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Lateral Meristems
Secondary article
Simon Turner, University of Manchester, Manchester, UK
Article Contents
. Introduction
Radial growth of plants is the result of activity of the lateral meristems. These meristems,
known as the vascular and cork cambiums, are active in areas of the plant where primary
growth has ceased and are therefore referred to as secondary meristems.
. Initiation of Secondary Thickening in Roots and Shoots
. Vascular Cambium and Phellogen (Cork Cambium)
. Fusiform and Ray Initials
. Induction, Activation and Regulation (Seasons)
Introduction
. Plant Growth Regulators
The development of most plant species is characterized by
an increase in girth. This increase occurs in regions of the
plant in which primary growth from the root and/or shoot
meristem has ceased, and is therefore termed secondary
growth. Secondary growth is the result of activity of the
vascular cambium and the cork cambium, which are
collectively known as lateral meristems. In many tree
species where the circumference of a tree may measure
several metres, this increase is due to successive years of
radial growth that is reinitiated from the lateral meristems
at the beginning of each growing season. One product of
the vascular cambium is wood and the activity of lateral
meristems is recorded within the wood by the annual
growth rings. The annual reinitiation of lateral meristem
activity during the growing seasons becomes a record of
growing conditions: years with favourable or poor conditions for growth are recorded as thick or thin growth rings
respectively. As some tree species may be several thousand
years old, lateral meristems are clearly capable of undergoing periods of intermittent growth almost indefinitely. In
addition to tree species, many herbaceous plants, including
the widely studied small crucifer Arabidopsis thaliana
Growth ring
Cambium
Phloem
Xylem
Radial
Tangential
Transverse
Figure 1 Diagram of a section of stem during its third year of secondary
growth. The three planes (transverse, radial and tangential) that are used to
examine the organization of the cambium and its derivatives are indicated.
(Dolan and Roberts, 1995), have been shown to undergo
secondary growth. This secondary growth is also an
integral part of development in most dicotyledonous
plants.
The lateral meristems encircle the body of the plant
(Figure 1). They are distinguished from apical meristems,
which form the primary body of the plant, in several ways,
but most noticeably in the proximity of the lateral
meristem to the tissues that they produce. A proper
understanding of lateral meristems may be considered as a
problem of two parts: (1) how are cell divisions in the
meristem regulated; and (2) what controls the differentiation of new cells into specialized cell types.
Initiation of Secondary Thickening in
Roots and Shoots
Shoots
Although the shoot and root apical meristem may be
distinguished very early in embryo development, the
cambium appears to initiate once primary growth has
ceased. Whilst the primary vascular system differentiates
from the cells of the procambium, it appears that some cells
in the procambium retain the ability to initiate lateral
meristem activity. Typical dicotyledonous patterns of
growth generate a stem containing discrete bundles of
xylem and phloem separated by an interfascicular (literally
between the bundles) region. Cambial activity is normally
first initiated within the vascular bundle. Whilst most
procambial cells differentiate into xylem or phloem, a few
cells remain undifferentiated and these cells initiate the
fascicular cambium. In some species with only very limited
secondary growth, cambial activity is limited solely to the
fascicular cambium; more commonly, however, a continuous ring of cambium is completed by activation of
parenchyma cells in the interfascicular region. Activity of
the cambium leads to an increase in the radius of the shoot
by the production of secondary xylem and phloem.
Initiation of the phellogen (cork cambium) normally
occurs after initiation of the cambium. In most instances,
ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net
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Lateral Meristems
the phellogen originates from a layer of cortical cells just
below the epidermis, although it may also originate from
the epidermis or from within the phloem in some species.
Roots
Vascular development in roots occurs from a central
vascular cylinder. Protoxylem development begins at
several points around the cylinder, with metaxylem
differentiating later and occupying the centre of the
cylinder. The protoxylem projections remain and are
named protoxylem poles. Phloem develops between the
poles. Initiation of the vascular cambium occurs in regions
of the root that have stopped elongating and starts
simultaneously in several regions between the primary
xylem and phloem. Divisions in the pericycle opposite the
protoxylem contribute cells to form the complete cambium
that encircles the primary vascular tissue. In common with
stems, the roots of woody plants also initiate a phellogen
that gives rise to a protective layer of periderm and
pericycle, which replaces the epidermis.
Vascular Cambium and Phellogen
(Cork Cambium)
Vascular cambium
The vascular cambium may be visualized as a layer of cells
that appear relatively undifferentiated sandwiched between the xylem (to the inside) and phloem (to the outside)
(Figure 2). To investigate fully the three-dimensional
organization of the cell layer, it has been necessary to
section in three different planes: transverse, radial and
tangential (see Figure 1). Problems encountered in visualizing the cambium are compensated for by the ability to trace
cell lineage easily. The direct proximity of cambium to the
cells derived from it clearly distinguishes the cambial
meristem from the primary meristems of the plant.
Within the cambium lie the initials. Periclinal divisions
within the initials generate new cells that differentiate into
xylem centripetally (towards the inside of the stem) or
phloem centrifugally (towards the outside of the stem).
