EMBRYOPSIDA Pirani & Prado (crown group)
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; 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, 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 multilaminate]; spores trilete [?level]; 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 embryophytes.
Abscisic acid, ?D-methionine +; sporangium with columella; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; 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 in the gametophyte; sporophyte long-lived, chlorophyllous, nutritionally largely independent of the gametophyte; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour; spores trilete.
Sporophyte well developed, branched, free living, sporangia several; apical meristem +.
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Photosynthetic red light response, passive control of leaf hydration; (condensed or nonhydrolyzable tannins/proanthocyanidins +); vascular tissue +, sieve cells +, tracheids +, in both protoxylem and metaxylem; endodermis +; root xylem exarch [development centripetal]; stem with an apical cell; leaf blade with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, lacking columella, eusporangiate [sporangia derived from periclinal divisions of several epidermal cells, wall multilayered]; stellate pattern split between doublet and triplet regions of transition zone; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, embryo with roots arising lateral to the main axis [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Branching ± monopodial; lateral roots +, endogenous, root cap +; tracheids with scalariform-bordered pits; leaves spirally arranged, 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, root apex multicellular; endodermis +; shoot apical meristem multicellular; lateral meristems +, 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, spiral, 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; 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, embryo axis straight, so 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, secondary veins pinnate, overall growth ± diffuse, venation hierarchical-reticulate, 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 binucleate at dispersal, mature male gametophyte trinucleate, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate 20-20,000 µm/hour, outer wall pectic, inner wall callose, 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 [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], 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.]; (vessels 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]]]: plant woody; (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 developing internally/adaxially to the corolla whorl and successively 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.]]]: nodes 3:3; 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 I / FABIDAE / [ZYGOPHYLLALES [the COM clade + the nitrogen-fixing clade]]: endosperm scanty.
[the COM clade + the nitrogen-fixing clade]: ?
[FABALES [ROSALES [CUCURBITALES + FAGALES]]] / the nitrogen-fixing clade: (N-fixing by associated root-dwelling bacteria); tension wood +; seed exotestal.
[ROSALES [CUCURBITALES + FAGALES]]: ovules 1-2/carpel, apical.
[CUCURBITALES + FAGALES]: ovary inferior; ovules 2/carpel; fruit 1-seeded, indehiscent.
FAGALES Engler Main Tree.
Plant ectomycorrhizal; (Frankia infection +, by root hairs); (flavonols), dihydroflavonols, ellagic acid +; (cork cambium outer cortical); vessel elements also with scalariform perforation plates; sieve tubes with non-dispersive P-protein bodies; buds perulate; lamina margins toothed, secondary veins proceeding straight to teeth, teeth not glandular, with higher-order veins convergent on them [urticoid]; plants monoecious, inflorescence with compact cymose clusters of flowers, flowers very small, (± monosymmetric by reduction), sessile; P +; nectary 0; staminate flowers: inflorescence a catkin; A opposite P; pollen oblate, thickened sexine arches going from pore to pore, visible as bands [arci], tectum ± spinulate, infratectum granular [?here], cavity between inner and outer pores [vestibulum]; carpellate flowers: style undivided, ± 0, stigma ± decurrent, linear, dry; ovules apical, pendulous, epitropous, unitegmic; megaspore mother cells several; ovules poorly developed at pollination, fertilization delayed; fruits dry; testa vascularized, not mechanical, exotesta often enlarged and persisting; cotyledons large. - 8 families, 33 genera, 1055 species.
Age. Ages for crown-group Fagales suggested by Cook and Crisp (2005) are 95-75 m.y., while Sauquet et al. (2011) give a range of dates from (124.8-)120.2-67.3(-48.9) m.y..
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. From the rich fossil record of Fagales, Friis et al. (2006a) suggested that all major fagalean lineages were present at the latest by the Cenomanian (early Late Cretaceous), ca 97 m.y.a., and fagalean leaf fossils are reported from Queensland, Australia then - at that time, Australia had barely separated from Antarctica (e.g. McLoughlin et al. 1995).
Flowers of some fossil taxa assigned here (the fossils are ca 84 m.y. old - see Herendeen et al. 1999) are substantially different from those of extant Fagales. Thus there are suggestions of nectary lobes between the stamens in the staminate and perfect flowers of Antiquacupula, the pollen has a perforate tectum, and the inner walls of the fruit loculi are glabrous; the flowers have a floral formula of P 3 + 3; A 12; G 3, the outer whorl of six stamens being opposite the tepals, the inner whorl alternating with them (Sims et al. 1998; Herendeen et al. 1999). Normanthus, from the late Cretaceous of Portugal, has perfect flowers with five perianth members that alternate with the stamens, there are two collateral carpels with separate and quite long styles, and the placentation is described as being parietal (Schönenberger et al. 2001b). If fossils like Normanthus are correctly associated with Betulaceae (see below), then floral evolution has clearly been highly homoplastic. Endressianthus has imperfect flowers, with stamens alternating with the tepals in the staminate flowers; Dahlgrenianthus has perfect flowers and a superior ovary with more or less separate styles (Friis et al. 2006a); while Archaefagacea has a tricarpellate gynoecium, two ovules per carpel and sometimes three-seeded fruits. Unnamed fossils from Massachusetts have a character combination of 3-merous flowers, 12 stamens, nectaries, inferior ovary, and single-seeded and very small fruits that may be dehiscent (Taylor et al. 2012). If they belong to stem Fagales, single-seeded fruits may have evolved before wind pollination; the very small size of the seeds/fruits (<2 mm long) is consistent with the age of the fossils, ca 75 m.y. in the Campanian (Taylor et al. 2012). Although Taylor et al. (2012) suggested that the members of the uniseriate perianth might be connate via hairs, the perianth bases are very small, in this respect being rather unlike sepals in the rosids.
Schönenberger et al. (2001b) and Friis et al. (2003a) give useful tables comparing the morphology of extant and fossil members of Fagales; see also Crepet et al. (2008), Takahashi et al. (2008a) and Taylor et al. (2012: some outgroups). For Normapolles-producing fossils, see below.
Bacterial/Fungal Associations. Fagales are the largest extant seed-plant clade in which ectomycorrhizal associations are pervasive. Some 10 clades of Agaricales, common on Fagales, are ectomycorrhizal, and their crown group origins are split almost equally between Late Cretaceous and Eocene (Ryberg & Matheny 2012); however, the relative timing of diversification of the fungi and of Fagales is unclear. In Boletales, at least, ectomycorrhizae may have evolved from brown rot fungi in the ecological context of soils low in nitrogen (and high in organic material) formed by the activities of these fungi. Dates of origin of ectomycorrhizal associations there - which happened more than once - are also late Cretaceous and younger (Eastwood et al. 2011). Some ectomycorrhizae form tuberculate structures on the roots (Smith & Pfister 2009).
Rusts on Fagales are predominantly members of Pucciniastraceae, a group also to be found on ferns (Savile 1979).
Associations with nitrogen-fixing bacteria are sporadic. One Frankia clade involved in nitrogen fixation is restricted to Fagales, although members of another clade are also to be found here (Clawson et al. 2004). For a summary of what is known about nitrogen fixation, see Santi et al. (2013).
Ecology & Physiology. Fagales are hardly particularly speciose (e.g. Magallón & Sanderson 2001), but, as with other ectomycorrhizal groups, members - especially Fagaceae - can dominate the forests in which they grow (see also Clade Asymmetries). The order is particularly well represented in forests in temperate forests and also in tropical montane regions.
