EMBRYOPSIDA Pirani & Prado

Gametophyte dominant, independent, multicellular, initially ±globular, not motile, branched; showing gravitropism; acquisition of phenylalanine lysase* [PAL], flavonoid synthesis*, microbial terpene synthase-like genes +, triterpenoids produced by CYP716 enzymes, CYP73 and phenylpropanoid metabolism [development of phenolic network], xyloglucans in primary cell wall, side chains charged; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; thalloid, leafy, with single-celled apical meristem, tissues little differentiated, rhizoids +, unicellular; chloroplasts several per cell, pyrenoids 0; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles/centrosomes in vegetative cells 0, microtubules with γ-tubulin along their lengths [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band + [with microtubules and F-actin; where new cell wall will form], phragmoplast + [cell wall deposition centrifugal, from around the anaphase spindle], plasmodesmata +; antheridia and archegonia +, jacketed*, surficial; mblepharoplast +, centrioles develop de novo, bicentriole pair coaxial, separate at midpoint, centrioles rotate, associated with basal bodies of cilia, multilayered structure + [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] (0), 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 +*, multicellular, growth 3-dimensional*, cuticle +*, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [MTOC = microtubule organizing centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, 1000 spores/sporangium, sporopollenin in the spore wall* laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae]; plastid transmission maternal; nuclear genome [1C] <1.4 pg, main telomere sequence motif TTTAGGG, KNOX1 and KNOX2 [duplication] and LEAFY genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA, minD, minE genes moved to nucleus; mitochondrial trnS(gcu) and trnN(guu) genes +.

Many of the bolded characters in the characterization above are apomorphies of more or less inclusive clades 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.

POLYSPORANGIOPHYTA†

Sporophyte well developed, branched, branching dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].

II. TRACHEOPHYTA / VASCULAR PLANTS

Sporophyte long lived, cells polyplastidic, photosynthetic red light response, stomata open in response to blue light; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; PIN[auxin efflux facilitators]-mediated polar auxin transport; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; roots +, often ≤1 mm across, root hairs and root cap +; stem apex multicellular [several apical initials, no tunica], with cytohistochemical zonation, plasmodesmata formation based on cell lineage; vascular development acropetal, tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; stomata numerous, involved in gas exchange; leaves +, vascularized, spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia adaxial, columella 0; tapetum glandular; ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; archegonia embedded/sunken [only neck protruding]; suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].

[MONILOPHYTA + LIGNOPHYTA]

Sporophyte growth ± monopodial, branching spiral; roots endomycorrhizal [with Glomeromycota], lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; nuclear genome size [1C] = 7.6-10 pg [mode]; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; mitochondrion with loss of 4 genes, absence of numerous group II introns; LITTLE ZIPPER proteins.

LIGNOPHYTA†

Sporophyte woody; stem branching lateral, meristems axillary; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].

SEED PLANTS† / SPERMATOPHYTA†

Growth of plant bipolar [roots with positive geotropic response]; plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].

EXTANT SEED PLANTS

Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); microbial terpene synthase-like genes 0; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignin chains started by monolignol dimerization [resinols common], particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; roots often ≥1 mm across, stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; 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; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; axillary buds +, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends], primary root/radicle produces taproot [= allorhizic], cotyledons 2; embryo ± dormant; chloroplast ycf2 gene in inverted repeat, trans splicing of five mitochondrial group II introns, rpl6 gene absent; ??whole nuclear genome duplication [ζ - zeta - duplication], 2C genome size (0.71-)1.99(-5.49) pg, two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.

EXTANT GYMNOSPERMS / PINOPHYTA / ACROGYMNOSPERMAE

Biflavonoids +; cuticle wax tubules with nonacosan-10-ol; ferulic acid ester-linked to primary unlignified cell walls, silica usu. low; root apical meristem organization?, protophloem not producing sieve tubes, with secretory cells, sieve area of sieve tube 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; parts of strobili spirally arranged; microsporangia abaxial, dehiscing by the action of the epidermis [= exothecium]; pollen tectate, endexine lamellate at maturity, esp. intine with callose; ovules aggregated into strobili, erect, 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 germinates on ovule, usu. takes 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 nuclei 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; genome size [1C] 10< pg [1 pg = 109 base pairs]; two copies of LEAFY gene [LEAFY, NEEDLY] and three of the PHY gene, [PHYP [PHYN + PHYO]], chloroplast inverted repeat with duplicated ribosomal RNA operons, mitochondrial rps3 gene with second intron [group II, rps3i2].

[CUPRESSALES [GNETALES + PINALES]]: tree, branched; compression wood + [reaction wood - much-thickened/lignified fibres on abaxial side of branch-stem junction]; wood pycnoxylic; torus:margo pits + [tracheid side walls], pits 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; nodes 1:1; axillary buds + (0); leaves with single vein, fasciculate, needle-like or flattened; plants monoecious; microsporangiophore/filament simple, hyposporangiate; dehiscing by the action of the hypodermis [endothecium]; pollen saccate, exine thick [³2 µm thick], granular; ovulate strobilus compound, erect, ovuliferous scales flattened, ± united with bract scales; ovules lacking pollen chamber, inverted [micropyle facing axis]; pollen buoyant, not wettable, pollen tube unbranched, growing towards the ovule, wall with arabinogalactan proteins; gametes non-motile, lacking walls, siphonogamy [released from the distal end of the tube]; female gametophyte lacking chlorophyll, 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]; one duplication in the PHYP gene line; germination phanerocotylar, epigeal, (seedlings green in the dark).

Note: In all node characterizations, boldface denotes a possible apomorphy, (....) denotes a feature the exact status of which in the clade is uncertain, [....] includes explanatory material; other text lists features found pretty much throughout the clade. Note that the particular node to which many characters, particularly the more cryptic ones, should be assigned is unclear. This is partly because homoplasy is very common, in addition, basic information for all too many characters 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 are the not-so-trivial issues of how character states are delimited and ancestral states are reconstructed (see above).

N.B.: "conifers" in the discussion below refers to Pinales and Cupressales together, a group also called Pinophyta, Coniferophyta, Coniferae, Pinopsida...

Age. Clarke et al. (2011: other ages) suggested a crown age for this clade of (286-)252(-212) m.y., Magallón et al. (2013) an age of ca 278 m.y., Won and Renner (2006) an age of (324-)298(-270) m.y., while ca 290 m.y. is the estimate in Ran et al. (2018a). The estimates by Crisp and Cook (2011: no Gnetales) of around 270 m.y. and of around 260.9 m.y. by Tank et al. (2015: Table S2) are broadly comparable. Leslie et al. (2012) suggested an age of around 350-275 m.y. and Ran et al. (2018b) an age of (312.6-)276.2(-206.7) m.y., but Zhou et al. (2014) and Magallón et al. (2015) offered appreciably younger ages of (187.3-)161.4(-147) and ca 127 m.y. respectively; see also P. Soltis et al. (2002).

What follows below is rather incomplete. The rich fossil record of stem [Cupressales [Gnetales + Pinales]] and of the three orders themselves, along with most of that of the gymnosperms as a whole, is largely ignored...

Evolution. Divergence & Distribution. Leslie et al. (2012) offer ages for several conifer clades (see below) and evaluate the fossil data critically; their four-gene tree is based on an almost complete sampling of the group. There are no known synapomorphies for a clade containing living and fossil conifers (e.g. Rothwell & Serbet 1994). However, the morphology of extinct conifers and coniferophytes is being re-evaluated as the morphologies of entire organisms are being assembled 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 the vegetative growth of the axis on which they occur (e.g. Hernandez-Castillo et al. 2001; Rothwell & Mapes 2001).

