Distinctive Wood Anatomy of the Root-Parasitic Family Lennoaceae (Boraginales)

Carlquist &IAWA Guilliams Journal – Wood38 (1), anatomy 2017: 3–12of Lennoaceae 3 Distinctive wood anatomy of the root-parasitic family Lennoaceae (Boraginales) Sherwin Carlquist and C. Matt Guilliams Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105, U.S.A. e-mail: [email protected] ABSTRACT The four species of Lennoaceae have strands of primary plus secondary xylem in a background of starch-rich parenchyma. These strands constitute a cylinder with large primary rays. The wood within these strands is markedly different from that of other families in the crown group of Boraginales such as Cordiaceae and Ehretiaceae, most of which are woody. Lennoaceae differ because they lack fibrous cells (libriform fibers), lack rays within the vascular strands, and have markedly elliptical vessel-to-vessel pits without vestures. Lennoaceae have secondary xylem with short, wide vessel elements with thick walls, horizontally elongate elliptical pits, simple perforation plates much narrower than the vessel lumen; variously uneven vessel wall thickenings; and axial parenchyma. The wood of Lennoaceae shows resemblances to unrelated succulents such as Kalanchoe (Crassulaceae) and Lithops (Aizoaceae). The vessel features also sug- gest adaptation to high water tensions as root parasites in desert areas, whereas the lack of imperforate tracheary elements may relate to support of the under- ground stem portions by sand or rock detritus. Habit and ecology are more im- portant in the architecture of lennoaceous xylem than systematic affinities. The four species of Lennoaceae differ from each other in minor xylary features. Key words: Ecological wood anatomy, holoparasites, perforation plates, succulent plant anatomy. INTRODUCTION Our knowledge of wood anatomy in angiosperms still tends to reflect a predominant interest in woody species, despite the inherent interest of wood anatomy in “non-woody” families such as Lennoaceae. Wood anatomy in these families often exempliies unusual xylem characteristics that relate to ecology and habit rather than to systematic position. The Lennoaceae consist of four species: Lennoa madreporoides Llave & Lex., Pholisma arenarium Nutt. ex Hook., P. culiacanum (Dressler & Kuijt) Yatskievych, and P. sonorae (Torr. ex A. Gray) Yatskievych (Yatskievych & Mason 1986). The latter two species have also been treated within a segregate genus, Ammobroma. Lennoa differs from Pholisma by its annual habit, diploid chromosome number (n = 9) and other features, whereas Pholisma consists of tetraploid (n = 18) perennials (Yatskievych & Mason 1986). © International Association of Wood Anatomists, 2017 DOI 10.1163/22941932-20170153 Published by Koninklijke Brill NV, Leiden 4 IAWA Journal 38 (1), 2017 The features of greatest interest of the group are its habit as a root parasite and its occurrence in sand or finely-divided rock particles (Dressler & Kuijt 1968), a substrate that permits seeds to sift down to the roots of host plants. In these habits, sand and rocky detritus may be shifted by wind action, burying the plants in the case of Pholisma. The stems are capable of branching and of penetrating to the substrate surface at flowering times; the original root connection may become deeply buried. Stems are thus supported by a sandy or granular rocky matrix, and are usually not visible because the plant produces one or more inflorescences upon reaching the surface. The stems of both Lennoa and Pholisma contain primary xylem but also produce secondary xylem in the vascular strands, which compose a loose cylinder, embedded in parenchyma, between the pith and cortical parenchyma. There has been no previous work on the anatomy of these vascular strands, although low-magnification transverse sections of stems of Lennoa and Pholisma are offered by Yatskievych & Mason (1986). The succulence of stems (as well as other structures) is a distinctive feature that should be considered in relation to the secondary xylem of the Lennoaceae. The parenchymatous nature of the stems, free from fibers, may relate to the supporting role of the substrate, but also may relate to the parasitic habit and the aridity of lennoaceous habitats. After the publication of Solereder’s (1885) thesis, there was a tendency to attribute similarities and differences to degree of relationship. Taxonomic closeness often does relate to similarity between particular species or genera in wood anatomy – but only if they are similar in ecological preferences, growth form, and degree of woodiness. Recognition of the predominant role of ecology in shaping wood evolution (Carlquist 1959, 1966, 1975; Baas 1976) has led to correlations between wood anatomy and vessel dimensions, as well as to numerous other subsidiary wood features. The