Int. J. Plant Sci. 160(6 Suppl.):S67–S80. 1999.

䉷 1999 by The University of Chicago. All rights reserved.

1058-5893/1999/16006S-0006$03.00

ANISOPHYLLY AND DORSIVENTRAL SHOOT SYMMETRY

Nancy G. Dengler1
Department of Botany, University of Toronto, Toronto, Ontario M5S 1A1, Canada

Anisophylly is a special case of shoot dorsiventral symmetry in which leaf size and form differ between
dorsal and ventral sides of the shoot. Anisophylly is normally coupled with leaf and stem asymmetry, modified
phyllotaxis, and anisoclady. Anisophylly may be expressed throughout the shoot system (habitual anisophylly)
or restricted to lateral shoots (lateral anisophylly). The combination of anisophylly, shoot dorsiventrality, and
plagiotropy has arisen numerous times during evolution of the land plants, most notably in the primarily
tropical families of Acanthaceae, Gesneriaceae, Melastomataceae, and Urticaceae. It is thought to represent
an adaptation that maximizes light capture in dimly lit understories. In species for which anisophylly is an
intrinsic expression of overall shoot symmetry, anisophylly and associated features of shoot dorsiventrality
are expressed early in development. In contrast, when expression of anisophylly depends on growth conditions,
anisophylly is secondarily imposed on early isophyllous leaf development. Despite more than a century of
experimentation, very little is understood about the physiological control of anisophylly and dorsiventrality.
Development of these features requires regulated suppression of some parts of the shoot and stimulation of
others. Shifts in the temporal and spatial patterns of growth suppression and enhancement occur during both
the ontogeny of an individual and during evolutionary change. Elucidating these processes for anisophyllous
shoot development also should have broader significance for understanding the evolution of other morpho-
logical innovations.

Keywords: anisophylly, dorsiventral shoot symmetry, leaf asymmetry, leaf development, phyllotaxis, anisoclady,
vegetative shoots.

Introduction shoot development is unclear. Growth hormones have been

Anisophylly is a special case of dorsiventral shoot transec-
tional symmetry in which leaves inserted on the dorsal and
ventral sides of the stem differ in size and shape. Anisophylly
is usually correlated with leaf asymmetry, modified phyllotaxis,
stem asymmetry, and the differential development of dorsal
and ventral axillary buds (anisoclady). Although anisophylly
coupled with extreme shoot dorsiventrality has been noted in
the botanical literature for well over a century, very little is
understood about this phenomenon, and significant questions
about its ecology, evolution, and development remain unan-
swered. Anisophylly has a broad systematic distribution within
the angiosperms (Figdor 1909; Troll 1937; Dengler 1992), a
pattern that implies multiple independent origins, but no one
has yet tested this specific hypothesis in a phylogenetic analysis.
From the earliest documentation of anisophylly, it has been
thought to be an adaption to dimly lit understory environments
(e.g., Goebel 1928; Givnish 1984), yet there are no ecological
studies dealing with anisophylly per se. The developmental
regulation of anisophylly and shoot dorsiventrality requires
that growth on either the dorsal or ventral side of the stem be
suppressed while the opposite side is enhanced. Despite a long
history of experimentation with the directionality of light and
gravity (e.g., Frank 1868; Kny 1873; Goebel 1928; Figdor
1909), the effect of environmental factors on anisophyllous
1
E-mail dengler@botany.utoronto.ca.
Manuscript received May 1999; revised manuscript received July 1999.
thought to play a role regulating anisophylly (e.g., Guttenberg
and Steinweg 1956; Guttenberg and Müller 1957), but there
are no contemporary studies taking advantage of current meth-
odologies and perspectives.
This article provides an overview of shoot dorsiventral sym-
metry in combination with anisophylly, including aspects of
leaf symmetry, phyllotaxis, and anisoclady. We attempt to iden-
tify what is already known about this highly integrated com-
plex of characteristics and where future research directions
might lie. Examples of some of the common variants of an-
isophylly are described, as are developmental aspects of an-
isophylly and shoot dorsiventrality in four model species. An-
isophylly and dorsiventrality develop through the enhance-
ment of growth in one part of the shoot and suppression in
another. Implications of physical constraints and environmen-
tal cues and of hormonal and microsurgical experiments for
understanding the regulation of this developmental pattern are
discussed. Since shifts in the temporal and spatial patterns of
growth enhancement and suppression have been important
agents of evolutionary change (Basile and Basile 1993; Tsukaya
1997), understanding the developmental regulation of an-
isophylly and dorsiventrality may also have broader implica-
tions for understanding the mechanisms behind other evolu-
tionary changes in organ size and symmetry.
Transectional Symmetry of the Shoot
Shoots display one of three types of transectional symmetry:
(1) radial symmetry, (2) bilateral symmetry, and (3) dorsiven-

