EXTANT SEED PLANTS
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 rich in guaiacyl units; true roots present, apex multicellular, xylem exarch, branching endogenous; arbuscular mycorrhizae +; shoot apical meristem multicellular, interface specific plasmodesmatal network; stem with ectophloic eustele, endodermis 0, xylem endarch, branching exogenous; vascular tissue in t.s. discontinuous by interfascicular regions; vascular cambium + [xylem ("wood") differentiating internally, phloem externally]; wood homoxylous, tracheids +; tracheid/tracheid pits circular, bordered; sieve tube/cell plastids with starch grains; phloem fibers +; stem cork cambium superficial, root cork cambium deep seated; nodes ?; stomata ?; leaf vascular bundles collateral; leaves spiral, simple, axillary buds?, prophylls [including bracteoles] two, lateral, veins -5 mm/mm2 [mean for all non-angiosperms 1.8]; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores, i.e. no distal pore for release of gametes] +, grains mono[ana]sulcate, exine and intine homogeneous, ovules unitegmic, crassinucellate, 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, with cell walls, with many flagellae; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large", first cell wall of zygote transverse, embryo straight, endoscopic [suspensor +], short-minute, with morphological dormancy, white, cotyledons 2; plastid transmission maternal; two copies of LEAFY gene, PHY gene duplication [N/O//A/C and P//BE lines], mitochondrial nad1 intron 2 and coxIIi3 intron present.
EXTANT GYMNOSPERMS/PINOPHYTA
Biflavonoids +; cuticle wax tubules with nonacosan-10-ol; ferulic acid ester-linked to primary unlignified cell walls; phloem with sieve and Strasburger cells, the sieve area with pores joining to form median cavity in the region of the middle lamella; stomata perigenous, stomatal poles raised above pore, no outer stomatal ledges or vestibule; transfusion tissue +; microsporophylls and megasporophylls forming determinate strobili/cones; pollen tecate, infratectum alveolate [esp. saccate pollen], endexine lamellate at maturity; ovule unitegmic, with pollen chamber [developing by breakdown of nucellar cells]; pollination droplet +, fertilisation 7 days to 4-6 months or more after pollination, pollen germinates in two or more days, tube grows at 1³-10(-20) µm/hour, breaks down sporophytic cells and grows away from ovule, wall of cellulose microfibrils, male gametophyte of two prothallial cells, tube cell, stalk/sterile cell, and two multiflagellate gametes, zooidogamy, male gametes released by the breakdown of the pollen grain wall; female gametophyte monosporic, with radially-elongated cells [alveoli] that grow centripetally, the nucleus being on the open face and connected to adjacent nuclei by spindle fibers; testa mainly of sarcotesta and sclerotesta, ± vascularised; chromosomes of male and female gametes line up on separate but parallel spindles, proembryo with many free-nuclear divisions; gametophyte persists in seed; genome size [1C value] intermediate, 3.5-14 pg; two copies of the LEAFY gene and three of the PHY gene [PHYN + PHYO, PHYP].
GINKGOALES + PINALES: wood pycnoxylic; bordered pits with margo-torus construction; phloem with scattered fibres alone [Cycadales?]; axillary buds +; sporangiophore/filament simple with terminal microsporangia.
PINALES Dumortier Main Tree, Synapomorphies.
Resin ducts/cells in phloem in vascular tissue [and elsewhere]; lignins lacking syringaldehyde [Mäule reaction negative]; cork cambium ± deep seated; bordered pits on tracheids round, opposite; compression wood +; nodes 1:1; leaves with single vein; microsporangia abaxial, dehiscing by the action of the hypodermis [endothecium], pollen exine thick [³2 µm thick], granular; ovulate strobilus compound, with ± united flattened ovuliferous and bract scales, pollen chamber 0; pollen tube unbranched, growing towards the ovule, prothallial cells 2, gametes non-motile, released from the distal end of the tube, siphonogamy; seed coat dry, not vascularised; 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; plastid and mitochondrial transmission paternal, one duplication in the PHYP gene line, one copy of the chloroplast inverted repeat missing. - 7 families, 68 genera, 545 species.