The rate of molecular evolution of conifers is substantially slower than that in woody angiosperms, let alone that of herbaceous angiosperms, although the rate of non-synonymous substitutions is higher, perhaps connected with their large populations, outcrossing, and overall low population structure (Buschiazzo et al. 2012; see Jaramillo-Correa et al. 2016; Ran et al. 2018a, also elsewhere under Pinaceae and Araucariaceae).

Conifers are unusual compared to other vascular plants in that they show a gradual increase in disparity, that is, the amount/extent of morphological variation in their taxa, since their initial appearance in the Carboniferous (Oyston et al. 2016), although more commonly initial radiation results in most of the morphospace that clades now occupy being filled very quickly.

The current distributions of many extant conifer groups is much smaller than and/or very different from their past distributions, thus McIver (2001) reported fossils of the African Widdringtonia (Cupressaceae) from rocks of Cretaceous age in Alabama (for distribution maps of all conifers, see Farjon & Filer 2013). Many conifers have fossil records going back to the Cretaceous; see Manchester (1999) for north temperate distributions). 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 to crown groups of/in those families.

Diversification in most conifer genera occurred in the Caenozoic, as emphasized by Klaus et al. (2017), indeeed, the median node age of Pinus is a mere 4.4 m. years. Leslie et al. (2012) observed 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) associated 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, had been 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.

Doyle (2009) discussed the evolution of exine morphology; granular exine may be an apomophy and then lost twice, or alveolar/honeycomb exine may be plesiomorphous, with granular exine gained three times, or the may be some other combination of gains and losses, but always adding up to three steps. Hence, the optimization here is an arbitrary choice! Franceschi et al. (2008) note possible anatomical apomorphies that are associated with defence against herbivorous insects.

Ecology & Physiology. There may not be that many species of conifers, but they are ecologically a very successful group. Dominating boreal forests in particular, but common in many other places outside the humid lowland tropics, they are more or less dominant in 39% of the world's forests - remarkable, since there are around 950 species of gymnosperms (545 conifers, the forest dwellers) to around 352,000 species of angiosperms - they are less than 0.27% of all seed plants (see also Ran et al. 2018a). Bond (1989), Keeley and Zedler (1998), Brodribb et al. (2012), Augusto et al. (2014) and others have emphasized that after the seedling stage conifers in general can out-compete angiosperms in a number of environments that are low in nutrients, being able to tolerate poor soil and extreme conditions such as drought and cold. 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; Augusto et al. 2014).

Sperry (2003), Pitterman et al. (2005), Hacke et al. (2005, 2015) 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 facilitating water transport, while the torus provides a valuable safety feature guarding against embolism as it will plug the pit if pushed against one side by pressure from the 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, since if the torus is relatively too narrow, air will seep in around the sides (Pittermann et al. 2010). Vascular tissue with tracheids only may be less hydraulically efficient than vascular tissue with vessels that have simple perforations, but they are tolerant of hydraulic stress and are resistant to cavitation, despite gymnosperms investing only about half as much as angiosperms in wall material - but at the same time they can make up the trunk of very large trees (Sperry 2003; Hacke et al. 2015). Lipid surfactants in the xylem of angiosperms, at least, i.a. coat nanobubbles as they form and so prevent the formation of embolisms and should be looked for here, too (Schenk et al. 2017). As Pitterman et al. (2005: p. 1924) note, "the evolution of the torus-margo membrane within the gymnosperm lineage from homogeneous pits was equivalent to the evolution of vessels within the angiosperms" (see also Wilson 2015; Hacke et al. 2015).

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). The plesiomorphic condition for controlling water flow in the leaf during drought is for rising foliar abscisic acid concentrations to cause the stomata to close; the tracheids are prone to cavitation (Brodribb et al. 2014), however, abscisic acid is not involved in stomatal closure in some other conifers, a change that can be placed at the [Taxaceae + Cupressaceae] node.

The diameter of first order roots is linked to mycorrhizal type and how the plant forages for nutrients, and it varies considerably (W. Chen et al. 2013, 2016), but no comprehensive survey seems to have been carried out.

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 conifers in particular is slower (Silver & Miya 2001), however, litter of the arbuscular mycorrhizal juniper has a lower C:N ratio than that of Pinus edulis and decomposes faster (Gehring et al. 2017b and references). Brown rot fungi like boletes are common on conifers, and they can access much of the cellulose in the cell wall but they cannot destroy lignin; they have often evolved from white-rot fungi (e.g. Floudas et al. 2012; Kohler et al. 2015), although the basal dacrymycete Calcera cornea may have evolved from a soft-rot ancestor (Nagy et al. 2015).

Many Pinaceae, ECM plants, grow successfully in low N conditions, while podocarps, AM plants, can grow 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, the basal area of angiosperm trees in forests with and without these emergents, but which are otherwise comparable, being similar (Enright & Ogden 1995; Aiba et al. 2007).

Pollination Biology & Seed Dispersal. For pollinators of fossil coniferales, see Peris et al. (2017). Fossils suggest Cheirolepidaceae were visited by Neuroptera ca 155 m.y.a. and by Diptera 130-105 m.y.a. (Peris et al. 2017).

Overall, there are three main kinds of reproductive cycles in Pinales, and these are based on how long reproduction takes, 2 or 3 years. In the two-year cycle, pollination, fertilization, etc. all occur in the second year. In the three-year cycle, there is variation in details of development, in particular, whether fertilization occurs in the second or third year (Turgeon et al. 1994).

For male cone variation and evolution, see Schulz et al. (2014). Much has been learned about pollination and pollen germination in conifers in the last few years, and this is summarized by Leslie et al. (2015a), although important work had been carried out about 80 years ago. Details of the fascinating story in Leslie et al. (2015a) depend on the topology of the tree used, which in Podocarpaceae, for instance, differs from that below (in such cases, data checked against Leslie et al. 2015b). Wind pollination is ubiquitous. The pollen grains directly impact the ovulate cones rather than being swept around them by a turbine-like action (Cresswell et al. 2007). There are correlations between the presence of pollen sacci or wings, exine thickness and structure, whether (no wings) or not (wings) the pollen is wettable/pollen buoyancy, ovule and cone orientation, and presence of a pollination drop (Tomlinson 1994; Little et al. 2014; Leslie et al. 2015a; for the composition of the pollination droplet, see Ziegler 1959; Nepi et al. 2009). It had been thought that the sacci on conifer pollen facilitated its dispersal by wind, however, they function more like water wings. The 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). Changes in pollination mechanisms seem not to be accompanied by changes in diversification rates, and although sacci have been lost several times, in no case have sacci re-evolved within esaccate clades, loss being something of a one-way street (Leslie et al. 2015a). 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 in other ancient gymnosperms (Leslie 2008).

Recent work suggests that the pollen story may be more complex. Sacci may indeed 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 Falcatifolium, the pollen will fall faster - as it may also if the surface of the pollen grain is not smooth (Grega et al. 2013). Furthermore, the pollination droplet may also be involved in insect pollination, as in a number of Gnetales. 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, 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). Proteins have been found in the pollination droplet, and these may be involved in defence against pathogens and in promoting male gametophyte development (Wagner et al. 2007).

For details of seed morphology, dispersal types, etc., and their evolution, see Contreras et al. (2016). Fleshy (the fleshiness is of several kinds) animal-dispersed seeds have evolved several times from winged seeds, but there have been no reversals, while the dry animal-dispersed seed type in Pinus has, hoever, reversed to the winged type (Contreras et al. 2016). 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 disseminules and monoecious and have dry disseminules; they note common transitions from the monoecy/fleshy to dioecy/fleshy combinations, although overall such features had little effect on diversification. 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). Variation in seed size links with dispersal mechanisms - abiotic dispersal < seed subtended by attractant tissues < attractant issues part of the seed - and there are also correlations with clades (Leslie & Beaulieu 2015; see also Leslie et al. 2017 for detailed discussion).