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S68 INTERNATIONAL JOURNAL OF PLANT SCIENCES

tral symmetry (fig. 1; Goebel 1928; Troll 1937; D. R. Kaplan,
unpublished manuscript). In radial shoots, the shoot system is
round in cross section and an infinite number of radii that
divide the shoot into equal halves can be drawn through its
center (fig. 1A). In bilateral shoots, the axis is flattened and
only two planes of symmetry pass through its center (fig. 1B).
In the most common form of bilateral symmetry, the transverse
plane is parallel to the plane of flattening and divides the shoot
into equal upper and lower halves. The median plane is at
right angles to the transverse plane and divides the shoot into
equal left and right sides. In dorsiventral shoots, the upper and
lower halves separated by the transverse plane are of unequal
size: when the upper (dorsal) half is larger, the shoot is epitonic;
when the lower (ventral) half is larger, the shoot is hypotonic
(fig. 1C). The median plane divides dorsiventral shoots into
equal right and left halves.
Leaf size, form, and placement are the most conspicuous
elements of shoot symmetry. The shape of the shoot apical
meristem often reflects the pattern of leaf arrangement, so that
shoot symmetry is recognizable within the apex. In some spe-
cies, secondary modification of stem cross-sectional shape and/
or torsional growth of internodes and petioles result in a new
symmetrical pattern that is superimposed on the first. Radial
shoots typically have round stems, helical or whorled phyl-
lotaxis, and symmetrical leaves (fig. 2A). Bilateral shoots typ-
ically have flattened stems, and phyllotaxis is either distichous,
with leaves borne in the transverse plane (fig. 2B), or opposite
decussate, with leaf pairs borne alternately in planes separated
by 90⬚ (fig. 2C, 2D). Opposite-decussate phyllotaxis may be
orthogonal, with leaves initiated successively in the transverse
and median planes (fig. 2C). In this case, size differences be-
tween leaves in transverse and median planes may occur, but
leaves are usually symmetrical. In diagonal decussate phyllo-
taxis, leaf pairs are initiated at 90⬚ from the previous pair but
at ca. 45⬚ from the transverse and median planes; leaves are
typically asymmetrical (fig. 2D).
In dorsiventral shoots, stems are either epitonic or hypotonic
as a result of differential primary thickening or secondary
growth (fig. 2E–2I). In some species, this is accentuated by the
formation of adventitious roots on the ventral side of the stem
and the displacement of leaves toward the dorsal side (fig. 3A;
Goebel 1928; Troll 1937; D. R. Kaplan, unpublished manu-
script). Phyllotaxis in dorsiventral shoots is typically distichous
(fig. 2E; fig. 3A, 3B), orthogonal decussate (fig. 2F; fig. 3C,
3F), or diagonal decussate (fig. 2G–2I; fig. 3H, 3I). For in-
stance, lateral shoots of Coffea arabica have an orthogonal-
decussate pattern of leaf initiation but both internode torsion
and petiole angle reorient leaves, resulting in dorsiventral shoot
symmetry (fig. 3C). Acer saccharum also has orthogonal phyl-
lotaxis; leaves borne on the dorsal and ventral sides of lateral
shoots retain their original positions but differ in size, giving
dorsiventral symmetry (figs. 2F, 3F). Dorsiventral shoots can
have striking leaf asymmetry: leaves are either epitonic, with
the largest lamina half oriented toward the dorsal side of the
shoot (e.g., fig. 2E), or hypotonic, with the largest lamina half
oriented toward the ventral side (e.g., fig. 2F, 2G). Dorsiventral
shoots with distichous or diagonal decussate symmetry com-
bine alternating leaf placement and alternating leaf symmetry,
a pattern referred to as pendulum symmetry (Charlton 1998).
Ficus pumila illustrates pendulum symmetry: the shoot has
mirror-image symmetry around the median plane, as leaves are
alternately right and left handed (fig. 3B). Leaves are epitonic,
but petiole torsion brings leaf blades into the transverse plane.
The asymmetric leaf bases fit neatly together, forming an al-
most continuous photosynthetic surface.
Shoot symmetry may vary within the same individual. In
species with an erect growth habit, the main axis is typically
orthotropic (having vertical orientation) and has radial sym-
metry, while lateral axes are plagiotropic (having horizontal
orientation) and have bilateral or, more often, dorsiventral
symmetry (e.g., fig. 3C, 3E–3G). In Populus deltoides (fig. 3E)
and in A. saccharum (fig. 3F), orthotropic main shoots have
radial symmetry, while lateral shoots have weakly expressed
dorsiventrality through reduced leaf size on the dorsal side of

Fig. 1 Shoot transectional symmetry. A, Radial symmetry; B, bilateral symmetry; C, dorsiventral symmetry showing differential growth on
dorsal and ventral sides of the shoot, giving either basitonic or hypotonic symmetry.

