Male Cone Evolution in Conifers: Not All That Simple

Abstract

Despite the simple structure of male conifer cones, there is an enormous variability in cone properties observed upon more careful examination. The diversity ranges from simple cones to compound cones. Moreover, cones can be distinguished according to different spatial distributions on the tree. Simple cones are distributed either as solitary cones or as fascicular or clustered aggregations, while compound cones only exhibit fascicular or clustered aggregations. Here, we demonstrate that these different spatial distribution patterns correlate with distinct leaf types and variable branching frequencies. Furthermore, we provide new insights into the evolution of the sporangiophore, particularly in Taxaceae. Two notably important and fast-evolving characters of conifers are the number of sporangia per sporangiophore and the number of sporangiophores per cone. We demonstrate, across many species and types of cones, how these characters are able to adjust according to the optimal amount of pollen.

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Schulz, C. , Klaus, K. , Knopf, P. , Mundry, M. , Dörken, V. and Stützel, T. (2014) Male Cone Evolution in Conifers: Not All That Simple. American Journal of Plant Sciences, 5, 2842-2857. doi: 10.4236/ajps.2014.518300.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Leslie, A.B., Beaulieu, J.M., Rai, H.S., Crane, P.R., Donoghue, M.J. and Mathews, S. (2012) Hemisphere-Scale Differences in Conifer Evolutionary Dynamics. Proceedings of the National Academy of Sciences of the United States of America, 109, 16217-16221.
http://dx.doi.org/10.1073/pnas.1213621109
[2] Little, D.P. (2006) Evolution and Circumscription of the True Cypresses (Cupressaceae: Cupressus). Systematic Botany, 31, 461-480.
http://dx.doi.org/10.1043/05-33.1
[3] Farjon, A. (2010) A Handbook of the World’s Conifers. Volume I, II, Brill, Leiden, Boston.
[4] Knopf, P., Schulz, C., Little, D.P., Stützel, T. and Stevenson, D.W. (2012) Relationships within Podocarpaceae based on DNA Sequence, Anatomical, Morphological, and Biogeographical Data. Cladistics, 28, 271-299.
http://dx.doi.org/10.1111/j.1096-0031.2011.00381.x
[5] Mao, K.S., Milne, R.I., Zhang, L.B., Peng, Y.L., Liu, J.Q., Thomas, P., Mill, R.R. and Renner, S.S. (2012) Distribution of Living Cupressaceae Reflects the Breakup of Pangea. Proceedings of the National Academy of Sciences of the United States of America, 109, 7793-7798.
http://dx.doi.org/10.1073/pnas.1114319109
[6] Little, D.P., Knopf, P. and Schulz, C. (2013) DNA Barcode Identification of Podocarpaceae—The Second Largest Conifer Family. PLOS ONE, 8, 1-11.
http://dx.doi.org/10.1371/journal.pone.0081008
[7] Rothwell, G.W. and Basinger, J.F. (1979) Metasequoiamilleri n.-sp., Anatomically Preserved Pollen Cones from the Middle Eocene (Allenby Formation) of Columbia. Canadian Journal of Botany-Revue Canadienne De Botanique, 57, 958-970.
http://dx.doi.org/10.1139/b79-118#.U4w8iShCCLc
[8] Serbet, R. and Stockey, R.A. (1991) Taxodiaceous Pollen Cones from the Upper Cretaceous (Horseshoe Canyon Formation) of Drumheller, Alberta, Canada. Review of Palaeobotany and Palynology, 70, 67-76.
http://dx.doi.org/10.1016/0034-6667(91)90078-H
[9] Smith, S.Y. and Stockey, R.A. (2002) Permineralized Pine Cones from the Cretaceous of Vancouver Island, British Columbia. International Journal of Plant Sciences, 163, 185-196.
http://dx.doi.org/10.1086/324553
[10] Chamberlain, C.J. (1935) Gymnosperms: Structure and Evolution (Reprint 1982). University of Chicago Press, Chicago.
