LIGNOPHYTA
Plant a shrub or tree; true roots +, origin endogeneous, root cap +, apex multicellular; endodermis +; shoot apical meristem multicellular; lateral meristems +, cork cambium producing cork abaxially, vascular cambium producing phloem abaxially and xylem adaxially; lamina with mean venation density 1.8 mm/mm2 (to 5 mm/mm2).
EXTANT SEED PLANTS/SPERMATOPHYTA
Plant woody, evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols, thus containing p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction; root xylem exarch, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular tissue around central pith [eustele], vascular bundles with interfascicular tissue, ectophloic, endodermis 0, xylem endarch; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium ["nodes 1:1"]; vascular bundles collateral [stem: phloem external; leaf: phloem abaxial]; stomata morphology?, pore opening controlled by abscisic acid; leaves with petiole and lamina, spiral, development basipetal, blade simple; axillary buds +, not associated with all leaves; prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg, gametes two, developing after pollination, with cell walls, flagellae numerous; ovules increasing considerably in size between pollination and fertilization, female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryo straight, shoot and root at opposite ends [allorrhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.
EXTANT GYMNOSPERMS/PINOPHYTA/ACROGYMNOSPERMAE
Biflavonoids +; cuticle wax tubules with nonacosan-10-ol; ferulic acid ester-linked to primary unlignified cell walls; phloem with sieve and Strasburger/albuminous cell pairs, the two not derived from the same immediate mother cell, sieve area with small pores generally less than 0.8 µm across that have cytoplasm and E.R., joining to form a median cavity in the region of the middle lamella, phloem fibres +, scattered; stomata subsidiary cells not produced from the same cell that gave rise to the guard cell initials [perigenous], stomatal poles raised above pore, no outer stomatal ledges or vestibule, epidermis lignified; sclereids +, ± tracheidal transfusion tissue +; buds with scale leaves/cataphylls; plants dioecious; microsporangium with exothecium; pollen tectate, infratectum alveolate [esp. saccate pollen], endexine lamellate at maturity; ovule unitegmic, with pollen chamber formed by breakdown of nucellar cells, nucellus massive; pollination droplet +, ovules aborting unless pollination occurs, fertilisation 7 days to 4-6 months or more after pollination, pollen germinates in two or more days, tube with wall of pectose + cellulose microfibrils, branched, growing away from ovule 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 producing a sterile cell and two gametes released by the breakdown of the pollen grain wall, male gametes with >1000 cilia; female gametophyte with radially-elongated cells [alveoli] that grow centripetally, the nucleus of the female gamete being on the open face and connected to adjacent nuclei by spindle fibres; seed fleshy, testa mainly of coloured sarcoexotesta and scleromesotesta, ± vascularized, and ± degenerating endotesta, ± vascularized; first zygotic nuclear division with chromosomes of male and female gametes lining up on separate but parallel spindles, embryogenesis initially nuclear; gametophyte persists in seed; genome size [1C value] 3.5-14 pg; two copies of LEAFY gene and three of the PHY gene, [PHYP [PHYN + PHYO]], second intron in the mitochondrial rps3 gene [group II, rps3i2].
PINALES Gorozh. Main Tree, Synapomorphies.
Tree branched; compression wood +; wood pycnoxylic; tracheid side wall pits with torus:margo construction, bordered; phloem with scattered fibres alone [Cycadales?], resin ducts/cells in phloem [and elsewhere]; lignins lacking syringaldehyde [Mäule reaction negative]; cork cambium ± deep seated; bordered pits on tracheids round, opposite; (cladoptosis +); nodes 1:1; axillary buds + (0); leaves with single vein; plants monoecious; microsporangiophore/filament simple with terminal microsporangia; microsporangia abaxial, dehiscing by the action of the hypodermis [endothecium]; pollen exine thick [³2 µm thick]; ovulate strobilus compound, ovuliferous scales flattened, ± united with bract scales; ovules lacking pollen chamber; pollen tube unbranched, growing towards the ovule, wall with arabinogalactan proteins, gametes non-motile, lacking walls, released from the distal end of the tube, siphonogamy; seed coat dry, not vascularized; proembryo with 2 to 4 nuclear divisions, with upper tier or tiers of cells from which secondary suspensor develops, elongated primary suspensor cells and basal embryonal cells [or some variant]; germination phanerocotylar, epigeal, (seedlings green in the dark); plastid and mitochondrial transmission paternal, one duplication in the PHYP gene line, one copy of chloroplast inverted repeat missing. - 7 families, 68 genera, 545 species.
Note: Possible apomorphies are now being added throughout the site; they are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is because there is very considerable homoplasy, with variation within and between clades, for most characters. Furthermore, the basic information for all too many characters is very incomplete, often coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed... In particular, if Gnetales are to be included here, depending on where they end up, apomorphies could change considerably.
Evolution. Divergence & Distribution. There are no known synapomorphies for a clade containing living and fossil conifers (e.g. Rothwell & Serbet 1994). The morphology of extinct conifers and coniferophytes is being re-evaluated as the morphologies of entire organisms are pieced together from what used to be separate form genera; the result is that many of the conventional taxonomic groupings are being radically overhauled (e.g. Rothwell et al. 2005; Hernandez-Castillo et al. 2009; see also below). As this is done, the extent of the diversity of these fossil plants is becoming clear. Not only are forked leaves common, but stomatal distribution, etc., may differ dramatically on leaves from the one plant, compound microsporangiate strobili are known (c.f. Gnetales!), as are megasporagiate strobili which do not terminate vegetative growth of the axis on which they occur (e.g. Hernandez-Castillo et al. 2001; Rothwell & Mapes 2001).
Clarke et al. (2011: 95% credibility intervals) suggested a crown age for this clade of (286-)252(-212) m.y., Magallón et al. (2013: with temporal constraints) suggested an age of ca 278.1 m.y.; in both Gnetales were included.
Leslie et al. (2012) suggest ages for several clades within Pinales (see below), and evaluate the fossil data critically; their four-gene tree is based on an almost complete sampling of the group. The current distributions of many extant conifer groups is much smaller than and/or very different from their past distributions. Many conifers have fossil records going back to the Cretaceous; see Manchester (1999) for north temperate distributions), McIver (2001) for fossils of the African Widdringtonia (Cupressaceae) in rocks of Cretaceous age in Alabama. For the early Tertiary 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) Tertiary phenomenon, which would question the attribution of early fossils at least to those families. Indeed, podocarps with broader leaves seem to have diversified considerably in the earlier Tertiary in the southern hemisphere (Brodribb & Hill 2004; Biffin & Lowe 2011 - see below).
Diversification in most conifer genera is Tertiary in age, but Leslie et al. (2012) note that divergence ages in most southern hemisphere clades is older than that of northern clades, and this is particularly true of the southern Cupressaceae-Callitroideae - its mean node age is four times that of the northern Cupressaceae-Cupressoideae. Leslie et al. (2012) aasociated this with the more equable climate in at least parts of the southern hemisphere compared with the major climate swings in the northern hemisphere beginning in the Oligocene.