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 DENGLER—ANISOPHYLLY AND DORSIVENTRAL SHOOT SYMMETRY
Fig. 2 Phyllotaxis and leaf symmetry in shoots with radial, bilat-
eral, and dorsiventral transectional symmetry. Leaves are numbered
from youngest to oldest. A, Radial shoot with helical phyllotaxis and
symmetrical leaves. B–D, Bilateral shoots. B, Distichous phyllotaxis
and symmetrical leaves. C, Orthogonal decussate phyllotaxis and sym-
metrical leaves. D, Diagonal decussate phyllotaxis and asymmetrical
leaves. E–I, Dorsiventral symmetry. E, Distichous phyllotaxis and ep-
itonic asymmetric leaves. F–I, Dorsiventral symmetry coupled with
anisophylly. F, Orthogonal decussate phyllotaxis. Leaves borne in
transverse plane have basitonic asymmetry. G–I, Diagonal decussate
phyllotaxis showing different patterns of leaf symmetry. G, “Selagi-
nella-type” leaf symmetry with both dorsal and ventral leaves hypo-
tonic. H, “Strobilanthes (=Goldfussia)-type” leaf symmetry with both
dorsal and ventral leaves epitonic. I, “Pellionia-type” leaf symmetry
with hypotonic dorsal leaves and epitonic ventral leaves.
the shoot. In Anisophyllea disticha, orthotropic shoots are ra-
dial, with helical phyllotaxis, but plagiotropic lateral shoots
are strongly dorsiventral and have tetrastichous phyllotaxis
(fig. 3G; see “Phyllotaxis,” below).
Syndrome of Anisophylly
Leaf Size and Form
Anisophylly is a special case of dorsiventral shoot symmetry
in which leaves on the dorsal and ventral sides of the stem
differ in size and/or shape. Anisophyllous shoots are typically
hypotonic, so that larger leaves are borne on the ventral side
and smaller leaves on the dorsal side of the stem (fig. 3D–3I;
fig. 4; fig. 5A; fig. 6A; fig. 7A; fig. 8A). For instance, although
shoots of Tsuga canadensis have helical phyllotaxis and initial
radial symmetry, leaves on the dorsal side of the shoot are
shorter and retain an abaxial-side-up orientation, in contrast
to the longer leaves borne in other parastichies that undergo
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S69
torsional growth so that they come to lie (mostly) adaxial-side
up in the transverse plane (fig. 3D). Populus deltoides also has
helical phyllotaxis, but leaves in the dorsalmost parastichy of
lateral shoots are smaller than those borne in other parastichies
(fig. 3E). In the orthogonal decussate lateral shoots of Acer
saccharum, leaf pairs in the median plane have a small dorsal
and a larger ventral leaf, while leaf pairs in the transverse pair
are intermediate in size and leaves tend to express hypotonic
symmetry (figs. 2F, 3F). In anisophyllous shoots with diagonal
decussate phyllotaxis such as Columnea species, leaves borne
in the two dorsal ranks are small and those in ventral ranks
larger (figs. 3H, 8A). In some extremely anisophyllous shoots,
such as the lateral branches of Anisophyllea disticha (figs. 3G,
5A; Dengler et al. 1989) and plagiotropic shoots of Pellionia
species, dorsal leaves are reduced to scales (fig. 3I; fig. 7A–7C;
Troll 1937; Magin 1982; Mueller and Dengler 1984). In a few
anisophyllous species such as Lycopodium complanatum, ven-
tral leaves are smaller than those of other ranks (Troll 1937).
The aquatic fern genus Salvinia displays an unusual form
of anisophylly (Croxdale 1978; Lemon and Posluszny 1997):
leaves are produced in whorls of three, each whorl with two
simple floating leaves toward the dorsal side of the floating
stem and one much branched submerged leaf inserted toward
the ventral surface of the stem. Successive leaf sets show mirror
symmetry, and the pattern of initiation is an expression of
complex pendulum symmetry (Charlton 1998).
Leaf Symmetry
Anisophylly is usually coupled with modified leaf symmetry.
Leaf asymmetry occurs in leaves borne in the transverse plane
in opposite-decussate shoots of A. saccharum (fig. 2F) and in
leaves borne in parastichies adjacent to the dorsal side of lateral
shoots in P. deltoides (Larson and Richards 1981). In these
examples, leaf asymmetry is subtle, but in some other species
it is very strongly expressed. For example, three different pat-
terns of leaf symmetry have been recognized in anisophyllous
shoots with diagonal decussate phyllotaxis (Goebel 1928; Troll
1937; Magin 1982; Charlton 1998). In the “Selaginella type,”
the broad half of the lamina is oriented toward the ventral
side of the shoot for both dorsal and ventral leaves so that
both leaves and stem are hypotonic (fig. 2G; fig. 6A, 6C). In
the “Stobilanthes (=Goldfussia) type,” leaf and stem symmetry
are uncoupled: leaves are epitonic, while the stem is hypotonic
(fig. 2H). In the “Pellionia type,” leaves of a pair have opposing
symmetries: the dorsal leaf is hypotonic, while the ventral leaf
is epitonic (fig. 2I; Magin 1982; Charlton 1998).
Phyllotaxis
Anisophylly is associated with a range of phyllotactic pat-
terns. Shoots with helical phyllotaxis and equal-sized leaf pri-
mordia may become secondarily anisophyllous by differential
growth of leaves in different positions around the axis. This
pattern is prominent in conifers such as T. canadensis, where
leaves borne in parastichies on the dorsal side of the stem
undergo reduced expansion (fig. 3D; Hallé et al. 1978). An-
isophylly develops in a few species with orthogonal-decussate
phyllotaxis, such as A. saccharum (figs. 2F, 3F), but a diagonal
decussate pattern of leaf placement is more common. Leaf pairs
are initiated at 90⬚, and growth of the dorsal member of each
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Fig. 3 Examples of shoot dorsiventrality and anisophylly. A, Dorsiventral rhizome of Iris sp. with distichous phyllotaxis. B, Dorsiventral
plagiotropic shoot of Ficus pumila with distichous phyllotaxis. C, Dorsiventral plagiotropic shoot of Coffea arabica with orthogonal decussate
phyllotaxis. D, Anisophylly and helical phyllotaxis in Tsuga canadensis. Arrows, small dorsal leaves. E, Anisophylly and helical phyllotaxis in
lateral shoot of Populus deltoides. Arrow, small dorsal leaf. F, Anisophylly and orthogonal decussate phyllotaxis in lateral shoot of Acer saccharum.
Arrows, small dorsal and large ventral leaf of a pair. G, Orthotropic isophyllous main shoot and plagiotropic anisophyllous lateral shoots of
Anisophyllea disticha. H, Ventral view of habitually anisophyllous shoot of Columnea sanguinea showing anthocyanin patches on abaxial side
of ventral leaves. Arrow, flower in ventral leaf axil. J, Dorsal view of habitually anisophyllous shoot of Pellionia pulchra. Arrow, scalelike dorsal
leaf (much smaller than visible stipule).

pair is suppressed, forming a four-ranked phyllotaxis with
small leaves in two dorsal ranks (fig. 2G–2I; figs. 5–8). In
some diagonal decussate species such as Selaginella martensii,
dorsal and ventral leaves appear to be initiated simultaneously
but become displaced from a common node during stem ex-
tension (fig. 6). In A. disticha, dorsal and ventral leaves appear
to be initiated sequentially, with more conspicuous internode
extension between them, a pattern described as tetrastichous
(Vincent and Tomlinson 1983; Dengler et al. 1989).
In some cases, the initial phyllotactic pattern becomes de-
velopmentally modified. In Columnea orientandina, leaves are
initiated in opposite pairs, with successive pairs at 90⬚. With
hypotonic shoot growth, leaves are displaced toward the dorsal
side of the stem, so that divergence angles between ventral
orthostichies increase, while those between dorsal orthostichies
decrease (fig. 4A; Sanchez-Burgos and Dengler 1988). In Pel-
lionia repens, hypotonic and torsional growth of stem inter-
nodes brings both dorsal orthostichies into the median plane,
while ventral orthostichies come to lie in the transverse plane
(fig. 4B; Magin 1982). In the plagiotropic lateral shoots of A.
disticha, dorsal and ventral ranks of leaves are displaced to-
ward the transverse plane, resulting in angles of divergence

