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Comparative Wood Anatomy of the Primuloid Clade (Ericales S.L.)

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Comparative Wood Anatomy of the Primuloid Clade (Ericales S.L.) Systematic Botany (2005), 30(1): pp. 163–183 ᭧ Copyright 2005 by the American Society of Plant Taxonomists Comparative Wood Anatomy of the Primuloid Clade (Ericales s.l.) FREDERIC LENS,1,3 STEVEN JANSEN,2,1 PIETER CARIS,1 LIESBET SERLET,1 and ERIK SMETS1 1Laboratory of Plant Systematics, Institute of Botany and Microbiology, Katholieke Universiteit Leuven, Kasteelpark Arenberg 31, B-3001 Leuven, Belgium 2Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, U.K. 3Author for Correspondence ([email protected]) Communicating Editor: Paul S. Manos ABSTRACT. The wood structure of 78 species from 27 genera representing the woody primuloids (Maesaceae, Myrsina- ceae, and Theophrastaceae) was investigated using light microscopy (LM) and scanning electron microscopy (SEM). Results indicated that the ray structure, the nature of mineral inclusions, and the occurrence of breakdown areas in rays can be used to separate the three primuloid families from each other. Within Ericales, the presence of exclusively multiseriate rays is synapomorphic for Myrsinaceae and Theophrastaceae, and the occurrence of breakdown areas in rays is synapomorphic for Myrsinaceae. Within Myrsinaceae, the wood structure of the mangrove genus Aegiceras differs because it has short vessel elements that are storied, non-septate fibers, a combination of low uni- and multiseriate rays, and multiseriate rays with exclusively procumbent body ray cells. The aberrant wood anatomy of Coris and Lysimachia can be explained by their secondary woodiness. Within Theophrastaceae, Clavija and Theophrasta can be distinguished from Bonellia, Jacquinia,and Deherainia.The recent division of Jacquinia s.l. into Jacquinia s.s. and Bonellia is supported by a difference in mineral inclusions. The primuloid clade is one of the few groups within considered sister to all other primuloids (Ka¨llersjo¨et the newly circumscribed Ericales that is well support- al. 2000). In addition, Ka¨llersjo¨etal. (2000) and An- ed based on molecular sequence data (Anderberg et al. derberg et al. (2001) proposed to place the former Pri- 2002; Bremer et al. 2002). The clade comprises five fam- mulaceaegenera Ardisiandra Hook.f.,Anagallis L., As- ilies, Maesaceae, Myrsinaceae, Primulaceae, Samola- terolinon Hoffmannsegg & Link, Coris L., Cyclamen L., ceae, andTheophrastaceae, and about 65 genera and Glaux L., Lysimachia L., Pelletiera A. St.-Hil., Stimpsonia 2600 species (Kubitzki 2004). More than half of the pri- C. Wright ex A. Gray, and Trientalis L. within the sister muloid representatives are woody, mostly small to me- family Myrsinaceae. Furthermore, another genus of dium-sized trees or shrubs, and sometimes lianas. The Primulaceae, Samolus,was placed as sister to the re- genus Samolus L. (Samolaceae), all Primulaceae, and a maining Theophrastaceae by the same authors. The fewMyrsinaceae taxa, representing ca. 20 genera and monophyly of the family Theophrastaceae excluding 1100 species, are herbs and therefore omitted from this Samolus is morphologically well supported (Sta˚hl study. The distribution of woody primuloids is mainly 2004a, b). Also floral ontogenetic work supported the tropical: Myrsinaceae are pantropical with several taxa family level for Samolus as sister to Theophrastaceae extending to tropical montane habitats, Theophrasta- (Caris and Smets 2004). These two families in turn are ceae are restricted to the neotropics, and Maesaceae sister to the Primulaceae-Myrsinaceae clade (Ka¨llersjo¨ are concentrated in the palaeotropics. Primulaceae, on et al. 2000). the other hand, grow in the temperate regions of the Besides these renewed family concepts, generic re- Northern Hemisphere, and Samolaceae have their alignments within primuloid families were proposed. main distribution in saline habitats of the Southern For instance, the monophyly of various Myrsinaceae Hemisphere (Ka¨llersjo¨etal. 2000). genera is still a matter of dispute (Sta˚hl andAnderberg All representatives of the primuloid clade have long 2004b), and recent molecular sequence data from been placed in the former Primulales (Pax 1889; Mez Theophrastaceae suggest that the orange-red flowered 1902, 1903), which were characterized by a set of floral Jacquinia L. species together with Jacquinia paludicola characteristics: (1) sympetalous flowers with functional Standl. and J. longifolia Standl. should be recognized as stamens as many as and opposite to the corolla lobes, aseparate genus Bonellia Colla in order to maintain the (2) a compound, mainly hypogynous ovary with one monophyly of the morphologically well supported style, and (3) few to many tenuinucellate, usually anat- genera Deherainia Decaisne and Votschia