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).
MONOCOTYLEDONS / MONOCOTYLEDONEAE / LILIANAE Takhtajan
Plant herbaceous, perennial, rhizomatous, growth sympodial; non-hydrolyzable tannins [(ent-)epicatechin-4] +, neolignans, benzylisoquinoline alkaloids 0, hemicelluloses as xylans; root apical meristem?; root epidermis developed from outer layer of cortex; trichoblast in atrichoblast [larger cell]/trichoblast cell pair, the former further from apical meristem, in vertical files, or hypodermal cells dimorphic; endodermal cells with U-shaped thickenings; cork cambium in root [uncommon] superficial; root vascular tissue oligo- to polyarch, medullated, lateral roots arise opposite phloem poles; primary thickening meristem +; vascular bundles in stem scattered, (amphivasal), closed, vascular cambium 0; tension wood 0; vessel elements in root with scalariform and/or simple perforations; tracheids only in stems and leaves; sieve tube plastids with cuneate protein crystals alone; stomata parallel to the long axis of the leaf, in lines; prophyll single, adaxial; leaf base sheathing, sheath open, petiole 0, blade linear, main venation parallel, main veins joining successively from the outside at the apex, transverse veinlets +, unbranched, vein/veinlet endings not free, margins entire, Vorläuferspitze +, colleters + ["intravaginal squamules"]; inflorescence terminal, racemose; flowers 3-merous [6-merous to the pollinator?], polysymmetric, pentacyclic; P = T, each with three traces, median T of outer whorl abaxial, aestivation open, members of whorls alternating, [pseudomonocyclic, each T member forming a sector of any tube]; stamens = and opposite each T member [primordia often associated, and/or A vascularized from tepal trace], anther and filament more or less sharply distinguished, anthers subbasifixed, endothecium from outer secondary parietal cell layer, inner secondary parietal cell layer dividing; G , with congenital intercarpellary fusion, opposite outer tepals [thus median member abaxial], placentation axile; ovule with outer integument often largely dermal in origin, parietal tissue 1 cell across; antipodal cells persistent, proliferating; fruit a loculicidal capsule; seed testal; endosperm with distinct nuclear and chalazal chambers, embryo long, cylindrical, cotyledon 1, apparently terminal, with a closed sheath, unifacial [hyperphyllar], both assimilating and haustorial, plumule apparently lateral; primary root unbranched, not very well developed, stem-borne roots numerous, hypocotyl short, (collar rhizoids +); cotyledon with a closed sheath, unifacial [hyperphyllar], both assimilating and haustorial; no dark reversion Pfr -> Pr; duplication producing monocot LOFSEP and FUL3 genes [latter duplication of AP1/FUL gene], PHYE gene lost. (Some synapomorphies - almost whatever the immediate sister taxa to monocots might be - are in bold.)
[ALISMATALES [PETROSAVIALES [[DIOSCOREALES + PANDANALES] [LILIALES [ASPARAGALES + COMMELINIDS]]]]]: ethereal oils 0; raphides + (druses 0); leaf blade vernation variants of supervolute-curved, (margins with teeth, teeth spiny); endothecium develops directly from undivided outer secondary parietal cells; tectum reticulate with finer sculpture at the ends of the grain, endexine 0; (septal nectaries + [intercarpellary fusion postgenital]).
[PETROSAVIALES [[DIOSCOREALES + PANDANALES] [LILIALES [ASPARAGALES + COMMELINIDS]]]]: cyanogenic glycosides uncommon; starch grains simple, amylophobic; leaf blade developing basipetally from hyperphyll/hypophyll junction [?level]; epidermis with bulliform cellls [?level]; stomata anomocytic, (cuticular waxes as parallel platelets); colleters 0.
Age. The crown-group age of this group ("core monocots") is ca 131 m.y. (Janssen & Bremer 2004). Magallón and Castillo (2009) suggest ca 150 m.y. for relaxed and 124 m.y. for constrained penalized likelihood datings of the crown group age, Bell et al. (2010) ages of (133-)124, 109(-99) m.y.; (127-)121, 109(-103) m.y. was estimated by Wikström et al. (2001: c.f. topology), and estimates were (132-)128(-121) m.y. in Merckx et al. (2008a) and 133-108 m.y. in Mennes et al. (2013).