Plant-Animal Interactions. Herbivory in gymnosperms as a whole is relatively low (Turcotte et al. 2014: see caveats). In an earlier survey (Turgeon et al. 1994), almost 400 species of insects were recorded as eating the cones, and of these almost half (184 spp.) were Lepidoptera. Larger genera involved include Megastigmus (torimyid Hymenoptera), Dioryctria (pyralid moth) and Cydia (a tortricid). Conifers have layers of polyphenol-containing parenchyma cells in the phloem, possibly offering some protection against insects (Li et al. 2012), while Pinaceae have resin ducts in both phloem and xylem and 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: q.v. fot possible conifer apomorphies associated with these interactions). The different 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). However, caterpillars of Yponomeutoidea-Argyresthidae, ditrysian moths and some leaf miners, are quite common here (Sohn et al. 2013). See below for some details about the interactions between bark beetles, their associated fungi, and the conifer host.

Favret and Voegtlin (2004), Meseguer et al. (2015) and R. Chen et al. 2016) discuss speciation of Cinara aphids, found on Cupressaceae and especially Pinaceae, see also below. Many of the wood-eating basal termites (their protozoans in theit guts can break down lignin) seem to like the wood of Pinales; the crown-group age of termites is Jurassic, ca (170-)149(-136) m.y.a. (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), Nagy et al. (2015). For the blue-staining ascomycete fungi associated with ambrosia beetles, see below.

Vegetative Variation. Secondary growth (only phloem is produced) has been reported from the leaves of a number of conifers, including those of Pinus longaeva the needles of which can live for 30 years or more (Ewers 1982; Hacke et al. 2015). There are short shoots in a number of taxa (see Dörken 2012 for a summary), and the shedding of branchlets, cladoptosis, which also occurs in taxa other than those with short shoots, is widespread (Burrows et al. 2007 and references; Dörken 2012). Below a distinction is made between evergreen and deciduous trees, the latter having no photosynthetic leaves during the winter, and cladoptosis, the shedding or abscission of branchlets. The latter may be the normal way in which leaves fall from the plant in both evergreen (e.g. Araucaria) and deciduous (e.g. Metasequoia) taxa and in those with (e.g. Pinus - evergreen) and without (e.g. Taxodium - deciduous) short shoots. (Note that the distinction between short and long shoots here is whether (long shoots) or not (short shoots) internodes are elongated.) 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 on the main axes are much more common, although most produce short shoots. Serial axillary buds occur in some taxa, particularly in those with cladoptosis since in their absence the supply of reserve meristems along a branch is reduced with the abscission of the branchlets; the oldest buds are furthest away from the axil.

Genes & Genomes. Chromosome number shows little variation in Pinales, and overall there is little polyploidy (Murray 2013; Scott et al. 2016). Based on their study of the coast redwood, Sequoia sempervirens, the only hexaploid in the whole group, Scott et al. (2016) emphasized the rarity of polyploidy in extant conifers, perhaps connected with their slow rate of diploidization. However, there appear to have been three genome duplications in the Pinales area, one in stem Pinaceae, another in stem [Taxaceae + Cupressaceae] (Sciadopitys was not examined), and a third in Welwitschia (Z. Li et al. 2015).

Conifers are noted for their very large nuclear genomes with 2C values of up to 72 pg (Zonneveld 2012); for 1C values, see the Plant DNA C-values Database (consulted vi.2013). These massive genomes are in part the result of the activity of a number of transposable elements that is not counteracted by mechanisms for slimming genomes, as in angiosperms (Ahuja & Neale 1005; Nystedt et al. 2013; see also Guan et al. 2016). 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 associated with 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 chloroplast inverted repeat had been lost in Pinales (the IRb copy) and in Cupressales (the IRa copy). Raubesen and Jansen (1992a), Lackey and Raubeson (2008), Hirao et al. (2008) and Yi et al. (2013: can the copies be distinguished?) also discuss the loss of a copy of the inverted repeat; Guo et al. (2014) and J. Li et al (2016) note that in both cases short and novel IRs have developed.

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 construction 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), and leaf traces can also make connections with xylem produced during the second and subsequent years (Maton & Gartner 2005). Which taxa (few? most?) have a foliar emdodermis is unclear (c.f. Lersten 1997; Dörken 2014).

Bisexual strobili have ovuliferous scales above the microsporangia, i.e., the same basic arrangement as in angiosperm flowers, and they are scattered through the clade (Flores-Rentería et al. 2011). Basic cone morphology is very variable. Conifer seed cones have become more massive and strongly constructed since the Triassic, and particularly the Jurassic, presumably in reponse to animal predation pressure (Leslie 2011b), and although Taxus, for instance, is distinctive among extant taxa in having tiny female cones each with a single, erect ovule, cones are often quite 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 frequently little evidence of an ovuliferous scale in the mature cone, which consists largely of bract scales (e.g. Schulz & Stützel 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).

For differences in the growth of the pollen tube in Pinaceae and angiosperms see Rounds and Bezanilla (2013); branched pollen tubes occur sporadically in Pinales (Friedman 1987 for references). Male gametes need 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 sometimes occurs 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.

Detailed studies on both fossil and extant conifers by Florin (e.g. 1951) laid the foundation for subsequent work on the group; see also Page (1990) and especially Gifford and Foster (1988), Farjon (2005b) for a bibliography and Farjon (2008) for an excellent general account; see also Debreczy and Rácz (2006), Eckenwalder (2009), Garnandt et al. (2011) and Plomion et al. (2011) for general information, Trapp and Croteau (2001a: resin biosynthesis), Geyler (1867), Barthelmess 1935, and Kumari (1963: nodal anatomy), Möller (1882: cork cambium), Napp-Zinn (1966) and Yao and Hu (1982), both leaf anatomy, Den Outer (1967) and Schulz (1990), both phloem anatomy, much detail unincorporated, Zhou and Jiang (1992: wood anatomy); see also Sivak (1975: detailed study of saccate pollen), 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 and 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), Mathews and Tremonte (2012: greening of seedlings in the dark), and Herrmann (1951: intergeneric grafting). A valuable resource is the Gymnosperm Database (Earle 1997 onwards).

Phylogeny. For more discussion on the the major groups of seed plants and their relationships, see angiosperms and seed plants, and for the five extant gymnosperm orders, see Cupressales, Cycadales, Gnetales, Ginkgoales and Pinales.

Within conifers, relationships are being 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 the tree above), Kelch and Cranfill (2000), Gugerli et al. (2001: e.g. the mitochondrial nadI gene), Rai et al. (2002, especially 2008a), Burleigh et al. (2012), 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.]...

In the previous paragraph, Gnetales are not mentioned - they were not included in the studies mentioned. Indeed, the position of Gnetales has long been problematical. Morphological analyses in the 1980s often recovered an [angiosperm + Gnetales] clade, other estant gymnosperms being quite separate - this is the anthophyte hypothesis (see the Cycadales page; Coiro et al. 2018 for a useful summary). However, the molecular work that soon started appearing wither removed Gnetales from both angiosperms and gymnosperms or, more often, linked Gnetales with gymnosperms. Of the mejor hypotheses, it was suggested that 1, Gnetales might be sister to a clade including all other seed plants (e.g. Sanderson et al. 2000: two genes, third positions only; Seider et al. 2002: rbcL gene only; Rydin et al. 2002: nuclear genes only; Rai et al. 2003: large chloroplast data set; Quandt et al. 2004: trnL intron; C.-S. Wu et al. 2012b: LBA, 2013: some analyses). Extant gymnosperms would then be paraphyletic (see also Burleigh & Mathews 2004; Rai & Graham 2010: [Pinales [Ginkgoales [Cycadales + Angiosperms]]]; C.-S. Wu et al. 2011b: only in maximum parsimony, high substitution rate; Z.-D. Chen et al. 2016).