[11] Schulz, C. and Stützel, T. (2006) Variability of Pollen Cones in Chamaecyparis as an Example for Cupressaceae Pollen Cones. Feddes Repertorium, 117, 146-157.
http://dx.doi.org/10.1002/fedr.200511085
[12] Dörken, V.M., Zhang, Z.X., Mundry, I.B. and Stützel, T. (2011) Morphology and Anatomy of Male Cones of Pseudotaxus chienii (W.C. Cheng) W.C. Cheng (Taxaceae). Flora, 206, 444-450.
http://dx.doi.org/10.1016/j.flora.2010.08.006
[13] Schulz, C., Jagel, A. and Stützel, T. (2003) Cone Morphology in Juniperus in the Light of Cone Evolution in Cupressaceae s.l. Flora, 198, 161-177.
http://dx.doi.org/10.1078/0367-2530-00088
[14] Schulz, C. and Stützel, T. (2007) Evolution of Taxodiaceous Cupressaceae (Coniferopsida). Organisms Diversity & Evolution, 7, 124-135.
http://dx.doi.org/10.1016/j.ode.2006.03.001
[15] Dörken, V.M. and Stützel, T. (2012) Proliferating Seed Cones in Metasequoia glyptostroboides Hu & Cheng (Cupressaceae s.l., Coniferales) Elucidating the Evolution of Seed Cones and Ovules in Cupressaceae s.l. and Maybe Conifers on the Whole. Feddes Repertorium, 122, 409-420.
http://dx.doi.org/10.1002/fedr.201200004
[16] Mohl, H.V. (1845) IV. über die Männlichen Blüthen der Coniferen. Vermischte Schriften Botanischen Inhalts, Tübingen, 45-61.
[17] Parlatore, F. (1868) Coniferae. In: de Candolle, A.P., Ed., Prodromus Systematis Regni Vegetabilis, Vol. 16, No. 2, G. Masson, Paris, 361-521.
[18] Mundry, I.B. and Mundry, M. (2001) Male Cones in Taxaceae s.l.—An Example of Wettstein’s Pseudanthium Concept. Plant Biology, 3, 405-416.
http://dx.doi.org/10.1055/s-2001-16466
[19] Duluhosch, H. (1937) Entwicklungsgeschichtliche Untersuchung über die Mikrosporophylle der Koniferen. Bibliotheca Botanica, 114, 1-24.
[20] Dupler, A.W. (1919) Staminate Strobilus of Taxus canadensis. Botanical Gazette, 68, 345-366.
http://www.jstor.org/stable/10.2307/2469243
http://dx.doi.org/10.1086/332570
[21] Worsdell, W.C. (1901) The Morphology of the “Flower” of Cephalotaxus. Annals of Botany, 15, 637-652.
http://aob.oxfordjournals.org/content/os-15/4/637
[22] Celakovsky, L. (1879) Zur Gymnospermie der Coniferen. Flora, 62, 257-264, 273-283.
[23] Goebel, K. (1923) Organographie der Pflanzen. Gustav Fischer, Jena.
[24] Pryer, K.M., Schneider, H., Smith, A.R., Cranfill, R., Wolf, P.G., Hunt, J.S. and Sipes, S.D. (2001) Horsetails and Ferns Are a Monophyletic Group and the Closest Living Relatives to Seed Plants. Nature, 409, 618-622.
http://dx.doi.org/10.1038/35054555
[25] Malaspina, T.T., Cecchi, L., Morabito, M., Onorari, M., Domeneghetti, M.P. and Orlandini, S. (2007) Influence of Meterological Conditions on Male Flowers Phenology of Cupressus sempervirens and Correlation with Pollen Production in Florence. Trees, 21, 507-514.
http://dx.doi.org/10.1007/s00468-007-0143-1
[26] Schulz, C., Knopf, P. and Stützel, T. (2005) Identification Key to the Cypress Family (Cupressaceae). Feddes Repertorium, 116, 96-146.
