DESCRIPTION OF THE PHYLUM CONIFEROPHYTA (COULTER 1912)

EUKARYA> ARCHAEPLASTIDA> VIRIDIPLANTAE> STREPTOBIONTA> EMBRYOPHYTA> TRACHEOPHYTA> SPERMOPHYTA> CONIFEROPHYTA

Coniferophyta (ko-ni-fe-RA-fa-ta) is made from two Latin and one Greek root that mean cone (conus); bear (fero); plant (phyto -φυτο). The reference is to plants that bear cones, a common attribute of most members of this phylum.

INTRODUCTION TO THE CONIFEROPHYTA The conifers are remarkably successful as a group, and are among the most common plants in many temperate, alpine, and sub-arctic environments (Figures 1-7). The conifers generally have strong monopodial (text with tooltip) Monopodial (adj.) pseudopodia describes the condition where an amoeboid makes a single major pseudopodium at a time. vegetative growth. Likely, the monopodial growth habit characteristic of many conifers served them in the evolutionary arms race with huge sauropods like Brachiosaurus. The stems and roots have an active vascular cambium (text with tooltip) A cambium is a zone of meristematic tissue which produces lateral growth in a plant axis. A vascular cambium produces xylem and phloem, a cork cambium occurs in the cortex and produces cork as a covering of older woody stems. , and produce large amounts of wood. This attribute, and their tendency to grow in almost pure stands of uniform age has made them economically important wood producers. The wood of conifers is relatively soft and is the wood of choice for framing homes and the production of plywood. Their leaves vary from needle-like to scale-like to strap-like. And most, but not all, are evergreen. Their reproductive structures almost always occur in strobili (text with tooltip) A strobilus is an axis of fertile appendages. A simple strobilus is an axis of sporophylls. A compound strobilus is an axis of simple fertile axes. Sometimes the compound cones have simple fertile axes that are reduced to a single sporophyll and appear to be simple strobili. . Some strobili are simple cones. That is, the cone segments that bear sporangia are modified leaves or sporophylls. Some conifers, however, have strobili that are individually reduced but are arranged on a common axis. In other words, a compound cone or strobilus is a strobilus of strobili. That is, each cone scale of a Pinus ovulate cone is a strobilus reduced to a flat, leaf-like axis with two seeds. Some of the earliest conifers like Cordaites (Cordaitopsida, Figure 8) had both compound staminate and ovulate strobili; however, Lebachia (Voltziopsida, Figure 9) had compound ovulate but simple staminate strobili. Like the voltziopsids, most modern conifers have compound ovulate cones and simple staminate cones. Today, taxa in the Taxales have simplified the ovulate cone to single scales. The life histories of the extant conifers are variations on that of Pinus (e.g. Figure 10). Early in the spring small simple strobili with abaxial (text with tooltip) Abaxial is derived from two Latin terms ab (away from) and axis (originally, the axil of a wagon). Abaxial (adj.) is a botanical term that means the underside of a leaf, or the side facing away from the stem (the axis). sporangia (microsporangia) on microsporophylls. The microspore mother cells undergo meiosis to form microspores within the microsporangium. A microspore becomes a pollen grain when the microspore divides to form a generative cell and a prothallial cell. The spore wall which is made of two layers, the entine and the exine, separates and the external wall becomes two balloon-like extensions (giving the pollen grain a Mickey Mouse appearance). The prothallial cell divides again to form two cells. This is what the gametophyte thallus has been reduced to in the conifers (and other seed plants). The generative cell divides to form a tube cell and a generative cell (this will divide once more to form the two sperm). The tube cell grows slowly through the megasporangial wall of the seed until 14 months after pollination the pollen tube enters the archegonial chamber. Months earlier, the ovule begins to develop on the adaxial surface of the megastrobilus cone scale. Before the formation of the megagametophyte, the ovule, which has its micropyle oriented toward the cone axis, exudes a droplet that catches pollen in the surface tension. When the droplet is reabsorbed, the pollen grains caught by it are pulled through the micropyle and into the pollen chamber (this step is called pollination). The megasporangium has a single megaspore mother cell which undergoes meiosis to form a linear tetrad of megaspores, three of which are aborted. The megaspore begins to undergo free-nuclear enlargement after which it becomes cellular. Some of the cells closest to the micropylar end differentiate into eggs (Pinus can have up to 11 eggs in a single ovule). Fertilization occurs 14 months later when the pollination tube enters the archegonial chamber and one of the two sperm fuse with the egg and a zygote is formed. The zygote begins to develop into an embryonic plant with multiple cotyledons. The mature seed has a seed coat formed by the integuments (parental 2N), a megasporangium (parental 2N), a megagametophyte (1N), and an embryo (daughter 2N). When released, the seed has an elongation of the integument which forms a propeller allowing for greater range of dispersal (Figure 10). Like ferns, conifers have been among the dominant plants almost from the time of their origin in the Carboniferous (Figures 8 and 9). They increased in importance well into the Mesozoic and were important members of the landscape when flowering plants appeared. The abundant conifers left remains of many fossils of their wood and leaves. In addition, the resin produced by most conifers has fossilized to form amber.

