Stem anatomy and development of successive cambia in Hebanthe eriantha (Poir.) Pedersen: a neotropical climbing species of the Amaranthaceae

Hebanthe eriantha (Poir.) Pedersen, a climbing species of the Amaranthaceae increases in stem thickness by forming successive cambia. The family is dominated by herbaceous species and is constantly under discussion due to its disputed nature of the meristem. In the young stem small alternate segments of vascular cambium cease to divide and new arc of cambium initiates outside to it. The newly formed arcs connect with pre-existing alternate segments of cambium to complete the ring. On the contrary, in thick stems, instead of small segments, complete ring of cambium is replaced by new one. These new alternate segments/cambia originate from the parenchyma cells located outside to the phloem produced by previous cambium. Cambium is storied and exclusively composed of fusiform initials while ray cells remain absent at least in the early part of the secondary growth. However, large heterocellular rays are observed in 15-mm diameter stems but their frequency is much lower. In some of the rays, ray cells become meristematic and differentiate into radially arranged xylem and phloem elements. In fully grown plants, stems are composed of several successive rings of secondary xylem alternating with secondary phloem. Secondary xylem is diffuse-porous and composed of vessels, fibres, axial parenchyma while exceptionally large rays are observed only in the outermost regions of thick stems. Vessel diameter increases progressively from the centre towards the periphery of stems. Although the origin of successive cambia and composition of secondary xylem of H. eriantha remains similar to other herbaceous members of Amaranthaceae, the occurrence of relatively wider and thick-walled vessels and large rays in fully grown plants is characteristic to climbing habit.     

Radial secondary growth and formation of successive cambia and their products in Ipomoea hederifolia L. (Convolvulaceae)

Ipomoea hederifolia stems increase in thickness using a combination of different types of cambial variant, such as the discontinuous concentric rings of cambia, the development of included phloem, the reverse orientation of discontinuous cambial segments, the internal phloem, the formation of secondary xylem and phloem from the internal cambium, and differentiation of cork in the pith. After primary growth, the first ring of cambium arises between the external primary phloem and primary xylem, producing secondary phloem centrifugally and secondary xylem centripetally. The stem becomes lobed, flat, undulating, or irregular in shape as a result of the formation of both discontinuous and continuous concentric rings of cambia. As the formation of secondary xylem is greater in one region than in another, this results in the formation of a grooved stem. Successive cambia formed after the first ring are of two distinct functional types: (1) functionally normal successive cambia that divide to form secondary xylem centripetally and secondary phloem centrifugally, like other dicotyledons that show successive rings, and (2) abnormal cambia with reverse orientation. The former type of successive rings originates from the parenchyma cells located outside the phloem produced by previous cambium. The latter type of cambium develops from the conjunctive tissue located at the base of the secondary xylem formed by functionally normal cambia. This cambium is functionally inverted, producing secondary xylem centrifugally and secondary phloem centripetally. In later secondary growth, xylem parenchyma situated deep inside the secondary xylem undergoes de‐differentiation, and re‐differentiates into included phloem islands in secondary xylem. © 2008 The Linnean Society of London, Botanical Journal of the Linnean Society, 2008, 158 , 30–40.     

Development of successive cambia and formation of flat stems in Rhynchosia pyramidalis (Lam.) Urb. (Fabaceae)

Stem flattening in Rhynchosia pyramidalis (Fabaceae) is achieved by the development of crescent-shaped successive cambia on two opposite sides of the stem (referred hereafter as distal side). Other lateral sides of the stem (adjacent to supporting host and its opposite side, referred as proximal sides) usually possess single cambium. In the young stems, parenchymatous cells located outside to protophloem of distal side dedifferentiate and develop small segments of cambium. Concomitant to bidirectional differentiation of the secondary xylem and phloem, these newly developed cambial segments also extend in tangential directions. Differential activity of newly developed crescent-shaped cambial segments deposits more secondary xylem at median position as compared to their terminal ends of the stem on distal side; consequently, it pushes the cambial segment outside, thus resulting in crescent-shaped arcs of the cambia only on two opposite sides. After the production of 1–2 mm of secondary xylem, they cease to divide and new segments of cambial arc develop on the same side in a similar fashion. Such repeated behaviour of successive cambia development consequently leads to the formation of tangentially flat stems. The secondary xylem is diffusely porous with indistinct growth rings and is composed of vessels (wide and narrow), fibres, axial ray parenchyma cells, while phloem consisted of sieve elements, companion cells, axial and ray parenchyma. Rays in both xylem and phloem are uni- to multiseriate and heterocellular. The structure of secondary xylem and development of successive cambia is correlated with climbing habit.     