Pollination Biology & Seed Dispersal. Wind pollination and monoecy pervade the order, although taxa like Lithocarpus and probably some fossil Fagaceae are pollinated by insects. Delayed fertilization, intermittent pollen tube growth (e.g. Sogo & Tobe 2005, 2006a, b, d [the last for a summary]), and chalazogamy (see e.g. Benson 1894; Nawashin 1899; Swamy 1948b and references) are also common, however, chalazogamy may not be plesiomorphic in the order. Fertilization in Nothofagaceae is unknown and both Fagaceae and Myricaceae are porogamous. Delayed fertilization, which also occurs in Fagaceae, is associated with the immaturity of the ovules at pollination and competition between the ovules and sometimes between the several embryo sacs that develop within the one ovule (see Sogo & Tobe 2005d). The immaturity of the ovules can be extreme, thus in Corylus avellana the ovules do not even begin to develop until after pollination (Germain 1994).
Fruits throughout the order are single-seeded (as is very common in wind-pollinated plants) whatever the number of ovules in the young ovary - note, however, this feature may be an apomorphy for [Fagales + Cucurbitales].
Plant-Animal Interactions. Lycaenidae caterpillars are quite commonly to be found on members of Fagales (see Fielder 1991). Phyllonorycter leaf-mining moths (Lepidoptera-Gracillariidae-Phyllocnistinae) are also especially speciose, with about half the known host records being on members of Fagales (Lopez-Vaamonde et al. 2003). Diversification of the moth clade seems to have occurred about 50.8-27.3 m.y.a., well after Fagales (see above) and the clade itself originated some 76.3-50.3 m.y.a. (Lopez-Vaamonde et al. 2006). Both Heterobathmidae (Nothofagaceae) and Eriocraniidae (Fagaceae, Betulaceae), clades rather "basal" in the lepidopteran tree, are also found on Fagales (Shields 1988).
Chemistry, Morphology, etc. Although the tepals in Fagales are small, they may have three traces, and petals with three traces are also found in some fossil taxa. Where change in infratectum structure is to be placed on the tree seems unclear when treated at the family level; either one gain, an ordinal apomorphy (see also Doyle 2009), and one reversion (Fagaceae), or two gains. However, since Fagus is also has a columellar infratectum, the former position is most reasonable; Normapolles pollen also has a granular infratectum. Carpel orientation and integument number are variable. Ovule structure is unclear in part because of the great development of megaspore mother cell tissue in some taxa and the relation of these mother cells to the cells of the mature embryo sac. Taylor et al. (2012) suggested that an ovule that is straight when young, becoming curved only later, might be a distinctive feature of the order. Germination is often both hypogeal and epigeal in the one family, but not in Casuarinaceae and Nothofagaceae.
For chemistry, see Giannasi (1986); for cork cambium initiation, see Weiss (1890); flower and inflorescence morphology, see Abbe (1974); vegetative morphology, see Hickey and Taylor (1991); pollen, see Zavada and Dilcher (1986), Feur (1991) and especially Friis et al. (2006a); embryology, Benson (1894) and Xing et al. (1998); and for fruit wall anatomy, see Soepadmo (1967b).
Phylogeny. Relationships within Fagales are becoming fairly well resolved, although the position of Myricaceae remains uncertain. Early studies include D. Soltis et al. (2000a: Rhoiptelea not included). Manos and Steele (1997) found that Myrica was sister to Betulaceae, etc., in a matK and combined matK + rbcL analysis, although support was weak (see also Sauquet et al. 2012: 67% bootstrap support), but sister to all Fagales except Nothofagaceae and Fagaceae in a rbcL analysis, the latter set of relationships also being found by Li et al. (2002: only 61% bootstrap support) using trnL-F sequence data. Cook and Crisp (2005) found the relationships [Juglandaceae [Myricaceae [Casuarinaceae + Betulaceae]]]. Li et al. (2004: six genes, all three genomes) found Myricaceae to be sister to [Juglandaceae + Rhoipteleaceae], although the support still was not strong; the tree here follows this topology. Herbert et al. (2006: three genes) find the same set of relationships, but again with little support for the position of Myricaceae; support was, however, good in the Bayesian analysis of Soltis et al. (2007a: sampling poor).
Previous Relationships. Fagales are the core of the old "Englerian" Amentiferae which have since been comprehensively demolished; a somewhat larger group, Juliflorae, included all broad-leaved angiosperms with very reduced flowers, so including Platanaceae, Lacistemaceae, Chloranthaceae, Piperaceae, etc. (e.g. Eichler 1878). Its members have since found resting places among many otherwise entirely unrelated groups within eudicots such as Malpighiales (Salicaceae), Proteales (Platanaceae), and Rosales (Ulmaceae and relatives: e.g. Qiu et al. 1998), and in or near the magnoliids (Piperaceae, Chloranthaceae). In the late nineteenth and early twentieth centuries in particular, a number of botanists thought that Amentiferae were primitive, and the chalazogamy common in the order was even thought to be intermediate between fertilization in some gymosperms and the porogamy of most angiosperms (e.g. Nawaschin 1895). Hamamelid taxa such as Altingiaceae and Hamamelidaceae were thought to be intermediate between Amentiferae and more conventional broad-leaved angiosperms, but they, too, are not related to Fagales (see Saxifragales here).
Fagales comprise the Faganae and two and a half more superorders in Takhtajan (1997).
Includes Betulaceae, Casuarinaceae, Fagaceae, Juglandaceae, Myricaceae, Nothofagaceae, Rhoipteleaceae, Ticodendraceae.
Synonymy: Juglandineae Thorne & Reveal, Myricineae Thorne & Reveal - Betulales Martius, Carpinales Döll, Casuarinales Berchtold & J. Presl, Corylales Dumortier, Juglandales Berchtold & J. Presl, Myricales Martius, Nothofagales Doweld, Quercales Burnett, Rhoipteleales Reveal
NOTHOFAGACEAE Kuprianova Back to Fagales
Chemistry?; sclereid nests?; peltate glandular hairs +; perulae decussate; leaves two-ranked (spiral), lamina vernation various, (punctate), margins also entire, stipules usu. peltate, enclosing colleters; P uniseriate; staminate flowers: P connate; A 10-15(-many), basifixed, connective usu. produced; pollen 3-10 equatorially colpate, aperture margins raised, surface warty-granular; carpellate flowers: 1-3 together; (staminodes +); G [2-3], median member abaxial; ovule with integument 4-7 cells across, parietal tissue ?1-2 cells across, nucellar cap 0, supra-chalazal tissue massive, postament +, flat-topped, large; megaspore mother cells?; fertilization?; cupule 2-(3-)4-valved, lamellate (0), fruits (1) 3(-7), lenticular (central) or triangular, wall with transversely elongated sclereids in middle; testa?; endosperm nuclear, cotyledons folded; n = 13.
1/35. New Guinea to South America (map: from Good 1974, slightly modified; green, Cretaceous to Mid-Tertiary fossils [also in Australia, New Zealand and South America where the genus is currently found], from Dettmann et al. 1990). [Photo - Branch.]
Age. Cook and Crisp (2005) estimated the age of crown group Nothofagaceae at only (66-)58-ca. 43(-ca 35[?-21]) m.y., i.e., after the first fossil records (see below), while Heads (2006), accepting the identity of those fossils, saw an age of around 72 m.y. at least, the massings of species seen today relecting ancestral massings. Sauquet et al. (2012) used a variety of calibrations and obtained ages ranged from (113.6-)100.3-23.5(-13.3) m.y..