Ecology & Physiology. Brodribb et al. (2012) emphasized that conifers in general can out-compete angiosperms in a number of environments that were not high in nutrients. There are at least four major clades involved: Pinaceae, mostly northern, [Araucariaceae + Podocarpaceae], mostly southern, and two major clades in Cupressaceae that have largely inhabited the northern and southern hemispheres since the Jurassic (Brodribb et al. 2012). Many conifers, but less the [Podocarpaceae + Araucariaceae] clade, tolerate extreme cold, they grow well in high-light environments, and despite lacking vessels their wood shows moderate hydraulic conductance and is resistant to cavitation, etc. (Brodribb et al. 2012). Litter and wood decay of conifers in general is slower than that of angiosperms (e.g. Wardle et al. 2008; Weedon et al. 2009), and root decay of Pinales in particular is slower (Silver & Miya 2001). Many Pinaceae grow successfully in low N and podocarps in low P conditions (Brodribb et al. 2012). Conifers frequently dominate the communities in which they grow, and are often long-lived plants; they prefer high-light conditions, not infrequently associated with infrequent catastrophic disturbances that allow seedling establishment. Emergent conifers in particular can have little effect on the forests in which they grow; the basal area of angiosperm trees in forests with or without these emergents, but which are otherwise comparable, are similar (Enright & Ogden 1995; Aiba et al. 2007). Finally, seventeen species of conifers scattered in Pinaceae, Araucariaceae, and Cupressaceae, along with 29 species of Dipterocarpaceae and especially Eucalyptus, are "giant trees" at least 70 m tall (Tng et al. 2012).
Leaf mass per unit area seems to be correlated with genome size, but this may be because of phylogenetic correlations (Beaulieu et al. 2007b).
Plant-Animal Interactions. Hudgins et al. (2003, 2004) examined the diversity of bark beetles in conifers in the context of various plant structures that might be defences against such beasts; Franceschi et al. (2005) elaborate on the pine-beetle story. Conifers in general have layers of polyphenol-containing parenchyma cells in the phloem, possibly offering some protection against insects. Pine beetles, Dendroctonus spp., can be noxious pests and invade living pines; they tend to have relatively few hosts, but outbreaks can be devastating (Kelley & Farrell 1998: host specificity; Wood 1982 and Wood & Bright 1992: the weevils). The bark beetles eat the wood despite the presence of resin ducts in both phloem and xylem in Pinaceae, and there are also intracellular crystals, etc., which could be protective. Blue-stain fungi, species from a few unrelated ascomycete genera that are carried by the pine beetles, can quickly invade the sapwood and render it non-functional, basically clogging it up and killing the plant surprisingly quickly; some, at least, also detoxify the plant's defences, so protecting the beetle (DiGuistini et al. 2011). Other families of Pinales have resin ducts only in the xylem and harbour a lower diversity of these beetles. 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). Various elements of the defences are constituive and/or inducible, methyl jasmonate being part of the inductive pathway (e.g. Hudgins et al.2003; Hudgins & Franceschi 2004).
Pitterman et al. (2005), Hacke et al. (2005) and Sperry et al. (2006) compare water transport in tracheids that have the torus:margo pits found in many conifers (including Ginkgo), with that in other kinds of tracheids and in vessels. Pore size in the margo is relatively large, while the torus provides a valuable safety feature guarding against embolism. Indeed, hydraulic conductance in tracheids with torus:margo pits is somewhat greater than in vessels of similar diameter when expressed on a sapwood area basis, while studies of cavitation in this system suggest that it is not connected with the size of the pores in the margo, but rather with the torus:pit aperture ratio (Pittermann et al. 2010).
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).
Pollination Biology & Seed Dispersal. Much has been learned about pollination and pollen germination in conifers in the last few years, although important early work had been carried out about 80 years ago. Pollen directly impacts the ovulate cones of conifers rather than being swept around the cone by a turbine-like action (Cresswell et al. 2007). It had been thought that the sacci on the pollen of some conifers facilitated its dispersal by wind, however, at least sometimes they probably function more like water wings; within Pinales there is a correlation between presence of pollen sacci or wings and exine thickness and structure, whether (no wings) or not (wings) the pollen is wettable, etc. (Tomlinson 1994). Pollen sacci help orient the pollen grains in the pollination droplet (Doyle & O'Leary 1935; Salter et al. 2002 and references), or, more particularly, when the ovules are inverted, a common condition, the pollen grains are wetted and float up to the micropyle where the saccus orients the grain on the nucellus, separating and exposing the sulcus through which the pollen tube germinates (Salter et al. 2002; Leslie 2010b). Sacci also help in the selection of pollen grains during pollination. Thus the proportion of saccate to non-saccate pollen grains inside the ovules is higher than that outside (Leslie 2009). In Phyllocladus and many taxa with erect ovules the pollination droplet is resorbed through the micropyle, and again the pollen grains are brought close to the nucellus; in Juniperus communis and other taxa this resorbtion may be an active process happening quite soon after the pollen grain lands (Mugnaini et al. 2007). There are further variants of these pollination mechanisms in Coniferales (Owens et al. 1998; Salter et al. 2002; Fernando et al. 2005 for references) and other ancient gymnosperms (Leslie 2008). For additional information on pollination, see Doyle (1945), Tomlinson (1994, 2000), Tomlinson et al. (1997), and Tomlinson and Takaso (2002).
for pollination, see Doyle (1945), Tomlinson (2000), Tomlinson et al. (1997), and Tomlinson and Takaso (2002), and for reproductive biology, Williams (2009)Recent work suggests that the situation is more complex. Sacci may increase the distance the pollen grain can travel before it falls to the ground, so facilitating wind dispersal (Schwendemann et al. 2007). However, this depends on the nature of the sacci; if they have extensive air sacs, as in Pinus, they are likely to travel further, but if the sacci are composed of denser material, as in Falcatfolium, then they will fall faster - as they may if the surface of the pollen grain is not smooth (Grega et al. 2013).
There is considerable variation in the development of the male gametophyte (Fernando et al. 2010: summary and terms used). Pollen germination varies, and the feature "pollen exine shed during microgametophyte germination", is likely to have evolved more than once (?three times) in Pinaceae alone (see also Rydin & Friis 2005); for cell death induced by the growing pollen tube, see Fernando et al. (2005 and references).
Bateman et al. (2011) 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.
Genes & Genomes. C.-S Wu et al. (2011b) suggested that a different copy of the inverted repeat had been lost in Pinaceae and in the clade making up the rest of the order. See also Raubesen and Jansen (1992a), Lackey and Raubeson (2008) and Hirao et al. (2008) for the loss of a copy of the inverted repeat, and Zonneveld (2012) for genome size.
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).
The interpretation of the stem apex in terms of the tunica-corpus layering is not easy (see Napp-Zinn 1966). I have not integrated much of the considerable variation in wood anatomy with the clades recognised here (see e.g. Zhou & Jiang 1992 for information). Cork cambium is often more or less deep seated, although in Sequoia and Phyllocladus (e.g.) is is superficial (Möller 1882). Calcium oxalate microcrystals are commonly found in some cell walls throughout the group (Fink 1991; Hudgins et al. 2003: ?Cephalotaxaceae, Sciadopityaceae), but their distribution in other gymnosperms is unclear; they may be absent. Their position within tissues is linked with the development of fibres, the amount of resin secreted, etc. (Hudgins et al. 2003). There is generally a single trace per leaf, but if the leaves are opposite, there may be two traces, but then they fuse before they enter the petiole (Namboodiri & Beck 1968a, b). Leaf traces can also make connections with xylem produced during the second and subsequent years (Maton & Gartner 2005), and secondary growth (only phloem is produced) has been reported from the leaves of a number of conifers (Ewers 1982). Short shoots occur in a number of taxa (see Dörken et al. 2012 for a summary), and branch shedding, also occurring in taxa other than those with short shoots, is widespread (Burrows et al. 2007 and references). Organised bud meristems usually occur in the axils of only some leaves, although more cryptic meristems are quite widespread (Namboodiri & Beck 1968a; Fink 1984; Burrows 1999, 2009); in taxa like Pinus and Sciadopitys axillary buds are much more common, although most produce short shoots.
