EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; rhizoids +, unicellular; acquisition of phenylalanine lysase [PAL], phenylpropanoid metabolism [lignans +, flavonoids + (absorbtion of UV radiation)], xyloglucans +; plant [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; cuticle +; cell wall also with (1->3),(1->4)-ß-D-MLGs [Mixed-Linkage Glucans]; chloroplasts per cell, lacking pyrenoids; 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; blepharoplast, bicentriole pair develops de novo in spermatogenous cell, associated with basal bodies of cilia [= flagellum], multilayered structure [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] + spline [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte dependent on gametophyte, embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, with at least transient apical cell [?level], sporangium +, single, 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, initially laid down in association with several trilamellar layers [white-line centred layers, i.e. walls multilamellate]; nuclear genome size <1.4 pg, LEAFY gene present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes.
Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Abscisic acid, ?D-methionine +; sporangium with tapetal layer, columella + [developing from endothecial cells], seta developing from basal meristem [between epibasal and hypobasal cells; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; spores trilete; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; shoot meristem patterning gene families expressed; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.
[Anthocerophyta + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour.
Sporophyte branched, branching apical, dichotomous; sporangia several, each opening independently; spore walls not multilamellate [?here].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Photosynthetic red light response; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); sporophyte soon independent, dominant, with basipetal polar auxin transport; lignins +; vascular tissue +sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem, plant endohydrous [physiologically important free water inside plant]; endodermis +; stem with an apical cell; branching dichotomous; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; tapetum glandular; gametophytes exosporic, green, photosynthetic; basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte branching ± indeterminate; root apex multicellular, root cap +, lateral roots +, endogenous; endomycorrhizal associations + [with Glomeromycota]; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; LITTLE ZIPPER proteins.
Sporophyte woody; lateral root origin from the pericycle; branching lateral, meristems axillary; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
Plants heterosporous; megasporangium surrounded by cupule [i.e. ovule +, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].
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 particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; root stele with xylem and phloem originating on alternate radii, cork cambium deep seated; 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 +; cork cambium superficial; 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.; axillary buds exogenous, (none; not associated with all leaves); prophylls two, lateral; leaves with petiole and lamina, development basipetal, blade simple; plant heterosporous, sporangia borne on sporophylls, sporophylls spiral; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation and deposition of sporopollenin from tapetum], exine and intine homogeneous; megasporangium indehiscent; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophytes dependent on sporophyte, apical cell 0, rhizoids 0; male gametophyte development initially endosporic, tube developing from distal end of grain, gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], 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.
EXTANT GYMNOSPERMS / PINOPHYTA / ACROGYMNOSPERMAE
Biflavonoids +; cuticle wax tubules with nonacosan-10-ol; ferulic acid ester-linked to primary unlignified cell walls; phloem sieve area with small pores generally less than 0.8 µm across that have cytoplasm and E.R., joining to form a median cavity in the region of the middle lamella, Strasburger/albuminous cells associated with sieve tubes [the two not derived from the same immediate mother cell], phloem fibres +; sclereids +, ± tracheidal transfusion tissue +; stomatal poles raised above pore, no outer stomatal ledges or vestibule, epidermis lignified; buds perulate/with cataphylls; lamina development marginal; plants dioecious; microsporangium with exothecium; pollen tectate, infratectum alveolate [esp. saccate pollen], endexine lamellate at maturity, esp. intine with callose; ovule unitegmic, with pollen chamber formed by breakdown of nucellar cells, nucellus massive; ovules increasing considerably in size between pollination and fertilization, but aborting unless pollination occurs; ovule with pollination droplet; pollen grain lands on ovule, germinates in two or more days, tube with wall of pectose + cellulose microfibrils, branched, growing at up to 10(-20) µm/hour, haustorial, breaks down sporophytic cells; male gametophyte of two prothallial cells, a tube cell, and an antheridial cell, the latter producing a sterile cell and 2 gametes; male gametes released by breakdown of pollen grain wall, with >1000 cilia, basal body 800-900 nm long; fertilization 7 days to 12 months or more after pollination, to ca 2 mm from receptive surface to egg; female gametophyte initially with central vacuole and peripheral nuclei plus cytoplasm, cellularization/alveolarization by centripetal formation of anticlinal walls, the inner periclinal face open, with a single nucleus connected to adjacent nuclei by spindle fibres; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; testa mainly of coloured sarcoexotesta, scleromesotesta, and ± degenerating endotesta; first zygotic nuclear division with chromosomes of male and female gametes lining up on separate but parallel spindles, embryogenesis initially nuclear, embryo ± chlorophyllous; gametophyte persists in seed; plastid and mitochondrial transmission paternal; nuclear genome size 8-32(-76) pg [1 pg = 109 base pairs]; two copies of LEAFY gene [LEAFY, NEEDLY] and three of the PHY gene, [PHYP [PHYN + PHYO]], second intron in the mitochondrial rps3 gene [group II, rps3i2].
PINALES Gorozh. Main Tree.
Tree branched; compression wood +; wood pycnoxylic; tracheid side wall pits with torus:margo construction, bordered; phloem with scattered fibres alone [Cycadales?], resin ducts/cells in phloem [and elsewhere]; lignins with guaiacyl units (G-lignin) [lacking syringaldehyde, Mäule reaction negative]; cork cambium ± deep seated; bordered pits on tracheids round, opposite; (cladoptosis +); nodes 1:1; axillary buds + (0); leaves with single vein; plants monoecious; microsporangiophore/filament simple with terminal microsporangia; microsporangia abaxial, dehiscing by the action of the hypodermis [endothecium]; pollen saccate, exine thick [³2 µm thick]; ovulate strobilus compound, ovuliferous scales flattened, ± united with bract scales; ovules lacking pollen chamber, inverted [micropyle facing axis]; pollen tube unbranched, growing towards the ovule, wall with arabinogalactan proteins; gametes non-motile, lacking walls, released from the distal end of the tube, siphonogamy; seed coat dry, not vascularized; embryo initially with 2 to 4 free-nuclear divisions, with upper tier or tiers of cells from which pro- or secondary suspensor develops, elongated primary suspensor cells and basal embryonal cells [or some variant]; germination phanerocotylar, epigeal, (seedlings green in the dark); plastid and mitochondrial transmission paternal, one duplication in the PHYP gene line, one copy of chloroplast inverted repeat missing. - 7 families, 68 genera, 545 species.
Age. Clarke et al. (2011: other ages) suggested a crown age for Pinales of (286-)252(-212) m.y., Magallón et al. (2013) an age of ca 278 m.y., and Won and Renner (2006) an age of (324-)298(-270) m.y. - all include Gnetales - while the estimate by Crisp and Cook (2011: no Gnetales) of around 270 m.y. is also broadly comparable. Leslie et al. (2012) suggested an age of around 350-275 m.y.a., but Zhou et al. (2014) and Magallón et al. (2015) suggested appreciably younger ages of (187.3-)161.4(-147) and ca 127 m.y.a. respectively; see also P. Soltis et al. (2002).
Note: (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed (see above). In particular, if Gnetales are to be included here, depending on where they end up, apomorphies could change considerably.
Evolution. Divergence & Distribution. There are no known synapomorphies for a clade containing living and fossil conifers (e.g. Rothwell & Serbet 1994). The morphology of extinct conifers and coniferophytes is being re-evaluated as the morphologies of entire organisms are pieced together from what used to be separate form genera; the result is that many of the conventional taxonomic groupings are being radically overhauled (e.g. Rothwell et al. 2005; Hernandez-Castillo et al. 2009; see also below). As this is done, the extent of the diversity of these fossil plants is becoming clear. Not only are forked leaves common, but stomatal distribution, etc., may differ dramatically on leaves from the one plant, compound microsporangiate strobili are known (c.f. Gnetales!), as are megasporagiate strobili which do not terminate vegetative growth of the axis on which they occur (e.g. Hernandez-Castillo et al. 2001; Rothwell & Mapes 2001).
Leslie et al. (2012) suggest ages for several clades within Pinales (see below), and evaluate the fossil data critically; their four-gene tree is based on an almost complete sampling of the group. The current distributions of many extant conifer groups is much smaller than and/or very different from their past distributions. Many conifers have fossil records going back to the Cretaceous; see Manchester (1999) for north temperate distributions), McIver (2001) for fossils of the African Widdringtonia (Cupressaceae) in rocks of Cretaceous age in Alabama. For the early Caenozoic fossil history of what are now East Asian endemics, see Ferguson et al. (1997) and Manchester et al. (2009) - genera in Taxaceae, Pinaceae, Sciadopityaceae and Cupressaceae are included. However, Biffin et al. (2010b) note that some calibration scenarios have crown-group divergence of Araucariaceae and Podocarpaceae largely a (mid-Cretaceous to) Caenozoic phenomenon, which would question the attribution of early fossils at least to those families. Indeed, podocarps with broader leaves seem to have diversified considerably in the earlier Caenozoic in the southern hemisphere (Brodribb & Hill 2004; Biffin & Lowe 2011 - see below).
Diversification in most conifer genera is Caenozoic in age, but Leslie et al. (2012) note that most southern hemisphere clades are older than northern clades, and this is particularly true of the southern Cupressaceae-Callitroideae - its mean node age is four times that of the northern Cupressaceae-Cupressoideae. Leslie et al. (2012) aasociated this with the more equable climate in at least parts of the southern hemisphere compared with the major climate swings in the northern hemisphere beginning in the Oligocene. Earlier, during the Palaeocene-Eocene thermal maximum, conifers, perhaps especially Cupressaceae and Podocarpaceae, were replaced by angiosperm-dominated vegetation (Wing & Currano 2013), although now, of course, Pinaceae dominate boreal forests in particular, and southern conifers, too, can be locally very abundant.
Franceschi et al. (2008) suggest possible anatomical apomorphies that are associated with defence against herbivorous insects. For distribution maps of all conifers, see Farjon and Filer (2013).
Ecology & Physiology.Bond (1989), Brodribb et al. (2012) and other have emphasized that conifers in general can out-compete angiosperms in a number of environments that are low in nutrients. There are at least four major clades involved: Pinaceae, mostly northern, [Araucariaceae + Podocarpaceae], now mostly southern, and two major clades in Cupressaceae that have largely inhabited the northern and southern hemispheres respectively since the Jurassic (Brodribb et al. 2012). Many conifers, but less the [Podocarpaceae + Araucariaceae] clade, tolerate extreme cold, they grow well in high-light environments, and despite lacking vessels their wood shows moderate hydraulic conductance and is resistant to cavitation, etc. (Brodribb et al. 2012).
Litter and wood decay of gymnosperms in general is slower than that of angiosperms (e.g. Wardle et al. 2008; Cornwell et al. 2008b; Weedon et al. 2009), and root decay of Pinales in particular is slower (Silver & Miya 2001). Brown rot fungi are common on Pinales. They can access much of the cellulose in the cell wall but they do not destroy the lignin; they may have evolved from white-rot fungi (e.g. Floudas et al. 2012; Kohler et al. 2015; the distinction between the two is somewhat artificial - Riley et al. 2014; Floudas et al. 2015). Many Pinaceae, ECM plants, grow successfully in low N conditions and podocarps, VAM plants, in low P conditions (Brodribb et al. 2012).
Conifers frequently dominate the communities in which they grow, and are often long-lived plants; the high-light conditions they prefer are often associated with infrequent catastrophic disturbances that allow seedling establishment. Some emergent and apparently dominant conifers (often other than Pinaceae) may have have remarkably little effect on the forests in which they grow, and the basal area of angiosperm trees in forests with and without these emergents, but which are otherwise comparable, are similar (Enright & Ogden 1995; Aiba et al. 2007).
