EXTANT SEED PLANTS

Plant woody, evergreen; nicotinic acid metabolised to trigonelline; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins rich in guaiacyl units; true roots present, xylem exarch; shoot apical meristem complex; arbuscular mycorrhizae +; stem with ectophloic eustele, endodermis 0, xylem endarch; vascular tissue in t.s. discontinuous by interfascicular regions; vascular cambium + [xylem ("wood") differentiating internally, phloem externally]; wood homoxylous, tracheids +; tracheid/tracheid pits circular, bordered; sieve tube/cell plastids with starch grains; phloem fibers +; stem cork cambium superficial, root cork cambium deep seated; nodes ?; leaf vascular bundles collateral; leaves spiral, simple, axillary buds?, prophylls [including bracteoles] two, lateral; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores] +, mono[ana]sulcate, pollen exine and intine homogeneous, ovules unitegmic, crassinucellate, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development endo/exosporic, gametes two, with cell walls; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large", first cell wall of zygote transverse, embryo straight, endoscopic [suspensor +], short-minute, with morphological dormancy, white, cotyledons 2; plastid transmission maternal; two copies of LEAFY gene, PHY gene duplication, mitochondrial nad1 intron 2 and coxIIi3 intron present.

MAGNOLIOPHYTA

Plant woody, evergreen; lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, cyanogenesis via tyrosine pathway, lignins derived from both coniferyl and sinapyl alcohols, containing syringaldehyde [in positive Maüle reaction, syringyl:guaiacyl ratio less than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0; stem with 2-layered tunica-corpus construction; wood fibers and wood parenchyma +; reaction wood ?, with gelatinous fibres; starch grains simple; primary cell wall mostly with pectic polysaccharides; tracheids +; sieve tubes eunucleate, with sieve plate, companion cells from same mother cell that gave rise to the tube, the sieve tube with P-proteins; nodes unilacunar; stomata with ends of guard cells level with aperture, paracytic; leaves with petiole and lamina [the latter formed from the primordial leaf apex], development of venation acropetal, 2ndary veins pinnate, fine venation reticulate, vein endings free; flowers perfect, polysymmetric, parts spiral [esp. the A], free, numbers unstable, P not differentiated, outer members not enclosing the rest of the bud, A many, development centripetal, with a single trace, introrse, filaments stout, anther ± embedded in the filament, tetrasporangiate, dithecal, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally by action of hypodermal endothecium, endothecial cells elongated at right angles to long axis of anther, tapetum glandular, binucleate, microspore mother cells in a block, microsporogenesis successive, pollen subspherical, binucleate at dispersal, trinucleate eventually, tectum continuous, endexine compact, lamellate only in the apertural regions, pollen tube elongated, with callose plugs, penetrating between cells, growth rate moderate, siphonogamy occuring, nectary 0, G free, several, ascidiate, with postgenital occlusion by secretion, few [?1] ovules/carpel, ovules marginal, anatropous, bitegmic, micropyle endostomal, integuments 2-3 cells thick, megasporocyte single, megaspore lacking sporopollenin and cuticle, chalazal, female gametophyte ?type, stylulus short, stigma ± decurrent, wet [secretory]; P deciduous in fruit; seed exotestal; double fertilisation +, endosperm ?diploid, cellular [first division oblique, micropylar end initially with a single large cell, chalazal end more actively dividing], copious, oily and/or proteinaceous, embryo cellular ab initio; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; whole genome duplication, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and PHYA/PHYC gene pairs.

Possible apomorphies are in bold. Note that the actual level to which many of these features, particularly the more cryptic ones, should be assigned is unclear, because some taxa basal to the [magnoliid + monocot + eudicot] group have been surprisingly little studied. Furthermore, details of relationships among gymnosperms will affect the level at which some of these characters are pegged.

NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessels +, elements with scalariform perforation plates; pollen tectate-columellate, tectum reticulate [perforated]; nucleus of egg cell sister to one of the polar nuclei; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.

PROTEALES [TROCHODENDRALES [BUXALES [GUNNERALES + CORE EUDICOTS]]]: ?

TROCHODENDRALES [BUXALES [GUNNERALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.

BUXALES [GUNNERALES + CORE EUDICOTS]: ?

GUNNERALES + CORE EUDICOTS: Ellagic and gallic acids common, cyanogenesis via phenylalanine, isoleucine or valine pathways; micropyle?; PI-dB motif +, small deletion in the 18S ribosomal DNA common.

CORE EUDICOTS: Root apical meristem closed; flowers rather stereotyped: 5-merous, parts whorled, K and C distinct, K with 3 traces, A = 2x K, internal to the C whorl, (numerous, but then often fasciculate and/or centrifugal), pollen tricolporate, (nectary disc +), [G 5], [3] also common, compitum +, placentation axile, stigma not decurrent; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; euAP1 + euFUL + AGL79 genes [duplication of AP1/FUL or FUL-like gene], PLE + euAG [duplication of AG-like gene: C class], SEP1 + FBP6 genes [duplication of AGL2/3/4 gene].

This clade is strongly supported, e.g. Chase et al. (1993), D. Soltis et al. (1997, 1999, 2003a), Hoot et al. (1998), Nandi et al. (1998), although Gunnerales (q.v.) have in the past also been associated with core eudicots; Gunnerales and core eudicots are sister taxa. Note that not all major groups have been sampled for the euAP1 gene, duplication of the C genes, etc. (e.g. Litt & Irish 2003; Kramer et al. 2004).

