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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1 23 Author's personal copy

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 Chalk and Chattaway (1937), but used also for sieve tubes, companion cells, and adjacent instances of interxylary phloem. Misapplica- parenchyma or other cells embedded within tions of this sort render the term included the secondary xylem of a stem or root that has phloem imprecise, and, in any case, are based a single vascular cambium. This definition is on topographic phloem distribution without presented to distinguish interxylary phloem regard to ontogenetic factors. The ontogeny of from a series of other histological phenomena phloem and xylem within various cambia that may have similar functions but are variants can be easily determined from the histologically and ontogenetically different. For mature histology, and thus can readily be example, the term successive cambia denotes a includedindefinitions of cambial variants. The series of vascular increments, each with second- term "included" suggests that the phloem in ary phloem, secondary xylem, and a vascular instances of successive cambia is embedded cambium, each of which ultimately originates within secondary xylem (as it is in the case of from the master cambium at the periphery of a interxylary phloem). In fact, the phloem in stem or root (Carlquist, 2007). The master examples of successive cambia lies between cambium produces secondary cortex (0 paren- secondary xylem (internal to it) and conjunctive chyma) to the outside, and to the inside, tissue (external to it) in each vascular increment. conjunctive tissue and vascular cambia to the The term internal phloem has likewise been inside of an axis. Each vascular cambium then contaminated by conflicting usages and should produces secondary phloem to the outside and be rejected. "Internal phloem" has been used to secondary xylem to the inside. The term refer to intraxylary phloem, but has been included phloem was misapplied to successive applied to other histological conditions. Signif- cambia in some (but not all) Nyctaginaceae by icantly, like "included" phloem, the term

BRITTONIA [VOL internal phloem is vague with respect to materials and methods used in those studies are ontogeny as well as location of phloem. given in the papers listed below. In all cases, Intraxylary phloem, although readily dis- however, the photographs and observations are tinguishable from interxylary phloem, may new. Re-studied materials include the following: have a similar physiological significance and Figure 1: Turbina stenosiphon (Hallier f.) is covered in a later section of this paper. The A. Meeuse (Convolvulaceae): Carlquist and present usages are consistent with those Hanson, 1991. adopted in earlier accounts of cambial var- Figure 2A–C: Thunbergia laurifolia Lindl. iants (Carlquist, 1988, 2001, 2007). For the (Acanthaceae): Carlquist and Zona, 1988 present, workers would be well advised to Figure 2D: Stylidium glandulosum Salisb. define the terms they use for cambial variants. (Stylidiaceae): Carlquist, 1981 Interpretation of functions of interxylary Figure 4: Pseudolopezia longiflora Rose phloem is further complicated by the fact that and Oenothera linifolia Nutt. (Onagraceae): in woody angiosperms as a whole, interxylary Carlquist, 1975. phloem occurs in only a relatively small Figure 6: Salvadora persica L.(Salvador- number of families and species. Even within aceae): Carlquist, 2002. a genus such as Combretum or Strychnos, Sources for material not previously studied some species have interxylary phloem, others are as follows: lack it, with no clear differences in habit or Figure 3: Orphium frutescens E. Mey. size of plant (van Vliet, 1979; Mennega, (Gentianaceae): Carlquist 8212, June 28, 1980). However, there is some correlation 2011 (SBBG). with systematic units within genera such as Figure 5: Craterosiphon scandens Eng. & these (van Vliet, 1979; Mennega, 1980). Gilg (Thymeleaceae): Breteler 1227 (WAG). – There is no unique function for interxylary Figure 7A B. Strychnos madagascariensis phloem; other phloem distributions seem to be Poir. (Loganiaceae): David Lorence 10285 adequate alternates. That does not mean, (PTBG), National Tropical Botanical Garden however, that interxylary phloem is not a living collections accession number 801348. – physiologically significant way of meeting a Figure 7C D. Combretum erythrophyllum plant's photosynthate conduction requirements. Sond. (Combretaceae): cultivated in the Wood anatomy contains many examples of Vavra Garden (formerly owned by University alternative ways of serving particular functions of California, Los Angeles). – (e.g., vestured pits, helical sculpture of vessel The sections in Figs. 3 and 7C D were surfaces, and vasicentric tracheids are probably derived from living material that was pre- all methods of minimizing embolism formation served in 50 % aqueous ethanol, sectioned on —or reversing that). Interxylary phloem, like a sliding microtome, and stained with a vestured pits, is a device that is homoplastic in Safranin-Fast Green combination. The section – woody angiosperms. In both instances, genetic in Fig. 7A B was derived from living information for the formation of these struc- material that was preserved in aqueous 50 % tures has not been frequently achieved phylo- ethanol. The sections were prepared by driving genetically, perhaps because a complex series a single-edged razor blade into a stem with the of genetic changes is required. The data aid of a hammer. The sections derived were presented here may offer interesting examples subjected to changes of distilled water, and that lend themselves to physiological studies. dried between glass slides under pressure (to Plant physiological studies have traditionally prevent curling), then sputter-coated with gold been done on economically important plants, and examined with a Hitachi S2600N scanning and none of the species with interxylary phloem electron microscope (SEM). has any major economic value. Aspects of Interxylary Phloem 1. Ontogenetic and Histological Criteria; Materials and methods Allied Phenomena. Some of the examples cited here are derived Because secondary xylem consists mostly from earlier wood anatomical surveys. The of cells with rigid walls, it is a clear and Author's personal copy

