Original URL: http://www.inform.umd.edu/PBIO/pb250/orig.html

PBIO 250 Lecture Notes

James L. Reveal

Norton-Brown Herbarium, University of Maryland


Origin and Classification

duckweeds
(Lemnaceae), Wolffia
Sequoia and Sequoiadendron
Eucalyptus (Myrtaceae)
"abominable mystery"
Darwin to Hooker in 1879: "The rapid development as far as we can judge of all the higher plants withing recent geological times is an abominable mystery"
not simple yet
  1. Beck, C.B. (ed.). 1976. Origin and early evolution of angiosperms. New York.

Characters of flowering plants - see this review - available only from on-campus sites

  1. vessels in the xylem
  2. sieve-tube members and companion cells in the phloem
  3. embryo sac of eight nuclei (one egg, two synergids, three antipodal and two polar)
  4. "double fertilization" with a nuclear product
closed carpels
primitive angiosperms are often vesselless
all angiosperms have sieve-tube members and companion cells
many exceptions of embryo sac nuclei number
all angiosperms exhibit "double" fertilization, but not a feature unique to flowering plants
Ephedra
"double" fertilization results in the formation of triploid endosperm only in flowering plants
Calycanthus - embryos develop adventitiously from the nucellus, and endosperm development is autonomous and then degenerates.
the nutritive tissue is the endosperm
many primitive angiosperms have unsealed carpels
the carpel is a specialized megasporophyll that enclose the ovules
pollen germinates on a stigmatic surface in all angiosperms
sepals, petals, stamens and carpels arranged in a flower composed of often complex parts -- be sure to follow the links!
angiosperms are "loosely" monophyletic, evolving from the gymnosperms; the angiosperms are a "natural" group
flowers themselves evolved over time

Origin of flowering plants
geologic time scale
Triassic (248-180 mybp)
Jurassic (135-180 mybp)
Cretaceous (135 to 65 mybp)
Lower Cretaceous: Ryazanian (132-135); Valanginian (130-132); Hauterivian (127-130); Barrenian (125-127); Aptian (122-125); Albian (110-122)
Upper Cretaceous: Cenomanian (100-110); Turonian (90-100); Coniacian (85-90); Santonian (80-85); Campanian (70-80); Maestrichtian (65-70) Tertiary: Paleocene (54-65), Eocene (38-54), Oligocene (25-38), Miocene (7-25), Pliocene (2.5-7), Pleistocene (0.01-2.5), Holocene (last 10000 yr)
Breakthrough Made in Dating of the Geological Record by F. J. Hilgen, W. Krijgsman, C. G. Langereis, and L. J. Lourens

The definition of the major gymnospermous groups (see Paul Kenrick and Peter Crane), with modifications, as outlined by:
  1. Rothwell, G.W. & R. Serbet. 1994. Lignophyte phylogeny and the evolution of spermatophytes: A numerical cladistic analysis. Syst. Bot. 19: 443-482.
  2. Crane, P.R. & P. Kenrick. 1997. Problems in cladistic classification: Higher-level relationships in land plants. Aliso 15: 87-104.
Division: Pinophyta (gymnosperms)
a good review in German; check out both links, and this one in English
seed ferns
fossil recored of the cycads
Kentucky fossils including several examples of gymnosperms
Subdivisions: Archaeopteridophytina; Lyginopteridophytina; Cordaixylophytina; Pinophytina
Classes: Archaeopteridopsida (progymnosperms); Lyginopteridopsida (seed ferns); Cordaitopsida (cordaites); Cycadopsida (cycads); Ginkgoopsida (ginkgos); Pinopsida ["Coniferopsida"] (conifers); Bennettitopsida (cycadeoids); Gnetopsida (gnetops)
Selected orders: Lyginopteridales, Caytoniales, Glossopteridales, Pentoxylales, Bennettitales
monosulcate versus tricolpate pollen
Ceratophyllum
Degeneria, Drimys, Magnolia
Families: Winteraceae, Magnoliaceae, Chloranthaceae, Piperaceae, Nymphaeaceae, Butomaceae, Alismataceae
pre-Cretaceous origin of angiosperm proposed by some in the 1950s
  1. Axelrod, D.I. 1952. A theory of angiosperm evolution. Evolution 4: 29-60.
  2. --. 1970. Mesozoic paleogeography and early angiosperm history. Bot. Rev. 36: 277-319.
long period of "cryptic" evolution caused by the early angiosperms being plants of arid regions with a diminutive habit and fundamentally gymnospermous pollen (and vegetative?) features
most supported a early Cretaceous origin until 1980s
  1. Scott, R.A., S. Barghoorn & E.B. Leopold. 1960. How old are the angiosperms? Amer. J. Sci. 258A: 284-299.
pre-Cretaceous origin now confirmed
  1. Sun, G., D.L. Dilcher, S. Zheng & Z. Zhou. 1998. In search of the first flower: A Jurassic angiosperm, Archaefructus, from northeast China. Science 282: 1692-1695.
Archaefructus has helically arranged conduplicate carpels that form small follicles; elongated stigmatic crests are conspicuous on each carpel; each unit is subtended by leaf-like structures; possibly visited by flies, but like Ascarina (Chloranthaceae) the flowers may have been wind-pollinated
other suggested, recently published Jurassic angiosperms from China appear to be gnetalan rather than angiospermous according to Sun et al.