Evolution. Because of the long history of Pinales, we cannot understand their evolution just by looking at their extant representatives, and it is clear that the apomorphies of extant conifers depend critically on fossil outgroups (e.g. Hart 1987). However, there are no known synapomorphies for a clade containing living and extinct conifers (e.g. Rothwell & Serbet 1994). Currently the morphology of extinct conifers and coniferophytes is being reevaluated 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 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 (cf. 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). Similarly, the current distributions of many extant conifer groups is much smaller than and/or very different from their past distributions which in many cases go back to the Cretaceous (e.g. Manchester 1999: N. temperate distributions0, thus McIver (2001) found 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.
A number of rusts, including those on ferns, Rosaceae, Grossulariaceae, etc., have part of their life cycles on Pinales, especially Pinaceae (Savile 1979b).
Ambrosia and bark beetles (Platypodinae, Scolytinae, weevils: see Wood 1982; Wood & Bright 1992) seem to have been associated ancestrally with conifers, then shifted on to angiosperms and finally back to conifers several times - their current diversity in Pinales is lower (Farrell et al. 2001); see also Powell et al. (1999) for other insect-conifer associations. Bark beetles make their gallery systems in phloem, ambrosia beetles in the wood, and they mostly live in dead or dying wood. Pine beetles of the genus Dendroctonus can be noxious pests invade that living pines; such species tend to have relatively few hosts, but outbreaks can be devastating (Kelley & Farrell 1998 for host specificty). Ambrosia beetles may also carry blue stain fungi (species from a few unrelated ascomycete genera) that may quickly invade the sapwood, rendering it useless, and the result is that the plant can die surprisingly quickly. Other fungi are involved, both in ambrosia and bark beetles. Some of the weevils cultivate and eat the fungus; development of cultivation is unreversed, and the weevils involved in it have highly modified cuticular structures that allow the transport of fungal spores (Beaver 1989; Jordal et al. 2008 and references). 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). Hudgins et al. (2003) examined the diversity of bark beetles in the context of various plant structures that might be defenses against such beasts; Francheschi 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. Many bark beetles are found growing on Pinaceae despite the constitutive presence of resin ducts in both phloem and xylem (i.e. the ducts do not develop in response to some trauma, etc., but are always to be found there), there are intracellular crystals, etc. Other families of Pinales have such ducts only in the phloem, but they also have large numbers of small, extracellular, calcium oxalate crystals and also stratified phloem (Pinaceae have scattered sclereid cells or sometimes groups of such cells), both possibly protective structures - and a lower diversity of these beetles. Keeling and Bohlmann (2006a [detailed discussion], 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.
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 (and 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 satefy 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.
Note that 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). In general, it seems that 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, the 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). Sacci also help in the selection of pollen grains during pollination: The proportion of saccate pollen grains inside the ovules in higher than that outside (Leslie 2009). Previously it had been thought that sacci facilitated wind dispersal of the pollen, and indeed they may also increase the distance the pollen grain can travel before it falls to the ground, so facilitating wind pollination (Schwendemann et al. 2007). 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 resorbtion of the ovule droplet 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 for references) and other ancient gymnosperms (Leslie 2008).
Chemistry, Morphology, etc. For fatty acids in the seeds, see Wolff et al. (2002 and references). 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). Leaf traces can also make connections with xylem produced during the second and subsequent years (Maton & Gartner 2005). 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 fibers, the amount of resin secreted, etc. (Hudgins et al. 2003). Secondary growth (only phloem is produced) has been reported from the leaves of a number of conifers (Ewers 1982).
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. In some of these taxa the male gametes are unequal, one even being extruded from the cytoplasm of the binucleate sperm cell in e.g. Podocarpus spp. and Taxus. In Dacrydium two gametes are present, but are of unequal size, while in at least some Gnetum, Podocarpus andinus, and Torreya taxifolia two unequally-sized male cells are produced (see 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 for references). Pinales show paternal transmission of plastids; mitochondrial transmission in taxa like Taxus is both paternal and maternal. The few records in other gymnosperms all suggest that maternal plastid transmission is widespread there (Chesnoy 1987; Neale et al. 1991; Mogensen 1996, summary of literature reports for Pinales; Cafasso et al. 2001 [cycads]; Wilson & Owens 2006 [podocarps]). 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 occured (Guillet-Claude et al. 2004).
For a classic study of both fossil and extant conifers, see Florin (e.g. 1951), for cleavage polyembryony, see Doyle and Brennan (1972), and for pollination, see Doyle (1945), Tomlinson (1994, 2000), Tomlinson et al. (1997), and Tomlinson and Takaso (2002). Page (1990) gives some general information, see also Geyler (1867), Barthelmess 1935, and Kumari (1963: nodal anatomy, taxa with opposite or whorled leaves tend to have 1:2 nodes), Möller (1882: cork cambium), Butts and Buchholz (1940: cotyledon number), Herrmann (1951: extensive intergeneric grafting seems possible), Napp-Zinn (1966: leaf anatomy), Den Outer (1967: phloem anatomy, much detail unincorporated), Gifford and Foster (1988: general, still a good survey), Schulz (1990: phloem anatomy), Zhou and Jiang (1992: wood anatomy), Raubesen and Jansen (1992a), Lackey and Raubeson (2008) and Hirao et al. (2009) (loss of a copy of the inverted repeat), Hill and Brodribb (1998: southern conifers), Owens et al. (1995b: cytoplasmic inheritance, nuclei sometimes incorporate cytoplasm), Mundry (2000: cone/strobilus development, with an emphasis on Taxaceae and friends), Trapp and Croteau (2001: resin biosynthesis), Sklonnaya and Ruguzova (2003: spermatogenesis), and seed anatomy (Bobrov & Melikian 2006: mention of both testa and tegmen). Farjon (2005b) has provided a bibliography for all conifers.
Phylogeny. Given the uncertainty in our knowledge of the relationships between the five major seed-plant clades, direct links are provided to the four others from here: Cycadales, Gnetales, flowering plants or Magnoliophyta , and Pinales; general discussion under 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 cf. 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), and Rai et al. (2002, and especially 2008a and references). Note that many details of the relationships suggested by the early morphological phylogeny of Hart (1987) have not been confirmed. It is now becoming more likely that Gnetales are to be included in Pinales (see discussion on Cycadales page).
There is perhaps some uncertainty in relationships in the Cephalotaxaceae-Taxaceae area, the two being tentatively bring combined here since there is some evidence that the exclusion of Cephalotaxus would make Taxaceae paraphyletic. Quinn et al. (2002) in a broad survey of Pinales found that Cephalotaxus, Torreya and relatives, and Taxus and relatives formed a polytomy in their unweighted rbcL and matK analysis; only when weights were applied did separate Cephalotaxaceae and Taxaceae become evident. Price (2006) looked at variation in the same two genes and found weak support for Cephalotaxus being embedded within Taxaceae, being 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. Somewhat similarly, these latter 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 Taxeae. Taxaceae s.l. lack sacci on their pollen (Anderson & Owens 2006). The sarcotesta of Cephalotaxus has been tentatively equated with the aril of Taxus (Mundry 2000), although the two would not seem to be homologous. Indeed, Taxaceae themselves have often been considered very different from all other extant conifers (e.g. Florin 1948, 1954; Miller 1999), but a reinterpretation of the nature of their reproductive structures (Stützel & Röwekamp 1999a) suggest that Taxus in particular can be linked with Torreya and then to other conifers. Of course morphological phylogenetic analyses (Hart 1987) and many molecular studies (see above) place them securely within the clade formed by the other conifers, rather than linking them to different fossil relatives (e.g. cf. Miller 1999).
Classification. Farjon (2001) has provided a checklist for the conifers as a whole.
Previous Relationships. Producing evolutionary classifications, or classifications that emphasise one or two favored morphological characters, remains popular (e.g. Keng 1975; Melikian & Bobrov 2000; Fu et al. 2004 [Nageiaceae and Podocarpaceae well separated], Bobrov & Melikian 2006 [Auraucariaceae and other conifers form a lineage quite distinct from Pinaceae and Sciadopityaceae]).
Includes Araucariaceae, Cupressaceae, Pinaceae, Podocarpaceae, Phyllocladaceae, Sciadopityaceae, Taxaceae.