Wood Anatomy and the Development of Interxylary Phloem of Ipomoea hederifolia Linn. (Convolvulaceae)

In Ipomoea hederifolia Linn., stems increase in thickness by forming successive rings of cambia. With the increase in stem diameter, the first ring of cambium also gives rise to thin-walled parenchymatous islands along with thick-walled xylem derivatives to its inner side. The size of these islands increases (both radially and tangentially) gradually with the increase in stem diameter. In pencil-thick stems, that is, before the differentiation of a second ring of cambium, some of the parenchyma cells within these islands differentiate into interxylary phloem. Although all successive cambia forms secondary phloem continuously, simultaneous development of interxylary phloem was observed in the innermost successive ring of xylem. In the mature stems, thick-walled parenchyma cells formed at the beginning of secondary growth underwent dedifferentiation and led to the formation of phloem derivatives. Structurally, sieve tube elements showed both simple sieve plates on transverse to slightly oblique end walls and compound sieve plates on the oblique end walls with poorly developed lateral sieve areas. Isolated or groups of two to three sieve elements were noticed in the rays of secondary phloem. They possessed simple sieve plates with distinct companion cells at their corners. The length of these elements was more or less similar to that of ray parenchyma cells but their diameter was slightly less. Similarly, in the secondary xylem, perforated ray cells were noticed in the innermost xylem ring. They were larger than the adjacent ray cells and possessed oval to circular simple perforation plates. The structures of interxylary phloem, perforated ray cells, and ray sieve elements are described in detail.     

Stem anatomy of the dwarf subshrub Cressa cretica L. (Convolvulaceae)

Stem anatomy and development of medullary phloem are studied in the dwarf subshrub Cressa cretica L. (Convolvulaceae). The family Convolvulaceae is dominated by vines or woody climbers, which are characterized by the presence of successive cambia, medullary- and included phloem, internal cambium and presence of fibriform vessels. The main stems of the not winding C. cretica shows presence of medullary (internal) phloem, internal cambium and fibriform vessels, whereas successive cambia and included phloem are lacking. However, presence of fibriform vessels is an unique feature which so far has been reported only in climbing members of the family. Medullary phloem develops from peri-medullary cells after the initiation of secondary growth and completely occupies the pith region in fully grown mature plants. In young stems, the cortex is wide and formed of radial files of tightly packed small and large cells without intercellular air spaces. In thick stems, cortical cells become compressed due to the pressure developed by the radial expansion of secondary xylem, a feature actually common to halophytes. The stem diameter increases by the activity of a single ring of vascular cambium. The secondary xylem is composed of vessels (both wide and fibriform), fibres, axial parenchyma cells and uni-seriate rays. The secondary phloem consists of sieve elements, companion cells, axial and ray parenchyma cells. In consequence, Cressa shares anatomical characteristics of both climbing and non-climbing members. The structure of the secondary xylem is correlated with the habit and comparable with that of other climbing members of Convolvulaceae.     

The Developmental Anatomy of the Root System in Yam Bean, Pachyrhizus erosus Urban

Investigations revealed that the anatomy of the primary radicularroot of yam bean (Pachyrhizus erosus L.) was typically dicotyledonousexcept that the xylem was not completely developed centripetally.Most of the roots had tetrarch xylem, although a few triarchand pentarch roots were also observed. In both tuberous andnon-tuberous roots, secondary thickening occurred by the formationof the meristematic vascular cambium which formed secondarytissues in a normal fashion. Subsequently, tuberization wasinitiated in the secondary xylem by the development of anomalous‘secondary’ cambia from parenchyma cells surroundingvessel elements. Anomalous ‘secondary’ cambia alsodeveloped from parenchyma cells not associated with vessels.Subsequently, anomalous ‘tertiary’ cambia differentiatedfrom tissues produced by the anomalous ‘secondary’cambia. Activities of these anomalous cambia resulted in theproduction of parenchyma storage cells and were chiefly responsiblefor the growth of the mature tuber. Pachyrhizus erosus L., yam bean, tuberous root, anatomy, anomalous ‘secondary’ cambia, anomalous ‘tertiary’ cambia, centripetal xylem development     