Fossils identified as belonging to all four subgenera are known from the Late Campanian 73-71 m.y.a. in Antarctica (Dettmann et al. 1990; Swenson et al. 2001), and Nothofagus-like pollen (Nothofagites) characterized southern temperate Gondwanan areas during the later Cretaceous (Nichols & Johnson 2008). Given such dates, the pollen types must have evolved in parallel (Cook & Crisp 2005) or have been misinterpreted - or some molecular estimates of the crown-group age are incorrect.
Evolution. Divergence & Distribution. The biogeography of Nothofagus has been much discussed - is the current distribution caused by continental drift (Heads 2006: global vicariance, Nothofagaceae the southern representatives of Fagales then distributed world-wide), or is dispersal involved (e.g. Swenson et al. 2001; in particular Sauquet et al. 2011)? Knapp et al. (2005) and Cook and Crisp (2005) suggested that Nothofagus reached New Zealand, at least, by long distance dispersal only ca 30 m.y.a., Brassospora-type plants having since become extinct there (see also Pole 2003; Waters & Craw 2006; Wallis & Trewick 2009). There are also reports of Tertiary Nothofagus pollen from the Gulf Coast of the USA as well as in the Pacific North West, which further complicate the issue (Elsik 1974). The general pattern of diversification in the family is the "broom and handle" type (Cook & Crisp 2005); either persistence of a lineage, or diversification followed by near-extinction and then diversification again.
Three pollen types occur together in an Oligocene locality in Tasmania and the fourth was found nearby (Hill 2001 and references), yet the distribution of Nothofagus currently spans latitudes from almost 0-50+o S.. So either the climatic preferences of the clades have changed, or there was a very distinctive climate in Tasmania then, or... (Hill & Brodribb 2006). Perhaps this is a late example of the intermingling of taxa with now very different climatic preferences in equable early Tertiary (normally Palaeocene-Eocene) climates.
For characters and clades, see Heenan and Smissen (2013).
Bacterial/Fungal Associations. Humphries et al. (1986: c.f. more recent ideas of relationships) discuss the parasites and associates of Nothofagus, and suggest the possibility of some co-evolution of the genus with Eriococcus scale insects that grow on it. The inaperturate discomycete Cyttaria grows on Nothofagus in both the Antipodes and South America, but neither in New Guinea nor in New Caledonia. Only subgenera Fuscospora and Lophozonia are affected, and the pattern of association of host and parasite is not simple; the split between Australian and New Zealand species of Cyttaria is estimated at ca 44.6-28.5 m.y. (K. Peterson et al. 2010), overlapping with Crisp and Cook's estimates above. The rust parasites of Nothofagaceae are rather different to those on other Fagales (Savile 1979).
Plant-Animal Interactions. The moth Heterobathmia, a genus perhaps 125 m.y. old and part of a clade (Micropterigidae) sister to all other Lepidoptera, makes its home exclusively on Nothofagus, both as an adult (it has jaws, and eats pollen) and as a caterpillar (see also Futuyma & Mitter 1996).
Chemistry, Morphology, etc. Nothofagus obliqua may have unilacunar nodes; does it have stipules?
Unlike Fagaceae, there is no obvious relationship between the number of fruits and the number of valves of the cupule. The central flower of the cupule often has two carpels, lateral flowers have three. Male flowers that apparently have many stamens are interpreted as being the result of the fusion of separate flowers of a dichasium (see also Betulaceae). Embryology is poorly known.
Further information may be found in Hill and Jordan (1993) and Kubitzki (1993b), both general, Hegnauer (1989, as Fagaceae: chemistry), Lersten and Horner (2008b: leaf crystals, etc., Fagaceae are similar), Philipson and Philipson (1979: leaf vernation), Rozefelds (1998) and Rozefelds and Drinnan (1998: stamens and staminate flowers), and Poole (1952: seed).
Phylogeny. Manos (1997), Knapp et al. (2005 and references) and Heenan and Smissen (2013) discuss relationships within the genus.
Classification. For sections, see Philipson and Philipson (1988), and for a checklist and bibliography, see Govaerts and Frodin (1998: in Fagaceae).
Previous Pelationships. Nothofagus has often been included in Fagaceae, as by Cronquist (1981) and Kubitzki (1993b).
[Fagaceae [Myricaceae [Juglandaceae + Rhoipteleaceae]] [Casuarinaceae [Ticodendraceae + Betulaceae]]]: bud scales spiral; leaves spiral; anthers dorsifixed.
Age. Estimates of the age of this node are (65-)61(-57) m.y.a. (Wikström et al. (2001) and (93-)90, 88(-84) m.y. old (Hengcheng Wang et al. 2009: Bayesian relaxed clock estimates up to 100 m.y.). Magallón and Castillo (2009) estimated an age of ca 93.5 m.y., Bell et al. (2010) ages of (68-)55, 55(-40) m.y., and Sauquet et al. (2011) an age of around 110.3 m.y..
Evolution. Plant-Animal Interactions. Larvae of Eriocranidae, a small group of near-basal lepidoptera, are found as leaf miners on this clade (Powell et al. 1998).
FAGACEAE Dumortier, nom. cons. Back to Fagales
Hairs often stellate/branched; sclereid nests in bark, cells with large rhomboidal crystals; veins often associated with crystals only; leaves (two-ranked, whorled), lamina vernation conduplicate-plicate, (margins entire; lobed; biserrate); inflorescence branched or not; flowers often trimerous; P biseriate [thus = T] or not, 4-6 (7)-lobed; staminate flowers: bract; A (4-)12(-20) (connective produced); pollen prolate-spheroidal, not spiny, tectum with ± flat-lying and fused rod-like elements [(micro)rugulate]; pistillode +; carpellate flowers: staminodes +; G [(2-)3-6(-15)], alternating with P, or median member abaxial; ovules (uni)bitegmic, "inner and outer integuments several cells thick", parietal tissue 4-5 cells across, supra-chalazal tissue massive; embryo sac with chalazal caecum; cupule of valves [one more than fruit number], ± spiny; fruit nut-like, trigonous, wall with lignified tissue on the outside, endocarp hairy inside; seed pachychalazal; (endosperm cellular); n = 12 (13, 21).
7[list]/670 - 2 subfamilies below. More or less worldwide (map: from Soepadmo 1972; Fl. N. Am. III. 1997).
Age. Estimates for the crown age of the family are 37-34 m.y.a. (Wikström et al. 2001), 77-67 m.y. (Cook & Crisp 2005), (45-)31, 28(-16) m.y.a. (Bell et al. 2010), or around 84.7 m.y. (Sauquet et al. 2012). However, the oldest Fagaceae fossils are some 90 m.y. old (Crepet et al. 2004 for references).
1. Fagoideae K. Koch
Ellagic acid 0; stomata also cyclocytic; staminate flowers: male inflorescence capitate; pollen exine fine scabrate; carpellate flowers: stigma capitate; ovule ?straight ["unanatropous"], micropyle bistomal, elongate, inner integument thinner than outer, nucellar cap ca 13 cells across; pollen tube at ovule at dormancy; cotyledons folded; germination epigeal.
1/10. Temperate N. hemisphere. [Photo - Fruiting Branch, © M. Brand.]
2. Quercoideae Õrsted
Inflorescence spike or catkin, staminate and carpellate flowers on separate inflorescences or not; staminate flowers: pollen exine also (micro)verrucate or smooth, infratectum granular, (pistillode secreting nectar); carpellate flowers: (style relatively long, occupying most of the gynoecium), stigmas capitate, decurrent, or punctiform and with a terminal pore; ovule with integuments the same length [micropyle endostomal?], parietal tissue one cell across, nucellar cap ca 2 cells across, (tracheids +); pollen tubes branched, in style at dormancy; cupule also cup-shaped, with scales; fruit also rounded, (endocarp glabrous inside - some subgenus Quercus); (endosperm with basi-lateral caecum); germination hypogeal or epigeal; rpl22 gene transferred from chloroplast to nucleus.
