Blackwell Science, LtdOxford, UKBOJBotanical Journal of the Linnean Society0024-4074The Linnean Society of London, 2005? 2005 1482 189206 Original Article SEED COAT MORPHOLOGY N. M. S. HASSAN ET AL. Botanical Journal of the Linnean Society, 2005, 148, 189–206. With 30 figures Seed coat morphology of Aizoaceae–Sesuvioideae, Gisekiaceae and Molluginaceae and its systematic significance FLS Department of Plant Systematics, University of Bayreuth, D-95440 Bayreuth, Germany Received December 2003; accepted for publication November 2004 Macro- and micromorphological characters of the seeds of 32 species belonging to Aizoaceae (26 species), Gisekiaceae (one species) and Molluginaceae (five species) were analysed for their taxonomic value. Seed morphology is found to be of considerable taxonomic value within the taxa investigated, although additional criteria are usually necessary for distinguishing the species. However, a subgroup of Trianthema, consisting of T. cussackiana, T. megasperma, T. pilosa, T. rhynchocalyptra and T. oxycalyptra var. oxycalyptra (Aizoaceae) shares the synapomorphy of seeds with scattered idioblast cells (papillae). There is little infrageneric variation within Sesuvium and Zaleya in contrast to Trianthema, whose seeds are considerably polymorphic. The fairly different seed structures found in Aizoaceae s.s. and Molluginaceae support their treatment as two distinct families. However, the position of Lineum (Molluginaceae) remains uncertain. Moreover, seed characters support the independence of Gisekia (Gisekiaceae) in a family of its own. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 148, 189–206. ADDITIONAL KEYWORDS: Cypselea – Gisekia – Limeum – micromorphology – SEM – Sesuvium – taxonomy – Trianthema – Zaleya. INTRODUCTION Aizoaceae Martynov is regarded as a paraphyletic family including five subfamilies (Bittrich & Hartmann, 1988). The relationship between Aizoaceae and Molluginaceae was disputed over many years after Hutchinson (1926) excluded Molluginaceae from Aizoaceae and established a separate family. Later, Pax & Hoffmann (1934) treated Molluginaceae as a subfamily within Aizoaceae. Some authors (Eckardt, 1964; Cronquist, 1968; Takhtajan, 1969) followed Hutchinson’s view and segregated Molluginaceae from Aizoaceae based on morphological characters. Richardson (1978), based on flavonoid contents, suggested that Aizoaceae s.s. and Molluginaceae are two distinct families. In addition, embryological (Masand & Kapil, 1966) and further biochemical data support the exclusion of Molluginaceae from Aizoaceae s.l. (cf. Singh, 1989). Hofmann (1973) and Ehrendorfer (1976) suggested an intermediate position for Molluginaceae *Corresponding author. E-mail: ulrich.meve@uni-bayreuth.de between Aizoaceae and Phytolaccaceae. Because Molluginaceae display many primitive characters, a position for this family near the base of Caryophyllidae was proposed (Bittrich & Hartmann, 1988). Molluginaceae is a rather heterogeneous family, and circumscription of its genera is not always undisputed. The detection of betalains in Gisekia L. reflects its close affinities to Phytolaccaceae, a placement also supported by rbcL/matK data (Cuénoud et al., 2002). As a result, Gisekia can be separated from non-pigmented genera (Limeum L.) and the other genera of Molluginaceae containing only anthocyanins (Mabry, Behnke & Eifert, 1976; Takhtajan, 1980; Brown & Varadarajan, 1985). Some authors treated Gisekia as a tribe (Gisekieae) in Aizoaceae (Müller, 1909; Pax & Hoffmann, 1934). Both Hutchinson (1959) and Eckardt (1964) included it in Molluginaceae again. Hofmann (1973), based on corresponding gynoecium morphology, pointed out the relationship of Gisekia to Phytolaccaceae; however, most morphological and anatomical data underline that Gisekia is most closely related to Molluginaceae. Nakai (1942) was the first to © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 148, 189–206 189 Downloaded from https://academic.oup.com/botlinnean/article-abstract/148/2/189/2420379 by guest on 09 June 2020 NASR M. S. HASSAN, ULRICH MEVE* and SIGRID LIEDE-SCHUMANN 190 N. M. S. HASSAN ET AL. Caryophyllales (Cactaceae and Portulacaceae) and Corner (1976) pointed out that seeds in Aizoaceae ancestors were probably covered by an aril. For subfamily Ruschioideae even an additional epicuticular layer consisting of rodlets up to 10 mm long has been described (Ehler & Barthlott, 1978). Some authors (Narayana, 1962; Prakash, 1967; Hartmann, 1993) observed that the integuments in Aizoaceae are composed of two layers except for Zaleya decandra, in which it is three-layered. In general, fruit and seed (shape, size and surface) show remarkable diversity in the Aizoaceae (Hartmann, 1993). The species-rich Aizoaceae–Ruschioideae, not included in this study, is fairly well known with regard to seed morphology (e.g. Liede, 1989, for Erepsia N.E. Br.; Hartmann, 1996, for Acrodon N.E. Br., Stoeberia L. Bolus). The aims of our study are (a) to show the different patterns or variations in ultrastructure of seed coat surface, and (b) to investigate and evaluate seed coat features in parts of Aizoaceae s.s., Gisekiaceae and Molluginaceae and evaluate their use for phylogenetic and taxonomic considerations. MATERIAL AND METHODS Our samples were taken from 32 specimens on loan from