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 DENGLER—ANISOPHYLLY AND DORSIVENTRAL SHOOT SYMMETRY
Fig. 4 Modified phyllotaxis in anisophyllous dorsiventral shoots.
A, Diagonal decussate phyllotaxis in anisophyllous shoots of Col-
umnea orientandina (Gesneriaceae). B, Diagonal decussate phyllotaxis
in anisophyllous shoots of Pellionia repens. Phyllotaxis becomes
strongly modified with shoot development so that dorsal leaves come
to lie in the median plane and ventral leaves in the transverse plane
(from Magin 1982). C, Tetrastichous phyllotaxis of lateral shoots of
Anisophyllea disticha. Leaves are initiated in sequence D1, V2, D3,
V4. Angles between orthostichies are either greater than or less than
90⬚.
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S71
190⬚ on the dorsal and ventral sides of the shoot and angles
!90⬚ toward the edges of the flattened shoot (figs. 4C, 5C;
Vincent and Tomlinson 1983; Dengler et al. 1989).
Goebel (1928) suggested that anisophylly might represent
an intermediate step in a developmental transition from radial
symmetry and decussate phyllotaxis to dorsiventral symmetry
and distichous phyllotaxis, such as occurs in seedlings of Ul-
mus effusa. He interpreted a single scale leaf followed by a
foliage leaf as representing a staggered anisophyllous pair
(Goebel 1928). More recent observations of the seedling of
Ulmus glabra indicate that the several scale leaves in this spe-
cies are truly bud scales, which may or may not be associated
with dormancy, and that the shift from decussate to distichous
phyllotaxis occurs without a transitory anisophyllous phase
(Charlton 1993a).
Anisoclady
Anisophylly is often correlated with differential development
of axillary buds (anisoclady). Two types of anisoclady occur:
helicoidal anisoclady, in which the preferred (larger) buds oc-
cur along a single foliar helix, and sectorial anisoclady, in
which the preferred buds occupy a sector of the shoot (Troll
1937; Carr 1984). Theligonum cynocrambe (Rubiaceae) dis-
plays a very unusual pattern in which both anisophylly and
anisoclady are expressed in a helicoidal pattern (Rutishauser
et al. 1998). However, in most anisophyllous species, shoots
display sectorial anisoclady. Typically, the preferred buds are
in axils of ventral leaves, and in some species with strongly
developed anisophylly, such as Pellionia daveauana and A.
disticha, buds are absent in axils of the scalelike dorsal leaves
(Magin 1982; Dengler and Donnelly 1987; Dengler et al.
1989). In Goldfussia glomerata, buds are present in both dor-
sal and ventral leaf axils but the preferred buds are associated
with dorsal leaves (Troll 1937; Charlton 1998). In species of
Columnea and other anisophyllous taxa of the Gesneriaceae,
axillary buds associated with ventral leaves are reproductive,
while those in the axils of smaller dorsal leaves are vegetative
(fig. 3H; Wiehler 1977; Sanchez-Burgos and Dengler 1988).
In this group of species, anisoclady is associated with polli-
nation by hummingbirds that hover beneath the shoot to feed
on the flowers borne in axils of the ventral leaves (Morley
1973; Wiehler 1977). The red anthocyanin patches on the
abaxial surface of the ventral leaves serve as a visual attractant
for these pollinators (fig. 3H).
Distribution of Anisophylly on the Plant
Goebel (1928) recognized two broad categories of an-
isophylly, based on distribution within the plant body: habit-
ual, where anisophylly is expressed throughout the adult shoot
system, and lateral, where anisophylly is restricted to plagio-
tropic lateral branches. Plants with habitual anisophylly have
a creeping or climbing growth habit, as in Selaginella martensii
or Pellionia daveauana (figs. 6A, 7A; Goebel 1928; Troll 1937;
Dengler 1983a; Mueller and Dengler 1984). Seedlings usually
are orthotropous and isophyllous, and the transition to pla-
giotropy and anisophylly occurs simultaneously with the
switch from juvenile to adult growth (Troll 1937). Habitual
anisophylly is often regarded as being constitutive in expres-
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Fig. 5 Dorsiventrality and anisophylly in lateral shoots of Anisophyllea disticha (Anisophylleaceae). A, Dorsal view of lateral shoot showing
asymmetric dorsal (D) and ventral (V) leaves. Scale bar = 2 cm. B, Scanning electron micrograph of apical view of lateral shoot apex. Phyllotaxis
is tetrastichous, and leaves are numbered in order of initiation (V2, D3, V4, D5). Scale bar = 50 mm. C, Cross section of shoot apex of plagiotropic
shoot showing early divergence in histology of dorsal (D) and ventral (V) leaves. Scale bar = 50 mm (from Dengler 1992).

sion and unaffected by experimental manipulation of light or
shoot orientation (Goebel 1928).
Habitual anisophylly can be sufficiently stable to be used as
a taxonomic character, as in Selaginella sect. Heterophyllum
(Hieronymus 1902). In some other taxa, however, expression
of habitual anisophylly appears to be facultative and varies in
response to changes in environmental factors. For instance,
Morley (1973, 1974) reported that Columnea species, partic-
ularly those with large leaves from shaded habitats, show con-
siderable plasticity in growth habit and degree of anisophylly,
apparently related to shoot orientation in relation to light
source. Wiehler (1978, 1983) also reported that the nodes of
a single shoot varied from isophylly to extreme anisophylly in
a group of Paradrymonia species, depending on crowding by
adjacent leaves under field conditions. In a recent treatment
of Columnea, Smith and Sytsma (1994) concluded that, while
the section Collandra is defined by the presence of an-
isophyllous leaves, the character of anisophylly should be ex-
cluded from a cladistic analysis of the genus as a whole. An-
isophylly occurs in three of six sections of Columnea and in
numerous other genera of the Gesneriaceae, a complex pattern
that makes it difficult to determine homologies (Smith and
Sytsma 1994).
Lateral anisophylly characterizes species with orthotropic,
isophyllous main axes and plagiotropic, anisophyllous lateral
branches. Lateral anisophylly has been reported in many
woody genera with helical phyllotaxis, such as Malus and Po-
pulus (fig. 3E; Schander 1958; Borsdorf 1966; Larson and
Richards 1981), or with decussate leaf arrangement such as
Acer, Aesculus, and Syringa (Goebel 1928; Troll 1937; Dostal
1967; D. R. Kaplan, unpublished manuscript). Lateral an-
isophylly has also been described in herbaceous genera such
as Coleus, Scrophularia, and Urtica (Goebel 1928). As with
habitual anisophylly, lateral anisophylly may be invariant in

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 DENGLER—ANISOPHYLLY AND DORSIVENTRAL SHOOT SYMMETRY S73

Fig. 6 Dorsiventrality and anisophylly in the habitually anisophyllous shoots of Selaginella martensii. A, Dorsal view of shoot showing
asymmetric dorsal (D) and ventral (V) leaves. Scale bar = 1 mm. B, Scanning electron micrograph of apical view of shoot apical meristem
showing early expression of size differences between dorsal (D1, D2) and ventral (V1, V2) leaves. Scale bar = 50 mm. C, Cross section of shoot
apex showing diagonal decussate phyllotaxis with two ranks of dorsal leaves (D1, D2, D3, D4) and two ranks of ventral leaves (V1, V2, V3,
V4). Scale bar = 50 mm (from Dengler 1992).

