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DEVELOPMENT, TAXONOMIC SIGNIFICANCE and ECOLOGICAL ROLE of the CUTICULAR EPITHELIUM in the SANTALALES Carol A. Wilson & Clyd

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DEVELOPMENT, TAXONOMIC SIGNIFICANCE and ECOLOGICAL ROLE of the CUTICULAR EPITHELIUM in the SANTALALES Carol A. Wilson & Clyd IAWA Journal, Vol. 24 (2), 2003: 129–138 DEVELOPMENT, TAXONOMIC SIGNIFICANCE AND ECOLOGICAL ROLE OF THE CUTICULAR EPITHELIUM IN THE SANTALALES by Carol A. Wilson & Clyde L. Calvin Department of Biology, Portland State University, Portland OR 97207, U.S.A. SUMMARY All genera in the mistletoe family Viscaceae develop a secondary protec- tive covering, the cuticular epithelium, that replaces the epidermis. The cuticular epithelium also occurs in the Eremolepidaceae and some genera within the related family Santalaceae. This secondary covering, unlike the periderm, lacks lenticels or their functional equivalent. We suggest that the cuticular epithelium provides a greater degree of control over tran- spirational water loss in older plant parts. The cuticular epithelium may arise in the epidermis, subepidermal layer, or in deeper tissues of the stem. Bark strands of the endophytic system, where they are in contact with either nonliving host tissues or the external environment, also form a cu- ticular epithelium. The epidermal feature, stomatal orientation, was also studied. All genera in the Viscaceae and Eremolepidaceae have stomata with a transverse orientation. The presence or absence of a cuticular epi- thelium and stomatal orientation are vegetative characters with potential taxonomic value. Key words: Cuticular epithelium, parasitic angiosperm, periderm, San- talales, stomatal orientation, transpiration, Viscaceae. INTRODUCTION In the vast majority of plants having secondary growth, the epidermis is replaced by a covering of secondary origin, the periderm. The first periderm may arise in the epi- dermis, the subepidermal layer, or in deeper tissues of the stem (Esau 1977). The roots of woody plants also form a periderm, although its origin is typically from pericyclic derivatives rather than from cortex or epidermis. The formation of a periderm in woody plants is not universal, however. In one plant family, the Viscaceae, a strikingly dif- ferent secondary protective covering – termed the cuticular epithelium – replaces the epidermis (Damm 1902; Calvin 1970; Wilson & Calvin 1996). The cuticular epithelium is a relatively thick tissue produced by living epidermal and subepidermal cell layers and is high in cutin. Older cuticular epithelia typically contain necrotic epidermal and subepidermal cells. The cuticular epithelium differs from the periderm in several ways. First, the periderm contains a discrete tissue-initiating layer, the phellogen, whereas tissue formation within the cuticular epithelium is more diffuse. Second, cells within the periderm are radially seriate when viewed in transverse sections of stem. This radial alignment of cell files Downloaded from Brill.com09/23/2021 11:08:58AM via free access 130 IAWA Journal, Vol. 24 (2), 2003 Wilson & Calvin — Cuticular epithelium in Santalales 131 is either poorly defined or absent in stems with a cuticular epithelium. Third, a promi- nent feature of most periderms is the presence of lenticels that allow for exchange of gases between the tissues of the stem and the external environment. Lenticels, or their functional equivalent, are absent in the cuticular epithelium (Damm 1902; Calvin 1970; Wilson & Calvin 1996). Fourth, the periderm has a high suberin content (Roelofsen 1959). In the cuticular epithelium suberin is absent or present as a minor constituent. Instead, successive cuticular layers assume the functional roles attributed to suberin in the periderm. A cuticular epithelium was first described for stems of the European mistletoe,Vis- cum L. (Damm 1902). Damm also noted the presence of a cuticular epithelium in stems of two additional genera of Viscaceae, Notothixos Oliver and Dendrophthora Eichler. Later, Calvin (1970) provided an account of the cuticular epithelium in stems of Phora- dendron Nutt. Wilson and Calvin (1996) confirmed the presence of a cuticular epithe- lium in stems of several species of the dwarf mistletoe, Arceuthobium M. Bieb., also in the Viscaceae. Korthalsella Tieghem and Ginalloa Korth., the remaining genera of Viscaceae, have not been examined previously for this character. Further, while a cutic- lar epithelium is known to occur in stems, its possible presence in the highly modified roots making up the endophytic system has not been determined previously. One additional morphological vegetative character, stomatal orientation with respect to the plant axis may have taxonomic potential within the Santalales. Past work has shown that a transverse orientation of stomata on stems is uncommon in angiosperms (Butterfass 1987). Butterfass concludes that a transverse orientation of