different herbaria or from fresh material collected by the first author (Table 1). Dry seeds, with the aril removed, when necessary, were mounted on stubs using double-sided adhesive tape. These samples were investigated under a stereo microscope and, goldsputtered, in a scanning electron microscope (SEM; scanned with a Philips XL-30 ESEM at 20 kV in Bayreuth, or scanned with a JEOL at 15 kV in Assiut). The terminology used for description follows Barthlott (1981, 1984) and Cutler (1979), with some modifications when necessary. RESULTS SEED CHARACTER ASSESSMENT (CF. TABLE FIGS 2; 1–30) Aril Aizoaceae s.l., arils are found in the subfamily Sesuvioideae only. The seeds of the species of Sesuvium L. investigated, S. maritimum, S. sessile, S. sesuvioides and S. verrucosum, are completely covered with a membraneous aril except for those of S. portulacastrum, which possess an aril covering up to half the seed surface (Figs 11, 12). A complete aril is also recorded for some species of Trianthema L., such as T. compacta, T. cussackiana, T. parvifolia, T. patellitecta, T. sheilae and T. triquetra. The investi- © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 148, 189–206 Downloaded from https://academic.oup.com/botlinnean/article-abstract/148/2/189/2420379 by guest on 09 June 2020 create the monotypic family Gisekiaceae. Recently, acceptance of Gisekiaceae has increased (e.g. Gilbert, 2000a). The position of Limeum within Molluginaceae was and is still a matter of debate. Moquin-Tandon (1849) and Heimerl (1889) placed this genus within Phytolaccaceae, which was followed by Dahlgren (1980). It has been found that Limeum, apart from a lack of pigments, has a different type of sieve element plastid inclusion (PIIIc≤f) (e.g. Behnke et al., 1983). It is therefore likely that Limeum represents a different lineage and hence deserves family status (Cuénoud et al., 2002). The most important synapomorphic character for Aizoaceae s.s. is the epidermal bladder cell of vegetative parts of the plants (Bittrich & Hartmann, 1988; Bittrich & Struck, 1989). Aizoaceae s.s. can be divided into five subfamilies: Aizooideae, Mesembryanthemoideae, Ruschioideae, Sesuvioideae and Tetragonioideae. Mesembryanthemoideae and Ruschioideae are monophyletic and sister to the likewise monophyletic Aizooideae, Sesuvioideae and Tetragonioideae. Although both groups are supported by a number of synapomorphic characters, the situation within the second group is less clear and verification of the presumed relationships among these subfamilies still needs verification (cf. Bittrich, 1990). Angiosperm taxa present remarkable diversity in seed size, shape, colour, and surface structure and sculpture (e.g. Martin & Barkley, 1961; Gunn & Seldin, 1976; Bhojwani & Bhatnagar, 1977; Sampathkumar & Ayyangar, 1982). The number of seeds produced per capsule can serve as a diagnostic character (Canne, 1979; Juan, Pastor & Fernández, 2000). Also, Barthlott & Ehler (1977) reported that the epidermal features are variable for angiosperm taxa and can be used to evaluate possible relationships. The seed coat is considered an important constituent in the development of Angiospermae (e.g.Windsor et al., 2000). It is less affected by environmental conditions than, for example, floral characters and often reflects genetic differences (e.g. Cutler & Brandham, 1977; Barthlott, 1984). The taxonomic importance of seed coat microsculpture has been proven by many authors (e.g. Hill, 1976; Seavey, Magill & Raven, 1977; Canne, 1980); in consequence, the number of such studies increased over the last decades. Barthlott (1981, 1984) summarized the diversity of seed surface sculpturing in detail, describing the following categories: (a) arrangement of cells, (b) shape of cells (primary sculpture), (c) relief of the outer cell wall (secondary sculpture) and (d) epicuticular secretions (tertiary sculpture). Rocén (1927) showed that ovule and seed structure are meaningful characters in Centrospermae. Barthlott (1983) found that arillate seeds and central field type of cuticular pattern are significant characters in SEED COAT MORPHOLOGY 191 Table 1. Voucher data for specimens used in the SEM studies Origin Voucher Aizoaceae s.s. Aizoanthemum hispanicum (L.) H. E. K. Hartmann Aizoon canariense L. Cypselea humifusa Turp. Mesembryanthemum cryptanthum Hook. f. Egypt Egypt Egypt Nederl. Antilles Egypt Mesembryanthemum crystallinum L. Mesembryanthemum nodiflorum L. Sesuvium hydaspicum (Edgew.) M. L. Gonçalves Sesuvium maritimum (Walter) Britton et al. Sesuvium portulacastrum (L.) L. Sesuvium sessile Pers. Sesuvium sesuvioides (Fenzl) Verdc. Sesuvium verrucosum Raf. Trianthema compacta C. White Trianthema glossistigma F. Muell. Trianthema megasperma A. Prescott Trianthema oxycalyptra var. oxycalyptra F. Muell. Trianthema patellitecta A. Prescott Trianthema pilosa F. Muell. Trianthema portulacastra L. Trianthema rhynchocalyptra F. Muell. Trianthema sheilae A.G. Mill. Trianthema triquetra Willd. ex Spreng. Trianthema turgidifolia F. Muell. Zaleya decandra (L.) Burm. f. Zaleya galericulata (Melville) H. Eichler Zaleya pentandra (L.) Jeffrey Gisekiaceae Gisekia pharnaceoides L. Molluginaceae Corbichonia decumbens (Forssk.) Exell Glinus lotoides L. Limeum obovatum Vicary Limeum viscosum (J.Gay) Fenzl Mollugo nudicaulis Lam. Egypt