Synonymy: Abietales Koehne, Actinostrobales Doweld, Araucariales Gorozh., Athrotaxidales Dowled, 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
PINACEAE F. Rudolphi Back to Pinales
Plant ectomycorrhizal; biflavonoids 0; resin ducts in wood and phloem; sieve cells with nacreous walls, plastids with protein fibers [also starch grains (and protein crystals)]; phloem with sclereids, fibers scattered, calcium oxalate crystals intracellular; (spur shoots +; plant deciduous); leaves with two vascular bundles; plant monoecious; 2 microsporangia/microsporophyll, sporangia superficial, pollen saccate (not), exine thin [2³ µm] except distally, alveolate; bracts free from the ovuliferous scale, ovules 2/scale, inverted, (pollination droplet 0); (pollen exine shed during germination - Larix, Pseudotsuga), sperm cells binucleate; "embryo tetrad" present [free-nuclear stage with only four nuclei]; seeds dry, with a terminal wing developing from adaxial side of scale (wingless); cotyledons (2-)4-11(-20); n = 12 (13, Pseudolarix = 22); plastid ndh genes and rps16 gene lost; 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. Pinaceae are known fossil only from the Early Cretaceous onwards (Miller 1999), and evidence suggests that they are sister to all other extant conifers. Hence the age of the lineage must be well over 200 million years, some 200-350 million years (see Eckert & Hall 2006). For divergence times within Pinaceae, see Wang et al. (2000: Pinus diverged from the rest ca 140 million years before present) and especially Eckert and Hall (2006); using fossil constraints, Eckert and Hall (2006) suggest that Pinus diverged 128 ± 4 million years before present, a much more recent date than they obtained using molecular estimates. Be that as it may, their restriction to temperate forests of the northern hemisphere is remarkable, and for the most part they are unable to compete in tropical broad-leaved rain forests (but see Pinus krempfii: Brodribb & Field 2008). There was a bout of diversification in the family in the Palaeocene (Le Page 2003; see also Wang et al. 2000). However, divergence estimates are very much up in the air; Gernandt et al. (2008: without constraints dates much older) obtained maximum dates of 195-173 million years (Jurassic) for Pinaceae crown group diversification, with Pinus diverging 165-148 million years ago.
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). Insect toxins are synthesised by endophytic associates of spruce (Findlay et al. 2003).
For a general discussion of resins and defence in Pinaceae, see the introduction to Pinales (above); Mumm and Hilker (2006) discuss the chemical defence of pines against foliovores in particular. Adelgidae (aphids) are restricted to Pinaceae, and include Adelges piceae and A. tsugae, serious introduced pests in North America (Havill et al. 2007). Cecidomyiid gall midges are quite common on the family in North America (Gagné 1989).
Economic Importance. 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 for host specificty; Wood 1982 and Wood & Bright 1992 for the weevils).
Chemistry, Morphology, etc. Pinus cuticular wax tubules look almost scalloped (cf. commelinids!), but this is because the tubules are densely aggregated (Wilhelmi & Barthlott 1997). The seed coat of Cedrus is vascularised. 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 Mirov (1967: monograph), Millar (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) and Napp-Zinn and Hu (1989), for the embryo, see Buchholz and (1931), 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. 2009).
Phylogeny. Relationships within Pinaceae are unclear, details depending on 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). The character, "pollen exine shed during germination", is likely to have evolved more than once (?three times) in Pinaceae (see also Rydin & Friis 2005). For the phylogeny of Pinus, see Syring et al. (2005), Gernandt et al. (2005), 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, have two vascular bundles, 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).
Synonymy: Abietaceae Berchtold & J. Presl, Cedraceae Vest, Piceaceae Gorozh.
[Araucariaceae [Phyllocladaceae + Podocarpaceae]] [Sciadopityaceae [Cupressaceae + Taxaceae]]: xylem and phloem resin ducts 0; calcium oxalate crystals numerous, extracellular; phloem stratified, with tangential bands of fibers, sclereids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial nadI gene intron 2 lost, two duplications in the PHYO clade [i.e. four copies of the PHY gene overall].
For other possible synapomorphies of this group, see Hart (1987). Isoflavonoids are known from Cupressaceae, Podocarpaceae and Araucariaceae (Reynaud et al. 2005).
Araucariaceae + Podocarpaceae: roots with nodules; prothallial cells divide [Phyllocladaceae?]; one ovule/ovulate scale; proembryo with 5 or 6 free-nuclear divisions; 2nd intron in nad1 lost.
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; stem apex with tunica/corpus construction; only resin plugs present in vascular tissue; pits on radial walls of tracheids touching, hexagonal in outline; single trace branching profusely in the cortex; stomata tetracytic; branches shed; leaves multiveined; plant monoecious to 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 grains intectate, granulate; pollen germinates on ovuliferous scale and tubes grow over the scales, prothallial cells numerous, sperm cells produced; seed winged [wing the entire bract scale] or not; free nuclear stage in proembryo many nucleate, central, embryonal cells surrounded by cap cells that degenerate; (germination cryptocotylar).