Evolution. Divergence & Distribution. Subsequent branching in this general part of the tree - i.e. the Petrosaviales, [Dioscoreales + Pandanales], and Liliales clades, and also crown group Petrosaviales itself, may be somewhere around 125-120 m.y.a. (ca 111 m.y. in Bremer 2000b), and the stem groups of all other orders, including those in the commelinid group, diverge by ca 115 m.y.a. or soon afterwards (Janssen & Bremer 2004). These and also many clades within all these orders may have originated in Southern Gondwana, i.e. Antarctica, Australasia, and southern South America (Bremer & Janssen 2006).
Phylogeny. Relationships between commelinids, Asparagales, Dioscoreales, Liliales, and Pandanales remained unclear for some time. In a smallish early study, Liliales were sometimes embedded in Asparagales (Eguiarte et al. 1994). A three-gene (rbcL, atpB, 18S RNA) study (Chase et al. 2000a) showed a polytomy of Petrosaviaceae, Dioscoreales, Pandanales, Liliales, Asparagales and commelinids, although a single shortest tree showed a pectinate structure with the taxa in the sequence followed here; another analysis with placeholders for taxa missing some sequences gave a similar structure, except that Pandanales and Liliales were sister taxa. (A combined morphological plus molecular tree in the same volume [Stevenson et al. 2000] suggested a substantially different set of relationships; bootstraps were not given.) Fay et al. (2000a) also suggested a sister relationship between Asparagales and commelinids, although sampling outside Asparagales was sketchy since it was outside their immediate interest. Hilu et al. (2003: matK) i.a. suggested that Orchidaceae might be separate from other Asparagales (the latter being sister to commelinids) and that Dioscoreales and Pandanales formed a clade.
However, a two-gene (matK, rbcL) study (Tamura et al. 2004a) began to clarify the situation. Petrosaviaceae (both genera - but see below for a possible third - were studied) were sister to a clade [[Dioscoreaceae + Pandanaceae] [Liliales [Asparagales + commelinids]]] (see Chase et al. 2000a above). Support was quite high (³85% bootstrap) for all order and family branches, although rather lower for [Asparagales + commelinids] (68%) (see also Tamura et al. 2004b, a smaller study). Davis et al. (2004) also found Petrosaviales to be sister to the same monocots, but with moderate to weak (>72%) support. Graham et al. (2006) in a study analysing considerable amounts of data also recovered relationships similar to those suggested by Tamura et al. (2004a), all sister taxon relationships in this area having 94% or more support, although that for [Liliales [commelinids + Asparagales]] was only 70% (see also Givnish et al. 2006b; Chase et al. 2006). Dioscoreales and Pandanales are sister taxa in most studies (e.g. Hilu et al. 2003; Chase et al. 2006; Qiu et al. 2010: support strong).
Areas of uncertainty remain. In other trees Dioscoreales and Pandanales are adjacent along the spine (e.g. Janssen & Bremer 2004; Bremer & Janssen 2006; Givnish et al. 2006b: not strongly supported), or Nartheciaceae linked with Pandanales, the combined group in turn joining with Liliales (Davis et al. 2004: summary of earlier literature on relationships of the two). A recent four-gene mitochondrial tree suggests the relationships [Asparagales [[Dioscoreales + Pandanales] [Liliales + Commelinids]]], but support is not strong (Qiu et al. 2010), while Davis et al. (2013) recovered a very weakly supported topology [Asparagales s. str. [Orchidaceae + Liliaceae]] in parsimony but not in maximum likelihood analyses.