Egypt Burkina Faso USA Kenya USA Namibia Saudi Arabia Australia Australia Australia Australia Australia Australia Egypt Australia Saudi Arabia Australia Australia Australia Australia Saudi Arabia Egypt Egypt El-Sayed s.n. (CAI) El-Sayed s.n. (CAI) El-Bakry 1092 (CAI) Van Proosdij 1126 (U) Hassan & El-Naggar s.n. (AST = Assiut University, proposed abbreviation) Hassan & El-Naggar s.n. (AST) Hassan & El-Naggar s.n. (AST) Madsen 5264 (S) Thomas et al. 103, 258 (NY) Robertson 3680 (WAG) Walker 1673 (NY) Van Slageren MSJB020 (WAG) Fayed s.n. Clarkson & Neldner 9509 (AQ) Latz 9572 (AD) Cowie 8758 (DNA) Fatchen 831 (AD) Egan & Bowlay 4974 (DNA) Lothian 1422 (AD) Hassan s.n. (AST) Smith 3660 (DNA) Collenette 9284 (E) Jessop 133 (AD) Latz 12861 (DNA) Dietrich s.n. (WAG) Michell & Risler 1717 (DNA) Fayed s.n. Osborn & Helmy s.n. (CAI) Osborn & Helmy s.n. (CAI) Egypt Egypt Sudan Sudan Sudan Fahmy & Hassib s.n. (CAI) Täckholm et al. s.n. (CAI) Drar 797 (CAI) Shabetai s.n. (CAI) Kassas s.n. (CAI) gated species of Molluginaceae possess an appendage as well. The seeds of Corbichonia Scop., and Mollugo L. lack an aril (Figs 23, 29) but they do have minute fleshy appendage-like processes (strophioles), whereas Glinus L. has long and slender strophioles (Fig. 26; cf. also Davis, 1967; Endress & Bittrich, 1993). An aril is absent in Gisekiaceae and in Limeum (Figs 25, 27). Seed shape Seed shape shows considerable variation among most of the taxa studied. In Aizoaceae seeds vary from reniform to rounded reniform, or orbicular to suborbicular. Seed shape is fairly variable in Sesuvium maritimum, where rounded reniform to suborbicular seeds occur. Ovoid seeds can be found in S. sessile, S. sesuvioides and Cypselea humifusa (Fig. 7). Trianthema triquetra and T. sheilae share a characteristic ovoid-elliptical seed shape (Fig. 19). Seed shape is ovoid-acuminate and flattish ovoid in Trianthema compacta and T. turgidifolia, respectively. In Mesembryanthemum L. seed shape is rather deltoid owing to a snout-like, elongated and curved micropylar region (Fig. 5). Gisekia pharnaceoides has ovoid-suborbicular seeds (Fig. 25), whereas members of the Molluginaceae have more or less reniform seeds. In Limeum, they are additionally flattened (slightly winged) (Fig. 27). Seed size Some variation in seed size was found. Cypselea humifusa and Trianthema compacta are characterized by © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 148, 189–206 Downloaded from https://academic.oup.com/botlinnean/article-abstract/148/2/189/2420379 by guest on 09 June 2020 Taxa 192 Character Seed size Seed number Seed colour Seed coat surface Epidermal cell shape Anticlinal wall boundaries Outer periclinal cell wall absent roundedreniform 1 ¥ 0.8 many black or dark brown concentrically to transversely ridged slightly sunken; straight to curved; covered with fine wax platelets A. canariense absent reniform 0.9 ¥ 0.7 many shiny black concentrically ridged isodiametric to penta-hexagonal; arranged in rows or scattered elongated; arranged in rows slightly or strongly convex; covered with fine wax platelets flat to strongly convex; smooth M. cryptanthum absent deltoid 0.7 ¥ 0.5 many light brown M. crystallinum absent deltoid 0.9 ¥ 0.7 many black or dark brown longitudinally and transversely ridged longitudinally and transversely ridged penta-hexagonal to elongated; arranged in rows elongated; arranged in rows M. nodiflorum absent deltoid 1 ¥ 0.7 many dark brown longitudinally and transversely ridged elongated; arranged in rows C. humifusa absent ovoid 0.3 ¥ 0.2 many light brown reticulate penta-hexagonal; randomly distributed S. hydaspicum absent suborbicular 1.4 ¥ 1.1 many black transversely ridged elongated; arranged in rows Aril Aizoaceae A. hispanicum slightly sunken; straight to strongly wavy; smooth indistinct to sunken; straight to curved; smooth deeply sunken; straight to curved; covered with fine wax platelets, and scattered coarse crystals indistinct to sunken; straight to curved; with very fine wax platelets slightly raised; straight to slightly wavy; smooth to finely folded highly raised; straight to slightly wavy; smooth to folded Downloaded from https://academic.oup.com/botlinnean/article-abstract/148/2/189/2420379 by guest on 09 June 2020 © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 148, 189–206 Seed shape Taxa flat to strongly convex; smooth strongly convex; covered with fine wax platelets flat to strongly convex; with very fine wax platelets flat; smooth to uneven concave; smooth N. M. S. HASSAN ET AL. Table 2. Characteristics of studied seeds Character Aril Seed shape Seed size Seed number Seed colour Seed coat surface Epidermal cell shape Anticlinal wall boundaries Outer periclinal cell wall rounded reniform suborbicular suborbicular 0.9 ¥ 0.7 many shiny black smooth indistinct indistinct flat; smooth 1.4 ¥ 1.2 many shiny black smooth, slightly ridged on the dorsal side indistinct to sunken; straight; smooth flat to convex; smooth ovoid ovoid rounded reniform ovoid acuminate 1 ¥ 0.9 1 ¥ 0.8 1 ¥ 0.8 many many many shiny black shiny black shiny black smooth smooth smooth indistinct to elongated; arranged in rows indistinct indistinct indistinct indistinct indistinct indistinct flat; smooth flat; smooth flat; smooth 0.5 ¥ 0.3 4–8 shiny black smooth, slightly ridged on