expression, as in Anisophyllea, or it may be facultative and
under the influence of correlative interactions with other
shoots. In a number of species, decapitation of the main or-
thotropic shoot results in reorientation of plagiotropic shoots
and loss of anisophylly, indicating that lateral anisophylly can
be fully reversible (Goebel 1928; Sinnott and Durham 1923;
White 1957; Richards and Larson 1981). Species with lateral
anisophylly may also vary in the longitudinal extent of an-
isophyllous expression: for instance, anisophylly is expressed
over the first 21 lateral branch nodes in Populus deltoides
(Larson and Richards 1981). Larson and Richards (1981)
showed that anisophylly is linked to the pattern of vascular
connections with the main shoot (see “Intrinsic Factors,” be-
low). This effect is eventually superseded by secondary growth,
however, and lateral shoots become secondarily isophyllous.
In some species, anisophylly is restricted to portions of the
adult shoot system. Shoots of Sanchezia are decussate: the
vegetative portion of the shoot is isophyllous, while the inflo-
rescence is anisophyllous and bears flowers in only two ranks
of bracts (Danert 1953; Sell 1968; Dormer 1972). Mono-
phyllea and several species of Streptocarpus (both Gesneri-
aceae) are anisocotylous: the mature shoot system is reduced
to a single greatly enlarged cotyledon that bears multiple in-
florescences (Jong and Burtt 1975; Tsukaya 1997). Although

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S74 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 7 Dorsiventrality and anisophylly in the habitually anisophyllous shoots of Pellionia daveauana (Urticaceae). A, Dorsal view of shoot
showing large ventral leaves (V) and minute dorsal leaves (arrow). Scale bar = 1 cm. B, Apical view of shoot. Scale bar = 1 cm. C, Dorsal view
of node showing small dorsal leaf (D) and stipules of dorsal (DS) and ventral leaves (VS). Scale bar = 2.5 mm. D, Scanning electron micrograph
of dorsal (D) and ventral (V) leaf primordia from the dorsal sidel. Note intrapetiolar stipules (S) and rotation of ventral leaf lamina toward
dorsal side of shoot. Scale bar = 50 mm. E, Cross section of shoot apex showing modified diagonal decussate phyllotaxis with small dorsal (D1,
D2, D3) and large ventral (V1, V2, V3) leaves. Note rotated lamina evident for ventral leaf (V3). Scale bar = 100 mm (from Dengler 1992).

anisocotyly presumably arose under different selective forces
than did other forms of anisophylly, the physiological control
of growth suppression in both phenomena may share features
in common (see “Development and Competition,” below; Ro-
senblum and Basile 1984; Tsukaya 1997).
Adaptive Significance of Anisophylly
Anisophylly has been regarded as an adaptation for the cap-
ture of light in shaded environments since the earliest botanical
descriptions of this phenomenon (Spencer 1874; Wiesner
1894; Goebel 1928). Anisophylly minimizes mutual shading
by leaves on a single shoot and maximizes light capture by the
large photosynthetic surface of ventral leaves through sup-
pression of dorsal leaf expansion. Givnish (1984) argued that
plagiotropic axes with distichous phyllotaxis should be fa-
vored in shady environments because reduction of self-shading
would have a large impact on net photosynthesis at near-com-
pensation-point light levels. In addition, the transpirational
costs of a strictly horizontal photosynthetic surface would be

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 DENGLER—ANISOPHYLLY AND DORSIVENTRAL SHOOT SYMMETRY S75

Fig. 8 Dorsiventrality and anisophylly in facultatively anisophyllous shoots of Columnea orientandina (Gesneriaceae). A, Apical view of
plagiotropic shoot showing smaller dorsal leaves (D) and larger ventral leaves (V). B, Dorsal view of plagiotropic shoot with strongly expressed
anisophylly. Arrows indicate minute dorsal leaves. C, Ascending shoot with very weakly expressed dorsiventrality and anisophylly. Arrows point
to smaller dorsal leaves at some nodes. A–C, Scale bar = 1 cm. D, Scanning electron micrograph of shoot apical meristem showing equal size
of leaf primordia. Scale bar = 100 mm (from Sanchez-Burgos and Dengler 1988).

very low in shaded environments. With a premium on close
packing of adjacent leaves on plagiotropic shoots, asymmetric
leaf bases would provide an additional advantage by filling in
the gaps and forming an almost continuous photosynthetic
surface. Givnish (1984) pointed out that anisophylly is prev-
alent in tropical families that are characterized by decussate
leaf arrangement such as the Acanthaceae, Gesneriaceae, Me-
lastomataceae, Rubiaceae, and Urticaceae. Anisophylly pro-
vides a “solution” to the problem of self-shading in decussate
shoots by reducing leaf size on the dorsal side of the shoot.
In some cases, the small dorsal leaves help to fill in the gaps
between adjacent leaves (e.g., fig 5A). Although there is strong
correlational evidence for the functional significance of an-
isophylly, field and experimental studies, especially those using
a comparative approach in a phylogenetic context, are lacking.
Developmental Basis of Anisophylly and
Shoot Dorsiventrality
Two general patterns emerge from a comparison of shoot
development in species with anisophyllous dorsiventral shoots:
either dorsiventrality and anisophylly are expressed at the
shoot apex and then amplified (or dampened) during devel-
opment, or expression of these traits is delayed and super-
imposed on earlier radial or bilateral symmetry and isophyl-
lous leaf development. Based on the examples studied to date,
the first pattern occurs in shoots where expression of symmetry
and anisophylly is fixed and appears to be an intrinsic property
of shoot organization (e.g., Anisophyllea, Selaginella, Pel-
lionia). The second pattern occurs in species where expression
of anisophylly is facultative and may or may not be expressed,
depending on growth conditions (e.g., Columnea).
Anisophyllea disticha
Anisophyllea disticha (Anisophylleaceae) is a small tropical
understory tree with strong shoot dimorphism: orthotropic
main axes bear helically arranged, symmetrical scale leaves,
while plagiotropic, dorsiventrally flattened lateral branches
bear dorsal scale leaves and larger ventral foliage leaves (fig.
5A; Hallé et al. 1978; Vincent and Tomlinson 1983; Dengler
et al. 1989). Leaf symmetry is the Selaginella type, with the
larger halves of both dorsal and ventral leaves directed toward
the ventral side of the shoot (fig. 2G; fig. 5A, 5C). The shoot
apical meristem of plagiotropic shoots is slightly flattened in
the transverse plane, reflecting the phyllotactic pattern (fig. 5B,
5C). Dorsal and ventral leaf primordia are similar in size and
shape at initiation and expand at the same rate for about the