Successive divisions lead to rows of cells originating on
both sides of the cambium. The fact that both xylem and
phloem originate from the same cells in the cambium is
demonstrated most clearly in meristems in which the
number of initials increases or decreases. An increase in the
number of cambial initials by anticlinal divisions (see
below) is matched by a corresponding increase in the
number of radial rows of both xylem and phloem.
Similarly, loss of cambial cells is matched by a corresponding decrease in the numbers of rows of both xylem and
phloem. Radial rows of cells that arise from the cambium
therefore have a common cell lineage. Differentiation into
2
Figure 2 Transverse section from the cambium from (a) Scots pine and
(b) silver birch at 200 and 400 original magnification, respectively.
The cambial zone (indicated by the bracket) separates the blue staining
xylem on the right from the phloem. The rays (r) are clearly visible running
through the cambium, xylem and phloem. The xylem of the pine is formed
of similar-sized tracheids, whereas the birch xylem is composed of large
vessel members and fibres, both of which arise in the same file of cells and
are consequently derived from the same cambial initial.
mature cells occurs as cells are moved away from the
cambium by new divisions. Consequently, the tissue also
records the stages in differentiation into the specialized cell
types of the vascular tissue, with the early stages of
differentiation seen close to the cambium and mature cells
further from the cambium. This feature of the cambium
makes it an attractive system for studying various aspects
of cell differentiation (Chaffey, 1999).
A central point of interest within the cambium is whether
the cambium contains a single layer of initials. The
observations outlined above argue indirectly that there is
only a single cell; consequently division or loss of this single
cell leads to a corresponding alteration in the number of
radial rows. Flanking the initials are layers of undifferentiated, actively dividing cells, which are the precursors to
xylem and phloem. Commonly xylem precursors (xylem
mother cells) divide more rapidly than the phloem
precursors, so that during a growing season more xylem
cells are produced. It has been hard to identify the cambial
ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net
Lateral Meristems
initials within these undifferentiated cell layers because
they often possess no obvious structural features to
distinguish them. Controversy exists to the exact nomenclature used. Some workers refer to only the single layer of
initials as the cambium, and the initials together with the
undifferentiated precursors of the xylem and phloem
(xylem and phloem mother cells) are termed the cambial
zone (Figure 2). Other workers refer to the cambium as both
the initials and the adjacent undifferentiated cells.
Phellogen
In contrast to the vascular cambium, which contains
distinctly different types of initials (see below), the
phellogen initials are of only one cell type. Anticlinal
divisions in the phellogen give rise to radial rows of cells
(Figure 3). Cells towards the outside differentiate as phellem
or cork, whereas those in the inside differentiate as
phelloderm or secondary cortex. Unequal numbers of cells
are produced on either side of the meristem: more new cells
arise towards the outside, producing more phellem than
phelloderm. Cells of the phellem become impregnated with
suberin and are dead at maturity. This process gives the
phellem its impervious and protective properties. The
phelloderm cells remain alive and may closely resemble the
cells of the cortex. The radial arrangement of these cells
(Figure 3), however, distinguishes them from the cortex laid
down during primary growth.
Figure 4 Radial (a,c) and tangential (b) sections of Scots pine and
silver birch, respectively. Radial sections show the files tracheids and
vessels that arise in the xylem from the long thin fusiform initial (f) and
fusiform initials that form the rays running horizontally (r). Sections from
the pine phloem (b) and pine xylem (d) show the simple patterns of
uniseriate rays in pine and more complex multiseriate rays in birch. Original
magnifications for radial sections (pine and birch) and tangential were
100, 400, 200 and 200, respectively.
2) clearly shows that fusiform initials correspond to the
Fusiform and Ray Initials
vessels members or tracheids and fibres of the xylem and
the sieve elements of the phloem. In contrast, the ray
initials correspond to the radial arrangement that runs
through both the xylem and the phloem (Figures 1 and 2).
Examination of radial or tangential sections through the
cambial zone reveals two very distinctive cell types (Figures 2
and 4). Fusiform initials are interspersed with ray initials.
Comparison of the cell type in the cambium with the cell
type in the mature tissue they produce (Figures 1 and
Fusiform initials
Figure 3 Radial section through the phellogen of silver birch. The cells are
clearly arranged in files and the phellem cells (ph) near the outside of the
stem are heavily suberinized.
Fusiform initials are elongate cells, which may be up to
9 mm long in some species. In contrast to the initials of
primary meristems, these cells are often highly vacuolated.