Stem anatomy of Dolichos lablab Linn (Fabaceae): Origin of cambium and reverse orientation of vascular bundles

Secondary growth in the stem of Dolichos lablab is achieved by the formation of eccentric successive rings of vascular bundles. The stem is composed of parenchymatous ground tissue and xylem and phloem confined to portions of small cambial segments. However, development of new cambial segments can be observed from the obliterating ray parenchyma, the outermost phloem parenchyma and the secondary cortical parenchyma. Initially cambium develops as small segments, which latter become joined to form a complete cylinder of vascular cambium. Each cambial ring is functionally divided into two distinct regions. The one segment of cambium produces thick-walled lignified xylem derivatives in centripetal direction and phloem elements centrifugally. The other segment produces only thin-walled parenchyma on both xylem and phloem side. In mature stems, some of the axial parenchyma embedded deep inside the xylem acquires meristematic activity and leads to the formation of thick-walled xylem derivatives centrifugally and phloem elements centripetally. The secondary xylem comprises vessel elements, tracheids, fibres and axial parenchyma. Rays are uni-multiseriate in the region of cambium that produces xylem and phloem derivatives, while in some of the regions of cambium large multiseriate, compound, aggregate and polycentric rays can be noticed.     

ANOMALOUS GROWTH AND VEGETATIVE ANATOMY OF SIMMONDSIA CHINENSIS

The anatomy of the stem, root, and leaf of Simmondsia chinensis (Link) Schneider was investigated, as well as the mode of tissue formation in the stem. Perivascular tissue is present as part of the primary body; outermost cell layers of this tissue mature as a fibrous sheath. The first short-lived extrafascicular cambium is generated within the remaining parenchymatous perivascular tissue. Successive independent extrafascicular cambia, organized as complete rings or large arcs, arise within peripheral conjunctive parenchyma produced by previous cambia. Extrafascicular cambia produce secondary xylem centripetally and conjunctive tissue bands and strands of secondary phloem centrifugally. Conjunctive tissue initials produce raylike structures of conjunctive tissue; true vascular rays are absent. The phellogen is actually a region of transition where the peripheral conjunctive parenchyma of previous extrafascicular cambia undergoes further cellular subdivision; a true phellogen is lacking. Xylem bands do not represent annual or seasonal growth increments, and secondary growth in Simmondsia is an unequivocal example of the “concentric” anomaly.     

Continuity of Procambium and Anomalous Cambium During Formation of Successive Cambia in Celosia argentea

The development of woody plants is related to the continuity of the procambium and cambium. Whether such a continuity is present in plants with successive cambia, especially in those, where the first cambium is formed outside the primary vascular bundles, has not been analyzed so far. Therefore, we studied the development of vascular meristem in Celosia argentea, in which the first and successive cambial cylinders arise outside the primary bundles and, intriguingly, in the literature are interpreted as developmentally independent structures. Our results showed that in C. argentea, the outermost procambial cells maintain their meristematic characteristics during differentiation of vascular bundles and divide periclinally, forming the zone of procambium-derived cells outside the primary bundles. This zone comprises parenchyma cells bordering the bundles, and a continuous ring of the incipient cambial cells neighboring the primary cortex. Later in the development, the ability to preserve the outermost cells in the cambium undifferentiated is repeated during the formation of successive cylinders of cambia. Together, our results clearly point to the developmental continuity of the procambium and successive cambia in C. argentea, despite their seemingly spatial distinctiveness. We postulate that the mechanism demonstrated in C. argentea is universal and orchestrates the development of successive cambia in other plant species.

     