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S76 INTERNATIONAL JOURNAL OF PLANT SCIENCES
first 15 plastochrons; ventral leaves eventually achieve a larger
mature size because of the longer duration of leaf expansion.
Ventral and dorsal leaves can be distinguished histologically
in the first few plastochrons; however, lamina cells of the small
dorsal leaves begin to enlarge and vacuolate very early, while
tissues of ventral leaves retain their meristematic appearance
for a greater number of plastochrons (fig. 5C). Dorsal and
ventral leaves differ anatomically at maturity, and only the
ventral foliage leaves develop a palisade layer in the ground
tissue (Dengler et al. 1989). Vegetative and reproductive buds
are formed in the axils of the large ventral leaves, but both
are completely absent from axils of dorsal leaves. Anisophylly
and anisoclady are strongly correlated with primary vascular
architecture: ventral leaves are supplied by a greater number
of leaf traces, and individual ventral traces have a larger cross-
sectional area with a higher rate of differentiation of tracheary
elements (Dengler et al. 1989).
Selaginella martensii
Selaginella martensii (Selaginellaceae) is habitually an-
isophyllous with plagiotropic, creeping shoots (fig. 6A; Den-
gler 1983a). The apical meristem is dorsiventrally flattened,
and leaves are initiated in a diagonal decussate pattern, with
the four ranks of leaves slightly displaced to the transverse
plane (fig. 6B, 6C). Leaf asymmetry is weakly developed in
this species but is of the Selaginella type, with hypotonic dorsal
and ventral leaves (figs. 2G, 6A). Leaf dimorphism is accen-
tuated in this species because the dorsal leaf develops an apical
spine and dorsal and ventral leaf shapes diverge at early plas-
tochrons. Ventral leaf primordia have a greater circumferential
extent from initiation and, although the epidermis is the pri-
mary photosynthetic layer at maturity, ventral leaves develop
more extensive mesophyll tissue (fig. 6C). Ventral leaves have
both a greater rate and greater duration of expansion, and
dorsal and ventral leaves differ in allometric relationship of
leaf length and width throughout development (Dengler
1983a, 1983b).
Pellionia daveauana
Pellionia daveauana (Urticaceae) is a creeping herbaceous
plant with strong shoot dorsiventrality (fig. 7A, 7B). The dor-
sal leaves are highly reduced, ephemeral scale leaves that are
much smaller than the stipule that develops from the leaf base
(fig. 7C). Phyllotaxis is diagonal decussate, with modified di-
vergence angles so that both dorsal and ventral orthostichies
are displaced toward the transverse plane (fig. 7E; Mueller and
Dengler 1984). The shoot apical meristem is dorsiventrally
flattened, with its wide diameter fluctuating between successive
plastochrons. Dorsal and ventral leaves of a pair are initiated
simultaneously, but the zone of leaf initiation has greater extent
on the ventral side of the apex, so that ventral primordia have
a greater volume than dorsal primordia from inception (fig.
7D). Ventral leaves form a leaf blade during the second plas-
tochron of development, while blade formation is completely
suppressed in the small dorsal leaves (fig. 7E; Mueller and
Dengler 1984). Ventral leaves have epitonic symmetry (fig. 2I)
and also display the “rotated lamina” syndrome: both halves
of the lamina extend toward the dorsal side of the shoot, ac-
centuating shoot dorsiventrality (fig. 7D, 7E; Charlton 1993b,
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1998). Leaf unfolding brings the adaxial surface of the leaves
into the transverse plane, optimizing photosynthetic surface.
Differences in blade development and in rate and duration of
growth result in very different allometric constants and final
sizes for dorsal and ventral leaves. Arrested expansion of the
dorsal leaves is also reflected in histological development: dor-
sal leaves lack the multiple epidermis, well-differentiated mes-
ophyll, and elaborated venation of ventral leaves (Mueller and
Dengler 1984). Primary vascular development of the shoot is
strongly correlated with dorsiventrality, anisophylly, and an-
isoclady: ventral leaves are supplied by a greater number of
vascular traces, and each trace has about 10 times the number
of tracheary elements of a dorsal leaf trace. The median leaf
trace extends acropetally into the ventral leaf primordium dur-
ing the first plastochron of leaf development, while the acrop-
etal extension of the dorsal leaf median trace is delayed until
the second plastochron (Dengler and Donnelly 1987).
Columnea orientandina
Shoots of Columnea orientandina (=Pentadenia orientan-
dina, Kvist and Skog 1993; Gesneriaceae) are facultatively an-
isophyllous. The species has a scrambling habit, and shoots
may be either ascending and weakly anisophyllous or more
plagiotropic and strongly anisophyllous (fig. 8A–8C). In the
most strongly dorsiventral shoots, the dorsal leaves are minute
(fig. 8B). A dorsal lamina is initiated, but both expansion and
histological differentiation are arrested (Sanchez-Burgos and
Dengler 1988). In shoots with less striking dorsiventrality, dor-
sal leaf lamina expansion is suppressed but dorsal leaves un-
dergo normal histogenesis. Regardless of the degree of an-
isophylly expressed within the shoot, dorsal and ventral leaf
primordia appear equivalent in size from inception to about
the third plastochron, when growth of the smaller dorsal leaf
is arrested or slows (fig. 8D; Sanchez-Burgos and Dengler
1988). The pattern of vascular supply to dorsal and ventral
leaves is identical, but differentiation of vascular tissue from
procambium reflects leaf expansion differences, so that small
dorsal leaves have much reduced lateral leaf traces in com-
parison with the ventral leaves of the same shoot (Morgan and
Dengler 1988).
Developmental Regulation of Anisophylly and
Shoot Dorsiventrality
Shoot dorsiventrality is widespread among the land plants,
and it is coupled with anisophylly in numerous taxonomic
groups (Figdor 1909; Goebel 1928; Troll 1937; Dengler 1992).
This systematic distribution and the differences in expression
patterns in diverse taxa indicate that anisophylly has evolved
independently several times, most likely in response to similar
selection pressures working on different ancestral back-
grounds. Thus, it is expected that anisophyllous species would
show a diversity of regulatory mechanisms that guide the de-
velopment of a dorsiventral shoot so that phyllotaxis, stem
and leaf expansion, and bud development are integrated. At
the same time, it is likely that more than one physical or phys-
iological factor regulates the development of anisophylly in an
individual species, providing the combination of “backup”
mechanisms that buffer the plant from transient external per-