2. A [Gnetales {Pinales and Cupressales}] clade - the Gnetifer hypothesis - has frequently been recovered (e.g. Samigullin et al. 1999: not all analyses; Antonov et al. 2000; Sanderson et al. 2000; Chaw et al. 2000; Gugerli et al. 2001: rather strong support; de la Torre et al. 2006: much hidden support, but not from the chloroplast partition, 2017; Wu et al. 2007; Rydin & Korall 2009: Bayesian analysis; Ran et al. 2010: the mitochondrial rps3 gene; Rai & Graham 2010: support not very strong; Burleigh et al. 2012; C.-S. Wu et al. 2013: some analyses; Magallón et al. 2013; Rothfels et al. 2015b; Ickert-Bond & Renner 2016; Puttick et al. 2018: a variety of analyses), and it is the preferred topology in Englund et al. (2011) and Groth et al. (2011).

3. Gnetales have also been found to be sister to Cupressaceae/Cupressales/conifer II group, the GneCup hypothesis, as in an analysis of an amino acid matrix derived from chloroplast genomes (Zhong et al. 2010; see also Ruhfel et al. 2014); both quickly-evolving proteins and also proteins in which there appeared to be much parallel evolution in Cryptomeria and the branch leading to all Gnetales were removed. If they were not removed, a clade [Cryptomeria + Gnetales] was obtained (Zhong et al. 2010; see also Moore et al. 2011; C.-S. Wu et al. 2013). Similarly, an analysis of variation in 83 plastid genes strongly suggested a grouping [Pinaceae [Gnetales + other Pinales]], although other relationships could not be entirely rejected (Chumley et al. 2008; see also Ruhfel et al. 2014; Evkaikina et al. 2017; Gitzendanner et al. 2018: chloroplast data). (Raubeson et al. (2006) found that Welwitschia grouped with Podocarpus, but this may be due to rate heterogeneity.)

4. Gnetales may be sister to the Pinaceae/Pinales/conifer I group, the GnePine hypothesis (e. g. Chaw et al. 2000; Bowe et al. 2000; Gugerli et al. 2001; Hajibabaei 2003; Burleigh & Mathews 2004, 2007c: supermatrix analyses; Hajibabaei et al. 2006: genes from all three compartments, sampling?; Qiu et al. 2007; Graham & Iles 2009; Finet et al. 2010: quite strong support; Soltis et al. 2011; Shen et al. 2017; evaluation of support). This topology was also found by Zhong et al. (2011, see also 2010; also C.-S. Wu et al. 2011b, 2014) when the most variable sites in concatenated alignments were removed, so reducing the LBA/heterotachy problem (clpP and matK genes in particular showed considerable heterotachy - Wu et al. 2011b), and by the concatenation-based transcriptome analyses of Wickett et al (2014). As Wu et al. (2011b: p. 1293) noted, "ndh genes (Braukmann et al. 2009) and the rps16 gene (Wu et al. 2007), and expansion of IRs to 3# psbA gene (Wu et al. 2007, 2009)" all supported this position. Although the possibility of any paraphyly of conifers has been strongly questioned (Rydin et al. 2002), a recent phylotranscriptomic study that included members of all gymnosperm families provides strong support for the GnePine hypothesis (Ran et al. 2018a), which is followed here.

There were some slight wrinkles. Xi et al. (2013b), using much nuclear and plastid data, although they included only ten gymnosperms, found a poorly to moderately supported [Gnetum + Pinaceae] clade in analyses of nuclear genes only. In analyses of chloroplast data a relationship with Cupressaceae was preferred (see also Davis et al. 2014a for the influence of different genomes); in both cases the alternative topology was rejected with a p-value of 0.001. This suggested to Xi et al. (2013b) that the two genomes of Gnetum had different histories. See also X.-Q. Wang and Ran (2014) for discussion; they noted that analyses of different classes of genes resulted in different topologies.

Overall, a position for Gnetales as sister to Pinales does seem most likely, indeed, there are some specific points of genomic similarity between Gnetum, etc., and some or all Pinales. There are also some morphological similarities between the two groups, perhaps particularly with Pinaceae. The binucleate sperm cells, basic proembryo structure, development of polyembryony, etc., of Ephedra agree with conifers in general and perhaps Pinaceae in particular (Ran et al. 2018a). Some Pinus species have mesogenous stomata in which the subsidiary cells are produced from the same initial that gives rise to the guard cells (Gifford & Foster 1989; see also Mundry & Stützel 2004), as in Gnetales. Strobili with both micro- and megasporangia are common as abnormalities in conifers (Chamberlain 1935; Rudall et al. 2011a) and of course occur normally in Gnetum. Of course, wherever Gnetales are placed, they will have numerous apomorphies. Thus although nearly all Pinales have megasporangiate strobili with spirally-arranged ovuliferous scales or modifications of them, Gnetales have decussating bracts (Magallón & Sanderson 2002); loss of the ovuliferous scale, etc., might also be apomorphies (Finet et al. 2010).

With the addition of Gnetales, relationships can be depicted as follows.


Cupressaceae Abies, etc Pinus, etc Pinaceae Araucariaceae Phyllocladaceae Podocarpaceae Cupressaceae Taxaceae Pinaceae Pinales Sciadopityaceae

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]). However, see Farjon (1990, 2005a, c, 2017) for detailed treatments of the conifers, Farjon (2001) for a checklist, and Christenhusz et al. (2011b) for a linear classification.

CUPRESSALES Link / Conifers II / Cupressophyta  - Main Tree

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; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], chloroplast IRa copy lost, but ycf2 and psbA regions retained, mitochondrial nadI gene intron 2 lost, also both rps3 introns, duplication in the PHYN clade. - 5 families, 57 genera, 383 species.

Note: In all node characterizations, boldface denotes a possible apomorphy, (....) denotes a feature the exact status of which in the clade is uncertain, [....] includes explanatory material; other text lists features found pretty much throughout the clade. Note that the particular node to which many characters, particularly the more cryptic ones, should be assigned is unclear. This is partly because homoplasy is very common, in addition, basic information for all too many characters 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 are the not-so-trivial issues of how character states are delimited and ancestral states are reconstructed (see above).

Age. Magallón et al. (2013: with temporal constraints) suggested an age of around (276.6-)259-256.9(-244.4) m.y. for this node and Won and Renner (2006) an age of (303-)273(-243) m.y., while around 249 m.y. is the estimate in Ran et al. (2018a) and (282.6-)177.5(-89.1) m.y. in Ran et al. (2018b: sampling), 230.9 m.y. in Tank et al. (2015: Table S2) and as little as 184 m.y. in Evkaikina et al. (2017).

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 disseminules and dioecy has evolved several times in members of this clade growing in the southern hemisphere (Leslie et al. 2013).

Genes & Genomes. Yi et al. (2013) note that the chloroplast accD gene is notably large here (see also Hirao et al. 2008), and that the small repeats that there are may be long enough to allow homologous recombination; overall, variation in the chloroplast genomes is very considerable (e.g. C.-S. Wu et al. 2011b; Wu & Chaw 2014, 2016). J. Li et al. (2016; see also W. Guo et al. 2014) discuss the evolution of the small trnQ inverted repeat in this clade; they suggest as a sequence: single copy (Podocarpaceae, Araucariaceae) → tandem repeat (Sciadopitys) → inverted repeat (the rest).

For mitochondrial genes, especially the rps3 gene, see Ran et al. (2010).