the dorsal side towards the hilum unsculptured with idioblasts simple concentrically ridged indistinct to elongated; arranged in rows indistinct to sunken; straight; smooth flat to slightly convex; smooth indistinct indistinct flat to papillose; smooth elongated; arranged in rows sunken to slightly raised; straight; smooth isodiametric to penta-hexagonal; randomly distributed isodiametric; randomly distributed slightly raised; straight to curved; smooth slightly concave to strongly convex; smooth to uneven convex at central portion or papillose; smooth slightly concave; uneven or with idioblasts complex flat to concave; smooth to uneven S. maritimum present S. portulacastrum present S. sessile S. sesuvioides S. verrucosum present present present T. compacta present T. cussackiana present suborbicular 1.7 ¥ 1.6 4–10 black T. glossistigma absent rounded reniform 1 ¥ 0.8 4–8 shiny black T. megasperma absent orbicular 2.5 ¥ 2.3 1 black with idioblasts simple T. oxycalyptra var. oxycalyptra absent rounded reniform 1.8 ¥ 1.4 6–9 black or dark brown with idioblasts complex T. parvifolia present orbicular 1 ¥ 0.9 2 shiny black ± concentrically ridged T. patellitecta present orbicular 1.4 ¥ 1.3 2 shiny black ± smooth (faintly reticulate) isodiametric to penta-hexagonal; randomly distributed isodiametrical to variable; randomly distributed slightly raised; curved; smooth slightly raised; straight to curved; smooth to folded slightly to deeply sunken; straight to slightly curved; smooth flat to slightly convex; smooth to uneven SEED COAT MORPHOLOGY 193 Downloaded from https://academic.oup.com/botlinnean/article-abstract/148/2/189/2420379 by guest on 09 June 2020 © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 148, 189–206 Taxa 194 Character Seed shape Seed size Seed number Seed colour Seed coat surface Epidermal cell shape Anticlinal wall boundaries Outer periclinal cell wall T. pilosa absent suborbicular 1.4 ¥ 1.2 2–3 black with idioblasts simple highly raised; straight; smooth flat to papillose; smooth to uneven T. portulacastra absent suborbicular 1.8 ¥ 1.6 3–12 black ± concentrically ridged highly raised; straight to curved; smooth flat to concave; smooth T. rhynchocalyptra absent suborbicular 1.2 ¥ 1 2 shiny black with idioblasts simple slightly raised; straight to curved; smooth flat to papillose; smooth T. sheilae present ovoidelliptical 1 ¥ 0.8 2 black ± concentrically ridged isodiametric to penta-hexagonal; randomly distributed isodiametric to penta-hexagonal; randomly distributed isodiametric to penta-hexagonal; randomly distributed penta-hexagonal; randomly distributed slightly raised; straight; smooth T. triquetra present ovoidelliptical 1.1 ¥ 0.9 (1)2 shiny black ± concentrically ridged isodiametric to penta-hexagonal; randomly distributed flat to slightly convex at central portion; smooth to uneven flat to concave; uneven T. turgidifolia absent flattish ovoid 1.6 ¥ 1.4 2–3 dark brown concentrically ridged Z. decandra absent orbicular 1.9 ¥ 1.8 4 black ridges randomly distributed isodiametric to penta-hexagonal; randomly distributed penta-hexagonal to elongated; randomly distributed highly raised; straight to slightly curved; smooth to finely folded flat to slightly raised; straight to curved; smooth flat to slightly concave; smooth slightly raised; straight; smooth flat to slightly concave; smooth Downloaded from https://academic.oup.com/botlinnean/article-abstract/148/2/189/2420379 by guest on 09 June 2020 © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 148, 189–206 Aril Taxa N. M. S. HASSAN ET AL. Table 2. Continued Aril Seed shape Seed size Seed number Seed colour Seed coat surface Epidermal cell shape Anticlinal wall boundaries Outer periclinal cell wall Z. galericulata absent orbicular 1.3 ¥ 1.2 4 black ridges randomly distributed slightly to highly raised; straight to curved; smooth flat to slightly concave; uneven Z. pentandra absent orbicular 1.4 ¥ 1.3 4 black ridges randomly distributed isodiametric to penta-hexagonal; randomly distributed isodiametric to penta-hexagonal; randomly distributed highly raised; straight; smooth to finely folded concave; smooth to uneven Gisekiaceae G. pharnaceoides absent ovoidsuborbicular 1.1 ¥ 0.9 1 shiny black or dark brown unsculptured penta-hexagonal very slightly raised; strongly wavy; smooth very slightly concave; smooth Molluginaceae C. decumbens present reniform 1.2 ¥ 0.8 many shiny black concentrically ridged elongated; arranged in parallel rows G. lotoides present subreniform 0.6 ¥ 0.4 many indistinct absent reniformflattened 1.8 ¥ 1.2 2 smooth with isolated papillae rough convex terminated with papillae; smooth flat to papillose; smooth L. obovatum shiny black or dark brown pale yellow slightly to deeply sunken; straight; smooth to porous surface indistinct highly raised; straight; laciniate flat; micropapillate L. viscosum absent reniformflattened 2 ¥ 1.4 2 pale yellow rough with ribs flat; micropapillate M. nudicaulis present rounded reniform 0.7 ¥ 0.5 many shiny black concentrically ridged highly raised; straight; with longitudinal striations slightly to deeply sunken; straight to curved; smooth to porous surface penta-hexagonal; randomly distributed penta-hexagonal; randomly distributed elongated to polygonal; arranged in parallel rows strongly convex, basally