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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 the location and sequences of cell types with cambium. The products of cambial action are secondary walls (which are readily seen in unambiguous, so that there is no need to sections of xylarium specimens) are quite develop definitions that exclude ontogenetic sufficient to permit any appearance to be aspects and are merely topographic in their referred to one of the categories accepted here. frame of reference (e.g., included phloem). To The difference between interxylary phloem be sure, xylarium specimens have poor preser- and successive cambia can be seen in Turbina vation of meristematic cells and of phloem, but stenosiphon (Fig. 1A–C)oftheConvolvula- Author's personal copy

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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, Successive cambia are increments of secondary in which both successive cambia (Fig. 1A–B) xylem and phloem, each produced by a and interxylary phloem (Fig. 1C) have been vascular cambium. The cambia, as well as shown to coexist in a single stem. Interestingly, conjunctive tissue and secondary cortex (0 a third phenomenon, intraxylary phloem, is also parenchyma) are produced by a master cambi- represented in Turbina stenosiphon (Fig. 1D). um (Carlquist, 2007). Conjunctive tissue is not Author's personal copy

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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 inverted orientation. This occurrence does is produced only by a vascular cambium. The underline the fact that occasionally one does example illustrated here, Turbina stenosiphon, see a cambial variant with atypical ontog- is unusual in having one vascular increment eny. At the same time, the rarity of such inverted in orientation, with that vascular occurrences reinforces the regularity of cambium producing phloem internally and phenomena described by the definitions xylem externally. This is the only instance I given: cambial variants are orderly, and know in which a vascular increment has this not "anomalous." Author's personal copy

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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 Intraxylary phloem is also present in Turbina stenosiphon (Fig. 1C) exempliﬁes all Turbina stenosiphon (Fig. 1D). Intraxylary of the features claimed by the deﬁnition. It is phloem occurs at the adaxial tips of vascular a strand of sieve tube elements and compan- bundles of a number of woody angiosperms ion cells surrounded by a sheath of paren- (for a list, see Metcalfe and Chalk, 1983, chyma. Because the parenchyma is formed by appendix). Cambial activity is found in a a vascular cambium, it can be termed axial minority of instances of intraxylary phloem, parenchyma. and there is no list of genera in which it is Author's personal copy

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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 has been figured in Operculina (Carlquist & illustrated in Fig. 1D. Where present, cambi- Hanson 1991; Carlquist, 2012,). um in intraxylary phloem acts unidirectional- Bicollateral bundle is a term that denotes ly, producing secondary phloem adaxially phloem at both the abaxial and adaxial rather than (as with an ordinary vascular surfaces of a bundle (as opposed to a cambium) abaxially. Secondary xylem is collateral bundle, which has phloem only produced by this cambium only rarely, but abaxially). Although the term does not spe- Author's personal copy

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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 growth in the bundle, as in Cucurbita or xylem in such a bundle, it is more commonly Solanum (Lycopersicon). Thus, there is an applied when there is little or no secondary overlap with the term "intraxylary phloem." Author's personal copy

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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 Strands of interxylary phloem are most Interxylary Phloem. commonly strands of axial parenchyma in Author's personal copy