Bisexual strobili that have ovuliferous scales above the microsporangia, i.e., the same basic arrangement as in angiosperm flowers, are scattered through the clade (Flores-Rentería et al. 2011). Basic cone morphology is very variable. Conifer seed cones have becoming more massive and strongly constructed since the Triassic, and particularly the Jurassic, presumably in reponse to animal predation pressure (Leslie 2011). Among extant taxa, Taxus has tiny female cones each with a single, erect ovule, but cones are often massive structures. The ovuliferous scale is often well-developed and the bract scale inconspicuous, or the bract and ovuliferous scales may be largely separate, as in Pseudotsuga, while in Cupressaceae there is little evidence of an ovuliferous scale in the mature cone, which consists largely of bract scales (Schulz & Stutzel 2007; Rothwell et al. 2011 for references). Understanding details of the morphological evolution of cones will depend on advances in our understanding of the fossil record, and it is likely that heterochrony has been involved; Cupressaceae can be linked with the fossil Voltziaceae (e.g. Rothwell et al. 2011). Developmental studies may also be of value. Thus Englund et al. (2011) found that gene expression patterns linked the epimatium of
A branched pollen tube occurs sporadically in Pinales (Friedman 1987 for references). The nature of the male gametes needs more study. Some taxa have binucleate sperm cells, i.e., a cell plate does not form in the spermatogeneous cell, or, if it does, it is incomplete. The male gametes here may be unequal in size, as in Dacrydium, and one may even be extruded from the cytoplasm, as in Podocarpus spp. and Taxus. In at least some Gnetum, Podocarpus andinus, and Torreya taxifolia two unequally-sized male cells are produced (Singh 1978 for literature; I am grateful to Ned Friedman for help in understanding this complicated pattern of variation). Double fertlization may sometimes occur in Pinales (Friedman 1992). The free-nuclear stage in the proembryo of Pinales is shorter than that of other gymnosperms, being only 5 or 6 rounds of nuclear division in Podocarpaceae and Araucariaceae and 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. There is extensive duplication of the knox-1 gene within Pinaceae, at least, although more general sampling is needed to pin down the point at which this duplication occurred (Guillet-Claude et al. 2004).
For a classic study of both fossil and extant conifers, see Florin (e.g. 1951); see also Page (1990) and especially Gifford and Foster (1988), Farjon (2005b) for a bibliography, and Debreczy and Rácz (2006) and Eckenwalder (2009) for general accounts. For cleavage polyembryony, see Doyle and Brennan (1972), and for reproductive biology, Williams (2009). See also Geyler (1867), Barthelmess 1935, and Kumari (1963: nodal anatomy), Möller (1882: cork cambium), Butts and Buchholz (1940: cotyledon number), Herrmann (1951: intergeneric grafting), Napp-Zinn (1966: leaf anatomy), Den Outer (1967) and Schulz (1990), both phloem anatomy, much detail unincorporated, Zhou and Jiang (1992: wood anatomy); see also Owens et al. (1995b: cytoplasmic inheritance, nuclei sometimes incorporate cytoplasm), Mundry (2000: cone/strobilus development, emphasis on Taxaceae and friends), Trapp and Croteau (2001a: resin biosynthesis), Sklonnaya and Ruguzova (2003: spermatogenesis), (Bobrov & Melikian 2006: seed anatomy, both testa and tegmen present?), and Mathews and Tremonte (2012: greening of seedlings in the dark). A valuable resource is Gymnosperm Database (Earle 1997 onwards)
Phylogeny. Given the uncertainty in our knowledge of the relationships between the major seed-plant clades, direct links to them are provided here: Cycadales, flowering plants, and Pinales; for general discussion, see seed plant evolution.
Within conifers, relationships are being substantially clarified. Pinaceae (Pinus, Cedrus, etc.) are sister to the rest, as a morphological cladistic analysis by Hart (1987) suggested some time ago (but c.f. Nixon et al. 1994; Doyle 1996b). Molecular data and additional morphological work largely confirm the relationships in the tree here, which is based on the work of Quinn et al. (2002: successive approximations weighting), see also Price et al. (1993), Tsumura et al. (1995: RFLP analysis, tree [unrooted] with the same topology as that used here), Kelch and Cranfill (2000), Gugerli et al. (2001: e.g. the mitochondrial nadI gene), Rai et al. (2002, especially 2008a), and, more recently, the four-gene analysis of Leslie et al. (2012) with its excellent sampling (but not Gnetum, etc.). However, the topologies in the scenarios of Biffin et al. (2010b) are either [Pinaceae [Podocarpaceae + Araucariaceae]] or [Pinaceae + Sciadopityaceae, etc.]... Gnetales are here included in Pinales (see discussion on Cycadales page).
For relationships in the Cephalotaxaceae-Taxaceae area, which for some time were rather uncertain, see below.
Classification. Producing evolutionary classifications, or classifications that emphasise one or two favored morphological characters, seems to remain popular with those working on conifers (e.g. Keng 1975; Melikian & Bobrov 2000; Fu et al. 2004 [Nageiaceae and Podocarpaceae well separated], Bobrov & Melikian 2006 [Araucariaceae and other conifers form a lineage quite distinct from Pinaceae and Sciadopityaceae]).
See Farjon (1990, 2005a, c) for detailed treatments of the conifers, Farjon (2001) for a checklist.
Includes Araucariaceae, Cupressaceae, Pinaceae, Podocarpaceae, Sciadopityaceae, Taxaceae.
Synonymy: Abietales Link, Actinostrobales Doweld, Araucariales Gorozh., Athrotaxidales Doweld, Cephalotaxales Reveal, Cunninghamiales Doweld, Cupressales Bromhead, Falcatifoliales Melikian & Bobrov, Metaxyales Doweld, Microstrobales Doweld & Reveal, Parasitaxales Melikian & Bobrov, Podocarpales Reveal, Saxegotheales Doweld & Reveal, Sciadopityales Reveal, Taxales Knobloch, Taxodiales Heintze - Araucariidae Doweld, Cupressidae Doweld, Pinidae Cronquist, Takhtajan, & Zimmermann, Podocarpidae Doweld & Reveal, Taxidae Reveal - Araucariopsida A. V. C. F. Bobrov & Melikian, Pinopsida Burnett, Podocarpopsida Doweld & Reveal, Taxopsida Lotsy - Pinophytina Reveal
Gnetaceae clade + Pinaceae: plant ectomycorrhizal; binucleate sperm cells, basic proembryo structure, development of polyembryony.
Evolution. Divergence & Distribution. Davies et al. (2011: 95% credibility intervals) suggested an age for this clade of (259-)219(-174) m.y.
PINACEAE F. Rudolphi Back to Pinales
Plant (deciduous), ectomycorrhizae +; specialized resin diterpenes, e.g. with abietane/pimarane skeletons, biflavonoids 0; xylem resin ducts +, inducible, (also constitutive); sieve cells with nacreous walls, sieve tube plastids also with protein fibres; phloem resin ducts +, constitutive or inducible, also with sclereids, intracellular calcium oxalate crystals, etc.; (axillary buds common, producing short shoots [leaf fascicles; spur shoots]), (plant deciduous); leaves with two vascular bundles; 2 microsporangia/ microsporophyll, sporangia superficial, pollen saccate (not), exine thin [2³ µm] except distally, (atectate, exine granular - Pseudotsuga, Larix [not saccate]); bracts free from the ovuliferous scale, ovules 2/scale, inverted, (pollination droplet 0); (pollen exine shed during microgametophyte germination - Larix, Pseudotsuga); free-nuclear stage with only four nuclei [= embryo tetrad]; seeds 2/scale, dry, winged, wing terminal, developing from adaxial side of scale, (from integument; wingless); (integument with resin canals); cotyledons (2-)4-11(-20); n = 12 (13, Pseudolarix = 22); plastid inverted repeat very small [e.g. ndh and rps16 genes lost], PHYP gene duplicated; genome size [1C value] large, 14-35 pg; germination epigeal (hypogeal - Keteleeria).