[27] Gerlach, D. (1984) Botanische Mikrotomtechnik, Eine Einführung, 2. Auflage, Thieme, Stuttgart.
[28] Gerstberger, P. and Leins, P. (1978) Rasterelektronenmikroskopische Untersuchungen an Blütenknospen von Physalis philadelphia (Solanaceae). Berichte der Deutschen Botanischen Gesellschaft, 91, 381-387.
[29] Hall, T. (2004) BioEdit. Ibis Therapeutics, Carlsbad.
http://mbio.ncsu.edu/BioEdit.html
[30] Vaidya, G., Lohman, D.J. and Meier, R. (2011) SequenceMatrix: Concatenation Software for the Fast Assembly of Multi-Gene Datasets with Character Set and Codon Information. Cladistics, 27, 171-180.
http://dx.doi.org/10.1111/j.1096-0031.2010.00329.x
[31] Edgar, R.C. (2004) MUSCLE: Multiple Sequence Alignment with High Accuracy and High Throughput. Nucleic Acids Research, 32, 1792-1797.
http://dx.doi.org/10.1093/nar/gkh340
[32] Nylander, J.A.A. (2004) MrModeltest Version 2. Program Distributed by the Author. Evolutionary Biology Centre, Uppsala University, Uppsala.
[33] Ronquist, F. and Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian Phylogenetic Inference under Mixed Models. Bioinformatics, 19, 1572-1574.
http://dx.doi.org/10.1093/bioinformatics/btg180
[34] Maddison, W.P. and Maddison, D.R. (2011) Mesquite: A Modular System for Evolutionary Analysis. Version 2.75.
http://mesquiteproject.org
[35] Paradis, E., Claude, J. and Strimmer, K. (2004) APE: Analyses of Phylogenetics and Evolution in R Language. Bioinformatics, 20, 289-290.
http://dx.doi.org/10.1093/bioinformatics/btg412
[36] Revell, L.J. (2012) Phytools: An R Package for Phylogenetic Comparative Biology (and Other Things). Methods in Ecology and Evolution, 3, 217-223.
http://dx.doi.org/10.1111/j.2041-210X.2011.00169.x
[37] RStudio (2012) RStudio: Integrated Development Environment for R (Version 0.96.122) [Computer Software], Boston. http://www.rstudio.com
[38] Bateman, R.M., Hilton, J. and Rudall, P.J. (2011) Spatial Separation and Developmental Divergence of Male and Female Reproductive Units in Gymnosperms, and Their Relevance to the Origin of the Angiosperm Flower. In: Wanntorp, L. and Ronse De Craene, L.P., Eds., Flowers on the Tree of Life, Cambridge University Press, Cambridge, 8-48.
http://dx.doi.org/10.1017/CBO9781139013321.002
[39] Wilde, M.H. (1975) New Interpretation of Microsporangiate Cones in Cephalotaxaceae and Taxaceae. Phytomorphology, 25, 434-450.
[40] Keng, H. (1969) Aspects of Morphology of Amentotaxus formosana with a Note on Taxonomic Position of the Genus. Journal of the Arnold Arboretum, 50, 432-448.
[41] Hernandez-Castillo, G.R., Rothwell, G.W. and Mapes, G. (2001) Compound Pollen Cone in a Paleozoic Conifer. American Journal of Botany, 88, 1139-1142.
http://www.amjbot.org/content/88/6/1139
http://dx.doi.org/10.2307/2657097
[42] Thomson, R.B. (1940) The Structure of the Cone in the Coniferae. Botanical Review, 6, 73-84.
http://dx.doi.org/10.1007/BF02879314
[43] Mundry, I.B. and Stützel, T. (2003) Morphogenesis of Male Sporangiophores of Zamia amblyphyllidia D.W. Stev. Plant Biology, 5, 297-310.
http://dx.doi.org/10.1055/s-2003-40791

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