SANTALALES Dumortier  Main Tree, Synapomorphies.

Mycorrhizae absent; polyacetylenes [triglycerides with C18 acteylenic acids], triterpenic sapogenins + [Loranthaceae?]; cork subepidermal; perforation plates not bordered; intervascular pits alternate; tension wood?; pericyclic fibers 0; (cuticle waxes with annular rodlets, palmone common); petiole/mesophyll with astrosclereids; lamina entire; inflorescences cymose; K often reduced, C valvate, A opposite C, epipetalous, anthers basifixed, pollen colpate or porate, disc +, 1 pendulous apotropous tenuinucellate ovule/carpel, micropyle endostomal, style +, stigma small, globose; fruit a drupe, 1-seeded, K persistent; seed coat crushed; endosperm cellular, chalazal haustorium +, embryo short/minute. - 8 families, 151 genera, 985 species.

See the Berberidopsidales page for discussion on the relationships of Santalales, which have no firm position as yet.

Anderson et al. (2005) date stem group Santalales at 115-113 million years before present, crown group members at 108-101 million years before present (sampling is adequate). Caterpillars of some Pieridae-Pierinae (ca 440 species recorded, but on only 9+ genera; 2/5 of all host-plant records) and Lycaenidae-Lycaeninae-Iolaini in particular are found on members of this order, Loranthaceae (especially), "Olacaceae" (= Ximenia/ Olax, Lycaeninae), Opiliaceae and Santalaceae being recorded hosts (Ehrlich & Raven 1964; Fiedler 1991, 1994; Congdon & Bampton 2000). The ancestors of the pierine butterflies seem for the most part to have eaten members of Brassicales and their initial santalalean hosts may have been Loranthaceae; again, there are no reports of caterpillars on free-living Santalales (Braby 2005; Braby & Trueman 2006; Braby et al. 2006: I thank M. F. Braby for information). Interestingly, a number of the adults of these butterflies have warning colourations on the undersides of the wings, and some caterpillars may also have warning colorations. However, it is unclear what compounds the insects might pick up from their santalalean hosts that would discomfit potential predators (Braby & Trueman 2006).

Although little is known about mycorrhizae in Santalales, the few taxa studied largely lack them (Landis et al. 2002), exceptions being Ongokea, Coula and Strombosia, scattered in ex-Olacaceae (Malécot 2002 for references). The absence of mycorrhizae, as well as that of root hairs which has been reported for the group (see below), could be connected with the adoption of the hemiparasitic habit.

There are several other distinctive features in Santalales whose systematic significance is unclear. Absence of root hairs may be a synapomorphy (Judd & Olmstead 2004), but are they also absent from Erythropalaceae? The pits are notably variously bordered throughout the order (Herendeen et al. 1999b); Carlquist (2006) suggests that non-bordered perforation plates is a possible similarity with Caryophyllales, although the that group may rather be closer to Dilleniales. The foliar vascular bundles may lack fibers (but cf. Olacaceae, Loranthaceae, ?some Opiliaceae). Terminal tracheids and cristarque cells are scattered, but their exact position on the tree is unclear (Baas et al. 1982; Kuijt & Lye 2005). Wax tubules with palmitone as the main wax occur in several members (Ditsch & Barthlott 1997). Tracheids in the nucellus has been reported from some species, as has vascular tissue reaching the embryo sac (Werker 1997). The mitochondrial coxII.i3 intron is absent in Comandra, the only member of the order to have been sampled.

Malécot (2002) provides a phylogeny based on the analysis of variation in four genes that emphasises members of the old Olacaceae; he discusses variation of morphological characters in the context of this phylogeny and also provides analyses of a combined morphological-molecular data set. Although there is still little well-supported structure along the spine of basal Santalales (= Olacaceae s.l.: see the tree given here), a number of clades appear to be fairly well established. Hence Malécot's results and classification are largely followed here; they suggest i.a. that (hemi)parasitism is derived within the clade (see also Malécot et al. 2004), the Erythropalaceae, sister to all other Santalales, being free-living. Within the Loranthaceae clade, Misodendraceae are often sister to [Schoepfiaceae + Loranthaceae], especially in analyses that include many taxa, although when the number of taxa is reduced they may be sister to Schoepfia in particular (Malécot 2002, see also Nickrent et al. 1998 ans especially Der é Nickrent 2008); this position is followed here. Erythropalaceae, although poorly supported, differ in many features other than life style from other Santalales, and many of these are probably plesiomorphic (data from Michaud 1966; Malécot 2002 - see also Malécot et al. 2004 for a morphological phylogenetic analysis). However, confirmation of where they should be placed on the tree waits for strongly-supported resolution of relationships within Santalales and between Santalales and other core eudicots. Malécot et al. (2004) found some support for Erythropalaceae, Ximenia plus some other genera, and most of the rest of Olacaceae (a very weakly supported clade) as successively sister to the rest of Olacales in a morphological analysis. Malécot and Nickrent (2008) found the old Olacaceae to form about eight clades basal to other Santalales, but relationships between these clades were unclear. Recently Nickrent et al. (2005) found that Mystropetalum, Dactylanthus, and Hachettia, three members of Balanophoraceae, formed a clade with 100% posterior probability that was sister to a clade made up of Schoepfia, Dendrophthoe and Santalum (almost 100%), the combined group having 100% support, so Balanophoraceae are included in Santalales here, but without any particular position in the clade (see also Barkman et al. 2007). Further work is needed to resolve details of all these relationships, especially increased sampling in Balanophoraceae, which are the only Santalales known to be holoparasitic. However, being holoparasitic, they lack most or all of the distinctive vegetative features of other Santalales.