11/210: Pinus (105), Abies (46), Picea (33). North Temperate (map: from Florin 1963; Farjon 1984, 1990a). [Photos - Collection]
Evolution. Divergence & Distribution. There are fossils identified as Pinaceae in ca 150 m.y.o. Upper Jurassic deposits (Rothwell et al. 2012; see also Miller 1999), while the recently-described Pinus yorkshirensis, a cone associated with needles, in Lower Cretaceous deposits 131-129 m.y. old forms a polytomy with extant and some other fossil species in morphological analyses (Ryberg et al. 2012). Fossils assigned to Pityostrobus are scattered through the family tree (Ryberg et al. 2012).
Magallón et al. (2013: with temporal constraints) suggested an age of (161.2-)153.8-153.1(-150.1) m.y. for crown Pinaceae. Various divergence estimates were provided by Gernandt et al. (2008), e.g. maximum dates of 196-173 m.y. (Jurassic) and 165-148 m.y. for Pinaceae crown and Pinus crown groups respectively, other clades were a little younger.
Fossil constraints yielded a stem-group age for Pinus of (132-)128(-124) m.y. (Eckert & Hall 2006). However, some estimates in Gernandt et al. (2008) yield estimates of ca 87-72 m.y. for crown Pinus, while Crisp and Cook (2011) suggested that Pinus and Picea diverged some time around the K/T boundary ca 65 m.y.a. For divergence times within Pinaceae, see also Wang et al. (2000: stem-group Pinus ca 140 m.y.o.) and Lin et al. (2010). Willyard et al. (2007) estimated upper (permineralized wood) and lower dates for divergence of Pinus subgenera of 85 and 45 m.y. respectively (for the latter, see also Magallón & Sanderson 2005), although there were bouts of speciation much later. Millar (1998) had suggested that Pinus subgenera Pinus and Strobus and some sections had separated by the middle of the Cretaceous, however, Cretaceous fossils ascribed to the genus have not yet been shown to nest within it (Klymiuk et al. 2011; Ryberg et al. 2011). Le Page (2003; see also Wang et al. 2000) thought that there was an episode of diversification in the family in the Palaeocene.
Ecology & Physiology. For general information, see Andersson (2005) and especially Brodribb et al. (2012). Pinaceae dominate huge areas of mostly cool temperate and boreal forests in the northern hemisphere, although in suitable conditions Pinus-dominated forests occur even in Costa Rica (Janzen 1983) and even south of the equator in montane Sumatra (Map: from White et al. 2000; Andersson 2008: see also Clade Asymmetries). The restriction of the family to these forests is remarkable, but for the most part Pinaceae are unable to compete in tropical broad-leaved rain forests (but see the relatively broad-leaved Pinus krempfii: Brodribb & Feild 2008). Live above-ground biomass estimates are in the order of 0.8-0.9x106 kg ha-1, Pseudotsuga menziesii perhaps even reaching 1.6x106 kg ha-1 (see Franklin & Dryness 1973).
Pinaceae dominate many (warm) temperate and boreal forests on less fertile soils (see below), where they thrive in high-light conditions; they have high leaf mass per unit area and also a very high leaf area index, and although seedlings of evergreen angiosperms have a lower photosynthetic rate they tolerate leaf water stress better (Fu et al. 2012). Fires open the forest canopy, so making conditions suitable for Pinus in particular, many species of which are adapted to fire-prone environments (Brodribb et al. 2012; see also Schwilk & Ackerley 2001; Keeley 2012). In Pinus, He et al. (2012; see also Bond & Midgley 2012) have dated the acquisition of thick bark that is resistant to low intensity fires to (147-)126(-105) m.y.a., and thick bark, often linked with serotinous cones and adapted to high intensity (crown) fires, to (96-)89(-80) m.y.a. (these dates clash with some of those above).
Plant-Animal Interactions. Ambrosia and bark beetles (Curculionidae: Platypodinae, Scolytinae: see Wood 1982; Wood & Bright 1992), highly derived weevils, seem to have been associated ancestrally with conifers - although this is perhaps questionable (Jordal et al. 2011) - then shifted on to angiosperms and finally back to conifers several times. Their current diversity in Pinales is lower than elsewhere (Farrell et al. 2001). Bark beetles make their gallery systems in phloem, ambrosia beetles in the wood (although early-branching members of the ambrosia beetle clade may still live in phloem), and they mostly live in dead or dying wood. Ambrosia beetles are haplodiploids that show parental care; they have intricate cuticular invaginations in which they carry a fungus inoculum and the beetle larvae eat yeast-like bodies proliferating in the galleries they make (Jordal et al. 2000; Cognato et al. 2011 and references). In those weevils that cultivate and eat fungi the mouth-parts are also much modified; development of cultivation is unreversed (Beaver 1989; Farrell et al. 2001; Jordal et al. 2008 and references, 2011). Not only pine beetles and fungi, but yeasts, bacteria (some nitrogen-fixing), parasitoids of the beetles and fungus-eating nematodes all form part of a very complex association (e.g. Rivera et al. 2009: yeasts and bark beetles). Pine beetles of the genus Dendroctonus can be noxious pests and invade living pines; such species tend to have relatively few hosts, but outbreaks can be devastating (Kelley & Farrell 1998 for host specificty).
Some 70 species of Adelgidae (aphids) are restricted to Pinaceae, and include Adelges piceae and A. tsugae, serious introduced pests in North America (Havill et al. 2007). There are five different generations in a single life cycle, the sexual, gall-forming generation being on Picea; as with other aphids, vertically transmitted bacteria are part of this ecosystem (Havill & Foottit 2007). Cecidomyiid gall midges are quite common on the family in North America (Gagné 1989). See Powell et al. (1999) for other insect-conifer associations.
Details of the evolution of the resin defence system (e.g. Hudgins et al. 2004) depend on the phylogeny of the family, which is currently unclear (see below). However, Pinaceae do have a very well-developed resin defence system, yet they are more susceptible to beetle attack than are other conifers (e.g. Hudgins et al. 2004, see above). Keeling and Bohlmann (2006a esp., b) describe terpenoid diversity and conifer defence mechanisms, a complex subject; it is unclear just what is responsible for the considerable diversity of terpenoids in conifers, although multisubstrate and multifunctional enzymes involved in terpenoid synthesis in Picea sitchensis (Sitka Spruce) could produce a variety of products from a variety of substrates (Hamberger et al. 2011). Iason et al. (2011) tested monoterpenes for protection against herbivory by capercaillie, bank voles, slugs, or red deer; some, but not all, worked (see also Hamberger et al. 2011: defensive properties of diterpene resin acids). Mumm and Hilker (2006) discuss the chemical defence of pines against foliovores in particular.
Bacterial/Fungal Associations. Ectomycorrhizal associations are particularly common in Pinaceae, and appropriate ECM fungi may have to be introduced if Pinus, for instance, is to be cultivated successfully. Crown group ages for the origins of ECM clades of Agaricales was found to be split about equally between the Late Cretaceous and Eocene, and for nearly all a Jurassic origin could be rejected (Ryberg & Matheny 2012), although it seems that Pinaceae had begun diverging by then (see above). Given current uncertainties over details of crown Pinaceae diversification, the relation between the evolution of ECM fungi and Pinaceae remains unclear. Furthermore, Pinus and Larix in particular may form ectendomycorrhizal associations with an ascomycete (Peterson 2013).
Bacteria associated with a particular kind of ECM on P. contorta, tuberculate ECM, a cluster of root tips surrounded by hyphae (see ectendomycorrhizae above), are thought to fix nitrogen (Paul et al. 2007). Wood of Pinaceae, as in other conifers, is broken down mostly by brown rot fungi. These fungi cannot degrade lignin, but break down cellulose and hemicellulose, leaving behind brown, crumbly detritus that is very rich in lignin and resitant to decay (Boddy & Watkinson 1995). Laccaria bicolor, a brown rot fungus, was found to take up nitrogen from springtails that it had first immobilized, and this nitrogen could be transferred to seedlings of Pinus strobus (Klironomos & Hart 2001).
A number of rusts, including those on ferns, have their aecial stages on Pinales, especially Pinaceae (Savile 1979b; Durrieu 1980). These include the white pine blister rust, Cronartium ribicola (alternate host Ribes, Grossulariaceae), a serious pathogen of white pine and its relatives.
In Pinus strobus endophytes synthesize antifungal metabolites, effective against Microbotryum violaceum, parasitic on some Caryophyllaceae (Sumarah et al. 2010, 2011), and endophyte metabolites in spruce may be toxic to insects (Findlay et al. 2003).
Genes & Genomes. For chloroplast genome rearrangements, notably extensive here, see Lin et al. (2010) and C.-S Wu et al. (2011a); the inverted repeat may be very much reduced in size in gneera scattered throughout the famly (Jansen & Ruhlmann 2012 for references).
Economic Importance. The majority of the world's lumber comes from softwood, and the majority of that comes from members of Pinaceae [?details].
Chemistry, Morphology, etc. Schultz (1990) notes that there are no phloem fibres in Pinaceae. Pinus cuticular wax tubules look almost scalloped (c.f. commelinids!), but this is because the tubules are densely aggregated (Wilhelmi & Barthlott 1997). Adult plants of Pinus have scale leaves alone on their long shoots; seedings may bear needles directly on long shoots. For the anatomy of Pinus needles, see Dörken and Stützel (2012); needles of subgenus Pinus are often described as having two vascular bundles, but there is a single vascular bundles with two parts separated by a parenchymatic band, the whole being surrounded by a common bundle sheath.
The seed coat of Cedrus is vascularized. The seed wing of Pinaceae is derived from the middle or stony layer of the integument. Cleavage polyembryony is common, as is true polyembryony (more than one archegonium is formed), but the seed generally contains only a single embryo.
For Pinus, see e.g. Mirov (1967: monograph), Richardson (1998: ecology and biogeography), and Farjon (2005a: monograph); for other Pinaceae, see Farjon (1990: general). For aspects of ovuliferous cone morphology and anatomy, see Hu et al. (1989), Napp-Zinn and Hu (1989), and Gernandt et al. (2011), for the embryo, see Buchholz and (1931), for seed coat development, see Owens and Smith (1964), and for general information, see the Gymnosperm Database. Esteban and de Palacios (2009) and Esteban et al. (2009) describe the wood anatomy of Abietoideae, and Braukmann et al. (2009) chart the extent of the loss of the ndh gene (see also Hirao et al. 2008).
Phylogeny. Relationships within Pinaceae are unclear and have depended on the kind of data analysed (morphology, molecules) and methods of analysis (parsimony, Bayesian) - see Tsumura et al. (1995), Wang et al. (2000), Rydin and Källersjö (2002), Liston et al. (2006b), and Gernandt et al. (2008). Studying the mitochondrial rps3 gene, Ran et al. (2010) found that Larix and Pseudotsuga were sister to all other Pinaceae. However, the main problem is the position of Cedrus with respect to Abietoideae (Abies, Keteleeria, Nothotsuga, Pseudolarix, Tsuga) and Pinoideae (Cathaya, Larix, Picea, Pinus, Pseudotsuga) (Holman et al. 2010). Thus Wang et al. (2000) placed Cedrus sister to the rest of the family, Gernandt et al. (2008) as sister to Abietoideae, while Liu et al. (2010) retrieved the clade [Cedrus [Abies + Keteleeria]] as sister to the rest of the family, although Tsuga and Pseudolarix were not sampled; Cathaya and Pinus formed a clade. Holman et al. (2010) nicely summarize the morphological evidence that is compatible with the relationship of Cedrus to either of those groups, or as sister to the whole family.
In a study with exhaustive sampling of conventional Pinaceae and all other Pinales except for Gnetum, etc., Leslie et al. (2012) found the set of relationships [[Cedrus [[Pseudolarix + Larix] [Abies + Keteleeria]] [[Pseudotsuga + Larix] [Pinus [Cathaya + Picea]]] (not all genera are mentioned).
For the phylogeny of Pinus, see Syring et al. (2005), Gernandt et al. (2005, 2011), and Eckert and Hall (2006). Pinus has two subgenera (see Gernandt et al. 2005 for an infrageneric classification). Leaves of subgenus Pinus, the hard pines, apparently have two vascular bundles (but see above), plesiomorphic, while those of subgenus Strobus, the soft pines, have but a single bundle. Analysis of nuclear ITS variation was largely uninformative in suggesting relationships between sections in Abies, but at lower levels was more useful (Xiang et al. 2009).
Classification. If the topology suggested by Leslie et al. (2012) holds up, a two subfamily classification, Abietoideae and Pinoideae, the subfamilies with the compositions of the two major clades recognized there, would be reasonable.
Synonymy: Abietaceae Gray, Cedraceae Vest, Piceaceae Gorozh.
[[Araucariaceae + Podocarpaceae] [Sciadopityaceae [Cupressaceae + Taxaceae]]] / Cupressophytes: highly oxygenated diterpenes with phenolic rings [phenolic abietanes]; xylem resin ducts +, (constitutive), (inducible); phloem resin ducts 0, calcium oxalate crystals numerous, extracellular, in wall, stratified, sclereids 0; (leaves opposite, sometimes then with two vascular traces); pollen grains atectate, exine granular; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial nadI gene intron 2 and both rps3 introns lost, duplication in the PHYN clade.
Evolution. Divergence & Distribution. Magallón et al. (2013: with temporal constraints) suggested an age of around (276.6-)259-256.9(-244.4) m.y. for this node.
For other possible synapomorphies of this group, see Hart (1987). Isoflavonoids are known from Cupressaceae, Podocarpaceae and Araucariaceae (Reynaud et al. 2005).
Genes & Genomes. For mitochondrial genes, especially the rps3 gene, see Ran et al. (2010).
Chemistry, Morphology, etc. For southern conifers, in part this clade, see Hill and Brodribb (1998: general) and Cox et al. (2007: oxygenated di- and tricyclic terpenoids.
[Araucariaceae + Podocarpaceae]: gums +; roots with endomycorrhizal nodules; prothallial cells divide; ovule one/ovulate scale; proembryo with 5 or 6 free-nuclear divisions; 2nd intron in nad1 gene lost.
Evolution. Divergence & Distribution. The age of this node has been estimated at (237-)205(-237) m.y. (Biffin et al. 2011a, 95% HPD; c.f. text and figs), 230-176 m.y. (Leslie et al. 2012), or around 243 m.y. (Magallón et al. 2013).
Chemistry, Morphology, etc. Chamberlain (1935) notes that there is no stalk cell per se in the male gametophyte, but when the generative cell divides, one of the cells produced dies, the other produces the gametes.
ARAUCARIACEAE Henkel & W. Hochst. Back to Pinales
Branches whorled, plagiotropic, branchlets frequently abscised as units; stem apex with tunica/corpus construction; phloem fibres not stratified; 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; branches shed; leaves multiveined, axillary meristems present on the trunk, undifferentiated, submerged by cork, persistent; (plants dioecious); to 20 microsporangia/microsporophyll; bract and ovulate scales fused (not in Araucaria); ovule inverted, pollination droplet 0, nucellus protrudes from the micropyle [?Araucaria]; pollen germinates on ovuliferous scale and tubes grow over the scales, prothallial cells numerous; seeds winged, wing developing from the entire bract scale (wingless); free nuclear stage in proembryo many nucleate, central, embryonal cells surrounded by cap cells that degenerate; (cotyledons 4 - some Araucaria0; (germination cryptocotylar).
3/33. Southern South America, Malesia to E. Australia and New Zealand (map: from Florin 1963; de Laubenfels 1988). [Photos - Collection.]
