LIGNOPHYTA

True roots +; lateral meristems: cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially.

EXTANT SEED PLANTS/SPERMATOPHYTA

Plant woody, evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols, thus containing p-hydroxyphenyl and guaiacyl lignin units, (lignins derived from p-coumaryl alcohol, i.e. S [syringyl] lignin units); true roots present, apex multicellular, xylem exarch, and branching endogenous; arbuscular mycorrhizae +; shoot apical meristem multicellular, interface specific plasmodesmatal network; stem with ectophloic eustele, endodermis 0, xylem endarch, branching exogenous; vascular tissue in t.s. discontinuous by interfascicular regions; vascular cambium + [xylem ("wood") differentiating internally, phloem externally]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, plastids with starch grains; phloem fibres +; stem cork cambium superficial, root cork cambium deep seated; leaves with single trace from sympodium ["nodes 1:1"]; stomata ?; leaf vascular bundles collateral; leaves megaphyllous [determinancy evolved first, then ad/abaxial symmetry], spiral, simple, lamina with vein density up to 5 mm/mm² [mean for all non-angiosperms 1.8]; axillary buds associated with at most some leaves; prophylls [including bracteoles] two, lateral; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores, i.e. no distal pore for release of gametes] +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, crassinucellate, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg, gametes two, developing after pollination, with cell walls, with many flagellae; 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 duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common, positive Maüle reaction [syringyl:guaiacyl ratio more 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; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, with gelatinous fibres; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cells from same mother cell that gave rise to the sieve tube; sugar transport in phloem passive; nodes unilacunar [1:?]; stomata with ends of guard cells level with pore, paracytic, outer stomatal ledges producing vestibule; leaves petiolate, lamina [formed from the primordial leaf apex], development of venation acropetal, 2ndary veins pinnate, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm², endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, polysymmetric, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P not sharply differentiated, with a single trace, outer members not enclosing the rest of the bud, often smaller than inner members; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, 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, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellar, endexine thin, compact, lamellate only in the apertural regions; nectary 0; G free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, megaspore tetrad linear, functional megaspore chalazal, lacking sporopollenin and cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; P deciduous in fruit; seed exotestal; pollen binucleate at dispersal, trinucleate eventually, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing at 80-600 µm/hour, with pectic outer wall, callose inner wall and callose plugs, growing between cells, penetration of ovules via micropyle [porogamous] within ca 18 hours, distance to first ovule 1.1.-2.1 mm, tube moves between nucellar cells; double fertilisation +, endosperm diploid, cellular [micropylar and chalazal domains develop diffently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo cellular ab initio, minute; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)_n]; whole genome duplication, ndhB gene 21 codons enlarged at the 5' end, 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 three copies of the PHY gene, [PHYB [PHYA + PHYC]].

Evolution. Possible apomorphies for flowering plants are in bold. Note that the actual level to which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is because some taxa basal to the [magnoliid + monocot + eudicot] group have been surprisingly little studied, there is considerable homoplasy as well as variation within and between families of the ANITA grade in particular for several of these characters, and also because details of relationships among gymnosperms will affect the level at which some of these characters are pegged. For example, if reticulate-perforate pollen is optimized to the next node on the tree (see Friis et al. 2009 for a discussion), it effectively makes the pollen morphology of the common ancestor of all angiosperms ambiguous... For other features such as details of sugar transport in the phloem, their placement on the tree is frankly speculative. Finally, for features such as parietal tissue/a nucellus only one (Nymphaeales) to three cells thick above the embryo sac and a stylar canal lacking an epidermal layer, although plesiomorphous for basal grade angiosperms (Williams 2009), I am unsure where on the tree a thicker nucellus and a stylar epidermal layer are acquired.

[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: vessels +, elements with elongated scalariform perforation plates; wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.

[ERICALES [ASTERID I + II]]: ovules tenuinucellate.

[ASTERID I + II] / CORE ASTERIDS: ellagic acid 0, non-hydrolysable tannins not common; sugar transport in phloem active; inflorescence basically cymose; C forming a distinct tube; A epipetalous, = and opposite sepals or P, polyandry associated with increased numbers of C or G, very uncommon; (pollen with orbicules); duplication of the PI gene.