Chemistry, Morphology, etc. For southern conifers, making up part of this clade, see Hill and Brodribb (1998: general) and Cox et al. (2007: oxygenated di- and tricyclic terpenoids; Yao and Hu (1982) and Dörken and Stützel (2012) discuss leaf anatomy.

Phylogeny. For relationships, see especialy Cycadales and Pinales, also angiosperms, Gnetales and Ginkgoales.

Includes Araucariaceae, Cupressaceae, Podocarpaceae, Sciadopityaceae, Taxaceae.

Synonymy: Actinostrobales Doweld, Araucariales Gorozhankin, 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, Podocarpidae Doweld & Reveal, Taxidae Reveal - Araucariopsida A. V. C. F. Bobrov & Melikian, Podocarpopsida Doweld & Reveal, Taxopsida Lotsy

[Araucariaceae + Podocarpaceae]: gums +; roots with endomycorrhizal nodules; lamina vascular bundles not surrounded by sheath; three-year reproductive cycle, fertilization in 3rd year - Pinus)discrete pollination droplet 0; male gametophyte: prothallial cells divide; ovule one/bract scale; proembryo with 5 or 6 free-nuclear divisions; mitochondrial genome paternally inherited; 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: latter age preferred), (237-)205(-177) m.y. (Biffin et al. 2011b: text, c.f. fig. 2), 230-176 m.y. (Leslie et al. 2012), around 243 m.y. (Magallón et al. 2013), ca 195 m.y. (Ran et al. 2018a), or (284-)250, 225(-202) m.y. (Kranitz et al. 2014).

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 remaining cell divides and produces the gametes.

ARAUCARIACEAE Henkel & W. Hochstetter  - Back to Pinales

Araucariaceae

Branches whorled, plagiotropic, branchlets ultimately abscise [cladoptosis]; secretory cells in the centre of the root; 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; axillary meristems present on the trunk, undifferentiated, submerged by cork, persistent; leaves multiveined, lamina (veins branching dichotomously at base), petiole 0; (plants dioecious); to 20 microsporangia/microsporophyll; pollen not saccate; tapetum amoeboid [Araucaria]; bract and ovuliferous scales fused (not in Araucaria); ovule erect, nucellus protrudes from micropyle [?Araucaria]; pollination droplet 0, pollen not buoyant, germinates on ovuliferous scale and tubes grow over the scales [extra-ovular caputure and germination], prothallial cells numerous; seeds developing in association with the bract scale, wings entire or (asymmetrically) bilobed (0)/wings derived from integument, entire; free nuclear stage in proembryo with many nuclei, central, embryonal cells surrounded by cap cells that degenerate; cotyledons (4 - some Araucaria), with (3-)4-8 vascular bundles [?Agathis]; n = 13, nuclear genome size [1C] 13.5-22.5 pg; (germination cryptocotylar).

3 [list]/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); Kunzmann (2007) put the divergence of Agathis and Wollemia at at least 110 m.y. ago. Crown-group Araucariaceae may be 185-165 m.y.o. - or perhaps around 167.2 m.y.o. (Laenen et al. 2014) or 205 m.y.o. (see also Stöckler et al. 2002; Wallis & Trewick 2009). Biffin et al. (2010b) suggest ages of (215-)191(-169) or (94-)65(-47) m.y., the latter being their preferred age; 225-185 m.y. is the estimate in Knapp et al. (2007), 172-162 m.y. in Wilf and Escapa (2014, q.v. for other dates) and (134-)94, 81(-60) m.y. in Kranitz et al. 2014). 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 in Patagonian middle Jurassic deposits ca 160 m.y.o. has been associated with the monotypic section Bunya (Florin 1963; Stockey 1982, 1994; Hill & Brodribb 1989; Kunzmann 2007; see also Escapa et al. 2018). However, identification of Araucarioxylon wood can be difficult (Ash & Creber 2000). The crown-group position of the ca 52.2 m.y.o. South American Agathis zamunerae (Wilf et al. 2014, see Escapa et al. 2018) is in conflict with some of the ages above.

Evolution: Divergence & Distribution. See also Kranitz et al. (2014) for more ages. 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 question the placement of the early fossils just mentioned in extant sections of Araucaria; indeed, they form a basal polytomy along with A. hunsteinii and A. bidwillii (Escapa et al. 2018: support low; see also Kranitz et al. 2014).

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; Kooymnan et al. 2014; Kranitz et al. 2014; Escapa et al. 2018 for discussion), fossils being known from Europe as recently as the very Late Cretaceous ca 66 m.y.a. just before the KP boundary (van der Ham et al. 2010). Eocene fossils are well known from Patagonia (Markhofer et al. 2015). Although Araucaria is currently diverse on New Caledonia, there is little genetic divergence between the species, suggesting that the genus has not been there long (Gaudeul et al. 2012; Kranitz et al. 2014). In gymnosperms in general, rates of genome change are low, as are speciation rates, the two being correlated; however, Araucariaceae have overall very low rates of genome change when compared with all other land plants (Puttick et al. 2015).

There are questions about the long-term persistence of Agathis in New Zealand since the Eocene or before; Knapp et al. (2007; see also Kranitz et al. 2014) discuss this possibility. Many floristic elements in the island that are known fossil there in the Oligocene-Miocene subsequently seem to have become extinct, their contemporary representatives being relatively recent immigrants (e.g. Jordan et al. 2010; Puente-Lelièvre et al. 2012), however, the distinctive frog Leiopelma may be an ancient lineage that has persisted on the islands (Carr et al. 2015). 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). Dilwynites pollen is similar to that of Wollemia and some species of Agathis (so it could be the stem group of these genera); it is widely disributed in austral areas, its first records being from the Late Cretaceous up to 93.9 m.y.a. (Mcphail et al. 2013).

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), Escapa and Catalano (2013: most quantitative). Apomorphies for the family may be affected by the position of Wollemia within it.

Ecology & Physiology. Leaves in Araucaria may stay on the plant for 25 years or so (references in Chabot & Hicks 1982).

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 was 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 the two species of Agathiphagus (Agathiphagidae), a small group of near-basal jawed lepidoptera, eat the seeds of Agathis, and they are known from Australia to the Pacific (Shields 1988; Powell et al. 1998); the moths can diapause for up to twelve years. It has been suggested that they diverged from the Nothofagus-eating Heterobathmidae as much as 158.5 m.y.a. (Wahlberg et al. 2013), although on balance a position sister to Micropterigidae, together forming the basal branch of the lepidopteran clade, is favoured (Regier et al. 2015; Kristiansen et al. 2015; see also Mitter et al. 2016).

Genes & Genomes. Araucariaceae have the largest plastid genomes (ca 145 kb) in Pinales but with the greatest percentage (41.5%<) of non-coding content, in the latter feature they are in line with seed plants in general, except other Pinales and Gnetales (C.-S. Wu & Chaw 2016).

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 may be connected with branch shedding or cladoptosis, which is particularly striking here (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. The seeds of Wollemia have integumentary wings, unlike the seeds of other members of the family (Contreras et al. 2016).

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. For a comprehensive phylogeny of Araucariaceae, see Escapa and Catalano (2013). 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), but the former position seems more likely. A [Wollemia + Agathis] clade was retrieved in the comprehensive four-gene tree in Leslie et al. (2012) and by Escapa and Catalano (2013). Within Agathis, the New Zealand endemic Agathis australis is sister to the rest of the genus (e.g. Escapa et al. 2018 and references).

Botanical Trivia. Araucaria columnaris, the New Caledonian endemic Cook pine, leans towards the south in the northern hemisphere and to the north in the southern hemisphere, and the higher the latitude, the more pronounced the lean (Johns et al. 2017).

