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. Back to Main Tree(1->3),(1->4)-ß-D-glucans
Age. Bell et al. (2010: Chloranthaceae sister to [Magnoliidae + everything else], but not monocots) suggested ages for this node of (152-)140(-128) or (135-)127(-119) m.y. depending on the method used. Clarke et al. (2011: 95% credibility intervals; also other estimates) a somewhat older age of (179-)152(-133) m.y., N. Zhang et al. (2012) an age of (163-)145(-133) m.y., Xue et al. (2012) an age of ca 146.4 m.y., and Magallón et al. (2013: with temporal constraints) an age of around (180.7-)158.7-151.6(-137.7) m.y. for this clade. Some other age estimates are yet older, ranging from (200-)174(-153) m.y. (with eudicot calibration) to (210-)184(-160) m.y. (without: Smith et al. 2010). Looking at the pattern of duplication of SEPALLATA genes, Yockteng et al. (2013) dated this node to somewhere around 187-137.4 m.y..
Evolution. Divergence & Distribution. For the distribution of isoquinoline alkaloids, alternatively known as 1-benzyltetrahydroisoquinoline alkaloids, 1-btiq alkaloids, see Waterman (1999, 2007). How to optimise them on the tree is unclear. They appear to b found in Chloranthaceae, the magnoliids, and eudicots, so if there is a clade [[Chloranthaceae + magnoliids] [monocots [Ceratophyllaceae + eudicots]]], as is recognized above, they may be best optimised here.
Ecology & Physiology. Foliar primary xylem with simple perforation plates in both protoxylem and metaxylem has evolved several times within this clade (Feild & Brodribb 2013). This then allowed the miniaturization of the foliar vein reticulum through the development of veins that are narrow yet conduct well, in turn allowing dense leaf venation and all that this entails in terms of high rates of photosynthesis and evaporation, etc..
Chemistry, Morphology, etc. The betalains of core Caryophyllales have biosynthetic similarities with these alkaloids. For the orientation of cellulose fibrils in the outer epidermal walls of root elongation zone, see Kerstens and Verbelen (2002); I do not know what happens in the ANITA grade and in gymnosperms, and magnoliids and eudicots are very poorly sampled. This is perhaps the best place to put triploid endosperm on the tree; the other would be as a synapomorphy for all angiosperms, but in that case it would subsequently be lost twice, or lost once and then regained.
Phylogeny. Relationships between the lineages immediately above the basal pectinations in the main tree, the ANITA grade (Amborellales, Nymphaeales and Austrobaileyales here), are being clarified, although some are still a little uncertain. The topology of the main tree in this area thus differs somewhat from that in A.P.G. II (2003). For further information, see especially the discussion immediately preceding the Magnoliales, i.e. the magnoliid clade, eudicots, and monocots are the other clades involved.
[CHLORANTHALES [[MAGNOLIALES + LAURALES] [CANELLALES + PIPERALES]]]: sesquiterpenes +; seed endotestal.
Age. Moore et al. (2010: 95% highest posterior density) estimate an age of (141-)136(-129) m.y. for this node and Xue et al. (2012) an age of ca 143.2 m.y.. Clarke et al. (2011: 95% credibility intervals) suggested a somewhat older age of (176-)149(-128) m.y., Soltis et al. (2008) estimated (168-)131(-126) m.y., and Magallón et al. (2013) an age of around 149.1 m.y..; see also Magallón (2009) for other dates around 140-150 m.y.a..
Doyle and Endress (2010) thought that the Pennipollis plant, from ca 120-115 m.y.a. in Portugal and originally linked to the monocots (Petersen et al. 2000b), was sister to Chloranthaceae, a family they considered to be sister to all angiosperms apart from the ANITA grade.
Evolution. Divergence & Distribution. Soltis et al. (2008) suggest ages for a number of branching points within this clade, but they are based on the topology [monocots [Chloranthaceae, magnoliids [Ceratophyllaceae + eudicots]]].
The character, "endotesta palisade, crystaliferous", could perhaps be placed at this node.
CHLORANTHALES Martius Main Tree.
Branching from the current flush; neolignans ?+; nodes often swollen; leaves opposite, joined by sheath, lamina margins toothed, teeth with lateral vein and others [hydathodal]; stipules +; flowers very small, monosymmetric by reduction, parts whorled; P 0, A 1, abaxial; G 1, ascidiate, postgenital fusion by secretion; ovule 1/carpel, apical, pendulous, straight; antipodal cells proliferating; fruit fleshy; endotesta palisade, lignified, crystalliferous; (endosperm starchy, grains clustered). - 1 family, 4 genera, 75 species.
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...
Synonymy: Chloranthineae Thorne & Reveal - Chloranthanae Doweld - Chloranthidae C. Y. Wu
CHLORANTHACEAE Sims, nom. cons. Back to Chloranthales
Evergreen; (vessels 0); primary stem with vascular cylinder; rays 6-10-seriate; nodes 1:1, 1:2, or ± 3:3, 2 traces from the central or all gaps, (+ split laterals); (sclereids - Hedyosmum); cuticle wax crystalloids 0; stomata variable, laterocytic, etc.; branching from current flush; lamina vernation conduplicate [Chloranthus], teeth with clear persistent swollen cap into which proceed higher order veins as well as secondaries or tertiaries; stipules small, paired, interpetiolar, usually on rim of sheath; (plants dioecious); inflorescence spicate (branched), flowers sessile; staminate flowers: A ± latrorse, lobed, or connective produced or not, (glandular); (apertures star-shaped monosulcate, polycolpate, polyporate); pistillode 0; carpellate flowers: (P +, ± connate, with windows - Hedyosmum); staminode 0; (ovary inferior), stigma ± expanded or not, dry ?or wet; ovules with outer integument 4-8 (2 - Ascarina) cells across, inner integument (3-)7-10 cells across, (micropyle bistomal), parietal tissue 6-8 cells across, nucellar cap +/0; fruit baccate or drupaceous, (bracts accrescent and succulent), (P persistent); coat ± tanniniferous, (mesotesta lignified - Chloranthus), tegmen ± crushed, (exo- and mesotegmen fibrous), endotegmen initially subpalisade; n = 8, 14, 15, chromosomes 1-4(-10: Hedyosmum) µm long.