ASTERID II / CAMPANULIDAE: myricetin 0; vessel elements with scalariform perforation plates; flowers rather small; style short; endosperm copious, embryo short/very short.

[ASTERALES [ESCALLONIALES [BRUNIALES [APIALES [PARACRYPHIALES + DIPSACALES]]]]] / APIIDAE: iridoids +; inflorescence?; C tube initiation early; G [2-3], inferior.

[ESCALLONIALES [BRUNIALES [APIALES [PARACRYPHIALES + DIPSACALES]]]]: ?

[BRUNIALES [APIALES [PARACRYPHIALES + DIPSACALES]][: ?

Evolution. Divergence & Distribution. Magallón and Castillo (2009) offer estimates of ca 93.6 and 93.9 million years for relaxed and constrained penalized likelihood datings respectively for the crown group, i.e. divergence of Bruniales, the stem group of this clade dating to 94.3 to 94.6 million years (relaxed and constrained again) - but note topology.

BRUNIALES Dumortier  Main Tree, Synapomorphies.

Plant woody, evergreen; iridoids?; nodes 1:1; flowers polysymmetric; anthers basifixed; G position?; ovules weakly crassinucellate. - 2 families, 14 genera, 79 species.

Evolution. Divergence & Distribution. Magallón and Castillo (2009) offer estimates of ca 93.6 and 93.9 million years for relaxed and constrained penalized likelihood datings respectively for stem group Bruniales - but note topology.

Yet another old, species poor but morphologically quite diverse clade that is placed along the spine of the asterid II clade....

Phylogeny. Backlund (1996) included Bruniaceae and Columelliaceae in Dipsacales, but other relationships have been suggested (Gustafsson et al. 1996; Backlund & Bremer 1997; Pyck & Smets 2000; Bell et al. 2001). For the possible association of Bruniaceae with Asterales, see Lundberg (2001e). A position of Columelliaceae s.l. (inc. Desfontainiaceae), in or near Dipsacales was suggested by Bremer et al. (2001) and especially by Lundberg (2001e), although the support was at best moderate. Indeed, Bruniaceae are sister (1.0 Bayesian p.p.) to Columelliaceae in many analyses in Winkworth et al. (2008a), although not when coding chloroplast sequences were used alone, while Soltis et al. (2011) found strong support for this clade only when mitochondrial genes were removed from the analysis; all things considered, the circumscription adopted here seems reasonable. Both palynology and wood anatomy had suggested a relationship between Columellia and Desfontainia (ex Loganiaceae) (Mennenga, in Leeuwenberg 1980), and this was strongly supported by rbcL and other data (see B. Bremer et al. 1994; Backlund & Bremer 1997; Bell et al. 2001).

Previous Relationships. In the first seven versions of this site (pre April 2008) it was thought appropriate to place Columelliaceae s.l. (= [Columelliaceae + Desfontainiaceae]) immediately before the ordinal characterisation of Dipsacales as it made morphological "sense". For instance, they all have opposite leaves, and Columellia has amoeboid tapetum (cf. Bremer et al. 2001) like Dipsacales although Desfontainia does not (Maldonado de Magnano 1986a). If the pair are not immediately related to Dipsacales, as now seems probable, the substantial similarity that they have with Dipsacales may indicate either substantial homoplasy or a suite of lower-level synapomorphies in the asterid II group of which there is currently no indication; the latter is less likely.

Indeed, various families have been placed here or elsewhere in the asterid II clade, but with uncertain support; recent work is clarifying their relationships (Winkworth et al. 2008a; Tank & Donoghue 2010). For Polyosmaceae and Escalloniaceae, here as Escalloniaceae, see Escalloniales; Paracryphiaceae, Quintiniaceae, and Sphenostemonaceae are combined as Paracryphiaceae and form a clade sister to Dipsacales; while Columelliaceae and Bruniaceae, together making up Bruniales, are dealt with below.

Includes Bruniaceae, Columelliaceae.