Santalales have often been compared with Icacinaceae (e.g. Takhtajan 1997), but there is little evidence suggesting such a relationship.

For general information, see Barlow (1997), Calder and Bernhardt (1983), and Reed (1955), for anatomy, see Baas et al. (1982), for hemi-parasitism, see Fineran (1991), and for additional information on relationships, see Nickrent and Duff (1996), Nickrent et al. (1998), for pretty much everything, see Parasitic Plants website (Nickrent 1998 onwards).

Includes Balanophoraceae, Erythropalaceae, Misodendraceae, Olacaceae, Opiliaceae, Loranthaceae, Santalaceae, Schoepfiaceae.

Synonymy: Anthobolales Dumortier, Balanophorales Dumortier, Erythropalales van Tieghem, Heisteriales van Tieghem & J. D. Hooker, Loranthales Dumortier, Olacales Bentham & J. D. Hooker, Viscales van Tieghem, Ximeniales van Tieghem - Balanophoranae Reveal, Santalanae Reveal - Loranthopsida Bartling, Santalopsida Brongniart

ERYTHROPALACEAE Miquel, nom. cons.   Back to Santalales

Trees, shrubs or lianes; (plants Al-accumulators; arbuscular mycorrhizae +; (laticifers +); vessel elements with scalariform perforations; rays <7 cells wide; sieve tubes with non-dispersive protein bodies; nodes 3:3 (5:5); petiole bundle annular (with adaxial plate); (epidermis lignified; with druses), stomata anisocytic (other), cuticular thickening +, large guard cell chamber; (hairs stellate); leaves spiral or 2-ranked, conduplicate; (plant dioecious), inflorescence various; flowers small, 3-6-merous, hypanthium + or 0, K small, often cupular, teeth inconspicuous, C basally connate and with adaxial hairs or not, A = or 2 (3) x C (some staminodial), connective massive (not), (pollen colporate), (disc 0; extrastaminal), G [(2)3(-5)] (semi-inferior), opposite K (opposite C) or odd member adaxial, septate (not), ovules (horizontal), (unitegmic), style short to long, stigma lobed or not; (K much accrescent); endosperm with starch or oil, embryo green, minute, cotyledons 1-2, connate or not; n = 16, 19, 20.

13/65. Pantropical, Southeast Asia, not Madagascar, New Guinea and to the S.E. (Map: from Michaud 1966; Sleumer 1984a, b; Malécot 2002).

The stamens differ quite considerably in size, and the smallest stamens are opposite the petals, the largest stamens opposite the sepals (Michaud 1966). The gynoecium is often 10-ridged.

For some information on pollen, see Lobreau-Callen (1982).

The name Erythropalaceae for this clade may be incorrect, but I will keep it as it is, pending further studies to clarify the phylogeny of this part of Santalales.

Synonymy: Coulaceae van Tieghem, Heisteriaceae van Tieghem, Octoknemaceae Solereder, nom. cons. (cristarque cells +; G inferior; fruit drupaceous; seed longitudinally ruminate, embryo short, radicle very long, cotyledons 6), Scorodocarpaceae van Tieghem, Strombosiaceae van Tieghem, Tetrastylidiaceae van Tieghem (anthers polythecate).

"Olacaceae" [[[Misodendraceae + Schoepfiaceae] Loranthaceae] [Opiliaceae + Santalaceae]]: root hemiparasites; vessel elements with simple perforations; rays >7 cells wide; nodes 1:1; sclerenchyma fibres of petiole and median vein 0; petiole bundle arcuate; stomata paracytic; silicification of some foliar mesophyll/epidermal cells; embryo sac with chalazal caecum and ± developed micropylar prolongation.

For some information on the physiological details of parasitism in this clade, see Stewart and Press (1990). Graniferous tracheary elements are found in the haustoria of several unrelated members of the clade; the granules are usually proteinaceous, but are made up of starch in Ximenia (Fineran & Ingerfeld 1982). It is difficult to assign ovary position to a particular place on the tree. Olaceae have a superior ovary, and so do [Exocarpos + Omphalomeria] " a basal clade" in Santalaceae (Der & Nickrent 2005), Loranthaceae are inferior, Schoepfiaceae are half inferior. Either there are independent origins for the characters of inferior ovary, or reversals, or even both.

Ovule, embryo sac and embryo development of many Santalales, but probably not Erythropalaceae, is more or less remarkable. Distinct ovules may not be recognizable, the embryo sacs being borne in a spherical body, the mamelon; this consists of a basal placenta and everything else. Individual embryo sacs may elongate greatly and approach the apex of the mamelon or even the stigma at the end of a long style; Haig (1990) suggests that this may represent competition between female gametes given that their normal spatial constraints (i.e., being enclosed in an organised ovule) are absent. In any event, after fertilization the embryo is "planted" back down at the base of the mamelon by the development of a long suspensor (Fagerlind 1947a, 1948; Maheshwari 1950; Ram 1970; Bhatnagar 1970; Bhandari & Vohra 1983; Johri et al. 1992; Shamrov et al. 2001, and references).