Seventeen species of conifers in Pinaceae, Araucariaceae, and Cupressaceae, along with 29 species of Dipterocarpaceae and especially Eucalyptus, are "giant trees" at least 70 m tall (Tng et al. 2012).
Sperry (2003), Pitterman et al. (2005), Hacke et al. (2005) and Sperry et al. (2006) compare water transport in tracheids that have the torus:margo pits found in many conifers (including Ginkgo), with that in other kinds of tracheids and in vessels. Pore size in the margo is relatively large, while the torus provides a valuable safety feature guarding against embolism. Indeed, hydraulic conductance in tracheids with torus:margo pits is somewhat greater than in vessels of similar diameter when expressed on a sapwood area basis, while studies of cavitation in this system suggest that it is not connected with the size of the pores in the margo, but rather with the torus:pit aperture ratio (Pittermann et al. 2010). Vascular tissue with tracheids only may be less hydraulically efficent, but they are tolerant of hydraulic stress and are resistant to cavitation, despite investing only about half as much as angiosperms in wall material - but at the same time they can be very large trees (Sperry 2003).
Another element in the control of water flow in conifers is transfusion tissue, groups of tracheid cells just outside the vascular bundles. These cells collapse as the leaf loses water and water deficits are not too great (<-3 MPa), but readily regain their size when the leaf becomes rehydrated. When collapsed, they reduce the flow of water from the xylem (Y.-J. Zhang et al. 2014).
Pollination Biology & Seed Dispersal. Much has been learned about pollination and pollen germination in conifers in the last few years, although important work had also been carried out about 80 years ago. Pollen directly impacts the ovulate cones of conifers rather than being swept around the cone by a turbine-like action (Cresswell et al. 2007). It had been thought that the sacci on the pollen of some conifers facilitated its dispersal by wind, however, they often function more like water wings; within Pinales there is a correlation between presence of pollen sacci or wings and exine thickness and structure, whether (no wings) or not (wings) the pollen is wettable, etc. (Tomlinson 1994). Pollen sacci help orient the pollen grains in the pollination droplet (Doyle & O'Leary 1935; Salter et al. 2002 and references), or, more particularly, when the ovules are inverted, a common condition, the pollen grains are wetted and float up to the micropyle where the saccus orients the grain on the nucellus, separating and exposing the sulcus through which the pollen tube germinates (Salter et al. 2002; Leslie 2010b). Sacci also help in the selection of appropriate pollen grains during pollination. Thus the proportion of saccate to non-saccate pollen grains inside the ovules is higher than that outside (Leslie 2009). The pollination droplet in Phyllocladus and many taxa with erect ovules is resorbed through the micropyle, and again the pollen grains are brought close to the nucellus; in Juniperus communis and other taxa this resorbtion may be an active process happening quite soon after the pollen grain lands (Mugnaini et al. 2007). There are further variants of these pollination mechanisms in Coniferales (Owens et al. 1998; Salter et al. 2002; Fernando et al. 2005 for references) and other ancient gymnosperms (Leslie 2008).
Recent work suggests that the situation is more complex. Sacci may increase the distance the pollen grain can travel before it falls to the ground, so facilitating wind dispersal (Schwendemann et al. 2007). However, this depends on the nature of the sacci; if they have extensive air sacs, as in Pinus, pollen is likely to travel further, but if the sacci are composed of denser material, as in Falcatfolium, then pollen will fall faster - as they may also if the surface of the pollen grain is not smooth (Grega et al. 2013). For additional information on pollination, see Doyle (1945), Tomlinson (1994, 2000, 2012), Tomlinson et al. (1997), and Tomlinson and Takaso (2002); see also Williams (2009).
There is considerable variation in the development of the male gametophyte (Fernando et al. 2010: summary and terms used). The actual process of pollen germination varies, and the feature "pollen exine shed during microgametophyte germination", is likely to have evolved more than once (?three times) in Pinaceae alone (see also Rydin & Friis 2005); for cell death induced by the growing pollen tube, see Fernando et al. (2005 and references).
Bateman et al. (2011; see also Givnish 1980) note a correlation between dioecy and fleshy, animal-dispersed seeds and monoecy and dry, wind-dispersed seeds in gymnosperms, a correlation that is evident within Pinales. Leslie et al. (2013) suggest that this is largely due to the persistence of groups which are dioecious and have fleshy fruits or monoecious and have dry fruits; they note common transitions from the monoecy/fleshy to dioecy/fleshy combinations. Pollen and dry seed cone size in particular correlates with branch thickness, etc., in conifers; fleshy seed cones are notably smaller than dry cones (Leslie et al. 2014).
Plant-Animal Interactions. Conifers in general have layers of polyphenol-containing parenchyma cells in the phloem, possibly offering some protection against insects. Pinaceae have resin ducts in both phloem and xylem, other Pinales have resin ducts only in the xylem. These other Pinales also have large numbers of small, extracellular, calcium oxalate crystals and stratified phloem, while Pinaceae have scattered sclereid cells or sometimes groups of such cells (e.g. Hudgins et al. 2003; Franceschi et al. 2008). Various elements of the defences are constitutive and/or inducible, methyl jasmonate being part of the inductive pathway (e.g. Hudgins et al. 2003; Hudgins & Franceschi 2004), and different herbivores elicit different responses by the plant (Moreira et al. 2013), and even within Pinus there is variation in how much particular defences are expressed constitutively (Carrillo-Gavilán et al. 2014).
Hudgins et al. (2003, 2004) examined the diversity of bark beetles in conifers in the context of various plant structures that might be defences against such beasts; Franceschi et al. (2005) elaborate on the pine-beetle story. Pine beetles, Dendroctonus spp., can be noxious pests and invade living pines; they tend to have relatively few hosts, but outbreaks can be devastating (Kelley & Farrell 1998: host specificity; Wood 1982 and Wood & Bright 1992: the weevils). The bark beetles eat the wood despite the presence of resin ducts in both phloem and xylem in Pinaceae, and there are also intracellular crystals, etc., which could be protective; other Pinales, which have resin ducts only in the xylem, harbour a lower diversity of these beetles. Blue-stain fungi, species from a few unrelated ascomycete genera that are carried by the pine beetles, can quickly invade the sapwood and render it non-functional, basically clogging it up and killing the plant surprisingly quickly; some, at least, also detoxify the plant's defences, so protecting the beetle (DiGuistini et al. 2011).
Many of the wood-eating basal termites (their protozoans in theit guts can break down lignin) seem to like the wood on Pinales; the crown-group age of termites is Jurassic in age, ca (170-)149(-136) m.y.o. (Bourguignon et al. 2014).
Bacterial/Fungal Associations. A number of rusts, including those on ferns, Rosaceae, Grossulariaceae, etc., have part of their life cycles on Pinales, especially Pinaceae (Savile 1979b). For foliar endophytes and their bacterial associates, see Hoffman and Arnold (2010). Basidiomycete brown rot fungi are common in coniferous forests and are also found in broad-leaved, more temperate forests, but they are at most uncommon in tropical forests (Gilbertson 1981); for the relationships of (and uncertain distinction between) brown and white rot fungi, see Riley et al. (2014).
Genes & Genomes. Conifers are noted for their very large nuclear genomes up to 72 pg (Zonneveld 2012); for 1C values, see Plant DNA C-values Database (consulted vi.2013). These massive genomes are the result of the activity of a number of transposable elements that are not counteracted by mechanisms for slimming genomes, as in angiosperms (Ahuja & Neale 1005; Nystedt et al. 2013). Note, however, that genome size in Pinales is quite similar to that in other gymnosperms. Reductions in genome size have probably occurred in Podocarpaceae and in particular in Gnetum, so the increase in size in gymnosperms is not totally a one-way ticket (c.f. Bennetzen & Kellogg 1997). Leaf mass per unit area seems to be correlated with genome size, but this may be because of phylogenetic correlations (Beaulieu et al. 2007b).
C.-S Wu et al. (2011b) suggested that a different copy of the inverted repeat had been lost in Pinaceae and in the clade making up the rest of the order. See also Raubesen and Jansen (1992a), Lackey and Raubeson (2008) and Hirao et al. (2008) for the loss of a copy of the inverted repeat.
There is extensive duplication of the knox-1 gene within Pinaceae, at least, although more general sampling is needed to pin down the point at which this duplication occurred (Guillet-Claude et al. 2004).
Chemistry, Morphology, etc. For fatty acids in the seeds, see Wolff et al. (2002 and references), and for resin composition and gum production, see Tappert et al. (2011). Conifer lignin, primarily made up of guaiacyl units, is denser, more highly condensed, has a larger polymer size, etc., than the S-rich lignins of angiosperms (Wagner et al. 20915).
The interpretation of the stem apex in terms of the tunica-corpus layering is not easy (see Napp-Zinn 1966). I have not integrated much of the considerable variation in wood anatomy with the clades recognised here (see e.g. Zhou & Jiang 1992 for information). Cork cambium is often more or less deep seated, although in Sequoia and Phyllocladus (e.g.) is is superficial (Möller 1882). Bark anatomy is very complex, but fortunately it has been studied in detail (e.g. Franceschi et al. 2008). Calcium oxalate microcrystals are commonly found in some cell walls throughout the group (Fink 1991; Hudgins et al. 2003: ?Cephalotaxaceae, Sciadopityaceae), but their distribution in other gymnosperms is unclear; they may be absent. Their position within tissues is linked with the development of fibres, the amount of resin secreted, etc. (Hudgins et al. 2003). There is generally a single trace per leaf, but if the leaves are opposite, there may be two traces, but then they fuse before they enter the petiole (Namboodiri & Beck 1968a, b). Leaf traces can also make connections with xylem produced during the second and subsequent years (Maton & Gartner 2005), and secondary growth (only phloem is produced) has been reported from the leaves of a number of conifers (Ewers 1982). Short shoots occur in a number of taxa (see Dörken et al. 2012 for a summary), and branch shedding, also occurring in taxa other than those with short shoots, is widespread (Burrows et al. 2007 and references). Organised bud meristems usually occur in the axils of only some leaves, although more cryptic meristems are quite widespread (Namboodiri & Beck 1968a; Fink 1984; Burrows 1999, 2009); in taxa like Pinus and Sciadopitys axillary buds are much more common, although most produce short shoots.
Bisexual strobili that have ovuliferous scales above the microsporangia, i.e., the same basic arrangement as in angiosperm flowers, are scattered through the clade (Flores-Rentería et al. 2011). Basic cone morphology is very variable. Conifer seed cones have becoming more massive and strongly constructed since the Triassic, and particularly the Jurassic, presumably in reponse to animal predation pressure (Leslie 2011). Among extant taxa, Taxus has tiny female cones each with a single, erect ovule, but cones are often massive structures. The ovuliferous scale is often well-developed and the bract scale inconspicuous, or the bract and ovuliferous scales may be largely separate, as in Pseudotsuga, while in Cupressaceae there is little evidence of an ovuliferous scale in the mature cone, which consists largely of bract scales (Schulz & Stutzel 2007; Rothwell et al. 2011 for references). Understanding details of the morphological evolution of cones will depend on advances in our understanding of the fossil record, and it is likely that heterochrony has been involved; Cupressaceae can be linked with the fossil Voltziaceae (e.g. Rothwell et al. 2011). Developmental studies may also be of value. Thus Englund et al. (2011) found that gene expression patterns linked the epimatium of Podocarpus with the ovuliferous scale of Pinus (see also e.g. Tomlinson & Takaso 2002), but not with the aril of Taxus. However, when comparing the expression of these genes in Cupressaceae, no particular similarities were observable (Groth et al. 2011).