constricted; with cross striations 195 Downloaded from https://academic.oup.com/botlinnean/article-abstract/148/2/189/2420379 by guest on 09 June 2020 Taxa SEED COAT MORPHOLOGY © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 148, 189–206 Character 196 N. M. S. HASSAN ET AL. 2 3 4 5 6 Figures 1–6. Scanning electron micrographs of seeds of Aizoaceae s.s. Figs 1, 2. Aizoanthemum hispanicum (s.n.). Figs 3, 4. Aizoon canariense (El-Bakry 1092). Figs 5, 6. Mesembryanthemum crystallinum (s.n.). Scale bars = 100 mm in Figs 1, 3, 5; 50 mm in Figs 2, 4, 6. the smallest seeds, measuring c. 0.3 ¥ 0.2 mm and 0.5 ¥ 0.3 mm, respectively. In contrast, T. megasperma has the largest seeds, c. 2.5 ¥ 2.3 mm (for seed sizes of the other species see Table 2). Seeds of Molluginaceae vary in the range 0.7– 1.2 ¥ 0.4–0.9 mm. Limeum species have the larges seeds, c. 1.8–2 ¥ 1.2–1.4 mm. Seed number The number of seeds per capsule can be categorized as follows: Aizoanthemum Dinter ex Friedrich, Aizoon L., Cypselea Turp. and Sesuvium have many seeds. There is considerable variation within Trianthema: a single seed is formed in T. megasperma; two seeds are typical of T. parvifolia, T. patellitecta, T. rhynchocalyptra, T. sheilae and T. triquetra (rarely one seed); 2–3 for T. pilosa and T. turgidifolia; 3–12 for T. portulacastra; 4–8 for T. compacta and T. glossistigma; 4–10 for T. cussackiana; and 6–9 for T. oxycalyptra var. oxycalyptra. Zaleya constantly has four seeds. Gisekia houses one seed per locule (Lu & Hartmann, 2003). The two species of Limeum contain two seeds © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 148, 189–206 Downloaded from https://academic.oup.com/botlinnean/article-abstract/148/2/189/2420379 by guest on 09 June 2020 1 SEED COAT MORPHOLOGY 8 9 10 11 12 Figures 7–12. Scanning electron micrographs of seeds of Aizoaceae s.s. Figs 7, 8. Cypselea humifusa (Van Proosdij 1126). Scale bars = 100 mm and 20 mm, respectively. Figs 9, 10. Sesuvium hydaspicum (Madsen 5264). Scale bars = 200 mm and 50 mm, respectively. Figs 11, 12. Sesuvium portulacastrum (Robertson 3680). Scale bars = 500 mm and 50 mm, respectively. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 148, 189–206 Downloaded from https://academic.oup.com/botlinnean/article-abstract/148/2/189/2420379 by guest on 09 June 2020 7 197 198 N. M. S. HASSAN ET AL. 14 15 16 17 18 Figures 13–18. Scanning electron micrographs of seeds of Aizoaceae s.s. Figs 13, 14. Trianthema glossistigma (Latz 9572). Scale bars = 200 mm and 50 mm, respectively. Figs 15, 16. Trianthema megasperma (Cowie 8758). Scale bars = 500 mm and 100 mm, respectively. Figs 17, 18. Trianthema oxycalyptra var. oxycalyptra (Fatchen 831). Scale bars = 500 mm and 100 mm, respectively. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 148, 189–206 Downloaded from https://academic.oup.com/botlinnean/article-abstract/148/2/189/2420379 by guest on 09 June 2020 13 SEED COAT MORPHOLOGY 20 21 22 23 24 Figures 19–24. Scanning electron micrographs of seeds of Aizoaceae s.s. and Gisekiaceae. Figs 19, 20. Trianthema sheilae (Collenette 9284). Scale bars = 200 mm and 50 mm, respectively. Figs 21, 22. Zaleya pentandra (s.n.). Scale bars = 500 mm and 50 mm, respectively. Figs 23, 24. Corbichonia decumbens (s.n.). Scale bars = 500 mm and 50 mm, respectively. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 148, 189–206 Downloaded from https://academic.oup.com/botlinnean/article-abstract/148/2/189/2420379 by guest on 09 June 2020 19 199 200 N. M. S. HASSAN ET AL. 26 27 28 29 30 Figures 25–30. Scanning electron micrographs of seeds of Gisekiaceae and Molluginaceae. Fig. 25. Gisekia pharnaceoides (s.n.). Scale bar = 500 mm. Fig. 26. Glinus lotoides (s.n.). Scale bars = 100 mm. Figs 27, 28. Limeum obovatum (Drar 797). Scale bars = 500 mm and 10 mm, respectively. Figs 29, 30. Mollugo nudicaulis (s.n.). Scale bars = 100 mm and 50 mm, respectively. for each, whereas the remaining species of Molluginaceae have several seeds. Seed colour Seed colour is significant in distinguishing some taxa. In Aizoaceae s.s., both Cypeselea humifusa and Mesembryanthemum cryptanthum have light brown seeds. Seeds of Sesuvium species (S. maritimum, S. portulacastrum, S. sessile, S. sesuvioides, S. verrucosum) are black and shiny, but non-brilliant in S. hydaspicum. Colours in Trianthema seeds vary from black, shiny black to dark brown, whereas seeds in Zaleya are black. Gisekiaceae and Molluginaceae have dark brown to shiny black seeds; only in Limeum spp. seeds are of an unusual pale yellow colour. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 148, 189–206 Downloaded from https://academic.oup.com/botlinnean/article-abstract/148/2/189/2420379 by guest on 09 June 2020 25 SEED COAT MORPHOLOGY General seed coat pattern Seed coat sculpture in Aizoaceae s.s. can be divided into four types: unsculptured, ridged, reticulate and papillose. Giseka has smooth seeds, but is additionally finely punctuated (pitted). Three types occur in Molluginaceae: rough, ridged and papillose. Anticlinal boundaries The manner of organization of the anticlinal boundaries is fairly variable. Within Aizoaceae s.s., we observe indistinct boundaries in most Sesuvium spp., and indistinct to sunken boundaries in S. portulacastrum (Fig. 12), Mesembryanthemum cryptanthum, M. nodiflorum and Trianthema compacta; indistinct to slightly raised boundaries in T. turgidifolia. Whereas slightly sunken boundaries are typical for Aizoanthemum and Aizoon, they are deeply sunken in M. crystallinum (Fig. 6); slightly to deeply sunken boundaries can be found in Trianthema patellitecta, and sunken to slightly raised ones are restricted to T. glossistigma (Fig. 14). The remaining taxa studied vary from having slightly to highly raised boundaries. The sculpture of anticlinal boundaries of most studied taxa varies considerably. It is smooth to folded (finely or, rarely, coarsely), straight or straight to curved. By contrast, Aizoon canariense has straight to strongly wavy boundaries (Fig. 4). In Gisekiaceae and Molluginaceae the anticlinal boundaries are characteristic. Very slightly raised, smooth and strongly wavy boundaries characterize Gisekia pharnaceoides, and slightly to deeply sunken ones are found in Corbichonia decumbens (Fig. 24) and Mollugo nudicaulis (Fig. 30). The latter two species have in common smooth to porous anticlinal boundaries (Figs 28, 32). Limeum obovatum and L. viscosum have strongly raised and straight anticlinal boundaries. In the former, they are broader and conspicuously laciniate (Fig. 28), whereas a longitudinal striation can be observed in the latter. Outer periclinal cell wall Outer periclinal cell walls do not play a major role in distinguishing the taxa of Aizoaceae s.s. Flat surfaces are shown in Cypselea humifusa (Fig. 8), Sesuvium maritimum, S. sessile, S. sesuvioides and S. verrucosum; flat to papillose ones in Trianthema cussackiana, T. megasperma (Fig. 16), T. pilosa and T. rhynchocalyptra; flat to convex ones in Mesembryanthemum cryptanthum and M. nodiflorum. There are concave surfaces in Sesuvium hydaspicum and Zaleya pentandra (perhaps sometimes due to shrinking processes as in Fig. 16), slightly concave in Trianthema glossistigma (Fig. 14), slightly or strongly convex in Aizoon hispanicum (Fig. 2) and strongly convex in Mesembryanthemum crystallinum (Fig. 6). Some taxa of Trianthema, e.g. T. megasperma (Fig. 16) and T. oxycalyptra (Fig. 18), have two distinct types of cells. Apart from the basal pattern, larger cells (idioblasts) are regularly interspersed. In T. cussackiana, idioblasts cover nearly the whole surface. In T. oxycalyptra, the large, elongated idioblasts cluster to complexes (Fig. 18). The remaining taxa in Aizoaceae s.s. are more or less flat to concave. Gisekia pharnaceoides has flat to very slightly concave periclinal walls (Fig. 25). Flat walls are seen in Limeum spp. (Fig. 28); flat to papillose ones in Glinum lotoides, which are terminated by a central papillae each in Corbichonia decumbens (Fig. 24) and strongly convex but basally constricted in Mollugo nudicaulis (Fig. 30). Surface sculpture Outer (secondary) wall sculpture shows that Aizoanthemum hispanicum and Mesembryanthemum crystallinum are conspicuously and densely covered with fine wax platelets (Figs 2, 6), but these are less © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 148, 189–206 Downloaded from https://academic.oup.com/botlinnean/article-abstract/148/2/189/2420379 by guest on 09 June 2020 Epidermal cells Outer wall outlines of epidermal cells of most of the studied taxa within Aizoaceae s.s. vary from isodiametrical-(penta)hexagonal to penta-hexagonal. However, some taxa have characteristic outlines, like the elongated ones of Aizoon canariense (Fig. 4), Mesembryanthemum crystallinum (Fig. 6), M. nodiflorum, Sesuvium hydaspicum (Fig. 10) and Trianthema glossistigma (Fig. 14). Penta-hexagonal to elongated epidermal cells occur in Zaleya decandra (Fig. 22) and Mesembryanthemum cryptanthum. Isodiametrical cells are represented in Trianthema megasperma and T. oxycalyptra var. oxycalyptra (Figs 16, 18). Sesuvium maritimum, S. Sessile, S. sesuvioides and S. verrucosum show an indistinct epidermal cell pattern, whereas indistinct to elongated epidermal cells are found in S. portulacastrum and T. compacta. The epidermal cells in Aizoaceae s.s. seem to be randomly distributed except for Aizoon canariense, Sesuvium hydaspicum (Fig. 10), S. portulacastrum (dorsally), T. compacta (dorsally only towards the hilum) and T. glossistigma (Figs 13, 14), where conspicuous cell rows can be observed. In Molluginaceae, epidermal cell shapes vary from penta-hexagonal as in Limeum spp. (Fig. 28) to elongated in Corbichonia decumbens (Fig. 24) or elongated-polygonal in Mesembryanthemum nudicaulis. In M. nudicaulis, unusual pores occur (Fig. 32). Glinus lotoides exhibits an undefined pattern. The arrangement of epidermal cells ranges from parallel rows in Corbichonia decumbens (Fig. 24) and Mollugo nudicaulis (Fig. 30) to randomly distributed in Gisekia pharnaceoides and Limeum spp. (Fig. 28). 