"OLACACEAE" R. Brown, nom. cons.   Back to Santalales - note, probably paraphyletic.

Trees, shrubs or lianes; (plants Al-accumulators); sieve tubes with non-dispersive protein bodies; cuticle wax crystalloids 0 (platelets); cuticular thickening +, guard cell chamber small; leaves spiral or 2-ranked, conduplicate; (plant dioecious), inflorescence various; flowers small, 3-6-merous, hypanthium + or 0, K small, often cupular, teeth inconspicuous, C (imbricate), basally connate and with adaxial hairs or not, A = or 2x C, (staminodes +), connective massive (not), (pollen colporate), (disc 0; extrastaminal), G [(2)3(-5)] (semi-inferior), opposite K (opposite C) or odd member adaxial, septate (not), ovules unitegmic, style short to long, stigma lobed or not; endosperm (helobial), with starch or oil, embryo green (often?), minute.

14[list]/103. Pantropical (subtropics). [Photo - Flower, Fruit, Fruit.]

1. Olacoideae

SiO₂ bodies in ray cells; (nodes 3:3 - Dulacia); A 1-2 x C, (staminodes 3-6), G [3], ridged or not, ovules unitegmic; (K much accrescent); cotyledons 0-1; n = 12.

3/57. Pantropical (also S.E. China, Formosa) (Map: from Sleumer 1984a, b; George 1984; Malécot 2002).

Again the smaller stamens may be opposite the petals, the larger stamens opposite the sepals. Olacoideae are ategmic, and Olax has endosperm haustoria reaching into the pedicel.

2. Anacalosoideae

(Arbuscular mycorrhizae + - Ongokea); (laticifers +); (bundle fibers +); flowers 4-5 merous; (A extrorse, porose or valvate; pollen 6-aperturate), G 2-3, ovules often bitegmic; (K much accrescent); cotyledons 0-2, connate or not; n = ?

7/32. Pantropical (SE China, Formosa) (Map: from Michaud 1966; van Balgooy 1993; Sleumer 1984a, b; Malécot 2002).

Synonymy: Aptandraceae Miers (A connate around style, anthers reflexed and so extrorse - 3 genera. Ongokea has polyacetylenes, just like other Olacaceae), Cathedraceae van Tieghem, Chaunochitonaceae van Tieghem, Harmandaceae van Tieghem

3. Ximenioideae

Nodes 3:3; ovules uni- or bitegmic; Flowers 4-5-merous, A 1-2 x C; cotyledons 2, connate or not; n = 12, 13; germination hypogeal.

4/13. Pantropical, warm temperate (Map: from van Balgooy 1993; George 1984; Sleumer 1984a, b; Malécot 2002).

Ximenia americana is crassinucellate.

Synonymy: Ximeniaceae Martinet

Within "Olacaceae", a number of taxa have green, zig-zag twigs; taxa with parallel tertiary venation are also quite common.

Brachynema has spiral leaves that are very unequal in size along the one innovation and blades with glandular teeth, the long petiole is pulvinate at both ends, and it has numerous other distinctive features. Although Lobreau-Callen (1980) placed it in Anacoloseae and Baas et al. (1982) paired it with Scorodocarpus in particular, it is best left unassigned to any family, and is here treated as an unplaced eudicot - see Brachynema.

Cristarque cells are reported by Breteler et al. (1996). There is considerable discussion as to the number of integuments (e.g. information in Maas et al. 1992; Breteler et al. 1996; Malécot 2002), as well as cotyledon number.

Some data are taken from Baas et al. (1982: anatomy), Lobreau-Callen (1980: pollen), Robertson (1982: general) and Sleumer (1984: general).

[[Misodendraceae + Schoepfiaceae] Loranthaceae] [Opiliaceae + Santalaceae]: guard cells not lignified; G not septate, ovules ategmic; testa 0; endosperm oily, starch 0.

Misodendraceae + Loranthaceae + Schoepfiaceae: cambium storied; petiole astrosclereids 0; guard cell thickenings?; epidermal cells sclerified, with druses; K minute, G [3].

MISODENDRACEAE J. Agardh, nom. cons.   Back to Santalales

Stem parasites; stem apex aborting; bundle fibers +; sieve tube plastids lacking starch and protein inclusions; plant dioecious; inflorescence (compound) raceme or spike; pedicels pubescent; staminate flowers: P 0, A 2-3, monothecal, pollen 4-12-colporate, spinuliferous; carpellate flowers: C 3, staminodes alternate with P, G 3, ovules straight [atropous]; fruit dry, attached to 3 much accrescent staminodes growing from slits in the ovary to one side of the attachment of the C; seed coat with some sclereids; endosperm 0-copious, embryo short to large, cotyledons connate [Misodendron, at least]; n = ?; germination epigeal.

1/8. Cool temperate South America (Map: from Heywood 1978). [Photos - Misodendron Flower, Misodendron Habit]

• Misodendraceae are dioecious stem parasites (their hosts are Nothofagaceae) that are recognizable by their stems, which are often thick, even when young, "giving the leafy species a rather elephantine appearance" (Kuijt 1969, p. 76). The leaves may be reduced, and those on flowering shoots are different from those on vegetative shoots; the two kinds of shoots are sharply distinguished. The flowers are small, and the small, nutlike fruits are very distinctive with their three, long, plumose attachments.

