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Development of Intraxylary Phloem in the Stem of Combretum Rotundifolium (Combretaceae)

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Development of Intraxylary Phloem in the Stem of Combretum Rotundifolium (Combretaceae) IAWA14 Journal, Vol. 32 (1), 2011: 14–24 IAWA Journal, Vol. 32 (1), 2011 DEVELOPMENT OF INTRAXYLARY PHLOEM IN THE STEM OF COMBRETUM ROTUNDIFOLIUM (COMBRETACEAE) Elaine Zózimo1, Neusa Tamaio1* and Ricardo Cardoso Vieira2 SUMMARY The present study focuses on the origin, secondary growth, and anatom- ical characteristics of the intraxylary phloem compared to the regular phloem in Combretum rotundifolium Rich. The intraxylary phloem first originates in the primary stem from the perimedullary procambium and, later, from the internal cambium that develops by differentiation of the perimedullary procambium and dedifferentiation of perimedullary parenchyma cells. Tangential sclerenchyma bands, irregular stratification of the cellular elements, and uniseriate rays are present in the regular phloem, but not in the intraxylary phloem. We are the first to report the presence of an unusual bidirectional internal cambium that produces pa- renchymatous cells centrifugally and intraxylary phloem centripetally. Key words: Cambial variants, intraxylary phloem, internal phloem, in- ternal cambium, Combretum rotundifolium, regular phloem. INTRODUCTION The intraxylary phloem involves the production of phloem in the pith’s periphery. In Combretum Loefl. (Combretaceae) intraxylary phloem (internal phloem) and/or interxylary phloem (included phloem) may be present (e.g. Solereder 1908; Metcalfe & Chalk 1950; Verhoeven & Van der Schijff 1974; Van Vliet 1979). The occurrence of intraxylary phloem is a synapomorphy of the order Myrtales, to which the Combretaceae belong (Stevens 2001 onwards; Judd et al. 2009). However, many aspects of intraxylary phloem development in the family and order remain unknown, as Quisqualis indica L. is the only species for which some stages of intraxylary phloem development have been described, including its origin from the procambium and its secondary growth resulting from the development of a unilaterally active internal cambium (Baranetzky 1900). Some data on intraxylary phloem for Combretum are available, including its ap- pearance as a ring or group arrangement and the occurrence of an internal cambium (Metcalfe & Chalk 1950; Verhoeven & Van der Schijff 1974; Tilney 2002). The regular phloem shares some characters with other genera of the Combretaceae, such as storied cellular elements, crystals and narrow rays (Den Outer & Fundter 1976). 1) Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Diretoria de Pesquisa Científica, Rua Pacheco Leão 915, 22460-030 Rio de Janeiro, RJ, Brazil. 2) Laboratório de Morfologia Vegetal da Universidade Federal do Rio de Janeiro, Depto de Botânica, IB, CCS, BL A, Sala A1-108, Av. Brigadeiro Trompowsky s.n., 21941-590 Ilha do Fundão, Rio de Janeiro, RJ, Brazil. *) Corresponding author [[email protected]]. Downloaded from Brill.com09/25/2021 09:14:58PM via free access Zózimo, Tamaio & Vieira — Intraxylary phloem in Combretum 15 In the present study, we describe the ontogeny of intraxylary phloem, thus provid- ing information on 1) primary and secondary origin of intraxylary phloem, and 2) the origin and activity of the internal cambium. Furthermore, we compare the intraxylary with the regular secondary phloem. MATERIAL AND METHODS Fresh material of the scandent shrub Combretum rotundifolium Rich. was collected at the Instituto de Pesquisas Jardim Botânico do Rio de Janeiro (RB 464426, RBw 8978). Two dried samples of the same species were obtained from the herbarium of the same institution (RB 204242, RB 25014). Samples of the shoot apex and stem segments at different developmental stages were fixed in FAA 70 (formaldehyde, acetic acid, 70% alcohol; 1:1:18) (Johansen 1940) and glutaraldehyde 2.5% in a phosphate buffer solution (Gabriel 1982). After dehydration in alcohol, the samples of the shoot apex and younger internodes were embedded in historesin (Gerrits & Smid 1983). Sections 3–5 µm thick were cut on a rotary microtome, and stained with toluidine blue 0.05% (O’Brien et al. 1964). Sections 18–20 µm thick of the more mature portions, some of which were embedded in polyethylene glycol (Rupp 1964), were cut transversally and longitudinally on a rotary microtome, and stained with astra blue and safranin (Kraus & Arduin 1997). After the staining process, the sections were mounted in synthetic resin. Anatomical terminology Six anatomical terms are adopted here, as follows: “perimedullary procambium” and “internal cambium” for the meristems in an atypical position, e.g. the peripheral area of the pith, and “regular procambium” and “regular cambium” for meristems in a typical position. Phloem produced externally and in the peripheral area of the pith is termed here as “regular phloem” and “intraxylary phloem”, respectively. The secondary phloem description follows the methodology of Richter et al. (1996). RESULTS First vascular tissue developmental stage (Fig. 1) A transverse section of the first internode shows that the regular procambium is initiated by an almost continuous band of cells with dense cytoplasm and conspicuous nuclei. At this stage, protophloem cannot be distinguished, but the first protoxylem elements are visible, bordered by peripheral pith parenchyma cells. Origin of the intraxylary phloem In the third internode, the vascular bundles consist of protophloem and protoxylem already differentiated in a collateral arrangement. The perimedullary procambium, which consists of 2–3 cell layers, becomes evident right below the protophloem and protoxylem, with the exception of four leaf trace regions (Fig. 2–4). Initially, the perimedullary procambium shows 1) segments that are connected to the regular pro- Downloaded from Brill.com09/25/2021 09:14:58PM via free access 16 IAWA Journal, Vol. 32 (1), 2011 cambium, and 2) segments that start actively generating phloem vascular cells (Fig. 4). Subsequently, all of these arcs differentiate into isolated groups of intraxylary phloem in the pith’s periphery immediately below the primary xylem (Fig. 5). Figures 1–5. Transverse sections of young stem showing development of perimedullary procam- bium and intraxylary phloem in Combretum rotundifolium. – 1: First visible protoxylem elements (arrow) and parenchyma cells bordering the protoxylem. – 2: Overview of third internode with depressed areas lacking perimedullary procambium (arrows) in the vascular system. – 3: Detail of figure 2, showing a depressed area without perimedullary procambium, with protoxylem (arrows) and parenchyma cells right below. – 4: Detail of figure 2, with collateral bundles and perimedullary procambium (arrows) with low activity, producing the first phloem cells (circle). – 5: Isolated strands of intraxylary phloem (circles) from perimedullary procambium. — Scale bar for 1, 3 & 5 = 25 µm; for 2 & 4 = 50 µm. → Figures 6–11. Transverse sections of young stem showing the development of the regular and in- ternal cambium, and of the intraxylary secondary phloem in Combretum rotundifolium. – 6: Well- developed regular cambium (large arrow), and intraxylary primary phloem with medullar ray (small arrow) in the pith’s periphery. – 7: Development of internal cambium (large arrow) from the perimedullary procambium. Small arrow indicates vascular ray of the intraxylary phloem. – 8: Areas of the pith’s periphery (arrows) lacking intraxylary phloem from the beginning of vas- cular differentiation. – 9: Development of internal cambium (large arrow) from parenchyma cell Downloaded from Brill.com09/25/2021 09:14:58PM via free access Zózimo, Tamaio & Vieira — Intraxylary phloem in Combretum 17 dedifferentiation on the pith’s periphery. Note the periclinal divisions in some of the cells (small arrow), and cells with obvious nuclei. – 10: Completely established single internal cambium with intraxylary secondary phloem (arrows). – 11: Bidirectional internal cambium activity with centrifugal axial and radial parenchyma cells (large arrow) and centripetal intraxylary phloem (small arrow). — Scale bar = 50 µm. Downloaded from Brill.com09/25/2021 09:14:58PM via free access 18 IAWA Journal, Vol. 32 (1), 2011 Asynchronous development of the regular and intraxylary phloem (Fig. 6) In the sixth internode, development of the regular cambium begins with regular procambium differentiation. During secondary growth, the intraxylary phloem is even more confined to the perimedullary region. The intraxylary phloem basically consists of sieve tube elements, companion cells, axial parenchyma cells and stretched medullary cells constituting the medullary rays. Vascular rays are absent, further characterizing the intraxylary phloem as still in its primary growth phase. Internal cambium development and activity In the eighth internode the start of secondary intraxylary phloem growth can be observed (Fig. 7). The internal cambium develops through differentiation of the peri- medullary procambium in the areas with intraxylary phloem. At this stage, the areas corresponding to the remains of foliar trace outputs remain without intraxylary phloem differentiation (Fig. 2, 3 & 8). In the tenth internode, new internal cambium segments are formed from a cellular dedifferentiation process whereby parenchyma cells located in the periphery of the pith undergo radial and tangential expansion followed by divisions, as evidenced by prominent nuclei and thin periclinal walls (Fig. 9). Subsequently, a complete cylinder of internal cambium is established, and intraxylary phloem production begins throughout the pith’s periphery (Fig. 10). The internal cambium functions bidirectionally, but with an unusual production
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