6/640: Quercus (400), Lithocarpus (120), Castanopsis (110). N. temperate, at higher elevations in the tropics, not S. Africa or New Zealand, barely in Australia. [Photo - Fruit]
Age. Estimates of the crown-group age of Quercoideae are around 55.2 m.y. (Sauquet et al. 2012).
Synonymy: Castaneaceae Brenner, Quercaceae Martinov
Evolution. Divergence & Distribution. The diversity of the family in the earlier Tertiary was considerable (Denk et al. 2012).
For character evolution and the biogeography of Fagaceae, see e.g. Manos and Stanford (2001) and Manos et al. (2002). Oh and Manos (2006, 2008) suggest that the apparently unitary scaly or spiny cup-shaped cupule that encloses a single, rounded fruit, the acorn, has evolved more than once within Quercoideae, while Cannon and Manos (2001) discussed the evolution of the fruits of a few species of Malesian Lithocarpus in which the receptacle almost entirely surrounds the seed and the smooth, shiny wall of an ordinary acorn is highly reduced.
Ecology & Physiology. Members of Fagaceae are often very common in north temperate areas, but also on hills and mountains in Central America and Malesia, and frequently dominate the vegetation. White oak (Quercus alba) alone represents (12-)19-26(-49)% of witness trees, i.e. trees that were probably present before Europeans arrived, in the oak-dominated forests of eastern North America (81% in some southern Illinois forests). White oak, with up to three more ectomycorrhizal species, two of which are usually other Fagaceae, are anything from (36-)50-80(-± 100)% of all trees (Abrams 2003). Six of the 30 species of Quercus growing in those forests are notable dominants (Abrams 1996). Many of these oaks like high light and quite dry conditions, and fires are quite common there; oak can replace pine in such situations (Adams 1992). Fagaceae, mostly Quercus are abundant in western North America, and in California the black oak, Quercus kelloggii, is particularly widespread and has the greatest timber volume of any oak (Waddell & Barrett 2005).
The American chestnut, Castanea dentata, previously the dominant large tree in some 800,000 km2 of forest in eastern North America and an important source of food for humans and other animals, now persists largely as suckers after its devastation by chestnut blight in the first half of last century (Thompson 2012: see below). Much of the chestnut forest has since been replaced by mixed oak or oak-hickory forests (Abrams 1996; see e.g. van der Gevel et al. 2012 for the future), so the forests remain dominated by ectomycorrhizal trees.
Pollination Biology & Seed Dispersal. Quercoideae such as Castanea and Castanopsis are insect pollinated.
Fertilization is porogamous, according to Johri et al. (1992), although it is much delayed (Sogo & Tobe 2006d and references; Deng et al. 2008). Red oaks (section Lobatae) take one and a half years to mature their fruits and the seeds are high in tannins and lipids; the fruits of white oaks (section Quercus) mature in about six months and their seeds are less rich in tannins and lipids, furthermore, their seeds tend to germinate faster. Much has been written about the behavior of animals that currently eat and disperse the acorns of these species. Thus squirrels tend to eat the embryos of white oaks before caching the fruits; in general they prefer to eat acorns of white oaks in the fall and to cache those of red oaks (Wood 2005 for literature).
Fagaceae may dominate the forests where they grow, and they can produce huge numbers of fruits, if somewhat erratically - the phenomenon of masting. When their abundance is combined with masting, the effect on the animals that eat these fruits is considerable, and, as with the mast-fruiting dipterocarps, some of the seed predators like Passenger Pigeons in eastern North America and wild pigs in Europe are (or were) migratory. The demise of the Passenger Pigeon (Ectopistes migratorius), which once made up 25-40% of the total avian biomass in North America, may have been hastened in part by the destruction of its food sources as settlers cleared woodlands for agriculture. Fagaceae - oaks, beech, chestnut - were a major element in its diet (Curran & Leighton 2000 and references).
Plant-Animal Interactions. Oaks support the highest diversity of herbivores of all temperate holarctic forest trees. Pearse and Hipp (2012) found that leaf defences in Quercus were highest at lower latitudes (little temperature fluctuation, mild winters, low minimum precipitation).
Theclines (Lycaenini) caterpillars are common on this family (Ehrlich & Raven 1964).
By some estimates half of all galls in the north temperate region are found on Fagaceae, especially on oaks - and perhaps especially in North America, where Quercus is particularly diverse (Mani 1964; Abrahamson et al. 1998). Gall wasps (Cynipini) are very nearly all to be found on oaks, and their galls have different morphologies depending on whether they are produced by sexual or agamic individuals; the overall morphological diversity of oak galls is remarkable (Redfern 2011). The some 1,000 species of gall wasps are perhaps two thirds of the known species in the whole Cynipidae (Csóka et al. 2005; Stone et al. 2009). Host plant conservatism here has persisted over the last ca 20 m.y. at least, and major clades of gall wasps usually have associations with major clades of oaks (Stone et al. 2009).
Bacterial/Fungal Associations. Chestnut Castanea dentata forests were utterly devastated by the introduced ascomycete fungus Cryphonectria parasitica (Endothia parasitica) over a period of less than forty years, 1900-1940 (Thompson 2012). Although chestnut plants can persist in the understorey for many years after initial infection because they sucker from collars of the dead old trees or from stumps, the suckers practically never reach reproductive age before being reinfected by the fungus (Schlarbaum et al. 1997).
Genes & Genomes. A mitochondrial gene has moved from the parasite Mitrastemon (Ericales) to its host, Quercus (Systma et al. 2009).
Chemistry, Morphology, etc. Syllepsis is very uncommon in the family (Keller 1994).
There has been much discussion over the morphological nature of the small protrusions surrounding the ovary, and the whole complex is often interpreted as a modified cymose inflorescence (e.g. Sims et al. 1998; Manos et al. 2001a; Pigg et al. 2001; Oh & Manos 2008 for references). When the cupule has valves, probably the plesiomorphic condition, there is one valve more than the number of fruits; the valves representing modified cymose part inflorescences (Fey & Endress 1983).
Denk and Grimm (2009) describe pollen morphology, focusing on Quercus; I use their terms. For the orientation of the carpels, see Endress (1977a) who show the median member of outer T whorl in both staminate and carpellate flowers as being abaxial (c.f. Sims et al. 1998). Variation in ovule and fruit is extensive, and is conveniently tabulated by Deng et al. (2008); the polarity of some of this variation is unclear. Hjelmqvist (1953) discussed the basi-lateral embryo sac/endosperm caecum he noted in some Quercoideae. For intergeneric and intersubfamilial graft hybrids, see Herrmann (1951).
See also Hegnauer (1966, 1989: general chemistry), Loreto et al. (2009: monoterpenes, isoprenoids in Quercus), Huang et al. (2011: ellagitannins with triterpene alcohol cores), Axelrod (1983: distributional history), Nixon (1989), Kubitzki (1993b: general), Lersten and Horner (2008b: leaf crystals, etc.; similar to Nothofagaceae) and Liu et al. (2009: stomata, hairs) for information.
Phylogeny. Fagus is sister to all other Fagaceae (Manos et al. 1993; Sauquet et al. 2012); Quercoideae s. str. are paraphyletic, Trigonobalanus being sister to the rest of the clade. For phylogeny see also Manos and Stanford (2001) and Manos et al. (2002). Li (1996) did not find Fagaceae to be monophyletic in his morphological analysis.