3/33. Southern South America, Malesia to E. Australia and New Zealand (map: from Florin 1963). [Photos - Collection]
Evolution. Araucariaceae are well known as fossils from the Mid Jurassic onwards, Araucaria in particular having been found in Triassic deposits in many parts of the world in both hemispheres (Florin 1963; Stockey 1982, 1994; Hill & Brodribb 1989). Sequeira and Farrell (2001) suggest 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. Agathiphagidae, a small group of lepidoptera with jaws, is found on the family (Shields 1988).
The recent discovery very close to Sydney of a few trees of the remarkable Wollemia, very similar to some fossil Araucariaceae (see e.g. Chambers et al. 1998; Pastoriza-Piñol 2007 for a general account), has occasioned some excitement.
Chemistry, Morphology, etc. Tomlinson (2008) notes that the axillary branches of Wollemiaare evident in the resting terminal bud, but do not grow out until extension growth of the latter starts. 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). 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) and especially the Gymnosperm Database, for comparative anatomy, see Thompson (1913), 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), for phylogeny, see Setoguchi et al. (1998), for growth patterns, see Tomlinson (2008) and Tomlinson and Murch (2009: Wollemia, also anatomy), and for possible apomorphies, perhaps including "dehiscent" seeds (i.e. separating from the cone-scale), see Cantrill and Raine (2006).
Phylogeny. Wollemia has variously been placed sister to Agathis or sister to the rest of the family (Gilmore & Hill 1997; Setoguchi et al. 1998).
PODOCARPACEAE Endlicher Back to Pinales
Roots with nodules [modified lateral roots]; 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] and nodes 1:2), (leaf multiveined [Nageia]); plants dioecious (monoecious); staminate plant: microsporophylls with two sporangia; pollen saccate, (Saxegothea, Phylocladus not), exine thin, except distally, alveolate; male gametophytes with 3-6(-8) prothallial cells, sperm cell binucleate, whether or not one nucleus is extruded; ovulate plant: ovulate scales not aggregated into cones, ± reduced, fused with ovule; ovule with epimatium, ± inverted (erect); epimatium fleshy or not in seed, (seed arillate - Phyllocladus); proembryo [E tier] cells binucleate; n = (9 - Phyllocladus)10(-13, 15-19).
17/125: Podocarpus (100), Dacrydium (20). Largely southern Hemisphere, scattered, N. to Japan, Central America and the Caribean (map: from Florin 1963). [Photos - Collection, Phyllocladus trichomanoides, Phyllocladus megasporangia, microsporangia.]
Evolution. Podocarpaceae are known as fossils from as early as the early Middle Triassic (Axsmith et al. 1998), and the distinctive root nodules are also known from the Triassic (Schwendemann et al. 2008). Although Podocarpaceae are still quite common, they are largely restricted to the southern hemisphere, including Antarctica; for the biogeography of the group, see Mill (2003).
For pollination, see Tomlinson et al. (1991, especially 1997: useful comparative tables) and Rydin and Friis (2005: correlation between absence of wings and the pollen exine being shed on germination); in Phyllocladus, which has erect ovules, the pollination droplet is actively resorbed.
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 (Feild & Brodribb 2005); its closest relatives are Lagarostrobus and <Manoao, from Tasmania and New Zealand (Sinclair et al. 2002; Rai et al. 2009; Lam et al. 2009).
Phyllocladus has phylloclades, flattened, photosynthetic stems; these bear highly reduced, scale-like leaves, and it is the axils of these leaves that the reproductive structures are found. The seedling has needle leaves.
Chemistry, Morphology, etc. For nodulation, see Becking (1965) and Russell et al. (2002: the fungus Glomus is involved, and nitrogen does not seem to be fixed in the nodules). Accessory transfusion tissue extends to the leaf margin in Podocarpus macrophyllus (Gifford & Foster 1989), but how widely this character occurs is unclear. 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 is controversial; Chamberlain (1935) interprets it as possibly being equivalent to the ovuliferous scale. Indeed, the single ovules of Podocarpaceae seem very different from the cones of other Pinales, however, 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), and for general information, see the Gymnosperm Database.
Phylogeny. RbcL analyses (Conran et al. 2000; Wagstaff 2004b) tend to result in Phyllocladus being embedded in Podocarpaceae, other analyses, whether (Quinn et al. 2002) or not (Sinclair et al. 2002) including rbcL sequences, have the two as sister groups. Peery et al. (2008) using the nuclear XDH gene also found Phyllocladus to be embedded in Podocarpaceae, and it is looking as if that is where it will have to go. for phylogeny, see also Kelch (1998), a comparison of morphology and molecules.