201 202 N. M. S. HASSAN ET AL. To conclude, with regard to testa characters the investigated taxa can be grouped as follows Type 1. Seeds smooth as in Sesuvium maritimum, S. portulacastrum, S. sessile, S. sesuvioides, S. verrucosum, Trianthema compacta and Gisekia pharnaceoides (anticlinals undulated), or ± smooth in Trianthema patellitecta; periclinals often flat, slightly convex or very slightly concave; anticlinals indistinct or sunken. Type 2. Seeds reticulate; light brown; anticlinals raised; periclinals flat; and testa cells large: Cypselea humifusa. Type 3. Seeds smooth, with large isolated papillae: Glinus lotoides. Type 4. Seeds ± unsculptured; periclinals with simple idioblasts as in Trianthema cussackiana, T. megasperma, T. pilosa, T. rhynchocalyptra, or idioblast complexes in T. oxycalyptra var. oxycalyptra; anticlinals often raised or rarely indistinct; testa cells small. Type 5. Seeds continuously ridged. Ridges arranged concentrically in Aizoon canariense, Trianthema glossistigma, T. turgidifolia or concentrically to transversely in Aizoanthemum hispanicum; periclinals flat, convex or slightly concave; anticlinals vary from slightly sunken to slightly raised or rarely flat. Type 6. Seeds continuously transversely ridged; periclinals concave; anticlinals highly raised: Sesuvium hydaspicum. Type 7. Seeds discontinuously ridged. Ridges arranged more or less concentrically (Trianthema parvifolia, T. portulacastra, T. sheilae, T. triquetra), or almost randomly distributed (Zaleya decandra, Z. galericulata, Z. pentandra); periclinals flat, concave or rarely slightly convex; anticlinals slightly or highly raised. Type 8. Seeds discontinuously longitudinally and/or transversely ridged; periclinals flat to strongly convex; anticlinals indistinct or sunken and partly undulating; testa cells large, smooth or with wax cover: Mesembryanthemum cryptanthum, M. crystallinum, M. nodiflorum. Type 9. Seeds concentrically ridged, periclinals convex with or without papillae; anticlinals with pores: Corbichonia decumbens, Mollugo nudicaulis. Type 10. Seeds with rough surface, sometimes associated with ribs; pale yellow; slightly winged; periclinals flat, micropapillate; anticlinals highly raised, laciniate or with longitudinal striations: Limeum obovatum, L. viscosum. DISCUSSION In Caryophyllales seed morphology is of considerable significance for species delimitation (e.g. in Arenaria L., Caryophyllaceae; cf. Wofford, 1981). Between Aizoaceae and Molluginaceae a wide range of variation in seed shape, size and sculpturing occurs, providing considerable information of taxonomic value. In Aizooideae s.s. seeds seem to be fairly similar across the generic boundaries; however, they comprise a range from nearly flat to subpapillate periclinal testa cells (compare with Australian Gunniopsis Pax, Jessop, 1986). The Aizoaceae–Aizooideae Aizoanthemum and Aizoon are represented by testa character type 5 (Figs 1–4). Consequently, those two species are very similar with regard to general structure, although seeds of Aizoanthemum are much more strongly sculptured. The high similarity between Aizoon canariense and Trianthema glossistigma (both grouped under type 5) is probably due to convergence. Recently, Aizoanthemum has been separated from Aizoon by Hartmann (2001) because of its hygrochastic capsules opening completely through expanding keels. Our data add no further support for Hartmann’s separation except for the stronger seed sculpture in Aizoanthemum. However, differences in seed structure are of quantitative nature only except for the additional wax crystals in Aizoanthemum. But this dissimilarity is similar to that found, for example, within Mesembryanthemum. Mesembryanthemum (Aizoaceae–Mesembryanthemoideae) is defined by the presence of staminodes and a semi-inferior ovary (e.g. Bittrich & Struck, 1989). The genus is also uniform in possessing a single seed type (see type 8; Figs 5, 6). According to Bittrich & Struck (1989), Mesembryanthemoideae constitute a natural group. Seeds in the most species-rich subfamily Ruschioideae show much agreement with Mesembryanthemum, with large and predominantly isodiametrical testa cells causing rather regular pat- © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 148, 189–206 Downloaded from https://academic.oup.com/botlinnean/article-abstract/148/2/189/2420379 by guest on 09 June 2020 prominent in M. nodiflorum. In addition, in M. crystallinum coarse wax crystals occur on the anticlinals (Fig. 6). The remaining taxa seem to have no wax coverage. Usually, the surfaces are very smooth or slightly uneven, rarely with additional single wax crystals. Secondary sculpturing varies from smooth in G. pharnaceoides, G. lotoides, C. decumbens or crossstriated in M. nudicaulis (Fig. 30) to micropapillate in the two species of Limeum (Fig. 28). SEED COAT MORPHOLOGY raised in the other species, and periclinal walls range from flat to slightly convex in T. sheilae to flat to concave in the remaining two species (e.g. Figs 21, 22). The close relationship among those taxa is also reflected in macromorphological features such as cymose inflorescences, flowers arranged in three-flowered dichasia, perianth not exceeding 3 mm in length and five stamens (up to 1 mm long) alternating with the perianth lobes. Finally, this relationship is corroborated by analysis of an nDNA marker (ITS, Hassan et al., in press). The occurrence of isolated idioblasts characterizes Trianthema megasperma, T. cussackiana, T. pilosa, T. rhynchocalyptra and T. oxycalyptra. All these species except T. cussackiana share the synapomorphic character of trichomes distributed over the plant’s surface. The correlation of morphological characters among T. megasperma, T. pilosa and T. rhynchocalyptra, again, is supported by ITS data (Hassan et al., in press). A unique seed coat morphology (Fig. 18) permits