Trigonobalanus was long known from Fraser's Hill in Peninsula Malaya, described only some 40 years ago from Mt Kinabalu in Borneo, then found in South America 20 years ago, then fossil in North America... The three extant species have been placed in three genera, but they form a single clade (Nixon & Crepet 1989 for information).
Oh and Manos (2006, 2008) suggest that Lithocarpus, which has fruits like those of Quercus, is polyphyletic, the South East Asian members grouping with Chrysolepis. Indeed, the single species from the Californian floristic province of West North America, L. densiflorus (now = Notholithocarpus), is in a clade with Quercus, Castanopsis, and Castanea. Quercus contains both species with fast-maturing (a few months) acorns and a pericarp that is glabrous inside - both derived characters - and species in which the acorns take 1 1/2 years to develop and the endocarp is hairy inside. For phylogenetic relationships within Quercus, see Manos et al. (1999) and Oh and Manos (2008); New and Old World species are in separate clades. However, detailed relationships may be difficult to disentangle if the various positions that different accessions of species like Q. ilex, Q. suber and Q. robur appear on the one tree is any indication (Simeone et al. 2013).
Classification. Govaerts and Frodin (1998) provide a checklist and bibliography for the family.
[[Myricaceae [Juglandaceae + Rhoipteleaceae]] [Casuarinaceae [Ticodendraceae + Betulaceae]]] / the Normapolles group: myricetin +; pollen pororate, exine of two layers separated by an alveolar zone and obviously expanded around the apertures; G ; ovule 1/flower; fertilization chalazogamous.
Age. This node has been dated to 47-46 m.y. (Wikström et al. 2001) and (50-)41, 37(-28) m.y. (Bell et al. 2010).
Evolution. Divergence & Distribution. The pollen of Betulaceae, Rhoipteleaceae and Juglandaceae, and to a lesser extent that of Fagaceae, is rather like that of the fossil Normapolles type; see Christopher (1979) and Batten (1980) for the classification of these grains, also papers in Rev. Palaeobot. Palynol. 35(2-3). 1981. Batten (1989; see also Clarke et al. 2011) in particular was cautious about the organismal connections of these grains, not all of which may have come from members of Fagales, and the grains did not always seem to be of wind-pollinated plants (Batten 1981). As he observed, "In due course it may be reasonable to refine the Normapolles as a distinct pre-juglandalean/myricalean order for plants which produced pollen grains of the Trudipollis-Oculipollis type and morphologically comparable forms" (Batten 1989: p. 19), and he even thought that Betulaceae, for instance, might not have Normapolles-producing ancestors. The grains have also been compared with those of Urticaceae and relatives and Proteaceae (Batten 1981). Odd character combinations in pollen of late Campanian/early Maastrichtian age ca 70.6 m.y.a. has been explained as the result of reticulate evolution (hybridization) (Hofmann et al. 2011).
Indeed, some fossil flowers producing pollen of the Normapolles type are perfect, rarely imperfect (the latter in Bedellia, Sims et al. 1999; ?Betulaceae), and with a simple, undifferentiated perianth. There is much variation, Bedellia having two five-parted whorls and Caryanthus two three-parted whorls (Sims et al. 1999: Table 2). As with other fossil Fagales (see above), relating these fossils to extant families is a challenge.
That being said, Normapolles pollen was abundant in the Turonian-Campanian of the Cretaceous, some 94-80 m.y.a., peaking in the Coniacian-Santonian ca 88 m.y.a., and occurring in much of the Northern Hemisphere from west Siberia to east North America in particular in the area 20-45oN (Cretaceous palaeolatitude: Kedves 1989; Sims et al. 1999; Friis et al. 2003a, esp. 2006a for a summary); Aquilapollenites is found to the north. Trees that perhaps produced Normapolles pollen may have dominated open late Cretaceous (Campanian) woodland in Texas, but this needs confirmation (Lehman & Wheeler 2001).
Chemistry, Morphology, etc. Several features of wood anatomy, including the presence of chambered crystals in the axial parenchyma, are common in the group (Carlquist 2002c), although this may properly be a feature of Fagales as a whole.
Normapolles pollen is oblate in shape and triaperturate with protruding, elaborate and strongly thickened apertural regions, the apertures themselves often being formed from expansions of the granular infratectal layer (see also Feuer 1991); the result is that the pollen is more or less triangular in transverse section. The apertures have internal pores and externally short colpi or pores. The wall is usually tectate-granular, but sometimes has an atectate polar zone, the surface being almost smooth to finely spinulate to rugulate. The infratectum is granular (details from Friis et al. 2003a). Corylus avellana has spongy endexine at the pore (Weber & Ulrich 2010).
[Myricaceae [Juglandaceae + Rhoipteleaceae]]: chains of crystal-containing cells in the wood; sieve tube P-protein bodies 0; peltate glandular hairs +; stipules 0; 1 flower/bract; stigma lamellular/laciniate; ovule single [per flower], straight, erect.
Age. This node has been dated to 38-36 m.y.a. (Wikström et al. 2001) or (43-)32, 29(-11) m.y. (Bell et al. 2010), but see other dates below.
Evolution. Divergence & Distribution. The evolution of features of inflorescence and ovule is particularly difficult to understand; they could be synapomorphies of the clade as a whole (as above), or be independent apomorphies of Myricaceae and Juglandaceae-Juglandoideae. Herbert et al. (2006) discuss possible synapomorphies around here.
Chemistry, Morphology, etc. The leaf teeth in Juglandaceae, Rhoipteleaceae and Myricaceae are intermediate in "type", having a ± splayed, (non)glandular apex, and the main tooth vein is joined by branches that leave below, or one of the branches may proceed above the tooth (Hickey & Taylor 1991).
MYRICACEAE Kunth, nom. cons. Back to Fagales
Roots often with N-fixing Frankia, rootlets clustered, of limited growth [Proteoid roots]; nodes also 1:1; lamina (pinnatifid), vernation conduplicate to curved, stipules 0 or ?foliaceous, lobed [Comptonia]; plants dioecious or monoecious; P 0, 6-lobed [Canacomyrica], staminate flowers: A 1-8(-20) (opposite P); carpellate flowers: (staminodes + - Canacomyrica); G [(3)], ?superior to inferior; ovule basal, integument 3-7 cells across, (bitegmic, ?micropyle - Canacomyrica), parietal tissue 6-9 cells across, central nucellar strand of elongated cells; megaspore mother cell single; fertilization porogamous; fruit a drupe; seed ?pachychalazal, testa ± thickened, vascularized; n = 8, 12.
3[list]/57: Myrica (55). ± Cosmopolitan but scatterd, including New Caledonia but not the Antipodes (map: Hultén 1958; van Balgooy 1974; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010). [Photos - Collection.]
Age. The divergence of Comptonia and Morella is estimated at around 24.9 m.y.a. (Sauquet et al. 2012).
Evolution. Divergence & Distribution. Comptonia, now restricted to eastern North America, was widespread in the Northern Hemisphere (including Greenland) in the Tertiary, with some records dating from the Late Cretaceous; most of the records are of the distinctive foliage (Liang et al. 2010). Canacomyrica, now endemic to New Caledonia, has been reported from New Zealand (Lee et al. 2001).
Bacterial/Fungal Associations. Myricaceae are associated with nitrogen-fixing Frankia and the rootlets are clustered and of limited growth; mycorrhizae appear to be absent (Hurd & Schwintzer 1997). Carboxylate exudation may help in phosphorus acquisition (Lambers et al. 2012b).