 DENGLER—ANISOPHYLLY AND DORSIVENTRAL SHOOT SYMMETRY
turbations yet allow responsiveness to meaningful environ-
mental variation.
Intrinsic Factors
In some cases, anisophylly may result from a simple physical
constraint and, once the constraint is lifted, anisophyllous leaf
production may switch over to isophyllous development. This
interpretation may apply to many examples of lateral an-
isophylly in woody plants (D. R. Kaplan, unpublished man-
uscript; Troll 1937). In lateral buds of Acer pseudoplatanus,
White (1955) observed that the first pair of primordia is borne
in the transverse plane and that primordia are of equal size.
The second primordium pair is initiated in the median plane
where the dorsal leaf primordium appears to be physically
constrained between the lateral shoot axis and the parent
shoot. Dorsal leaf primordia are smaller than ventral leaf pri-
mordia and give rise to smaller leaves. White (1957) also noted
that anisophylly disappears during the second year of growth,
when leaf primordia are formed without this constraint. He
distinguished such primary anisophylly (determined in the bud)
from secondary anisophylly in which equal-sized primordia of
a pair formed unequal mature leaves, presumably in response
to shading and the directionality of light. The best character-
ized example of anisophylly developing as the result of a pre-
sumed constraint occurs in the lateral shoots of Populus del-
toides. Larson and Richards (1981) demonstrated a strong
correlation between the smaller blade size of dorsally placed
leaves and leaf trace connections with the main shoot axis:
leaf traces of dorsal leaves were directed upward in the main
axis, toward the shoot apex, while leaf traces of ventral leaves
were directed downward and connected directly to antecedent
leaves that could act as a source of nutrients and growth sub-
stances. The smaller half of asymmetric leaf blades was also
supplied by upwardly direct traces. Anisophylly in P. deltoides
was expressed in leaf primordia within lateral buds but was
absent in the first overwintering bud of a lateral shoot and in
its subsequent extension growth. Anisophylly of first year lat-
eral shoots was reduced when the main shoot was decapitated
and growth of the lateral assumed a vertical orientation but
was never completely eliminated (Richards and Larson 1981).
Differences between the dorsal and ventral sides of the shoot
in vascular supply and in timing of vascular differentiation in
Pellionia daveauana and Anisophyllea disticha might be con-
strued as constraints on the developmental potential of dorsal
leaves. However, despite the strong correlation between sup-
pression of vascular development and of leaf development, it
is not possible to attribute causality. In fact, it is as likely that
suppression of dorsal leaf growth reduces the source of phys-
iological signals required for normal vascular development as
that limited vascular development constrains dorsal leaf
growth.
External Cues
The final degree of expression of shoot dorsiventrality and
anisophylly may depend on external cues, whether or not the
rudiments of these features are preformed (i.e., arise before
shoot expansion from the bud). Light and gravity are two
directional environmental signals that would be experienced
differently by the dorsal and ventral sides of a plagiotropic
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S77
shoot and have long been thought to influence expression of
these features. Numerous early experiments attempted to de-
termine the relative roles of light and gravity in the develop-
ment of shoot dorsiventrality and anisophylly, often with con-
flicting results. For instance, Frank (1868) twisted plagiotropic
shoots of Picea through 180⬚ and found that anisophylly was
reduced but not completely reversed. Kny (1873) repeated the
experiment with Abies shoots and reported that anisophylly
was completely lost in the next year’s growth. Goebel (1928)
and Figdor (1909) extended these experiments and concluded
that directionality of both light and gravity was important for
the expression of anisophylly.
More recently, the effect of light and gravity on the expres-
sion of anisophylly has been investigated in Selaginella kraus-
siana, using a controlled experimental design missing from
many early studies (Bilderback 1984a, 1984b). Bilderback
(1984a) cultured shoot tips in vials that were placed horizon-
tally, either with the dorsal side up or the dorsal side down,
and then illuminated from either the top or the bottom. When
vials were oriented so that the ventral side of the shoot was
up and then illuminated from the same side, shoots underwent
a resupination through 130⬚ so that dorsal side was reoriented
toward the source of light. When vials were oriented so that
the dorsal side was up and then illuminated from below, shoots
still made a hairpin turn that brought the dorsal side of the
shoot into position so that it was directly illuminated. Only
blue and white wavelengths elicited this response, suggesting
that signal perception and response was shared with other
phototropic responses. Shoots that were placed in darkness
lacked these responses, indicating that gravity alone did not
have an effect on shoot orientation. The treatments used in
these experiments did not alter dorsiventrality and anisophylly
per se (only shoot orientation) but provide a model of the kind
of experiments needed to demonstrate the relative effects of
these environmental cues on development.
Light intensity may also influence anisophyllous develop-
ment, particularly in species that are phenotypically plastic for
this trait such as Paradrymonia ciliosa (Wiehler 1978). In this
species, phyllotaxis is diagonal decussate and leaf primordia
of a pair are identical up to the second plastochron, presum-
ably a reflection of equivalent developmental potential (Den-
gler and Sanchez-Burgos 1988). Both leaves of a pair initiate
a lamina at this stage, but further expansion of the small dorsal
leaf is arrested. Unlike other examples of phenotypically plastic
leaf development where there is a continuum in leaf form be-
tween the largest and smallest leaves (e.g., C. orientandina;
Sanchez-Burgos and Dengler 1988), leaves of P. ciliosa expand
either as large laminate or as small linear structures. On a
single shoot, nodes may bear a pair of isophyllous laminar
leaves, or an anisophyllous pair of one laminar and one linear
leaf, or more rarely, a pair of linear leaves. Reduced light in-
tensity increases the degree of overall shoot anisophylly (ex-
pressed as the mean ratio of leaf lengths at all nodes of a shoot),
both by increasing the proportion of nodes on a shoot bearing
anisophyllous leaf pairs and by increasing the size of the ex-
