DESCRIPTION OF THE GYMNOSPERMS

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

Gymnosperm (DZHIM-no-sperm) is an informal term for all seed plants that have exposed ovules so that pollen enters the micropyle. The term is derived from two Greek roots that mean naked (gymnos -γυμνός) and seed (sperma -σπέρμα).

INTRODUCTION TO THE GYMNOSPERMS Gymnosperms include all seed-bearing plants whose ovules (text with tooltip) An ovule is a structure that contains the megagametophyte in seed plants. The megagametophyte remains within the megasporangium (the nucellus), which is surrounded by layers of integuments. After fertilization, the ovule develops into a seed. are exposed such that the pollen (text with tooltip) The collective mass of grains produced within the anthers of flowering plants or the male cones of a gymnosperm. In all seed plants, pollen is generated by the development of a microspore into a microgametophyte. The germination of the pollen grain leads to the development of a pollen tube, which delivers two sperm or sperm nuclei to the egg in the ovule. In flowering plants, mature microgametophyte has only two cells, a tube cell and a generative cell. goes through the micropyle (text with tooltip) An opening in the integuments of an ovule that exposes part of the megasporangial wall (a chamber called a pollen chamber in gymnosperms). Thus, in gymnosperms, pollen enters the micropyle and germinates in the pollen chamber. However, because the micropyle is not exposed in flowering plants, their pollen germinates on the stigma. The pollen tube grows through the style, and enters the ovule through the micropyle. during pollination. The seed (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. , one of the most marvelous products of evolution, is so complex that all seed plants must be monophyletic. The vegetative tissues, particularly the stems, support that concept. Further confirmation comes from Chaw et al. (2000) who examined relationships among all living groups of seed plants based on nuclear, chloroplast and mitochondrial similarities. [Read about the Seed Habit and its evolution in the Pteridospermophyta]. The seed habit of most vascular plants almost certainly evolved within a heterosporous (text with tooltip) Heterosporous plants have sporangia that produce spores of different sizes: megaspores (large) and microspores (small). Megaspores produce archegoniate gametophytes, and microspores produce antheridial gametophytes. line of Progymnospermaophyta. Because the seed, the structure that contained the megagametophyte, was retained on the parent plant, the microgametophyte had to be able to move. In this scenario, the microgametophyte was retained within the microspore (text with tooltip) Microspores is a small spore, and the term is applied to many different types of spores in the microbial eukaryotes and plants. Usually, they are the products of meiosis. wall and became pollen. The megagametophyte was retained within the wall of the megasporangium and covered by several integuments that were derived from the parent plant. Figure 1 illustrates the salient features of the seed habit with pollen emerging from the microsporangium. The ovule (text with tooltip) An ovule is a structure that contains the megagametophyte in seed plants. The megagametophyte remains within the megasporangium (the nucellus), which is surrounded by layers of integuments. After fertilization, the ovule develops into a seed. (on the right in Figure 1) illustrates how the integument does not completely close at the apex (the micropyle) and creates a chamber in which the pollen germinates and sends a haustorium (text with tooltip) Modified hyphae of parasitic fungi that penetrate host cell. (called a pollen tube) through the megasporangial wall (the nucellus (text with tooltip) Central part of a plant ovule; contains the embryo sac. ) into the megagametophyte where one or more endosperm (text with tooltip) The nutritive storage tissue that grows from the fusion of a sperm cell with polar nuclei in the embryo sac. ). After maturation. the seed has three generations: the integument and nucellus are parental sporophyte, the endosperm is megagametophyte, and the embryo is the daughter sporophyte.

FIGURE 1. The seed habit is characterized by the megagametophyte retained on the parent plant and enclosed in sporophytic tissue (integument); the seed habit also requires that the microgametophyte be enclosed in a pollen coat and transported to the megagametophyte for development and release of sperm. Early pollen — sometimes called “prepollen” — retained the plesiomorphic character of being trilete. Therefore, “pollen” is a functional, not morphological, term.

Image and description from: http://www.ucmp.berkeley.edu/IB181/VPL/Osp/OspD/OspD11.gif

The relationships between the seed-bearing plants are quite unsettled and seem to vary according to the types of analyses, and alternative hypotheses abound. Sanderson et al. (2000) consider the placement of the gnetophytes in the seed plants (in additon to the Gne-Pine Hypothesis, Figure 2-A). They explore different evolutionary scenarios (see Figure 2-B through 2-D). Each is supported differentially by molecular evidence, developmental evidence, anatomical evidence, and paleontological evidence. Sanderson et al. (2000) used two chloroplast photosystem genes, psaA and psbB. Then, they looked for differential signal from the first, second, and third codon positions. The first two positions of the codon supported the Gne-Pine Hypothesis (Figure 2-A) or the Gymnosperm Hypothesis (Figure 2-C). The third codon position supported the Gnetales Hypothesis in which the gnetophytes are sisters to all living seed plants, making the Gymnosperms paraphyletic. Curiously, none of their analyses, nor other analyses of Chaw et al. (2000), Bowe et al. (2000), and Qiu et al. (2006 & 2007) supported the Anthophyte Hypothesis (Figure 2-D), the hypothesis that is most strongly supported by anatomy and development. Sanderson et al. (2000) blame the incongruence on problems with long-branch attraction, error related to molecular sequences because they have few character states (four bases) per position and can serendipitously coincide in rapidly-evolving lines. Burleigh and Mathews (2004) had the same results with five different genes (18S rRNA, 26S rRNA, rbcL, atpB, and matK. After eliminating the fastest-evolving regions, they had a strong signal for the Gne-Pine Hypothesis. The results led Mathews (2009) to consider the problems raised by the seed plant phylogenies and concluded that because most of the lines are extinct, molecular data alone may give skewed information and cannot answer some of the most important questions about the rooting of the seed plants or the sister group of the flowering plants. Certainly, the elucidation of the closest relatives of the gnetophytes will be very important in sorting out the seed plant branch of the plant tree.

