Phylogeny and Evolution of Vascular Plants

Abstract

Vascular plants play a major role in global carbon cycling and are of fundamental importance to life on earth. Over the last half‐century, phylogenetic studies of morphological and molecular data have brought tremendous progress in our understanding of origin, phylogeny and evolution of these plants. It is clear that they evolved from a bryophytic ancestor, which likely resembles hornworts in the modern earth flora. Among all living vascular plants, lycophytes represent the first diverging lineage. Ferns and other free‐sporing vascular plants make up a clade called monilophytes, which are sister to seed plants. Extant gymnosperms form a monophyletic group in most molecular studies, but this result may need further investigation as morphological support is lacking. Among living angiosperms, , Nymphaeales and Austrobaileyales have been unequivocally demonstrated to represent the oldest lineages, a result that will facilitate solving Darwin's abominable mystery – the origin of angiosperms.

Key Concepts

  • Origin of vascular plants: Current phylogenetic and fossil evidence tends to support bryophytes as a paraphyletic group and thus vascular plants originated from a bryophytic ancestor.
  • Phylogeny and evolution of life cycle in land plants: The bryophytic origin of vascular plants supports antithetic theory: The multicellular diploid sporophyte generation in land plants was an interpolation of a new structure derived from delay of meiosis in the life cycle, and continuously increased as plants evolved, eventually outweighing the haploid gametophyte generation.
  • Relationships among early vascular plants: The long‐standing issue of how several relictual vascular plant lineages are related to each other have been finally resolved, with lycophytes representing the oldest living member of vascular plants and Equisetum being sister to a group composed of Psilotaceae and eusporangiate and leptosporangiate ferns.
  • Monilophytes and origin of seed plants: Among extant free‐sporing vascular plants, Equisetum, Psilotaceae and ferns together make up a monophyletic group called monilophytes, which is sister to seed plants.
  • The first angiosperms: Among all living angiosperms, Amborella, a shrub from New Caledonia, and Nymphaeales represent the basalmost lineages and they could offer some clues to what the first angiosperms looked like.
  • Phylogenomics and phylogeny: The colossal amount of information that is being unearthed from genomes is enabling a new quantum leap in phylogenetics and evolutionary biology, but the data need to be carefully and rigorously analysed so that the results are not simply trees with high statistical support, and instead can withstand repeated falsification tests.

Keywords: angiosperms; eudicots; evolution; hornworts; monilophytes; origin; phylogeny; phylogenomics; rosids; vascular plants

Figure 1. A consensus phylogeny of vascular plants and their outgroup. Relationships that are still controversial are indicated with red lines, and those that are unresolved are shown by polytomies. Acronym: COM – Celastrales, Oxalidales and Malpighiales.
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References

Arber EAN and Parkin J (1908) Studies on the evolution of the angiosperm. The relationship of the angiosperms to the Gnetales. Annals of Botany 22: 489–515.

Barkman TJ, Chenery G, McNeal JR, et al. (2000) Independent and combined analyses of sequences from all three genomic compartments converge on the root of flowering plant phylogeny. Proceedings of the National Academy of Sciences of the United States of America 97: 13166–13171.

Bierhorst DW (1971) Morphology of Vascular Plants. New York, NY: The Macmillan Company.

Bowe LM, Coat G and dePamphilis CW (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 of the United States of America 97: 4092–4097.

Bower FO (1908) The Origin of A Land Flora: A Theory Based upon the Facts of Alternation. London: MacMillan and Co., Ltd.

Čelakovsky L (1874) Ueber die verschiedenen Formen und die Bedeutung des Generationwechsels der Pflanzen. Sitzungsberichte der koeniglichen Boehmischen Gesellschaft der Wissenschaften in Prag 2: 21–61.

Chang Y and Graham SW (2011) Inferring the higher‐order phylogeny of mosses (Bryophyta) and relatives using a large, multigene plastid data set. American Journal of Botany 98: 839–849.

Chase MW, Soltis DE, Olmstead RG, et al. (1993) Phylogenetics of seed plants ‐ an analysis of nucleotide sequences from the plastid gene rbcL. Annals of the Missouri Botanical Garden 80: 528–580.

Chaw SM, Parkinson CL, Cheng YC, Vincent TM and Palmer JD (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 of the United States of America 97: 4086–4091.

Crane PR (1985) Phylogenetic analysis of seed plants and the origin of angiosperms. Annals of the Missouri Botanical Garden 72: 716–793.

Dahlgren R and Bremer K (1985) Major clades of the angiosperms. Cladistics 1: 349–368.

Donoghue MJ and Doyle JA (1989) Phylogenetic analysis of angiosperms and the relationships of Hamamelidae. In: Crane PR and Blackmore S (eds) Evolution, Systematics, and Fossil History of the Hamamelidae, vol. 1, pp. 17–45. Oxford: Clarendon Press.

Doyle JA and Donoghue MJ (1986) Seed plant phylogeny and the origin of angiosperms ‐ an experimental cladistic approach. Botanical Review 52: 321–431.

Doyle JA (2006) Seed ferns and the origin of angiosperms. Journal of Torrey Botanical Society 133: 169–209.