Successive cambia in Aizoaceae: products and process

The transverse and longitudinal sections of the stems and roots of 11 genera of Aizoaceae, representing a wide range of growth forms from hard fibrous stems to fibre‐free roots, were studied using light microscopy and scanning electron microscopy. In most of the genera, fibres are the first xylary product of each vascular cambium, followed by vessels in a parenchyma background. Variations on this pattern help to prove that fibres are produced by vascular cambia, except in Ruschia and Stayneria, in which both the lateral meristem and the vascular cambia produce fibres. Cylinders of conjunctive tissue parenchyma that alternate with the vascular cylinders are produced by the lateral meristem. The concept that the lateral meristem gives rise to the vascular cambia and secondary cortex is supported by photographic evidence. Radial divisions occur in the origin of the lateral meristem, and then again as vascular cambia arise from the lateral meristem; these radial divisions account for storeying in fibres and conjunctive tissue. Raylessness characterizes all Aizoaceae studied, with the exception of Tetragonia, which also differs from the remaining genera by having vasicentric axial parenchyma, a scattering of vessels amongst fibres, and the presence of druses instead of raphides. Several vascular cambia are typically formed per year. Several vascular cambia are active simultaneously in a given stem or root. Roots have fewer fibres and more abundant conjunctive tissue parenchyma than stems. Successive cambia result in an ideal dispersion of vascular tissue with respect to water and photosynthate storage and retrieval capabilities of the parenchyma, and to liana stem plans. The distribution and relative abundance of fibres, vessels, secondary phloem, and conjunctive tissue parenchyma relate primarily to habit and are not a good source of systematic data, with the probable exception of Tetragonia. The general pattern of lateral meristem and vascular cambial ontogeny is the same as in other families of the core Caryophyllales, although the patterns of the tissues produced are diverse. © 2007 The Linnean Society of London, Botanical Journal of the Linnean Society, 2007, 153 , 141–155.     

ORIGIN AND ACTIVITY OF SUCCESSIVE CAMBIA IN CYCAS (CYCADALES)

Observations of the vascular tissue of Cycas shoots have provided supporting evidence that the first vascular cambium as well as subsequent successive cambia are simultaneously active. The establishment of the second cambium occurs during the seedling stage, and differentiates mainly within the cortical cells. However, cambial activity also occurs within phloem parenchyma cells of the first vascular cylinder. Tracheids in the first and the successive vascular cylinders are generally of the same length; however, there is a trend toward increasing length within the successive cylinders, possibly because the successive cambia are long-lived.     

Wood and stem anatomy of woody Amaranthaceae s.s.: ecology, systematics and the problems of defining rays in dicotyledons

Wood and stem anatomy is studied for seven species of six genera (root anatomy also reported for one species) of Amaranthaceae s.s. Quantitative data on vessels correlate closely with relative xeromorphy of respective species, agreeing with values reported for dicotyledons without successive cambia in comparable habitats. Libriform fibre abundance increases and vessel diameter decreases as stems and roots of the annual Amaranthus caudatus mature. Long, thick-walled fibres in Bosea yervamora may be related to the upright nature of elongate semi-climbing stems. Non-bordered or minutely bordered perforation plates characterize Amaranthaceae, as they do most other Caryophyllales. Amaranthaceae have idioblastic cells containing druses, rhomboidal crystals or crystal sand: these forms intergrade and seem closely related. Rays are present in secondary xylem of the Amaranthaceae studied. Cells intermediate between ray cells and libriform fibres occur in Charpentiera elliptica . Degrees of diversity in rays and reports of raylessness in Amaranthaceae induce discussion of definition and identification of rays in dicotyledons; some sources recognize both rays and radial plates of conjunctive tissue in Amaranthaceae. The action of successive cambia is described: lateral meristem periclinal divisions produce secondary cortex externally, conjunctive tissue internally and yield vascular cambia as well. Vascular cambia produce secondary phloem and secondary xylem, in both ray and fascicular zones, as in a dicotyledon with a single cambium. Identification of meristem activity and appreciation of varied ray manifestations are essential in understanding the ontogeny of stems in Amaranthaceae (which have recently been united with Chenopodiaceae).  © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society , 2003, 143 , 1–19.     

SUCCESSIVE CAMBIA IN THE STEM OF PHYTOLACCA DIOICA

Phytolacca dioica L., an evergreen tree of the Phytolaccaceae, is one of the species of Phytolacca which shows anomalous secondary thickening in its stem. This mode of thickening has been regarded as successive cambial activity or alternatively, in some more recent interpretations, as thickening by unidirectional activity of a cambial zone. The stem thickening of P. dioica is of the former type. The cambium produces fascicular strands, showing centrifugal differentiation of xylem and centripetal differentiation of phloem on opposite sides of the cambial layer, and rays are produced between the fascicular areas. In both xylem and phloem the younger elements are closer to the cambium than the older elements. Succeeding cambia arise periodically by periclinal divisions in a layer of parenchyma cells two or three cells beyond the outermost intact phloem derived from the current cambium. Each cambium forms a few parenchyma cells on both sides before it forms derivatives which mature into lignified xylem elements or conductive elements of the phloem. The parenchyma thus formed toward the outside later becomes the site of the origin of the succeeding cambium. Only one or two layers of this phloem parenchyma go on to form the new cambium; the remaining cells accumulate between the outermost phloem and the cortex. P. weberbaueri shows stem structure similar to P. dioica. P. meziana, a shrub, shows normal stem structure.     