A branched pollen tube occurs sporadically in Pinales (Friedman 1987 for references). The nature of the male gametes needs more study. Some taxa have binucleate sperm cells, i.e., a cell plate does not form in the spermatogeneous cell, or, if it does, it is incomplete. The male gametes here may be unequal in size, as in Dacrydium, and one may even be extruded from the cytoplasm, as in Podocarpus spp. and Taxus. In at least some Gnetum, Podocarpus andinus, and Torreya taxifolia two unequally-sized male cells are produced (Singh 1978 for literature; I am grateful to Ned Friedman for help in understanding this complicated pattern of variation). Double fertlization may sometimes occur in Pinales (Friedman 1992). The free-nuclear stage in the proembryo of Pinales is shorter than that of other gymnosperms, being only 5 or 6 rounds of nuclear division in Podocarpaceae and Araucariaceae and even fewer in other members of the order (Owens et al. 2003c). Embryo size is rather variable, although it is often rather larger than that of the common ancestor of extant seed plants; in Pinus it may be close to the length of the seed.
For a classic study of both fossil and extant conifers, see Florin (e.g. 1951); see also Page (1990) and especially Gifford and Foster (1988), Farjon (2005b) for a bibliography and Farjon (2008) for an excellent general account; Debreczy and Rácz (2006) and Eckenwalder (2009) offer other general accounts. See also Trapp and Croteau (2001a: resin biosynthesis), Geyler (1867), Barthelmess 1935, and Kumari (1963: nodal anatomy), Möller (1882: cork cambium), Napp-Zinn (1966: leaf anatomy), Den Outer (1967) and Schulz (1990), both phloem anatomy, much detail unincorporated, Zhou and Jiang (1992: wood anatomy); see also Owens et al. (1995b: cytoplasmic inheritance, nuclei sometimes incorporate cytoplasm), Williams (2009: reproductive biology), Mundry (2000: cone/strobilus development, emphasis on Taxaceae and friends), Sklonnaya and Ruguzova (2003: spermatogenesis), (Bobrov & Melikian 2006: seed anatomy, both testa and tegmen present?), Buchholz (1929: embryogeny), Butts and Buchholz (1940: cotyledon number), Hill and de Fraine (1908, 1909: seedlings), and Herrmann (1951: intergeneric grafting). A valuable resource is Gymnosperm Database (Earle 1997 onwards).
Phylogeny. Given the uncertainty in our knowledge of the relationships between the major seed-plant clades, direct links to Cycadales, Gnetales, Ginkgoales, and flowering plants are provided; for general discussion on relationships, see above and for more discussion about the immediate relatives of Gnetales, see the Gnetales page.
Within conifers, relationships are being substantially clarified. Pinaceae (Pinus, Cedrus, etc.) are sister to the rest, as a morphological cladistic analysis by Hart (1987) suggested some time ago (but c.f. Nixon et al. 1994; Doyle 1996b). Molecular data and additional morphological work largely confirm the relationships in the tree here, which is based on the work of Quinn et al. (2002: successive approximations weighting), see also Price et al. (1993), Tsumura et al. (1995: RFLP analysis, tree [unrooted] with the same topology as that used here), Kelch and Cranfill (2000), Gugerli et al. (2001: e.g. the mitochondrial nadI gene), Rai et al. (2002, especially 2008a), and, more recently, the four-gene analysis of Leslie et al. (2012) with its excellent sampling (but not Gnetum, etc.) and Ruhfel et al. (2014). However, the topologies in the scenarios of Biffin et al. (2010b) are either [Pinaceae [Podocarpaceae + Araucariaceae]] or [Pinaceae + Sciadopityaceae, etc.]... Gnetales are here included in Pinales (see discussion on Cycadales page).
For relationships in the Cephalotaxaceae-Taxaceae area, which for some time were rather uncertain, see below.
Classification. Producing evolutionary classifications, or classifications that emphasise one or two favored morphological characters, seems to remain popular with those working on conifers (e.g. Keng 1975; Melikian & Bobrov 2000; Fu et al. 2004 [Nageiaceae and Podocarpaceae well separated], Bobrov & Melikian 2006 [Araucariaceae and other conifers form a lineage quite distinct from Pinaceae and Sciadopityaceae]).
See Farjon (1990, 2005a, c) for detailed treatments of the conifers, Farjon (2001) for a checklist, and Christenhusz et al. (2011b) for a liner classification.
Includes Araucariaceae, Cupressaceae, Pinaceae, Podocarpaceae, Sciadopityaceae, Taxaceae.
Synonymy: Abietales Link, Actinostrobales Doweld, Araucariales Gorozh., Athrotaxidales Doweld, Cephalotaxales Reveal, Cunninghamiales Doweld, Cupressales Bromhead, Falcatifoliales Melikian & Bobrov, Metaxyales Doweld, Microstrobales Doweld & Reveal, Parasitaxales Melikian & Bobrov, Podocarpales Reveal, Saxegothaeales Doweld & Reveal, Sciadopityales Reveal, Taxales Knobloch, Taxodiales Heintze - Araucariidae Doweld, Cupressidae Doweld, Pinidae Cronquist, Takhtajan, & Zimmermann, Podocarpidae Doweld & Reveal, Taxidae Reveal - Araucariopsida A. V. C. F. Bobrov & Melikian, Pinopsida Burnett, Podocarpopsida Doweld & Reveal, Taxopsida Lotsy - Pinophytina Reveal
[GNETALES + PINALES]: tree branched; wood pycnoxylic; tracheid side wall pits with torus:margo construction, bordered; phloem fibres 0; axillary buds at at least some of the nodes; microsporangiophore/filament simple with terminal microsporangia; microsporangia abaxial, dehiscing by the action of the hypodermis [endothecium]; plastid ndh genes lost/pseudogenized.
Age. Davies et al. (2011: 95% credibility intervals) suggested an age for this clade of (259-)219(-174) m.y.; Magallón et al. (2013) suggested that it was about 312 m.y.o., while (259-)219(-174) m.y. is the age suggested by Clarke et al. (2011); the age of a [Gnetales + Pinales] clade is estimated at 181-140.1 m.y. (Naumann et al. 2013).
PINACEAE F. Rudolphi Back to Pinales
Plant (deciduous), ectomycorrhizal association +; specialized resin diterpenes, e.g. with abietane/pimarane skeletons, biflavonoids 0; xylem resin ducts +, inducible, (also constitutive); sieve cells with nacreous walls, sieve tube plastids also with protein fibres; phloem resin ducts +, constitutive or inducible; phloem fibres 0; sclereids with intracellular calcium oxalate crystals, etc.; axillary buds common, (producing short shoots, spur shoots), (plant deciduous); leaves with two vascular bundles; 2 microsporangia/microsporophyll, sporangia superficial, pollen saccate, exine thin [2³ µm] except distally; bracts free from the ovuliferous scale, ovules 2/bract scale, (pollination droplet 0); free-nuclear stage with only four nuclei [= embryo tetrad]; seeds 2/scale, dry, winged, wing terminal, developing from adaxial side of scale, (from integument; wingless); (integument with resin canals); cotyledons (2-)4-11(-20); n = 12 (13); plastid inverted repeat very small, ndh and rps16 genes lost/pseudogenes, PHYP gene duplicated; germination epigeal; (mitochondrial transmission maternal - Pinus).
11/231. North Temperate (map: from Florin 1963; Farjon 1984, 1990a). [Photos - Collection.]
Age. Magallón et al. (2013) suggested an age of (161.2-)153.8-153.1(-150.1) m.y. for crown Pinaceae, He et al. (2012) an age of around 237 m.y. ago. Various divergence estimates were provided by Gernandt et al. (2008), e.g. maximum dates of 271-173 m.y. (Jurassic) or 148-136 m.y.a., while around 175 m.y. is the estimate in Leslie et al. (2012); crown and stem ages of 100 and 263 m.y.a. respectively were suggested by Quirk et al. (2012).
1. Abietoideae Sweet
(Pollen with circular inflated frill - Tsuga); (mature female cones erect), (cones fall to bits); (germination hypogeal - Keteleeria); n = 22 - Pseudolarix).
5/64: Abies (48). North temperate to boreal, mountains, Central America, North Africa.
Age. He et al. (2012) suggested an age of ca 200 m.y. for the beginning of Abietoideae diversification.
2. Pinoideae W. Hochst.
(leaves in fascicles on short shoots - Pinus); (pollen smooth), (atectate, exine granular, shed during microgametophyte germination - Larix, Pseudotsuga).
5/167: Pinus (113), Picea (38). North temperate to Boreal, mountains, to West Malesia.
Age. An approximate age for crown-group Pinoideae is 155 m.y. (He et al. 2012).
Evolution. Divergence & Distribution. There are fossils identified as Pinaceae in ca 150 m.y.o. Upper Jurassic deposits (Rothwell et al. 2012; see also Miller 1999), while the recently-described Pinus yorkshirensis, a cone associated with needles in Lower Cretaceous deposits 131-129 m.y. old, forms a polytomy with extant and some other fossil species in morphological analyses (Ryberg et al. 2012). Cretaceous fossils ascribed to the genus have not yet been shown to nest within it (Klymiuk et al. 2011; Ryberg et al. 2011); fossils assigned to Pityostrobus are scattered through the family phylogeny (Ryberg et al. 2012).
Stem ages for Pinus are around 95 or 73 m.y.a. (B. Wang & Wang 2014), ca 126 m.y.a. (He et al. 2012), ca 140 m.y. (X.-Q. Wang et al. (2000), or ca 180 m.y. (Lockwood et al. 2013: Picea is sister). Although Naumann et al. (2013) date the Pinus/Picea split to around 33.1-29.3 m.y.a, dates in angiosperms were the focus of this study, it is clear that estimates for the age of Pinus are pretty much around the clock. A stem-group age for Pinus of (132-)128(-124) m.y. was suggested by Eckert and Hall (2006), while Crisp and Cook (2011) suggested a stem-group age (Pinus and Picea diverge) of around the K/T boundary ca 65 m.y. ago. Estimates in Gernandt et al. (2008) are ca 87-72 m.y. for crown Pinus, while others are much older, 165-148 m.y. ago. Willyard et al. (2007) estimated upper (permineralized wood) and lower dates for divergence of Pinus subgenera of 85 and 45 m.y. respectively (for the latter, see also Magallón & Sanderson 2005), although there were bouts of speciation much later. On the other hand, Millar (1998) suggested that Pinus subgenera Pinus and Strobus and some sections had separated by the middle of the Cretaceous. Crown-group Pinus is estimated to be (96-)89(-80) m.y.o. by He et al. (2012); the age of (80.1-)58.8(-45) m.y.o. was suggested by B. Wang and Wang (2014: some estimates older), with most BEAST crown-group ages for both subgenera being 22-20 m.y.a., although some are as much as 50 m.y. ago. For other divergence times within Pinaceae, see also X.-Q. Wang et al. (2000) and Lin et al. (2010).