PODOCARPACEAE Endlicher  - Back to Pinales

Podocarpaceae

Podocarpic acid + [particular diterpene with phenolic ring]; (positive Maüle reaction); (nodes 1:2); sclereids numerous, with large lumen; transfusion tissue in leaf in patches lateral to vascular bundles, laterally-elongated sclereids in middle of lamina; microsporophylls with two sporangia; pollen exine thin, except distally; male gametophytes with 3-6(-8) prothallial cells, sperm nuclei unequal in size (one extruded); proembryo [E tier] cells binucleate; propagules fleshy; polyembryony common; cotyledon with two vascular bundles [?all]; nuclear genome size [1C] 4-11 pg (-13.8 pg - Manaoa colensoi).

17 [list]/186. Southern Hemisphere, to Japan, Central America and the Caribbean.

Age. The clade (Phyllocladus + Podocarpus] is ca 102 m.y.o. (Magallón et al. 2013), while other estimates are substantially older, (194-)145(-99) m.y. in Biffin et al. (2011b: c.f. Fig. 2) and still older, (259.2-)230.3, 226.9(-196.7) m.y. (Quiroga et al. 2016) - note the topologies of the last two.

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; leaves petiolate, held vertically, ?isobifacial; pollination droplet 0; ovuliferous cone facing sideways [= lateral], two ovules/scale, nucellus protrudes from micropyle; pollen germinates on ovuliferous scale and tubes grow over the scales [extra-ovular caputure and germination]; whole cone ± fleshy; n = 12.

1/1: Saxegothaea conspicua. South Chile and Argentina.

Synonymy: Saxegothaeaceae Doweld & Reveal

2. The Rest.

Leaves (opposite [Microcachrys]), petiolate or not, lamina (broad, with transfusion tissue), (multiveined, branching dichotomous - Nageia); plants dioecious (monoecious); (pollen not saccate - Phyllocladus), exine alveolate/honeycomb; ovuliferous scales not aggregated into cones (yes - Microcachrys), ± reduced, fused with ovule and ± enveloping it [looking like an integument]; (ovule erect); pollination droplet spreads along surface of scale, scavenges pollen; ovuliferous scale fleshy [= epimatium], fleshy (not); n = (9-)10(-15, 17-19).

16/185: Podocarpus (107), Dacrydium (20). Largely southern Hemisphere, scattered, N. to Japan, Central America and the Caribbean (map: from Florin 1963; Dalling et al. 2011; Adie et al. 2011). [Photos - Collection, Phyllocladus trichomanoides, Phyllocladus megasporangia, microsporangia.]

Evolution: Divergence & Distribution. Until the end of the Eocene Podocarpaceae were very common in southern Patagonia and dominated Antarctic forests - they were then replaced with Nothofagaceae (for their biogeography, etc., see Mill (2003), Kooyman et al. (2014), Pujana and Ruiz (2017), etc.. Retrophyllum, which still grows in south South America is known fossil from end-Cretaceous Argentina 67-66 m.y.a. (Wilf et al. 2017b). There are other Podocarpaceae currently not growing in the New World in Palaeocene/Eocene deposits in Argentinia (Kooyman et al. 2014; Merkhofer 2015 for references), and there are also well-substantiated reports of members of the family from the northern hemisphere in the Cretaceous and Early Caenozoic, e.g. Prumnopitys anglica from Eocene southeast England (Greenwood et al. 2013 and references). However, Pujana and Ruiz (2017) note that Podocarpoxylon fossils, quite common in the northen hemisphere, are unaccompanied by other remains that might be placed in Podocarpaceae and so are themselves unlikely to be Podocarpaceae, while this was not the case with fossils of that genus from the southern hemisphere.

\Podocarpaceae are still quite common and may dominate the vegetation, largely in the southern hemisphere, however, as Australia has dried out during the Caenozoic, podocarps have become 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) or earlier (Quiroga et al. 2016). Diversification in clades whose members have flattened foliage is notably greater, but younger, and is dated to (94-)64(-38) m.y.a. (Brodribb & Hill 2004; Biffin & Lowe 2011; Biffin et al. 2011b; Brodribb & Feild 2010), and crown-group Podocarpus, with 107 species representing well over half the family, is (81.8-)65.2, 60(-52.2) m.y.o., i.e. late Cretaceous or early Palaeogene, although it could be up to 37 m.y. older (Quiroga et al. 2016). Leslie et al. (2012) and Quiroga et al. (2016) offer more dates for splits within Podocarpaceae. Dacrydium may have moved into South East Asia via the Ninety East Ridge and India (Morley 2011). For possible roles of New Caledonia and New Zealand in the persistence of Podocarpaceae, see Condamine et al. (2016: metapopulations on ephemeral islands?).

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). Extant Podocarpaceae with broad leaves are shade tolerant and prefer warmer and higher rainfall conditions, and they also have fleshy diaspores, the often brightly-coloured seed being associated with a fleshy epimatium (Farjon 2018). Foliage variation in Podocarpaceae is considerable. 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, probably slightly after the venation density of angiosperm leaves increased - (94-)64(-38) versus 109-60 m.y. ago. In taxa like the spiral-leaved Afrocarpus the leaves orient themselves to form a spray of foliage, all leaves having their upper surfaces uppermost in the spray, but in the amphistomatous Retrophyllum all leaves twist in the same direction so the upper surface may face the lower side of the spray (Wilf et al. 2017b). 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 known from the Triassic and Jurassic (Biffin et al. 2011b).

Podocarp leaves decompose only slowly (although there are few studies on this), with a high concentration of condensed tannins (Ushio et al. 2017), 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). Soils beneath the tree may be low in both N and P, but Dacrydium gracilis, at least, effectively removes the little inorganic N that is there, while saprophytic microbes may contribute to the high acid phosphatase activity in the soil which relieves the P limitation (Ushio et al. 2017).

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, what these nodules might do is poorly understood (Dickie & Holdaway 2011).

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 mycoheterotroph, 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; Merckx et al. 2013).

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); if that genus is sister to the rest of the family, one may have to rethink aspects of the evolution of pollination mechanisms in Podocarpaceae (c.f. Leslie et al. 2015). See also Little et al. (2014) for pollination.

For details of seed morphology, dispersal, etc., and their evolution, see Contreras et al. (2016); the diaspores are usually fleshy and animal-dispersed, the epimatium/ovuliferous scale being variously developed and more or less surrounding the seed.

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 that dysploid chromosome evolution was quite common 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?). For cuticular features and how they may be affected by the environment, see Clugston et al. (2017). 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 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). The epimatium may be free from or adnate to the integument (see also Contreras et al. 2016 for seed morphology). Phyllocladus is sometimes described as having an aril, although this is more probably a somewhat reduced and retarded epimatium (de Laubenfels 1988).

The pollen of Phyllocladus has often been described as having a wing (e.g. Singh 1978), but a wing seems to be absent. 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). Cleavage 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 Podocarpus, see Mill (2014: summary of literature) and for 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, and for cuticle morphology, see Mills and Schilling (2009) and for wood anatomy, see Woltz et al. (2009 and references).

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; Quiroga et al. 2016). 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; c.f. Quiroga et al. 2016: Lagarostrobus in a different part of the family). 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; Quiroga et al. 2016: sister to [Microcachrys [Pherosphaera [Acomopyle + ...]]]; Leslie et al. 2012). This has considerable implications for character evolution in the clade; as Mabberley (2007) noted, the plant has some features reminiscent of Araucariaceae. For relationships within Podocarpus, see Biffin et al. (2011, 2012) and Quiroga et al. (2016).