stomata is more common in plant groups with succulent members. We have slide preparations of many species of Viscaceae. Because host /parasite tis- sue relationships were our main interest, we focused mainly on study of the endophytic system. However, we usually also prepared stem and leaf material for microscopic study. This report utilizes these slide preparations, as well as materials prepared from herbarium specimens, to elaborate on the occurrence and functional role of the cutic- ular epithelium in the plant family Viscaceae. Where possible, stomatal orientation was also determined. Selected genera in four other families of the Santalales – Santalaceae, Eremolepidaceae, Loranthaceae, and Misodendraceae – were also examined for com- parative purposes. We are interested in identifying vegetative characters having po- tential taxonomic value for mistletoes because few characters are known for reduced members of this group. MATERIALS AND METHODS Field collected aerial shoot and endophytic system tissues of Arceuthobium and Pho- radendron were used in this study (Table 1). Materials were embedded in paraffin, sec- tioned at 8–12 µm using a rotary microtome and stained with either safranin-fast green or tannic acid-ferric chloride-lacmoid. These prepared specimens were augmented by small samples (Table 1) obtained from herbarium sheets at the University of California, Berkeley, Herbarium (UC) and Portland State University Herbarium (HPSU). These samples were softened (Schmid & Turner 1977) and free-hand sections were prepared. Downloaded from Brill.com09/23/2021 11:08:58AM via free access 130 IAWA Journal, Vol. 24 (2), 2003 Wilson & Calvin — Cuticular epithelium in Santalales 131 Table 1. Species analyzed for the presence (+) or absence (–) of a cuticular epithelium (CE) and stomatal orientation (St-Or). Stomata orientation is either transverse (tv) or vertical (vt). Family / genus CE St-Or Material studied or reference Viscaceae Arceuthobium americanum Nutt. ex Engelm. + Tv Calvin US01-03 (HPSU) globosum Hawksworth & Wiens + Tv Authorʼs prepared slides tsugense (Rosendahl) G.N. Jones + Tv Authorʼs prepared slides Dendrophthora clavata (Benth.) Urb. + Tv Damm (1902); Butterfass (1987) Korthalsella complanata (v. Tiegh.) Engl. + Tv Forbes 187 (UC) Ginalloa arnottiana Korth. + Tv Clemens 18028 (UC) Notothixos subaureus Oliver + Tv Blakely s.n. July 1921 (UC) Phoradendron macrophyllum (Engelm.) Cockerell + Tv Calvin US00-08 (HPSU) californicum Nutt. + Tv Calvin US00-09 (HPSU) Viscum album L. + Tv Damm (1902); Butterfass (1987) Santalaceae* Exocarpus bidwellii Hook. f. + Tv Calvin & Wilson NZ98-05 (HPSU) Eremolepidaceae Antidaphne viscoidea Poepp. & Endl. + Tv Weston 4213 (UC) Eubrachion ambiguum (Hook. & Arn.) Engl. + Tv Herter 82379 (UC) Lepidoceras chilense (Molina) Kuijt + Tv Eyerdam 10609 (UC) Loranthaceae** Tupeia antarctica (Cham. & Schldl.) Korth. – Vt Oeuci s.n. 6 May 1930 (UC) Misodendraceae Misodendrum brachystachyum DC. – Vt S. Carlquist (pers. comm.) * Butterfass (1987) records 10 additional genera of Santalaceae with transverse stomata on stems. ** Butterfass (1987) records two genera of Loranthaceae with transverse stomata on stems. Some sections were stained with Sudan IV, safranin, and/or phloroglucinol-HCl to en- hance cellular and extracellular materials. The prepared slides and tissue samples from herbarium sheets allowed us to study the stem anatomy of all seven genera compris- ing the Viscaceae, as well as selected members of related families. Sherwin Carlquist provided the information on Misodendrum G.Don f. in the Misodendraceae (Table 1). Specimens were also examined for stomatal orientation. In most angiosperm families stomata are vertically oriented or parallel with the longitudinal axis of the stem. A few families have transverse stomata, where the long axis of stomata is perpendicular to the longitudinal axis of the stem (Butterfass 1987). The herbarium sheets from which samples were taken and the genera examined are given in Table 1. RESULTS We found that a cuticular epithelium is present in two genera of the Viscaceae – Kort- halsella and Ginalloa – that had not previously been examined for this character. These findings confirmed that stems of all genera within the Viscaceae develop a thick cuticular layer covering epidermal cells (Fig. 1). Prominent pegs of cuticular material also form Downloaded from Brill.com09/23/2021 11:08:58AM via free access 132 IAWA Journal, Vol. 24 (2), 2003 Wilson & Calvin — Cuticular epithelium in Santalales 133 Fig. 1–5. Transverse and longitudinal sections through older stems of Viscaceae genera. – 1–4: Phoradendron macrophyllum. – 1: Break, (b) in continuity of thick cuticular layer (cl), × 100. – 2: Repair of break in cuticular layer by formation of new layer beneath, × 100. – 3: Detail of Figure 2 showing presence of new cuticular layer in space between anticlinal wall (da) and inner periclinal wall, ×
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