Divisions in fusiform initials are mostly periclinal. These
divisions are unusual for plant cells because they occur
vertically and the new wall is formed down the long axis of
the cell. Formation of the new cell wall starts in the region
of the nucleus and forms outwards towards the ends of the
cell. Occasionally anticlinal divisions occur, which increase
the number of initials and accommodate the increase in
girth of the tree as it grows. In tree species with long
fusiform initials, such as conifers, the anticlinal divisions
occur in the transverse plane, halving the length of the
initial. The length of initials is maintained by tip growth
from the two daughter cells. Such divisions have been
termed pseudotransverse. In dicotyledonous species there
is a reduction in the length of initials that appears to be
correlated with the phylogenetic relationship of the trees,
with the most primitive species having the longest fusiform
ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net
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Lateral Meristems
initials. The reduction in length of fusiform initials is
accompanied by a progressive reduction in the length of
vessel members. In some advanced tree species the initials
are very short and anticlinal divisions are vertical. In these
species the fusiform initials are arranged in strict rows, an
arrangement described as storied cambium.
Ray initials
Ray initials are isodiametric cells that are arranged in single
(uniseriate) or multiple (multiseriate) vertical rows
(Figure 4). The organization of rays (Figure 4) is highly
dynamic. Increase in the height and width of rays occurs as
a result of divisions of ray initials. In addition, new ray
initials may arise from fusiform initials, either by a division
that cuts off the tip or by an anticlinal division in which the
new wall curves to meet the side wall. The number of rays
may also be increased by tip growth from fusiform initials,
which results in an existing ray being split into two.
Induction, Activation and Regulation
(Seasons)
As activation of the interfascicular cambium appears to
spread away from the vascular bundles, it was once
assumed that a signal was propagated from the active
cambium in the vascular bundle (see above). A series of
classical experiments by Siebers (1971) on castor seedlings
suggests that this may not be the case. Razor blades were
inserted into the stems of castor seedlings to isolate the
interfascicular region from the vascular bundle. This
isolation had no apparent affect on the ability of the
interfascicular region to form an active cambium. In
further experiments a block of interfascicular region was
excised and then replaced in the opposite direction. The
explants went on to develop an interfascicular cambium,
but with the orientation reversed, such that xylem was now
formed on the inside of the stem and phloem on the outside.
These experiments led to the idea that the cambium, with a
distinctive polarity, is determined before any visual sign of
cambial activity and that the formation of the cambium is
not dependent on a signal from adjacent cells.
Trees from temperate regions undergo a period of
dormancy during the winter months. The vascular
cambium contracts to a layer that may be only 1–3 cells
wide. Resumption of growth the following spring commences with a period of cell division before cell differentiation, which leads to an increase in the size of the cambium
zone. In other tree species, dormancy may be controlled by
water availability. Some trees from tropical regions appear
to grow almost continuously and lack growth rings.
4
Plant Growth Regulators
Resumption of cambial activity is a regulated process that
resumes round the circumference of the tree. In addition, it
appears that cambial activity is linked to the growth of the
crown. Such correlations have led to the idea that cambial
activity is regulated by some kind of morphogen. An
excellent candidate for a factor that controls cambial activity
is the plant growth regulator auxin (Uggla et al., 1998).
For more than 100 years it has been known that cambial
activity is inhibited in shoots from which the buds have
been removed. Activity can be resumed by the application
of auxin; conversely, application of auxin transport
inhibitors decreases cambial activity. If the source of auxin
required for cambial activity is considered to be the young
growing leaves, then auxin provides a link between crown
growth and cambial activity. Recent and very accurate
measurements of auxin in the cambial region have shown
that auxin levels are high in the cambial zone and that levels
decline rapidly in developing xylem and phloem. Such
experiments suggest that this radial auxin gradient may
convey important positional information in the control of
cell division and cell differentiation within the cambial zone
(Uggla et al., 1996, 1998).
It has been suggested that, to explain the process of cell
division and cell differentiation, gradients of at least two
different regulators are required. In addition to auxin,
gibberellin and sucrose, abundant in the phloem, have both
been implicated in cambial growth and vascular tissue
differentiation (Roberts, 1988).
References
Chaffey N (1999) Cambium: old challenges – new opportunities. Tree 13:
138–151.
Dolan L and Roberts K (1995) Secondary thickening in roots of
Arabidopsis thaliana – anatomy and cell surface changes. New
Phytologist 131: 121–128.
Roberts LW (1988) Hormonal aspects of vascular differentiation. In:
Roberts LW, Gahan PB and Aloni R (eds) Vascular Regulation and
Plant Growth Regulators, pp. 22–38. Berlin: Springer.
Siebers AM (1971) Initiation of radial polarity in the interfascicular
cambium of Ricinus communis L. Acta Botanica Neerlandica 20: 343–355.
Uggla C, Moritz T, Sandberg G and Sundberg B (1996) Auxin as a
positional signal in pattern formation in higher plants. Proceedings of
the National Academy of Sciences of the USA 93: 9282–9286.
Uggla C, Mellerowicz EJ and Sundberg B (1998) Indole-3-acetic acid
controls cambial growth in Scots pine by positional signalling. Plant
Physiology 117: 113–121.
Further Reading
Aloni R (1987) Differentiation of vascular tissue. Annual Reviews of
Plant Physiology 38: 179–204.
Larson PR (1994) The Vascular Cambium; Development and Structure.
Berlin: Springer.
Steeves TA and Sussex IM (1989) Patterns in vascular development.
Cambridge: Cambridge University Press.
ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net