For a disussion on the biogeography of the family, see X.-Q. Wang and Ran (2014). Pinus seems to have been a mid-latitude (30-50o N) plant in the Cretaceous, but in the warm Palaeocene and Eocene it retreated to higher latitudes, although also persisting near the equator. With the climatic deterioration of the Late Eocene-Oligocene, it moved back to mid latitudes while persisting at higher latitudes (Miller 1993). Indeed, in high latitude Canadian Eocene floras Pinaceae could be quite common (N. McIver & Basinger 1999). He at al. (2012) looked at the origin of fire-associated traits in Pinus, and found that thick bark characterised the whole genus, with its origin being somewhere between 126-89 m.y.a. (age spreads greater), while very thick bark, branch shedding and serotiny were common in subgenus Pinus, whose diversification was dated at (96-)89(-80) m.y.a; grass-like seedlings were uncommon (He at al. noted that thick bark and serotiny were found in a few other Pinales). Le Page (2003; see also X.-Q. Wang et al. 2000) thought that there was an episode of diversification in Pinaceae in the Palaeocene, while Lockwood et al. (2013) dated diversification of Picea to the middle Oligocene, only (37-)28(-21) m.y. ago. In Abies there is weak support for the Californian endemic A. bracteata being sister to the rest of the genus, and section Balsamea is apparently of hybrid origin; crown-group Abies is estimated to be (73.4-)48.6(-33.7) m.y.o. (Xiang et al. 2014).
Ecology & Physiology. For general information, see Andersson (2005) and especially Brodribb et al. (2012). Pinaceae dominate huge areas of mostly cool-temperate and boreal forests in the northern hemisphere where they are generally to be found on nutrient-poor soils, although in suitable conditions Pinus-dominated forests occur in Costa Rica (Janzen 1983) and even south of the equator in montane Sumatra (Map: from White et al. 2000; Andersson 2008: see also Clade Asymmetries). Pinaceae thrive in high-light conditions; they have high leaf mass per unit area and also a very high leaf area index, and although seedlings of evergreen angiosperms have a lower photosynthetic rate they tolerate leaf water stress better (Fu et al. 2012). Longevity of pine and spruce needles increases in colder, northern latitudes, and they may live for 12 years or more in Picea (Reich et al. 2014a). For the most part Pinaceae are unable to compete in tropical broad-leaved rain forests (but see the relatively broad-leaved Pinus krempfii: Brodribb & Feild 2008).
Many Pinaceae tolerate burning. Fires open the forest canopy, so making conditions suitable for Pinus in particular, many species of which are adapted to fire-prone environments (Brodribb et al. 2012; see also Schwilk & Ackerley 2001; Keeley 2012; Pausas 2015). He et al. (2012; see also Bond & Midgley 2012) thought that in Pinus thick bark resistant to low intensity fires and the shedding of dead lower branches that would tend to prevent crown fires evolved around (147-)126(-105) m.y.a.; this is the age of stem Pinus, so it assumes that evolution of these features occured as the genus split from the [Picea + Cathaya] clade. Very thick bark and serotinous cones are an ecological syndrome adapted to high intensity (crown) fires, and this syndrome is dated to (96-)89(-80) m.y.a., the age of crown-group Pinus (He at al. 2012). Juveniles, with their long and very dense needles covering the growing point (the grass stage), can also tolerate burning. Interestingly, although Pinus with lts long needles has relatively well-aerated and very flammable litter like that of many/most other gymnosperms, needles of many other Pinaceae are smaller and the litter is compact and much less flammable (Cornwell et al. 2015). When the phylogeny of Pinaceae settles down, one can start thinking about the evolution of this set of traits - small needles, non-flammable litter is probably derived, but what about the situation in Pinus? Aside from the issue of fire, wood of Pinaceae, as in other conifers, is broken down mostly by brown rot fungi. These fungi cannot degrade lignin, but readily break down cellulose and hemicellulose, leaving behind brown, crumbly detritus that is very rich in lignin and resistant to decay (Boddy & Watkinson 1995).
Estimates of live above-ground biomass in Pinaceae-dominated forests are in the order of 0.8-0.9x106 kg ha-1, Pseudotsuga menziesii perhaps even reaching 1.6x106 kg ha-1 (see Franklin & Dryness 1973). Figures for the total above + below ground carbon in boreal forests are about 505 PgC, ca 34.2 kgC m-2, and a mean turnover time of (45.4-)53.3(-73.4) years (Carvalhais et al. 2014: tables S1 and S2). The fraction of biomass in the foliage decreases with latitude, that in the root tends to increase, both changes connected with the increased longevity of the needles and associated low values of new leaves produced annually in far northern conifers (Reich et al. 2014a: p. 13705 has it backwards; see Reich 2014b: fig. 2). Accumulation of non-flammable litter under genera like Tsuga and Picea can be massive, and it can also protect the trees against ground fires, while accumulation of litter under Pinus, much more flammable, is less (Cornwell et al. 2015 and references).
Pinaceae, in North America species of Pinus and Tsuga in particular, can be very heavily infested by bark beetles, a variety of fungi, dwarf mistletoes, etc., that can have major negative effects on the plants, especially when they are stressed. The effects of these organisms are exacerbated by the tendency of the conifers to be locally so abundant, and there can be very extensive die-off; this is discussed further below under plant-animal interactions.
Some Pinaceae may have foliar bacterial endophytes that fix nitrogen (Carrell & Frank 2014).
For aging and the bristlecone pine, Pinus longaeva, see Munné-Bosch (2014 and references).
Pollination Biology & Seed Dispersal. See above, under the order. Doyle and O'Leary (1935b) described the distinctive pollination in Larix and Pseudotsuga where the pollen, which lacks sacci, lands on an almost stigmatic extension of the integument, the margins of which tend to inroll; pollen tubes develop only when the pollen is in contact with the nucellus (Larix), or contact is not needed (Pseudotsuga).
Pinaceae tend to show (weak) masting behaviour (Koenig & Knops 2000).
Plant-Animal Interactions. Ambrosia and bark beetles (Curculionidae-Scolytinae: see Wood 1982; Wood & Bright 1992; Six 2012), highly derived weevils, seem to have an ancestral association with conifers - although this is perhaps questionable (Jordal et al. 2011). Bark beetles, some 3,700 species, make their gallery systems in phloem, and members of genera like the North American Dendroctonus and the Northern Hemisphere Ips can be highly noxious pests, and a few invade living pines (e.g. Franceschi et al. 2005; Six 2012). Although the beetles tend to have relatively few hosts, outbreaks can be devastating, colonizing beetles being attracted to trees by pheromones produced by beetles that are already there (Kelley & Farrell 1998 for host specificty; Franceschi et al. 2005). Drought conditions may make the trees more susceptible to attack, but other factors must also be involved (Netherer et al. 2015). Many bark beetles are associated with blue-stain fungi, mostly ascomycetes such as the unrelated Ophiostoma and Ceratocystis as well as a few basidiomycetes, and these grow into the sapwood and help hasten the death of the infected tree (Franceschi et al. 2005).
Ambrosia beetles, some 3,400 species, mostly tunnel in dead or dying wood, although early-branching members of the ambrosia beetle clade may still live in phloem. They are haplodiploids that show parental care. Adults have intricate cuticular invaginations in which they carry a fungus inoculum, and the beetle larvae eat yeast-like bodies proliferating from these fungi in the galleries they make (Jordal et al. 2000; Cognato et al. 2011 and references). In those weevils that cultivate and eat fungi the mouth-parts are also much modified; development of cultivation is unreversed (Beaver 1989; Farrell et al. 2001; Jordal et al. 2008 and references, 2011). Not only beetles and fungi, but yeasts, bacteria (some nitrogen-fixing), parasitoids of the beetles and fungus-eating nematodes all form part of a very complex association (e.g. Rivera et al. 2009: yeasts and bark beetles). A very interesting association, but here angiosperm hosts are more common, the evolution of the ambrosia feeding habit, which happened 8 times or more, being associated with shifts to angiosperms (Six 201).
Some 70 species of Adelgidae (aphids) are restricted to Pinaceae, and include Adelges piceae and A. tsugae, serious introduced pests in North America, the wooly adelgid, Adelges tsugae, being a major pest of hemlock, Tsuga canadense (Havill et al. 2007). There are five different generations in a single life cycle, the sexual, gall-forming generation being on Picea; as with other aphids, vertically transmitted bacteria are part of this ecosystem (Havill & Foottit 2007). Cecidomyiid gall midges are quite common on the family in North America (Gagné 1989). See Powell et al. (1999) for other insect-conifer associations.
Details of the evolution of the resin defence system (e.g. Hudgins et al. 2004) depend on the phylogeny of the family, which is currently unclear (see below). However, Pinaceae do have a very well-developed resin defence system, yet they are more susceptible to beetle attack than are other conifers (e.g. Hudgins et al. 2004, see above). Keeling and Bohlmann (2006a esp., b) describe terpenoid diversity and conifer defence mechanisms, a complex subject; it is unclear just what is responsible for the considerable diversity of terpenoids in conifers, although multisubstrate and multifunctional enzymes involved in terpenoid synthesis in Picea sitchensis (Sitka Spruce) could produce a variety of products from a variety of substrates (Hamberger et al. 2011). Iason et al. (2011) tested monoterpenes for protection against herbivory by capercaillie, bank voles, slugs, or red deer; some, but not all, worked (see also Hamberger et al. 2011: defensive properties of diterpene resin acids). Pine needle phenolics and pine stem resins are constitutively more abundant in Nearctic than in Palaearctic Pinus, but there was no differernce between the two groups in how inducible these defences were (Carrillo-Gavilán et al. 2014: seedlings examined). Mumm and Hilker (2006) discuss the chemical defence of pines against foliovores in particular; for conifer exudates, see Lambert et al. (2007a).
Most species of the dwarf mistletoe Arceuthobium (Santalaceae-Visceae) parasitize Pinaceae, with a few species also growing on Juniperus, in Cupressaceae (Farjon 2008); they can be serious pests of Pinus in particular (Unger 1992).
Bacterial/Fungal Associations. Ectomycorrhizal associations are particularly common in Pinaceae, and appropriate ECM fungi may have to be introduced if Pinus, for instance, is to be grown successfully. Crown group ages for the origins of ECM clades of Agaricales were split about equally between the Late Cretaceous and Eocene, and for nearly all a Jurassic origin could be rejected; Pinaceae-associated fungi were linked with both the Eocene and the Late Cretaceous dates (Ryberg & Matheny 2012). The ECM \sebacina clade in Sebacinales seems to have evolved on North American temperate Pinaceae (87-)57, 45(-30) m.y.a. (Tedersoo et al. 2014a: stem and crown fungal ages). However, many estimates suggest that Pinaceae had begun diverging long before then (see above). Given current uncertainties over details of crown Pinaceae diversification, the relation between the evolution of ECM fungi and Pinaceae remains unclear. Furthermore, Pinus and Larix in particular may also form ectendomycorrhizal associations with an ascomycete (Peterson 2013).
Bacteria associated with a particular kind of ECM on P. contorta, tuberculate ECM, a cluster of root tips surrounded by hyphae (see ectendomycorrhizae above), are thought to fix nitrogen (Paul et al. 2007). Laccaria bicolor, a brown rot fungus, was found to take up nitrogen from springtails that it had first immobilized, and this nitrogen could be transferred to seedlings of Pinus strobus (Klironomos & Hart 2001).
A number of rusts, including those on ferns, have their aecial stages on Pinales, especially Pinaceae (Savile 1979b; Durrieu 1980). These include the white pine blister rust, Cronartium ribicola (alternate host Ribes, Grossulariaceae), a serious pathogen of white pine and its relatives.
In Pinus strobus endophytes synthesize antifungal metabolites, effective against Microbotryum violaceum, parasitic on some Caryophyllaceae (Sumarah et al. 2010, 2011), and endophyte metabolites in spruce may be toxic to insects (Findlay et al. 2003).
Genes & Genomes. For chloroplast genome rearrangements, notably extensive here, see Lin et al. (2010) and C.-S Wu et al. (2011a); the inverted repeat may be very much reduced in size in genera scattered throughout the famly (Jansen & Ruhlmann 2012 for references). Mitochondrial transmission is maternal in Pinus (Neale & Sederoff 1989; X.-R. Wang 1996); B. Wang and Wang (2014) discuss the complex history of mitochondrial inheritance in the genus.
Economic Importance. The majority of the world's lumber comes from softwood, and the majority of that comes from members of Pinaceae [?details].
Chemistry, Morphology, etc. Schultz (1990) notes that there are no phloem fibres in Pinaceae. Pinus cuticular wax tubules look almost scalloped (c.f. commelinids!), but this is because the tubules are densely aggregated (Wilhelmi & Barthlott 1997). For the anatomy of Pinus needles, see Dörken and Stützel (2012); needles of subgenus Pinus are often described as having two vascular bundles, but there is a single vascular bundles with two parts separated by a parenchymatic band, the whole being surrounded by a common bundle sheath. Adult plants of Pinus have scale leaves alone on their long shoots; seedings may bear needles directly on long shoots.Mathews and Tremonte (2012: greening of seedlings in the dark)
The seed coat of Cedrus is vascularized. The seed wing of Pinaceae is derived from the middle or stony layer of the integument. Cleavage polyembryony is common, as is true polyembryony (more than one archegonium is formed), but the seed generally contains only a single embryo.
For Pinus, see e.g. Mirov (1967: monograph), Richardson (1998: ecology and biogeography), and Farjon (2005a: monograph); for other Pinaceae, see Farjon (1990: general). For aspects of ovuliferous cone morphology and anatomy, see Hu et al. (1989), Napp-Zinn and Hu (1989), and Gernandt et al. (2011), for the embryo, see Buchholz (1931), for seed coat development, see Owens and Smith (1964), and for general information, see the Gymnosperm Database. Esteban and de Palacios (2009) and Esteban et al. (2009) describe the wood anatomy of Abietoideae, and Braukmann et al. (2009) chart the extent of the loss of the ndh gene (see also Hirao et al. 2008).
Phylogeny. Relationships within Pinaceae are unclear and have depended on the kind of data analysed (morphology, molecules) and methods of analysis (parsimony, Bayesian) - see Tsumura et al. (1995), Wang et al. (2000), Rydin and Källersjö (2002), Liston et al. (2006b), and Gernandt et al. (2008). Studying the mitochondrial rps3 gene, Ran et al. (2010) found that Larix and Pseudotsuga were sister to all other Pinaceae. However, the main problem is the position of Cedrus with respect to Abietoideae (Abies, Keteleeria, Nothotsuga, Pseudolarix, Tsuga) and Pinoideae (Cathaya, Larix, Picea, Pinus, Pseudotsuga) (Holman et al. 2010). Thus Wang et al. (2000) placed Cedrus sister to the rest of the family, Gernandt et al. (2008) as sister to Abietoideae (see also C. Hou et al. 2015), while Liu et al. (2010) retrieved the clade [Cedrus [Abies + Keteleeria]] as sister to the rest of the family, although Tsuga and Pseudolarix were not sampled; Cathaya and Pinus formed a clade. Holman et al. (2010) nicely summarize the morphological evidence that is compatible with the relationship of Cedrus to either of those groups, or as sister to the whole family.
In a study with exhaustive sampling of conventional Pinaceae and all other Pinales except for Gnetum, etc., Leslie et al. (2012) found the set of relationships [[Cedrus [Pseudolarix [Nothotsuga + Tsuga]] [Abies + Keteleeria]] [[Pseudotsuga + Larix] [Pinus [Cathaya + Picea]]]. The same two major groups were recovered by Lockwood et al. (2013), although major groupings were not the focus of that study and details of relationships within the two groups differed; see also He et al. (2012), Ruhfel et al. (2014), and C. Hou et al. (2015).
For the phylogeny of Pinus, see Syring et al. (2005), Gernandt et al. (2005, 2011), and Eckert and Hall (2006). Pinus has two subgenera (see Gernandt et al. 2005 for an infrageneric classification). Leaves of subgenus Pinus, the hard pines, apparently have two vascular bundles (but see above), plesiomorphic, while those of subgenus Strobus, the soft pines, have but a single bundle. Analysis of nuclear ITS variation was largely uninformative in suggesting relationships between sections in Abies, but at lower levels was more useful (Xiang et al. 2009); in a more extensive study (genes from all three compartments), Xiang et al. (2014) largely resolved relationships in the genus. Lockwood et al. (2013) provide a detailed phylogeny of Picea, sister to Pinus.
Classification. If the topology suggested by Leslie et al. (2012) holds up, a two subfamily classification, Abietoideae and Pinoideae, the subfamilies being the two major clades recognized there, is reasonable (see above).
Botanical Trivia Living up to 4,700 years or more, the bristlecone pine, Pinus longaeva, is the longest-living non-clonal seed plant (Munné-Bosch 2014 and references); its needles, which can live for some 40 years (Wikipedia), are the longest-lived leaves of all land plants except Welwitschia.
Synonymy: Abietaceae Gray, Cedraceae Vest, Piceaceae Gorozh.
[[Araucariaceae + Podocarpaceae] [Sciadopityaceae [Cupressaceae + Taxaceae]]] / Cupressophytes: highly oxygenated diterpenes with phenolic rings [phenolic abietanes]; xylem resin ducts +, (constitutive), (inducible); phloem resin ducts 0, calcium oxalate crystals numerous, extracellular, in wall, phloem fibres stratified, sclereids 0; (leaves opposite, sometimes then with two vascular traces); pollen grains atectate, exine granular; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial nadI gene intron 2 and both rps3 introns lost, duplication in the PHYN clade.
Age. Magallón et al. (2013: with temporal constraints) suggested an age of around (276.6-)259-256.9(-244.4) m.y. and Won and Renner (2006) an age of (303-)273(-243) m.y. for this node.
Evolution. Divergence & Distribution. For other possible synapomorphies of this group, see Hart (1987). Isoflavonoids are known from Cupressaceae, Podocarpaceae and Araucariaceae (Reynaud et al. 2005).
Ecology & Physiology. This node is distinctive in having low leaf nitrogen, extant gymnosperms as a whole already having a relatively high ratio of leaf mass per area (Cornwell et al. 2014).
Pollination Biology & Seed Dispersal. The combination of dry fruits and dioecy has evolved several times in members of this clade growing in the southern hemisphere (Leslie et al. 2013).
Genes & Genomes. For mitochondrial genes, especially the rps3 gene, see Ran et al. (2010).
Chemistry, Morphology, etc. For southern conifers, in part this clade, see Hill and Brodribb (1998: general) and Cox et al. (2007: oxygenated di- and tricyclic terpenoids.
[Araucariaceae + Podocarpaceae]: gums +; roots with endomycorrhizal nodules; prothallial cells divide; ovule one/bract scale; proembryo with 5 or 6 free-nuclear divisions; 2nd intron in nad1 gene lost.
Age. The age of this node has been estimated at (287-)257(-228) m.y. (Won & Renner 2006), (318-)263(-223) and (255-)198, 177(-157) m.y. (Biffin et al. 2010b), (237-)205(-177) m.y. (Biffin et al. 2011b: text, c.f. fig. 2), 230-176 m.y. (Leslie et al. 2012), or around 243 m.y. (Magallón et al. 2013).
Chemistry, Morphology, etc. Chamberlain (1935) notes that there is no stalk cell per se in the male gametophyte, but when the generative cell divides, one of the cells dies, the other divides and produces the gametes.
ARAUCARIACEAE Henkel & W. Hochst. Back to Pinales
Branches whorled, plagiotropic, branchlets frequently abscised as units [cladoptosis]; stem apex with tunica/corpus construction; phloem fibres scattered; only resin plugs present in vascular tissue; pits on radial walls of tracheids touching, hexagonal in outline; single leaf trace branching profusely in the cortex; stomata tetracytic, usu. traversely oriented; leaves multiveined, axillary meristems present on the trunk, undifferentiated, submerged by cork, persistent; (plants dioecious); to 20 microsporangia/microsporophyll; pollen not saccate; tapetum amoeboid [Araucaria]; bract and ovulate scales fused (not in Araucaria); pollination droplet 0, nucellus protrudes from micropyle [?Araucaria]; pollen germinates on ovuliferous scale and tubes grow over the scales, prothallial cells numerous; seeds winged, wing developing from the entire bract scale (wingless); free nuclear stage in proembryo many nucleate, central, embryonal cells surrounded by cap cells that degenerate; cotyledons (4 - some Araucaria), with (3-)4-8 vascular bundles [?Agathis]; (germination cryptocotylar).
3/33. Southern South America, Malesia to E. Australia and New Zealand (map: from Florin 1963; de Laubenfels 1988; Cretaceous and Jurassic fossils, green, from Sequiera & Farrell 2001). [Photos - Collection.]
Age. Divergence of Wollemia from other Araucariaceae has been dated to a mere (37-)18(-younger) m.y.a. (Crisp & Cook 2011); on the other hand, Leslie et al. (2012) dated the divergence of Araucaria from the [Wollemia + Agathis] clade to 185-165 m.y. - or perhaps 205 m.y. (see also Stöckler et al. 2002; Wallis & Trewick 2009), Kunzmann (2007) put the divergence of Agathis and Wollemia at at least 110 m.y.a., and Biffin et al. (2010b) suggest ages of (215-)191(-169) or (94-)65(-47) m.y.; 225-185 m.y. is the estimate in Knapp et al. (2007) and 172-162 m.y. in Wilf and Escapa (2014, q.v. for other dates). Dating here is in more than its normal mess.
Araucariaceae are well known as fossils from the Mid Jurassic (ca 175 m.y.a.) onwards. Araucaria in particular is found in even older Triassic deposits in many parts of the world in both hemispheres; the remarkably preserved A. mirabilis has been associated with the monotypic section Bunya (Florin 1963; Stockey 1982, 1994; Hill & Brodribb 1989; Kunzmann 2007). However, identification of Araucarioxylon wood can be difficult (Ash & Creber 2000).
Evolution. Divergence & Distribution. Biffin et al. (2010b, esp. 2011b) noted that stem-group calibration scenarios make crown-group divergence of Araucariaceae largely a (mid-Cretaceous to) Caenozoic phenomenon (see also Crisp & Cook 2011). This would both question the placement of these early fossils in extant sections and the long-term persistence of Agathis in New Zealand since the Eocene or before. Knapp et al. (2007) also discuss this possible persistence; although many floristic elements in the island that are known fossil there in the Oligocene-Miocene subsequently became extinct, their contemporary representatives being relatively recent immigrants (e.g. Jordan et al. 2010; Puente-Lelièvre et al. 2012), the distinctive frog Leiopelma, for example, seems to represent an ancient lineage on the islands (Carr et al. 2015).
The current southern distribution of Araucaria is best interpreted as a relict of a much more widespread range (Stockey 1982; Hill & Brodribb 1989; Kunzmann 2007; Givnish & Renner 2004 for discussion). Although Araucaria is diverse on New Caledonia, there is little genetic divergence between the species, suggesting that divergence there is recent (Gaudeul et al. 2012). Agathis was until recently thought to be Australian, but well-preserved and abundant fossils have turned up in Patagonian Eocene deposits about 52.2 m.y.; they were previously identified as Zamia (Wilf et al. 2014).
The quite recent discovery very close to Sydney of a few trees of the remarkable Wollemia, very similar to some fossil Araucariaceae (Jones et al. 1995; see e.g. Pastoriza-Piñol 2007 for a general account), occasioned some excitement. However, if Wollemia diverged from other Araucariaceae less than 37 m.y.a. (Crisp & Cook 2011), comparison of Wollemia with these Cretaceous fossils may be inappropriate (c.f. Chambers et al. 1998).