Evolution. Divergence & Distribution. In line with the suggested age of the clade (see above), 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, its current southern distribution being interpreted as a relict distribution (Florin 1963; Stockey 1982, 1994; Hill & Brodribb 1989; Kunzmann 2007).
However, Biffin et al. (2010b, esp. 2011b) noted that stem-group calibration scenarios have crown-group divergence of Araucariaceae largely a (mid-Cretaceous to) Tertiary phenomenon (see also Crisp & Cook 2011). This would both question the placement of these early fossils in extant sections and the long-term persistence of Agathis in New Zealand since the Eocene or before. Recently, Leslie et al. (2012) dated the divergence of Araucaria from the [Wollemia + Agathis] clade to 185-165 m.y., more consistent with the attribution of these fossils (see also Stöckler et al. 2002; Knapp et al. 2007; Wallis & Trewick 2009).
Although Araucaria is diverse on New Caledonia, there is little genetic divergence between the species, suggesting that divergence is recent there, too (Gaudeul et al. 2012).
The 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, divergence of Wollemia from other Araucariaceae has been dated to a mere (37-)18(-younger) m.y.a. (Crisp & Cook 2011), suggesting that comparison of Wollemia with Cretaceous fossils may be inappropriate (c.f. Chambers et al. 1998); on the other hand, Leslie et al. (2012: supplement) suggest divergence just before the K/T boundary, while Kunzmann (2007) put the divergence of Agathis and Wollemia at at least 110 m.y.a. Dating here is more than its normal mess.
For possible apomorphies, perhaps including "dehiscent" seeds (i.e. seeds separating from the cone-scale), see Cantrill and Raine (2006).
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).
Plant-Animal Interactions. Sequeira and Farrell (2001) suggested that the association between Araucaria and the scolytine Tomicini bark beetles is probably Cretaceous in age; the beetles seem to have moved on to Araucaria from angiosperms, and from thence moved on to Pinaceae. García Massini et al. (2011) found evidence of wood-boring beetles, fungi, and mites in fossilized araucarian wood of Middle Jurassic age from Argentinian Patagonia.
Caterpillars of Agathiphagidae, a small group of near-basal lepidoptera with jaws, eat seeds of Agathis from Australia to the Pacific (Shields 1988; Powell et al. 1998).
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) notes 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). 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 pollen grains do not rupture when placed in water (Tomlinson 1994).
For general information, see Stockey (1982), Bieleski and Wilcox (2009), Gee and Tidwell (2010: literature from late Triasssic to end Cretaceous), and especially the Gymnosperm Database, for comparative anatomy, see Thompson (1913), for axillary buds, see Burrows (1999 and references, 2009), for details of reproductive biology compared with those of other Pinales, see Owens et al. (1995a, b, c), for pollen morphology, see Dettmann and Jarzen (2000), and for phylogeny, see Setoguchi et al. (1998).
Phylogeny. Wollemia has been placed variously sister to Agathis or sister to the rest of the family (Jones et al. 1995; Gilmore & Hill 1997; Setoguchi et al. 1998; S. S. Renner in Kunzmann 2007), the particular position being sensitive to the choice of outgroups (Knapp et al. 2007). A [Wollemia + Agathis] clade was retrieved in the comprehensive four-gene tree in Leslie et al. (2012).
PODOCARPACEAE Endlicher Back to Pinales
Podocarpic acid + [particular diterpene with phenolic ring]; (nodes 1:2); sclereids numerous, with large lumen; transfusion tissue in patches lateral to vascular bundles in leaf, laterally-elongated sclereids in middle of lamina; (leaves opposite [Microcachrys]; plants dioecious (monoecious); microsporophylls with two sporangia; pollen exine thin, except distally; male gametophytes with 3-6(-8) prothallial cells, sperm nuclei unequal in size (one extruded); ovule ± inverted; proembryo [E tier] cells binucleate.
Saxegothea Lindley
Plants monoecious; pollen not saccate; two ovules/scale; n = 12.
1/1: Saxegothaea conspicua. South Chile and Argentina.
The Rest.
(Leaves broad, with transfusion tissue), (multiveined - Nageia); plants dioecious (monoecious); pollen saccate, (not Phylocladus), exine alveolate; ovulate scales not aggregated into cones (yes - Microcachrys), ± reduced, fused with ovule, ± enveloping ovule; (ovule erect); adnate ovulate scale/integument fleshy [epimatium], fleshy (not); n = (9 - Phyllocladus)10(-13, 15-19).
16/125: Podocarpus (100), Dacrydium (20). Largely southern Hemisphere, scattered, N. to Japan, Central America and the Caribean (map: from Florin 1963; Dalling et al. 2011; Adie et al. 2011). [Photos - Collection, Phyllocladus trichomanoides, Phyllocladus megasporangia, microsporangia.]
Evolution. Divergence & Distribution. Podocarpaceae are known as fossils (Rissikia) from the Middle Triassic of Antarctica ca 225 m.y.a., although the material has since been lost (apparently 2 ovules/scale, see also Saxegothea: 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).
Although Podocarpaceae are still quite common and may dominate the vegetation, they are largely restricted to the southern hemisphere, including Antarctica, where they are found as fossils; for their biogeography, see Mill (2003). Podocarpaceae with broad leaves are shade tolerant and prefer warmer and higher rainfall conditions (c.f. Cupressaceae and other Podocarpaceae with narrower, imbricate leaves), and as Australia dried out during the Tertiary, podocarps became less common there (e.g. Brodribb & Hill 1997, 2004; Biffin et al. 2011b). Diversification in clades whose members have imbricate leaves began in the Late Jurassic ca 150 m.y.a. (Biffin et al. 2011b); diversification in clades whose members have flattened foliage is notably greater than in clades with imbricate leaves, and is dated to (94-)64(-38) m.y.a. (c.f. Biffin & Lowe 2011; Biffin et al. 2011b; Brodribb & Feild 2010). Leslie et al. (2012) offer other dates for splits within Podocarpaceae. Dacrydium may have moved into South East Asia via the Ninety East Ridge and India (Morley 2011).
Ecology & Physiology. Podocarps are slow-growing, long-lived, light-demanding specialists that often grow in nutrient-poor soils, but are mostly poorly adapted to dessication stress; they can be dominants or emergents in southern forests (Brodribb 2011; Coomes & Bellingham 2011). Their leaves decompose only slowly (although there are few studies on this), carbon/lignin build up in the soil, nutrients are sequestered, and soil fertility is further reduced (Wardle et al. 2008); they have been described as ecosystem engineers because of this combination of features (Coomes & Bellingham 2011).
Root nodules in Podocarpaceae can occur in longitudinal rows and represent modified lateral roots (Becking 1965; Duhoux et al. 2001). The fungus Glomus is involved, and nitrogen does not seem to be fixed (Russell et al. 2002), however, the function of these nodules is poorly understood (Dickie & Holdaway 2011).
Biffin and Lowe (2011, see also Biffin et al. 2011b) suggest that podocarps with broad leaves or functionally equivalent structures like the phylloclades of Phyllocladus evolved about four times. This has been dated to a time slightly after the venation density of angiosperm leaves increased - (94-)64(-38) versus 109-60 m.y.a. (Biffin & Lowe 2011; Biffin et al. 2011b; Brodribb & Feild 2010).
The New Caledonian Parasitaxus usta is hemiparasitic on the roots of Falcatifolium taxoides, another podocarp, 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).
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).
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 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).
Chemistry, Morphology, etc. For secondary metabolites in Podocarpus s.l., see Abdillahi et al. (2010); taxol has been found in Afrocarpus gracilior (fungi involved here, too?). Accessory transfusion tissue extends to the lamina margin in Podocarpus macrophyllus and a number of other species of the genus (Gifford & Foster 1989; Knopf 2012; Knopf et al. (2012) provide many details of foliar anatomy for the whole group.
