Dahlgren, Copenhagen, and to D. F.
Cutler and M. Gregory, Kew, amongst others for their valuable suggestions to
improvements of the manuscript.
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