Download Interxylary phloem: Diversity and functions Sherwin Carlquist

Interxylary phloem: Diversity and functions
Sherwin Carlquist
Brittonia
ISSN 0007-196X
Brittonia
DOI 10.1007/s12228-012-9298-1
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Interxylary phloem: Diversity and functions
SHERWIN CARLQUIST
Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105, USA;
e-mail: [email protected]
Abstract. Interxylary phloem is here defined as strands or bands of phloem embedded
within the secondary xylem of a stem or root of a plant that has a single vascular
cambium. In this definition, interxylary phloem differs from intraxylary phloem, bicollateral bundles, pith bundles, and successive cambia. The inclusive but variously
applied terms included phloem and internal phloem must be rejected. Histological
aspects of interxylary phloem are reviewed and original data are presented. Topics
covered include duration of interxylary phloem; relationship in abundance between
sieve tubes in external phloem and interxylary phloem; distinctions between interxylary and intraxylary phloem; presence of parenchyma, fibers, and crystals in the
interxylary phloem strands; development of cambia within interxylary phloem strands; three-dimensionalization and longevity of phloem, systematic distribution of interxylary phloem; physiological significance; and habital correlations. No single
physiological phenomenon seems to explain all instances of interxylary phloem occurrence, but rapidity and volume of photosynthate transport seem implicated in most
instances.
Key Words: Bicollateral bundles, included phloem, intraxylary phloem, photosynthate conduction, successive cambia.
Interxylary phloem consists of strands of
sieve tubes, companion cells, and adjacent
parenchyma or other cells embedded within
the secondary xylem of a stem or root that has
a single vascular cambium. This definition is
presented to distinguish interxylary phloem
from a series of other histological phenomena
that may have similar functions but are
histologically and ontogenetically different. For
example, the term successive cambia denotes a
series of vascular increments, each with secondary phloem, secondary xylem, and a vascular
cambium, each of which ultimately originates
from the master cambium at the periphery of a
stem or root (Carlquist, 2007). The master
cambium produces secondary cortex (0 parenchyma) to the outside, and to the inside,
conjunctive tissue and vascular cambia to the
inside of an axis. Each vascular cambium then
produces secondary phloem to the outside and
secondary xylem to the inside. The term
included phloem was misapplied to successive
cambia in some (but not all) Nyctaginaceae by
Chalk and Chattaway (1937), but used also for
instances of interxylary phloem. Misapplications of this sort render the term included
phloem imprecise, and, in any case, are based
on topographic phloem distribution without
regard to ontogenetic factors. The ontogeny of
phloem and xylem within various cambia
variants can be easily determined from the
mature histology, and thus can readily be
included in definitions of cambial variants. The
term "included" suggests that the phloem in
instances of successive cambia is embedded
within secondary xylem (as it is in the case of
interxylary phloem). In fact, the phloem in
examples of successive cambia lies between
secondary xylem (internal to it) and conjunctive
tissue (external to it) in each vascular increment.
The term internal phloem has likewise been
contaminated by conflicting usages and should
be rejected. "Internal phloem" has been used to
refer to intraxylary phloem, but has been
applied to other histological conditions. Significantly, like "included" phloem, the term
Brittonia, DOI 10.1007/s12228-012-9298-1
ISSN: 0007-196X (print) ISSN: 1938-436X (electronic)
© 2013, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A.
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internal phloem is vague with respect to
ontogeny as well as location of phloem.
Intraxylary phloem, although readily distinguishable from interxylary phloem, may
have a similar physiological significance and
is covered in a later section of this paper. The
present usages are consistent with those
adopted in earlier accounts of cambial variants (Carlquist, 1988, 2001, 2007). For the
present, workers would be well advised to
define the terms they use for cambial variants.
Interpretation of functions of interxylary
phloem is further complicated by the fact that
in woody angiosperms as a whole, interxylary
phloem occurs in only a relatively small
number of families and species. Even within
a genus such as Combretum or Strychnos,
some species have interxylary phloem, others
lack it, with no clear differences in habit or
size of plant (van Vliet, 1979; Mennega,
1980). However, there is some correlation
with systematic units within genera such as
these (van Vliet, 1979; Mennega, 1980).
There is no unique function for interxylary
phloem; other phloem distributions seem to be
adequate alternates. That does not mean,
however, that interxylary phloem is not a
physiologically significant way of meeting a
plant's photosynthate conduction requirements.
Wood anatomy contains many examples of
alternative ways of serving particular functions
(e.g., vestured pits, helical sculpture of vessel
surfaces, and vasicentric tracheids are probably
all methods of minimizing embolism formation
—or reversing that). Interxylary phloem, like
vestured pits, is a device that is homoplastic in
woody angiosperms. In both instances, genetic
information for the formation of these structures has not been frequently achieved phylogenetically, perhaps because a complex series
of genetic changes is required. The data
presented here may offer interesting examples
that lend themselves to physiological studies.
Plant physiological studies have traditionally
been done on economically important plants,
and none of the species with interxylary phloem
has any major economic value.
materials and methods used in those studies are
given in the papers listed below. In all cases,
however, the photographs and observations are
new. Re-studied materials include the following:
Figure 1: Turbina stenosiphon (Hallier f.)
A. Meeuse (Convolvulaceae): Carlquist and
Hanson, 1991.
Figure 2A–C: Thunbergia laurifolia Lindl.
(Acanthaceae): Carlquist and Zona, 1988
Figure 2D: Stylidium glandulosum Salisb.
(Stylidiaceae): Carlquist, 1981
Figure 4: Pseudolopezia longiflora Rose
and Oenothera linifolia Nutt. (Onagraceae):
Carlquist, 1975.
Figure 6: Salvadora persica L.(Salvadoraceae): Carlquist, 2002.
Sources for material not previously studied
are as follows:
Figure 3: Orphium frutescens E. Mey.
(Gentianaceae): Carlquist 8212, June 28,
2011 (SBBG).
Figure 5: Craterosiphon scandens Eng. &
Gilg (Thymeleaceae): Breteler 1227 (WAG).
Figure 7A–B. Strychnos madagascariensis
Poir. (Loganiaceae): David Lorence 10285
(PTBG), National Tropical Botanical Garden
living collections accession number 801348.
Figure 7C–D. Combretum erythrophyllum
Sond. (Combretaceae): cultivated in the
Vavra Garden (formerly owned by University
of California, Los Angeles).
The sections in Figs. 3 and 7C–D were
derived from living material that was preserved in 50 % aqueous ethanol, sectioned on
a sliding microtome, and stained with a
Safranin-Fast Green combination. The section
in Fig. 7A–B was derived from living
material that was preserved in aqueous 50 %
ethanol. The sections were prepared by driving
a single-edged razor blade into a stem with the
aid of a hammer. The sections derived were
subjected to changes of distilled water, and
dried between glass slides under pressure (to
prevent curling), then sputter-coated with gold
and examined with a Hitachi S2600N scanning
electron microscope (SEM).
Aspects of Interxylary Phloem
Materials and methods
Some of the examples cited here are derived
from earlier wood anatomical surveys. The
1. Ontogenetic and Histological Criteria;
Allied Phenomena.