Previous Relationships. Phyllocladus, with its phylloclades, highly reduced leaves that may lack any associated leaf gaps, distinctive pollen capture, etc., has long been considered very distinctive, sometimes being separated from all other conifers (e.g. Keng 1974, 1979; see also Tomlinson et al. 1989, 1997; cf. Quinn 1986).
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 germination [microgametophyte naked], prothallial cells 0.
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
Leaves reduced to scales, short shoots as photosynthetic cladodes; plant monoecious; microsporophyll with flattened apical expansion, (1-)2 microsporangia/microsporophyll, pollen microtuberculate (microechinate); 7-9 inverted ovules/ovuliferous scale, pollen chamber?; seeds narrowly winged; n = 10.
1/1: Sciadopitys verticillata. C. and S. Japan (map: from Florin 1963). [Sciadopitys Photos - Collection]
Fossils of Sciadopitys are known from the Upper Cretaceous and are common in the European Tertiary.
There has been much debate over whether the photosynthesising structures ofSciadopitys are phylloclades - perhaps formed by the connation of two leaves - or cladodes, basically stem structures. The two vascular bundles, each with its own endodermis, have abaxial xylem and adaxial phloem, a rather odd arrangement, and Sporne (1965) notes that on occasion branches develop from these leafy structures, so rather favoring the latter alternative (see also Farjon 2005c).
For pollen, see Page (1990), for a monograph, see Farjon (2005c), and for general information, see the Gymnosperm Database.
Cupressaceae + Taxaceae: cone scales opposite; megasporangia hypodermal [?level].
CUPRESSACEAE Bartling Back to Pinales
(Stem apex with tunica/corpus construction); xylem or phloem resin ducts inducible [seperate clades]); branchlets deciduous; leaves shed along with branches, scale- or needle-like, (opposite - Cupressus, etc., and nodes 1:2); plant ?; (1-)2-10(-14) microsporangia/microsporophyll, pollen microverrucate; ovuliferous scales small (usu. not obvious at all; large, Taxodium and relatives), (bract scale fleshy - Juniperus; with adaxial development), 1-9(-many) erect or inverted ovules/scale; seeds winged or not; (cotyledons -9(-15)); n = 11.
30/133: Juniperus (52 [ca 50-70 - Adams 2004]), Callitropsis (18), Callitris (14), Cupressus (12). 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. The telial stage of Gymnosporangium rust is common on some Cupressaceae, especially Juniperus, while the aecial stage characterises Rosaceae-Maloideae (Savile 1979b).
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).
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).
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). Cupressus has turned out to be polyphyletic and is now restricted to the Old World (Xiang & Li 2005; especially Little 2006).
For cone morphology, see Farjon and Garcia (2003) and Schulz and Stützel (2007: interesting analysis, but unfortunately Juniperus etc. not included).
Phylogeny. 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).
Classification. 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).
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 Brechtold & 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 fibers in phloem crystalliferous, sclereids + [Taxus]; pollen inaperturate; ovules erect; pollen chamber +, pollination drops +; male gametes unequal in size.
6/30. Northern Hemisphere, scattered, also New Caledonia.
2-3 microsporangia/microsporophyll; ovuliferous scale much reduced, 2 ovules/scale; female gametophyte with 1024-4096 free nuclei; seed coat vascularised, with sarco- and sclerotesta; 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 axils of vegetative leaves; female gametophyte with ca 256 free nuclei; seed arillate; 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). [Photos - Collection.]
Synonymy: Amentotaxaceae Kudô & Yamamoto, Austrotaxaceae Nakai, Torreyaceae Nakai
Evolution. Taxol and related compounds are synthesised 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).
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. Taxus and its imediate relative have female cones with a single ovule and the seed is surrounded by an aril.
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. Page (1990) also included Amentotaxus in Cephalotaxaceae, although he noted that affinities between the two were "somewhat enigmatic"; a family as so delimited appears para- or polyphyletic in Quinn et al. (2002) and Price (2003). 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.
Classification.
for general information, see the Gymnosperm Database.Previous Classifications. Cephalotaxaceae and Taxaceae have sometimes been separated (see introduction to Pinales above).