Lennoaceae show that the more radical the departure of a clade in terms of ecology, growth form, and physiology, the more pronounced the differences are with respect to wood anatomy. Indeed, for many years, the taxonomic affinities of the lennoids were not understood. There were comparisons with monotropoid Ericaceae and other groups of plants now thought to be unrelated, a history detailed by Yatskievych & Mason (1986) and the Boraginales Working Group (2016). One may choose to follow the monofamilial Boraginales (sole family, Boragina- ceae) as advocated by APG III, (2009 and APG IV (2016), or the multifamilial equivalent (Boraginales Working Group 2016). The latter has been followed here, so that Len- noaceae rather than Boraginaceae subfamily Lennoideae is cited throughout the paper. Molecular data have been interpreted as showing that the Lennoaceae are sister to Ehretiaceae (Gottschling et al. 2001; Langström & Chase 2002; Gottschling 2003), in a clade that also includes Cordiaceae as well as Coldeniaceae and Hoplestigmataceae. Most of this clade consists of woody trees (see Rabaey et al. 2010). The most recent treatment recognizes these groupings as families of Boraginales rather than subfamilies of Boraginaceae s.l. (Boraginales Working Group 2016). The APG delimitations of families of angiosperms (e.g., APG III 2006; APG IV 2016) tended to accept larger, more inclusive families with more numerous subfamilies. Although this procedure does emphasize relationships, it has the disadvantage of promoting large, heterogeneous Carlquist & Guilliams – Wood anatomy of Lennoaceae 5 families that cannot be readily defined, and thus have not been universally accepted by systematists. One example is the Brassicales, which now include 19 families; alterna- tive treatments would lead to combining, say, Capparaceae, Cleomaceae, Brassicaceae, Stixaceae, Borthwickiaceae, and other families into a Capparaceae s. l., despite the distinctive features, some newly described, of the component families (Carlquist 2016). If we keep in mind the woody nature of Cordiaceae and Ehretiaceae, a woodiness probably basic in Boraginales (Boraginales Working Group 2016), we have a way of throwing into relief the roles of physiology, ecology, habitat, and habit in shaping the architecture of stems and secondary xylem. MATERIAL AND METHODS As a generalization, liquid-preserved material is always preferable to dried material in anatomical studies. However, scanning electron microscopy (SEM) shows that phloem details are often not well preserved by ordinary (ethanol) means of fixation (phloem of long-lived phloem cells, such as those of palms, is an exception). Despite the highly succulent nature of stems of the Lennoaceae, the xylem of their vascular strands is not degraded by drying (Fig. 1A, 2A, 3A, 4A), and is suitable for SEM study. This is fortu- nate, because the widespread distribution of the four species and the small population sizes make collection of living material of the species logistically problematic. Material of the four species was obtained from herbarium specimens, cited in the captions for figures. Stem portions were boiled in water and then stored in 50% aque- ous ethanol. Sections were cut by hand, using single-edged razor blades. Transverse and radial sections of stems were easily obtained, perhaps because the texture of the starch-filled stems made them suited for this procedure. Sections were subjected to three 12-hour changes of distilled water, and then dried between pairs of clean glass slides (with pressure applied to each pair) on a warming table. The dried sections were then mounted on aluminum stubs, sputter-coated with gold, and examined with a Hitachi S2600N SEM. Taxonomic nomenclature follows that of Yatskievych & Mason (1986). The phylo- genetic constructions of Boraginales by the Boraginaceae Working Group (2016) are adopted here. Low-power transverse sections of stems of Lennoa and Pholisma are offered by Yatskievych & Mason (1986). Comparison of their illustrations with the SEM preparations shows no difference in cell proportions except for phloem, which is crushed in the dried material (e.g., Fig. 1A, 2A) and remains crushed in material treated with boiling water. RESULTS Lennoa madreporoides (Fig. 1) Vascular strands are rather small and tangentially narrow (Fig. 1A). Axial parenchyma is about as common as the vessels (Fig. 1A, arrows). The earliest portion of each strand consists of protoxylem, which is small in extent compared to the secondary xylem (defined by the presence of pitting rather than annular or helical bands). Imperforate tracheary elements (e.g., libriform fibers) are absent. Perforation plates 6 IAWA Journal 38 (1), 2017 Figure. 1. Xylem of Lennoa madreporoides stem, UC

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