Because secondary xylem consists mostly
of cells with rigid walls, it is a clear and
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CARLQUIST: INTERXYLARY PHLOEM
FIG. 1. Transections of stem of Turbina stenosiphon (Convolvulaceae), to show diverse types of vascular
histology. A–B. Successive cambia. A. Three vascular increments, each with secondary xylem (sx) and secondary
phloem (sp); the middle vascular increment has an inverted orientation (ivi), atypical for successive cambia. B. Higher
power, area corresponding to center of A. The inverted increment (ivi) above has produced secondary phloem
adaxially and secondary xylem abaxially; the crushed secondary phloem (csp) was produced by the inverted
increment. The normal increment below has produced secondary phloem abaxially and secondary xylem adaxially. C.
Strand of interxylary phloem, surrounded by fibrous secondary xylem. D. Intraxylary phloem strand (itp) adaxial to
protoxylem (upper left). A cambium (arrows) has developed in the strand and has produced secondary phloem (sp)
adaxially. Pith parenchyma, some of which has been converted to pith sclereids (ps) below.
easily read record of the action of the vascular
cambium. The products of cambial action are
unambiguous, so that there is no need to
develop definitions that exclude ontogenetic
aspects and are merely topographic in their
frame of reference (e.g., included phloem). To
be sure, xylarium specimens have poor preservation of meristematic cells and of phloem, but
the location and sequences of cell types with
secondary walls (which are readily seen in
sections of xylarium specimens) are quite
sufficient to permit any appearance to be
referred to one of the categories accepted here.
The difference between interxylary phloem
and successive cambia can be seen in Turbina
stenosiphon (Fig. 1A–C) of the Convolvula-
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FIG. 2. Sections of rayless stems containing interxylary phloem. A–C. Thunbergia laurifolia (Acanthaceae). A–B.
Transections. A. Low power to show secondary phloem (sp) above), and secondary xylem below, with the vascular
cambium (vc) between them. The secondary xylem is composed of an axial parenchyma (pax: gray) background in
which bands or strands of fibrous vessel-bearing xylem (fx: darker) are embedded. B. Higher power photograph to
show the strands of sieve tubes (st) in the axial parenchyma backgrounds. Fibrous xylem may deiverge from each
other (di) by means of parenchyma or may actually break apart (br) due to tensions during growth. C. Radial section to
show sieve plates (sp) in sieve tubes (darker gray), sheathed by parenchyma of the interxylary strand (pix, lighter
gray); the fibrous xylem cells (fx) are narrower and stain more darkly. Stylidium glandulosum (Stylidiaceae),
transection of stem portion with secondary growth. The vascular cambium (vc) is essentially unifacial, producing
secondary xylem externally but nothing more than perhaps a single layer of secondary cortex externally; a phellogen
(pg) has developed in the innermost cortical cells. Seven arrows indicate strands of interxylary phloem, which are very
narrow and consist of only two to four cells each.
ceae. This species is the first, to my knowledge,
in which both successive cambia (Fig. 1A–B)
and interxylary phloem (Fig. 1C) have been
shown to coexist in a single stem. Interestingly,
a third phenomenon, intraxylary phloem, is also
represented in Turbina stenosiphon (Fig. 1D).
Successive cambia are increments of secondary
xylem and phloem, each produced by a
vascular cambium. The cambia, as well as
conjunctive tissue and secondary cortex (0
parenchyma) are produced by a master cambium (Carlquist, 2007). Conjunctive tissue is not
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CARLQUIST: INTERXYLARY PHLOEM
FIG. 3. Transections of stem of Orphium frutescens (Gentianaceae). A. Low power photograph to illustrate that
secondary phloem (sp) contains only a few strands of sieve tubes (st); the remainder is parenchyma. Vascular cambium
(vc) at the juncture with secondary xylem. The secondary xylem consists of fibrous xylem (fx) in which strands or
bands of interxylary phloem (ip) are located. B. Intermediate power photograph to illustrate that the interxylary
phloem may take the form of strands (ip) or bands (ipb) located in a background of vessel-bearing fibrous xylem (fx).
C–E. Higher power photographs to illustrate intersections between rays (r) and interxylary phloem (ip) in relation to
the fibrous xylem (fx) background. C. Two strands of interxylary phloem are separated by a ray. D–E. Instances in
which sieve-tube elements and companion cells are derived from ray initials, and in which phloem ray tissue therefore
contains phloem.
a form of axial parenchyma; axial parenchyma
is produced only by a vascular cambium. The
example illustrated here, Turbina stenosiphon,
is unusual in having one vascular increment
inverted in orientation, with that vascular
cambium producing phloem internally and
xylem externally. This is the only instance I
know in which a vascular increment has this
inverted orientation. This occurrence does
underline the fact that occasionally one does
see a cambial variant with atypical ontogeny. At the same time, the rarity of such
occurrences reinforces the regularity of
phenomena described by the definitions
given: cambial variants are orderly, and
not "anomalous."
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FIG. 4. Transections of stems of Onagraceae. A–B. Pseudolopezia longiflora. A. Tangentially wide interxylary
phloem band (ipb) embedded in a background of starch-rich fibers (srf). B. Section showing secondary phloem (sp) in
upper half, divided from the secondary xylem, below, by the vascular cambium (vc). Strands of sieve tubes (st) are
scarce in the secondary phloem. Fibers of the secondary xylem are rich in starch (srf). C–D. Stem transections of
Oenothera linifolia. C. First-year xylem: strands of interxylary phloem (ip) are relatively numerous, but short-lived;
gaps appear in them due to collapse of sieve tubes; phloem parenchyma cells surround the gaps. D. Second-year
xylem: strands of interxylary phloem (ip) are few but functional.
The interxylary phloem strand illustrated in
Turbina stenosiphon (Fig. 1C) exemplifies all
of the features claimed by the definition. It is
a strand of sieve tube elements and companion cells surrounded by a sheath of parenchyma. Because the parenchyma is formed by
a vascular cambium, it can be termed axial
parenchyma.
Intraxylary phloem is also present in
Turbina stenosiphon (Fig. 1D). Intraxylary
phloem occurs at the adaxial tips of vascular
bundles of a number of woody angiosperms
(for a list, see Metcalfe and Chalk, 1983,
appendix). Cambial activity is found in a
minority of instances of intraxylary phloem,
and there is no list of genera in which it is
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CARLQUIST: INTERXYLARY PHLOEM
FIG. 5. Stem sections of Craterisiphon scandens (Thymeleaceae). A. Low power photograph of wood transection
to illustrate that earlier-formed secondary xylem is devoid of interxylary phloem, whereas more recently-formed wood
contains bands of interxylary phloem (ipb). B. Intermediate power photograph of transection to illustrate the extent of
two interxylary phloem bands (ixb). C. High-power wood transection photograph of an interxylary phloem strand and
a ray (r); ap 0 axial parenchyma (related to vessel); cs 0 crystal sand; f 0 intrusive fiber in interxylary phloem; sp 0
sieve plate as seen in transection. D. Longisection of interxylary phloem strand: f 0 intrusive fibers; pix 0 parenchyma
of interxylary phloem; sp 0 sieve plates (seen obliquely).
present or absent. It is present in the strand
illustrated in Fig. 1D. Where present, cambium in intraxylary phloem acts unidirectionally, producing secondary phloem adaxially
rather than (as with an ordinary vascular
cambium) abaxially. Secondary xylem is
produced by this cambium only rarely, but
has been figured in Operculina (Carlquist &
Hanson 1991; Carlquist, 2012,).