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 [Taxaceae + Cupressaceae]]: secretory cells in the centre of the root [?or next node up]; two-year reproductive cycle/three-year, fertilization in 2nd/3rd year; pollen without sacci, not buoyant, exine shed on microgametophyte germination [microgametophyte naked]; ovuliferous cone horizontal to pendant, with <10 basal sterile scales; bract scale becoming narrowed at the base; ovuliferous scale adnate at base of bract scale, ovules erect, becoming inverted; prothallial cells 0; seed winged, 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; ca 230 m.y. is the estimate in Ran et al. (2018a).

Evolution: Genes & Genomes. The occurence of chloroplast genome isomers is scattered in this clade, but they are particularly common in Cupressoideae (Hsu et al. 2016; Qu et al. 2017).

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

Sciadopityaceae

Short shoots ultimately abscised [= cladoptosis]; roots with endomycorrhizal nodules; subsidiary cells 8-12/stoma; leaves on long shoots reduced to scales; short shoots +, with a pair of connate needles, apically bifid (not), vascular bundles surrounded by sheaths, petiole 0; 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, margin of ovuliferous scales fringed, ± connate; pollen chamber?; seeds (1-)7-9(-12)/scale; n = 10, nuclear genome size [1C] ca 20 pg, chloroplast accD gene to nucleus.

1 [list]/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). It has been found in Eocene Baltic amber 47-34 m.y.o. (Sadowski et al. 2016a).

Genes & Genomes. For the distinctive chloroplast genome of Sciadopitys with two inverted repeats and the formation of four chimaeric gene clusters, see J. Li et al. (2016) and Hsu et al. (2016); the former estimated that the chloroplast accD gene moved to the nucleus soon after Sciadopitys split from the other Cupressales.

Chemistry, Morphology, etc. There has been much debate over whether the photosynthesising structures of Sciadopitys 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, perhaps a rather odd arrangement for a leaf-derived structure. 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 considered the "needles" 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). The "needle" is thus comparable with the fascicles of separate needles in Pinaceae.

For a monograph, see Farjon (2005c), and for general information, see the Gymnosperm Database, for pollen, see Page (1990) and Uehara and Saichi (2011), and for ovule and cone, see Takaso and Tomlinson (1991).

[Taxaceae + Cupressaceae]: subsidiary cells 4-7/stoma; lamina vascular bundles ?surrounded by sheath; microsporangia hypodermal in origin; chloroplast trnQ IR +.

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.y.; ca 208 m.y. is the figure in Ran et al. (2018a).

Evolution. Ecology & Physiology. The evolution of cavitation-resistant xylem and stomata that stay open during periods of drought (Brodribb et al. 2014) can perhaps be placed at this node, although not all species show this combination of characters - Cunninghamia, Sequoiadendron and Glyptostrobus are examples.

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).

TAXACEAE Berchtold & J. Presl  - Back to Pinales

Bands of fibres in phloem crystalliferous, sclereids + [Taxus]; resin canal below vascular bundle in leaf; leaves shortly petiolate; plant dioecious (monoecious); pollen cones compound (simple), sporangiophores peri-(also hypo-)sporangiate, [pendulous from peltate scutellum to abaxial and with a phyllome-like adaxial process], pollen shed at 1-cell stage, inaperturate; ovuliferous cone pendulous, scales opposite; (ovules erect), pollen chamber +; male gametes unequal in size; disseminule fleshy, seed not winged, coat vascularized, with sarco- and sclerotesta; nuclear genome [1C] 11.5-30 pg.

6 [list]/30. Northern Hemisphere, scattered, also New Caledonia.

Age. The age of this node is (231-)187(-144) m.y. (Won & Renner 2006) or ca 134 m.y. (Ran et al. 2018a).

1. Cephalotaxus Siebold & Zuccarini

Cephalotaxaceae

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.

Taxaceae

Wood and phloem lack resin canals [?family]; (resin canals in leaf 0); 2-10 microsporangia/microsporophyll (partly connate - Austrotaxus); 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 [Amentotaxus], 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. Pollination Biology & Seed Dispersal. Fleshy disseminulkes occur throughout Taxaceae (see Leslie et al. 2017).

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). Cuticle/epidermis micromorphology is quite extensive (Elpe et al. 201), as is leaf anatomy (Ghimire et al. 2014a), but they do not suggest broad relationships.

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) and Dörken and Nimsch (2016), 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).

CUPRESSACEAE Bartling  - Back to Pinales

Cupressaceae

(Root stele pentarch); wood rays <10 cells tall; (stem apex with tunica/corpus construction); xylem or phloem resin ducts inducible [in separate clades]); branchlets deciduous [?level]; foliar resin canal single, abaxial to vascular bundle; leaves ± amphistomatic, shed along with branches; pollen cones in clusters/pseudowhorls; (1-)2-10(-14) microsporangia/microsporophyll; pollen shed at 2-cell stage; male gametophyte without sterile cell, gametes with separate cell walls; bract and seed scale ± evident, ovules develop on the base of the subtending scale [= subaxillary]; seed winged; n = 11; chloroplast large inverted repeat 0, smaller IR duplicating the trnQ gene, mitochondrial transmission paternal.

30 [list - as subfamilies]/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.y.; ca 171 m.y. is suggested by Ran et al. (2018a).

Jurassic fossils placed in crown-group Cupressaceae in morphological analyses, specifically in a clade along with Cunninghamis and Taiwania, in turn part of a pentatomy that made up the family as a whole (Escapa et al. 2008), are known from both Yorkshire, England - Elatides, Bajocian, ca 169 m.y.o. (Harris 1943), and Chubut, Argentina - Austrohamia, also early Jurassic and also known from China (Escapa et al. 2008; Bodnat & Escapa 2016).

1. Cunninghamioideae Silba

Cunninghamia

Leaves linear, twisted at the base, (margin denticulate), amphistomatous, petiole 0; 3(-6) microsporangia/microsporophyll; ovuliferous cone initially pendulous, bract scales lacking adaxial stomata; ovuliferous scale soon degenerating [small, <1/3 length of cone scale, free, margin initially 3-lobed], ovules 2-3(-6)/scale; seeds ca 2/bract scale; nuclear genome [1C] ca 12.5 pg.

1/2. Laos, Vietnam, Southern China, Taiwan (map: from Farjon & Filer 2013).

Synonymy: Cunninghamiaceae Siebold & Zuccarini

[Taiwanioideae [Athrotaxidoideae [Sequoioideae [Taxodioideae [Callitroideae + Cupressoideae]]]]]: extensions of torus in tracheidal pit; ovuliferous cone not proliferating.

2. Taiwanioideae L. C. Li

Leaves shortly linear, amphistomatous, petiole 0; bract scales with adaxial stomata, not narrowed at the base; ovuliferous cone initially erect, ovuliferous scale invisible; ovules (1-)2/bract scale, subaxillary; seeds ca 2/bract scale; nuclear genome [1C] ca 11.5 pg.

1/2. Northern Myanmar and Vietnam, S.W. China, Taiwan.

Synonymy: Taiwaniaceae Hayata

[Athrotaxidoideae [Sequoioideae [Taxodioideae [Callitroideae + Cupressoideae]]]]: pollen surface microverrucate/papillate.

3. Athrotaxidoideae L. C. Li

Leaves scale-like to linear, petiole 0; ovuliferous cone initially ?, ovuliferous scale soon degenerating, ovules 1-9/bract scale, adaxial thickening developing on adaxial side of bract scale above ovules after pollination; nuclear genome [1C] ca 10 pg.

1/2. Tasmania.

Synonymy: Athrotaxidaceae Doweld

[Sequoioideae [Taxodioideae [Callitroideae + Cupressoideae]]]: ?wood anatomy.