Interxylary phloem: Diversity and functions

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.     

Cellular events during interfascicular cambium ontogenesis in inflorescence stems of Arabidopsis

Development of cambium and its activity is important for our knowledge of the mechanism of secondary growth. Arabidopsis thaliana emerges as a good model plant for such a kind of study. Thus, this paper reports on cellular events taking place in the interfascicular regions of inflorescence stems of A. thaliana, leading to the development of interfascicular cambium from differentiated interfascicular parenchyma cells (IPC). These events are as follows: appearance of auxin accumulation, PIN1 gene expression, polar PIN1 protein localization in the basal plasma membrane and periclinal divisions. Distribution of auxin was observed to be higher in differentiating into cambium parenchyma cells compared to cells within the pith and cortex. Expression of PIN1 in IPC was always preceded by auxin accumulation. Basal localization of PIN1 was already established in the cells prior to their periclinal division. These cellular events initiated within parenchyma cells adjacent to the vascular bundles and successively extended from that point towards the middle region of the interfascicular area, located between neighboring vascular bundles. The final consequence of which was the closure of the cambial ring within the stem. Changes in the chemical composition of IPC walls were also detected and included changes of pectic epitopes, xyloglucans (XG) and extensins rich in hydroxyproline (HRGPs). In summary, results presented in this paper describe interfascicular cambium ontogenesis in terms of successive cellular events in the interfascicular regions of inflorescence stems of Arabidopsis.     

Structure and ontogeny of successive cambia in Tetrastigma (Vitaceae), the host plants of Rafflesiaceae

Successive cambia in Vitaceae have been reported solely for Tetrastigma, a diverse genus of lianas found primarily in tropical Asia, extending into Australia. However, the structure and origin of these successive cambia have never been fully studied. Here we report the presence of this cambial variant in Tetrastigma retinervum and T. voinierianum, and describe its ontogeny in detail in the latter. New cambia appear successively in stems of Tetrastigma differentiating from the innermost parenchyma cells of the primary phloem, which are located interior to the pericyclic fiber strands. This study constitutes the first report of successive cambia being derived from primary phloem parenchyma in woody plants as a whole. Both species are members of Tetrastigma clade VI, the most species‐rich lineage within the genus. The examination of mature stems of additional species of Tetrastigma should determine the distribution of this unique type of cambial variant in the genus and enhance our understanding of the adaptive significance of this unusual character.     

How to catch the patch? A dendrometer study of the radial increment through successive cambia in the mangrove Avicennia

Background and Aims

Successive vascular cambia are involved in the secondary growth of at least 200 woody species from >30 plant families. In the mangrove Avicennia these successive cambia are organized in patches, creating stems with non-concentric xylem tissue surrounded by internal phloem tissue. Little is known about radial growth and tree stem dynamics in trees with this type of anatomy. This study aims to (1) clarify the process of secondary growth of Avicennia trees by studying its patchiness; and (2) study the radial increment of Avicennia stems, both temporary and permanent, in relation to local climatic and environmental conditions. A test is made of the hypothesis that patchy radial growth and stem dynamics enable Avicennia trees to better survive conditions of extreme physiological drought.

Methods

Stem variations were monitored by automatic point dendrometers at four different positions around and along the stem of two Avicennia marina trees in the mangrove forest of Gazi Bay (Kenya) during 1 year.

Key Results

Patchiness was found in the radial growth and shrinkage and swelling patterns of Avicennia stems. It was, however, potentially rather than systematically present, i.e. stems reacted either concentrically or patchily to environment triggers, and it was fresh water availability and not tidal inundation that affected radial increment.

Conclusions

It is concluded that the ability to develop successive cambia in a patchy way enables Avicennia trees to adapt to changes in the prevailing environmental conditions, enhancing its survival in the highly dynamic mangrove environment. Limited water could be used in a more directive way, investing all the attainable resources in only some locations of the tree stem so that at least at these locations there is enough water to, for example, overcome vessel embolisms or create new cells. As these locations change with time, the overall functioning of the tree can be maintained.