Bicollateral bundle is a term that denotes
phloem at both the abaxial and adaxial
surfaces of a bundle (as opposed to a
collateral bundle, which has phloem only
abaxially). Although the term does not spe-
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FIG. 6. Transections of stem of Salvadora persica (Salvadoraceae). A. Low power photograph to illustrate
secondary phloem (top 2/5 of picture) and secondary xylem (sx), bottom 3/5 of photograph, indicating various
quantities of parenchyma (pa) within the secondary xylem. B. High power photograph of a portion of the transection
shown in A; secondary phloem (sp, above) contains a single strand of sieve tube elements (to right of the letters sp);
below the vascular cambium (arrows) is a strand of fibrous xylem containing two vessels; the remainder of the
secondary xylem consists of parenchyma (pa). C–E. High power photographs to show interxylary phloem. C. Juncture
between secondary phloem (sp) and secondary xylem, with vascular cambium (arrow) between them. In the secondary
phloem, a strand of sieve tubes is seen (left); in the secondary xylem, a ray (r) and a young strand of interxylary
phloem (left of the letters ip) are embedded in axial secondary xylem that consists of parenchyma (pa), with no fibers
present. D. A strand of interxylary phloem of intermediate age, farther from the vascular cambium; some of the
phloem is crushed (cip); below that, phloem is function, and the formation of a cambium in the interxylary phloem
strand is denoted by arrows. E. An older strand of interxylary phloem; all of the phloem is crushed (cip).
cifically exclude the presence of secondary
xylem in such a bundle, it is more commonly
applied when there is little or no secondary
growth in the bundle, as in Cucurbita or
Solanum (Lycopersicon). Thus, there is an
overlap with the term "intraxylary phloem."
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CARLQUIST: INTERXYLARY PHLOEM
FIG. 7. Stem transections to show interxylary phloem. A–B. Strychnos madagascariensis (Loganiaceae). Stem
transections seen with SEM. A. Low power micrograph, to show a typical large interxylary phloem strand (ip) in a
fibrous xylem (fx) background; bark (b) at top of photograph. B. High power photograph corresponding to lower left
portion of the strand shown in A; a cambium (c, plus arrows) has formed within the interxylary phloem strand; cpa 0
crushed parenchyma, fx 0 fibrous xylem; np 0 newer phloem; op 0 older phloem. C–D. Light photomicrographs of
stem transections of Combretum erythrophyllum (Combretaceae). C. An interxylary phloem strand near the vascular
cambium (which is not shown, but is just above the top of the photograph); a cambium (c, plus arrow) has recently
formed within the interxylary phloem strand, but there is no crushed phloem; cpa 0 crystal-bearing parenchyma; fp 0
functional phloem; fx 0 fibrous secondary xylem. D. An older strand of interxylary phloem, in which a cambium (c,
plus arrow) has been active; crushed phloem (cp) forms a conspicuous band; cpa 0 crystal-bearing parenchyma; fp 0
functional phloem; fx 0 fibrous xylem.
2. Parenchyma Associated with Strands of
Interxylary Phloem.
Strands of interxylary phloem are most
commonly strands of axial parenchyma in
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which there is a central core of sieve tube
elements and companion cells. This is most
easily seen in Thunbergia (Fig. 2A–C). Thunbergia is a vine and the diameter of the sieve
tubes is larger than in the average nonvining
eudicot. In longisections, one can see sieve
plates in the strands of interxylary phloem
(Fig. 2C). The fibrous xylem consists of nonseptate libriform fibers (Fig. 2C, fx). Thunbergia is rayless, so all of the thin-walled parenchyma seen in Fig. 2A–C is axial parenchyma.
Parenchyma associated with interxylary phloem
is transversely subdivided into strands, much
like axial parenchyma in typically woody
eudicots. Axial parenchyma in Thunbergia
separates bands and strands of vessel-containing
fibers (Fig. 2A, B), which occasionally break
(Fig. 2C, br) in response to stem growth and
torsion. Axial parenchyma in Thunbergia thus
serves a mechanical function that can often be
served by wide rays in scandent woody plants.
Stylidium glandulosum (Fig. 2D), a subshrub, also has rayless wood. The strands of
interxylary phloem (arrows) consist of little
more than a sieve tube element plus a companion cell each, and are quite inconspicuous. An
occasional axial parenchyma cell is present in
these strands. Stylidium and Thunbergia form
extremes with respect to quantity of parenchyma associated with phloem.
Intermediate quantities of parenchyma characterize the strands of most species that have
interxylary phloem (Figs. 3A–E, 4A and 6C–E).
The varied quantities of parenchyma observed
in strands of interxylary phloem may be keyed
to diverse physiological functions, but there has
been no experimental work on this topic.
3. Rays and Interxylary Phloem.
By implication, interxylary phloem occurs
as vertical strands in axial xylem. This is
clearly demonstrated by most species (e.g.,
Thunbergia, Fig. 2A–C). In most species that
have interxylary phloem, rays either do not
cross strands of interxylary phloem (Fig. 6A–
E) or if they do (Fig. 5A–B), The ray cells
retain their typical histological characteristics.
Orphium (Fig. 3) provides some examples of
this latter condition, but it also, in a few
places, forms sieve tube elements and companion cells in rays. In Fig. 3C, instances of
typical interxylary phloem strands that do not
intersect rays are shown.
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In Fig. 3D and E, instances in which
portions of rays have been converted to sieve
tube elements and companion cells are shown
(r 0 rays). One should note that ray cells in
Orphium are predominantly upright, as one
would expect from a secondarily woody plant
(Carlquist, 1962, 2009), so conversion of ray
cells to sieve tube elements and companion
cells is really not contrary to the expected
direction of conduction. If one scans larger
areas of Orphium wood transections, one sees
that interxylary phloem occurs as either
strands or bands (Fig. 3A, B). The ratio of
bands that contain sieve tube elements and
companion cells in ray areas to those that do
not is perhaps only one band out of twenty.
4. Diversity in Patterns: Strands, Bands,
Relative Abundance.
Interxylary phloem is usually seen as cylindrical strands (Figs. 1C and 2B). These strands
can range from inconspicuous and few celled,
as in Stylidium, to large and obvious, even
perceptible without microscopy, as in Strychnos
(Fig. 7A) and Combretum (Fig. 7C, D).
Interxylary phloem is often present in the form
of tangential bands (Figs. 4A and 5A. Bands
and strands may occur together.
Salvadora (Fig. 6) appears to have bands
rather than cylindrical strands of interxylary
phloem (e.g., Fig. 6C) because the parenchyma
surrounding the strands occurs as tangential
bands (Fig. 6A, B). Salvadora exemplifies the
point that parenchyma may be much more
abundant in transectional area than the strands
of phloem in embedded in the parenchyma.
5. Cell Contents: Crystals, Starch, etc.
Crystals occur in parenchyma that sheathes
phloem in a large number of the species that
have interxylary phloem. Exceptions can be
cited in the case of Stylidium (Fig. 2D)
Orphium (Fig. 3) and Salvadora (Fig. 6).
Although not shown here, prismatic crystals occur in the axial parenchyma bands that
contain phloem in stems of Thunbergia alata
Bojer ex Sims (Carlquist and Zona, 1988;
Carlquist, 2001). Raphides are present in such
parenchyma in Onagraceae (Carlquist, 1975).
Crystal sand is present in axial parenchyma of
interxylary phloem strands in Craterosiphon
(Fig. 5C; SEM photos in Carlquist, 2001).