Vidal-Russell and Nickrent (2006, 2007) estimate that stem parasitism in Misodendraceae evolved some time after the divergence of this clade, ca 75 million years before present, but well before stem parasitism in Loranthaceae, ca 40 million years before present.

According to Takhtajan (1997) the pollen is colpate. Antidaphne seems to have three vascular traces in its cotyledons.

For general information, see Kuijt (1969), for seeds and seedlings, see Kuijt (1982: corrections to earlier work), for details of wood anatomy, see Carlquist (1985c), and for a phylogeny, see Vidal-Russell and Nickrent (2007)..

SCHOEPFIACEAE Blume   Back to Santalales

Aliform confluent parenchyma +; hairs unicellular; bract immediately below and surrounding G; flowers distylous, C tubular, with adaxial hairs, pollen tetrahedral, heteropolar, colporate, apertures ± confluent, ektexine psilate, G semi-inferior, basally septate, ovules ?unitegmic; embryo short; n = 12.

3/55: Quinchamalium (25). Central and South America, a few species in tropical South East Asia-Malesia (Map: incomplete, from Sleumer 1984, South East Asian mainland only approximate distribution). [Quinchamalium flower.]

That Schoepfia is rather different from Olacaceae has often been remarked (e.g. Metcalfe & Chalk 1950; Sleumer 1984); the latter noted that the wood had aliform-confluent parenchyma. There are prominent bracteoles immediately below its flowers which look not unlike those of Loranthaceae, and the calyx and pollen of Schoepfia are also similar to those of Loranthaceae. However, pollen aperture development in Schoepfia follows Garside's Rule, there being three pores at four points in the tetrad (see Blackmore & Barnes 1995). Arjona, ex Santalaceae, is sister to Schoepfia (Malécot 2002), and Quinchamalium, another ex Santalaceae, is also to be included in this clade; support for these relationships is strong (Vidal-Russell & Nickrent 2006; Der & Nickrent 2008). The family description has not yet been modified to take into account these two genera, however, the family is poorly known.

Synonymy: Arjonaceae van Tieghem

LORANTHACEAE Jussieu, nom. cons.   Back to Santalales

Ellagic acid +; parenchyma apotracheal; cuticular epithelium developing; (stomatal orientation transverse); indumentum quite often complex; leaves opposite (spiral); (plant dioecious); flowers (slit-monosymmetric), (3-)5-6(-9)-merous, C (0), connate, (A septate), pollen usu. triradiate to triangular, apertures confluent or not, G 1-5(-many) [from "ovules"], inferior, placentation (axile - Lysiana) basal, ovules 4-12, not clearly distinguished, gametophyte growing (to tip of style) or not; fruit a berry (nut), "hypostase" [= collenchymatous zone below the embryo sacs] +, mesocarp viscous, with rubber; endosperm copious, composite [derived from several ovules], suspensor long, first cleavage of zygote vertical [?distribution], embryo green; n = (8-)12.

68[list]/950 - 2 groups below. World-wide.

1. Nuytsia

Fruit dry, winged; cotyledons 3-4, foliaceous.

1/1: Nuytsia floribunda. S.W. Australia (Map: from FloraBase 2006).

2. The Rest

Stem parasites, forming burl at point of attachment and with epicortical roots running over the surface and often forming secondary burls; embryo ± plug-shaped, (cotyledons connate): no radicle, primary haustorium +; (germination cryptocotylar).

67/950: Tapinanthus (250), Amyema (95), Psittacanthus (50), Struthanthus (50), Phthirusa (40). World-wide; although common in Australia and apparently (one might have thought) easily dispersed, unknown from Tasmania (Map: from Meusel et al. 1965; Jäger 1970; Barlow 1983; Polhill & Weins 1998). [Photo - Flower]

• Loranthaceae are usually stem parasites that form secondary points of attachment along the stem. They are recognizable by their more or less opposite, often rather thick and brittle (especially when dry) leaves with entire margins and inconspicuous venation born on stems that are not jointed. Their 4-5-merous flowers are usually quite long, narrowly tubular and brightly colored - often red and/or orange - and lack much in the way of a calyx; the ovary is inferior and the fruits are fleshy. The flowers often have a bract/bracteoles at the base and immediately to one side of the ovary.

How loranthaceous seeds are dispersed, whether after moving through the gut, or by regurgitation, varies; the behaviour of the disperser is sometimes modified in distinctive ways. Thus Dicaeidae are involved in the pollination of Malesian Loranthaceae, in some taxa the flower opens only if it is pecked by the bird. Dicaediae are also involved in dispersal, the seeds passing very quickly through the gut and being deposited on a branch, the bird sometimes showing distinctive behaviour as it defecates, swinging its body parallel to the branch so the seed lands on the branch (Docters van Leeuwen 1954 in particular; Polhill & Wiens 1998 and references). Loranthaceae are the major hosts for caterpillars of pierid and lycaenid butterflies in Santalales (see introduction to Santalales for literature). Within Iolaini (Lycaenidae) caterpillar preferences show quite a good agreement with the classification of Pohill (1998), in particular, most Iolaini are found either on tapinanthoid or taxilloid genera, the two main African groups of the family (Congdon & Bampton 2000). Caterpillars of the pierid Delias occur on Malesian Loranthaceae (Docters van Leeuwen 1954).