identification of T. oxycalyptra var. oxycalyptra (cf. also Clark & Jernstedt, 1978). However, the characteristic idioblast complexes of the testa have probably evolved easily from single idioblasts such as those of T. megasperma (Fig. 16). Micromorphological diversity is very high in Trianthema compared with the other Sesuvioideae genera, but also compared with the genus- and species-rich Ruschioideae. In the latter, the testa patterns rarely vary considerably within a single genus (except for large ‘dust-bin genera’ as such as Lampranthus N. E. Br. or Ruschia Schwantes, e.g. Liede, 1989). Usually, a particular seed type is fairly dominant within a single genus (Liede, 1989; Hartmann, 1996). Zaleya is represented by type 7 only. The ornamentation of the seed coat of Zaleya is similar to Trianthema but it is more prominently ridged. The three species of Zaleya investigated share colour, shape and most other seed features (e.g. Figs 23, 24). Both Z. pentandra and Z. galericulata constitute a very well-supported clade based on sequence data of the ITS region (Hassan et al., in press). Zaleya had previously been included in Trianthema, but it was separated from Trianthema based on the possession of capsules with a two-valved operculum, two locules, four ovules and two stigmas (Jeffrey, 1960; Hartmann, 2001). Gisekia pharnaceoides (Gisekiaceae) seeds are simple and smooth (see type 1). They mainly differ from the smooth seeds of Sesuvium species in the possession of broad and undulate anticlinal boundaries in addition to pitted periclinal walls (Fig. 25). Gilbert (1993) stated that Gisekia has no really unique characters but possesses distinct combinations. This is true for the seed coat as well, because highly signifi- © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 148, 189–206 Downloaded from https://academic.oup.com/botlinnean/article-abstract/148/2/189/2420379 by guest on 09 June 2020 terns (cf. Liede, 1989; Hartmann, 1996). Some taxa are additionally equipped with (knobby) papillae (Acrodon; Hartmann, 1996), similar to those of Trianthema (Aizoaceae–Sesuvioideae). But this coincidence could be also of convergent nature. Aizoaceae–Sesuvioideae seeds were shown to be fairly homogeneous, although some special seed types are interspersed. Cypselea humifusa represents a single and unique seed type. The unusual ovoid seeds have smooth and large testa cells with raised anticlinal walls, leading to a conspicuously reticulate pattern of the seed surface (Figs 7, 8). This peculiarity underlines the isolated position of this genus, which comprises just three species (according to Hartmann, 2001) restricted to the Americas including the Caribbean. Five of the six species of Sesuvium investigated show simple and smooth seeds. Only S. hydaspicum differs largely with its strong transverse ridges. Although it is superficially similar to other seeds of our type 7, it is different because the ridges are due to convex isodiametric cells alternating with elongated depressed ones in the depression in between. Seed morphology points to a closer relationship of Sesuvium hydaspicum with Zaleya and Trianthema than with Sesuvium. However, S. hydaspicum (Figs 9, 10) has been included in S. sesuvioides (e.g. Hartmann, 2001), but was reinstated by Gonçalves (Gilbert, Hartmann & Edwards, 2000), because he (Gonçalves in Gilbert et al., 2000) considered that S. sesuvioides should be used only for certain Angolan and Namibian specimens with smooth seeds. Molecular analysis (ITS; Hassan, Thiede & Liede-Schumann, in press) shows that both taxa, although not conspecific, are indeed closely related. However, seed coat features contradict this result. Both taxa still need attention with regard to further characters such as chromosome numbers and ecological behaviour. Trianthema seeds are spread over four of our types (types 1, 4, 5 and 7), demonstrating a fairly variable genus, but without questioning its single genus status. Seeds vary from continuously concentrically ridged in Trianthema glossistigma and T. turgidifolia to discontinuously ± concentrically ridged in T. parvifolia, T. portulacastra, T. sheilae and T. triquetra, whereas T. patellitecta shows faintly reticulate seeds. Moreover, the differences in morphological characters among those species are considerable. However, Trianthema parvifolia, T. sheilae and T. triquetra can be grouped together based on seed features such as more or less equal size, shiny black colour and orbicular shape in T. parvifolia, or ovoid-elliptical in T. sheilae and T. triquetra. Epidermal cells are isodiametric to penta-hexagonal in T. parvifolia and T. triquetra and pentahexagonal in T. sheilae. Anticlinal wall boundaries vary from highly raised in T. triquetra to slightly 203 204 N. M. S. HASSAN ET AL. REFERENCES Barthlott W. 1981. Epidermal and seed surface applicability and some evolutionary aspects. Nordic Journal of Botany 1: 345–355. Barthlott W. 1983. New evidence from the ultrastructural and micromorphological fields in angiosperm classification. Nordic Journal of Botany 3: 43–66. Barthlott W. 1984. Microstructural features and seed surface. In: Heywood V, Moore DM, eds. Current concepts in plant taxonomy. London: Academic Press, 95–105. Barthlott W, Ehler N. 1977. 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