4. Sequoioideae Quinn

(Plant deciduous); shoots abscise [= cladoptosis]; (leaves opposite - M); ovuliferous cone initially erect; bract scales (opposite - Metasequoia), ovuliferous scale invisible; ovules 1-10/bract scale, in two (three - Sequoiadendron) series, adaxial thickening developing above ovules after pollination; pollination droplets coalescing; ovuliferous scales apparent after pollination; nuclear genome [1C] 9.5-10.5(-29 - Sequoia) pg. M = Metasequoia.

3/3: China, Pacific North America.

Synonymy: Metasequoiaceae Hu & W. C. Cheng, Sequoiaceae Luersson

[Taxodioideae [Callitroideae + Cupressoideae]]: ovules axillary to cone [= bract] scale, straight at maturity.

5. Taxodioideae K. Koch

(Plant deciduous); iso/chamaecydin + [terpenoids]; shoots ultimately abscise [cladoptosis]; ovuliferous cone initially pendulous (horizontal), ovuliferous scale late-developing, conspicuous after pollination, ovules 1-2(-5)/cone scale; (seed not winged - Taxodium); nuclear genome [1C] 9-10.5 pg.

3/4: East Asia, E. North America, Mexico.

Synonymy: Cryptomeriaceae Gorozhankin, Taxodiaceae Saporta

[Callitroideae + Cupressoideae]: fertile cone scales whorled, ovuliferous scale 0. (map: from Florin 1963, 1966; Farjon 2005c). [Photos - Collection.]

6. Callitroideae Saxton

(Leaves opposite); ovuliferous cone erect to pendulous, fertile cone scales 2 whorls, (central columella +); ovules 1-2(-3)/scale, (in two rows).

10/32: Callitris (15). Southern Hemisphere.

Synonymy: Actinostrobaceae Lotsy, Callitridaceae Seward, Diselmaceae A. V. Bobrov & Melikian, Fitzroyaceae A. V. Bobrov & Melikian, Libocedraceae Doweld, Neocallitropsidaceae Doweld, Pilgerodendraceae A. V. Bobrov & Melikian, Widdringtoniaceae Doweld

7. Cupressoideae Sweet

(Iso/chamaecydin +); nodes 1:2; leaves opposite [not in some seedlings], scale-like to linear; pollen cones often on elongated axes; (1-)2-10(-14) microsporangia/microsporophyll; fertile cone scales 2-6 whorls, (fleshy - Juniperus), (central columella 0); ovules 1-9(-many)/scale, in 1-6 rows (ovules 12< scale), (ovule 1/cone, terminal or not - Microbiota); (cone fleshy, not opening); seeds (not winged); cotyledons (-9(-15)), nuclear genome size [1C] 9-14(-38 - Juniperus) pg.

29/131: Juniperus (67), Cupressus (12). Esp. Northern Hemisphere, also N.E. Africa.

Synonymy: Arceuthidaceae A. V. Bobrov & Melikian, Juniperaceae Berchtold & J. Presl, Limnopityaceae Hayata, Microbiotaceae Nakai, Platycladaceae A. V. Bobrov & Melikian, Tetraclinaceae Hayata, Thujaceae Burnett, Thujopsidaceae Bessey

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 Spencer et al. place it. >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 may 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). Cunninghamia itself is known from the Late Cretaceous (Buczkowski et al. 2015 and references). Herrera et al (2016) review fossils that can be linked to Cunninghamia and Taiwania (these are basal clades of Cupressaceae). The largely New Guinean Papuacedrus is known from Eocene deposits in Argentinia (Wilf et al. 2009; see also Kooyman et al. 2014: this and other genera). Wilf and Escapa (2014) suggest some fossil-based dates within this clade.

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 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-resistant 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. (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 the basal topology of the family, [Cunninghamioideae [Taiwanioideae [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, while loss of ovuliferous scales and other characters are best placed within the family and are not apomorphies for it (see above). For apomorphies for basal members of Cupressaceae, somewhat adjusted above, see Schulz and Stützel (2007: unfortunately Juniperus etc. not included), for wood anatomy and phylogeny, see Román-Jordán et al. (2016).

Ecology & Physiology. Biomass estimates for forests with Sequoia sempervirens are 2.3 x 106 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.

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 when there is pollen from other Cupressaceae in the pollination drops, but not when there is pollen from angiosperms or Pinus.

For monoecy, dioecy, etc., see Jagel and Dörken (2015a). There is paternal apomixis in Cupressus dupreziana, unknown in any other seed plant (but c.f. androgenesis in Solanaceae); here the embryo develops from unreduced male gametes (Pichot et al. 2000, 2001).

For details of seed morphology, dispersal, etc., and their evolution, see Contreras et al. (2016); dry and winged (the wings develop from the ovules) seeds are common, but Juniperus is noted for its fleshy disseminules.

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).

Genes & Genomes. See Zonneveld (2014) for discussion of genome size in taxa like Juniperus; there are connections with polyploidy, as elsewhere in Pinales.

Cryptomeria japonica has a much reduced chloroplast inverted repeat containing only a few genes (Hirao et al. 2008), and the loss of this repeat in Cupressaceae is connected with the fact that the plastome size is often small in Cupressaceae, as in Callitris where it is only about 121 kb (Wu & Chaw 2016). For the organization of the chloroplast genome in the whole family, see C.-S. Wu and Chaw (2016) and Qu et al. (2017) and references. Wu and Chaw (2016) noted the frequency of inversions within this clade - there are some 28 - compared to other conifers (Araucariaceae, for example have none, Taxaceae and Podocarpaceae only one).

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 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 (= cone) scales (Zhang et al. 2004; see also Farjon 2005c; Jagel & Dörken 2015a), but Cryptomeria has several "teeth" on the ovuliferous scale and some other subfamilies have structures that appear to be much reduced ovuliferous scales (see also Schulz & Stützel 2007). However, the ovuliferous scales and ovules may be interpreted as the products of serial buds in the axils of the bract scales, the oldest buds being furthest away from the bract scale, rather as are sometimes found in the vegetative part of the plant (Dörken & Rudall 2018: note interpretation of epidermal layer surrounding the ovule in terata). In some Cupressoideae the ovules are not axillary (Jagel & Dörken 2015a). There is substantial variation in how the cone develops, the seeds being enclosed in various ways (e.g. Jagel & Dörken 2014; Dörken & Rudall 2018) and varying considerably in both their numbers and positional relationships to the bract scales (e.g. Jagel & Dörken 2015a).

For a monograph (and far more) see Farjon (2005c); general information can be found in the Gymnosperm Database. For some terpenoids, see Otto et al. (2002), and for cone and ovule morphology, see e.g. Lemoine-Sébastien (1968a, b), Takaso and Tomlinson (1989, 1990, 1992), Jagel and Stützel (2001), Farjon and Garcia (2003 and references) and Jagel and Dörken (2014, 2015a, b).

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 probably [Cunninghamioideae [Taiwanioideae [Athrotaxidoideae [Sequoioideae [Taxodioideae [Cupressoideae + Callitridoideae]]]]]] (Mao et al. 2012: support usu. strong; Sen et al. 2016; Z.-D. Chen et al. 2016: no Athrotaxis), but 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 analyses two or more members of the first three branches may unite to 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. Indeed, Zhu et al. (2018) found that a ca 15 kb part of the plastome, the ycf1/2 area, helped to produce the conflicting relationships that have been obtained in this area (e.g. Farjon et al. 2002; Little et al. 2004; Mao et al. 2010; Terry & Adams 2015 and references), inclusion of that segment in plastome analyses giving a [Juniperus + Cupressus] clade, while in other analyses the clade {Cupressus [Xanthocyparis [Callitropsis + Hesperocyparis]]] was recovered. This ycf1/2 area is evidence of a very ancient introgression event some 60-40 m.y.a. (Zhu et al. 2018).

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), Little (2006) and Zhu et al. (02018) and for those 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.