For possible apomorphies, perhaps including "dehiscent" seeds (i.e. seeds separating from the cone-scale), see Cantrill and Raine (2006) and Escapa and Catalano 2013: most quantitative).
Pollination Biology. The time from pollination to fertilization in Agathis australis is about twelve months, although this includes three months after pollination before the pollen grain germinates, and then another three months over winter when nothing much happens (Owens et al. 1995b). The pollen grains do not rupture when placed in water (Tomlinson 1994).
Plant-Animal Interactions. Sequeira and Farrell (2001) suggested that the association between Araucaria and the scolytine Tomicini bark beetles is probably Cretaceous in age; the beetles seem to have moved on to Araucaria from angiosperms, and from thence moved on to Pinaceae. García Massini et al. (2011) found evidence of wood-boring beetles, fungi, and mites in fossilized araucarian wood of Middle Jurassic age from Argentinian Patagonia.
Caterpillars of Agathiphagoidea, a small group of near-basal jawed lepidoptera, eat seeds of Agathis, and they are known from Australia to the Pacific (Shields 1988; Powell et al. 1998). They diverged from the Nothofagus-eating Heterobathmioidea as much as 158.5 m.y.a. (Wahlberg et al. 2013).
Chemistry, Morphology, etc. For the essential oils of Wollemia, see Staniek et al. (2010 and references), and for a possible taxol-producing endophyte, see Strobel et al. (1997).
Tomlinson (2008) noted that the axillary branches of Wollemia are evident in the resting terminal bud, but do not grow out until extension growth of the latter starts; there are undifferentiated resting meristems in the axils of the leaves of the main axis which develop if the apical meristem is destroyed (Tomlinson & Huggett (2011). The single leaf trace divides into three or more as it proceeds into the leaf (Tomlinson 2008; Tomlinson & Murch 2009), and this is connected with branch shedding or cladoptosis (Looy 2013 and references). Araucariaceae also have platelet structures in their cuticular waxes (Wilhelmi & Barthlott 1997); the stomata of Araucaria have a wax plug which may block penetration of fungal hyphae (Mohammadian et al. 2009 - see also Winteraceae).
Cones of Araucaria have a "ligule" that is more or less adnate to the ovule.
For general information, see Stockey (1982), Bieleski and Wilcox (2009), Gee and Tidwell (2010: literature from late Triasssic to end Cretaceous), and especially the Gymnosperm Database, for comparative anatomy, see Thompson (1913), for axillary buds, see Burrows (1999 and references, 2009), for details of reproductive biology compared with those of other Pinales, see Owens et al. (1995a, b, c), for pollen morphology, see Dettmann and Jarzen (2000), and for phylogeny, see Setoguchi et al. (1998).
Phylogeny. Wollemia has been placed variously sister to Agathis or sister to the rest of the family (Jones et al. 1995; Gilmore & Hill 1997; Setoguchi et al. 1998; S. S. Renner in Kunzmann 2007), the particular position being sensitive to the choice of outgroups (Knapp et al. 2007). A [Wollemia + Agathis] clade was retrieved in the comprehensive four-gene tree in Leslie et al. (2012) and by Escapa and Catalano (2013); cladoptosis is particularly striking here (Looy 2013).
For a comprehensive phylogeny of Araucariaceae, with synapomorphies for the various clades, etc., see Escapa and Catalano (2013).
PODOCARPACEAE Endlicher Back to Pinales
Podocarpic acid + [particular diterpene with phenolic ring]; (positive Maüle reaction); (nodes 1:2); sclereids numerous, with large lumen; transfusion tissue in patches lateral to vascular bundles in leaf, laterally-elongated sclereids in middle of lamina; (leaves opposite [Microcachrys]; plants dioecious (monoecious); microsporophylls with two sporangia; pollen exine thin, except distally; male gametophytes with 3-6(-8) prothallial cells, sperm nuclei unequal in size (one extruded); ovule ± inverted; proembryo [E tier] cells binucleate; polyembryony common; cotyledon with two vascular bundles [?all]; 2C genome size 8-18 pg (-27.7 pg - Manaoa colensoi).
Age. This clade (Phyllocladus + Podocarpus] is ca 102 m.y.o. (Magallón et al. 2013); estimates are substantially older, (194-)145(-99) m.y., in Biffin et al. (2011b: c.f. topology, also Fig. 2).
Fossil Podocarpaceae (as Rissikia) are known from the Middle Triassic of Antarctica ca 225 m.y.a., although the material has since been lost (apparently the fossils had 2 ovules/scale, see also Saxegothaea: Townrow 1967; Eckert & Hall 2006; Axsmith et al. 1998; Biffin et al. 2011b: Suppl. 4; Rothwell et al. 2012). Distinctive podocarp root nodules are known from very well-preserved fossils from the Early Triassic, ca 240 m.y.a. (Schwendemann et al. 2008, esp. 2011).
1. Saxegothaea Lindley
Plants monoecious; pollen not saccate; pollination droplet 0; two ovules/scale, nucellus protrudes from micropyle; pollen germinates on ovuliferous scale and tubes grow over the scales; n = 12.
1/1: Saxegothaea conspicua. South Chile and Argentina.
Synonymy: Saxegothaeaceae Doweld & Reveal
2. The Rest.
(Leaves broad, with transfusion tissue), (multiveined - Nageia); plants dioecious (monoecious); (pollen not saccate - Phyllocladus), exine alveolate; ovulate scales not aggregated into cones (yes - Microcachrys), ± reduced, fused with ovule, ± enveloping ovule [looking like an integument]; (ovule erect); ovular scale fleshy [= epimatium], fleshy (not); n = (9 - Phyllocladus)10(-13, 15-19).
16/185: Podocarpus (107), Dacrydium (20). Largely southern Hemisphere, scattered, N. to Japan, Central America and the Caribean (map: from Florin 1963; Dalling et al. 2011; Adie et al. 2011). [Photos - Collection, Phyllocladus trichomanoides, Phyllocladus megasporangia, microsporangia.]
Evolution. Divergence & Distribution. Although Podocarpaceae are still quite common and may dominate the vegetation, they are largely restricted to the southern hemisphere, and are well known as fossils from Antarctica; for their biogeography, see Mill (2003). However, there are well-substantiated reports of members of the family from the northern hemisphere in the Cretaceous and Early Caenozoic (Greenwood et al. 2013 and references).
Extant Podocarpaceae with broad leaves are shade tolerant and prefer warmer and higher rainfall conditions (c.f. Cupressaceae and other Podocarpaceae with narrower, imbricate leaves), and as Australia dried out during the Caenozoic, podocarps became less common there (e.g. Brodribb & Hill 1997, 2004; Biffin et al. 2011b). Diversification in clades whose members have imbricate leaves began in the Late Jurassic ca 150 m.y.a. (Biffin et al. 2011b); diversification in clades whose members have flattened foliage is notably greater, but younger, and is dated to (94-)64(-38) m.y.a. (c.f. Biffin & Lowe 2011; Biffin et al. 2011b; Brodribb & Feild 2010). Leslie et al. (2012) offer other dates for splits within Podocarpaceae. Dacrydium may have moved into South East Asia via the Ninety East Ridge and India (Morley 2011).
Ecology & Physiology. Podocarps are slow-growing, long-lived, light-demanding specialists that often grow in nutrient-poor soils, but are mostly poorly adapted to dessication stress; they can be dominants or emergents in southern forests (Brodribb 2011; Coomes & Bellingham 2011). Their leaves decompose only slowly (although there are few studies on this), carbon/lignin build up in the soil, nutrients are sequestered, and soil fertility is further reduced (Wardle et al. 2008); they have been described as ecosystem engineers because of this combination of features (Coomes & Bellingham 2011).
There are often root nodules in Podocarpaceae. The roots involved tend to be superficial, and the nodules may be in longitudinal rows and represent modified lateral roots (Becking 1965; Duhoux et al. 2001). The fungus Glomus is involved, and nitrogen does not seem to be fixed (Russell et al. 2002), however, the function of these nodules is poorly understood (Dickie & Holdaway 2011).
Biffin and Lowe (2011, see also Biffin et al. 2011b) suggest that podocarps with broad leaves or functionally equivalent structures like the phylloclades of Phyllocladus evolved about four to six times. This has been dated to a time slightly after the venation density of angiosperm leaves increased - (94-)64(-38) versus 109-60 m.y.a.. These broad-leaved podocarps are now largely meso-megathermal shade-tolerant plants (high rates of transitions from microthermal) while the imbricate-leaved taxa are mostly microthermal (high rates of transitions from meso-megathermal: Biffin & Lowe 2011; Biffin et al. 2011b; Brodribb & Feild 2010). Fossils with apparent affinities to podocarps and with broad leaves are also known from the Triassic and Jurassic (Biffin et al. 2011b).
The New Caledonian Parasitaxus usta is hemiparasitic on the roots of Falcatifolium taxoides, another podocarp, where it taps the xylem and from which it obtains water and nutrients (the stomata of Parasitaxus are insensitive to light), and is also a myco-heterotroph, obtaining carbon from an ?ectomycorrhizal fungus that is also associated with its host and whose hyphae grow through the vascular systems of both host and parasite (Woltz et al. 1994; Feild & Brodribb 2005).
Pollination Biology & Seed Dispersal. There is a correlation between the absence of pollen wings and the shedding of the pollen exine when the microgametophyte germinates. In Phyllocladus, which has erect ovules, the pollination droplet is actively resorbed (see Tomlinson et al. 1991, esp. 1997: useful comparisons; Rydin & Friis 2005). For pollen tube growth in Saxegothaea, see Doyle and O'Leary (1935a).
Vegetative Variation. Phyllocladus has phylloclades, flattened, photosynthetic stems; these bear highly reduced, scale-like leaves which may lack leaf gaps, and it is in the axils of these leaves that the reproductive structures are found. The seedling has more conventional needle-like leaves. The foliar units of podocarps with flattened foliage units, whether leaves or phylloclades, have transfusion tissue or there are several veins, unlike the single vein and absence of transfusion tissue in the leaves of other podocarps (Biffin et al. 2011b).
Genes & Genomes. Quinn et al. (2002) noted a tendency to dysploid chromosome evolution in the group.
Chemistry, Morphology, etc. For secondary metabolites in Podocarpus s.l., see Abdillahi et al. (2010); taxol has been found in Afrocarpus gracilior (fungi involved here, too?). Accessory transfusion tissue extends to the lamina margin in Podocarpus macrophyllus and a number of other species of the genus (Gifford & Foster 1989); Knopf et al. (2012) provide many details of foliar anatomy for the whole group.
The pollen of Phyllocladus has often been described as having a wing (e.g. Singh 1978), but a wing seems to be absent. The morphological nature of the epimatium has occasioned some controversy. Chamberlain (1935) interpreted it as possibly being equivalent to the ovuliferous scale (see also Tomlinson & Takaso 2002; Englund et al. 2011 [similarity confirmed by gene expression data]), and functionally, perhaps, it can be considered equivalent to the second integument of an angiosperm ovule - hence the anatropy of the ovules here (Endress 2011b). Phyllocladus is sometimes described as having an aril, although this is more probably a somewhat reduced and retarded epimatium (de Laubenfels 1988). Although the single ovules of most Podocarpaceae do seem very different from the multiovulate cones of most other Pinales, Lower Cretaceous podocarps with more conventional bract-scale complexes, as in the extant Saxegothaea, have been described (X. Wang et al. 2008). For details of embryogeny, see Buchholz (1941), and for nucleus number in the E-tier cells, see also Quinn (1986). Clevage and true polyembryony are common in Podocarpaceae, indeed, embryos seem able to develop from almost any cell of the early embryo (Buchholz 1941; for polyembryony, see also Doyle and Brennan (1972: integrate this character better).