Pollination Biology & Seed Dispersal. Although fertilization is porogamous, it is delayed as in other Fagales, the pollen tubes pausing in their growth on the nucellar surface; this method of fertilization, described as pseudoporogamy, may be derived (Sogo & Tobe 2006a, b). The flowers of plants of some species differ in sex from year to year (Jurzyk 2005 and references).
Chemistry, Morphology, etc. Bracteoles may be present or not. Although the ovary appears to be superior, as in Comptonia, it is often so highly reduced that any traces of its inferior construction would be lost, however, in Canacomyrica, from New Caledonia, staminodes are borne on top of the ovary and there is a six-lobed perianth. In some species of Myrica the ovary is invested by tissue from a meristem developing below the flower, even below the bracteoles, which are then borne on the flower. The flowers of Canacomyrica have three "bracts" (Herbert et al. 2006) - do these represent a floral bract plus two bracteoles/prophylls? Kubitzki (1993b) draws the ovule of Canacomyrica as being basal, straight, and with a much elongated integument forming an apical tube; Herbert et al. (2006) simply describe the ovules as being bitegmic.
For chemistry, see Hegnauer (1969, 1990), for the staminate flowers, see Macdonald (1978), for general information, see Kubitzki (1993b), and for wood anatomy, see Carlquist (2002c).
Synonymy: Canacomyricaceae Doweld
[Juglandaceae + Rhoipteleaceae]: leaves compound, odd-pinnate; P 4; endosperm 0; x = 16.
Age. This node is around 85.8 m.y. old (Sauquet et al. 2012).
Chemistry, Morphology, etc. For karyomorphology, see Oginuma (1999).
Classification. Including Rhoipteleaceae in Juglandaceae s.l. is optional in A.P.G. II (2003); the two were merged in A.P.G. III (2009).
JUGLANDACEAE Perleb, nom. cons. Back to Fagales
Flavones, naphthoquinones, raffinose and stachyose [phloem exudate] +; nodes also 5:5; leaves spiral, leaflets subopposite, (vernation involute or ± conduplicate [Alfaroa]), (margins entire); (inflorescence branched); (P 0-3); staminate flowers: A 2-many; pollen porate, apertures usu. elongate; pistillode +; carpellate flowers: ?staminodes; G [(3, 4)], median or transverse, median member adaxial, apically 1-locular, loculi often divided [false septae], (stigmas not decurrent), often commissural; ovule born at the top of the incomplete septum, erect, integument 6-10 cells across, (lobed), parietal tissue 3-11 cells across, nucellar cap ca 2 cells across [Juglans]; megaspore mother cells numerous; (fertilization porogamous); fruit drupaceous, nut, samaroid, or winged by persistent bracts, pericarp intrusive; seed large, pachychalazal, cotyledons much folded.
7-10[list]/50 - 2 groups below. North temperate, S. to Argentina and Malesia. [Photo - Collection.]
Age. Crown-group Juglandaceae are perhaps around 72.6 m.y. old (Sauquet et al. 2012).
The oldest fossils assignable to Juglandaceae may be some 98-83 (Budvaecarpus) or 88-73 m.y. old (Crepet et al. 2004 for references) or 78 m.y. (Manos et al. 2007, based on the age of Caryanthus).
1. Engelhardioideae Iljinskaya
Leaf parenchyma with druses [basal - none]; buds lacking scales; leaves (opposite), even-pinnate, leaflets usu. entire, (involute - Pterocarya); female flowers: inflorescence catkinate or almost cone-like; bracts 3-lobed, bracteoles 0-2, adnate to lower half of ovary; (stigma carinal); nuts with a layer of fibrous cells.
3-4/14. Himalayas to Malesia, Mexico to Colombia (map: see Meusel et al. 1965; Manchester 1987).
Age. The crown-group age of this clade is around 36.2 m.y. (Sauquet et al. 2012); estimates in (Manos et al. (2007) are around 44 m.y..
Synonymy: Engelhardiaceae Reveal & Doweld, Platycaryaceae Doweld
2. Juglandoideae Eaton
Vessel elements with simple perforation plates alone; (pith chambered); staminate flowers: bracts 1-lobed; pollen usu. at least 26 µm [17-26 µm is the plesiomorphic condition] (with 4 or more pores); carpellate flowers: bracts unlobed, bracteoles usually lateral and adnate to the ovary; nuts with sclereids in shell, (endocarp with lacunae; outer part of fruit dehiscing [Carya]); (n = 15).
5/35. Temperate N. hemisphere, only 1 sp. in Europe, Central America and Andes (map: see Meusel et al. 1965; Manchester 1987).
Age. Crown-group Juglandoideae have been dated to around 65 m.y.a. (Sauquet et al. 2012), while Manos et al. (2007) gave a range of estimates between about 52 to ca 67 m.y.. On the other hand, Bell et al. (2010) suggested that Carya and Juglans (on the two branches of this clade) diverged only (8-)4(-1) m.y.a. and Wikström et al. (2001) suggested an age of 7-6 m.y.a..
Evolution. Divergence & Distribution. Details of timing of diversification in the family are unclear, with great variation in the estimates given for Juglandoideae in particular (Manos et al. 2007).
Several extant genera found as fossils in North America and especially Europe do not grow there now (Manchester 1987); for the early Tertiary fossil history of what are now East Asian endemics, see Manchester et al. (2009). A number of extinct genera, some showing very interesting combinations of characters, are known from early Tertiary deposits in North America, and the family was very diverse there (Manchester 1991; Elliott et al. 2006). Manos et al. (2007) integrate several fossils with molecular data.
Pollination Biology & Seed Dispersal. A form of heterodichogamy is known from Juglandaceae (Renner 2001 for references). Platycarya (Engelhardioideae) is distinctive in having sticky pollen and strongly scented flowers, which suggests insect pollination (Li et al. 2005 and references).
Taxa with biotic dispersal of their seeds may have evolved in the early Tertiary from wind-dispersed taxa (Tiffney 1986).
Chemistry, Morphology, etc. Triads of flowers are found as abnormalities (Manning 1940). Perfect flowers are known from Platycarya, although normally the cone-like inflorescences have male and female flowers together and the bracts are not part of the fruit (Li et al. 2005). Genera with opposite leaves (Alfaroa, Oreomunnea) have spiral leaves in seedlings. The stigma may be commissural or not and the orientation of the carpels varies (Manos & Stone 2001 for a summary). Pororate pollen in Juglandaceae is unlike that in other Fagales (Feuer 1991).
For chemistry, see Hegnauer (1966, 1989), for general information, see Stone (1993), and for fertilization, see Luza and Polito (1991 and references).
Phylogeny. For relationships in the family, see Gunter et al. (1994) and especially Manos and Stone (2001); Engelhardia may be paraphyletic. Platycarya linked with Juglandoideae in the analysis of Sauquet et al. (2012), but its position there was not clear; it was sister to the rest of the subfamily in Manos et al. (2008). Engelhardia is sister to the rest of Engelhardoideae in Manos et al. (2007).
Classification. Manos and Stone (2001) provide a revised classification of the family; adjustments to current generic limits are needed.
RHOIPTELEACEAE Handel-Mazzetti, nom. cons. Back to Fagales
Chemistry?; cork?; sieve tube protein bodies?; buds not perulate; leaves two-ranked, stipules asymmetrically caudate; inflorescence branched, flowers in triads; staminate flowers: A 6; pollen 3-colporate [ectoapertures elliptic, not round], exine folded [plicate], vestibulum 0; carpellate flowers: inflorescence catkinate; G, median, axaial fertile, stigmas flattened, commissural, recurved; ovule campylotropous, bitegmic, micropyle?; fertilization unknown; fruit a samaroid nut; P persistent; testa?.