Druses occur in the phloem-ensheathing paren-
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CARLQUIST: INTERXYLARY PHLOEM
chyma of Combretum (Fig. 7C–D, cpa). The
positioning of druses in interxylary phloemadjacent parenchyma in Combretum as well as
in cases of crystal occurrence in other genera
listed in the present study suggests that
crystal-bearing sheaths may deter predation
of interxylary phloem by chewing beetles.
Such positioning of crystals is often seen
in relation to phloem in bark of many
woody species.
In woods of Onagraceae, starch is common
in libriform fibers adjacent to strands of
interxylary phloem (Fig. 4A–B, srf; Carlquist,
1975). However, starch is notably absent in
the parenchyma sheathing the phloem strands
in that family (Fig. 4A–B). This circumstance
suggests that starch storage and active transport of soluble photosynthates are distinct
functions performed by these two respective
tissues.
6. Libriform Cells in Interxylary Phloem.
Because the root word "liber" refers to
phloem, sieve tube elements (and their associated companion cells) could be included as
"libriform elements" but that is not usually
done. "Libriform" implies an elongated form,
and usually refers to fibers. Certainly sievetube elements in Craterisiphon are elongate,
their length easily determined from presence
of sieve plates (Fig. 5D). Curiously, however,
extraxylary fibers mature in the interxylary
phloem bands of Craterisiphon (Fig. 5B, C).
These fibers are gelatinous, and in permanent
slides, the secondary walls shrink away from
the primary walls (Fig. 5C). The fibers are
instrusive, and their tips (Fig. 5D, f) do not
align with the sieve plates of the sieve tube
elements, which are shorter than the fibers.
7. Timing of Interxylary Phloem Onset.
Presence of interxylary phloem may change
in abundance with age of stem. This is evident
in Fig. 5A for Craterisiphon. In this stem,
interxylary phloem is absent in earlier-formed
secondary xylem. This has been reported in
other species, such as Azima tetracantha Lam.
of the Salvadoraceae. Den Outer and van
Veenendaal (1995) describe interxylary phloem
strands throughout the stem of this species.
Their stem was larger in diameter than the one I
studied (Carlquist, 2002); at the periphery of the
stem I studied, interxylary phloem production
had just begun. In other Salvadoraceae, such as
Dobera (Carlquist, 2002) and Salvadora
(Fig. 6), interxylary phloem production begins
early and remains constant in abundance.
Mennega (1980) in her study of wood of
Strychnos and other Loganiaceae mentions
that interxylary phloem has not been reported
in some species (cf. Pfeiffer, 1926) in which
only small diameter stems were available,
whereas larger-diameter stems prove to have
interxylary phloem.
An apparent exception to this trend
occurs in Oenothera linifolia, in which
interxylary phloem strands are fewer and
smaller in second-year wood of stems
(Fig. 4D) as compared to first-year wood
(Fig. 4C). The occurrence of this trend is
somewhat masked by the fact that in firstyear wood, parenchyma cells of the strands
enlarge and develop secondary walls after
the collapse of sieve tube elements and
companion cells.
Pfeiffer (1926), following Schenck (1895)
reports sieve tube elements in secondary
xylem of Mucuna altissima DC. as a late or
subsequent (nachträglich) development
compared with maturation of other cell
types nearby.
8. Comparison between Interxylary Phloem
and Secondary Phloem in a Single Stem.
Comparisons of this sort are lacking, presumably because dried material rather than
liquid-preserved material has been studied,
and because soft tissues do not survive sliding
microtome sectioning as well as harder (fibrous) tissues. The question that arises in
connection with comparison of these two
phloem regions within a given stem is whether
in stems that have interxylary phloem, sieve
tube elements are less abundant in secondary
phloem (outside the vascular cambium) than in
stems that lack interxylary phloem. The answer
to this question, based on a small sample, is yes,
although variability is evident. Whether bark
thickness relates to distribution of sieve tube
elements in interxylary phloem vs. secondary
(0 external, or bark) secondary phloem is not
known, and needs investigation.
The most notable example is found in
Stylidium species that have secondary growth
(most species of the genus lack secondary
growth). Stylidium glandulosum (Fig. 2D)
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produces at most one layer of cells external to
the vascular cambium, and the cells of that
layer are best described as parenchyma.
These cells are not radially aligned with the
innermost cortical parenchyma layer, in
which phellogen develops (Fig. 2D, pg).
Thus, there is no true secondary phloem,
and no sieve tubes external to the cambium.
This was reported, although not thoroughly
illustrated, earlier (Carlquist, 1981).
Orphium (Fig. 3A) and Pseudolopezia
(Fig. 4B) show a relative paucity of sieve tubes
and companion cells in secondary phloem.
Relatively extensive areas of secondary phloem
consist exclusively of phloem parenchyma,
with only a few, isolated strands of sieve tube
elements and companion cells present.
Some degree of variability occurs in Salvadora (Fig. 6). In some areas of secondary
phloem, sieve tube elements and companion
cells are relatively sparse (Fig. 6A–B), whereas
in others, they are rather more common
(Fig. 6C). As a generalization, however, Salvadora—as well as the other interxylary-phloembearing eudicots for which data are reviewed
here—have fewer sieve tube elements and
companion cells in secondary phloem (bark)
than is typically observed in eudicots that lack
interxylary phloem.
9. Organographic Distribution.
Work in wood anatomy remains biased
toward stems, for understandable reasons. In
fact, so few xylarium specimens are of root
material that no indication of site of origin on
the plant is given on most specimens; the
default assumption is that stem material is
involved. (Whether the material comes from
main stem or branches is likewise never
indicated on xylarium labels).
Some workers have mentioned interxylary
phloem in roots or rhizomes. For example,
Pfeiffer (1926) reports interxylary phloem
"islands" (interxylären Inseln) in transections
of roots and rhizomes of Cochlearia armoracia L., Brassica napus L., B. rapa L., and
Raphanus sativus L. Metcalfe and Chalk
(1950), citing Pfeiffer's (1926) reports, mentioned "secondary interxylary bundles" in the
unlignified xylem of the rhizomes of Armoracia lapathifolia Gileb. and in the root of
Brassica napus, B. rapa, and Raphanus
sativus. The overlapping nature of these reports
[VOL
and the impreciseness of the term "secondary
interxylary bundles" underlines the need for
more extensive studies not merely to confirm
the histological nature of these instances, but to
determine the ontogenetic origin of these
"bundles" or "islands." The lack of reports of
such appearances in the stems of Brassicaceae
is, however, notable in this regard.
Pfeiffer (1926) assigned histological
appearances in the roots of Scolopia atropoides Bercht. & Presl (Solanaceae) to the
concept of interxylary phloem. He likewise
referred similar vascular tissue in roots of
Browallia viscosa HBK. (Solanaceae) to this
category. Pfeiffer (1926) also reproduces a
believable drawing of interxylary phloem in
thin-walled root secondary xylem of Atropa
belladonna L. (Solanaceae) by Leisering
(1899), so there is reason to credit his concept
of interxylary phloem in that species as the
same as mine. Stem interxylary phloem has
not been reported in Atropa. Pfeiffer (1926)
reports interxylary phloem for roots of Ipomoea versicolor Meissn. (Convolvulaceae),
but does not note it in stems of this species.