The pollen of Phyllocladus has often been described as having a wing (e.g. Singh 1978), but a wing seems to be absent. The morphological nature of the epimatium has occasioned some controversy. Chamberlain (1935) interpreted it as possibly being equivalent to the ovuliferous scale (see also Tomlinson & Takaso 2002; Englund et al. 2011 [similarity confirmed by gene expression data]), and functionally, perhaps, it can be considered equivalent to the second integument of an angiosperm ovule - hence the anatropy of the ovules here (Endress 2011b). Phyllocladus is sometimes described as having an aril, although this is more probably a somewhat reduced and retarded epimatium (de Laubenfels 1988). Although the single ovules of most Podocarpaceae do seem very different from the cones of other Pinales, Lower Cretaceous podocarps with more conventional bract-scale complexes have been described (X. Wang et al. 2008). For nucleus number in the E-tier cells, see Quinn (1986). Quinn et al. (2002) note the tendency to dysploid chromosome evolution in the group.
For cuticle morphology, see Mills and Schilling (2009), for wood anatomy, see Woltz et al. (2009 and references), 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.
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, have 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). The Other groupings of genera are becoming evident (Kelch et al. 2010), including the dacrydioid and podocarpoid clades (Knopf et al. 2012). The closest relatives of Parasitaxus are Lagarostrobus and Manoao, from Tasmania and New Zealand - [Parasitaxus [Lagarostrobus + Manoao]] (Sinclair et al. 2002; Rai et al. 2009; Lam et al. 2009).Saxegothaea has some support as being sister to the rest of the family (Knopf et al. 2012, but c.f. Leslie et al. 2012), and this has considerable implications for character evolution in the clade; as Mabberley (2007) noted, the plant does have some features reminiscent of Araucariaceae....
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, Dacrycarpaceae Melikian & A. V. Bobrov, Falcatifoliaceae Melikian & A. V. Bobrov, Halocarpaceae Melikian & A. V. Bobrov, Microcachrydaceae Doweld & Reveal, Microstrobaceae Doweld & Reveal, Nageiaceae D. Z. Fu, Parasitaxaceae Melikian & A. V. Bobrov, Phyllocladaceae Bessey, Pherosphaeraceae Nakai, Prumnopityaceae Melikian & A. V. Bobrov, Saxegotheaceae Doweld & Reveal
[Sciadopityaceae [Cupressaceae + Taxaceae]]: pollen without sacci, exine shed on microgametophyte germination [microgametophyte naked]; prothallial cells 0; seed wing developing from the integument.
Evolution. Divergence & Distribution. Leslie et al. (2012) estimate an age for this node of over 250 m.y..
Chemistry, Morphology, etc. The pollen grains expand and rupture when placed in water (Tomlinson 1994), and the intine-clad pollen may deform more easily and so be tranferred along the narrow micropylar canal (Takaso & Owens 2008). Whether or not all taxa have male gametes each surrounded by cell walls needs to be confirmed (see Singh 1978).
SCIADOPITYACEAE Luersson Back to Pinales
Roots with endomycorrhizal nodules; leaves on long shoots reduced to scales, branchlets deciduous [= short shoots], short shoots +, with a pair of connate needles, apically bifid (not); microsporophyll with flattened apical expansion, (1-)2 microsporangia/microsporophyll; pollen surface microtuberculate (microechinate) exine granules confluent by sporopollenin deposition; sterile cell?; ovules usu. >7/ovuliferous scale, inverted, pollen chamber?; seeds (1-)7-9(-12)/scale, narrowly winged; n = 10.
1/1: Sciadopitys verticillata. C. and S. Japan (map: from Florin 1963). [Sciadopitys Photos - Collection]
Evolution. Divergence & Distribution. Fossils of Sciadopitys are known from the Upper Cretaceous onwards, although, apart from fossils from Japan and the Upper Pliocene of Germany, the identities of many are questionable (Stockey et al. 2005). Sciadopitys may have diverged from the [Taxaceae + Cupressaceae] clade in the late Permian, over 250 m.y.a. (Leslie et al. 2012).
Chemistry, Morphology, etc. There has been much debate over whether the photosynthesising structures ofSciadopitys are some kind of phylloclade - perhaps formed by the connation of two leaves - or cladodes, basically stem structures. The two vascular bundles, each with its own endodermis, tend to have have abaxial xylem and adaxial phloem, a rather odd arrangement. Sporne (1965) noted that on occasion branches develop from these leafy structures, so perhaps favoring the cladode hypothesis (see also Farjon 2005c). However, Dörken and Stützel (2011) examined probably only the second known case of intermediate structures, and consider the photosynthesizing structures to be two congenitally connate needle leaves, the orientation of the vascular tissue resulting from the relation of the leaves to the axis that bore them (see also Dörken & Stützel 2012).
For pollen, see Page (1990) and Uehara and Saichi (2011), for a monograph, see Farjon (2005c), and for general information, see the Gymnosperm Database.
[Cupressaceae + Taxaceae]: cone scales opposite; megasporangia hypodermal [?level].
Evolution. Divergence & Distribution. Leslie et al. (2012) estimate a crown age of 217-197 m.y., Mao et al. (2012) an age of (293-)245, 242(-194) m.y., estimates in Yang et al. (2012) span 237-192 m.y. and in Magallón et al. (2013) ca 175.4 m.y..
Chemistry, Morphology, etc. Burrows (2009) noted that axillary buds occur in several members of this clade, but they were superficial and so did not form shoots in older branches - c.f. Araucariaceae. Gene expression studies suggest little in common between the scaly structures of the Cupressaceae cones studied and the arils of Taxus with the ovuliferous scales of Pinaceae... (Englund et al. 2011; Groth et al. 2011).
CUPRESSACEAE Bartling Back to Pinales
(Stem apex with tunica/corpus construction); xylem or phloem resin ducts inducible [in separate clades]); branchlets deciduous; leaves scale- or needle-like, (opposite - Cupressus, etc., and nodes 1:2), shed along with branches; (plant dioecious); (1-)2-10(-14) microsporangia/microsporophyll; pollen surface microverrucate; ovuliferous scales small (usu. not obvious at all; large, Taxodium and relatives), (bract scale fleshy - Juniperus; with adaxial development), ovules 1-9(-many)/scale, erect or inverted; male gametophyte without sterile cell, gametes with separate cell walls; seeds /scale, winged from integument or not; (cotyledons -9(-15)); n = 11.
30/133: Juniperus (67), Callitropsis (18), Callitris (14), Cupressus (12). Esp. Northern Hemisphere, more scattered in south temperate regions, also N.E. Africa; individual genera are from either Northern or Southern Hemispheres (map: from Florin 1963, 1966; Farjon 2004c). [Photos - Collection.]
Evolution. Divergence & Distribution. Cupressoideae are predominantly northern in their current distributions and Callitroideae are predominantly southern, a vicariance pattern that may reflect the break-up of Pangaea. 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; Yang et al. 2012, q.v. 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 Tertiary 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) suggested that Juniperus and Cupressus s.l., most of whose species are adapted to dry conditions, diverged 38.7-32 m.y.a., while figures in Leslie et al. (2012) are 53-33 m.y. (and some much older). Mao et al. (2010; see also Adams & Schwarzbach 2013) throught that there was E->W migration across the North Atlantic Land Bridge in Juniperus, initially Eurasian in distribution, around 47-30.3 m.y.a. (see see Mao et al. 2010 for more dates). Arid-adapted members of Callitroideae diversified some 52.6-34 m.y.a. (Pittermann et al. 2012); Leslie et al. (2012) suggest that diversification began a little before the K/T boundary ca 65.5 m.y.a. and continued throughout the Tertiary.
Ecology & Physiology. Biomass estimates for Sequoia sempervirens are 2.3x106 kg ha-1 (Franklin & Dryness 1973).
For details of xylem function in relation to the environment in Cupressaceae, see Pittermann et al. (2010). The initial preferences for the family were mesic conditions, but Pittermann et al. (2012) noted that a number of species of both Cupressoideae and Callitroideae had evolved drought resistance, their xylem-specific conductivity and stomatal conductances being lower, and also their CO2 assimilation rates were much reduced. The cost of these adaptations was slow growth.
Bacterial/Fungal Associations. The telial stage of Gymnosporangium rust is common on some Cupressaceae, especially Juniperus, while the aecial stage characterises Rosaceae-Maloideae (Savile 1979b).
Pollination Biology. In Cupressus dupreziana paternal apomixis, a phenomenon unknown from any other seed plant, occurs; here the embryo develops from unreduced male gametes (Pichot et al. 2000, 2001).
Genes & Genomes. Cryptomeria japonica has a much reduced inverted repeat with few genes duplicated in it (Hirao et al. 2008).
Chemistry, Morphology, etc. Characters of wood anatomy may yield phylogenetically interesting variation (Schulz & Stützel 2007), but state delimitation is difficult; for epidermal morphology, see Ma et al. (2009). Proliferation of the ovuliferous cones is common, and its distribution, too, may be of phylogenetic interest (Schulz & Stützel 2007). Scales on the ovuliferous cones are wedge-shaped to peltate. A number, perhaps a majority, of Cupressaceae lack ovuliferous scales, having only bract scales (Zhang et al. 2004; see also Farjon 2005c), while Cryptomeria has several "teeth" on the ovuliferous scale - perhaps a reversion to a plesiomorphic morphology (see also Schulz & Stützel 2007).
For cone morphology, see Farjon and Garcia (2003) and Schulz and Stützel (2007: interesting analysis, but unfortunately Juniperus etc. not included).
Phylogeny. Page (1990) suggested that there were "fundamental" differences between Cupressaceae and Taxodiaceae in the morphology of their reproductive parts, but in the tree of Quinn et al. (2002) Cupressaceae s. str. are embedded in a paraphyletic Taxodiaceae which form a basal grade. Phenetic analyses had earlier suggested the combination of the two (Eckenwalder 1976), and they are combined in Farjon (2005c). For relationships within Cupressaceae, see Brunsfeld et al. (1994), Gadek et al. (2000), Kusumi et al. (2000), Farjon et al. (2002), Brunsfeld et al. (2003), and Little et al. (2004). The basic phylogenetic structure of the family is [Cunninghamioideae [Taiwanoideae [Athrotaxidoideae [Sequoioideae [Taxodioideae [Cupressoideae + Callitroideae]]]]]] (Mao et al. 2012), although Yang et al. (2012) found the subfamilial order in the middle of the tree to be ... [Sequoioideae [Athrotaxidoideae ... Callitris is paraphyletic, although morphological (Piggin & Bruhl 2010) and molecular (Pye et al. 2003) studies do not agree as to exactly how extensive the paraphyly is...
For relationships in Juniperus, see Mao et al. (2010) and Adams and Schwarzbach (2013).
Classification. Having 22 family names for ca 30 genera says a lot about the past. For a monograph (and far more) see Farjon (2005c); general information can of course be found in the Gymnosperm Database. For generic limits around Cupressus, see Price and Adams (2009) and Little (2006) and around Callitris, see Pye et al. 2003) and Piggin and Bruhl (2010). Cupressus has turned out to be polyphyletic and is now restricted to the Old World (Xiang & Li 2005; especially Little 2006); for an account of the genus, see Adams (2010).
Botanical Trivia. Juniperus forms the highest known forest growing at some 4,900 m altitude on the Tibetan Plateau (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.
Synonymy: Actinostrobaceae Lotsy, Arceuthidaceae A. V. C. F. Bobrov & Melikian, Arthrotaxidaceae Doweld, Callitraceae Seward, Cryptomeriaceae Gorozh., Cunninghamiaceae Siebold & Zuccarini, Diselmaceae A. V. C. F. Bobrov & Melikian, Fitzroyaceae A. V. C. F. Bobrov & Melikian, Juniperaceae Berchtold & J. Presl, Libocedraceae Doweld, Metasequoiaceae Hu & W. C. Cheng, Microbiotaceae Nakai, Neocallitropsidaceae Doweld, Pilgerodendraceae A. V. C. F. Bobrov & Melikian, Platycladaceae A. V. C. F. Bobrov & Melikian, Sequoiaceae Luersson, Taiwaniaceae Hayata, Taxodiaceae Saporta, Tetraclinaceae Hayata, Thujaceae Burnett, Thujopsidaceae Bessey, Widdringtoniaceae Doweld
TAXACEAE Berchtold & J. Presl Back to Pinales
Bands of fibres in phloem crystalliferous, sclereids + [Taxus]; plant dioecious (monoecious); pollen inaperturate; ovules erect; pollen chamber +, pollination drop +; male gametes unequal in size; seed coat vascularized, with sarco- and sclerotesta.
6/30. Northern Hemisphere, scattered, also New Caledonia.
2-3 microsporangia/microsporophyll; ovuliferous scale much reduced, ovules 2/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
Wood and phloem lack resin canals; 2-6 microsporangia/microsporophyll; ovule solitary, on shoot in axil of vegetative leaf; female gametophyte with ca 256 free nuclei; (seed arillate - Taxus); embryo short/minute (cotyledons 3); n = 7, 11, 12.
5/24: Taxus (8). Scattered in the Northern Hemisphere, esp. South East Asia, also New Caledonia (map: from Florin 1963; de Laubenfels 1988). [Photos - Collection.]
Synonymy: Amentotaxaceae Kudô & Yamamoto, Austrotaxaceae Nakai, Torreyaceae Nakai
Evolution. Bacterial/Fungal Associations. Taxol and related compounds are synthesized by Taxus and also by several fungi that either grow in the soil around the plant or are endophytes (Cassady et al. 2004 and references), and it has been suggested that 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).
The scales subtending the ovules of Austrotaxus are spiral. Taxaceae s.l. lack sacci on their pollen (Anderson & Owens 2006). 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 their reproductive structures (Stützel & Röwekamp 1999a) suggest that Taxus in particular can be linked with Torreya and then to other conifers.
For the morphology of Taxus and relatives, see Hart and Price (1990), for male reproductive structures, see Wang et al. (2008), for male gametes, see Chamberlain (1935) and Singh (1978), for the megasporangiate cone, see André (1956) and Liang and Wang (1989), for embryology in general, see Chen and Wang (1990: the sperm range from somewhat to very unequal in size), and for a general account, see Cope (1998).
Phylogeny. Cephalotaxaceae and Taxaceae are combined here because on balance the evidence suggests that the exclusion of Cephalotaxus would make Taxaceae paraphyletic. Page (1990) included Amentotaxus in Cephalotaxaceae, although he noted that affinities between the two were "somewhat enigmatic"; a family as so delimited appears para- or polyphyletic to Taxaceae s. str., c.f. e.g. Price (2003) and Hao et al. (2010). Quinn et al. (2002) in a broad survey of Pinales found that Cephalotaxus, Torreya and relatives, and Taxus and relatives formed a tritomy in their unweighted rbcL and matK analyses; only when weighted were Cephalotaxaceae and Taxaceae separate. Price (2006) looked at variation in the same two genes and found weak support for Cephalotaxus as sister to [Amentotaxus + Torreya]; sampling overall was poor, but good for Taxaceae s.l., and support for the monophyly of Taxaceae s.l. was strong. These relationships were found by Wang et al. (2003) in analyses of trnL/F singly and when combined with rbcL data, but not in an analysis of rbcL alone, when Cephalotaxus alone was sister to Taxaceae. 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 phylogeny, see also Cheng et al. (2000). Rai et al. (2009) also found Cephalotaxaceae were sister to Taxaceae.
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).