1[list]/1: Rhoiptelea chiliantha. China, northern Vietnam, but fossil pollen from E. North America (map: from Fu 1992).
Chemistry, Morphology, etc. The ovary of Rhoiptelea is presumably secondarily superior.
For chemistry, see Hegnauer (1990), for pollen, see Friis et al. (2006a), for the breeding system, Sun et al. (2006), and for general information, see Wu and Kubitzki (1993).
Casuarinaceae [Ticodendraceae + Betulaceae]: dihydroflavonols +[?]; pollen tubes branched; stigmas elongate.
Age. This node has been dated to 36-35 m.y.a. (Wikström et al. 2001), 81-71 m.y. or less m.y. (Cook & Crisp 2005), (36-)29, 27(-18) m.y.a. (Bell et al. 2010) and ca 87.2 m.y. (Sauquet et al. 2012).
The age in Cook and Crisp (2005) was driven in part by the assignment of the fossil Endressianthus, ca 71 m.y.o., to the stem of this clade.
Evolution. Pollination Biology & Seed Dispersal. Sogo and Tobe (2008) suggest that the chalazogamous fertlization that occurs in all families of this clade is similar down to the details of where the pollen tube growth is temporarily delayed. The branching of pollen tubes may occur when they have "lost their way" (Sogo & Tobe 2008: p. 624).
CASUARINACEAE R. Brown, nom. cons. Back to Fagales
Roots with N-fixing Frankia, rootlets clustered, of limited growth [Proteoid roots]; flavonols, biflavonoids +, flavones, myricetin 0; nodes 1:1; banded apotracheal parenchyma +; broad compound rays + (0); stomata usu. tetracytic [hidden], transversely oriented [?sampling]; leaves 4-16-whorled, scale-like, margins entire, stipules 0; plant monoecious or dioecious, inflorescences capitate-spicate, one flower/bract, bracts and bracteoles ± well-developed; staminate flowers: P 2 ["inner bracteoles"], median; A 1, filaments incurved in bud, anthers ± longer than connective; pollen granular layer 0; pistillode 0; carpellate flowers: bracteoles large; P 0; staminodes 0; G with abaxial member only fertile, stigma wet; ovules bitegmic, micropyle endostomal, outer integument 3-4 cells across, inner integument 2-3 cells across, parietal tissue 5-7 cells across, supra-chalazal tissue massive, tracheids +, vascular bundle branched in chalaza; megaspore mother cells numerous, embryo sacs several, with chalazal caecum (reaching the funicle); fruit a samara, freed as the much accrescent bracteoles separate; seed coat adnate to pericarp; endosperm 0; n = 8[Gymnostoma]-14.
4[list]/95. South East Asia and Malesia to the S.W. Pacific, esp. Australia (map: from Coetzee & Muller 1984; Fl. Austral. 3. 1989; fossils blue, see references below). [Photo - Collection.]
Evolution. Divergence & Distribution. Casuarinaceae fossils are known from Tertiary deposits in South Africa, the Ninety East Ridge in the Indian Ocean, and Argentina (Coetzee & Muller 1984; Hill & Brodribb 2001); material from the Eocene of Patagonia has been placed in Gymnostoma (Zamaloa et al. 2006). Casuarinaceae were especially prominent in the lower Middle Miocene of New Zealand (Lee et al. 2001; Pole 2003).
Some diversification in Allocasuarina may be associated with the aridification of the Nullarbor Plain some 14-13 m.y.a. that separated eastern and western clades (Crisp & Cook 2007).
Ecology & Physiology. For a switch from scleromorphy (Gymnostoma) to xeromorphy, perhaps some time in the Miocene, see Hill and Brodribb (2001).
Bacterial/Fungal Associations. Nitrogen-fixing is known from the family, and Casuarina plays an important role in agriculture in parts of montane New Guinea, both in providing firewood and in fixing nitrogen for the sweet potato crop. Cluster roots are common (see Subbarao & Rodríguez-Barranco 1995 for microbial associates, etc.). In New Caledonian Gymnostoma, at least, there are also root nodules, themselves modified roots, that are formed in association with ectomycorrhizal fungi (Duhoux et al. 2001), however, species like C. glauca may be endomycorrhizal (Duponnois et al. 2003). The Frankia strains found in Casuarinaceae live in a close to obligate association with their hosts, and have not been found in the soil outside the native range of the family (Norman et al. 2006).
Chemistry, Morphology, etc. Do flavananols occur in this family? The starch grains are distinctive (Czaja 1978). Crystals have been observed in the cuticle (Flores & Moseley 1982).
The texture of what some have called the outer and inner bracteoles of the male flowers is very different; the latter are called the perianth here, however, inflorescence development is clearly very complex (Flores & Moseley 1982). In a floral diagram, Swamy (1948b) showed the carpels as being collateral, but he talked about them as if they were superposed. The ovules are described as being orthotropous (straight) by Johnson and Wilson (1993), but they are drawn as anatropous by Treub (1891), Swamy (1948) and Flores and Moseley (1982). The nucellus of C. montana protrudes broadly between the integuments, so the ovule is naked and there is a sort of nucellar beak, but this is because of the great development of the megaspore mother cells in the lower part of the nucellus (Swamy 1948). There are no transitional leaves between the cotyledons and scale leaves, and there is a whorl of buds at the cotyledonary node.
See Rogers (1982a), Dilcher et al. (1990) and Johnson and Wilson (1993) for general information; also Moseley (1948: wood anatomy), Hegnauer (1964, 1989: chemistry), and Sogo et al. (2001: fertilization).
Phylogeny. Steane et al. (2003) provide a phylogeny of the family. Although the monophyly of Causarina s.l. has never been in doubt, it has been split into four genera, themselves probably monophyletic; Gymnostoma is sister to the rest of the family and has many plesiomorphous features. Both its carpels are fertile (although this feature is likely to be an apomorphy, given the situation in the rest of the order), with 2 ovules/carpel, its stem stomata are not hidden, and perhaps n = 8.
[Ticodendraceae + Betulaceae]: sclereid nests in bark, cells with large rhomboidal crystals; mucilage cells +; leaves two-ranked; anther thecae ± separate.
Age. The age of this node is about 302-211 m.y. (Forest et al. 2005: huge confidence intervals), around 76.7 m.y. (Sauquet et al. 2012) or about 143 or 88 m.y. (Grimm & Renner 2013).
TICODENDRACEAE Gómez-Laurito & L. D. Gómez P. Back to Fagales
Buds not perulate?; foliar hypodermal idioblasts +; hairs T-shaped, unicellular, not glandular; stipules encircling the stem; plant (polygamo-)dioecious; staminate flowers: inflorescence erect; P 0; A 8-10+, filaments = or longer than anthers; carpellate flowers: flower single; ?P minute, connate; (staminodes +); G ?tangentially arranged, with divided loculi; ovules hemitropous, integument 20-30 cells across, parietal tissue ca 6 cells across, nucellar cap 0; fruit drupaceous; exotestal cells initially radially elongated, all cells ± thick-walled and tanniniferous; endosperm development?; n = 13.
1[list]/1: Ticodendron incognitum. Central America (map: from Hammel & Burger 1991). [Photo - Fruit.]
Evolution. Divergence & Distribution. Fruits assignable to Ticodendron (Ferrigocarpus) have been found in Eocene deposits from Oregon and in the London Clay; they are up to ca 50 m.y. old (Manchester & Renner 2005; Manchester 2011).