Synonymy: Columelliales Doweld, Desfontainiales Takhtajan

BRUNIACEAE Candolle, nom. cons.   Back to Bruniales

Ericoid shrubs, with lignotubers; myricetin +, iridoids?; stomata cyclocytic, orientation transverse; leaves spiral, small, close-set, lamina linear, margins entire, stipules often minute, colleter-like (0); blade margins entire, apex glandular; inflorescence racemose or spicate; flowers often small, (4-merous); (K connate), C often clawed (connate); A (adnate to C), anthers ± elongate; nectary +/0; G [2], ± inferior, ?oblique, placentation apical-axile, stigma capitate; ovules 2/carpel, micropyle long, endothelium 0, hypostase +; fruit achenial or nut-like, single-seeded, K persistent; seed (arillate), coat ?; endosperm type?, haustoria?.

6/81[list]/75. South Africa, almost entirely the Cape Province, also KwaZulu-Natal (map: from Claßen-Bockhoff 2000). [Photo - Flowers.]

1. Linconieae Quint & Claßssen-Bockhoff

Stomata with cuticular rim; petals hard in texture; anthers sagittate, with sterile tip; (G [3]), styles separate; (fruits with two seeds); n = ?

1/3. The Cape.

Audouineae + Brunieae: ?

2. Audouineae Niedenzu

(Stomata with cuticular rim); (flowers single; inflorescence involucrate); anther thecae parallel, connate their entire length; (pollen 4-5-colpate); (G [1, 3]), styles separate to connate; (ovules to 8/carpel); n = 11.

2/14. Southwestern part of the Western Cape.

3. Brunieae Quint & Claßssen-Bockhoff

(Lignotubers 0); inflorescence capitate, (involucrate), (with terminal flower and development centrifugal), (flowers single), etc.; anthers versatile, thecae (to rotund); (pollen to 10-colporate); (G [1]), (superior), styles separate or connate; ovules 1(-10)/carpel; (fruit with fleshy accrescent K; dehiscent, also splitting adaxially); (seeds arillate); n = 22, 23.

3/64. Brunia (37). Esp. the Western Cape (Eastern Cape; KwaZulu-Natal).

• Bruniaceae are ericoid shrubs with closely-set needle-like leaves with entire margins from the Cape region of South Africa which often have a black projection at the apex; the leaves are spirally arranged. The often small flowers are frequently aggregated into more or less capitate inflorescences, the adaxial surfaces of the petals showing a diversity of swellings or ridges. The ovary is more or less inferior.

Evolution. Divergence & Distribution. There is a striking similarity between the flowers of Actinocalyx, from the Upper Cretaceous (Santomasian/Campanian) of Sweden, and those of Bruniaceae (Hall 1987). Stem group Bruniaceae may be up to 107 million years old, although probably somewhat less, yet much crown-group diversification has occurred within the last 20 million years (Quint & Claßen-Bockhoff 2008).

Floral Biology & Seed Dispersal. Myrmechory occurs in this clade (Lengyel et al. 2010).

Chemistry, Morphology, etc. Bruniaceae are poorly known. The leaf apex has suberised cells produced by a localised cork cambium. The corolla "tube" is at least sometimes formed by adnation of the filaments to adjacent free petals, but the petals are developmentally initally free (Quint & Claßen-Bockhoff 2006b). The androecium is often weakly monosymmetric, the abaxial pair of stamens being larger than the others. Gynoecial variation is considerable; in genera like Berzelia where there is only a single carpel (really pseudomonomery?), there is only a single locule, ovule and style. The ovules may be pleurotropous (van Tieghem 1898), and there are only one or two cells between the megaspore mother cells and the nucellar epidermis.

Some information is taken from from Saxton (1910 - no endothelium is shown), Jay (1968a: chemistry), Hall (1988: pollen), Dahlgren and van Wyk (1988), Gregory (1998: anatomy), Endress and Stumpf (1991), Claßen-Bockhoff (2000: detailed discussion of inflorescences), and Quint and Claßen-Bockhoff (2006b: floral ontogeny); for wood anatomy, see Carlquist (1978b).

Phylogeny. There is strongly supported phylogenetic stucture within the family: [Linconieae (Linconia only, anther thecae apically connate and sterilised) [Audoinieae (anther thecae adnate to connective their entire length) + Brunieae]] (Quint & Claßssen-Bockhoff 2006a).