BRITTONIA [VOL which there is a central core of sieve tube In Fig. 3D and E, instances in which elements and companion cells. This is most portions of rays have been converted to sieve easily seen in Thunbergia (Fig. 2A–C). Thun- tube elements and companion cells are shown bergia is a vine and the diameter of the sieve (r 0 rays). One should note that ray cells in tubes is larger than in the average nonvining Orphium are predominantly upright, as one eudicot. In longisections, one can see sieve would expect from a secondarily woody plant plates in the strands of interxylary phloem (Carlquist, 1962, 2009), so conversion of ray (Fig. 2C). The fibrous xylem consists of non- cells to sieve tube elements and companion septate libriform fibers (Fig. 2C,fx).Thunber- cells is really not contrary to the expected gia is rayless, so all of the thin-walled paren- direction of conduction. If one scans larger chyma seen in Fig. 2A–C is axial parenchyma. areas of Orphium wood transections, one sees Parenchyma associated with interxylary phloem that interxylary phloem occurs as either is transversely subdivided into strands, much strands or bands (Fig. 3A, B). The ratio of like axial parenchyma in typically woody bands that contain sieve tube elements and eudicots. Axial parenchyma in Thunbergia companion cells in ray areas to those that do separates bands and strands of vessel-containing not is perhaps only one band out of twenty. fibers (Fig. 2A, B), which occasionally break (Fig. 2C, br) in response to stem growth and 4. Diversity in Patterns: Strands, Bands, torsion. Axial parenchyma in Thunbergia thus Relative Abundance. serves a mechanical function that can often be Interxylary phloem is usually seen as cylin- served by wide rays in scandent woody plants. drical strands (Figs. 1C and 2B). These strands Stylidium glandulosum (Fig. 2D), a sub- can range from inconspicuous and few celled, shrub, also has rayless wood. The strands of as in Stylidium, to large and obvious, even interxylary phloem (arrows) consist of little perceptible without microscopy, as in Strychnos more than a sieve tube element plus a compan- (Fig. 7A)andCombretum (Fig. 7C, D). ion cell each, and are quite inconspicuous. An Interxylary phloem is often present in the form occasional axial parenchyma cell is present in of tangential bands (Figs. 4A and 5A.Bands these strands. Stylidium and Thunbergia form and strands may occur together. extremes with respect to quantity of parenchy- Salvadora (Fig. 6) appears to have bands ma associated with phloem. rather than cylindrical strands of interxylary Intermediate quantities of parenchyma char- phloem (e.g., Fig. 6C) because the parenchyma acterize the strands of most species that have surrounding the strands occurs as tangential interxylary phloem (Figs. 3A–E, 4A and 6C–E). bands (Fig. 6A, B). Salvadora exemplifies the The varied quantities of parenchyma observed point that parenchyma may be much more in strands of interxylary phloem may be keyed abundant in transectional area than the strands to diverse physiological functions, but there has of phloem in embedded in the parenchyma. been no experimental work on this topic. 5. Cell Contents: Crystals, Starch, etc. 3. Rays and Interxylary Phloem. Crystals occur in parenchyma that sheathes By implication, interxylary phloem occurs phloem in a large number of the species that as vertical strands in axial xylem. This is have interxylary phloem. Exceptions can be clearly demonstrated by most species (e.g., cited in the case of Stylidium (Fig. 2D) Thunbergia, Fig. 2A–C). In most species that Orphium (Fig. 3) and Salvadora (Fig. 6). have interxylary phloem, rays either do not Although not shown here, prismatic crys- cross strands of interxylary phloem (Fig. 6A– tals occur in the axial parenchyma bands that E) or if they do (Fig. 5A–B), The ray cells contain phloem in stems of Thunbergia alata retain their typical histological characteristics. Bojer ex Sims (Carlquist and Zona, 1988; Orphium (Fig. 3) provides some examples of Carlquist, 2001). Raphides are present in such this latter condition, but it also, in a few parenchyma in Onagraceae (Carlquist, 1975). places, forms sieve tube elements and com- Crystal sand is present in axial parenchyma of panion cells in rays. In Fig. 3C, instances of interxylary phloem strands in Craterosiphon typical interxylary phloem strands that do not (Fig. 5C; SEM photos in Carlquist, 2001). intersect rays are shown. Druses occur in the phloem-ensheathing paren- Author's personal copy

2013] CARLQUIST: INTERXYLARY PHLOEM chyma of Combretum (Fig. 7C–D, cpa). The had just begun. In other Salvadoraceae, such as positioning of druses in interxylary phloem- Dobera (Carlquist, 2002)andSalvadora adjacent parenchyma in Combretum as well as (Fig. 6), interxylary phloem production begins in cases of crystal occurrence in other genera early and remains constant in abundance. listed in the present study suggests that Mennega (1980) in her study of wood of crystal-bearing sheaths may deter predation Strychnos and other Loganiaceae mentions of interxylary phloem by chewing beetles. that interxylary phloem has not been reported Such positioning of crystals is often seen in some species (cf. Pfeiffer, 1926) in which in relation to phloem in bark of many only small diameter stems were available, woody species. whereas larger-diameter stems prove to have In woods of Onagraceae, starch is common interxylary phloem. in libriform fibers adjacent to strands of An apparent exception to this trend interxylary phloem (Fig. 4A–B, srf; Carlquist, occurs in Oenothera linifolia,inwhich 1975). However, starch is notably absent in interxylary phloem strands are fewer and the parenchyma sheathing the phloem strands smaller in second-year wood of stems in that family (Fig. 4A–B). This circumstance (Fig. 4D) as compared to first-year wood suggests that starch storage and active trans- (Fig. 4C). The occurrence of this trend is port of soluble photosynthates are distinct somewhat masked by the fact that in first- functions performed by these two respective year wood, parenchyma cells of the strands tissues. enlarge and develop secondary walls after the collapse of sieve tube elements and 6. Libriform Cells in Interxylary Phloem. companion cells. Because the root word "liber" refers to Pfeiffer (1926), following Schenck (1895) phloem, sieve tube elements (and their asso- reports sieve tube elements in secondary ciated companion cells) could be included as xylem of Mucuna altissima DC. as a late or "libriform elements" but that is not usually subsequent (nachträglich) development done. "Libriform" implies an elongated form, compared with maturation of other cell and usually refers to fibers. Certainly sieve- types nearby. tube elements in Craterisiphon are elongate, their length easily determined from presence 8. Comparison between Interxylary Phloem of sieve plates (Fig. 5D). Curiously, however, and Secondary Phloem in a Single Stem. extraxylary fibers mature in the interxylary Comparisons of this sort are lacking, pre- phloem bands of Craterisiphon (Fig. 5B, C). sumably because dried material rather than These fibers are gelatinous, and in permanent liquid-preserved material has been studied, slides, the secondary walls shrink away from and because soft tissues do not survive sliding the primary walls (Fig. 5C). The fibers are microtome sectioning as well as harder (fi- instrusive, and their tips (Fig. 5D, f) do not brous) tissues. The question that arises in align with the sieve plates of the sieve tube connection with comparison of these two elements, which are shorter than the fibers. phloem regions within a given stem is whether in stems that have interxylary phloem, sieve 7. Timing of Interxylary Phloem Onset. tube elements are less abundant in secondary Presence of interxylary phloem may change phloem (outside the vascular cambium) than in in abundance with age of stem. This is evident stems that lack interxylary phloem. The answer in Fig. 5A for Craterisiphon.Inthisstem, to this question, based on a small sample, is yes, interxylary phloem is absent in earlier-formed although variability is evident. Whether bark secondary xylem. This has been reported in thickness relates to distribution of sieve tube other species, such as Azima tetracantha Lam. elements in interxylary phloem vs. secondary of the Salvadoraceae. Den Outer and van (0 external, or bark) secondary phloem is not Veenendaal (1995) describe interxylary phloem known, and needs investigation. strands throughout the stem of this species. The most notable example is found in Their stem was larger in diameter than the one I Stylidium species that have secondary growth studied (Carlquist, 2002); at the periphery of the (most species of the genus lack secondary stem I studied, interxylary phloem production growth). Stylidium glandulosum (Fig. 2D) Author's personal copy