The root parasitic habit, as in Nuytsia, is probably plesiomorphic in the family, since Nuytsia is sister to the rest of the family (Vidal-Russell & Nickrent 2005). It is also known from Atkinsonia (S.E. Australia) and Gaiodendron (Central and South America), other genera that may also be near the base of the phylogeny, although there is rather weak support for the stem parasite Notanthera being sister to all Loranthaceae except Nuytsia (Wilson & Calvin 2006a, b). It is estimated that the stem/branch parasitic habit evolved ca 40 million years before present (Vidal-Russell & Nickrent 2006). In such parasites, the host-parasite junction may be much swollen, producing wood roses in the host. Details of the morphological nature of the association bewteen stem parasite and hosts varies, and the epicortical roots - which may be plesiomorphous in the aerial parasites - form either sympodial or monopodial systems (e.g. Polhill & Weins 1998; Calvin & Wilson 2006; Wilson & Calvin 2006b). Wilson and Calvin (2006a, b) discuss the evolution of the various kinds of host attachments, although given the weak support for relationships at the base of the tree it is premature to worry too much about how many times aerial parasitism has evolved. Some Loranthaceae are hyperparasites, parasitizing other Loranthaceae. In Australia, the shapes of loranth leaves and of the eucalyptus host on which they grow are similar; explanations for this vary and this phenomenon is at most uncommon elsewhere (Barlow & Wiens 1977). Pollination in a few taxa is explosive.

Mitochondrial genes from a presumably root-parasitic member of Loranthaceae seem to have been acquired by the fern Botrychium, perhaps via a common mycorrhizal associate (Davis et al. 2005b). However, in general mycorrhizae are not very common in Santalales and if the gene transfer took place in Asia, as is suggested, the apparent absence of root-parasitic Loranthaceae from that area is notable - perhaps they have gone extinct.

The embryo sac in Moquiniella is some 48 mm long, the longest in the angiosperms; it grows up the style and then may grow back downwards after reaching the stigma (this is sometimes called an embryo sac haustorium - see Mikesell 1990), and other members of the family have embryo sacs nearly as long. Both Cronquist (1981) and Takhtajan (1997) describe the endosperm as being starchy, but it is not so scored in Malécot (2002). In many Old World Loranthaceae the cotyledons are connate, but not basally; the plumule emerges through the basal slit (Kuijt 1969).

Polysymmetrical 6-merous flowers seem to be plesiomorphous in the family (Wilson & Calvin 2006).

Loranthaceae and Viscaceae (here included in Santalaceae) have often been considered to be close, even being put in a single family, but there are numerous features separating the two; Kuijt (1969), Raj (1970) and Polhill and Wiens (1998) provide useful tables of differences, and see also Santalaceae here. Thus the viscous covering of the seeds is mesocarpial in origin, being outside the vascular bundles (cf. Viscaceae [= Santalaceae]). Furthermore, the fruits contain rubber (and are used in bird lime), another difference between Loranthaceae and Viscaceae. Although some Loranthaceae such as Phthirusa have very small flowers and congested inflorescences, they still may readily be separated from Viscum and its relatives. Plants of the latter are often lighter green in color, they lack the roots running over the surface of the host, the flowers are often three-merous, and the endosperm is green, etc.

For embryology, etc., see Raj (1970), for seedlings of neotropical Loranthaceae, see Kuijt (1982), for foliar anatomy, see Kuijt and Lye (2005: terminal tracheids and cristarque cells common), and for phylogeny, see Vidal-Russell and Nickrent (2005; summary).

Synonymy: Dendrophthoaceae Nakai, Elytranthaceae Nakai, Gaiadendraceae Nakai, Nuytsiaceae Nakai, Psittacanthaceae Nakai

Opiliaceae + Santalaceae: P as a single whorl only.

The single perianth whorl is probably equivalent to the corolla of other members of the order, where the calyx is often small; Hiepko (1984) called this single whorl the perianth in Opiliaceae only because there was no obvious calyx.

OPILIACEAE Valeton, nom. cons.   Back to Santalales

Root parasitic trees or shrubs (lianes); tanniniferous?; wood often fluorescing; nodes 1:(1), 3, 5; mesophyll lacking sclerified cells; cystoliths +/0; stomata paracytic, transversely oriented on the stem [Anthoboleae]; leaves 2-ranked to spiral; inflorescences axillary ,(catkin-like, with large bracts), (plant dioecious), flowers small, (3-)4-6(-8)-merous; hypanthium + or 0, P free to ± connate (carpellate flower of Gjellerupia 0), A adnate to P or not, pollen usu. colporate, microechinate, triangular, (nectaries alternating with A), G [2-5] (half inferior), placentation free central, 1(-few) embryo sacs only, (erect, basal - Agonandra), style short or 0, stigma ± capitate; (pedicel swollen, coloured - Anthoboleae); endosperm copious, also oily, embryo rather short, cotyledons 2-4; germination epigeal; n = 10.

13[list]/60: Exocarpus (26). Pantropical (Map: from Stauffer 1959; Hiepko 1984, 2000). [Photo - Flower]

• Opiliaceae may be recognised by their leaves, which are often 2-ranked, lack much in the way of venation, and may have small bumps because of the cystoliths. The flowers are small and are borne in inflorescences which are often almost catkin-like when young; there is only one perianth whorl. The ovary is superior.

Metcalfe and Chalk (1950) describe a branching system of lignified cells connecting veins in Olacaceae s. str., i.e. not including Anthoboleae. Agonandra and Anthoboleae have amphistomatic leaves; andgreen twigs. Stauffer (1959) suggested that there might be viscin in the fruits of some Anthoboleae.

The Australian Anthobolus, ex Santalaceae, may belong here (Der & Nickrent 2005, 2008, support strong), and it, like other members of the family, has a superior ovary. Other related Santalaceae, i.e. Anthoboleae, are close to Santalum and relatives (Der & Nickrent 2008: support strong); Stauffer (1959), who monographed Anthoboleae, considered that it was closer to Santalaceae than to Opiliaceae.

For embryology, see Ram (1970).

Synonymy: Cansjeraceae J. Agardh, Exocarpaceae J. Agardh

SANTALACEAE R. Brown, nom. cons.   Back to Santalales

Woody or herbaceous root (stem) parasites, (endophytic - Arceuthobium); ellagic acid 0; cuticular epithelium common; (cuticle waxes as rodlets); guard cell thickenings unknown; epidermal cells sclerified, with druses; stem stomata transversely oriented; leaves spiral to opposite (margins with spines - Ionidium); flowers small, (3-)4-5(-8)-merous; hypanthium + [nectary on inside] or 0, P connate or not, frequently a patch of hairs when A are inserted, pollen various, (nectaries alternating with A), G [2-5], ± inferior, odd member abaxial, placentation free central, ovules straight [atropous] (anatropous), or not distinguishable, stigma often capitate or lobed; fruit [mesocarp stony] also baccate; endosperm (helobial; green), starchy or not, embryo short to long; n = 5-7.

44[list]/990: Thesium (325), Phoradendron (235 - see Kuijt 2003), Viscum (65), Dendrophthora (65), Santalum (sandalwood: see Harbaugh & Badlwin 2007, perhaps two Australia -> Hawaii, 2 migrations out of Hawaii). World-wide, esp. tropics (Map: see Meusel et al. 1965; Hawksworth & Wiens 1972; George 1984; Jalas & Suominen 1976; Polhill & Weins 1998). [Photos - Acanthosyris fruit.]

Viscum minimum, from the eastern Cape, has aerial stems about 3 mm long only, and with a single internode (Don Kirkup, pers. comm.); these arise from the endophytic portion of the plant.

Hopelessly paraphyletic, perhaps 5-6 clades if Viscaceae are excluded, but deeper nodes in the clade are currently not well supported. Indeed, Der and Nickrent (2005, 2008) found seven well-supported clades in Santalaceae, between which relationships were unclear; Der and Nickrent (2005) proposed to recognise them all as families...

Some species of Exocarpus lack expanded leaves; their branches are flattened and photosynthetic.

Viscaceae are indeed distinctive. They can be characterised as follows: Stem parasites often with haustoria ramifying through the host, no roots running over the surface of the host°; toxic polpypeptides +; cuticular epithelium developing; stems brittle and jointed°, stomata transverse; cuticle waxes usu. platelets with irregular margins; leaves opposite, 2ndary veins usu. ± palmate, petiole obscure; plant usu. monoecious°, no bract and bracteole immediately under the ovary°; K 0, P 3-4-merous°, short°, A (polythecate), opening by pores°, pollen spherical°, G 3-4, inferior, 2 "ovules"°, usu. mamelon +, embryo sac bisporic° (Allium type); "berry" sometimes explosive, viscous covering incomplete, inside the vascular bundles°, polysaccharide threads and mucilage°, thin endocarp +° (always?); suspensor short or 0, endosperm green°, starchy, zygote cleavage vertical, embryo green, apparently with 1 cotyledon [= 2 connate]; n = 10-14(-17): inc. Arceuthobiaceae, Bifariaceae, Ginalloaceae, and Phoradendraceae. Characters with ° after them differentiate Viscaceae s. str. from Loranthaceae - they are neither close nor morphologically very similar beyond superficialities! Arceuthobium is a major pest on conifers, causing extensive witches' brooms and the death of the host. Expanded wood roses may be produced by the host, but only where the parasite attaches; some are endophytes. Some Viscaceae are wind pollinated. The development of the ovule and embryo is distinctive, e.g., there is no suspensor (Ross & Sumer 2005 and references). However, as Der and Nickrent (2008) note, the mistletoe habit seems to have evolved at least twice in Santalaceae, genera like Dendromyza representing an independent acquisition of the habit.

When a cuticular epithelium develops, there is no cork cambium. Subepideraml cells divide irregularly, the outer walls being cutinised; the cuticular epithelium lacks both suberin (cf. cork) and lenticels (Wilson & Calvin 2003). It is present in the old Eremolepidaceae and Viscaceae, as well as some, but possibly not all Santalaceae s. str. Stomata in the stem and of leaf are commonly tranversely oriented (Butterfass 1987). Thesium has starchy endosperm. Some Santalaceae have recurrent bundles in the gynoecium, perhaps evidence of receptacular epigyny (Eyde 1975, and references). A very large genome with a C value of some 350 picograms or more is found in Viscum alone of the Santalales examined (Leich et al. 2005).

See Wiens and Barlow (1971) for cytology, Hawksworth and Wiens (1972) for the economically very important Arceuthobium, Nickrent et al. (1998) for relationships, Leins (2000) for floral morphology of Viscum, Wilson and Calvin (2003) for some aspects of anatomy, and Norverto (2004: wood anatomy and evolution).

Synonymy: Anthobolaceae Dumortier, Arceuthobiaceae Nakai, Bifariaceae Nakai, Canopodaceae C. Presl, Eremolepidaceae Nakai (cuticular epithelium developing; stem stomata transverse; leaves spiral; inflorescence catkin-like; pollen spherical, no obvious placenta, ovules in base of ovary, embryo sac bisporic; viscous covering complete or not; endosperm green - Eremolepis n = 10, Lepidoceras sister to Eubrachion, Antidapne n = 13 perhaps separate, one of the 5-6 "Santalaceae" s. str. lineages, with growth like Notanthera (Loranthaceae), some with green endosperm - Lepidocerataceae Nakai), Ginalloaceae Nakai, Osyridaceae Rafinesque, Phoradendraceae H. Karsten, Thesiaceae Vest, Viscaceae Batsch

BALANOPHORACEAE L. C. & A. Richard, nom. cons.   Back to Unplaced

Echlorophyllous root parasites from underground tuber-like structures either parasite or parasite-host mixed, these rupture and leave a collar-like structure at ground level; tanniniferous; roots 0; cuticle wax crystalloids 0; stems endogenous; leaves spiral, 2-ranked, whorled or 0; inflorescence ± capitate, spicate, or racemose, terminal, plant monoecious or dioecious; flowers small; staminate flowers: P 0, 3-4(-8), valvate, (basally connate), A = and opposite P, (1-2, esp when P = 0), extrorse, usu. connate, (thecae connate), pollen (trinucleate), tricolpate, tri- or pantoporate, pistillode 0; carpellate flowers: P 0 or minute, staminodes 0, G [2, 3(-5)], (inferior), [2 transverse - Rhophalocnemis], or acarpellate, ovules ategmic, 1 (bisporic Allium type) embryo sac/ovary, antipodal cells 0 or short-lived, styles separate or style single, stigma ± expanded; fruits minute, drupes or nut-like; endosperm +, embryo short to undifferentiated; n = 14, ?16, 18; germination via germ tube.

17[list]/50: Balanophora (15). Mostly tropical (Map: from Hansen 1972, 1980, 1986; van Balgooy 1975). [Photo - Flower]

• Balanophoraceae are echlorophyllous yellow to red or brown root parasites whose aerial stem arises from a collar-like structure borne at ground level. The dense inflorescence is racemose, bearing many minute flowers.

Langsdorffia, Thonningia and Balanophora have balanophorin, a wax-like substance, rather than starch as the main reserve. Weber (1986) noted several distinctive structures in gross morphology and detailed anatomy of the haustoria of Mystropetalon such as runners that produced additional haustoria and graniferous tracheary cells in these haustoria that were similar to comparable structures in Santalales, however, graniferous cells occur in other root parasites including Krameriaceae and Orobanchaceae (Fineran & Ingerfeld 1982). Mystropetalon also has a clearly inferior ovary (see below) and cuboid pollen with pores at the eight corners and other variously angled pollen is known from other Santalales. The mitochondral genes cox1, atp1 and matR showed massive divergence (Barkman et al. 2007: Ombrophytum only sampled).

It often is very difficult to understand the morphology of the flower, whether the ovary is superior or inferior, etc., indeed, development of the gynoecium of Balanophora is perhaps best compared with that of the nucellus, hence the morphology of the "fruit" is unclear. For cautionary comments on attempts to determine ovule type and orientation in the family, see Holzappel (2001) - but problems are hardly surprising, perhaps, if Balanophoraceae are to be compared with the hemiparasitic Santalales. Holzappel noted a pseudoendothelium was quite common in the family. Dactylanthus lacks any seed coat, and one of the cells produced by the first division of the endosperm never divides further - this is then perhaps to be compared with the chalazal haustorium in other Santalales. In Helosis the inner layer of cells of the seed coat is massively thickened on the inner and anticlinal walls, while in Balanophora it is the outer layer that is thickened; taxa like Hachettia are more complex.

Balanophoraceae can be included in Santalales (Nickrent 2002; Nickrent & Duff 1996; especially Nickrent et al. 2005), and Cronquist (1968) suggested simlar relationships. Takhtajan (1997) linked Balanophoraceae with Cynomoriaceae (here Saxifragales), Rafflesiales (here Malpighiales) and Hydnoraceae (here Piperales), including them all in his Magnoliidae; within Balanophorales he included all the families in synonymy here apart from Hachetteaceae as separate families.

Takhtajan (1988, 1997) provides much information under the segregate families mentioned below, including Hachettiaceae and Lathraeophyllaceae (= Helosidaceae); see also Harms (1935b), Kuijt (1969), and the Parasitic Plants website.

Synonymy: Dactylanthaceae (Engler) Takhtajan, Hachetteaceae Doweld, Helosidaceae (Schott & Endlicher) Bromhead, Langsdorffiaceae Pilger, Lophophytaceae (Schott & Endlicher) Bromhead, Mystropetalaceae J. D. Hooker, Sarcophytaceae A. Kerner, Scybaliaceae A. Kerner