Classification. Claßssen-Bockhoff et al. (2011) propose a tribal classification based on the phylogeny by Quint and Claßssen-Bockhoff (2006a). For a somewhat dated monograph, see Pillans (1947).

Previous Relationships. Bruniaceae have often been linked with the South African Grubbiaceae, here in Cornales (see Hall 1987 for some references), but the similarities between the two probably reflect the fact that they grow in similar habitats.

Synonymy: Berzeliaceae Nakai

COLUMELLIACEAE D. Don, nom. cons.   Back to Bruniales

Cork cambium deep-seated; pericyclic fibres 0; petiole bundles arcuate; bud without scales; leaves opposite, petiole bases meeting, lamina margins toothed; inflorescence terminal, cymose; flowers medium-sized; anther connective well-developed, style long; ovules many/carpel, endothelium poorly developed; K persistent in fruit; seeds many, anticlinal exotestal cells much thickened, with plasmodesmata.

2[list]/5. Costa Rica to Chile, montane in the tropical part of this area.

Columellia D. Don

Shrubs or trees; plant bitter tasting, iridoids 0; central petiole bundle much the largest; cuticle waxes as tubules; lamina (with glands on lower surface), teeth glandular (0); flowers (4-8-merous); K ± valvate; A 2, latrorse, thecae semicircular, attached their length to expanded connective; tapetum amoeboid; G [2], largely inferior, placentation intrusive parietal or lobed-axile, stigma with two broad lobes, almost cup-like; ovules ?tenuinucellate?; fruit septicidal and part loculicidal down the sides; exotestal cells elongated; endosperm type?; n = ?

1/4. S. Colombia to Bolivia, in the Andes (map: from Brizicky 1961). [Photo - Flower]

Desfontainia Ruíz & Pavón

Shrubs; route I secoiridoids +, tannin 0; scattered sclereids in the pericyclic position; lamina vernation conduplicate, teeth spiny, colleters +; flowers usu. single; K connate at base, C contorted, A adnate in throat, thecae ± embedded in connective, filaments stout; G [5(-7)], opposite petals, placentation axile but apically parietal, stigma only slightly expanded; ovule with integument 6-9 cells across; fruit a berry; exotestal cells polygonal, outer walls pectic, other walls, especially anticlinal, lignified; endosperm haustoria small; n = 7.

1/1: Desfontainia spinosa. Costa Rica to Chile. [Photo - Flower]

Symonymy: Desfontainiaceae Pfeiffer

Evolution. Divergence & Distribution. Another old, species-poor but morphologically quite diverse clade that occurs in South America and is in the asterid II clade....

Chemistry, Morphology, etc. The intervascular pits of Desfontainia are scalariform or circular and bordered, not vestured. All the cells in even the young stem are slightly lignified. Myricetin? The two stamens of Columellia are the adaxial pair and have latrorse, semicircular thecae attached their length to an expanded connective; the anthers are described as being extrorse by Backlund and Donoghue (1996). Although both Desfontainia and Viburnum have similar, smooth pollen orbicules, these are also quite widely distributed in Gentianales, at least (Vinckier & Smets 2002). Maldonado de Magnano (1986a) suggests that the ovules of Desfontainea are weakly crassinucellate, with a single layer of nucellar cells between the megaspore and the nucellar epithelium; an endothelium is at most poorly developed, and there is a large haustorial suspensor.

For Columellia information was taken from Hasselberg (1937), Stern et al. (1969: anatomy), Backlund and Donoghue (1996: general), and Gregory (1998: anatomy), for waxes, see Theisen and Barthlott (1994) and Fehrenbach and Barthlott (1988: cuticle platelets as ribbons and rodlets). Further data from: Zak & Jaramillo 3266. For Desfontainia information was taken from Backlund and Donoghue (1996) and Hasselberg (1937). Further data from: Qin 710 and Zarucchi et al. 5195.

Previous Relationships. The relationships of Columelliaceae have long been uncertain; the family was placed in Rosales by Cronquist (1981) and in Hydrangeales by Takhtajan (1997). Desfontainiaceae have usually been considered to be entirely unrelated and included in the heterogeneous Loganiaceae.