4[list]/75: Hedyosmum (45). Tropics and subtropics, not Africa (Madagascar - Ascarina only) (map: from Verdcourt 1986; Todzia 1988). [Photo - Leaf, Flower.]
Age. Despite the age of the clade (see below), some estimates are that crown group diversification is quite recent, being mostly within the last 60-29 m.y. (Zhang & Renner 2003b; Soltis et al. 2008). However, Magallón and Castillo (2009) estimated the crown group age at ca 153.6 or 125 m.y., Wikström et al. (2001) at 131-121 m.y., Bell et al. (2010) at around 121 or around 98 m.y.a., depending on the analysis, Antonelli and Sanmartín (2011: fossil-based) suggested ages of (112-)111(-110) or thereabouts, while Zhang et al. (2011) provided another series of age estimates, some of which are dramatically older than the others depending on their calibration and the analytical methods used.
Chloranthaceous fossils are common, diverse, and world-wide in distribution in the early angiosperm fossil record. Distinctive fossil pollen grains, Asteropollis, are first known from the Barremian-Aptian of the early Cretaceous, some 125 m.y. before present (Friis et al. 1997; Doyle 1999; Eklund 1999, but c.f. Clarke et al. 2011, questions over dating); these grains have been identified as belonging to Hedyosmum (see also Crepet & Nixon 1996; Eklund et al. 2003; Friis et al. 2005; Martínez et al. 2013). Doyle and Endress (2007) and Clarke et al. (2011) discuss other palynomorphs that have been associated with Chloranthaceae; some fossil androecia assigned to the family have spiraperturate pollen that is in situ (Crane et al. 1989)!
Evolution. Divergence & Distribution. With older estimates of the family age, all genera had separated by ca 90 m.y.a. (e.g. Wikström et al. 2000; Antonelli & Sanmartín 2011). Diversification within Hedyosmum could be dated to (57.1-)43.3(-30.1) or (43-)35.6-(25.9) m.y.a. depending on the method used, and was in part associated with the Andean uplift, although the family as a whole showed a pattern of gradual extinction over time (Antonelli & Sanmartín 2011).
For general morphological evolution, living and fossil Chloranthaceae integrated, see Eklund et al. (2004). Endress (2001) emphasized what he considered to be the plesiomorphic floral morphology of the family. However, there is no evidence that it is a member of the ANITA grade, and several aspects of its floral morphology and development, including the loss of any perianth, are clearly derived (e.g. Li et al. 2005). Given the relationships within the family (see below), simple parsimony suggests that perfect flowers are developed from imperfect flowers (see also Doyle & Endress 2011).
Chemistry, Morphology, etc. Although benzylisoquinoline alkaloids apparently have not been detected in Chloranthaceae, (S)norcolaurine synthase activity is high, suggesting that they may be found here (Liscombe et al. 2005). Roots - presumably those of the seedlings and young plants - seem not have any secondary thickening (Blanc 1986)?
For some discussion of infloresecence morphology, see Doria et al. (2012). The perianth of Hedyosmum has unique, schizogenous apertures/windows (Doria et al. 2012 and references). Crane et al. (1989), Crepet and Nixon (1997), Eklund et al. (1997), Eklund (1999), and others discuss the nature of the androecium in the family, a matter over which there has been considerable controversy. In Chloranthus it has been suggested that the androecium is lobed, with 2 or 4 dithecal stamens(!!?), and that staminate flowers of Hedyosmum have hundreds of anthers, however, here as elsewhere staminate flowers seem to have but a single dithecal stamen (Kong et al. 2002, and references). Doria et al. (2012) illustrate a superior gynoecium in Hedyosmum. The stylulus is filled with secretion. Endress and Igersheim (1997) describe the stigma as being wet (c.f. Todzia 1988). The ovule in Chloranthus is not quite straight ("subatropous" - Yamada et al. 2001a). For variation in micropyle type, see Heo and Tobe (1995). Johri et al. (1992) noted that the endosperm stores oil, but there may also be starch. The cotyledonary nodes has split laterals (Bailey 1956).
For general information, see Swamy (1953), Todzia (1988, 1993) and Eklund (1999), for chemistry, see Hegnauer (1964, 1989), embryology, see Vijayaraghavan (1964), young plants, see Blanc (1986), general vegetative anaomy, see Metcalfe (1987), for wood anatomy, see Carlquist (1992a), and for floral development, see Endress (1987b) and G. S. Li et al. (2005).
Phylogeny. Within Chloranthaceae, morphological analyses, including details of wood anatomy, suggested the genus pairs [Ascarina + Hedyosmum], mainly woody, plant monoecious to dioecious, and [Chloranthus + Sarcandra], herbaceous to semi-shrubby, flowers perfect. In molecular work (Qiu et al. 1999), on the other hand, the relationships [Hedyosmum [Ascarina [Chloranthus + Sarcandra]]] were found. Although there was strong support, the sampling was rather minimal, but the same set of relationships were confirmed by Zhang and Renner (2003b) and Zhang et al. (2011), both with a much improved sampling. They have also been found in subsequent morphological analyses with constrained outgroups (Doyle et al. 2003; Eklund et al. 2004).
Synonymy: Hedyosmaceae Caruel