FIGURE 1. A wizened bristlecone pine (Pinus), one of the longest-lived species on earth. Image from http://www.science.siu.edu/landplants/Coniferophyta/coniferophyta.html	FIGURE 2. Sequoia, a genus of giant and long-lived trees. This plant shows the typical monopodial growth habit of many conifers. Image from http://sysnet.ucsd.edu/~iramani/sequoia/Standing%20tall%20-%20Giant%20sequoia.htm	FIGURE 3. The berry-like cones of the red cedar (Juniperus). Image from http://www.ces.ncsu.edu/depts/hort/consumer/factsheets/trees-new/
FIGURE 4. Araucaria with a typical monopodial growth habit. Image from http://www.anbg.gov.au/anbg/conifers/araucaria-cunning.html	FIGURE 5. The stalked “fruit” of Podocarpus. The fleshy fruit-like structure beneath the seed is a modified fleshy megasporophyll called an aril (text with tooltip) Outgrowths of the funiculus (stalk that attaches the ovule to the placenta), forming a cup-shaped appendage or outer covering of a seed. . Image from http://farrer.riv.csu.edu.au/ASGAP/APOL25/mar02-5l.html	FIGURE 6. Cephalotaxus also has seeds (text with tooltip) Unit of sexual reproduction in some plants. Formed when an ovule is fertilized and comprised of outer coat that encloses stored food and an embryo. borne on a lateral branch that we interpret as a very loose ovulate cone. Image from http://www.richmond.edu/~jhayden/conifers/cephalotaxus.html
FIGURE 7. The seeds of Taxus are borne in arils that occur individually on the stem. Image from http://www.funet.fi/pub/sci/bio/life/plants/magnoliophyta/pinophytina/taxaceae/taxus/	FIGURE 8. A reconstruction of Cordaites, a very successful Paleozoic conifer that had long strap-like leaves. Image from http://www.ucmp.berkeley.edu/seedplants/cordaitales/cordaites.gif	FIGURE 9. A compression of a Lebachia leafy branch from the lower Mesozoic. Image from http://www.ucmp.berkeley.edu/IB181/VPL/CorCon/CorConVGIII.html

FIGURE 10. Pinus Life History. A. Mature plant, B. Staminate cones, C. Abaxial microsporangium, D. Mature pollen grain, E. Ovulate cone, F. Pine ovule on the adaxial surface of the ovulate cone scale illustrating pollination, G. Fertilization after the pollen tube enters the archaegonial chamber, H. Detail of the pollen tube with the two sperm, I. Maturing seed with endosperm and embryo, J. Mature seed with developed embryo, K. A germinating seedling. From Norstog (1976)

SYSTEMATICS OF THE CONIFEROPHYTA The origin of conifers has been a puzzle. Their similarities to the progymnosperms have led authors like Pearson (1995) to place them near the root of the gymnosperm phylogeny. Crane (1996, Tree of Life Project) and Tudge (2000) show the conifers emerging with the ginkgophytes and cycads as sisters to the gnetophyte-flowering plant clade. Chaw et al. (2000) and Bowe (2000) present similar analyses based on multiple genes (3 genomes: nuclear, mitochondrial, and chloroplast) in which Ginkgo is a sister to the gnetophyte-conifer clade. Their analyses show the conifers separating into two groups. Conifer group 1 is made of the Pinaceae and the Gnetophytes. Conifer group 2 is all of the other extant conifers. The relative position of the gnetophytes appears to be key not only to understanding the confers, but also the topology of the spermophyte branch of the plant tree. The gne-pine hypothesis suggests that the gnetophytes are sisters to Pinaceae and emerge within the conifers (e.g. Chaw et al. 2000, Soltis et al. 2002, Matthews 2009). Other analyses (e.g. Zhong et al. 2010, Zhong et al. 2011) suggest the gne-cup hypothesis in which the gnetophytes are sisters to the Cupressopsida clade of the conifers. Other analyses (e.g. Ran et al. 2010) show that the gnetophytes are sisters to the conifers or sisters to all living seed-bearing plants (e.g. Rai et al. 2008). Fossil and morphological analyses associate the gnetophytes with the flowering plants (Hilton and Bateman 2006, Doyle 2006). Doyle (2006), Hilton and Bateman (2006), and Tomescu (2008) summarize molecular and morphological cladistic analyses which point the conifers in two different directions. The molecular work embeds the gnetophytes in a conifer clade that includes the Pinales. The morphological analyses based on ovule position, sperm transfer support the molecular trees. However, Tomescu (2008), whose analysis is centered on leaf organization, suggests that the gnetophytes are separate from the conifers. Figure 11 is an integration of molecular, anatomical, developmental, and fossil work. In our system, the conifers are monophyletic with the Pinaceae sisters to the rest of the extant conifers (the Cupressopsida). The gnetophytes are sisters to the conifers and the flowering plants are basal to the conifers+gnetophytes+ginkgophytes. Based on this topology, we have organized the living conifers into two classes: Pinopsida (1 family) and Cupressopsida (6 families). This is very different from the classical systematic treatments of the conifers (e.g. Bold et al. 1987) in which the conifers are separated according to the ovulate cones: Coniferopsida (compound ovulate cones) and Taxopsida (simple, reduced isolated ovules on sporophylls).