For cuticle morphology, see Mills and Schilling (2009), for wood anatomy, see Woltz et al. (2009 and references), for Podocarpus, see Mill (2014: summary of literature), Phyllocladus, see Quinn (1986: embryogeny) and Tomlinson et al. (1989: cone, etc.). For general information, see Turner and Cernusak (2011: Smithsonian Contrib. Bot. 95. 2011), and the Gymnosperm Database.
Phylogeny. For phylogeny, see also Kelch (1998), a comparison of morphology and molecules. RbcL analyses (Conran et al. 2000; Wagstaff 2004b) tended to place Phyllocladus within Podocarpaceae, other analyses, whether (Quinn et al. 2002) or not (Sinclair et al. 2002) including rbcL sequences, placed the two as sister groups. Inclusion in Podocarpaceae is likely, as in Peery et al. (2008: nuclear XDH gene), and it was in the small prumnopityoid clade in the combined analysis of Knopf et al. (2012: support in/for this clade not strong in single gene analyses; see also Biffin et al. 2011a, b). Other groupings of genera are becoming evident (Kelch et al. 2010), including the dacrydioid and podocarpoid clades (Knopf et al. 2012). The closest relatives of Parasitaxus are Lagarostrobus and Manoao, from Tasmania and New Zealand - [Parasitaxus [Lagarostrobus + Manoao]] (Sinclair et al. 2002; Rai et al. 2009; Lam et al. 2009). Saxegothaea has some support as being sister to all the rest of the family (Knopf et al. 2012, but c.f. Biffin et al. 2011a, b: sister to [Microcachrys [Pherosphaera [Acomopyle + ...]]]; Leslie et al. 2012), and this has considerable implications for character evolution in the clade; as Mabberley (2007) noted, the plant does have some features reminiscent of Araucariaceae. For relationships within Podocarpus, see Biffin et al. (2011, 2012).
Classification. Phyllocladus has long been considered very distinctive, so distinctive that it has sometimes been separated from all other conifers (e.g. Keng 1974, 1979).
Synonymy: Acmopylaceae Melikian & A. V. Bobrov, Bracteocarpaceae Melikian & A. V. Bobrov, Dacrycarpaceae Melikian & A. V. Bobrov, Falcatifoliaceae Melikian & A. V. Bobrov, Halocarpaceae Melikian & A. V. Bobrov, Lepidothamnaceae Melikian & A. V. Bobrov, Microcachrydaceae Doweld & Reveal, Microstrobaceae Doweld & Reveal, Nageiaceae D. Z. Fu, Parasitaxaceae Melikian & A. V. Bobrov, Pherosphaeraceae Nakai, Phyllocladaceae Bessey, Prumnopityaceae Melikian & A. V. Bobrov
[Sciadopityaceae [Cupressaceae + Taxaceae]]: pollen without sacci; ovule orientation various; pollen exine shed on microgametophyte germination [microgametophyte naked]; ovule with pollination droplet; prothallial cells 0; seed wing developing from the integument, narrow.
Age. Leslie et al. (2012) estimate an age for this node of over 250 m.y., some time in the late Permian.
Chemistry, Morphology, etc. The pollen grains expand and rupture when placed in water (Tomlinson 1994), and the intine-clad pollen, although sometimes much larger than the pollen grain itself, may deform more easily and so be tranferred along the narrow micropylar canal (Takaso & Owens 2008). Whether or not all taxa have male gametes each surrounded by cell walls needs to be confirmed (see Singh 1978).
SCIADOPITYACEAE Luersson Back to Pinales
Roots with endomycorrhizal nodules; leaves on long shoots reduced to scales, branchlets deciduous [= short shoots]; subsidiary cells 8-12/stoma; short shoots +, with a pair of connate needles, apically bifid (not); pollen cones in clusters/pseudowhorls; microsporophyll with flattened apical expansion, (1-)2 microsporangia/microsporophyll; pollen inaperturate, surface microtuberculate (microechinate), exine granules confluent by sporopollenin deposition; sterile cell?; ovules (1-)7-9(-12)/bract scale, ovuliferous scales ± connate, pollen chamber?; seeds (1-)7-9(-12)/scale; n = 10.
1/1: Sciadopitys verticillata. C. and S. Japan (map: from Florin 1963). [Sciadopitys Photos - Collection]
Evolution. Divergence & Distribution. Fossils of Sciadopitys are known since the Upper Cretaceous, but apart from material from Japan and the Upper Pliocene of Germany, the identities of many are questionable (Stockey et al. 2005).
Chemistry, Morphology, etc. There has been much debate over whether the photosynthesising structures ofSciadopitys are some kind of phylloclade - perhaps formed by the connation of two leaves - or cladodes, basically stem structures. The two vascular bundles, each with its own endodermis, tend to have have abaxial xylem and adaxial phloem, a rather odd arrangement. Sporne (1965) noted that on occasion branches develop from these leafy structures, so perhaps favoring the cladode hypothesis (see also Farjon 2005c). However, Dörken and Stützel (2011) examined probably only the second known case of intermediate structures, and consider the photosynthesizing structures to be two congenitally connate needle leaves, the orientation of the vascular tissue resulting from the relation of the leaves to the axis that bore them (see also Dörken & Stützel 2012).
For pollen, see Page (1990) and Uehara and Saichi (2011), for a monograph, see Farjon (2005c), and for general information, see the Gymnosperm Database.
[Cupressaceae + Taxaceae]: subsidiary cells 4-7/stoma; microsporangia hypodermal in origin.
Age. Leslie et al. (2012) estimate that these two families diverged 217-197 m.y.a., Mao et al. (2012) offer an age of (293-)245, 242(-194) m.y., while estimates in Yang et al. (2012) are 217-197 m.y. (or perhaps 237 m.y.), in Won and Renner (2006) they are (265-)227(-189) m.y., while in Magallón et al. (2013) they are ca 175.4 m. years.
Chemistry, Morphology, etc. Cunninghamia and Taxus had by far the thickest roots (roots developing after root pruning) of the fourteen species of seed plants examined (B. Liu et al. 2015). Burrows (2009) noted that axillary buds occur in several members of this clade, but they were superficial and so did not form shoots in older branches - c.f. Araucariaceae.
Gene expression studies suggest little in common between the scaly structures of the Cupressaceae cones studied and the arils of Taxus with the ovuliferous scales of Pinaceae... (Englund et al. 2011; Groth et al. 2011).
CUPRESSACEAE Bartling Back to Pinales
(Stem apex with tunica/corpus construction); xylem or phloem resin ducts inducible [in separate clades]); branchlets deciduous; foliar vascular bundle single, abaxial to vascular bundle; leaves ± amphistomatic, awl-shaped, with acuminate tip, shed along with branches; (plant dioecious); pollen cones in clusters/pseudowhorls; (1-)2-10(-14) microsporangia/microsporophyll; pollen shed at 2-cell stage, surface microverrucate; ovules becoming inverted; male gametophyte without sterile cell, gametes with separate cell walls; n = 11.
30/133. Esp. Northern Hemisphere, more scattered in south temperate regions. [Photos - Collection.]
Age. Mao et al. (2012) offer an age of (259-)219, 211(-168) m.y. for crown Cupressaceae, while estimates in Yang et al. (2012) are (231-)229, 197(-186) m. years.
1. Cunninghamioideae Silba
Leaves twisted at the base, (margin denticulate); 3(-6) microsporangia/microsporophyll; ovules 2-3(-6)/bract scale, ovuliferous scale small [<1/3 length of cone scale], free, initially 3-lobed, later with (0) 1, 3 tips.
1/2. Eastern Asia (map: from Farjon & Filer 2013).
Synonymy: Cunninghamiaceae Siebold & Zuccarini
2. The Rest.
Leaves (opposite - Cupressus, etc., and nodes 1:2), shape various, (twisted at the base); (plant dioecious); pollen cones often on elongated axes; (1-)2-10(-14) microsporangia/microsporophyll; pollen shed at 2-cell stage, surface microverrucate; (cone scales opposite), (bract scale fleshy - Juniperus; with adaxial development), ovuliferous scales none (stout protuberance), ovules 1-9(-many)/bract scale, (erect); male gametophyte without sterile cell, gametes with separate cell walls; seeds (in axil of bract scale), (not winged from integument); (cotyledons -9(-15)); n = 11.
29/131: Juniperus (67), Callitropsis (18), Callitris (14), Cupressus (12). Esp. Northern Hemisphere, more scattered in south temperate regions, also N.E. Africa; individual genera are from either Northern or Southern Hemispheres (map: from Florin 1963, 1966; Farjon 2005c). [Photos - Collection.]
Synonymy: Actinostrobaceae Lotsy, Arceuthidaceae A. V. Bobrov & Melikian, Arthrotaxidaceae Doweld, Callitridaceae Seward, Cryptomeriaceae Gorozh., Diselmaceae A. V. Bobrov & Melikian, Fitzroyaceae A. V. Bobrov & Melikian, Juniperaceae Berchtold & J. Presl, Libocedraceae Doweld, Limnopityaceae Hayata, Metasequoiaceae Hu & W. C. Cheng, Microbiotaceae Nakai, Neocallitropsidaceae Doweld, Pilgerodendraceae A. V. Bobrov & Melikian, Platycladaceae A. V. Bobrov & Melikian, Sequoiaceae Luersson, Taiwaniaceae Hayata, Taxodiaceae Saporta, Tetraclinaceae Hayata, Thujaceae Burnett, Thujopsidaceae Bessey, Widdringtoniaceae Doweld
Evolution. Divergence & Distribution. For the Middle Jurassic ca 173 m.y.o. fossil Scitistrobus duncaanensis, see Spencer et al. (2015); it has some similarities with Voltziales, e.g. the ovules are attached to to the free tips of the ovuliferous scale, but in the compact cone, etc., it is assignable to Cupressaceae, and that is where they place it. Cupressoideae are predominantly northern in their current distributions and Callitroideae are predominantly southern, a vicariance pattern that may reflect the break-up of Pangaea (see also X.-Q. Wang & Ran 2014 for a summary). The split between the two is dated to (183-)153(-124) m.y. or (193.2-)178.2-143.0(-134.3) m.y. (Mao et al. 2012; see Z.-Y. Yang et al. 2012 for more dates). However, there has been much E.-W. and some N.-S. movement even of extant genera, thus the southern Widdringtonia is found in 97 m.y.o. rocks from North America (McIver 2001) and northern Sequoioideae in rocks from the Upper Cretaceous of Queensland (Peters & Christophel 1978: its leaves are like those of the southern Arthrotaxis). Crown Callitroideae have been dated to 71.9-51.9 m.y. (Leslie et al. 2012: other estimates older), and crown Cupressoideae are somewhat older. However, the age of a clade including Sequoia, Callitroideae, and Cupressoideae has also been estimated at a mere 66.4 m.y. (Magallón et al. 2013).
There is a rich Cretaceous fossil record of cupressoid plants like Elatides and Hughmillerites that have ovuliferous scales and spiral cone scales, plesiomorphic features, and several of these fossils form a clade with extant Cunninghamia, even if, as might be expected with fossil material, support is not overwhelming (Shi et al. 2014). Their fossil record, from the northern hemisphere and stretching back to the Late Jurassic ca m.y.a. (Rothwell et al. 2011), suggests that plants with similar morphologies formed an important early radiation in Cupressaceae (e.g. Shi et al. 2014; Atkinson et al. 2014). Indeed, if the basal topology of the family [Cunninghamioideae [Taiwanoideae [Athrotaxidoideae [....]]] is confirmed (see below), then features common to these genera (e.g. Atkinson et al. 2014) will be features for the family as a whole. Wilf and Escapa (2014) suggest some fossil-based dates for within this clade.