There are obviously many residual opportunities for confirmation or reassignment into
other catergories of interxylary phloem
reports. New discoveries remain to be made,
as in Turbina stenosiphon (Fig. 1C). The
material available to earlier workers was limited,
and often was biased in favor of plants which
were naturally-occurring or grown in Europe,
and in favor of stems rather than roots of those.
10. Cambial Activity within Interxylary
Phloem.
Scott and Brebner (1889) described development of cambial activity in the interxylary
phloem strands of Strychnos, based upon
living material cultivated in greenhouses.
Scott and Brebner figured large strands of
interxylary phloem much like the one figured
here (Fig. 7A, B). They reported crushed
phloem on the abaxial side of the strands with
cambial activity, so that the cambia in these
strands produces secondary phloem externally, thereby in the same direction as the
vascular cambium. This activity agrees with
the findings reported here (Fig. 7A, B).
Despite the disadvantage of working with
herbarium material, Mennega (1980) reported
the above facts accurately in a survey of
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CARLQUIST: INTERXYLARY PHLOEM
woods of Strychnos (and other Loganiaceae).
As Mennega (1980) stated, not all species of
Strychnos have interxylary phloem in the
stems, even when large-diameter stems are
examined. A study devoted to one species, S.
millepunctata Leeuwenberg (van Veenendaal
& den Outer, 1993) includes some excellent
SEM images that reinforce the findings of
Scott and Brebner (1889).
Note should be taken that cambial activity
in the interxylary phloem strand begins soon
after a strand is produced by the vascular
cambium. Cambial action is evident from the
radial seriation of the cells produced by the
interxylary phloem cambium (Fig. 7B, np).
The earlier-formed interxylary phloem cells
may not show radial seriation (Fig. 7B, op).
The amount of secondary phloem produced by
cambial activity within a strand is evident from
the quantity of radially seriate phloem cells in
the phloem as well as the amount of crushed
phloem on the abaxial side of the strand. Bark
of Strychnos (Fig. 7A, top) is relatively poor in
sieve tube element production.
Large interxylary phloem strands occur in
the African species of Combretum of the
Combretaceae (van Vliet, 1979), but not all of
them. Histological and ontogenetic details
given to date are relatively few because most
specimens studied are from herbarium material or xylarium blocks. Somewhat thick
sliding microtome sections of liquid-preserved material presented here (Fig. 7C, D)
illustrate that Combretum interxylary phloem
strands are histologically similar to those in
Strychnos and like them in the timing of
cambial initiation within the strand. Strands
close to the vascular cambium (Fig. 7C)
already show the beginning of cambial
activity on the adaxial side of the strand.
Older strands (Fig. 7D) show crushed phloem
(cp) conspicuously, and a continuation of
cambial activity within the strands. Interxylary phloem strands in Combretum are composed of fibriform (Fig. 7C, fp) cells (when
seen in longisection) and crystalliferous parenchyma cells (cpa) that contain druses.
Cambial activity is reported here in the
interxylary phloem strands of one other family,
Salvadoraceae, although attention has not hitherto been called to this phenomenon (Carlquist,
2002), presumably because it is so inconspicuous. In young strands of interxylary phloem of
Salvadora persica (Fig. 6C, bottom, ip) there
are only sieve tube elements and companion
cells that have been derived from the vascular
cambium. Crushed phloem and cambial activity
within younger strands is not observed, contrary
to the conditions in Combretum and Strychnos.
In moderately old interxylary phloem
strands of Salvadora, no radial seriation of
cells is evident (Fig. 6D). Cambial activity
(arrows) is minimal. Some collapsed phloem
(Fig. 6D, cip) is evident, but the accumulation
is not prominent. Earlier formed (older)
interxylary phloem strands show a greater
amount of crushed phloem (Fig. 6E).
There is a correlation between size of
interxylary phloem strands and presence of
cambial action within these strands, when one
compares the interxylary phloem of Combretaceae, Loganiaceae, and Salvadoraceae to that of
other families. These families are woody,
ranging from shrubs to trees, and preservation
of phloic pathways by means of active replacement of sieve tube elements and companion
cells by cambial activity within the strands
seems a strategy that is correlated with habit.
11. Relationship between Intraxylary Phloem
and Interxylary Phloem.
The present study endorses the term intraxylary phloem to refer to phloem strands that
occur adjacent to protoxylem, at margins of
the pith. This term does not equate entirely to
the term "bicollateral bundle" (see “Aspects
of Interxylary Phloem”, section 1), in which
minimal accumulation of secondary xylem is
implied. Approximately equal amounts of
phloem are seen external and internal to the
xylem in species with bicollateral bundles,
whereas in instances referred to the concept
of intraxylary phloem, the amount of phloem
formed externally from the vascular cambium
can be relatively large, whereas the intraxylary phloem strands are relatively finite in
size. Because of the uneasy coexistence of
these terms, listings of families that exemplify
one or the other concept have not always been
assembled based on critical review of material.
In addition, misapplication of these terms
creates problems. Pfeiffer (1926) cited instances of phloic strands in the pith, for example.
One can, however, cite particular families
and genera in which intraxylary phloem is
characteristically present. Metcalfe and Chalk
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(appendices, 1950, 1983) presented such lists.
In their listings, Metcalfe and Chalk distinguished between families that characteristically have intraxylary phloem (bold face) and
those in which intraxylary phloem is occasionally reported (ordinary font) or infrequent
or perhaps dubious (italics). The families of
Myrtales figure prominently in the list
(Combretaceae, Crypteroniaceae, Lythraceae,
Melastomataceae, Myrtaceae, Oliniaceae,
Onagraceae, Penaeaceae, and Punicaceae).
Interestingly, interxylary phloem also occurs
in an appreciable number of species in three
of these families (Combretaceae, Melastomataceae, and Onagraceae). A similar link
between intraxylary phloem presence and
interxylary phloem occurrence can be cited
for other families in the Metcalfe and Chalk
(1950) list (Gentianaceae, Loganiaceae, Stylidiaceae, and Thymeleaceae) as well as
Leptadenia, an asclepioid genus of Apocynaceae (Singh, 1943; Patil & Rajput, 2008).
Thus, intraxylary phloem may be a kind of
"precursor" for interxylary phloem formation
in a given species. In developmental terms,
the genetic information for the formation of
strands of phloem within the xylem (interxylary) as well as internal to (adaxial to) the xylem
(intraxylary) may be similar. Exceptions to this
concept can certainly be listed (e.g., Salvadoraceae lack intraxylary phloem), and this theory
may apply only in particular clades.
The physiological implications of this
connection between the two sites of phloem
formation are, however, even more interesting. In, say, Myrtales, why do only some of
the species that have intraxylary phloem go
on to produce interxylary phloem?
One of the most interesting aspects of
interxylary phloem is the development of a
cambium in intraxylary phloem in some
instances. This is illustrated for Turbina
stenosiphon (Fig. 1D), but occurs in other
eudicots, such as Cucurbitaceae (Carlquist,
1992; Patil et al., 2011).
When cambium develops within a strand of
intraxylary phloem, the secondary phloem it
yields is always produced toward the center
of the stem, rather than toward the outside
(the latter, of course, is what happens in the
formation of bark by the vascular cambium).
The inverted nature of the secondary phloem
production by cambia at intraxylary phloem
[VOL
sites is also indicated by the fact that in a few
species, the intraxylary phloem cambium also
produces some secondary xylem (in an
external, or abaxial, direction). This has been
illustrated for Operculina palmeri (Wats.)