Chemistry, Morphology, etc. The nodes are trilacunar, judging from the condition in the outer cortex. Lersten and Horner (2008c) describe hypodermal idioblasts (they also occur below the midrib); these sometimes contain druses, and the authors suggest that they may be an apomorphy for the family. Almost all the leaf teeth are vascularized directly by secondary veins, unlike Betulaceae.
The bracteoles of the carpellate flowers have groups of vascularized scales in their axils, suggesting that the carpellate inflorescence has a fundamentally cymose construction. The embryology is poorly known, but the vascularization of the integument is extremely well developed.
For information, see Kubitzki (1993b: general), Carlquist (1991a: wood), Feuer (1991: pollen), Tobe (1991: floral morphology), and Sogo and Tobe (2008: fertilization).
Classification. For a checklist and bibliography, see Govaerts and Frodin (1998).
BETULACEAE Gray, nom. cons. Back to Fagales
Trees or shrubs; flavones +; stratified phloem +; sieve tube P-protein usu. 0; lamina vernation usu. laterally or vertically conduplicate, colleters +; plant monoecious or dioecious, catkinate, (bracts peltate); P 0-6, staminate flowers: filaments ± divided), anthers longer than connective; pollen starchy; G 0; carpellate flower: inflorescence catkinate; A 0; G [(3)], collateral, septae incomplete, (short style +); ovules (1-4/carpel), collateral (superposed), lower part of integument vascularized; embryo sacs several; n = 8, 11, 14; horizontal transfer of rps11 gene; sporophytic incompatibility system present.
6[list]/145 - 2 groups below. North Temperate, to Andes and Sumatra (map: from Meusel et al. 1965; Hultén 1971). [Photo - Flower.]
Age. Crown-group Betulaceae may be around 131-115 m.y. (Forest et al. 2005: large confidence intervals), about 64 m.y. (Sauquet et al. 2012), or about 63-43 m.y. (Grimm & Renner 2013: preferred age, one estimate twice this).
The oldest fossils assignable to the family are from 94-83 m.y.a. (see Crepet et al. 2004 and Forest et al. 2005 for references); Bedellia pusilla, the plant involved, was described from east North America (Sims et al. 1999). Normanthus and Endressanthus, from the late Cretaceous of Portugal, may also be close to the root of the Betulaceae clade (Friis et al. 2005), but note that the former is described as having perfect flowers with five perianth members that alternate with the stamens and an ovary with parietal placentation (Schönenberger et al. 2001b; Friis et al. 2003a).
1. Betuloideae Arnott
No spirally-thickened vessel elements; peltate glandular hairs +; (leaves spiral - Alnus); carpellate flowers: (inflorescence cone-like - Alnus); P 0 (2); parietal tissue 1-2 cells across, nucellar cap ca 2 cells across; (megaspore mother cell 1); infructescence with woody or scaly bracts separate from fruit, nut small [<3 mm long], ± flattened, samaroid.
2/95: Betula (60). N. hemisphere, to South America; montane in tropics.
Age. The two genera diverged 25-19 m.y.a. (Wikström et al. 2001) or (28-)20, 18(-10) m.y.a. (Bell et al. 2010). Other estimates are older: 109-92 m.y. (Forest et al. 2005: large confidence intervals) or about 60-38 m.y. (Grimm & Renner 2013: preferred age, some estimates almost twice this).
2. Coryloideae J. D. Hooker
Spirally-thickened vessel elements, tracheids +; lamina vernation conduplicate-plicate [Corylus]; cymule with <3 flowers; staminate flowers: P 0; A hairy; carpellate flowers: (inflorescence 1-5-flowered, ± erect - Corylus); P +; integument ca 6 cells across, parietal tissue 4-8 cells across, nucellar cap 0-2 cells across, supra-chalazal tissue massive, (tracheids +); megaspore mother cells (1-)numerous, embryo sac with chalazal caecum; pollen tube penetrates the chalazal/lateral pole of the embryo sac; fruit with accrescent leafy bracteoles [from one or two orders of branching]; nuts large, not or little flattened.
4/50. N. Temperate, South East Asia, Central America.
Age. The crown-group age of Coryloideae is estimated at 87.5-70 m.y. (Forest et al. 2005: large confidence intervals) or about 39-22 m.y. (Grimm & Renner 2013: preferred age, other estimates quite similar).
Synonymy: Carpinaceae Vest, Corylaceae Mirbel
Evolution. Bacterial/Fungal Associations. Alnus is well known as a N-fixing plant, and may be used in land remediation. Cluster roots have been reported from the genus (Shane & Lambers 2005) and carboxylate exudation may help in phosphorus acquisition (Lambers et al. 2012). Although there are reports that Alnus may lack ectomycorrhizae (Michelsen et al. 1998), Põlme et al. (2013) reported a diverse assemblage of ECM fungi - although compared with other ectomycorrhizal plants they may not be that diverse and are rather species-specific (Walker et al. 2013). Indeed, the co-occurence of nitrogen fixation and the ectomycorrhizal habit is rather unusual (but see Fabaceae), and the fungi may help enhance phosphorus acquisition by the plant (Walker et al. 2013).
Ecology & Physiology. Betula grows with other ectomycorrhizal trees in the boreal forest, and it can also be a major component of the biomass in tundra vegetation (Chapin & Körner 1995).
Pollination Biology & Seed Dispersal. Heterodichogamy is reported from Corylus (Renner 2001 for references). In Corylus avellana in particular there may be three to five months between pollination and fertilization. Ovules start to develop about half way through this period and the developing nuts are already 7-10 mm across at the time of fertilization. If pollination does not occur, the stigma may remain receptive for up to three months (Germain 1994).
Chemistry, Morphology, etc. Alnus has a single adaxial prophyll.
Staminate flowers in Coryloideae are sometimes reported as being single (e.g. Mabberley 1997), however, as Abbe (1935) noted, there are usually three together; the staminate "flower" of Ostrya, with some 15 pairs of half stamens, is apparently pseudanthial in nature, also being derived from three flowers (Abbe 1935, 1974; Macdonald in Sattler 1973: see also Nothofagaceae). In staminate flowers of Corylus the perianth is reduced to a ridge. Betula has three carpellate flowers per bract. The orientation of stamens or carpels in the flower may change during development in Betula (Lin et al. 2010); see Endress (2008c) for the structural lability of female flowers of Carpinus betulus. The ovary of Corylus is not always obviously inferior.
See Crane (1989) and Kubitzki (1993b), both general, Endress (1967: general, comparison with Hamamelidaceae, Corylopsis is the link), Hegnauer (1964, 1989: chemistry), Horne (1914), Heller (1935) and Abbe (1935), all flowers, inflorescences, Manchester and Chen (1998), Benson et al. (1906: pollination, etc., of Carpinus); Nawaschin (1899: ditto of Corylus), and Dahl and Fredrikson (1996: fertilization) for more information.
Phylogeny. Although Li et al. (2004) suggested that Betuloideae were paraphyletic, with Alnus and Betula being successively sister to the rest of the family, Forest et al. (2005), analysing variation in ITS and the 5S spacer, recovered the two subfamilies above as monophyletic (see also Grimm & Renner 2013). The monophyly of Ostrya and Carpinus is unclear, as are many of the basic characters of Coryloideae (see Yoo & Wen 2002, 2007, 2008). See also Z.-D. Chen et al. (1999) for phylogeny and evolution.
Classification. The two subfamilies are sometimes recognised as families, as by Brummitt (1992).
For a checklist and bibliography, see Govaerts and Frodin (1998: as Corylaceae and Betulaceae).