There was much Caenozoic extinction, probably around the Oligocene-Miocene boundary ca 23 m.y.a., and diversification in extant genera can be dated to after this period (Crisp & Cook 2011; Mao et al. 2012; Pittermann et al. 2012). Pittermann et al. (2012; see also Edwards & Donoghue 2013) suggested that Juniperus and Cupressus s.l., most of whose species have become adapted to dry conditions and have developed cavitation-resitant xylem, diverged 38.7-32 m.y.a., while figures in Leslie et al. (2012) are 53-33 m.y. (and some much older). Mao et al. (2010; see also Adams & Schwarzbach 2013) throught that there was E->W migration across the North Atlantic Land Bridge in Juniperus, initially Eurasian in distribution, around 47-30.3 m.y.a. (see see Mao et al. 2010 for more dates). Arid-adapted members of Callitroideae diversified some 52.6-34 m.y.a. (Pittermann et al. 2012); Leslie et al. (2012) suggest that diversification began a little before the K/T boundary ca 65.5 m.y.a. and continued throughout the Caenozoic.
If Cunninghamia is sister to the rest of the family (see below), and then followed by genera like Arthrotaxis and Taiwania, then loss of ovuliferous scales and other characters are best placed within the family and are not apomorphies for it.
Ecology & Physiology. Biomass estimates for Sequoia sempervirens are 2.3x106 kg ha-1 (Franklin & Dryness 1973).
For details of xylem function in relation to the environment in Cupressaceae, see Pittermann et al. (2010). The initial preferences for the family were mesic conditions, but Pittermann et al. (2012) noted that a number of species of both Cupressoideae and Callitroideae had evolved drought resistance, their xylem-specific conductivity and stomatal conductances being lower, and also their CO2 assimilation rates were much reduced. The cost of these adaptations was slow growth.
Bacterial/Fungal Associations. The telial stage of Gymnosporangium rust is common on some Cupressaceae, especially Juniperus, while the aecial stage characterises Rosaceae-Maloideae (Savile 1979b).
Pollination Biology. For the active and irreversible withdrawal of pollination drops within half an hour of deposition of pollen, see Dörken and Jagel (2014); this happens also with pollen from other Cupressaceae, but not with pollen from angiosperms and Pinus.
In Cupressus dupreziana paternal apomixis, a phenomenon unknown from any other seed plant, occurs; here the embryo develops from unreduced male gametes (Pichot et al. 2000, 2001).
Genes & Genomes. Cryptomeria japonica has a much reduced inverted repeat with few genes duplicated in it (Hirao et al. 2008).
Chemistry, Morphology, etc. Characters of wood anatomy may yield phylogenetically interesting variation (Schulz & Stützel 2007), but state delimitation is difficult; for epidermal morphology, see Ma et al. (2009).
Proliferation of the ovuliferous cones is common, and the distribution of this feature, too, may be of phylogenetic interest (Schulz & Stützel 2007). Scales on the ovuliferous cones are wedge-shaped to peltate. Most Cupressaceae lack ovuliferous scales, having only bract scales (Zhang et al. 2004; see also Farjon 2005c), but Cryptomeria has several "teeth" on the ovuliferous scale - perhaps a reversion to a plesiomorphic morphology (see also Schulz & Stützel 2007).
For a monograph (and far more) see Farjon (2005c); general information can of course be found in the Gymnosperm Database. For cone morphology, see Farjon and Garcia (2003 and references) and Schulz and Stützel (2007: interesting analysis, but unfortunately Juniperus etc. not included).
Phylogeny. Page (1990) suggested that there were "fundamental" differences between Cupressaceae and Taxodiaceae in the morphology of their reproductive parts, but in the tree of Quinn et al. (2002) Cupressaceae s. str. are embedded in a paraphyletic Taxodiaceae which form a basal grade. Phenetic analyses had earlier suggested the combination of the two (Eckenwalder 1976), and they are combined in Farjon (2005c). For relationships within Cupressaceae, see Brunsfeld et al. (1994), Gadek et al. (2000), Kusumi et al. (2000), Farjon et al. (2002), Brunsfeld et al. (2003), and Little et al. (2004).
The basic phylogenetic structure of the family is [Cunninghamioideae [Taiwanoideae [Athrotaxidoideae [Sequoioideae [Taxodioideae [Cupressoideae + Callitroideae]]]]]] (Mao et al. 2012: support, inc. for basal branches, usu. strong), although Z.-Y. Yang et al. (2012) found the subfamilial order in the middle of the tree to be [... [Sequoioideae [Athrotaxidoideae [...]]]]. Thus the phylogeny is strongly pectinate basally, although in some morphological analysis two or more members of the first three branches may form a single clade (e.g. Rothwell et al. 2011).
Callitris is paraphyletic, although morphological (Piggin & Bruhl 2010) and molecular (Pye et al. 2003) studies do not agree as to how extensive the paraphyly is. For relationships in Juniperus, see Mao et al. (2010) and Adams and Schwarzbach (2013). Cupressus has turned out to be polyphyletic and is now restricted to the Old World (Xiang & Li 2005; especially Little 2006). Terry and Adams (2015: sampling slight) suggest relationships in this area are [Cupressus [Juniperus [Hesperocyparis, Callitropsis, Xanthocyparis]]], although chloroplast data were a bit wayward.
Classification. Having 24 family names for ca 30 genera says a lot about the past. For generic limits around Cupressus, which has turned out to be polyphyletic, see Price and Adams (2009) and Little (2006) and around Callitris, see Pye et al. 2003) and Piggin and Bruhl (2010). For an account of Cupressus, see Adams (2010).
Botanical Trivia. Juniperus grows at some 4,900 m altitude on the Tibetan Plateau and forms the highest known forest (Opganoorth et al. 2010). The tallest living tree in the world is a coast redwood Sequoia sempervirens, at about 115.5 metres (379 feet), although the giant redwood (Sequoiadendron giganteum is larger and Eucalyptus regnans was almost certainly taller.
TAXACEAE Berchtold & J. Presl Back to Pinales
Bands of fibres in phloem crystalliferous, sclereids + [Taxus]; resin canal below vascular bundle in leaf; plant dioecious (monoecious); pollen shed at 1-cell stage, inaperturate; cone scales opposite; ovules erect; pollen chamber +, pollination drop +; male gametes unequal in size; seed not winged, coat vascularized, with sarco- and sclerotesta.
6/30. Northern Hemisphere, scattered, also New Caledonia.
Age. The age of this node is (231-)187(-144) m.y. (Won & Renner 2006).
1. Cephalotaxus Siebold & Zuccarini
2-3 microsporangia/microsporophyll; ovuliferous scale much reduced, ovules 2/bract scale; female gametophyte with 1024-4096 free nuclei; ?embryo; n = 12.
1/6. E. Himalayas to Japan (map: from Florin 1963). [Cephalotaxus koreana Photos - Collection, C. fortunei, Collection.]
Synonymy: Cephalotaxaceae F. W. Neger
2. The Rest.
Wood and phloem lack resin canals [?family]; (resin canals in leaf 0); 2-10 microsporangia/microsporophyll (partly connate - Austrotaxus), pendulous from peltate scutellum to abaxial and with a phyllome-like adaxial process; bract and ovuliferous scale 0, ovule solitary, on shoot in axil of vegetative leaf; female gametophyte with ca 256 free nuclei; (seed "arillate" - Taxus); embryo short/minute (cotyledons 3); n = 7, 11, 12.
5/24: Taxus (8). Scattered in the Northern Hemisphere, esp. South East Asia, also New Caledonia (map: from Florin 1963; de Laubenfels 1988). [Photos - Collection.]
Age. The age of the [Torreya + Taxus] clade is some 138 m.y. (Magallón et al. 2013).
Synonymy: Amentotaxaceae Kudô & Yamamoto, Austrotaxaceae Nakai, Torreyaceae Nakai
Evolution. Bacterial/Fungal Associations. Taxol and related compounds are synthesized by Taxus and also by several fungi that either grow in the soil around the plant or are endophytes (Cassady et al. 2004 and references), and the fungus may have acquired the ability to synthesize taxol from the plant (Strobel et al. 1996). Pestalotiopsis guepinii, which can synthesize taxol, is also endophytic in Wollemia (Araucariaceae), etc. (Strobel et al. 1997)
Chemistry, Morphology, etc. (S)norcolaurine synthase activity is high in both Cephalotaxus and other Taxaceae; this might suggest that benzyisoquinoline alkaoids may be found here (Liscombe et al. 2005). Cephalotaxus contains some very distinctive alkaloids (Parry et al. 1980). There is quite a bit of variation in leaf anatomy, but it does not suggest particular relationships (Ghimire et al. 2014a).
For male cones and their similarities, see Mundry and Mundry (2001). Taxaceae s.l. lack sacci on their pollen (Anderson & Owens 2006). The scales subtending the ovules of Austrotaxus are spiral. Taxus and its immediate relative have female cones with a single ovule and the seed is surrounded by an aril. The sarcotesta of Cephalotaxus has been tentatively equated with the aril of Taxus (Mundry 2000), although the two would not seem to be homologous. A reinterpretation of the female reproductive structures (Stützel & Röwekamp 1999a) suggest that Taxus in particular can be linked with Torreya and then to other conifers; its aril is the equivalent of the sarcotesta of other taxa.
For the morphology of Taxus and relatives, see Hart and Price (1990), for male reproductive structures, see Wang et al. (2008), for male gametes, see Chamberlain (1935) and Singh (1978), for the megasporangiate cone, see André (1956) and Liang and Wang (1989), for embryology in general, see Chen and Wang (1990: the sperm range from somewhat to very unequal in size), and for a general account, see Cope (1998).
Phylogeny. Cephalotaxaceae and Taxaceae are combined here because on balance the evidence suggests that the exclusion of Cephalotaxus would make Taxaceae paraphyletic. Page (1990) included Amentotaxus in Cephalotaxaceae, although he noted that affinities between the two were "somewhat enigmatic"; a family as so delimited appears para- or polyphyletic to Taxaceae s. str., c.f. e.g. Price (2003) and Hao et al. (2010). Quinn et al. (2002) in a broad survey of Pinales found that Cephalotaxus, Torreya and relatives, and Taxus and relatives formed a tritomy in their unweighted rbcL and matK analyses; only when weighted were Cephalotaxaceae and Taxaceae separate. Price (2006) looked at variation in the same two genes and found weak support for Cephalotaxus as sister to [Amentotaxus + Torreya]; sampling overall was poor, but good for Taxaceae s.l., and support for the monophyly of Taxaceae s.l. was strong. These relationships were found by Wang et al. (2003) in analyses of trnL/F singly and when combined with rbcL data, but not in an analysis of rbcL alone, when Cephalotaxus alone was sister to Taxaceae (for the latter relationship, see also Rai et al. 2009). The work of Rai et al. (2008a) also supports a broad circumscription of Taxaceae, as does that of Leslie et al. (2012). Although Hao et al. (2008) preferred to keep the two families separate, support for this was low; for phylogenies, see also Cheng et al. (2000) and Ghimire and Heo (2014a: morphology only).
Previous Classifications. Cephalotaxaceae and Taxaceae have sometimes been separated (see introduction to Pinales above). Taxus has sometimes been considered quite distinct from all other conifers, the Taxopsida supposedly being well separate from Coniferopsida since pernaps the late Palaeozoic (Florin 1958, also Florin 1949, 1954; Miller 1999).