Howe of the Convolvulaceae (Carlquist &
Hanson 1991; Carlquist 2012,).
12. Systematic Occurrence of Interxylary
Phloem.
As noted above, understanding the systematic occurrence of interxylary phloem is a
work in progress. Several reports must be
regarded as tentative, while others are likely
incorrect. The latter are difficult to prove
definitively, because interxylary phloem may
occur infrequently in a few species. The late
onset of interxylary phloem production, mentioned for Azima and Strychnos, is another
reason to be cautious where lists are
concerned. The multiplicity of individuals
who report instances of interxylary phloem
results in variable criteria and thus lack of
precision in application of the concept.
The following list contains instances that
appear well substantiated on the basis of
supporting drawings or photographs. Earlier
workers occasionally conflated interxylary
phloem (formed from a single vascular
cambium) with instances of successive cambia under the inclusive rubric "included
phloem." That vague umbrella usage was
followed by IAWA Committee (1989).
Instances of successive cambia are not included in this list. The listing is similar to that
presented earlier (Carlquist, 2001), but with
some emendations. Following this list, a
compilation of dubious, incorrect, or unusual
instances that do not conform to the working
definition of interxylary phloem.
Apocynaceae (including Aslepiadaceae):
Asclepias, Ceropegia, Leptadenia (Singh,
1943; Patil & Rajput, 2008).
Brassicaceae: roots and rhizomes of Brassica spp., Cochlearia, and Raphanus
(Pfeiffer, 1926).
Combretaceae: Calycopteris, Combretum,
Guiera, Thiloa (van Vliet, 1979; den Outer &
van Veenendaal, 1995; Rajput et al., 2009).
Convolvulaceae: Ipomoea versicolor
Meissn. roots and hypocotyl (Scott, 1891);
Turbina stenosiphon (infrequent; new report,
above).
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Fabaceae: Mucuna altissima DC. (Schenck
1893).
Gentianaceae: Crawfordia, Chiroma, etc.
(Pfeiffer, 1926); Ixanthus (Carlquist, 1984);
roots of some other genera (Pfeiffer, 1926).
Icacinaceae: Chlamydocarya, Sarcostigma,
etc. (Lens et al., 2008).
Lythraceae: roots of Lythrum salicaria L.
(Gin, 1909).
Malpighiaceae: Dicella, Stigmaphyllon,
Tetrapteris (Pfeiffer, 1926).
Melastomataceae: six genera (Chalk &
Chattaway, 1937; Metcalfe & Chalk, 1950).
Onagraceae: at least seven genera (Carlquist,
1975, 1977, 1983, 1987).
Salvadoraceae: all genera (den Outer & van
Veenendaal, 1981; Carlquist, 2002).
Solanaceae: roots and rhizomes of Atropa
belladonna L.; roots of Datura stramonium
L. and Scolopia sp. (Pfeiffer, 1926).
Stylidiaceae: Stylidium (Carlquist, 1981).
Thymeleaceae: Aquilaria and eight other
genera (Pfeiffer, 1926; Solereder, 1908; Metcalfe
& Chalk, 1950); Craterosiphon (above).
Special cases:
Coccinia (Cucurbitaceae) develops cambia
adjacent to rays (Carlquist, 1992) or within axial
parenchyma of secondary xylem (Patil et al.,
2011). In both of these instances, these unusual
cambia produce secondary phloem, but no
secondary xylem. Because the secondary phloem in both instances lies within the confines of
secondary xylem, the phloem produced by these
cambia can be called interxylary phloem. The
terminological choice by Patil et al. (2011) is
therefore acceptable, but one should note that
Coccinia represents an unusual instance.
Excluded instances or dubious cases in
need of re-examination:
Acanthaceae: Barleria (Pfeiffer, 1926)
Apocynaceae: Lyonsia, Mandevilla, and
Parsonsia were cited by Pfeiffer (1926), but
his definition of interxylary phloem was
wider than mine and is not followed here.
Asteraceae: Stoebe (Adamson, 1934).
Bignoniaceae: Distictis, Haplolophium,
and Pithococtenium (Pfeiffer, 1926).
Convolvulaceae: Cuscuta (Pfeiffer, 1926)
Clusiaceae: Endodesmia roots (Pfeiffer, 1926).
Euphorbiaceae: Dalechampia (Pfeiffer, 1926)
Loranthaceae: Nuytsia (original data; reported
as a case of interxylary phloem by Pfeiffer,
1926; Nuytsia has successive cambia).
Sapindaceae: Serjania (Pfeiffer, 1926).
Urticaceae: Myriocarpa is cited by Chalk
and Chattaway (1937) on the basis of large
parenchyma strands within the secondary
xylem. In fact, these strands, as they conceded, do not contain phloem. Rather, the
parenchyma strands exemplify the phenomenon of fiber dimorphism (Carlquist, 1958,
1961). The occurrence of this kind of
parenchyma in Urticaceae has been confirmed
by Bonsen and ter Welle (1984).
Study of liquid-preserved material is needed to resolve cases considered dubious here,
because sieve tube elements do not survive
drying very well. The erroneous report of
Myriocarpa exemplifies this. Likewise, roots
provide logistical problems for investigation.
The few reports of interxylary phloem in
roots (Weiss, 1880; Gin 1909; Solereder,
1908; Pfeiffer, 1926) are tantalizing because
they suggest more instances might be found.
13. Physiological Significance.
The study of interxylary phloem (as well as
allied phenomena: intraxylary phloem, bicollateral bundles) is obviously still incomplete
with respect to descriptive anatomy. The
understanding of the physiological significance
of these structural modes of phloem occurrence
is a promising topic for exploration. Nevertheless, we can ask questions about function based
on our present understanding of anatomy.
Physiological studies, like anatomical studies,
are most actively pursued in species of economic interest. In fact, none of the species
known to have interxylary phloem is of any
major economic importance. Living material of
many of the species is not easy to access. Thus,
progress in investigation of how interxylary
phloem works has been slow. The topics listed
below may be regarded as points for departure
of physiological studies.
(a) Conduction rather than storage. Onagraceae show that parenchyma associated
with sieve tube elements and companion cells
in interxylary phloem strands is deficient in
starch, but tissues distal to the strands (mostly
libriform fibers) are rich in starch (Carlquist,
1975). This clearly suggests a marked division of labor, in which interxylary phloem
strands represent a conductive tissue, whereas
the ground tissue of the secondary xylem is
converted into a significant starch reservoir.
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Lack of starch in the parenchyma that
sheathes sieve tube elements is evident in
examples other than Onagraceae reviewed
here: Acanthaceae (Fig. 2A–C), Stylidiaceae
(Fig. 2D), Gentianaceae (Fig. 3), Thymeleaceae (Fig. 5) Salvadoraceae (Fig. 6), Loganiaceae (Fig. 7A–B) and Combretaceae
(Fig. 7C–D) can be cited in this regard.
(b) Conduction to large photosynthate sinks.
A number of species with interxylary phloem
strands have large fruit size (Strychnos: Leeuwenberg, 1980)) simultaneous production of
large numbers of flowers and fruits (Oenothera)
or other organographic features (sudden flushes
of growth, Strychnos) that suggest a relationship between interxylary phloem and intense
photosynthate utilization. Large inflorescences
in which numerous flowers open at about the
same time (Combretum) are pertinent in this
regard.
