|DIVERSITY OF LIFE|
Gymnosperms include all seed-bearing plants whose ovules are exposed such that the pollen goes through the micropyle during pollination. The seed, 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].
Pearson (1995) illustrated the seed plants as forming an early radiation event of Pteridospermophytes that gave rise to two main branches. One line led to the rest of the Pteridospermophyta, the Cycadeoidophyta, and the Gnetophyta. The other branch led to the Coniferophyta, Ginkgophyta, Cycadophyta, and the Angiospermophyta. Curiously, the cycads in Pearson's scheme are closest to the flowering plants. However, his whole phylogenetic scheme for the seed plants seems unlikely to me because it runs counter to the evidence of morphology, development, and paleontology.
Tudge (2000) and the Crane (1996; Tree of Life Project) illustrate similar relationships between seed plant taxa (see Figure 1). Both are summaries based on combinations of molecular, morphological, developmental, and paleontological data. Their conclusions are:
The molecular phylogenetic analyses of Chaw et al. (2000), Bowe et al. (2000), and Qiu et al. (2006 & 2007) show the flowering plants as sisters to the gymnosperms. Further, they show that the cycads and ginkgophytes are basal in the gymnosperm line. An interesting outcome of their molecular analyses is the monophyletic clade, Pinaceae + Gnetophyta (called the Gne-Pine Hypothesis, Figure 2-A).
|FIGURE 1. MAJOR CLADES OF THE GYMNOSPERMS. This figure is an adaptation of Crane (1996) from the Tree of Life Project. Clade 1 includes all of the plants with the seed habit. Clade 2 contains the early seed ferns, which are sisters to all other seed-bearing plants. Clade 3 is the late seed ferns plus the angiosperms. This is a paraphyletic group which includes the Mesozoic pteridosperms, cycads, conifers, ginkgophytes and the cycadeiods+gnetophytes+angiosperms..|
Alternative hypotheses abound in considering the relationships between the seed plants. 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.
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).|
The question of the position of the pteridosperms in the seed plants cannot be answered by molecular means. 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. A hint of the true complexity of the Seed Plants can be seen in Figure 3, a figure from Doyle (2006).
|FIGURE 3. The Phylogeny of Seed Plants from Doyle (2006) as used in Mathews (2009). I have marked the groups that have traditionally been referred to as Pteridosperms with an asterisk (*), which illustrates the polyphyletic nature of the group. Note that Doyle, a paleontologist, illustrates a modification of the Anthophyte Hypothesis with the Gnetophytes in the clade with the Flowering Plants but sisters to the Flowering Plants + Cycadeoids.|
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, I will continue to use that source until a clear consensus develops regarding the molecular evidences. Those taxa that are marked with an cross (+) are extinct (as are all lower taxa within that taxon). Orders are followed by representative genera.
Crossotheca, Lagenostoma, Lyginopteris.
Alethopteris, Dolerotheca, Medullosa, Neuropteris, Pachytesta.
Callandrium, Callistophyton, Callospermarium, Idanothekion.
Bowenia, Ceratozamia, Cycas, Dioon, Encephalartos, Lepidozamia, Macrozamia, Microcycas, Stangeria, Zamia.
PHYLUM GINKGOPHYTACLASS GINKGOOPSIDA
Ginkgo, Baieria+, Ginkgoites+.
Amyelon, Cardiocarpus, Cordaianthus, Cordaites, Premnoxylon.
Abies, Cedrus, Larix, Pinus, Pseudolarix, Pseudotsuga, Tsuga, Picea,
Cryptomeria, Cunninghamia, Metasequoia, Sciadopitys, Sequoia, Sequoiadendron, Taxodium.
Callitris, Chamaecyparis, Cupressus, Juniperus, Thuja.
Agathis, Araucaria, Aucarioxylon+.
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.
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/
Doyle, J. A. 2006. Seed ferns and the origin of angiosperms. Journal of the Torrey Botanical Society 133(1): 169-209.
Mathews, S. 2009. Phylogenetic relationships among seed plants: Persistent questions and the limits of molecular data. American Journal of Botany. 96(1): 228-236.
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.
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.
Tudge, C. 2000. The Variety of Life, A Survey and a Celebration of all the Creatures That Have Ever Lived. Oxford University Press. New York.
By Jack R. Holt and C.A. Iudica. Last revised: 04/02/2012