EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; rhizoids +, unicellular; flavonoids + [absorbtion of UV radiation]; protoplasm dessication tolerant [plant poikilohydric]; cuticle +; cell walls with (1->4)-ß-D-glucans [xyloglucans], lignin +; several chloroplasts per cell; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic, centrioles develop de novo, associated with basal bodies of flagellae, multilayered structure +, proximal end of basal bodies lacking symmetry, stellate pattern associated with doublet tubules of transition zone; spermatozoids with a left-handed coil; male gametes with 2 lateral flagellae; oogamy; diploid embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, sporangium +, single, with polar transport of auxin, dehiscence longitudinal; meiosis sporic, monoplastidic, microtubule organizing centre associated with plastid, cytokinesis simultaneous, preceding nuclear division, sporocytes 4-lobed, with a quadripolar microtubule system; spores in tetrads, sporopollenin in the spore wall, wall with several trilamellar layers [white-line centred layers, i.e. walls multilamellate]; close association between the trnLUAA and trnFGAA genes on the chloroplast genome.
Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant; characters mentioned are those of the common ancestor of the group.
Abscisic acid, ?D-methionine +; sporangium with seta, seta developing from basal meristem [between epibasal and hypobasal cells], sporangial columella + [developing from endothecial cells]; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; spores trilete; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.
[Anthocerophyta + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous, nutritionally largely independent of the gametophyte; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour.
Sporophyte well developed, branched, free living, sporangia several; spore walls not multilamellate [?here]; apical meristem +.
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Photosynthetic red light response; water content of protoplasm relatively stable [plant homoiohydric]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); vascular tissue +, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem; endodermis +; root xylem exarch [development centripetal]; stem with an apical cell; branching dichotomous; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; tapetum glandular; gametophytes exosporic, green, photosynthetic; stellate pattern split between doublet and triplet regions of transition zone; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, embryonic axis not straight [root lateral with respect to the longitudinal axis; plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Branching ± monopodial; lateral roots +, endogenous, root apex multicellular, root cap +; tracheids with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; male gametes multiflagellate, basal bodies staggered, blepharoplasts paired; chloroplast long single copy ca 30kb inversion [from psbM to ycf2].
Plant woody; lateral root origin from the pericycle; branching lateral, meristems axillary; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant 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 [hence with p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, not medullated [no pith], cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular cylinder around central pith [eustele], phloem abaxial [ectophloic], endodermis 0, xylem endarch [development centrifugal]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium [nodes 1:1]; stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; leaves with petiole and lamina, development basipetal, blade simple; axillary buds +, (not associated with all leaves); prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, lacking sporopollenin, megasporangium indehiscent; pollen grains landing on ovule; male gametophyte development initially endosporic, lacking chlorophyll, tube developing from distal end of grain, gametes two, developing after pollination, with cell walls; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [zeta duplication], 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.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, 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, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; 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 cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes 1:?; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, venation hierarchical-reticulate, secondary veins pinnate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P +, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; 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, endothecium +, endothecial cells elongated at right angles to long axis of anther; (tapetum glandular), cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine +, thin, compact, lamellate only in the apertural regions; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, 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, functional megaspore, chalazal, lacking cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; supra-stylar extra-gynoecial compitum +; ovule not increasing in size between pollination and fertilization; pollen grains landing on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, much larger than ovule at time of fertilization; endosperm diploid, cellular, heteropolar [micropylar and chalazal domains develop differently, 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; dark reversal Pfr → Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; 2C genome size 1-8.2 pg [1 pg = 109 base pairs], whole nuclear genome duplication [epsilon duplication]; protoplasm dessication tolerant [plant poikilohydric]; 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]].
[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.
[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood +; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.
[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [possible position]; pollen tube growth intra-gynoecial; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).
[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.
EUDICOTS: (Myricetin, delphinidin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; K/outer P members with three traces, ("C" +, with a single trace); A few, (polyandry widespread, initial primordia 5, 10, or ring, ± centrifugal), filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?
[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).
[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.
[BUXALES + CORE EUDICOTS]: ?
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one place]; micropyle?; whole nuclear genome duplication [palaeohexaploidy, gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.
[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls, internal/adaxial to the corolla whorl, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G , G  also common, when [G 2], carpels superposed, compitum +, placentation axile, style +, stigma not decurrent; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression.
[DILLENIALES [SAXIFRAGALES [VITALES + ROSIDS s. str.]]]: stipules + [usually apparently inserted on the stem].
[SAXIFRAGALES [VITALES + ROSIDS]] / ROSANAE Takhtajan / SUPERROSIDAE: ??
[VITALES + ROSIDS] / ROSIDAE: anthers articulated [± dorsifixed, transition to filament narrow, connective thin].
ROSIDS: (mucilage cells with thickened inner periclinal walls and distinct cytoplasm); embryo long; genome duplication; chloroplast infA gene defunct, mitochondrial coxII.i3 intron 0.
ROSID II / MALVIDAE / [[GERANIALES + MYRTALES] [CROSSOSOMATALES [PICRAMNIALES [SAPINDALES [HUERTEALES [MALVALES + BRASSICALES]]]]]]: ?
Evolution. Divergence & Distribution. Hengchang Wang et al. (2009: penalized likelihood dates) suggested that rapid radiation within Malvidae occurred (113-)107-83(-76) m.y.a., while Moore et al. (2010: 95% HPD) suggest ages of (104-)102(-97) m.y., Xue et al. (2012) of around 84 m.y., while about 103.2 m.y. is the age in Naumann et al. (2013).
Phylogeny. See the Dilleniales and the Saxifragales pages for further discussion on the relationships of the malvids and of the [Geraniales + Myrtales] clade in particular. Geranium, the only representative of the order studied, was sister to all other rosids except Vitaceae in a study by Zhu et al. (2007, support weak); their position is also unstable in a rbcL analysis of all angiosperms (Hilu et al. 2003). In some earlier trees, Crossosoma (Crossosomatales) was also included or was nearby, see e.g. Morgan and Soltis (1993), Chase et al. (1993), while in Price and Palmer (1993: rbcL analysis) Biebersteinia (see Sapindales here) was still tentatively included in Geraniales. Savolainen et al. (2000a) found the order to be monophyletic, but with only 52% support (see also Savolainen et al. 2000b); Crossosomatales were still its sister group, but with still less support. However, Soltis et al. (2011, see also Moore et al. 2011) find strong support for relationships in the clade as shown in the Summary Tree, those for [Malvales + Brassicales] at 85% ML bootstrap and for [Geraniales + Myrtales] at 79% being the weakest; all other rleationships along the spine have ³99% ML bootstrap (see also Ruhfel et al. 2014). For further discussion of the relationships of the malvids, an ancestor of which may have been involved in an ancient hybridization, see the Zygophyllales page.
Fernando et al. (1995) placed Picramniaceae, ex Simaroubaceae, between Rosid I, which includes Surianaceae and Irvingiaceae (ex Simaroubaceae), and Rosid II, which includes Simaroubaceae themselves, but a position along the spine of the rosid II clade is best.
[GERANIALES + MYRTALES]: ellagic acid +; K persistent in fruit.
Evolution. Divergence & Distribution. The age of this node is variously 89-83 m.y. (Anderson et al. 2005), (103-)100(-97) m.y. (Wikström et al. 2001), (114-)107(-100) and (90-)83(-76) m.y. (Hengchang Wang et al. 2009), ca 108 m.y. (Magallón & Castillo 2009: topology uncertain), (121-)115, 107(-103) or (122-)116, 108(-104) m.y. (Bell et al. 2010: topology uncertain), (99-)91(-77) m.y. (N. Zhang et al. 2012) or about 79 m.y. (Xue et al. 2012). Ca 88.2 m.y. is the age suggested by Sytsma et al. (2014) and around 92.5 m.y. by Naumann et al. (2013).
GERANIALES Berchtold & J. Presl Main Tree.
Vessel elements with simple perforation plates; nodes also 3<:3<; lamina margins gland-toothed; inflorescence cymose; nectary outside A; A obdiplostemonous; G opposite petals, ?style, stigma dry; (outer integument largely dermal in origin); fruit dehiscence?; seed testal. - 5 families, 17 genera, 836 species.
Age. Geraniales can be dated to 86-80 m.y. (Anderson et al. 2005); other estimates are provided by Wikström et al. (2001) - (98-)94, 88(-84) m.y.a., Hengchang Wang et al. (2009) - (109-)103(-97) and (74-)68(-62) m.y., Bell et al. (2010) - (106-)93, 87(-74) m.y., and Palazzesi et al. (2012) - just under 50 m.y., but c.f. Sytsma et al. (2014) who suggested 89-76 m.y. in a reanalysis of the same data.
Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed (see above).
Evolution. Divergence & Distribution. Geraniales are poorly understood, and although a smallish group, they are morphologically quite heterogeneous, which, coupled with lingering uncertainty over their exact phylogenetic position and internal relationships, still makes thinking of apomorphies difficult (Kubitzki 2006a). Palazzesi et al. (2012) discuss the evolution of the whole group in some detail, but Sytsma et al. (2014) should be consulted fot a reanalysis of their data, which yielded a number of different and mostly significantly older dates; adding rosid stem priors was a major cause of the differences.
Chemistry, Morphology, etc. Geraniaceae and Vivianiaceae have a layer of small hypodermal druse-containing cells in the calyx (Kenda 1956). Indeed Weigend (2006: 217) suggests that there might be "a close and possibly exclusive relationship between Geraniaceae and Ledocarpaceae." He lists numerous characters suggesting such a relationship, and these will need to be critically evaluated. Thus he notes that in both the basal ovules in the ovary tend to develop into seeds (although Boesewinkel (1997) mentions that it is the upper ovules of Caesarea [Vivianaceae] that develop into seeds), the nature of the campylotropy of the ovules differs, the fruits of Rhyncotheca (Vivianaceae) differ rather strongly from the superficially similar fruits of Geraniaceae, etc. (although both do have a column). Furthermore, Weigend (2006) suggests that the fruits of Ledocarpaceae are septicidal or septifragal, although Boesewinkel (1997) describes them (apart from Rhyncotheca) as being loculicidal; in fact, the fruits of Balbisia, at least, show variation. Nevertheless, as Weigend's lists and the descriptions here suggest, there are a number of similarities between the two. Bortenschlager (1967) provides a comprehensive pollen survey of Geraniaceae in the old sense, i.e. including things like Dirachmaceae (Rosales), also Vivianaceae which, although no longer in Geraniaceae, at least are still in Geraniales. Details of the distribution of the rpl16 intron in the order are unclear (see Geranioideae: c.f. Downie & Palmer 1992b).
Phylogeny. Savolainen et al. (2000a) found the order to be monophyletic, but with only 52% support (see also Savolainen et al. 2000b). The tree prior to Oct. 2012 - [Geraniaceae [[Melianthaceae + Francoaceae] [Vivianaceae + Ledocarpaceae]]] - was based on these and other studies, although sampling was inconsistent, etc.; Melianthaceae included Greyia. However, the clade [Greyiaceae + Francoaceae] has been strongly supported (Morgan & Soltis 1993; Price & Palmer 1993; Soltis & Soltis 1997), but Soltis et al. (2007a) found the set of relationships [Geraniaceae [Viviana [Bersama [Francoa + Greyia]]]] (see also Bell et al. 2010). Palazzesi et al. (2012: trnL-F, ITS) on the other hand, recovered a tree [Geraniaceae [Melianthaceae [Vivianaceae [Francoaceae + Greyiaceae]]]] (names as used here), with support for all clades strong except that for the [Vivianaceae [Francoaceae + Greyiaceae]] clade, although in the chronogram there is a tree with the topology [Geraniaceae [Vivianaceae [Melianthaceae [Francoaceae + Greyiaceae]]]].
Classification. Although Palazzesi et al. (2012) recognise Hypseocharitaceae, it is small and reasonably included in Geraniaceae, on the other hand, Francoaceae and Greyiaceae have little in common.
Previous Relationships. The circumscription of this clade is somewhat unexpected, largely because Geraniaceae and Oxalidaceae have previously been considered very close (e.g. Cronquist 1981). Geraniaceae in particular included genera now widely dispersed in the rosids, but it has not previously been linked with Greyiaceae or Melianthaceae. Francoaceae have been associated with or even included in Saxifragaceae.
Includes Francoaceae, Geraniaceae, Greyiaceae, Melianthaceae, Vivianiaceae.
Synonymy: Francoales Martius, Greyiales Takhtajan, Ledocarpales Doweld, Melianthales Doweld - Geranianae Reveal - Geraniopsida Meisner
GERANIACEAE Jussieu, nom. cons. Back to Geraniales
Herbs; hydrolysable tannins, (petroselenic acid - Geranium) +; leaves spiral (opposite), pinnate, leaflets not articulated, secondary veins often palmate; inflorescence cymose, often pseudoumbellate; C contorted; nectaries opposite sepals, vascularized; pollen ?often starchy; ovules often campylotropous, micropyle zig-zag; K persistent in fruit; endotesta palisade, with light line, crystalliferous, much thickened, unlignified, exotegmen palisade, lignified, anticlinal walls sinuous.
7[list]/805 - 2 groups below. Temperate and warm temperate. [Photos - Collection]
Age. Palazzesi et al. (2012) opined that Hypseocharis diverged from the rest of the family (42.8-)36.9(-5.7) m.y.a., although a reworked estimate is (72-)62(-52) m.y. (Sytsma et al. 2014), while Fiz-Palacios et al. (2008) suggested an age of 55 m.y. for this split.
Perennial ± acaulescent herbs, tuberous, or thick taproots; anatomy?; stipules 0; A 5, 15 [10 in pairs opp. C], ca 12 ovules/carpel, style filform, stigma capitate, ?surface; fruit a loculicidal capsule (septicidal, almost with mericarps - H. tridentata), filaments also persistent; endosperm scanty, cotyledons spiral; n = ?
1/1-3. S.W. Andean South America (Map: from Slanis & Grau 2001).
Synonymy: Hypseocharitaceae Weddell
2. Geranioideae Arnott
(Shrubs; stem succulents, geophytes); hairs glandular; (vessel elements with scalariform perforation plates); rays often 0; stem often jointed; petiole bundles annular (medullary bundles +); cuticle waxes 0 (rodlets); leaves (opposite), also simple and lobed, lamina vernation conduplicate-plicate, (petiolar spines + - Sarcocaulon), stipules 2, often well developed, interpetiolar or cauline, colleters +; (flowers monosymmetric); K quincuncial [Geranium], aristate; C (4), often salverform, (petals fringed); (nectariferous spurs +), (adaxial nectary only, "adnate" to pedicel - Pelargonium; nectary opposite C - Monsonia); (A 15 [=5 x ]; 2-5; 7; antepetalous whorl staminodial), filaments ± connate basally; (tapetum amoeboid); pollen grains tricellular, (tricolpate), 40-140 µm long; G [(2-)5], true style short, stout, hollow [?always], stigma lobed; ovules 1-2/carpel, apical, campylotropous by development of cells of the inner integument, (micropyle exostomal; ovules apotropous, outer integument 2-3 cells across, inner integument 2-3 cells across, parietal tissue ca 4 cells across, (nucellar cap +); embryo sac invades and obliterates apical nucellar tissue; fruit with upper part of ovary elongating [the "stylar" beak], septicidal, dividing into mericarps which curl upwards and separate from columella, whether or not seeds disperse separately; exotestal cells undistinguished, stellate, stomata +, (endotegmen slightly lignified); endosperm 0, embryo green (Geranium, at least), curved, cotyledons accumbent or longitudinally folded, radicle ± as long as rest of embryo; n = 4, 7-14, etc; inversions in cp DNA, trnT-GGU gene loss, group II intron between nad1 b/c exons, rpl16 and rps16 intron loss, etc.; sporophytic incompatibility system present.
5/865: Geranium (430), Pelargonium (280), Erodium (80), Monsonia (40: inc. Sarcocaulon). Temperate and warm temperate, esp. southern Africa (map: from van Steenis & van Balgooy 1966; Hultén 1971; Wickens 1976; Meusel et al. 1978; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003; Aedo et al. 2005).
Age. The crown group age of Geranioideae is estimated at (71-)54, 48(-33) m.y. (Bell et al. 2010) or some (50-)48, 37(-34) m.y. old (Wikström et al. 2001); Palazzesi et al. (2012) suggest an age of slightly less than 30 m.y., but (57-)48(-39) m.y. is the figure in Sytsma et al. (2014), see also 47-38 m.y. in Fiz et al. (2008).
Synonymy: Erodiaceae Horaninow
Evolution. Divergence & Distribution. Diversification of Pelargonium (and Monsonia), some 155 species of which are succulents (Nyffeler & Eggli 2010b), in South Africa seems to have occurred ca 30-10 m.y. before present as aridification set in, while diversification of the Geranium-Erodium clade occurred at roughly the same time in Eurasia and the Mediterranean, perhaps in response to climate change and mountain uplift there (Fiz et al. 2008); however, Fiz-Palacios et al. (2010) suggest that the ancestral area of Erodium was Asia, where it arose ca 18 m.y.a.. Palazzesi et al. (2012) in general offer younger estimates for splits within Geranioideae, but c.f. Sytsma et al. (2014) for a reanalysis of their data.
Struck (1997) and Bakker et al. (1999, 2000, 2004, 2005) discuss the phylogeny and diversification of Pelargonium in the Cape region; there is striking vegetative and floral variation, and almost 100 species are geophytes (Procheŝ et al. 2006). Leaf shape and scent is notably variable, and Jones et al. (2009) discuss foliar evolution. Divergence of the Cape fynbos clades of Pelargonium may have occurred some (13.6-)10.6(-3.7) m.y.a., diversification in the Succulent Karoo starting a little earlier (Verboom et al. 2009). All told, some 222 of the 280-300 species of the genus are restricted to southern Africa, and the genus is a major element of the endemic flora of the Cape floristic region (Albers & Becker 2010 for a summary).
Pollination Biology & Seed Dispersal. Some southwest African Geraniaceae are pollinated by three species of (extremely) long-tongued dipteran Nemestrinidae flies, overall, perhaps 25% of the species may be so pollinated (Manning & Golblatt 1996, 1997; Goldblatt & Manning 2000). A number of species of Geranium, at least, are revolver flowers. In species like G. robertianumwith a salverform corolla the flower develops in such a way that each "tube" is made up of six adjacent parts from four floral whorls - a remarkable example of synorganisation that does not involve any fusion of parts (Endress 2010d). Pollination in G. thunbergii, at least, is promiscuous, bees, flies and butterflies all being involved and they are inconstant from year to year (Kandori 2002).
The two adaxial petals of Pelargonium alone may bear markings, rather than the abaxial petal(s), as is common in flowering plants. Darwin (1859) noted that the central flower of a Pelargonium inflorescence might lose its adaxial markings and also its nectary. This would be expected of a peloric flower which has become "ventralised", i.e. the morphology of the abaxial sector of the flower extends to the adaxial sector, so the markings on the adaxial petals and the adaxial nectary disappear.
Whether seeds of Geranioideae are catapulted or mericarps are the unit of dispersal, the fruit wall has a stiff outer layer and an inner layer that contracts as it dries, the awn variously coiling and bending as a result (Abraham & Elbaum 2013). The awn of the mericarp is variously coiled, and hygroscopic movements of the awn may result in the seeds being "planted" in the soil, as in some Poaceae (Stamp 1989 and references), while hairs on the awn may aid in wind dispersal (Abraham & Elbaum 2013). Physical dormancy of seeds is common in the family (Gama-Arachchige et al. 2010).
Genes & Genomes. Palmer et al. (1987) noted extensive expansion of the inverted repeat (IR) in Pelargonium, and genomic changes in Geranioideae plastids are remarkably extensive. The chloroplast genome may greatly expand, largely because of the IR expansion, and although the IR is the largest known for any flowering plant (in Pelargonium, it may sometimes be entirely absent in Erodium. There are also very extensive rearrangements, duplications, increases in GC content and substitution rates, and other genome changes, and ndh genes in the chloroplast may be lost (Chumley et al. 2006; Guisinger et al. 2008, 2011: sampling not bad; Jansen 2009 [summary]; Weng et al. 2013). It is noteworthy that this variation occurs within clades (= genera, species), taxa like Erodium carvifolium and California showing little change, although the former has has lost its inverted repeat (Weng et al. 2013). Guisinger et al. (2011) suggest that this variation is the result of relaxed selection after improper DNA repair caused by mutation(s) in nuclear DNA-repair genes.
Parkinson et al. (2005) and Bakker et al. (2006a) found very great increases in the rate of evolution of the mitochondrial gene nad1 throughout this part of the family, and especially in Pelargonium, but not in Hypseocharis (see also Palmer et al. 2000). This has been observed in other mitochondrial genes, as well (Mower et al. 2007; Guisinger et al. 2008), but Weng et al. (2012), while observing that both plastid and mitochondrial genes had accelerated substitution rates, noted that the rate might not be the same throughout the phylogeny or through the whole gene and it might be the result of either increased mutation rate or of selection.
Biparental transmission of plastids has been recorded from Pelargonium, at least, and in hybrids, incompatability between chloroplasts from one parent and the hybrid genome may result in the death of those chloroplasts and thus to variegation (Weihe et al. 2009; see also Wicke et al. 2011; Apitz et al. 2013).
Chemistry, Morphology, etc. Boesewinkel (1988) described the corolla of Hypseocharis as being often imbricate, while Weddell (1861: vol. 2: 289) illustrated it as being contorted (see also Takhtajan 1997). Monsonia may have nectaries axillary to the sepals or on the abaxial bases of the stamens (Aldasoro et al. 2001). When there are fifteen stamens, there are antepetalous stamen pairs, as is common in obdiplostemony (Ronse Decraene et al. 1996; see also Rama Devi 1991), or there may be five groups of three connate stamens (Aldasoro et al. 2001). Campylotropy is by inpushing of the inner integument (Albers & Van der Walt 2006 and references). There has been major movement of ribosomal protein and succinate dehydrogenase genes from the mitochondrion in Erodium (Adams & Palmer 2003).
Some information on ovule morphology is taken from Mauritzon (1934), on embryology is taken from L. L. Narayana (1970), on ovule and testa development from Boesewinkel and Been (1979), on nectaries from Link (1990), on floral morphology from Erbar (1998), on the seed coat from Meisert et al. (2001), on seed coat anatomy and dormancy from Gama-Arachchige et al. (2010), on Monsonia, perhaps paraphyletic, from Aldasoro et al. (2001), on Hypseocharis, from Slanis and Grau (2001), and general information from Albers and Van der Walt (2006). There is information on chemistry in references included in Lis-Balchin (2002); for petroselenic acid, see Tsevegsuren et al. (2004).
Phylogeny. Hypseocharis is sister to the other members of the family (e.g. Price & Palmer 1993; Bakker et al. 1998). The genus is in need of further study; if H. tridentata, with septicidal (and ventricidal) capsule dehiscence, is sister to the rest of the genus, simple optimisation of fruit characters on the tree becomes interesting. Other relationships are [Pelargonium [Monsonia [Geranium + Erodium]]] (see also Palazzesi et al. 2012); the position of the monotypic California is unclear (Fiz et al. 2008).
For a phylogeny of Erodium, see Fiz et al. (2006); there has been substantial dispersal. Within Pelargonium A 2-7, either x = 11, chromosomes 1.5³ µm long or x = 9, chromosomes 1.5-3.0 µm long; for a well-sampled phylogeny, see Röschenbleck et al. (2014).
Classification. Recognising Hypseocharis as a family was an option in A.P.G. II (2003), but a broad circumscription of Geraniaceae is adopted here (see also APG 2009: Hypseocharis has even been placed in a monotypic order, Hypseocharitales [Takhtajan 1997], although mercifully placed near Geraniales in the sequence). Röschenbleck et al. (2014) provide an infrageneric classification of Pelargonium.
Previous Relationships. Hypseocharis used to be included in Oxalidaceae (Hutchinson 1973; Cronquist 1981), but nectaries, testa anatomy, etc., place it unambiguously here (e.g. Boesewinkel 1988; Rama Devi 1991). Also, its leaflets are not strongly articulated with the petiole, as they are in Oxalidaceae. On the other hand, Geraniaceae used to include taxa like Biebersteiniaceae (Sapindales) and Dirachmaceae (Rosales).
Botanical Trivia. The geranium of the window sill is really a Pelargonium.
[Melianthaceae [Vivianaceae [Greyiaceae + Francoaceae]]]: at least traces of inulin +; leaves spiral, insertion rather broad; inflorescence terminal, racemose.
Age. Wikström et al. (2001) estimated the age of this node at (74-)67, 59(-52) m.y.a., and while comparable estimates in Palazzesi et al. (2012) are only (42.8-)31.4(-20.2) m.y., those in Bell et al. (2010) are (94-)77, 70(-51) m.y..
Information on seed anatomy is taken from Danilova (1996)
Classification. Melianthaceae and Francoaceae were placed in a single family by Savolainen et al. (2000b); many of the characters given there that linked the two may be plesiomorphic.
MELIANTHACEAE Horaninow, nom. cons. Back to Geraniales
Shrubs to trees; odoriferous [nasty, mustard], ellagic acid, glucuronide triterpenoid saponins, bufadienolides [cardiac glycosides] +; cork cambium subepidermal to outside phloem; nodes multilacunar; petiole with ring of bundles (cortical or medullary bundles +); styloids +; cuticle waxes usu. 0; leaves odd-pinnate, leaflets articulated, vernation conduplicate, secondary venation pinnate, margins strongly serrate to entire, stipule single, intrapetiolar, (base not very broad - Bersama); inflorescence terminal or axillary, (with conspicuous sterile flowers at apex); flowers ± monosymmetric, resupinate; K 5, or 2 connate + 3, adaxial weakly spurred or not, C 4-5, clawed, unequal, recurved or not; nectary large, adaxial or annular; A 4-5, (connate basally), dorsifixed, anther endothecium not fibrous [Melianthus], tapetal cells 3-nucleate; G [(3-)4-5(-7)], glandular hairs inside the loculus, style impressed, long, stigma punctate or capitate; ovules 1-5/carpel, apical or basal, apotropous to pleurotropous, micropyle endostomal, outer integument 16-20 cells across, inner integument 3-4 cells across; fruit a loculicidal capsule; (seed arillate - Bersama); exotesta palisade, crystalliferous, outer wall thick, tegmen crushed; endosperm thick- or thin walled, starchy, thick-walled, or with amyloid [xyloglucans - Melianthus], embryo small to medium; n = 18 (19).
2[list]/8. Africa (map: modified from Culham et al. 2007, see Trop. Afr. Fl. Pl. Ecol. Distr. 6. 2011). [Photo - Inflorescence, Inflorescence.]
Age. Crown-group Melianthaceae are (33.8-)26.9(-20.0) m.y. (Linder et al. 2006), (14.9-)10(-5.7) m.y. (Palazzesi et al. 2012) or (20-)14.4(-10) m.y. (Sytsma et al. 2014).
Evolution. Divergence & Distribution. Diversification within Melianthus happened some (26.2-)19.7(-12.2) m.y.a (Linder et al. 2006, q.v. for more dates, etc.), but c.f. the later dates suggested by Palazzesi et al. (2012) and Systma et al. (2014), who link diversification to the beginning of aridifiaction in South Africa.
Chemistry, Morphology, etc. Hutchinson (1973) described a disc lining the inside of the K. The number of nuclei in the pollen grain is unclear (Dahlgren & van Wyk 1988). For the ovules of Bersama, which face away from each other, see Danilova (1996). For information given by Khushalani (1963), the ovules of Melianthus major may be multiplicative - the parietal tissue was only ca 10 cells across initially. She also described a nucellar cap 8-11 cells across, but it was apparently formed from hypodermal cells.
For a general account, see Linder (2006), for node and petiole anatomy, see Hilger (1978a, b), for anatomy, see Gornall and Al-Shammary (1998), for embryogenesis, see Steyn et al. (1986). for floral development, see Ronse Decraene et al. (2001b), for seeds of Melianthus, see Guérin (1901) and Corner (1976), for anthers, see Endress & Stumpf (1991), and for flower and fruit, see Doweld (2001a: c.f. micropyle type).
Phylogeny. Melianthus major is probably sister to the rest of the genus (Linder et al. 2006).
Classification. A.P.G. (2003) suggested as an option separating Melianthaceae and Francoaceae, an option which was followed in early versions of this site; later the two were combined in both (see A.P.G. 2009).
Previous Relationships. Melianthaceae were included in Sapindales by Cronquist (1981), who dismissed any idea of a relationship between them and Greyiaceae.
Synonymy: Bersamaceae Doweld
[Vivianaceae [Greyiaceae + Francoaceae]]: ?
VIVIANIACEAE Klotzsch Back to Geraniales
(Thorns +); ?inulin; ?nodes; wood rayless; leaves opposite, simple, (lamina margins entire), stipules 0, but a line across the stem; K aristate, C contorted; pollen grains spherical, 23-40 µm long, polypantoporate, with microspines; style short, style branches/stigmas separate, long, stigma dry, margins ± revolute; ovule with micropyle endostomal, apices of integuments 3-4 cells across, parietal tissue ca 6 cells acroos, (nucellar cap 2 cells across), funicle with hairs; fruit a loculicidal capsule; exotesta and endotegmen more or less tanniniferous; endosperm ± copious, walls thick, pitted, embryo curved.
4[list]/18. W. South America, S. Brasil.
Age. The crown-group age of Vivianaceae is about 27.5 m.y. (Palazzesi et al. 2012) or (44-)35(-28) m.y. (Sytsma et al. 2014).
Woody herb (annual); glandular hairs +; chemistry?; cork?, cambium storied; nodes 1:1; cuticle waxes ± band-like or 0; lamina white-hairy below, secondary veins subpalmate; (flowers 4-merous); K valvate, basally connate, strongly 8- or 10-ribbed; (C 2-lobed); nectary glands alternating with C; (A 4, 5, 15); G [(2) 3], odd member abaxial; ovules 2/carpel, superposed; seed (hairy), raphe tanniniferous; (exotegmen thick-walled, elongated, not lignified - Caeserea); endosperm copious, initially with some starch, embryo green, root long; n = 7.
1 or 4 (Lefor 1975)/6. Chile, S. Brasil (map: from Lefor 1975).
Shrubs; anatomy?; cuticle waxes as platelets; (leaves deeply lobed); epicalyx + or 0; (K acute; C 0); (pollen inaperturate - Balbisia, Wendtia); nectary 0; G [3, 5], opposite sepals, stigmas drying dark; ovules 2 collateral or superposed-many/carpel, nucellar cap +; (fruit septicidal or more or less septifragal); (exotesta of slime cells - Balbisia); endosperm scanty (thin-walled), cotyledons spiral (straight); embryo colour?; n = 9.
3/12. W. South America, especially the Andes (map: modified from Culham 2007).
Synonymy: Ledocarpaceae Meyen, Rhyncothecaceae Jussieu
Evolution. Divergence & Distribution. For diversification within Vivianaceae, see Palazzesi et al. (2012) and Sytsma et al. (2014) - it began in southern South America prior to the Andean orogeny.
Chemistry, Morphology, etc. Boesewinkel (1997) described ovules and seeds, while Weigend (2005) detailed some aspects of floral morphology and pollination, and later (Weigend 2006) provided an account of the whole family, also with data on wood and leaf anatomy, inflorescence morphology, etc. There is some conflict in the various accounts (see also introduction to Geraniales). Endosperm type/development is unknown
The vessel elements of Viviania sometimes have a single bar across the perforation.
The inflorescence of Viviania can be replaced all or in part by a branched thorn. The stamens of Viviana are much longer than the stigma/styles. The fruits of Balbisia may be more or less septifragal (with a loculicidal slit, too) or clearly loculicidal.
See Carlquist (1985b) for wood anatomy, Narayana and Rama Devi (1995) for general information, Mauritzon (1933), for embryology, Palazzesi et al. (2012) for pollen, M. S. Dunthorn (pers. comm.) for nodal anatomy of Viviania; for carpel orientation, see Baillon (1874) and Knuth (1931).
Phylogeny Wendtia is sister to Balbisia (Price & Palmer 1993). Palazzesi et al. (2012) found the relationships [Viviania [Rhynchotheca + Balbisia]] (Fig. 4), but support for the sister-group relationship of the latter pair of genera was not strong, and in the chronogram (Fig. 5) relationships are [Balbisia [Viviania + Rhynchotheca]] (for the latter topology, see also Systma et al. 2014).
Classification. Viviana, and Balbisia and relatives, were placed in a single family by Savolainen et al. (2000b), but the support for a sister-group relationships was not strong; A.P.G. (1998, 2003, 2009) kept them separate. However, in view of the strong support for the combined group in Palazzesi et al. (2012), and the characters its members have in common, it is recognized here as a single family.