BRITTONIA [VOL produces at most one layer of cells external to and the impreciseness of the term "secondary the vascular cambium, and the cells of that interxylary bundles" underlines the need for layer are best described as parenchyma. more extensive studies not merely to confirm These cells are not radially aligned with the the histological nature of these instances, but to innermost cortical parenchyma layer, in determine the ontogenetic origin of these which phellogen develops (Fig. 2D,pg). "bundles" or "islands." The lack of reports of Thus, there is no true secondary phloem, such appearances in the stems of Brassicaceae and no sieve tubes external to the cambium. is, however, notable in this regard. This was reported, although not thoroughly Pfeiffer (1926) assigned histological illustrated, earlier (Carlquist, 1981). appearances in the roots of Scolopia atro- Orphium (Fig. 3A)andPseudolopezia poides Bercht. & Presl (Solanaceae) to the (Fig. 4B) show a relative paucity of sieve tubes concept of interxylary phloem. He likewise and companion cells in secondary phloem. referred similar vascular tissue in roots of Relatively extensive areas of secondary phloem Browallia viscosa HBK. (Solanaceae) to this consist exclusively of phloem parenchyma, category. Pfeiffer (1926) also reproduces a with only a few, isolated strands of sieve tube believable drawing of interxylary phloem in elements and companion cells present. thin-walled root secondary xylem of Atropa Some degree of variability occurs in Salva- belladonna L. (Solanaceae) by Leisering dora (Fig. 6). In some areas of secondary (1899), so there is reason to credit his concept phloem, sieve tube elements and companion of interxylary phloem in that species as the cells are relatively sparse (Fig. 6A–B), whereas same as mine. Stem interxylary phloem has in others, they are rather more common not been reported in Atropa. Pfeiffer (1926) (Fig. 6C). As a generalization, however, Salva- reports interxylary phloem for roots of Ipo- dora—as well as the other interxylary-phloem- moea versicolor Meissn. (Convolvulaceae), bearing eudicots for which data are reviewed but does not note it in stems of this species. here—have fewer sieve tube elements and There are obviously many residual oppor- companion cells in secondary phloem (bark) tunities for confirmation or reassignment into than is typically observed in eudicots that lack other catergories of interxylary phloem interxylary phloem. reports. New discoveries remain to be made, as in Turbina stenosiphon (Fig. 1C). The 9. Organographic Distribution. material available to earlier workers was limited, Work in wood anatomy remains biased and often was biased in favor of plants which toward stems, for understandable reasons. In were naturally-occurring or grown in Europe, fact, so few xylarium specimens are of root and in favor of stems rather than roots of those. material that no indication of site of origin on the plant is given on most specimens; the 10. Cambial Activity within Interxylary default assumption is that stem material is Phloem. involved. (Whether the material comes from Scott and Brebner (1889) described devel- main stem or branches is likewise never opment of cambial activity in the interxylary indicated on xylarium labels). phloem strands of Strychnos, based upon Some workers have mentioned interxylary living material cultivated in greenhouses. phloem in roots or rhizomes. For example, Scott and Brebner figured large strands of Pfeiffer (1926) reports interxylary phloem interxylary phloem much like the one figured "islands" (interxylären Inseln) in transections here (Fig. 7A, B). They reported crushed of roots and rhizomes of Cochlearia armor- phloem on the abaxial side of the strands with acia L., Brassica napus L., B. rapa L., and cambial activity, so that the cambia in these Raphanus sativus L. Metcalfe and Chalk strands produces secondary phloem external- (1950), citing Pfeiffer's (1926) reports, men- ly, thereby in the same direction as the tioned "secondary interxylary bundles" in the vascular cambium. This activity agrees with unlignified xylem of the rhizomes of Armor- the findings reported here (Fig. 7A, B). acia lapathifolia Gileb. and in the root of Despite the disadvantage of working with Brassica napus, B. rapa, and Raphanus herbarium material, Mennega (1980) reported sativus. The overlapping nature of these reports the above facts accurately in a survey of Author's personal copy