Instances of bicollateral bundles can be
cited here. Large fruits in Cucurbitaceae and
Solanaceae require rapid input of photosynthates that may be related to supernumerary
phloem formations.
(c) Enhanced rate of photosynthate conduction: the case of Orphium.
This topic is allied to the above, but
differs in stressing the rapid, simultaneous
flowering of an entire plant. Orphium
frutescens (Gentianaceae) has interxylary
phloem. Orphium is a small shrub or
subshrub that flowers during its first year of
growth. During some subsequent year, flowering is so extensive and simultaneous that the
plant devotes its entire reserves of photosynthates to the flowering/fruiting process and dies.
At this point, it is a monocarpic plant, although
one would not have designated it as such in
prior years.
I have cultivated Orphium frutescens in my
garden and attempted to prolong the vegetative growth of a plant by removing all flowers
during its summer flowering season. In the
sixth year of growth, it produced only
branches that terminated in flowers, with no
side branches with vegetative buds. At that
point, there was no longer any possibility of
deterring flowering, and the plant flowered,
fruited, and rapidly died after fruiting. An
event of this sort seems correlated with the
presence of interxylary phloem throughout
the stem of Orphium.
[VOL
To be sure, there are many monocarpic
plants that lack interxylary phloem. We do
not know about their phloem abundance or
phloem conductive patterns, because phloem
of monocarpic plants has not been the subject
of a study. One can, however, cite such plants
as species of Oenothera (Onagraceae) that are
biennials—in a sense, short-lived monocarpic
plants. There is interxylary phloem in these.
With relationship to Onagraceae as a whole, I
suggested (Carlquist, 1975) that "Production of
large flowers or large quantities of flowers
during a short period might be related to
massive starch reserves and interxylary phloem
for rapid transport of sugars." In this regard, we
may note that Fuchsia (Onagraceae), which
does not have interxylary phloem, produces
flowers slowly over a long period of time
(sometimes throughout the entire year).
(d) Phloem pathway multiplication and
longevity. If interxylary phloem is produced
continuously over a period of time, the
aggregate quantity of sieve tube elements
and companion cells in a stem (or root) soon
exceeds the potential amount of phloem in
bark. This is a feature relevant to conduction
only if older interxylary phloem stays active.
The occurrence of cambial activity producing
new sieve tube elements and companion cells
in interxylary phloem strands, as in Combretum, Salvadora, and Strychnos, attests to
interxylary phloem longevity. We do not know,
however, about the longevity of interxylary
phloem strands in other species, such as the
eight genera of Thymeleaceae (some trees:
Aquilaria) that have interxylary phloem.
We do know that secondary phloem is
active in earlier increments of species with
successive cambia (Carlquist, 2007). Anatomical studies show that each vascular
cambium continues indefinitely to produce
secondary phloem—eventually ceasing activity in older parts of larger stems.
Reports of sustained longevity of secondary xylem, related to capability to reverse
embolisms (e.g., Sperry, 1985), is indirect
evidence of prolonged phloem function.
Functioning of phloem without simultaneous
functioning of adjacent vessels (or tracheids)
is unlikely: The two are probably correlated
(although studies of this are lacking).
(e) Phloem pathway three-dimensionalization. Strands of interxylary phloem are an
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CARLQUIST: INTERXYLARY PHLOEM
ideal way of dispersing phloem throughout a
stem or root as a means of aiding storage and
retrieval of photosynthates. Validation of this
speculation can be found in the examples,
cited above for Brassicaceae and Solanaceae,
in which interxylary phloem occurs in roots
but is apparently absent in stems of particular
species. Similar hypotheses were entertained
with respect to successive cambia, which are
also an ideal mechanism for distributing
xylem and phloem throughout a stem or root,
as in the beet, Beta (Carlquist, 2007).
(f) Phloem pathway protection. Interxylary
phloem strands are often ideally protected by
their location within a fibrous background. That
such fibrous backgrounds function in maintaining or prolonging safety of the strands has not
been tested, although simple experiments incising bark to see whether interxylary phloem
suffices for conductive needs would be easy to
do. The evidence of placement and multiplicity
suggests possible isolation from phytophagous
insects and possibly other influences. The
abundance of crystals in parenchyma sheaths
of interxylary phloem strands in Acanthaceae
(Thunbergia), Combretaceae (Combretum),
Onagraceae (all genera with interxylary phloem), and Thymeleaceae (Craterosiphon) seems
like an indirect evidence of predation deterrence.
(g) Lianoid correlations and other habit
considerations. The proportion of genera and
species with interxylary phloem that has a
lianoid habit is much higher than one would
expect on the basis of the frequency of lianas
and vines in eudicots as a whole. Families
(and pertinent genera) in this regard include
Acanthaceae (Thunbergia), asclepioid Apocynaceae (Asclepias, Ceropegia, Leptadenia),
Combretaceae (several genera), Convolvulaceae (Ipomoea, Turbina), Cucurbitaceae
(Cucurbita, Lagenaria), Icacinaceae (several
genera), Malpighiaceae (several genera), and
Thymeleaceae (Craterosiphon).
Histologically similar phenomena (e.g.,
successive cambia) are also represented in a
larger than expected number of lianoid genera
(Carlquist, 1988, 2001, 2007). These constructions include intraxylary phloem, bicollateral bundles, successive cambia, and
secondary xylem dispersed by parenchyma
proliferation (e.g., Bauhinia, Mendoncia), as
shown by the listings in appendices of
Metcalfe and Chalk (1950, 1983).
The parenchyma sheathing of phloem
strands is conspicuous in many instances
of interxylary phloem, such as Thunbergia
(Acanthaceae) and Craterosiphon (Thymeleaceae) in the present study. These suggest enhanced flexibility, a feature ascribed
to parenchyma of lianas by Schenck
(1895). In these examples, interxylary
phloem and parenchyma presence is less
in earlier-formed wood, then increases with
age, suggesting parenchyma becomes more
important as self-support decreases and
response to torsion and displacement of stems
increases.
A relatively small number of tree species
have interxylary phloem, but there are some
notable instances of interxylary phloem occurrence in tree Loganiaceae (Mennega,
1980) and Thymeleaceae (Pfeiffer, 1926).
Examples should be examined on the basis
of individual species, rather than strictly
grouped according to habit.
(h) Longevity and other physiological phenomena. Many fascinating questions regarding interxylary phloem occurrence remain to
be asked and answered. Among these is the
longevity of interxylary phloem. Circumstantial evidence may be obtainable from whether
or not secondary xylem of a range of ages in
a given stem is functional or not, but phloem
itself tends to be good evidence, because it
collapses so readily if it no longer functions
(e.g., Salvadora, Fig. 6). Correlations between longevity of functioning in phloem
and that in xylem vessels are to be expected.
Phloem longevity is generally thought to be
only a year or two, but greater longevity has
been demonstrated in some angiosperms
(Parthasarathy 1980).
Acknowledgments
For providing material, thanks are due Dr.
David Lorence for stems of Strychnos madagascariensis (National Tropical Botanical Garden), Dr. Peter H. Raven of the Missouri
Botanic Garden for stems of various Onagraceae, and the University of California of
California at Santa Barbara living greenhouse
collections for material of Salvadora. John
Bleck provided seeds of Orphium frutescens
from which my specimens were cultivated.