FIGURE 11. The relationships between spermophytes (seed plants) is an integration of molecular studies (Chaw et al. 2000, Soltis et al. 2002, Matthews 2009, Zhong et al. 2010, Zhong et al. 2011, Ran et al. 2010, Rai et al. 2008), anatomy and fossil evidence (Doyle 2006, Hilton and Bateman 2006, and Tomescu 2008). In this cladogram, the conifers (taxa in shaded box) are monophyletic and include the extinct Cordaitopsida and Voltziopsida. The gnetophytes are sisters to the conifers.

LITERATURE CITED Banks, H. P. 1975. Reclassification of Psilophyta. Taxon. 24: 401-413. Bierhorst, D. W. 1971. Morphology of Vascular Plants. In: N. H. Giles and J. G. Torrey. The MacMillan Biology Series. The MacMillan Co. New York. Bold, H. C., C. J. Alexopoulos, and T. Delevoryas. 1987. Morphology of Plants and Fungi. 5th Edition. HarperCollins Publishers, Inc. New York. Cantino, P., J. A. Doyle, S. W. Graham, W. S. Judd, R. G. Olmstead, D. E. Soltis, P. S. Soltis, and M. J. Donoghue. 2007. Towards a phylogenetic nomenclature of Tracheophyta. Taxon 56(3): E1-E44. Chaw S.-M., C. L. Parkinson, Y. Cheng, T. M. Vincent, and J. D. Palmer. 2000. Seed plant phylogeny inferred from all three plant genomes: Monophyly of extant gymnosperms and origin of Gnetales from Conifers. Proceedings of the National Academy of Sciences (USA) 97:4086-4086. Crane, P. 1996. Spermatopsida. Seed Plants. Version 01 January 1996 (temporary). http://tolweb.org/Spermatopsida/20622/1996.01.01 in The Tree of Life Web Project, http://tolweb.org/ Dittmer, H. J. 1964. Phylogeny and Form in the Plant Kingdom. Van Norstrand Company, Inc. New York. Doyle, J. A. 1998b. Phylogeny of vascular plants. Annual Review of Ecology and Systematics. 29:567-599. Doyle, J. A. 2006. Seed ferns and the origin of angiosperms. Journal of the Torrey Botanical Society. 133(1): 169-209. [C] Hilton, J. and R. M. Bateman. 2006. Pteridosperms are the backbone of seed-plant phylogeny. Journal of the Torrey Botanicaal Society. 133(1): 119-168. Kenrick, P. and P. R. Crane. 1997b. The Origin and Early Diversification of Land Plants: A Cladistic Study. Smithsonian Institute Press. Washington, D.C. Matthews, S. 2009. Phylogenetic relationships among seed plants: persistent questions and the limits of molecular data. American Journal of Botany. 96(1): 228-236. Northington, D. K. and J. R. Goodin. 1984. The Botanical World. Times Mirror/Mosby College Publishing, St. Louis. Pearson, L. C. 1995. The Diversity and Evolution of Plants. CRC Press. New York. Rai, H. S., P. A. Reeves, R. Peakall, R. G. Olmstead, and S. W. Graham. 2008. Inference of higher-order conifer relationships from multi-locus plastid data set. Botany. 86:658-669. Ran, J-H., H. Gao, X-Q. Wang. 2010. Fast evolution of the retroprocessed mitochondrial rps3 gene in Conifer II and further evidence for the phylogeny of gymnosperms. Molecular Phylogenetics and Evolution. 54: 136-149. Soltis, D. E., P. S. Soltis, and M. J. Zanis. 2002. Phylogeny of seed plants based on evidence from eight genes. American Journal of Botany. 89:1670-1681. Tomescu, A. M. F. 2008. Megaphylls, microphylls and the evolution of leaf development. Trends in Plant Science. 14(1): 5-12 Zgurski, J. M., H. S. Rai, Q. M. Fai, D. J. Bogler, and J. Francisco-Ortega. 2008. How well do we understand the overall backbone of cycad phylogeny? New insights from a large, multigene plastid data set. Molecular Phylogenetics and Evolution. 47: 1232-1237. Zhong, B., T. Yonezawa, Y. Zhong, and M. Hasegawa. 2010. The position of Gnetales among seed plants: overcoming pitfalls of chloroplast phylogenomics. Molecular Biology and Evolution. 27(12): 2855-2863. Zhong, B., O. Deusch, V. V. Goremykin, D. Penny, P. J. Biggs, R. A. Atherton, S. V. Nikiforova, and P. J. Lockhart. 2011. Systematic error in seed plant phylogenomics. Genome Biology and Evolution. 3: 1340-1348.

By Jack R. Holt. Last revised: 04/16/2020