2013] CARLQUIST: INTERXYLARY PHLOEM woods of Strychnos (and other Loganiaceae). Salvadora persica (Fig. 6C,bottom,ip)there As Mennega (1980) stated, not all species of are only sieve tube elements and companion Strychnos have interxylary phloem in the cells that have been derived from the vascular stems, even when large-diameter stems are cambium. Crushed phloem and cambial activity examined. A study devoted to one species, S. within younger strands is not observed, contrary millepunctata Leeuwenberg (van Veenendaal to the conditions in Combretum and Strychnos. & den Outer, 1993) includes some excellent In moderately old interxylary phloem SEM images that reinforce the findings of strands of Salvadora, no radial seriation of Scott and Brebner (1889). cells is evident (Fig. 6D). Cambial activity Note should be taken that cambial activity (arrows) is minimal. Some collapsed phloem in the interxylary phloem strand begins soon (Fig. 6D, cip) is evident, but the accumulation after a strand is produced by the vascular is not prominent. Earlier formed (older) cambium. Cambial action is evident from the interxylary phloem strands show a greater radial seriation of the cells produced by the amount of crushed phloem (Fig. 6E). interxylary phloem cambium (Fig. 7B, np). There is a correlation between size of The earlier-formed interxylary phloem cells interxylary phloem strands and presence of may not show radial seriation (Fig. 7B, op). cambial action within these strands, when one The amount of secondary phloem produced by compares the interxylary phloem of Combreta- cambial activity within a strand is evident from ceae, Loganiaceae, and Salvadoraceae to that of the quantity of radially seriate phloem cells in other families. These families are woody, the phloem as well as the amount of crushed ranging from shrubs to trees, and preservation phloem on the abaxial side of the strand. Bark of phloic pathways by means of active replace- of Strychnos (Fig. 7A, top) is relatively poor in ment of sieve tube elements and companion sieve tube element production. cells by cambial activity within the strands Large interxylary phloem strands occur in seems a strategy that is correlated with habit. the African species of Combretum of the Combretaceae (van Vliet, 1979), but not all of 11. Relationship between Intraxylary Phloem them. Histological and ontogenetic details and Interxylary Phloem. given to date are relatively few because most The present study endorses the term intra- specimens studied are from herbarium mate- xylary phloem to refer to phloem strands that rial or xylarium blocks. Somewhat thick occur adjacent to protoxylem, at margins of sliding microtome sections of liquid-pre- the pith. This term does not equate entirely to served material presented here (Fig. 7C, D) the term "bicollateral bundle" (see “Aspects illustrate that Combretum interxylary phloem of Interxylary Phloem”, section 1), in which strands are histologically similar to those in minimal accumulation of secondary xylem is Strychnos and like them in the timing of implied. Approximately equal amounts of cambial initiation within the strand. Strands phloem are seen external and internal to the close to the vascular cambium (Fig. 7C) xylem in species with bicollateral bundles, already show the beginning of cambial whereas in instances referred to the concept activity on the adaxial side of the strand. of intraxylary phloem, the amount of phloem Older strands (Fig. 7D) show crushed phloem formed externally from the vascular cambium (cp) conspicuously, and a continuation of can be relatively large, whereas the intra- cambial activity within the strands. Interxy- xylary phloem strands are relatively finite in lary phloem strands in Combretum are com- size. Because of the uneasy coexistence of posed of fibriform (Fig. 7C, fp) cells (when these terms, listings of families that exemplify seen in longisection) and crystalliferous pa- one or the other concept have not always been renchyma cells (cpa) that contain druses. assembled based on critical review of material. Cambial activity is reported here in the In addition, misapplication of these terms interxylary phloem strands of one other family, creates problems. Pfeiffer (1926) cited instan- Salvadoraceae, although attention has not hith- ces of phloic strands in the pith, for example. erto been called to this phenomenon (Carlquist, One can, however, cite particular families 2002), presumably because it is so inconspicu- and genera in which intraxylary phloem is ous. In young strands of interxylary phloem of characteristically present. Metcalfe and Chalk Author's personal copy

