Skip to main content
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2000 Jun 29;355(1398):769–793. doi: 10.1098/rstb.2000.0615

Vegetative and reproductive innovations of early land plants: implications for a unified phylogeny.

K S Renzaglia 1, Duff RJT 1, D L Nickrent 1, D J Garbary 1
PMCID: PMC1692784  PMID: 10905609

Abstract

As the oldest extant lineages of land plants, bryophytes provide a living laboratory in which to evaluate morphological adaptations associated with early land existence. In this paper we examine reproductive and structural innovations in the gametophyte and sporophyte generations of hornworts, liverworts, mosses and basal pteridophytes. Reproductive features relating to spermatogenesis and the architecture of motile male gametes are overviewed and evaluated from an evolutionary perspective. Phylogenetic analyses of a data set derived from spermatogenesis and one derived from comprehensive morphogenetic data are compared with a molecular analysis of nuclear and mitochondrial small subunit rDNA sequences. Although relatively small because of a reliance on water for sexual reproduction, gametophytes of bryophytes are the most elaborate of those produced by any land plant. Phenotypic variability in gametophytic habit ranges from leafy to thalloid forms with the greatest diversity exhibited by hepatics. Appendages, including leaves, slime papillae and hairs, predominate in liverworts and mosses, while hornwort gametophytes are strictly thalloid with no organized external structures. Internalization of reproductive and vegetative structures within mucilage-filled spaces is an adaptive strategy exhibited by hornworts. The formative stages of gametangial development are similar in the three bryophyte groups, with the exception that in mosses apical growth is intercalated into early organogenesis, a feature echoed in moss sporophyte ontogeny. A monosporangiate, unbranched sporophyte typifies bryophytes, but developmental and structural innovations suggest the three bryophyte groups diverged prior to elaboration of this generation. Sporophyte morphogenesis in hornworts involves non-synchronized sporogenesis and the continued elongation of the single sporangium, features unique among archegoniates. In hepatics, elongation of the sporophyte seta and archegoniophore is rapid and requires instantaneous wall expandability and hydrostatic support. Unicellular, spiralled elaters and capsule dehiscence through the formation of four regular valves are autapomorphies of liverworts. Sporophytic sophistications in the moss clade include conducting tissue, stomata, an assimilative layer and an elaborate peristome for extended spore dispersal. Characters such as stomata and conducting cells that are shared among sporophvtes of mosses, hornworts and pteridophytes are interpreted as parallelisms and not homologies. Our phylogenetic analysis of three different data sets is the most comprehensive to date and points to a single phylogenetic solution for the evolution of basal embryophytes. Hornworts are supported as the earliest divergent embryophyte clade with a moss/liverwort clade sister to tracheophytes. Among pteridophytes, lycophytes are monophyletic and an assemblage containing ferns, Equisetum and psilophytes is sister to seed plants. Congruence between morphological and molecular hypotheses indicates that these data sets are tracking the same phylogenetic signal and reinforces our phylogenetic conclusions. It appears that total evidence approaches are valuable in resolving ancient radiations such as those characterizing the evolution of early embryophytes. More information on land plant phylogeny can be found at: http: //www.science.siu.edu/ landplants/index.html.

Full Text

The Full Text of this article is available as a PDF (2.6 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Duff R. J., Nickrent D. L. Phylogenetic relationships of land plants using mitochondrial small-subunit rDNA sequences. Am J Bot. 1999 Mar;86(3):372–386. [PubMed] [Google Scholar]
  2. Hanson D. T., Swanson S., Graham L. E., Sharkey T. D. Evolutionary significance of isopreneemission from mosses. Am J Bot. 1999 May;86(5):634–639. [PubMed] [Google Scholar]
  3. Lewis L. A., Mishler B. D., Vilgalys R. Phylogenetic relationships of the liverworts (Hepaticae), a basal embryophyte lineage, inferred from nucleotide sequence data of the chloroplast gene rbcL. Mol Phylogenet Evol. 1997 Jun;7(3):377–393. doi: 10.1006/mpev.1996.0395. [DOI] [PubMed] [Google Scholar]
  4. Malek O., Lättig K., Hiesel R., Brennicke A., Knoop V. RNA editing in bryophytes and a molecular phylogeny of land plants. EMBO J. 1996 Mar 15;15(6):1403–1411. [PMC free article] [PubMed] [Google Scholar]
  5. Manhart J. R. Phylogenetic analysis of green plant rbcL sequences. Mol Phylogenet Evol. 1994 Jun;3(2):114–127. doi: 10.1006/mpev.1994.1014. [DOI] [PubMed] [Google Scholar]
  6. Nishiyama T., Kato M. Molecular phylogenetic analysis among bryophytes and tracheophytes based on combined data of plastid coded genes and the 18S rRNA gene. Mol Biol Evol. 1999 Aug;16(8):1027–1036. doi: 10.1093/oxfordjournals.molbev.a026192. [DOI] [PubMed] [Google Scholar]
  7. Pirozynski K. A., Malloch D. W. The origin of land plants: a matter of mycotrophism. Biosystems. 1975 Mar;6(3):153–164. doi: 10.1016/0303-2647(75)90023-4. [DOI] [PubMed] [Google Scholar]
  8. Qiu Y. L., Cho Y., Cox J. C., Palmer J. D. The gain of three mitochondrial introns identifies liverworts as the earliest land plants. Nature. 1998 Aug 13;394(6694):671–674. doi: 10.1038/29286. [DOI] [PubMed] [Google Scholar]
  9. Qiu YL, Palmer JD. Phylogeny of early land plants: insights from genes and genomes. Trends Plant Sci. 1999 Jan;4(1):26–30. doi: 10.1016/s1360-1385(98)01361-2. [DOI] [PubMed] [Google Scholar]
  10. Soltis P. S., Soltis D. E., Wolf P. G., Nickrent D. L., Chaw S. M., Chapman R. L. The phylogeny of land plants inferred from 18S rDNA sequences: pushing the limits of rDNA signal? Mol Biol Evol. 1999 Dec;16(12):1774–1784. doi: 10.1093/oxfordjournals.molbev.a026089. [DOI] [PubMed] [Google Scholar]
  11. Steinhauser S., Beckert S., Capesius I., Malek O., Knoop V. Plant mitochondrial RNA editing. J Mol Evol. 1999 Mar;48(3):303–312. doi: 10.1007/pl00006473. [DOI] [PubMed] [Google Scholar]
  12. Vaughn K. C., Harper J. D. Microtubule-organizing centers and nucleating sites in land plants. Int Rev Cytol. 1998;181:75–149. doi: 10.1016/s0074-7696(08)60417-9. [DOI] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES