EMBRYOPSIDA Pirani & Prado (crown group)
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; flavonoids + [absorbtion of UV radiation]; protoplasm dessication tolerant [plant poikilohydric]; cuticle +; cell walls with (1->4)-ß-D-glucans [xyloglucans], lignin +; rhizoids unicellular; 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]; spores trilete; close association between the trnLUAA and trnFGAA genes on the chloroplast genome.
Note that many of the bolded characters in the characterization above are apomorphies in the streptophyte clade along the lineage leading to the embryophytes rather than being apomorphies of the crown embryophytes.
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; 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.
[Hornworts + 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, sporangia derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; tapetum glandular; 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 with xylem and phloem originating on alternate radii, vascular tissue not medullated, 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 first endo- then exosporic, 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.
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 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, becoming 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; embryogenesis cellular; 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.
Age. The age of this branching point is estimated at (190-)167(-47) m.y. (95% HPD, Smith et al. 2010, Table S3), while a fossil-based estimate is ca 100 m.y. (Crepet et al. 2004). [Check]
Phylogeny. Relationships between the lineages immediately above the basal pectinations in the main tree, the ANITA grade - Amborellales, Nymphaeales and Austrobaileyales here - have been for some time unclear. The topology [[Chloranthaceae + magnoliids] [monocots [Ceratophyllaceae + eudicots]]] is preferred here. Thus Hilu et al. (2003: a matK analysis alone), suggested that Ceratophyllaceae were sister to eudicots (see also D. Soltis et al. 2000; Borsch et al. 2005: three rapidly evolving genes, 62% jacknife, 96% posterior probabilities; Müller et al. 2006: 96% posterior probability; some analyses in Saarela et al. 2007; Soltis et al. 2007a: support weak; Qiu & Estabrook 2008; most analyses in Drew et al. 2014)). Jansen et al. (2006b) and Hansen et al. (2007) found support for a sister-group relationship between Chloranthales and the magnoliids. Ruhfel et al. (2014: whole chloroplast genomes) did not find strongly supported relationships around here, and although Chloranthaceae tended to be sister to Magnoliales and Ceratophyllaceae to the eudicots, while in Drew et al. (2014) most analyses retrieved the clades [Chloranthaceae + magnoliids] and [Ceratophyllaceae + eudicots], although they also found one or two other topologies.
The positions of Ceratophyllaceae and Chloranthaceae have been particularly uncertain, and Piperales have also tended to wander around the tree. Indeed, Graham et al. (2005) found that the inclusion of Ceratophyllum and Chloranthaceae in analyses could destabilise relationships among other early branching clades, e.g., the position of the monocots became labile. Soltis et al. (2005b) had very reasonably summarized their discussion on relationhips in this area by showing a pentatomy of Ceratophyllaceae, Chloranthaceae, eudicots, magnoliids, and monocots (see also P. Soltis et al. 1999). Interestingly, Piper has the "monocot" pattern of PHY genes (A, B, C genes only), while Ceratophyllum has PHYE (Mathews et al. 1995).
Many topologies other than those mentioned in the preceding paragraph have been obtained. There has been weak support for an (eu)magnoliid clade being sister to the eudicots (e.g. D. Soltis et al. 2000; P. Soltis et al. 2000; Wu et al. 2007; Qiu & Estabrook 2008 [compatibility analysis]); in the first study Chloranthales, monocots, and Piperales were successively sister to the remaining taxa, but these relationships also had little support. Zanis et al. (2002) analysed 11 genes from all genomes and found some support for the magnoliids (strong support for this clade) as being sister to eudicots, with Chloranthaceae, and [monocots + Ceratophyllaceae] occurring as successively more basal branches; below these were the ANITA grade (see also Graham & Olmstead 2000; Borsch et al. 2003). Support for some of these nodes depended on the method of analysis (see also Borsch et al. 2000; Graham & Olmstead 2000; Hilu et al. 2001; Whitlock et al. 2001; Zanis et al. 2002) or the particular gene studied (see Duvall & Bricker 2002: nuclear 18s; Hilu et al. 2003: matK; Duvall et al. 2006: nuclear 18S in particular causes problems). Parkinson et al. (1999) found some evidence for a [Piperales + eudicot] clade, but support was weak. Davis et al. (2004) found the magnoliids to be sister to monocots, with Chloranthaceae and Ceratophyllaceae successively sister to a clade including the few eudicots in the analysis, but support was not exactly overwhelming (the best supported topology in Duvall et al. 2006 is somewhat similar). There was fairly good support for a clade [monocots + Ceratophyllaceae] in a compartmentalised 6-gene analysis (Zanis et al. 2003; see also Qiu et al. 1999; some analyses in Saarela et al. 2007). Müller et al. (2006) found very poorly supported relationships between Chloranthaceae and monocots, which together linked with the magnoliids. In work by Whitlock et al. (2002) largely similar groupings were recognised, but support was only moderate; the exact position of Chloranthaceae remained unclear. Some analyses suggested the possibility of a sister taxon relationship between Chloranthaceae and eudicots (Borsch et al. 2003). Hilu et al. (2003) in a matK analysis, suggested that magnoliids were sister to monocots, although the support was weak in parsimony analyses if 100% posterior probabilities in Bayesian analyses, furthermore, in the latter case only, [Chloranthacaeae + monocots] were sister to magnoliids, although the probabilities there were low. Qiu et al. (2005; see also Löhne & Borsch 2005) found initial rather strong bootstrap support for an association between monocots and Ceratophyllaceae in a 9-gene analysis being vitiated by the failure to obtain much support in any of the subanalyses and by details of the topology obtained in the 9-gene analysis itself (e.g. Acorus sister to the Alismatales that were included) that are rather improbable. Other studies also show no clear pattern (e.g. Jansen et al. 2006a; Qiu et al. (2006b). The analyses in Mathews (2006a) preferred an unresolved position for Chloranthales and Ceratophyllales above the Austrobaileyales. Duvall et al. (2006) and Qiu et al. (2010: chloroplast data, support weak) found a relationship between Chloranthales and Ceratophyllales, as did N. Zhang et al. (2012), that clade being successively sister to the magnoliids and monocots (see also Doyle & Endress 2014). Soltis et al. (2007a) found that relationships of Chloranthaceae were unclear and there was very weak support for monocots as sister to [magnoliids, Chloranthaceae, eudicots, etc.]. Although relationships between basal angiosperms were not their focus, Xue et al. (2012) found the relationships [monocots [eudicots [Ceratophyllaceae + Piperaceae]] in a ML analysis of whole chloroplast genomes. In Ruhfel et al. (2014: whole chloroplast genomes) Piperales were sister to Ceratophyllaceae in amino acid analyses, for example, while one tree in Drew et al. (2014) even had a clade [Chloranthaceae [monocots [Ceratophyllaceae + Piperaceae]]].
Morphology in particular has quite often suggested that more or less herbaceous clades like Piperales, Chloranthaceae, and Nymphaeales might be related to monocots, the pal(a)eoherb hypothesis (see e.g. Donoghue & Doyle 1989; Taylor & Hickey 1992; Endress 2000). Analysis of combined morphological and molecular data found that Piperales were sister to monocots (Doyle & Endress 2000, support weak). Although quite popular in the latter years of the last century, the palaeoherb support comes from homoplasies associated with the adoption of the herbaceous habit. Indeed, Piperales are now firmly (usually!) embedded in the magnoliid clade while Nymphaeales are very near the base of the whole angiosperm clade.
Some resolution may be on the way. Thus Graham et al. (2005) found a rather weakly supported (73% bootstrap) [monocot + eudicot] grouping, but this was weaker when Chloranthaceae and Ceratophyllaceae were included; Xue et al. (2012: whole chloroplast genomes) also found the relationships in the Summary Tree. Evolution of some floral developmental genes, e.g. in the C and D lineages, are also consistent with such relationships (Kramer et al. 2004). The positional relationships between members of the androecium and the perianth, the stamens being individually opposite perianth members, and perhaps some other characters (trimery of some floral whorls is fairly widespread within Ranunculales) are also consistent with such relationships. (There is the same perianth member/stamen relationship in magnoliids like Lauraceae.) Variation in how calcium oxalate is synthesized may also be of phylogenetic interest, although sampling is very poor; neither members of the ANITA grade nor magnoliids have been examined. Vacuolar crystal formation associated with membranes and paracrystalline bodies with widely spaced subunits are found in eudicots (crystals seem also to be formed in other ways here), while in monocots there are no membrane complexes and the paracrystalline bodies have closely spaced subunits (Horner & Wagner 1995; Evert 2006). Some patterns of RNA editing may be phylogenetically informative at this level (Logacheva et al. 2008).
Other studies have found this [monocot + eudicot] grouping; Jansen et al. (2006b: 37 whole chloroplast genomes, see also Zhengqiu et al. 2006), Cai et al. (2006: 35 whole chloroplast genomes, neither Chloranthales, Ceratophyllales, nor any member of Austrobaileyales included), and Duvall et al. (2006: four genes, three compartments, nuclear PHYC gene, 18S being excluded; overall, a relationships between magnoliids and monocots was preferred), Mathews (2006a: three PHY genes, 105 taxa), and Hansen et al. (2007: 61 protein-coding chloroplast genes). When sequences of complete chloroplast genomes are analysed, an association between monocots and eudicots is more strongly suggested. Thus Jansen et al. (2007) found good support for a [monocot + eudicot] grouping, a number of alternative topologies being excluded, but support in Moore et al. (2007) was somewhat less strong. Ceratophyllum, with quite a long branch, was sister to eudicots (in some reconstructions, Piper, with a very long branch, was also involved), and Chloranthus was sister to the magnoliids with moderate to strong support (Jansen et al. 2007), a position also found by Saarela et al. (2007), many analyses in Moore et al. (2007, 2010), and Smith et al. (2010).
However, in Moore et al. (2010) there were a variety of other "minority" relationships - Ceratophyllum or [Ceratophyllum + Piper] as sister to monocots, and Chloranthaceae sister to a clade including magnoliids, monocots, and eudicots; the latter pair of relationships with moderate jacknife support were found by Davis et al. (2013) in their comprehensive chloroplast analysis focussing on monocots. Goremykin et al. (2009b) found a [Ceratophyllum + magnoliid] clade (Chloranthaceae were not included) after removing 2,500 highly variable positions from the analysis of chloroplast genome data; with the removal of 1,000 positions Ceratophyllum was sister to a [monocot + eudicot] clade. Analyses of morphological data gave a grouping [Ceratophyllum + Chloranthaceae] with quite strong support (Endress & Doyle 2009; see also Huang et al. 2010, weak support using the ycf2 gene; Moore et al. 2011, very weak support). Finally, in the massive parsimony analysis of Goloboff et al. (2009) a set of relationships [Ceratophyllum [[Amborella + Nymphaeales]....[[Chloranthaceae + monocots] eudicots]]] was retrieved, Duarte et al. (2010) found the relationships [monocots [magnoliids + eudicots]], and Tamura et al. (2011: 6 plastid, 7 mitochondrial, and 1 nuclear genes sequenced) found some support for a [Piperales + monocot] clade, as did Barrett and Davis (2011: or [Piperales + Ceratophyllales] the sister group). For another study, see Fiz-Palacios et al. (2011).
Lee et al. (2011) found a clade with monocots sister to all angiosperms minus Nymphaeales and Amborellales, and also a [magnoliid + eudicot] clade, both with strong support. Although this may be a sampling problem (no Austrobaileyales, Chloranthales or Ceratophyllales were included), Lee et al. (2011) initially looked at almost 23,000 sets of orthologues from nuclear genomes of 101 genera of land plants (most taxa represented by ESTs, genes included if represented in as few as 4 taxa). Finally, one alignment of 18S/26S nuclear ribosomal data suggest a clade [Ceratophyllaceae + Tofieldiaceae] embdeedded with the monocots, but thankfully with little support (Maia et al. 2014), and these relationships were not retrieved in other analyses.
Nevertheless, pending further studies, the relationships [[Chloranthales + magnoliids] [monocots [Ceratophyllales + eudicots]]] are used as a basis for further discussion, rather different from the relationships suggested in the first six editions of this site and also from the tree in A.P.G. II (2003) and Soltis et al. (2005b). Direct links are provided to the pages where the main clades just mentioned are discussed further: Ceratophyllales, Chloranthales, eudicots, and monocots.
[CHLORANTHALES [[MAGNOLIALES + LAURALES] [CANELLALES + PIPERALES]]]: sesquiterpenes +; seed endotestal.
[[MAGNOLIALES + LAURALES] [CANELLALES + PIPERALES]] / MAGNOLIIDS / MAGNOLIANAE Takhtajan: (neolignans +); vessels solitary and in radial multiples, (with simple perforation plates in primary xylem); (sieve tube plastids with polygonal protein crystals); lamina margins entire; A many, spiral [possible position here], extrorse; ovules with hypostase, nucellar cap +, raphal bundle branches at the chalaza; antipodal cells soon die. Back to Main Tree
4 orders, 20 families, 9900 species.
Age. Crown group magnoliids diverged 134.5-125.7 m.y.a. (Moore et al. 2007), while Bell et al. (2010: note topology) suggested ages of (138-)122(-108) or (130-)125(-121) m.y. depending on the method used. Magallón and Castillo (2009) estimated crown group divergence at ca 201.7-198.2 and 128-127.7 m.y.a.. Other estimates range from (181-)155(-136) m.y. old (with eudicot calibration) to (198-)163(-138) m.y. (without: Smith et al. 2010), to around 139.1-133.1 m.y. (Naumann et al. 2013), (144-)116(-89) m.y. (N. Zhang et al. 2012), (152.7-)117.3(-39.1) m.y. (Xue et al. 2012), or (155-)149, 137(-131) m.y. (Wikstöm et al. 2001), while Magallón et al. (2013: with temporal constraints) suggested an age of around (167.2-)147.7-142.6(-128.5) m.y. for this clade.
An earlier fossil-based estimate for both stem and crown divergence is ca 98 m.y. (Crepet et al. 2004: magnoliids sister to monocots). For summaries of the fossil history of the group, especially prominent in the Mid Cretaceous and later, see Friis et al. (1997, 2006, 2011).
Evolution. Ecology & Physiology. This clade has distinctively large leaves (Cornwell et al. 2014); magnoliids are generally plants of well watered, warm, and equable conditions.
Plant-Animal Interactions. Caterpillars of Papilionidae-Papilioninae butterflies are notably common (almost 33% of the records) on members of this group; they are, however, not known on Myristicaceae, in Laurales they predominate on Lauraceae, and in Piperales two clades in particular are found on Aristolochiaceae (see Scriber et al. 1995 for references; Zakharov et al. 2004; ; Simonsen et al. 2011; Condamine et al. 2011). They are also commonly found on Rutaceae, which have similar alkaloids.
Chemistry, Morphology, etc. Hegnauer (1990) discussed the chemistry of the Polycarpicae, which includes Austrobaileyales and Ranunculales; similar isoflavonoids are found in Magnoliaceae, Lauraceae and Chloranthaceae.
For a convenient summary of a number of features of wood anatomy, see Herendeen et al. (1999b). Magnolioid roots are scattered through the clade, being recorded from a number of woody members of Laurales and Magnoliales. These roots are stout, often ³3 mm across, lack root hairs (?always), and are endomycorrhizal - associated conditions (see Baylis 1975; St John 1980). Taxa with broadly lobed leaf blades are scattered throughout this clade (but not in the small Canellales). See Erbar (1983, inc. Illicium) for carpel morphology and Ronse Decraene and Smets (1992b) for androecial morphology.
Phylogeny. Although the sister group relationship of Piperales with Canellales in particular is at first sight unexpected, the magnoliid clade as a whole and the relationships within the group are turning out to be quite robust (Massoni et al. 2014: good generic sampling, 12 markers from three compartments). There was not much morphological support for this grouping (Doyle & Endress 2000); features like tectum structure, etc., showing considerable variation (J. A. Doyle 2005). However, molecular support for the clade has been increasing in successive studies (e.g. Qiu et al. 1999, 2000, 2005: support levels depend on the analysis, the node sometimes collapses], 2006b, 2010; Zanis et al. 2002; Jansen et al. 2006b; Zhengqiu et al. 2006; Cai et al. 2006; Müller et al. 2006: support for [Canellales + Piperales] poor; Jansen et al. 2007: little maximum parsimony support; Moore et al. 2007: group not in all analyses; Soltis et al. 2007a; Soltis et al. 2011). Support includes the possession of unique indels (Löhne & Borsch 2005). Soltis et al. (2007a) found weak support for a grouping [Magnoliales + Canellales]; relationships in Bell et al. (2010) are [Piperales [Laurales [Canellales + Magnoliales]]], although they have little support.
[MAGNOLIALES + LAURALES]: cuticle waxes as annularly-ridged rodlets, palmitol the main wax; A whorled; pollen 1-2 nexine foliations, outer member massive, lamellate endexine; (supra-stylar extra-gynoecial compitum/pollen tube growth); carpel cross-zone initiated late; ovules 1(-2)/carpel, basal, erect, apotropous; fruitlets 1-seeded.
Age. Magallón and Castillo (2009) suggest that the two clades diverged ca 198.2 and 127.7 m.y.a. - relaxed and constrained penalized likelihood datings, while Magallón et al. (2013) suggested an age of around 137.2 m.y. and Naumann et al. (2013) an age of around 129.5 or 126.4 m.y.. Xue et al. (2012) estimated an age of only 104.5 m.y., the lowest estimate so far.
Evolution. Ecology & Physiology. A major increase in seed mass, and to a lesser extent an increase in plant height and in leaf mass per area (SLA) can be pinned to this node (Cornelissen et al. (2014; for seed size, see also Moles et al. 2005a; Sims 2012).
Divergence & Distribution. There is considerable variation as to how the androecium is initiated; it would not take much for "flowers with inner staminodes" to be an apomorphy at this level. For the supra-stylar compitum, see Wang et al. (2011).
MAGNOLIALES Bromhead Main Tree.
Vessels in multiples; secondary phloem stratified; pith septate [with sclerenchymatous diaphragms]; nodes 3:3; petiole vasculature an arc with an adaxial plate; branching from the current innovation; leaves two-ranked, lamina vernation conduplicate; "bract" sheathing; P whorled; G occluded by fusion and secretion; ovule with outer integument 5-10 cells across, obturator +; seeds medium-sized, testa vascularized, multiplicative; endosperm ?type, ruminate, ruminations irregular. - 5 families, 154 genera, 2929 species.
Age. Magallón and Castillo (2009) suggest possible ages for the crown group of around 171.5 and 116.6 m.y., Bell et al. (2010) ages of (96-)76, 69(-50) m.y.; other ages are (119-)113, 108(-102) m.y. (Wikstöm et al. 2001).
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...
Evolution. Divergence & Distribution. There is extensive discussion on character evolution in Sauquet et al. (2003), and much of the character hierarchy here is based on this paper. However, where characters like extrorse/introrse anther dehiscence and ruminate/non-ruminate testa are placed on the tree depends on how the characters are optimised, or even defined (e.g. ruminate endosperm). There is also some conflict with the positions of characters as they are optimised on a more extensive tree for basal angiosperms, although less detailed for Magnoliales (c.f. Ronse De Craene et al. 2003, also Judd et al. 2003). Doyle and Endress (2000) and Soltis et al. (2005) suggest additional characters for the clade, including reduced fibre pit borders, palisade parenchyma, foliar astrosclereids, and pollen with continuous tectum; Doyle and le Thomas (2012) outline pollen evolution. More characters may well need to be added to the apomorphy scheme for the order.
Chemistry, Morphology, etc. Intra- and interfamilial variation of morphological characters that are frequently used to reconstruct phylogenies is considerable, in particular, Furness et al. (2002) emphasize the variability of microsporogenesis in the order.
The "bracts" with sheathing bases that have been reported for a number of Magnoliales (Endress & Armstrong 2011: condition in Degeneriaceae?), are perhaps a little unexpected since the leaf bases in the clade tend to be quite narrow - except for the stipulate Magnoliaceae. Deroin (2010) noted a tendency for the vasculature of the perianth and/or androecium in some Annonaceae and Magnoliaceae to be pentamerous.
For additional information, see Benzing (1967) and Sugiyama (1976a, b, 1979), all nodal anatomy, considerable variation in cotyledonary node, Hiepko (1964b: perianth vasculature), Endress (1977b, 1986a, 1994a: floral morphology), van Heel (1981, 1983: carpel development), Erbar and Leins (1983: floral development), Metcalfe (1987: general anatomy), Taylor and Hickey (1995: general), Ronse Decraene and Smets (1996a: androecium), Kimoto and Tobe (2001: embryology), and Kim et al. (2003, 2004: AP3 and P1 genes: Myristicaceae not sampled).
Phylogeny. Molecular data suggested that Myristicaceae are sister to the rest of the order, but support was only moderate (D. Soltis et al. 2000); the addition of morphological data strengthened that position, and also placed Magnoliaceae as sister to the remaining taxa (Doyle & Endress 2000), although the latter position had only moderate support (c.f. P. Soltis et al. 2000; see also Sauquet et al. 2001). The family pairs [Annonaceae + Eupomatiaceae] and [Degeneriaceae + Himantandraceae] are both well supported (D. Soltis et al. 2000; P. Soltis et al. 2000; Doyle & Endress 2000). Other studies confirm these relationships (Sauquet et al. 2003; Müller et al. 2006), and they are followed here, however, considerable uncertainty remains about the position of Magnoliaceae in particular. Some genes seems to have particularly disconcerting effect, thus the 26S rDNA gene caused the association of Degeneriaceae with Myristiccaeae, and this was not because of a mislabelled sequence (Massoni et al. 2014).
Hilu et al. (2003: matK analysis alone, ?sampling) found a somewhat different but poorly supported set of relationships, and Qiu et al. (2010: mitochondrial genes) also recovered a somewhat different topology, Degeneriaceae being sister to the rest of the order minus Myristicaceae, although again support was weak. Soltis et al. (2011) found that Magnoliaceae were sister to the rest of the order, the clade [Degeneriaceae + Myristicaceae] had good support although otherwise support was weak; this unexpected topology was ascribed to signal from rDNA sequences. Finally, Morton (2011: nuclear gene Xdh) found a set of relationships [Himantandraceae [Myristicaceae [Degeneriaceae [the rest]]]].
Includes Annonaceae, Degeneriaceae, Eupomatiaceae, Himantandraceae, Magnoliaceae, Myristicaceae.
Synonymy: Annonales Berchtold & Presl, Degeneriales C. Y Wu et al., Eupomatiales Reveal, Himantandrales Doweld & Shevyryova, Myristicales Berchtold & Presl - Magnoliineae, Myristicineae Chatrou - Annonanae Doweld, Magnolianae Takhtajan - Magnoliidae Takhtajan - Magnolipsida Brongniart - Magnoliid I group (Nandi et al. 1998).
MYRISTICACEAE R. Brown Back to Magnoliales
Tree, branches plagiotropic, pseudowhorled; exudate +, red; isoflavonoids, flavonoids diverse [flavones +], polyketide [acetogenins], (tryptamine) alkaloids +, isoquinoline alkaloids 0; cork also in outer cortex; primary stem ± with continuous cylinder; vessel elements with simple or scalariform(-reticulate) perforations; tannin-containing tubes in the xylem; sieve tubes with non-dispersive protein bodies, (plastids with protein crystalloids and starch); petiole bundles bicollateral; (branched) sclereids or fibres +; (acicular) crystals +; hairs branched, arbuscular to stellate (T-shaped); cuticle waxes as platelets; (leaves spiral), (lamina lobed - some Knema); plants dioecious; flowers small (<1 cm across), polysymmetric, receptacle small; P (2-)3(-5), uniseriate, connate; staminate flowers: A whorled (spiral), 2-40, connate (not), (anthers unithecate); (pollen inaperturate, ulceroid, spiraperturate, ektexine granular), pollen aperture membrane sculpted; pistillode 0; carpellate flowers: staminodes 0; G 1; (stylulus ± long), stigma 2-lobed to peltate; ovule 1/carpel, subbasal, inner integument (3-)7-10 cells across; fruit a follicle, dehiscing abaxially as well, (indehiscent); seed large [³1 cm across], pachychalazal, aril +, micropylar-funicular, vascularized, (aril small); exotesta thick-walled, endotesta palisade, lignified, crystalliferous, tegmen multiplicative or not, exotegmen with fibres or sclerotic or tracheidal cells, chalaza massive, with a lignified counter-palisade; endosperm nuclear, with (starch and) oil; embryo with hypocotyl not developed; n = 20, 22, 25, 26; germination epigeal, phanerocotylar, or hypogeal.
20[list]/475: Myristica (175), Horsfieldia (100), Knema (95), Virola (60). Pantropical, few mainland Africa (map: from de Wilde 2000 [Indo-Malesia]; Heywood 2007; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003).[Photo - Carpellate flower, Fruit].
Age. Crown-group Myristicaceae are estimated to be a mere 21-15 m.y. old (J. A. Doyle et al. 2004).
The discovery of fossil seeds apparently of Myristicaceae from the Eocene (London Clay) does not bear on the crown-group age because they cannot be placed precisely on the tree of the family (J. A. Doyle et al. 2008a).
Floral formula: * P ; A [2-40]: * P ; G 1.
Evolution. Divergence & Distribution. Crown-group diversification in Myristicaceae, some 21-15 m.y.a., is very recent indeed given possible stem ages of the family that are over 100 m.y. more (see above), its distribution throughout the humid tropics, and its apparently low dispersability (J. A. Doyle et al. 2004). Sauquet et al. (2003) found that there was a long branch leading to crown Myristicaceae and little molecular divergence between its extant members, which might also suggest recent diversification. In this respect Myristicaceae can be compared with Annonaceae, also pantropical but a little younger; there diversification may have begun mid-Cretaceous or slightly later (Doyle et al. 2004; Scharaschkin & Doyle 2005; esp. Couvreur et al. 2011a; Doyle et al. 2012).
See Chatrou (2003) for possible apomorphies.
Ecology & Physiology. Myristicaceae are disproportionally well represented (11 of the 57 species of the family recorded) of the 227 common trees (d.b.h. at least 10 cm) of the Amazonian forests (ter Steege et al. 2103).
Pollination Biology & Seed Dispersal. Polllination is the Indo-Malesian region, at least, is by small beetles (Corlett 2004).
Genes & Genomes. Isozyme duplication (in Myristica) suggests ancient polyploidy (Soltis & Soltis 1990).
Chemistry, Morphology, etc. There are free phloem strands in the center of the midrib bundle. The wood rays are not notably broad.
Inflorescence morphology is a little confusing. Ronse de Craene (2010; see also Armstrong & Tucker 1986) shows a large, abaxial "bracteole" in addition to paired lateral prophyllar/bracteolar-like structures that may (staminate inflorescence) or may not subtend buds. The "bract" immediately below the staminate flower of Myristica fragrans has a very broad base.
There are three traces per perianth lobe (Siddiqui & Wilson 1976). The synandrium of Myristica has a sterile apex, probably axial (Armstrong & Tucker 1986), and judging from the vasculature, the unithecal anthers found in some species of Myristica represent half of a divided bithecal anther (Wilson & Maculans 1967; Armstrong & Tucker 1986); anthers in Knema are tetrasporangiate (Xu & Ronse de Craene 2010a). For the complex vascularisation of the carpel in Myristica, see Wilson and Maculans (1967), and for the vascularization of the ovule in Myristica fragrans, see Dickison (2000). A small structure developing between the two integuments is reported by Nair (1972). Corner (1976) commented on the complexity of the seed coat in Myristicaceae which is as elaborate as that of any other angiosperm. Not all taxa appear to have a multiplicative testa, and some have a multiplicative tegmen; the ruminations may develop best in the pachychalazal part of the seed.
For more information, see Kühn and Kubitzki (1993: general), de Wilde (2000: Malesian Myristicaceae), Hegnauer (1969, 1990: chemistry), Kerster and Baas (1981: anatomy), Cremers (1973) and Jiménez-Rojas et al. (2002), both growth patterns, Sauquet (2003: androecium), Sauquet and Le Thomas (2003: pollen), Mauritzon (1939a) and Endress (1973), both seeds, and Oginuma et al. (2012: chromosome numbers, a few South East Asian-Malesian taxa only known).
Phylogeny. Relationships within the family are unclear. The African and Madagascan taxa may form a clade, possibly sister to Compsoneura (but perhaps long branch attraction), overall, geography and relationships may be summarized as [[Asia + America] [Madagascar and Africa]]. Within Asian/Malesian Myristicaceae, Knema and Myristica may be sister taxa. Sauquet et al. (2001, 2003), Sauquet (2003) and Sauquet and Le Thomas (2003) suggest that the free stamens (in some species they are numerous and apparently spirally inserted) and small aril of Mauloutchia, apparently plesiomorphic features, are in fact more likely to be derived.
[Magnoliaceae [[Degeneriaceae + Himantandraceae] [Eupomatiaceae + Annonaceae]]]: primary stem with distinct bundles [eustele]; wood with broad rays; flowers solitary, large [>1.5 cm across]; P = K + C; A many, spiral [possible position here], filaments with three veins, anther thecae separate, embedded in the broad connective, connective prolonged [one position]; tectum imperforate; G spiral; ovule with funicular obturator; ³1 seeds/fruitlet; 10-aa deletion in PI-derived motif in AP3 gene.
Age. This node can be dated to 120-100 m.y.a. (Doyle et al. 2004), also (108-)101, 97(-90) m.y.a. (Wikström et al. 2001), (106-)102(-98) m.y.a. (Su & Saunders 2009), ca 114.7 m.y. (Naumann et al. 2013), or as recently as ca 71.1 m.y.a. (Magallón et al. 2013).
Chemistry, Morphology, etc. There is more than one kind of cortical vascular system here, and what parts of the flower are supplied by which system varies (Ronse De Craene et al. 2003, see also Deroin 1991, 1999a).
MAGNOLIACEAE Jussieu Back to Magnoliales
(Deciduous); (silicon concentration high), sesquiterpene lactones +; vessel elements with simple and scalariform perforation plates, (walls vestured - Liriodendron); wood fluorescing; (secondary phloem ± stratified, rays broad); (sieve tube plastids with polygonal protein crystalloids and starch - Magnolia); nodes >6:>6; pith septate; resin cells +; petiole also with medullary bundles (strictly annular - Liriodendron); leaves also spiral, lamina vernation laterally or vertically conduplicate (supervolute-curved), stipules +, sheathing stem, open opposite petiole; (dioecious); flowers terminal or axillary, ± polysymmetric; receptacle much elongated; P 2, 3 + 3, or 3 + many, K and C ± distinguishable, ± whorled; (A introrse - Magnolia), (endothecium biseriate), (filament vein single), tapetal cells multinucleate; pollen grains boat-shaped; G 1-many, fusion complete, but secretory canal +, stigma (terminal), dry, elongate (not); ovules(1-)2-12(-16)/carpel, micropyle exo/bistomal/zig-zag, outer integument 4-10 cells across, inner integument 2-3(-4) cells across, parietal tissue 2-8 cells across; fruit dehiscing abaxially (circumscissile), (indehiscent, winged); sarcotesta +, endotesta lignified [fibres], (tegmen ± tanniniferous), (testa inconspicuous - Liriodendron); endosperm not ruminate, (nuclear - "Magnolia" septentrionalis); n = 19.
2[list]/227: Magnolia (ca 225). The Americas (but not W. North America), and South East Asia to Malesia (map: from Good 1974; Lozana-Contreras 1994).[Photo - Collection.]
Age. Molecular estimates of the crown group age are (54-)36, 33(-17) m.y. (Bell et al. 2010: note topology) or (86-)79, 70(-63) m.y. (Wikström et al. 2001).
Archaeanthus, a Cenomanian fossil of some 98 m.y. in age from North America, may be assignable to Magnoliaceae (Dilcher & Crane 1984); it is placed sister to the family in the constrained morphological analysis of Doyle and Endress (2010). It has follicular fruits that fall off the axis each follicle having 10-18 winged seeds. Romanov and Dilcher (2013: ?outgroup) placed Archaeanthus, along with Liriodendroidea, known from its winged seeds, as sister to Liriodendron, which would call into question the accuracy of the molecular estimates above.
Lesqueria, from about the same period, may also belong around here; it has similar fruits (Crane & Dilcher 1984). The fruits of Protomonimia, in Turonian deposits from Japan ca 91 m.y. old, have several carpels borne in spirals on a concave axis; there is a stigmatic crest. The young seeds have a thick testa, the exotesta being palisade and with sinuous anticlinal cell walls (Nishida & Nishida 1988); they may be of a taxon somewhere near Magnoliaceae, although i.a. the shape of its receptacle is very different.
Evolution. Divergence & Distribution. Liriodendron was widely distributed in the Northern Hemisphere in the early Tertiary (Ferguson et al. 1997). For divergence ages of and within Magnolia, see Azuma et al. 92001) and Nie et al. (2008).
Pollination Biology. Beetles are common pollinators, and the flowers of species like Magnolia ovata, pollinated by dynastid scarab beetles, are thermogenic (Seymour 2001; Gottsberger et al. 2012). Floral scents of the family have been extensively studied (Azuma et al. 1999; Gottsberger et al. 2012).
Genes & Genomes. Both isozyme duplication and stomatal size increase over time suggest ancient polyploidy (Soltis & Soltis 1990; Masterson 1994).
Chemistry, Morphology, etc. Sclerenchymatous diaphragms in the pith of the stem are particularly conspicuous in the Michelia group of Magnolia. Terminal tracheids are commonly silicified, forming distinctive phytoliths (Piperno 2006).
The endexine is lamellate and the columellae fused-granular (Xu & Kirchoff 2008). Nectar is secreted from the exposed surfaces of the carpels in some species of Magnolia. The micropyle is exostomal in the Michelia group of Magnolia. The seed of Magnolia may dangle from the open fruitlet attached by extended annular thickenings of the protoxylem vessels.
Liriodendron: leaves lobed, with palmate secondary veins; petiole bundle strictly annular; fruit a samara, single-seeded; seeds lack a sarcotesta, mesotesta more or less sclerotic; endosperm slight and not ruminate. Magnolia: leaves entire; anthers introrse; ovule lacks a funicular obturator(?); fruit dehiscent. but not adaxial (so the fruit is not a follicle in the strict sense); sarcotesta +, scleroendotesta with crystals and lignified fibrils in the cells; endosperm copious. There is also a simple or tubular pore in the seed coat that marks the passage of the vascular bundle through the sclerotesta (Xu 2003).
Some information is also taken from Hegnauer (1969, 1990: chemistry), Bouman (1977: ovules and seeds of Liriodendron), Nooteboom (1993: general), Yamada et al. (2003b: ovules), Pan et al. (2003) and especially Fu et al. (2012 and references), both embryology, Xu (2006) and Xu and Rudall (2006: floral development), and Xu and Kirchoff (2008: pollen morphology); see Azuma et al. (2000), Ueda et al. (2000) and Wang et al. (2006) for molecular phlogenies, Figlar (2000) for branching patterns, Charlton (1994) and Liao and Xia (2007) for phyllotaxis and vernation.
Phylogeny. Magnolia s. str. is pretty wildly paraphyletic, and section Talauma is sister to the rest of Magnolia (Qiu et al. 1995; Kim et al. 2001a, b). Spport along the backbone of then genus (s.l.) is poor, although there are 11 or more well-supported clades along it (Azuma et al. 2001, 2011; Nie et al. 2008; Kim & Suh 2013).
Classification. It seems best to expand Magnolia to encompass the whole of the current Magnolieae; the family thus includes only two genera and tribes are superfluous; see also Nooteboom (2000) and Kim and Suh (2013) for suggestions about classification. However, Romanov and Dilcher (2013) need an order for the family, while Xia (2012) and Sima and Lu (2012) provide a reclassification of Magnolia in which it is divided into 16 genera placed in two tribes... For a checklist and bibliography (under some old generic names), see Frodin and Govaerts (1996).
Synonymy: Liriodendraceae F. Barkley
[[Degeneriaceae + Himantandraceae] [Eupomatiaceae + Annonaceae]]: flower haplomorphic; anthers valvate, inner staminodes +; pollen smooth, exine thin, [0.2-1.3 µm across], nexine foliations?, infratectum granular; style with differentiated transmission tissue; seed ruminations irregular [DELTRAN optimization], mesotesta fibrous.
Age. Endressinia brasiliana, from the Brazilian Crato formation of some 113 m.y.a. has i.a. distinctive glandular staminodia. It is placed sister to this clade by Doyle and Endress (2010), largely confirming the position suggested by Mohr and Bernardes-de-Oliviera (2004).
Chemistry, Morphology, etc. Doyle (2007) noted that the venation here is often poorly differentiated and so of low rank (but c.f. many Annonaceae, albeit not "basal" members) - I have not placed this character on the tree. For the inner staminodes that are often so conspicuous in the flowers, and their function in pollination - food for pollinators, attractants - see Endress (1984).
[Degeneriaceae + Himantandraceae]: flowers axillary; nexine foliations absent; outer integument with annular opening; x = 12.
Age. The age of this node is around (59-)42, 38(-22) m.y. (Bell et al. 2010) or (80-)73, 63(-56) m.y. (Wikström et al. 2001), c.f. topology.
DEGENERIACEAE I. W. Bailey & A. C. Smith Back to Magnoliales
Alkaloids 0; cork ?; vessel elements with scalariform perforation plates; sieve tube plastids with polygonal protein crystalloids and starch; nodes 5:5; petiole also with medullary bundles; secretory cells 0; cuticle waxes as platelets; leaves spiral; bracts?; K 3, C many, whorled; pollen boat-shaped; G 1, basally ascidiate, occluded by fusion only, stigmatic crest much elongated; ovules many/carpel, outer integument 7-8 cells across, inner integument ca 3 cells across, funicle long; fruit a follicle; exotestal cells palisade, thin-walled, sarcomesotesta +, endotesta with lignified internal fibrils; suspensor massive, embryo with 3 (4) cotyledons.
1[list]/2. Fiji, Viti Levu (map: original!).
Chemistry, Morphology, etc. Some information is taken from Hegnauer (1973, 1990, as Winteraceae: chemistry) and Kubitzki (1993b: general).
HIMANTANDRACEAE Diels Back to Magnoliales
Polyketide alkaloids only; vessel elements with simple (and scalariform) perforations; sieve tubes with non-dispersive protein bodies; trichomes peltate; cuticle wax crystalloids 0; branching?; P or bract + bracteoles enclosing the flower in 2 series, caducous, or 2 connate + 4 connate; "C" 3-23 [staminodial]; pollen scabrate; additional staminodes with glands; G 6-30, (1) 2 pendulous ovules/carpel; fruit ± syncarpous, drupaceous, with several stones; seeds laterally flattened, ?ruminations; testa not multiplicative, endotesta aerenchymatous; endosperm development?; seedling?
1 (Galbulimima)[list]/2. The Celebes, New Guinea and N.E. Australia (map: from Hoogland 1972; Endress 1983). [Photo - Flower, Fruit, Buds, Habit]
Chemistry, Morphology, etc. For the testa, see Doweld and Shevyryova (1997); the ruminations are at best obscure. The perianth may be staminodial in origin; according to Johri et al. (1992) the outer integument is not vascularized. Some other information is taken from Hegnauer (1966, 1989: chemistry) and Endress (1993: general).
[Eupomatiaceae + Annonaceae]: sieve tube plastids also with polygonal protein crystalloids; rays 8-15-seriate; petiole bundles arcuate; prophyll single, adaxial; lamina vernation conduplicate; inflorescence +; nexine foliations undifferentiated; fruit ± berry-like.
Age. Estimates of the time of divergence of these two families vary considerably: Around (69-)55, 50(-35) m.y. (Bell et al. 2010), ca 64.75 m.y. (Naumann et al. 2013), (97-)91, 82(-76) m.y. (Wikström et al. 2001), and (110.4-)106.3(-102.0) m.y. (Couvreur et al. 2011a: HPD estimates). Other suggested ages are (110.4-)101.7(-99.4) m.y. (Surveswaran et al. 2010: HPD estimates), (101.5-)98.0(-94.9) m.y. (Su & Saunders 2009), or somewhere between 84.7 and 62.6 m.y. (Erkens et al. 2009: a variety of estimates); see also the estimate of 109-100 m.y.a. in Pirie and Doyle (2012).
Evolution. Divergence & Distribution. Optimisation of prophyll position on the tree is uncertain. Adaxial prophylls are common in Annonaceae, including Anaxagorea, although some taxa have paired, lateral prophylls (Fries 1911).
EUPOMATIACEAE Orban, nom. cons. Back to Magnoliales
Also rhizomatous, with xylopodium or root tubers; pith not septate; vessel elements with scalariform perforation plates; secondary phloem stratification?; sieve tubes with non-dispersive protein bodies [check], plastids also with protein rods; nodes (5-)7(-11):(5-)7(-11); secretory cells +; (stomata anomocytic); trunk leaves spiral; inflorescence fasciculate; receptacle concave, calyptra +, thick, deciduous, with sclereids, phyllotaxis spiral; P 0; A introrse, staminodes 15+, petal-like, connate basally, with many glands; pollen with encircling equatorial sulcus; G many, ± connate, ascidiate, occluded by fusion only, placentation sublaminar, stigma flat, papillate; ovules 2-11/carpel; fruit a "berry"; testa ?not vascularized, exotestal cells with thickened unlignified walls, endotesta unlignified, exotegmic cells cuboid, slightly lignified, endotegmic cells enlarged, crushed; n = 10; germination epigeal/phanerocotylar.
1[list]/3. New Guinea and E. Australia (map: from Hoogland 1972; Endress 1983). [Photos - Flower, Flower]
Chemistry, Morphology, etc. The main axes are mixed, initially being orthotropic and bearing spirally-arranged leaves, later becoming more or less plagiotropic and with 2-ranked leaves. There are about three two-ranked bracts on the pedicel; the calyptra itself is often interpreted as being a modified, amplexicaul bract (e.g. Endress 2003b; esp. Kim et al. 2005b). There is no evidence of isozyme duplication (Soltis & Soltis 1990).
Some information is taken from Hegnauer (1966, 1989: chemistry), Endress (1983, 1993: general) and Rix and Endress (2007: an easy account).
ANNONACEAE Jussieu Back to Magnoliales
Vessel elements with simple perforation plates; parenchyma in bands joining rays; lateral traces leaving stele well before central trace; sieve tube plastids also with protein filaments; epidermal cells with single crystals [?level]; (inflorescence leaf-opposed); pedicels articulated [level?]; flowers 3-merous, polysymmetric, pistillate and staminate phase flowers not on same plant; P very thick, 3, ± calycine, valvate, + 3 + 3, ± corolline, open to valvate; A whorled, filaments with a single vein; G plicate; funicle short; monocarp abscission at the base; endotestal plug +, mesotesta with several layers of longitudinal and internally of transverse fibres, aerenchyma internal; vascular bundle in antiraphe.
129/2220 [list] - four groups below. Largely tropical.
Age. Crown group diversification may have occurred (90.4-)89.5(-89) m.y.a. (Su & Saunders 2009: calibration on Futabanthus), 82-57 m.y.a. (J. A. Doyle et al. 2004), ca 84 m.y.a. (Scharaschkin & Doyle 2005; check), or 98-86 m.y. (Pirie & Doyle 2012); see Couvreur et al. (2011a) for other estimates.
Futabanthus, based on fossil flowers from the late Cretaceous (Early Coniacian, ca 89 m.y.a.) of Japan, can perhaps be assigned to crown-group Annonaceae (Takahashi et al. 2008b).
1. Anaxagoreoideae Chatrou, Pirie, Erkens & Couvreur
Ray cells with druses; uniseriate hairs terminate in a rounded cell, other hairs ± stellate; (petiole vascular tissue ± annular; with adaxial bicollateral plate; small arcuate bundles variously arranged); stomata allelocytic; trunk leaves 2-ranked; anther connective tongue-like, inner staminode secretions 0; orbicules +; G 3, receptacular vascular system 0; ovules 2/carpel; fruit an explosively dehiscent follicle; seed asymmetric; endotesta aerenchymatous, tegmen alone involved in ruminations, with oil globules; n = 8.
1/21. Tropical America, Sri Lanka to West Malesia, also Halamahera and Ceram (map: from Maas & Westra 1984, 1985). [Photo - Flower, Fruit, Fruit.]
Age. Divergence within Anaxagorea may have begun ca 44 m.y.a. (Scharaschkin & Doyle 2005) or 57-16 m.y.a. (Pirie & Doyle 2012).
[Ambavioideae [Malmeoideae + Annonoideae]]: ray cells lacking druses; trunk leaves spiral (two-ranked); (outer staminodes +), inner staminodes 0; ovules with outer integument 4-6 cells across, inner integument 2-4 cells across, nucellar cap to 5 cells across; fruit berrylets, (monocarp abscission at the apex); seed symmetric, with perichalazal ring; amyloid [xyloglucans] in endosperm +. (map: from Aubréville 1974a; Trop. Afr. Fl. Pl. Ecol. Distr. 1. 2003.)
Age. This node has been dated to (84.4-)74.7(-63.6) m.y.a. (Su & Saunders 2009), (76.6-)68, 64.5(-53.0) m.y. (Erkens et al. 2009), 70-65 m.y.a. (Couvreur et al. 2011a) and 90-73 m.y.a. (Pirie & Doyle 2012).
2. Ambavioideae Chatrou, Pirie, Erkens & Couvreur
Anther connective ± tongue-like to peltate-truncate; carpels 3-8, stipe articulated, (extragynoecial compitum + - Cananga), ovules (1)2-16/carpel, middle integument + (0), 4-6 cells across; (seed arillate), (endosperm ruminations lamelliform); n = 7, 8.
9/50: Drepananthus (26). Tropical, inc. Madagascar.
Age. Crown-group Ambavioideae have been dated to (80.9-)57.0(-52.3) m.y.a. (Surveswaran et al. 2010), (78-)69.4(-60.2) m.y. (Couvreur et al. 2011) and 59-27 m.y.a. (Pirie & Doyle 2012).
[Malmeoideae + Annonoideae]: (polyacetylenes +); neolignans 0?; petioles short; anther connective peltate-truncate; (pollen inaperturate), tectum retiperforate, infratectum columellate (granular), outer foliation of nexine massive; ovules 1-many/carpel,
Age. This node has been dated to (69-)66.7-56.6(-54.3) m.y. (Richardson et al. 2004), (78.1-)67.3(-55.2) m.y. (Su & Saunders 2009) and 86-71 m.y.a. (Pirie & Doyle 2012).
3. Malmeoideae Chatrou, Pirie, Erkens & Couvreur / The Short Branch Clade
(anther connectives not expanded/not covering the thecae); (pollen globose, ± spiny, disulcate/cryptoaperturate); (G 1), (stigma large/ peltate); (ovules 1/carpel); (tegmen with oil globules); endosperm ruminations spiniform (lamelliform); (mesotesta with transverse fibres only - Polyalthia); (inversion in the large single copy region - Miliuseae).
Polyalthia (100), Monoon (56), Pseuduvaria (50), Unoniopsis (45). Lowland tropics.
Age. The age of crown-group Malmeoideae has been dated to (66.1-)62.5-53.1(-49.5) m.y. (Richardson et al. 2004), (55.1-)39.8(-26.7) m.y. (Su & Saunders 2009) and 70-62 or 54-34 m.y.a. (Pirie & Doyle 2012, q.v. for several other estimates).
4. Annonoideae Rafinesque / The Long Branch Clade
(Lianes), (deciduous); (trunk leaves 2-ranked); (C 3); (anthers locellate), (outer staminodes +); pollen (in tetrads or polyads), in/omniaperturate, (exine foliations numerous), orbicules usu. 0; (G connate); (middle integument + - Artabotrys); (fruit follicle/dehiscing abaxially); endosperm ruminations lamelliform (irregular); n = 7-9.
Guatteria (280), Annona (120-175, soursop, sweetsop: inc. Rollinia), Xylopia (100-160), Uvaria (110-150), Artabotrys (100), Goniothalamus ([50-]130), Duguetia (70-95), Fissistigma (60), Monanthotaxis (55), Friesodielsia (50-60). Predominantly lowland tropics, rarely temperate.
Age. Crown-group Annonoideae may be (62.5-)60.2-51.1(48.7) (Richardson et al. 2004), (70.5-)59.6(-48.1) m.y. old (Su & Saunders 2009) or 80-64 m.y.a. (Pirie & Doyle 2012, also other estimates).
To be assigned to the above two subfamilies.
acetogenins [antimicrobial] +; terminal cell of uniseriate hairs pointed (hairs stellate); (primary stem with continuous cylinder); cambium storied; (sieve tube plastids also with protein fibres); petiole bundle also annular; branched sclereids or fibres common; secretory cells +; (prophyll single, adaxial); inflorescence cymose (leaf opposed), or flowers axillary; flowers A (³3), (latrorse, introrse), tapetal cells amoeboid, multinucleate; (microsporogenesis successive); (pollen grains with circular sulcus), (tricellular); G (3-)many (syncarpous; parietal placentation), when 3 opposite outer P, stigma capitate to U-shaped, wet, extragynoecial compitum common; (nucellar cap 0); (sarcotesta +), endotesta crystalliferous, (with thin walled, longitudinal fibres); germination epigeal/crypto- or phanerocotylar.
Synonymy: Hornschuchiaceae J. Agardh, Monodoraceae J. Agardh [where?]
Floral formula - Anaxagoreoideae: * K 3; C 3 + 3; A many, + severalo; G 3.
Everything Else: * K 3; C 3 + 3; A many; G 1-many.
Evolution. Divergence & Distribution. The biogeography and diversification of the family has been much studied (see also Doyle et al. 2004; Richardson et al. 2004; Su & Saunders 2009; Surveswaran et al. 2010). Erkens et al. (2012b; ?program) found little in the way of changes in diversification rates in the family, speciation behaving as if it were a random branching process, and so there was little need to invoke key innovations.
In any event, it is clear from the above dates that much diversification happened after the break-up of the continents and is Tertiary in age. Couvreur et al. (2011a) contrast the diversification in Annonoideae and Malmeoideae. The former began to diversify ca 66 m.y.a. and the latter much later, ca 33 m.y.a.; the former has about twice as many species as the latter, even if rather paradoxically the latter may have a higher diversification rate - once it got going (see Couvreur et al. 2011a; Thomas et al. 2012, older, but similar disparity: both give other ages). However, although stem age estimates of these subfamilies are in the 70 million year range, crown ages vary widely, the age of Couvreur et al. (2011a) being the youngest, and that of Piries and Doyle (2012) the oldest, a crown group estimate of (70-)66(-62) my. Su and Saunders (2009) offer dates for additional splits in the family, focusing on Pseuduvaria, and Thomas et al. (2012) and Pirie and Doyle (2012) give many dates for divergences within both main subfamilies.
The Old World Uvaria may have originated (38.4-)31.6(-25.1) m.y.a. in Africa, whence it dispersed to other parts of the Old World (Zhou et al. 2012: HPD). Indeed, Thomas et al. (2014) suggest thatc there have been around 11 dispersals from Africa to Asia, and only one from Asia to Africa; Late Palaeocene to late Miocene are the suggested times. The large New World genus Guatteria has undergone much speciation in (Amazonian) South America perhaps 8.8-4.9 m.y. before present, having moved to South America from Central America, perhaps from Africa via Europe (Erkens 2007; Erkens et al. 2007a, b, 2009).
Ecology & Physiology. Annonaceae are important lianes of the tropical South East Asian forests (Gentry 1991), and there have been several origins of this habit within Annonoideae (Meinke et al. 2011). Artabotrys, one of these lianes, has curved hooks on the ultimate branches; these are modified inflorescences. The orthotropic stems may have stout, paired and rather vicious thorns. The other lianes do not have hooks or thorns, and development of the liane habit varies.
The family is notably common in terms of both numbers of species (number three in the list) and individuals in the Amazonian tree flora, but includes only 4 of the 227 species that make up half the stems 10 cm or more d.b.h. in the forests there (ter Steege et al. 2013).
Pollination Biology & Seed Dispersal. Saunders (2010: good photographs) summarizes variation in floral morphology in the context of pollination. The flowers are protogynous (Gottsberger 1970). Flowers in which the stamens are enclosed in some sort of bowl-shaped structure are common, and there are often floral rewards on the inner surfaces of the inner perianth whorl. Pollination of the more or less odoriferous flowers is predominantly - and perhaps ancestrally - by small beetles, but there is also fly pollination (e.g. Su et al. 2008) and pollination by thrips, bees, cockroaches, etc. (Corlett 2004; Saunders 2012; Gottsberger 1970, 2012); a variety of scents is produced (Goodrich 2012 and references). The tough, apically expanded connective that predominates in stamens of Annonoideae and Malmeoideae may protect the pollen from the depradations of unwanted visitors (Gottsberger 1999, 2012; Silberbauer-Gottsberger et al. 2003). The flowers of some Annonaceae show thermogenesis (Seymour 2001), and some kind of extracarpellary compitum is common (Deroin 1991). The internal staminodes of Anaxagorea cover the gynoecium in the staminate floral phase, apparently preventing selfing (Gottsberger 2012; Saunders 2012). For pollen evolution, see Doyle et al. (2000) and especially Doyle and le Thomas (2012).
Nearly all Annonaceae have perfect flowers, and protogyny will not prevent movement of pollen from one flower to another on the same plant. However, individual plants have flowers either at the pistillate or at the staminate phase, so preventing selfing (Pang & Saunders 2014).
Dispersal of fruit is predominantly by mammals and birds. The lianes of tropical South East Asia are notably important food resouces for frugivores because they fruit more or less continually (Leighton " Leighton 1983).
Vegetative Variation. The main axes of Annonaceae are often mixed (?Troll's model), initially being orthotropic and with spirally-arranged leaves, later being more or less plagiotropic with two-ranked leaves (see also Eupomatia), while taxa such as Asimina and Annona have orthotropic axes with 2-ranked leaves (Johnson 2003). Johnson and Stull (2014) outline variation in the family, and the optimisation above is based on their work. How Meiocarpidium (Ambavioideae) grows is unknown. In general, axillary branches depart from the stem slightly to one side of the axil. Branches generally have plagiotropic leaves, and in some Xylopia, etc., the plagiotropic branch systems are frondose and very beautiful.
Genes & Genomes. For the chloroplast inversion in Miliuseae,see Arias et al. (2014); for probable intergeneric hybridization between Dasymaschalon and Friesodielsia, see Guo et al. (2014).
Chemistry, Morphology, etc. Protoberberidine alkaloids are reported from Annonaceae (Wink 2008). Cork in the roots of Goniothalamus may be superficial (Blunden & Kyi 1974). The wood occasionally fluoresces. Terminal tracheids are fairly commonly silicified (Piperno 2006). For the petiolar anatomy of Anaxagorea, see Jovet-Ast (1942) and Maas and Westra (1984); it is unlikely that there are annular petiolar bundles, although the midrib anatomy can be complex. Tetrameranthus sometimes seems to have opposite leaves; according to George Schatz (pers. comm.) it lacks plagiotropic branches and all branches have spirally-arranged leaves.
The pollen tetrads can be very large and with a massive exine (Tsou & Johnson 2003 and references). There are reports that the pollen grains of both Annona and Asimina may germinate via the proximal pole (Hesse et al. 2009a), although in the former (and some other genera) individual grains of the tetrad may rotate during development (Tsou & Fu 2002, 2006; Lora et al. 2009b). Xylopia, like Anaxagorea also with follicles, has micropylar-arillate seeds (Corner 1976); other genera may also have reduced arils (Svoma 1997). Reports that the micropyle is formed by both integuments need to be confirmed (c.f. Svoma 1998b). Monodora (derived) has a rather thin outer integument, and anatomy of the seed coat of Ambavioideae with a third integument (Zwischenintegument) can be complex (Christmann 1986; see also Perisamy & Swamy 1961).
For an introduction to Annonaceae and much more besides, see the papers in Bot. J. Linnean Soc. 169(1). 2012, including Erkens et al. (2012a) for a comprehensive bibliography; see Kessler (1993) and Bakker (2000a, b) for general information. Also Hegnauer (1964, 1989: chemistry), Jovet-Ast (1942: indumentum and anatomy), Junikka and Koek-Noorman (2007: bark anatomy), Koek-Noorman and Westra (2012: wood anatomy), van Setten and Koek-Noorman (1986: leaf anatomy), Sun et al. (2008: epidermal anatomy), van der Wyck and Canright (1956: anatomy), Fries (1919: inflorescence morphology), Deroin (1991b: stigmatic surface and carpel morphology), Steinecke (1993: esp. flower and fruit), Rudall and Furness (1997: tapetum), Svoma (1998a: seeds), van Setten and Koek-Noorman (1992: fruits and seeds), Endress (2011b: ovules), Deroin (1999a: receptacular vascular system), Couvreur et al. (2008a: evolution of syncarpy, etc.), Couvreur et al. (2008b: Monodora group), Chaowasku et al. (2008: Miliusa et al.) and Doyle (2014: summary), all pollen, Lora et al. (2009: infraspecific variation in number of pollen nuclei in Annona cherimola), Corner (1949: seed anatomy), and Okada and Ueda (1984) and Morawaetz (1986, 1988), esp. cytology. For floral (developmental) morphology, see van Heusden (1992), Ronse Decraene and Smets (1990b), Leins and Erbar (1980, 1982, 1996, 2010), Xu and Ronse De Craene (2010b), Endress (1975: carpel and stamen development), and Endress and Armstrong (2011: Anaxagorea).
Phylogeny. See Doyle and le Thomas (1994, 1996) for morphological phylogenies and character evolution, and for a molecular phylogeny of Anaxagorea that is integrated with morphological variation, see Scharaschkin and Doyle (2005, 2006). The position of Unonopsis on the tree has been somewhat erratic, perhaps because of ancient paralogy (Pirie et al. 2007).
For relationships in Ambavioideae, see Surveswaran et al. (2010); the basic phylogenetic structure seems to be [Meiocarpidium [Tetrameranthus et al. + Cananga et al.]].
Two major clades make up the rest of the family (see also Richardson 2004). Malmeoideae include a polyphyletic Polyalthia (Richardson et al. (2004). This clade is not very speciose, mostly lacking large genera aside from Polyalthia, and has relatively little internal molecular divergence (hence its early name, the short-branch clade: Mols et al. 2008a; Xue et al. 2011). New World members of this clade form a monophyletic group (Pirie et al. 2006). For Pseuduvaria, see Su and Saunders (2006) and Su et al. (2008, 2010), while for the relationships and dimemberment of Polyalthia, see Xue et al. (2011, 2012). Mols et al. (2008b) explore character evolution within Malmeoideae, while Chaowasku et al. (2014) clarify relationships within the large clade that makes up Miliuseae, although support for the branches along the spine was still somewhat ambigous, and they optimised the disributions of a number of characters on their tree. Annonoideae include the inaperturate pollen clade; here there is more molecular divergence (hence its name, the long branch clade: see also J. A. Doyle et al. 2004; Pirie et al. 2005). Uvaria is polyphyletic (Mols et al. 2004), and Zhou et al. (2009a, esp. b, 2010) suggested that its limits be extended; geography and phylogeny correlate quite well. The limits of genera like Dasymaschalon and Friesodielsia are also unclear (Wang et al. 2012: indepdendent loss and subsequent parallel evolution in taxa that have lost their inner petals). )For Guatteria, see Erkens (2007) and Erkens et al. (2007a, b).
Classification. The classification outlined by Chatrou et al. (2012) is followed here, although they also recognize tribes; their principles of classification are clearly explained. The limits of genera and hence the numbers of their included species in Annonoideae seem particularly uncertain. Zhou et al. (2010) clarify the limits of Uvaria, Xue et al. (2011, 2012) those of Polyalthia, while Surveswaran et al. (2010) discuss generic limits in the ambavioid clade. For a checklist of the New World species of the genus, see Maas et al. (2011); Annonbase should also be consulted.