Some myco-heterotrophic taxa cause problems. Thus Neyland (2002) found that Thismia was sister to a well supported Burmannioideae, but with less support, but Burmanniaceae s.l. did not link with other Dioscoreales. Analysis of 26S rDNA sequences suggested that Corsiaceae were polyphyletic; Arachnitis perhaps being sister to Thismia and/or Burmannia (Neyland & Hennigan 2003; G. Petersen et al. 2006b: combined analysis). A recent analysis of plastid loci also failed to include Arachnitis in Liliales, and perhaps it is to be included in the commelinids (Kim et al. 2012). However, these relationships need to be confirmed.
Classification. Since no firm association of Petrosaviaceae with any other order has been supported, and its phylogenetic position, as in the tree here, seems well supported, a monofamilial Petrosaviales is appropriate.
PETROSAVIALES Takhtajan Main Tree.
Stem with a ring of bundles; sieve tube plastids also with polygonal protein crystalloids; inflorescence bracts +; microsporogenesis simultaneous; pollen surface gemmate; septal nectaries +; styluli +; fruit a follicle; seed endotestal. - 1 family, 2 genera, 4 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: Miyoshiales Nakai - Petrosaviineae Shipunov
(Plant echlorophyllous, myco-heterotrophic, vascular bundles in stem forming a cylinder, vessels 0 - Petrosavia); plant glabrous; leaves spiral, scaly on rhizome, base?; bracteoles sublateral (0); T members with a single trace, whorls slightly differentiated [outer somewhat smaller], tube at most short; A inserted at base of T or free; (pollen gemmate - Japonolirion); ovary superior to semi-inferior, partly connate, plicate, fusion (congenital and) postgenital, stigma subcapitate or decurrent; ovules 4-many/carpel, ana-campylotropous, integumentary obturator +; fruit also septicidal [Japonolirion], T persistent [?Petrosavia]; seeds obliquely arranged, winged or not, endotegmen crushed, contents persist; embryo small; n = 12, 13, 15; seedling?
2[list]/4. Japan and China, W. Malesia (map: from Jessop 1979).
Age. Crown group Petrosaviaceae date to ca 123 m.y. (Janssen & Bremer 2004) or (134-)99, 89(-62) m.y. (Bell et al. 2010); estimates were (102-)108(-87) m.y. in Merckx et al. (2008a) and 96-8 m.y. in Mennes et al. (2013).
Evolution. Divergence & Distribution. This is not exactly a clade in which there has been much divergence.
Genes & Genomes. For evolution (loss of genes, etc.) in the chloroplast genome of the myco-heterotroph Petrosavia, see Logacheva et al. (2014); rather unusually for such systems, there has been extensive rearrangment of the genome.
Chemistry, Morphology, etc. The roots of Petrosavia have an unmedullated, four-radiate stele. Remizowa (2011) suggested that the position of the septal nectaries in both the ascidiate and plicate zone of the gynoecium might be unique and so a synapomorphy for this tiny but quite heterogeneous clade.
For general information, see Tamura (1998: Nartheciaceae) and especially Cameron et al. (2003), for anatomy, see Stant (1970), for pollen, see Caddick et al. (1998), for sieve tube plastids, see Behnke (2003), for floral and inflorescence morphology, see Remizowa et al. (2006a, b) and Tobe (2008), and for the embryology of Petrosavia, see Tobe and Takahashi (2009: nice comparative table).
Phylogeny. Isidrogalvia (as I. schomburgkiana, Tofieldiaceae!) was placed sister to Petrosavia (L.-Y. Chen et al. 2013) in a study focusing on the aquatic Alismatales - a rather remarkable position that needs confirmation.
Previous Relationships. Petrosaviaceae have often been included in other families. Dahgren et al. (1985) placed them - along with genera here placed in Nartheciaceae and Tofieldiaceae - in Melianthaceae, and while Tamura (1998) recognised a Petrosaviaceae, this also included members of Tofieldiaceae and Nartheciaceae. Petrosaviaceae s. str. (i.e. Petrosavia alone) were placed in Triuridales by Cronquist (1981) and in Triurididae by Takhtajan (1997); the latter included a monogeneric Japonoliriaceae in his Melanthiales-Liliidae.
Synonymy: Japonoliriaceae Takhtajan, Miyoshiaceae Nakai