Edwards D, Davies KL and Axe L (1992) A vascular conducting strand in the early land plant Cooksonia. Nature 357: 683–685.

Endress PK and Matthews ML (2006) First steps towards a floral structural characterization of the major rosids. Plant Systematics and Evolution 260: 223–251.

Friis EM, Crane PR and Pedersen KR (2011) Eary Flowers and Angiosperm Evolution. Cambridge: Cambridge University Press.

Fritsch FE (1945) Studies in the comparative morphology of the algae. IV. algae and archegoniate plants. Annals of Botany 9: 1–29.

Gifford EM and Foster AS (1989) Morphology and Evolution of Vascular Plants, 3rd edn. New York: W. H. Freeman and Company.

Goremykin V, Bobrova V, Pahnke J, et al. (1996) Noncoding sequences from the slowly evolving chloroplast inverted repeat in addition to rbcL data do not support Gnetalean affinities of angiosperms. Molecular Biology and Evolution 13: 383–396.

Graham SW and Olmstead RG (2000) Utility of 17 chloroplast genes for inferring the phylogeny of the basal angiosperms. The American Journal of Botany 87: 1712–1730.

Gray J (1993) Major Paleozoic land plant evolutionary bio‐events. Palaeogeography Palaeoclimatology Palaeoecology 104: 153–169.

Heath TA, Hedtke SM and Hillis DM (2008) Taxon sampling and the accuracy of phylogenetic analyses. Journal of Systematics and Evolution 46: 239–257.

Kelch DG, Driskell A and Mishler BD (2004) Inferring phylogeny using genomic characters: a case study using land plant plastomes. In: Goffinet B, Hollowell V and Magill R (eds) Molecular Systematics of Bryophytes, pp. 3–11. St. Louis: Missouri Botanical Garden Press.

Kenrick P and Crane PR (1997a) The Origin and Early Diversification of Land Plants: A Cladistic Study. Washington, D. C.: Smithsonian Institution Press.

Kenrick P and Crane PR (1997b) The origin and early evolution of plants on land. Nature 389: 33–39.

Knie N, Fischer S, Grewe F, Polsakiewicz M and Knoop V (2015) Horsetails are the sister group to all other monilophytes and Marattiales are sister to leptosporangiate ferns. Molecular Phylogentics and Evolution 90: 140–149.

Linnaeus C (1751) Philosophia Botanica. Stockholmiae: apud Godofr. Kiesewetter.

Liu Y, Cox CJ, Wang W and Goffinet B (2014) Mitochondrial phylogenomics of early land plants: mitigating the effects of saturation, compositional heterogeneity, and codon‐usage bias. Systematic Biology 63: 862–878.

Loconte H and Stevenson DW (1990) Cladistics of Spermatophyta. Brittonia 42: 197–211.

Lu J‐M, Zhang N, Du X‐Y, Wen J and Li D‐Z (2015) Chloroplast phylogenomics resolves key relationships in ferns. Journal of Systematics and Evolution 53: 448–457.

Manhart JR (1995) Chloroplast 16S rDNA sequences and phylogenetic relationships of fern allies and ferns. American Fern Journal 85: 182–192.

Mathews S and Donoghue MJ (1999) The root of angiosperm phylogeny inferred from duplicate phytochrome genes. Science 286: 947–950.

Mathews S, Clements MD and Beilstein MA (2010) A duplicate gene rooting of seed plants and the phylogenetic position of flowering plants. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 365: 383–395.

Mishler BD and Churchill SP (1984) A cladistic approach to the phylogeny of the bryophytes. Brittonia 36: 406–424.

Moore MJ, Hassan N, Gitzendanner MA, et al. (2011) Phylogenetic analysis of the plastid inverted repeat for 244 species: insights into deeper‐level angiosperm relationships from a long, slowly evolving sequence region. International Journal of Plant Sciences 172: 541–558.

Naylor GJP and Brown WM (1997) Structural biology and phylogenetic estimation. Nature 388: 527–528.

Nickrent DL, Parkinson CL, Palmer JD and Duff RJ (2000) Multigene phylogeny of land plants with special reference to bryophytes and the earliest land plants. Molecular Biology and Evolution 17: 1885–1895.

Nishiyama T, Wolf PG, Kugita M, et al. (2004) Chloroplast phylogeny indicates that bryophytes are monophyletic. Molecular Biology and Evolution 21: 1813–1819.

Nixon KC, Crepet WL, Stevenson D and Friis EM (1994) A reevaluation of seed plant phylogeny. Annals of the Missouri Botanical Garden 81: 484–533.

Philippe H, de Vienne DM, Ranwez V, et al. (2017) Pitfalls in supermatrix phylogenomics. European Journal of Taxonomy 283: 1–25.

Popper K (2002) The Logic of Scientific Discovery. London & New York: Routledge Classics.

Pryer KM, Smith AR and Skog JE (1995) Phylogenetic relationships of extant ferns based on evidence from morphology and rbcL sequences. American Fern Journal 85: 205–282.

Pryer KM, Schneider H, Smith AR, et al. (2001) Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409: 618–622.