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(appendices, 1950, 1983) presented such lists. sites is also indicated by the fact that in a few In their listings, Metcalfe and Chalk distin- species, the intraxylary phloem cambium also guished between families that characteristi- produces some secondary xylem (in an cally have intraxylary phloem (bold face) and external, or abaxial, direction). This has been those in which intraxylary phloem is occa- illustrated for Operculina palmeri (Wats.) sionally reported (ordinary font) or infrequent Howe of the Convolvulaceae (Carlquist & or perhaps dubious (italics). The families of Hanson 1991; Carlquist 2012,). Myrtales figure prominently in the list (Combretaceae, Crypteroniaceae, Lythraceae, 12. Systematic Occurrence of Interxylary Melastomataceae, Myrtaceae, Oliniaceae, Phloem. Onagraceae, Penaeaceae, and Punicaceae). As noted above, understanding the system- Interestingly, interxylary phloem also occurs atic occurrence of interxylary phloem is a in an appreciable number of species in three work in progress. Several reports must be of these families (Combretaceae, Melastoma- regarded as tentative, while others are likely taceae, and Onagraceae). A similar link incorrect. The latter are difficult to prove between intraxylary phloem presence and definitively, because interxylary phloem may interxylary phloem occurrence can be cited occur infrequently in a few species. The late for other families in the Metcalfe and Chalk onset of interxylary phloem production, men- (1950) list (Gentianaceae, Loganiaceae, Styl- tioned for Azima and Strychnos, is another idiaceae, and Thymeleaceae) as well as reason to be cautious where lists are Leptadenia, an asclepioid genus of Apocyna- concerned. The multiplicity of individuals ceae (Singh, 1943; Patil & Rajput, 2008). who report instances of interxylary phloem Thus, intraxylary phloem may be a kind of results in variable criteria and thus lack of "precursor" for interxylary phloem formation precision in application of the concept. in a given species. In developmental terms, The following list contains instances that the genetic information for the formation of appear well substantiated on the basis of strands of phloem within the xylem (interxy- supporting drawings or photographs. Earlier lary) as well as internal to (adaxial to) the xylem workers occasionally conflated interxylary (intraxylary) may be similar. Exceptions to this phloem (formed from a single vascular concept can certainly be listed (e.g., Salvador- cambium) with instances of successive cam- aceae lack intraxylary phloem), and this theory bia under the inclusive rubric "included may apply only in particular clades. phloem." That vague umbrella usage was The physiological implications of this followed by IAWA Committee (1989). connection between the two sites of phloem Instances of successive cambia are not information are, however, even more interest- cluded in this list. The listing is similar to that ing. In, say, Myrtales, why do only some of presented earlier (Carlquist, 2001), but with the species that have intraxylary phloem go some emendations. Following this list, a on to produce interxylary phloem? compilation of dubious, incorrect, or unusual One of the most interesting aspects of instances that do not conform to the working interxylary phloem is the development of a definition of interxylary phloem. cambium in intraxylary phloem in some Apocynaceae (including Aslepiadaceae): instances. This is illustrated for Turbina Asclepias, Ceropegia, Leptadenia (Singh, stenosiphon (Fig. 1D), but occurs in other 1943; Patil & Rajput, 2008). eudicots, such as Cucurbitaceae (Carlquist, Brassicaceae: roots and rhizomes of Bras- 1992; Patil et al., 2011). sica spp., Cochlearia,andRaphanus When cambium develops within a strand of (Pfeiffer, 1926). intraxylary phloem, the secondary phloem it Combretaceae: Calycopteris, Combretum, yields is always produced toward the center Guiera, Thiloa (van Vliet, 1979; den Outer & of the stem, rather than toward the outside van Veenendaal, 1995; Rajput et al., 2009). (the latter, of course, is what happens in the Convolvulaceae: Ipomoea versicolor formation of bark by the vascular cambium). Meissn. roots and hypocotyl (Scott, 1891); The inverted nature of the secondary phloem Turbina stenosiphon (infrequent; new report, production by cambia at intraxylary phloem above). Author's personal copy

2013] CARLQUIST: INTERXYLARY PHLOEM

Fabaceae: Mucuna altissima DC. (Schenck Sapindaceae: Serjania (Pfeiffer, 1926). 1893). Urticaceae: Myriocarpa is cited by Chalk Gentianaceae: Crawfordia, Chiroma, etc. and Chattaway (1937) on the basis of large (Pfeiffer, 1926); Ixanthus (Carlquist, 1984); parenchyma strands within the secondary roots of some other genera (Pfeiffer, 1926). xylem. In fact, these strands, as they conced- Icacinaceae: Chlamydocarya, Sarcostigma, ed, do not contain phloem. Rather, the etc. (Lens et al., 2008). parenchyma strands exemplify the phenome- Lythraceae: roots of Lythrum salicaria L. non of fiber dimorphism (Carlquist, 1958, (Gin, 1909). 1961). The occurrence of this kind of Malpighiaceae: Dicella, Stigmaphyllon, parenchyma in Urticaceae has been confirmed Tetrapteris (Pfeiffer, 1926). by Bonsen and ter Welle (1984). Melastomataceae: six genera (Chalk & Study of liquid-preserved material is need- Chattaway, 1937; Metcalfe & Chalk, 1950). ed to resolve cases considered dubious here, Onagraceae: at least seven genera (Carlquist, because sieve tube elements do not survive 1975, 1977, 1983, 1987). drying very well. The erroneous report of Salvadoraceae: all genera (den Outer & van Myriocarpa exemplifies this. Likewise, roots Veenendaal, 1981; Carlquist, 2002). provide logistical problems for investigation. Solanaceae: roots and rhizomes of Atropa The few reports of interxylary phloem in belladonna L.; roots of Datura stramonium roots (Weiss, 1880;Gin1909; Solereder, L. and Scolopia sp. (Pfeiffer, 1926). 1908; Pfeiffer, 1926) are tantalizing because Stylidiaceae: Stylidium (Carlquist, 1981). they suggest more instances might be found. Thymeleaceae: Aquilaria and eight other genera (Pfeiffer, 1926; Solereder, 1908;Metcalfe 13. Physiological Significance. &Chalk,1950); Craterosiphon (above). The study of interxylary phloem (as well as Special cases: allied phenomena: intraxylary phloem, bicol- Coccinia (Cucurbitaceae) develops cambia lateral bundles) is obviously still incomplete adjacent to rays (Carlquist, 1992)orwithinaxial with respect to descriptive anatomy. The parenchyma of secondary xylem (Patil et al., understanding of the physiological significance 2011). In both of these instances, these unusual of these structural modes of phloem occurrence cambia produce secondary phloem, but no is a promising topic for exploration. Neverthe- secondary xylem. Because the secondary phlo- less, we can ask questions about function based em in both instances lies within the confines of on our present understanding of anatomy. secondary xylem, the phloem produced by these Physiological studies, like anatomical studies, cambia can be called interxylary phloem. The are most actively pursued in species of eco- terminological choice by Patil et al. (2011)is nomic interest. In fact, none of the species therefore acceptable, but one should note that known to have interxylary phloem is of any Coccinia represents an unusual instance. major economic importance. Living material of Excluded instances or dubious cases in many of the species is not easy to access. Thus, need of re-examination: progress in investigation of how interxylary Acanthaceae: Barleria (Pfeiffer, 1926) phloem works has been slow. The topics listed Apocynaceae: Lyonsia, Mandevilla, and below may be regarded as points for departure Parsonsia were cited by Pfeiffer (1926), but of physiological studies. his definition of interxylary phloem was (a) Conduction rather than storage. Ona- wider than mine and is not followed here. graceae show that parenchyma associated Asteraceae: Stoebe (Adamson, 1934). with sieve tube elements and companion cells Bignoniaceae: Distictis, Haplolophium, in interxylary phloem strands is deficient in and Pithococtenium (Pfeiffer, 1926). starch, but tissues distal to the strands (mostly Convolvulaceae: Cuscuta (Pfeiffer, 1926) libriform fibers) are rich in starch (Carlquist, Clusiaceae: Endodesmia roots (Pfeiffer, 1926). 1975). This clearly suggests a marked divi- Euphorbiaceae: Dalechampia (Pfeiffer, 1926) sion of labor, in which interxylary phloem Loranthaceae: Nuytsia (original data; reported strands represent a conductive tissue, whereas as a case of interxylary phloem by Pfeiffer, the ground tissue of the secondary xylem is 1926; Nuytsia has successive cambia). converted into a significant starch reservoir. Author's personal copy

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Lack of starch in the parenchyma that To be sure, there are many monocarpic sheathes sieve tube elements is evident in plants that lack interxylary phloem. We do examples other than Onagraceae reviewed not know about their phloem abundance or here: Acanthaceae (Fig. 2A–C), Stylidiaceae phloem conductive patterns, because phloem (Fig. 2D), Gentianaceae (Fig. 3), Thymelea- of monocarpic plants has not been the subject ceae (Fig. 5) Salvadoraceae (Fig. 6), Loga- of a study. One can, however, cite such plants niaceae (Fig. 7A–B) and Combretaceae as species of Oenothera (Onagraceae) that are (Fig. 7C–D) can be cited in this regard. biennials—in a sense, short-lived monocarpic (b) Conduction to large photosynthate sinks. plants. There is interxylary phloem in these. A number of species with interxylary phloem With relationship to Onagraceae as a whole, I strands have large fruit size (Strychnos:Leeu- suggested (Carlquist, 1975) that "Production of wenberg, 1980)) simultaneous production of large flowers or large quantities of flowers large numbers of flowers and fruits (Oenothera) during a short period might be related to or other organographic features (sudden flushes massive starch reserves and interxylary phloem of growth, Strychnos) that suggest a relation- for rapid transport of sugars." In this regard, we ship between interxylary phloem and intense may note that Fuchsia (Onagraceae), which photosynthate utilization. Large inflorescences does not have interxylary phloem, produces in which numerous flowers open at about the flowers slowly over a long period of time same time (Combretum) are pertinent in this (sometimes throughout the entire year). regard. (d) Phloem pathway multiplication and Instances of bicollateral bundles can be longevity. If interxylary phloem is produced cited here. Large fruits in Cucurbitaceae and continuously over a period of time, the Solanaceae require rapid input of photosyn- aggregate quantity of sieve tube elements thates that may be related to supernumerary and companion cells in a stem (or root) soon phloem formations. exceeds the potential amount of phloem in (c) Enhanced rate of photosynthate conduc- bark. This is a feature relevant to conduction tion:thecaseofOrphium. only if older interxylary phloem stays active. This topic is allied to the above, but The occurrence of cambial activity producing differs in stressing the rapid, simultaneous new sieve tube elements and companion cells flowering of an entire plant. Orphium in interxylary phloem strands, as in Combre- frutescens (Gentianaceae) has interxylary tum, Salvadora, and Strychnos, attests to phloem. Orphium is a small shrub or interxylary phloem longevity. We do not know, subshrub that flowers during its first year of however, about the longevity of interxylary growth. During some subsequent year, flower- phloem strands in other species, such as the ingissoextensiveandsimultaneousthatthe eight genera of Thymeleaceae (some trees: plant devotes its entire reserves of photosyn- Aquilaria) that have interxylary phloem. thates to the flowering/fruiting process and dies. We do know that secondary phloem is At this point, it is a monocarpic plant, although active in earlier increments of species with one would not have designated it as such in successive cambia (Carlquist, 2007). Ana- prior years. tomical studies show that each vascular I have cultivated Orphium frutescens in my cambium continues indefinitely to produce garden and attempted to prolong the vegeta- secondary phloem—eventually ceasing activ- tive growth of a plant by removing all flowers ity in older parts of larger stems. during its summer flowering season. In the Reports of sustained longevity of second- sixth year of growth, it produced only ary xylem, related to capability to reverse branches that terminated in flowers, with no embolisms (e.g., Sperry, 1985), is indirect side branches with vegetative buds. At that evidence of prolonged phloem function. point, there was no longer any possibility of Functioning of phloem without simultaneous deterring flowering, and the plant flowered, functioning of adjacent vessels (or tracheids) fruited, and rapidly died after fruiting. An is unlikely: The two are probably correlated event of this sort seems correlated with the (although studies of this are lacking). presence of interxylary phloem throughout (e) Phloem pathway three-dimensionaliza- the stem of Orphium. tion. Strands of interxylary phloem are an Author's personal copy

2013] CARLQUIST: INTERXYLARY PHLOEM ideal way of dispersing phloem throughout a The parenchyma sheathing of phloem stem or root as a means of aiding storage and strands is conspicuous in many instances retrieval of photosynthates. Validation of this of interxylary phloem, such as Thunbergia speculation can be found in the examples, (Acanthaceae) and Craterosiphon (Thyme- cited above for Brassicaceae and Solanaceae, leaceae) in the present study. These sug- in which interxylary phloem occurs in roots gest enhanced flexibility, a feature ascribed but is apparently absent in stems of particular to parenchyma of lianas by Schenck species. Similar hypotheses were entertained (1895). In these examples, interxylary with respect to successive cambia, which are phloem and parenchyma presence is less also an ideal mechanism for distributing in earlier-formed wood, then increases with xylem and phloem throughout a stem or root, age, suggesting parenchyma becomes more as in the beet, Beta (Carlquist, 2007). important as self-support decreases and (f) Phloem pathway protection. Interxylary response to torsion and displacement of stems phloem strands are often ideally protected by increases. their location within a fibrous background. That A relatively small number of tree species such fibrous backgrounds function in maintain- have interxylary phloem, but there are some ing or prolonging safety of the strands has not notable instances of interxylary phloem oc- been tested, although simple experiments incis- currence in tree Loganiaceae (Mennega, ing bark to see whether interxylary phloem 1980) and Thymeleaceae (Pfeiffer, 1926). suffices for conductive needs would be easy to Examples should be examined on the basis do. The evidence of placement and multiplicity of individual species, rather than strictly suggests possible isolation from phytophagous grouped according to habit. insects and possibly other influences. The (h) Longevity and other physiological phe- abundance of crystals in parenchyma sheaths nomena. Many fascinating questions regard- of interxylary phloem strands in Acanthaceae ing interxylary phloem occurrence remain to (Thunbergia), Combretaceae (Combretum), be asked and answered. Among these is the Onagraceae (all genera with interxylary phlo- longevity of interxylary phloem. Circumstan- em), and Thymeleaceae (Craterosiphon) seems tial evidence may be obtainable from whether like an indirect evidence of predation deterrence. or not secondary xylem of a range of ages in (g) Lianoid correlations and other habit a given stem is functional or not, but phloem considerations. The proportion of genera and itself tends to be good evidence, because it species with interxylary phloem that has a collapses so readily if it no longer functions lianoid habit is much higher than one would (e.g., Salvadora, Fig. 6). Correlations be- expect on the basis of the frequency of lianas tween longevity of functioning in phloem and vines in eudicots as a whole. Families and that in xylem vessels are to be expected. (and pertinent genera) in this regard include Phloem longevity is generally thought to be Acanthaceae (Thunbergia), asclepioid Apoc- only a year or two, but greater longevity has ynaceae (Asclepias, Ceropegia, Leptadenia), been demonstrated in some angiosperms Combretaceae (several genera), Convolvula- (Parthasarathy 1980). ceae (Ipomoea, Turbina), Cucurbitaceae (Cucurbita, Lagenaria), Icacinaceae (several genera), Malpighiaceae (several genera), and Acknowledgments Thymeleaceae (Craterosiphon). For providing material, thanks are due Dr. Histologically similar phenomena (e.g., David Lorence for stems of Strychnos mada- successive cambia) are also represented in a gascariensis (National Tropical Botanical Gar- larger than expected number of lianoid genera den), Dr. Peter H. Raven of the Missouri (Carlquist, 1988, 2001, 2007). These con- Botanic Garden for stems of various Onagra- structions include intraxylary phloem, bicol- ceae, and the University of California of lateral bundles, successive cambia, and California at Santa Barbara living greenhouse secondary xylem dispersed by parenchyma collections for material of Salvadora.John proliferation (e.g., Bauhinia, Mendoncia), as Bleck provided seeds of Orphium frutescens shown by the listings in appendices of from which my specimens were cultivated. Metcalfe and Chalk (1950, 1983). Mark Olson and Edward L. Schneider provided Author's personal copy

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