Sta˚hl (Ka¨llers- ropous, bitegmic ovules set on a free-central to basal jo¨andSta˚hl 2003; Sta˚hl and Ka¨llersjo¨ 2004). placenta (Cronquist 1988). Family concepts within the The wood anatomy of primuloid families is poorly primuloid clade have changed considerably during the known. The most detailed overview was presented by last 10 years. Based on molecular and morphological Metcalfe and Chalk (1950), based on nine Myrsinaceae data, the genus Maesa Forssk. was removed from Myr- genera, four Theophrastaceae genera, and Maesa. Other sinaceae and elevated to family level (Anderberg and noteworthy studies that included a restricted number Sta˚hl 1995; Anderberg et al. 1998, 2000; Caris et al. of primuloids were presented by Moll and Janssonius 2000; Sta˚hland Anderberg 2004a). Now, Maesaceae are (1926), Williams (1936), De´tienne et al. (1982), Suzuki 163 164 SYSTEMATIC BOTANY [Volume 30 and Noshiro (1988), Ogata and Kalat (1997), and Sosef bars in M. lanceolata. Intervessel pits alternate (Fig. 1D), et al. (1998). 4–6 ␮minsize, non-vestured. Vessel-ray pits similar This work aims to present a detailed wood anatom- to intervessel pits in shape and size, sometimes having ical overview of Maesaceae, Myrsinaceae, and Theo- scalariform pits with distinct borders in M. indica, M. phrastaceae, using light microscopy (LM) and scan- ramentacea,andM. schweinfurthii;vessel ray-pits main- ning electron microscopy (SEM). The anatomical vari- ly scalariform with strongly reduced to nearly simple ation observed will be compared with the recent fa- pits in M. lanceolata (Fig. 1H) and M. macrothyrsa, 10– milial and generic realignments within the primuloid 30 ␮minsize. Helical sculpturing indistinctly present clade, taking ecological and physiological aspects into throughout body of vessel elements, or restricted to account. In addition, some selected wood features will tails of vessel elements. Tangential diameter of vessels be plotted on a simplified molecular tree to trace evo- (30-)40–100(-120) ␮m, (18-)20–90(-101) vessels per lutionary patterns. This study also addresses the pos- mm2,vessel elements (330-)460–850(-1070) ␮m long. sibilities of secondary woodiness within primuloids, Tracheids absent. Fibers septate, thin- or thin- to thick- since Anderberg et al. (2001) suggested that the ances- walled, (520-)870–1270(-1560) ␮m long, with simple to tor of the Samolaceae-Theophrastaceae-Primulaceae- minutely bordered pits concentrated in radial walls, Myrsinaceae clade could be herbaceous. pit borders 2–3 ␮mindiameter. Axial parenchyma scanty paratracheal (Figs. 1A, B); 2–4 cells per paren- MATERIALS AND METHODS chyma strand. Uniseriate rays always present (Figs. 1E, ␮ In total, 92 wood specimens representing 78 species and 27 gen- F), (160-)330–1430(-2100) m high, consisting of up- erawereinvestigated using LM and SEM (Appendix 1). Twenty right cells, 0(-2-)6 rays per mm. Multiseriate rays 2–5(- one genera of Myrsinaceae sensu Sta˚hland Anderberg (2004b), 8-)seriate, (200-)470–2590(-7000) ␮m (and even more) fivegenera of Theophrastaceae (including Bonellia)andthegenus high, 0(-4-)6 rays per mm, consisting of predominantly Maesa were included. procumbent body ray cells (Fig. 1G) or a mixture of Wood sections of about 25 ␮m thick were cut using a sledge microtome. After bleaching, staining and dehydrating, the tissues procumbent, square, and upright body ray cells, and were mounted in euparal. Preparations for macerations and SEM 1–4 upright rows of marginal ray cells; sheath cells are according to Jansen et al. (1998). The wood anatomical ter- present. Breakdown areas in rays absent. Gummy de- minology follows the ‘‘IAWA list of microscopic features for hard- posits in ray cells. Very few prismatic crystals in pro- wood identification’’ (IAWA Committee 1989), except for the term ‘breakdown areas in rays’ which is illustrated by Aegiceras Gaertn. cumbent and upright ray cells of M. indica. Pith cells in the CSIRO family key for hardwood identification (Ilic 1987). homogeneous. According to Webber (1938), these structures are ‘intercellular cav- Myrsinaceae. Taxa studied: Aegiceras 1/2, Afrardisia ities possibly of normal occurrence’ and were called ‘gum cysts’ Mez 1/16, Ardisia Sw. 4/250, Badula Juss. 1/17, Coris by Panshin (1932) or ‘schizogenous secretory cavities’ by Metcalfe and Chalk (1950). Breakdown areas in rays often contain orange 1/2, Ctenardisia Ducke 1/2, Cybianthus Mart. 7/150, to dark brown substances including neutral lipids and hydroben- Discocalyx (A. DC.) Mez 2/50, Embelia Burm. f. 4/130, zoquinones, a typical compound that is observed in five Myrsi- Geissanthus Hook.f.2/30, Grammadenia Benth. 2/7, He- naceaegenera and in Maesa. Hydrobenzoquinones are also present berdenia Banks ex A. DC. 1/1, Lysimachia 2/150, Myr- in epithelial cells surrounding secretory cavities in both vegetative
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