Mark Olson and Edward L. Schneider provided
Author's personal copy
BRITTONIA
helpful suggestions. Use of laboratory facilities,
including the SEM, at Santa Barbara Botanic
Garden, is gratefully acknowledged.
Literature Cited
Adamson, R. S. 1934. Anomalous secondary thickening
in Compositae. Annals of Botany 48: 505–514.
Bonsen, K. J. & B. J. H. ter Welle. 1984. Systematic
wood anatomy of the Urticaceae. Botanisches Jarhbuch Systematik 105: 49–71.
Carlquist, S. 1958. Wood anatomy of Heliantheae
(Compositae). Tropical Woods 108: 1–30.
———. 1961. Comparative plant anatomy. Holt, Rinehart & Winston, New York.
———. 1962. A theory of paedomorphosis in dicotyledonous woods. Phytomorphology 12: 30–45.
———. 1975. Wood anatomy of Onagraceae, with notes
on alternative modes of photosynthate movement in
dicotyledon woods. Annals of the Missouri Botanical
Garden 62: 386–424.
———. 1977. Wood anatomy of Onagraceae: additional
species and concepts. Annals of the Missouri Botanical Garden 64: 627–637.
———. 1981. Types of cambial activity and wood
anatomy in Stylidium (Stylidiaceae). American Journal of Botany 68: 778–785.
———. 1983. Wood anatomy of Onagraceae; Further
species; root anatomy; significance of vestured pits
and other structures in the dicotyledons. Annals of the
Missouri Botanical Garden 69: 755–769.
———. 1984. Wood anatomy of some Gentianaceae:
systematic and ecological conclusions. Aliso 120:
573–582.
———. 1987. Wood anatomy of noteworthy species of
Ludwigia (Onagraceae) with relation to ecology and
systematics. Annals of the Missouri Botanical Garden75: 889–896.
———. 1988. Comparative wood anatomy, ed. 1.
Springer Verlag, Berlin & Heidelberg.
———. 1992. Wood anatomy of selected Cucurbitaceae
and its relationship to habit and systematics. Nordic
Journal of Botany 12: 347–355.
———. 2001. Comparative wood antomy, ed. 2.
Springer Verlag, Berlin & Heidelberg.
———. 2002. Wood and bark anatomy of Salvadoraceae: ecology, relationships, histology of interxylary
phloem. Journal of the Torrey Botanical Society 129:
10–20.
———. 2007. Successive cambia revisited: ontogeny,
histology, diversity, and functional significance. Journal of the Torrey Botanical Society 134: 301–332.
———. 2009. Xylem heterochrony: an unappreciated
key to angiosperm origins and diversification. Botanical Journal of the Linnean Society 161: 26–65.
———. 2012. How wood evolves: a new synthesis.
Botany 90: 901–140.
——— & M. A. Hanson. 1991. Wood anatomy of
Convolvulaceae: a survey. Aliso 13: 51–94.
——— & S. Zona. 1988 Wood anatomy of Acanthaceae: a survey. Aliso 12: 201–227.
[VOL
Chalk, L. & M. M. Chattaway. 1937. Identification of
woods with included phloem. Tropical Woods 50: 1–31.
den Outer, R. W. & W. L. M. van Veenendaal. 1995.
Development of included phloem in the stem of
Combretum nigricans (Combretaceae). IAWA Journal
16: 151–158.
Gin, A. 1909. Réchérches sur les Lythracées, Travaux del
la Laboratoire des Materiels Medicaux, Paris 6:1–166.
IAWA Committee. 1989. List of microscopic features
for hardwood identification. IAWA Bulletin, new
series, 10: 219–882.
Leeuwenberg, A. J. M., ed. 1980. Angiospermae:
Ordnung Gentianales Fam. Loganiaceae. Die natürlichen Pflanzefamilien Band 28BI: 1–155. Ducker &
Humblot, Berlin.
Leisering, B. 1899. Über die Entwicklungeschichte des
interxylären Leptoms bei den Dicotyledonen. Thesis,
Berlin.
Lens, F, J. Kårehed, P. Baas, S. Jansen, D. Rabaey, S.
Huysmans, T. Hamann & E. Smets. 2008. The
wood anatomy of the polyphyletic Icacinaceae s. l.,
and their relationships within asterids. Taxon 57:
525–552.
Mennega, A. 1980. Anatomy of the secondary xylem. In
A. J. M. Leeuwenberg, ed. Angiospermae: Ordnung
Gentianales Fam. Loganiaceae. Die natürlichen Pflanzenfamilien Band 28BI. Duncker & Humblot, Berlin.(pp. 112—161.
Metcalfe, C. R., & L. Chalk. 1983. Anatomy of the
dicotyledons. Clarendon Press, Oxford.
——— & ———. 1983. Anatomy of the dicotyledons,
ed. 2. Vol. 2. Wood structure and conclusion of the
general introduction. Clarendon Press, Oxford.
Parthasarathy, M. V. 1980. Mature phloem of perennial
monocotyledons. Berichte der deutschen botanischen
Gesellschaft 93: 57–70.
Patil, V. S. & K. S. Rajput. 2008. Structure and
development of inter- and intraxylary phloem in
Leptadenia reticulata (Asclepiadaceae). Polish Botanical Journal 53: 5–13.
Patil, V. S., C. R. Marcati & K. S. Rajput. 2011,
Development of intra- and interxylary secondary
phloem in Coccinia indica (Cucurbitaceae). IAWA
Journal 32: 475–491.
Pfeiffer, H. 1926. Das abnorme Dickenwachstum.
Handbuch der Pflanzenanatomie 2 Abteilung 2 Teil,
9: 1–243. Gebrüder Borntraeger, Berlin.
Rajput, K. S., V. S. Patil & K. S. Rao. 2009.
Development of included phloem of Calycopteris
floribunda Lamk. (Combretaceae). Journal of the
Torrey Botanical Society 136: 302–312.
Schenck, H. 1893. Beiträge zur Biologie und Anatomie
der Lianen in Besonderen der in Brasilien einheimsche Arten. 2. Beiträge zur Anatomie der Lianen. In
A. F. W. Schimper, ed. Botanische Mittheilungen der
Tropens (pp. 1–271). G. Fischer, Jena.
Scott, D. H. 1891. On some points in the anatomy of Ipomoea
versicolor Meissn. Annals of Botany 5: 173–180.
Scott, D. H. & G. Brebner. 1889. On the anatomy and
histology of Strychnos. Annals of Botany 3: 275–
302.
Singh, B. 1943. The origin and distribution of inter- and
intraxylary phloem in Leptadenia. Proceedings: Plant
Sciences 18: 14–19.
Author's personal copy
2013]
CARLQUIST: INTERXYLARY PHLOEM
Solereder, H. 1908. Systematic anatomy of the dicotyledons (trans. Boodle & Fritsch). Clarendon Press,
Oxford.
Sperry, J. S. 1985. Xylem embolism in the palm Rhapis
excelsa. IAWA Bulletin, new series 6: 283–292.
Van Veenendaal, W. L. H., & R. W. den Outer.
1993. Development of included phloem and organiza-
tion of the phloem network in the stem of Strychnos
millepunctata (Loganiaceae). IAWA Journal 14: 253–
265.
Van Vliet, G. J. C. M. 1979. Wood anatomy of the
Combretaceae. Blumea 25: 141–223.
Weiss, J. E. 1880. Anatomie und Physiologie der
fleischig verdickter Wurzeln. Flora 70: 81–119.