panded laminar leaves. Earlier reports that anisophylly was
enhanced by reduced light level (e.g., Goebel 1928) might be
primarily attributable to the shade leaf response of many plant
species: ventral leaves might respond to shading by expansion,
S78 INTERNATIONAL JOURNAL OF PLANT SCIENCES
while dorsal leaves might be unable to overcome growth sup-
pression and respond to reduced irradiance.
Recent identification of genes that act in the perception,
signal transduction, or response to gravity and light (e.g., Rob-
son and Smith 1996) indicate that it will be possible in the
future to determine developmental mechanisms required for
some forms of dorsiventrality and anisophylly and to compare
them among related taxa in a meaningful way.
Competition and Suppression
Although a phylogenetic analysis of the occurrence of an-
isophylly has not been attempted, it likely represents the de-
rived condition in the clades in which it occurs (Dengler 1992).
This pattern indicates that anisophylly requires modification
of preexisting developmental pathways so that growth of
leaves on one side of a dorsiventral shoot is suppressed. Many
evolutionary innovations require that suppression of growth
be regulated in time and space (Basile and Basile 1993), and
experiments with plant growth regulators give an indication
of how this may occur at the physiological level. Guttenberg
and Steinweg (1956) applied auxin to shoots of Centradenia
floribunda, a habitually anisophyllous species, and showed
that growth of the smaller dorsal leaves was preferentially
stimulated, so that the size differential between dorsal and
ventral leaves was reduced. Guttenberg and Müller (1957)
showed that removal of the leaf subtending an axillary bud
reduced anisophylly in axillary shoots of Coleus blumei and
suggested that competition for nutrients or hormone levels
explained correlational growth in this species.
Further support for a role of plant growth substances in the
developmental regulation of anisophylly comes from experi-
ments on the dorsiventral shoots of leafy liverworts (Basile and
Basile 1993). Genera that normally have distichous phyllotaxis
could be induced to form a third rank of leaves on the ventral
side of the stem through the application of antagonists of either
auxin or ethylene. They also found that antagonists of hy-
droxyproline-rich cell wall proteins induced a similar effect.
As related genera are characterized by the consistent presence
of ventral leaves, Basile and Basile (1993) hypothesized that
evolutionary change in the Jungermanniales involved loss of
leaf production on the ventral side of the stem through sup-
pression of normal cell enlargement and accompanying cell
division or by alteration of the physical properties of cell walls
that might influence morphogenesis by altering tensile and
compressive forces within the shoot apex region.
Tsukaya (1997) provided strong support for the role of com-
petition in the inhibition of one cotyledon of a pair in the
anisocotylous species Monophyllea horsfieldii. Cotyledons are
identical morphologically at germination and, based on mi-
crosurgical experiments, have an equal potential for continued
growth for a short period after germination. After this period,
however, one cotyledon appears to be able to out-compete the
other and then to inhibit its growth (Tsukaya 1997). In some
cases, the suppressed cotyledon can be released from suppres-
sion by surgical removal of the dominant cotyledon (Tsukaya
1997). Rosenblum and Basile (1984) also found that exoge-
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nous application of growth hormones could stimulate coty-
ledon growth in Streptocarpus species. Like apical dominance,
anisophylly and shoot dorsiventrality may be regulated by
competition between dorsal and ventral regions of the shoot
for growth regulators or nutrients. Competition may be par-
ticularly important in facultative anisophylly since light may
indirectly influence hormone level through photosynthate
status.
Even if hormones such as auxin are shown to play a role
in stimulating and/or inhibiting growth in dorsiventral shoots,
active hormone level would be only one step in a complex
developmental process. Recent advances in understanding the
development of dorsiventral symmetry in floral meristems
might contribute a clue that would help identify one element
in the developmental regulation of dorsiventrality in vegetative
shoots—or at least suggest a parallel mechanism. Based on a
phenotypic analysis of mutant plants and an in situ hybridi-
zation study of expression in wildtype plants, it appears that
the cycloidea gene is a major regulator of floral symmetry in
Antirrhinum majus (Luo et al. 1996). During wildtype floral
development, cycloidea is expressed in the dorsal region of the
floral meristem, initially in a domain just two to four cells
wide at the junction of the floral and inflorescence meristems.
The domain of cycloidea expression within the floral meristem
is well defined before organ formation and coincides with the
positions of the dorsal sepal, dorsal petals, and dorsal stam-
inode (Luo et al. 1996). Comparison of wildtype and mutant
phenotypes indicates that cycloidea acts to suppress growth in
the dorsal portion of the flower and that it also influences
asymmetry of the lateral petals and stamen filaments. Although
it is unknown at this time whether cycloidea or other genes
play a role in defining dorsal and ventral domains in vegetative
shoots, it is to be expected that similar mechanisms would
operate during the development of dorsiventrality in an-
isophyllous shoots.
In summary, a wealth of information on anisophylly and
other forms of shoot dorsiventrality is embedded in the bo-
tanical literature of the past 125⫹ yr. In fact, anisophylly was
something of a “hot topic” at the turn of the last century.
Despite long-term and recurring interest in the topic, it is still
difficult to make definitive statements about the developmental
mechanisms, adaptive significance, or the evolutionary origin
of this syndrome of morphological traits. All of these issues
warrant further study in themselves, and their elucidation
should also have broader significance for understanding the
developmental basis of shifts in size and symmetry of plant
organs during the evolution of descendant from ancestral taxa.
Acknowledgments
I thank Ronald E. Dengler for photographs, Meaghan
Brierly for drawings, and Petra Donnelly for preparing other
illustrations. I am grateful to Hirokazu Tsukaya for discussion;
to Allan Charlton, Rolf Rutishauser, and Connie Soros for
helpful comments on the manuscript; and to Donald R. Kaplan
for providing preprints of unpublished chapters.
 DENGLER—ANISOPHYLLY AND DORSIVENTRAL SHOOT SYMMETRY
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