[Greyiaceae + Francoaceae]: inflorescence with sterile bracts at apex; bracteoles 0; A weakly secondarily obdiplostemonous, anthers basifixed, endothecium surrounds thecae; ovary sulcate; ovules many/carpel, pleurotropous; fruit a septicidal capsule; endotesta fibrous, anticlinal walls thickened and lignified.
Age. This node is dated at (45-)38(-31) m.y. (Wikström et al. 2001), (17.7-)11.2(-5.9) m.y.a. (Palazzesi et al. 2012, but c.f. Sytsma et al. 2014 - [35-]27[-15] m.y.), or (32-)19(-8) m.y. (Bell et al. 2010).
GREYIACEAE Hutchinson, nom. cons. Back to Geraniales
Shrubs to small trees; ellagic acid, B-ring deoxyflavonoids +; cork cambium subepidermal to outside pericycle; (largely phloic medullary bundles +); cambium storied; pericyclic fibres +; nodes multilacunar; petiole bundles arcuate, with adaxial smaller inverted series and abaxial series; raphides +; cuticle waxes usu. 0; leaves simple, sheath adnate to the stem, detaching from stem along with petiole and lamina, lamina vernation conduplicate, secondary veins palmate, margin bluntly serrate, teeth hydathodal, stipules 0, or +; K 5, imbricate, C 5, imbricate; nectaries 10, stalked, peltate-/anvil- shaped; A long-exserted; G [(4-6)], opposite C or K, style continuous with ovary, long, stigma slightly expanded and ridged, wet; ovules (micropyle exo- or endostomal), outer integument 3-7 cells across, inner integument 2-4 cells across; fruit valves also opening internally; exotesta crystalliferous, outer wall thick, hypostase massive; endosperm starchy, thick-walled; n = 16-17.
1[list]/3. South Africa, Swaziland. [Photo - Inflorescence.]
Age. Divergence between the extant species of Greyia is put at a mere (0.8-)0.4(-0.07) m.y.a. (Palaszzesi et al. 2012).
Chemistry, Morphology, etc. The abscission of leaf sheath plus attached rest-of-leaf is helped by the activity of the cork cambium.
For general information, see Linder (2006: as Melianthaceae), for node and petiole anatomy, see Hilger (1978a); further information is taken from Bohm and Chan (1992: B-ring deoxyflavonoids), Hideux and Ferguson (1976: pollen), Ramamonjiarisoa (1980) and Gregory (1998), both anatomy, Steyn et al. (1986: embryogenesis), Dahlgren and van Wyk (1988: stipules), Endress and Stumpf (1991: stamens), Nemirovich-Danchenko (1995: seed coat anatomy), and Steyn and van Wyk (1987) and Ronse Decraene and Smets (1999), both floral development.
Previous Relationships. Greyiaceae were included in Sapindales by Cronquist (1981).
FRANCOACEAE A. Jussieu, nom. cons. Back to Geraniales
Perennial herbs; flavonols, tannins of any sort 0, anthocyanin in roots, inulin?; cork ?; young stem with pseudosiphonostele; nodes 3:5; petiole bundle arcuate, with lateral annular bundles; hairs uniseriate, secretory; leaves pinnate or simple, lamina vernation conduplicate-plicate, (secondary veins pinnate); inflorescence scapose, (branched); flowers poly- or monosymmetric; K 4-5, induplicate-valvate, C (3) 4-5, clawed or not; stamens (= and opposite sepals), tapetum multinucleate [Francoa]; pollen with complex endapertures; nectary intrastaminal, lobed; G [4(-5)], placentation parietal [Francoa], style short, ± impressed, stigmas sessile, commissural; ovules with bistomal micropyle, outer integument ca 2 cells across, inner integument ca 3 cells across, parietal tissue 3-6 cells across, ncellar caps ca 2 cells across, postament +, funicular obturator +; embryo sac elongated; exotestal cells palisade, thickened, endotestal cells elongated, (with all walls thickened), tegmen of pigmented cells; endosperm nuclear, embryo short, radicle with anthocyanin [Francoa]; n = 20, 26.
2[list]/2. Chile. [Photo - Francoa Habit © Gardenweek.org]
Evolution. Divergence & Distribution. Divergence between Francoa and Tetilla is dated at ca 4 m.y.a. (Palazzesi et al. 2012).
Chemistry, Morphology, etc. The stem has an endodermoid layer.
Francoa: A 8, Tetilla: A = K (both described as diplostemonous and septicidal in e.g. Klopfer 1972a, 1973; Linder 2006). There is a large chalazal endosperm sac that remains free-nuclear longer than the rest of the endosperm (Gaümann 1919). Krach (1976) compared the testa anatomy with that of Cunoniaceae.
Other references: for general information, see Linder (2006: as Melianthaceae), for seed anatomy, see Nemirovich-Danchenko (1994a), for vegetative anatomy, see Gregory (1998), for floral development of Francoa, see Ronse Decraene and Smets (1999), and for embryology, see Gaümann (1919) and Mauritzon (1933).