Puttick MN, Morris JL, Williams TA, et al. (2018) The Interrelationships of land plants and the nature of the ancestral embryophyte. Current Biology 28: 733–745.

Qiu Y‐L, Lee JH, Bernasconi‐Quadroni F, et al. (1999) The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402: 404–407.

Qiu Y‐L, Li LB, Wang B, et al. (2006) The deepest divergences in land plants inferred from phylogenomic evidence. Proceedings of the National Academy of Sciences of the United States of America 103: 15511–15516.

Qiu Y‐L, Li L, Wang B, et al. (2010) Angiosperm phylogeny inferred from sequences of four mitochondrial genes. Journal of Systematics and Evolution 48: 391–425.

Qiu Y‐L, Taylor AB and McManus HA (2012) Evolution of the life cycle in land plants. Journal of Systematics and Evolution 50: 171–194.

Raubeson LA and Jansen RK (1992) Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants. Science 255: 1697–1699.

Renzaglia KS, Duff RJ, Nickrent DL and Garbary DJ (2000) Vegetative and reproductive innovations of early land plants: implications for a unified phylogeny. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 355: 769–793.

Rothfels CJ, Li FW, Sigel EM, et al. (2015) The evolutionary history of ferns inferred from 25 low‐copy nuclear genes. American Journal of Botany 102: 1089–1107.

Rothwell GW and Serbet R (1994) Lignophyte phylogeny and the evolution of spermatophytes ‐ a numerical cladistic analysis. Systematic Botany 19: 443–482.

Rothwell GW (1999) Fossils and ferns in the resolution of land plant phylogeny. Botanical Review 65: 188–218.

Rydin C and Friis EM (2010) A new Early Cretaceous relative of Gnetales: Siphonospermum simplex gen. et sp. nov. from the Yixian Formation of Northeast China. BMC Evolutionary Biology 10: 183.

Saarela JM, Rai HS, Doyle JA, et al. (2007) Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree. Nature 446: 312–315.

Shen H, Jin D‐M, Shu J‐P, et al. (2018) Large‐scale phylogenomic analysis resolves a backbone phylogeny in ferns. Gigascience 7: 1–11.

Soltis PS, Soltis DE and Chase MW (1999) Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402: 402–404.

Soltis DE, Smith SA, Cellinese N, et al. (2011) Angiosperm phylogeny: 17 genes, 640 taxa. American Journal of Botany 98: 704–730.

Stevenson DW and Loconte H (1996) Ordinal and familial relationships of pteridophyte genera. In: Camus JM, Gibby M and Johns RJ (eds) Pteridology in Perspective: Proceedings of the Holttum Memorial Pteridophyte Symposium, Kew 1995, pp. 435–467. Kew: Royal Botanic Garedens.

Stewart WN (1983) Paleobotany and the Evolution of Plants. Cambridge: Cambridge University Press.

Strother PK, Al‐Hajri S and Traverse A (1996) New evidence for land plants from the lower Middle Ordovician of Saudi Arabia. Geology 24: 55–58.

Swofford DL, Olsen OJ, Waddell PJ and Hillis DM (1996) Phylogenetic inference. In: Hillis DM, Moritz C and Mable BK (eds) Molecular Systematics, 2nd edn, pp. 407–514. Sunderland, MA: Sinauer.

Taylor WA, Strother PK, Vecoli M and Al‐Hajri S (2017) Wall ultrastructure of the oldest embryophytic spores: Implications for early land plant evolution. Revue de Micropaleontologie 60: 281–288.

Walker JW and Doyle JA (1975) The bases of angiosperm phylogeny: palynology. Annals of the Missouri Botanical Garden 62: 664–723.

Wellman CH, Osterloff PL and Mohiuddin U (2003) Fragments of the earliest land plants. Nature 425: 282–285.

Wickett NJ, Mirarab S, Nguyen N, et al. (2014) Proceedings of the National Academy of Sciences of United States of America: E4859–E4868 (published online).

Wodehouse RP (1935) Pollen Grains: their Structure, Identification and Significance in Science and Medicine. New York: McGraw‐Hill Book Co., Inc.

Zeng L, Zhang Q, Sun R, et al. (2014) Resolution of deep angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times. Nature Communications 5: 4956.

Further Reading

Crum H (2001) Structural Diversity of Bryophytes. Ann Arbor, MI: The University of Michigan Herbarium.

Felsenstein J (2004) Inferring Phylogenies. Sunderland, Massachusetts: Sinauer.

Gensel PG and Edwards D (2001) Editors. Plants Invade the Land: Evolutionary & Environmental Perspectives. New York: Columbia University Press.

Kramer KU and Green PS (1990) Editors. The Families and Genera of Vascular Plants, vol. I. Springer‐Verlag, Berlin: Pteridophytes and Gymnosperms.

Kumar S, Stecher G and Tamura K (2016) MEGA7: molecular evolutionary genetic analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874.

Stevens, P. F. (2017) Angiosperm Phylogeny Website. Version 14, http://www.mobot.org/MOBOT/research/APweb/.

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Qiu, Yin‐Long(Nov 2018) Phylogeny and Evolution of Vascular Plants. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0027471]