A. THE GNE-PINE HYPOTHESIS	B. THE GNETALES HYPOTHESIS
C. THE GYMNOSPERM HYPOTHESIS	D. THE ANTHOPHYTE HYPOTHESIS
FIGURE 2. FOUR MAJOR SEED PLANT EVOLUTIONARY SCENARIOS. Different hypotheses for the relationships between the living seed plants as discussed by Sanderson et al. (2000) and Burleigh and Mathews (2009).

Because living spermophytes are remnants of a once diverse set of seed-bearing taxa that have a geological history going back to the Devonian, the living taxa that are part of the continuum appear to be distinct and isolated. Figure 3 is a composite of molecular (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). We have accepted the Gymnosperm Hypothesis as the most conservative of the four in Figure 2. The extant higher taxa of the seed plants are scattered among extinct lines, mostly of taxa identified as pteridosperms. Thus, the problems of the relative positions of the living plant groups is an artifact of the remnants, only two of which are speciose: Coniferophyta and Angiospermophyta. The question of the position of the pteridosperms in the seed plants cannot be answered by molecular means alone. Indeed, they may represent a level of organization such that an adequate understanding of them likely will bring about a restructuring of the seed plant taxa. That can be accomplished only by more extensive paleontological and anatomical work. Obviously, much more has to be done in order to sort out relationships of the groups well enough to produce a phylogenetic taxonomy that is consistent with all of the evidence. Therefore, because the system of Bold et al. (1987) reflects the classical system for the gymnosperms, we will continue to use that source until a clear consensus develops regarding the molecular evidences.

FIGURE 3. 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 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. Bowe, L. M., G. Coat, and C. W. dePamphilis. 2000. Phylogeny of seed plants based on all three genomic compartments: Extant gymnosperms are monophyletic and Gnetales’ closest relatives are conifers. Proceedings of the National Academy of Sciences (USA) 97:4092-4097. Burleigh, J. G. and S. Mathews. 2004. Phylogenetic signal in nucleotide data from seed plants: Implications for resolving the seed plant tree of life. American Journal of Botany. 91(10): 1599-1613. 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. 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] Friedman, W. E. 1990a. Double fertilization in Ephedra, a nonflowering seed plant: its bearing on the origin of angiosperms. Science 247:951-954. Friedman, W. E. 1990b. Sexual reproduction in Ephedra nevadensis (Ephedraceae): further evidence of double fertilization in a nonflowering seed plant. American Journal of Botany. 77:1582-1598. Friedman, W. E. 1992. Evidence of a pre-angiosperm origin of endosperm: implications for the evolution of flowering plants. Science 225:336-339. Friedman, W. E., R. C. Moore, and M. D. Purugganan. 2004. The evolution of plant development. American Journal of Botany 91: 1726-1741. Friedman, W. E. 1994. The evolution of embryogeny in seed plants and the developmenal origin and early history of endosperm. American Journal of Botany. 81:109:153-226. Friedman, W. E. and S. K. Floyd. 2001. Perspective: The origin of flowering plants and their reproductive biology – a tale of two phylogenies. Evolution 55:217-231. 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, DC. 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. Qiu, Y. L., L. Li, B. Wang, Z. Chen, V. Knoop, M. Groth-Malonek, O. Dombrovska, J. Lee, L. Kent, J. Rest, G.F. Estabrook, T.A. Hendry, D.W. Taylor, C.M. Testa, M. Ambros, B. Crandall-Stotler, R.J. Duff, M. Stech, W. Frey, D. Quandt, and C.C. Davis. 2006. The deepest diverges in land plants inferred from phylogenomic evidence. Proceedings of the National Academy of Sciences. 103:15511-15516. Qiu, Y. L., L. Libo, B. Wang, Z. Chen, O. Dombrovska, J. Lee, L. Kent, R. Li, R. Jobson, T. A. Hendry, D. W. Taylor, C. M. Testa, and M. Ambros. 2007. A nonflowering land plant phylogeny inferred from nucleotide sequences of seven chloroplast, mitochondrial, and nuclear genes. International Journal of Plant Science. 168(5): 691-708. 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. Sanderson, M. J., M. F. Wojciechowski, J.-M. Hu, T. Sher Khan, and S. G. Brady. 2000. Error, bias, and long-branch attraction in data for two chloroplast photosystem genes in seed plants. Molecular Biology and Evolution. 17(5): 782-797. 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. Zhu, W.-Q. and P. Kenrick. 1999. A Zosterophyllum-like plant from the lower Devonian of Yunnan Province, China. Review of Palaeobotany and {alynology. 105: 111-118.

By Jack R. Holt. Last revised: 04/02/2014