some suggest a multiple origin of angiosperms but Bennettitalian ancestory probable
  1. Crane, P.R. 1985. Phylogenetic analysis of seed plants and the origin of angiosperms. Ann. Missouri Bot. Gard. 72: 716-793.
  2. --. 1986. "The morphology and relationships of Bennettiales," pp. 163-175. In: R.A. Spicer & B.A. Thomas (eds.), Systematic and taxonomic approaches in palaeobotany. Oxford.
  3. -- & P. Kenrick. 1997. Problems in cladistic classification: Higher-level relationships in land plants. Aliso 15: 87-104.
  4. Crepet, W.L. 1979. Some aspects of the pollination biology of Middle Eocene angiosperms. Rev. Palaeobot. Palynol. 27: 213-238.
  5. Dilcher, D.L. 1979. Early angiosperm reproduction: An introductory report. Rev. Palaeobot. Palynol. 27: 291-328.
  6. Doyle, J.A. & M.J. Donoghue. 1986. Seed plant phylogeny and the origin of angiosperms: An experimental cladistic approach. Bot. Rev. (Lancaster) 52: 321-431.
  7. --, -- & E.A. Zimmer. 1994. Integration of morphological and ribosomal RNA data on the origin of angiosperms. Ann. Missouri Bot. Gard. 81: 419-450.
  8. -- & L.J. Hickey. 1976. "Pollen and leaves from the mid-Cretaceous Potomac Group and their bearing on early angiosperm evolution," pp. 139-206. In: C.B. Beck (ed.), Origin and early evolution of angiosperms. New York.
  9. Friis, E.M., W.G. Chaloner & P.R. Crane. 1987. The origin of angiosperms and their biological consequences. Cambridge.
  10. Hickey, L.J. & J.A. Doyle. 1977. Early Cretaceous fossil evidence for angiosperm evolution. Bot. Rev. 43: 2-104.
  11. Hughes, N.F. 1976. Palaeobiology of angiosperm origins. Cambridge.
  12. --. 1994. The enigma of angiosperms origins. Cambridge.
  13. Krassilov, V.A. 1991. The origin of angiosperms: New and old problems. Trends Ecol. Evol. 6: 215-220.
  14. Spicer, R.A. & B.A. Thomas (eds.). 1986. Systematic and taxonomic approaches in palaeobotany. Oxford.
  15. Stewart, W.N. & G.W. Rothwell. 1993. Paleobotany and the evolution of plants, ed. 2. Cambridge.
  16. Taylor, T.N. 1981. Paleobotany: An introduction to fossil plant biology. New York.
  17. -- & E.L. Taylor. 1993. The biology and evolution of fossil plants. Englewood Cliffs.
  18. Thomas, B.A. & R.A. Spicer. 1987. The evolution and palaeobiology of land plants. Sydney.
modern Gnetopsida sister-group to modern angiosperms
Sanmiguelia lewesii - palm-like leaves
Synangispadixis tidwellii - "staminate flower" an erect cluster of densely compact anthers
Axelrodia burgeri - "ovulate flower" with a whorl of three tepaloid segments subtended by a whorl of narrow leaf-like bracts with a single central pistil.
a primitive angiosperm with both monocot and dicot features, fide Cornet (1989)
  1. Brown, R.W. 1956. Palmlike plants from the Dolores Formation (Triassic), southwestern Colorado. U.S. Geol. Surv. Prof. Pap. 274H: 205-209.
  2. Cornet, B. 1986. The reproductive structures and leaf-venation of a Late Triassic angiosperm Sanmiguelia lewisii. Evol. Theory 7: 231-309.
  3. --. 1989. The reproductive morphology and biology of Sanmiguelia lewisii, and its bearing on angiosperm evolution in the Late Triassic. Evol. Trends Pl. 3: 25-51.
  4. Tidwell, W.D., A.D. Simper & G.F. Thayn. 1977. Additional information concerning the controversial Triassic plant: Sanmiguelia. Palaeontographica 163B: 143-151.
Rothwell & Serbet diagram the relationship among the higher gymnosperms and angiosperms as follows:
     Pentoxyl. Bennettit. Angiosp. Eph. Wel. Gnet.
        \        \          \       \    \   /
         \        \          \       \    \ /
        __\ _ _ _ _\ _ _ _ _ _\ _ _ _ \ _ _/

In more general terms, the overall relationship is like that given below in a figure from Auburn University


several fossil pollen genera may be angiospermous from the Late Triassic of Virginia (1989)
a dicot-like leaf and two putative angiosperm reproductive structures found in late Carnian of the late Triassic of North Carolina and Virginia

  1. Cornet, B. 1989. Late Triassic angiosperm-like pollen from the Richmond Rift Basin of Virginia, U.S.A. Palaeontographica 213B: 37-87.
  2. --. 1992. Angiosperm-like pollen flora of the ammonite-dated Oxfordian (Upper Jurassic) of France. Rev. Palaeo-bot. Palynol. 71: 269-294.
  3. --. 1992. Dicot-like leaf and flowers from the Late Triassic tropical Newark Supergroup rift zone, U.S.A. Mod. Geol. 19: 81-99.
  4. Crane, P.R. 1993. Time for the angiosperms. Nature 366: 631-632.
  5. --, M.J. Donoghue, J.A. Doyle & E.M. Fries. 1989. Angiosperm origin. Nature 342:131.
some evidence that Ephedra is closer to Gnetum , as traditionally believed, contrary to what is given in the above
  1. Osborn, J.M., T.N. Taylor and M.R. de Lima. 1993. The ultrastructure of fossil ephedroid pollen with gnetalean affinities from the Lower Cretaceous of Brazil. Rev. Palaeobot. Palynol. 77: 171-184.
molecular-clock calculations place origin in Triassic at about 230 mybp (Wolfe et al.); Carboniferous at about 300 mybp (Martin et al.)
  1. Martin, W., A. Gierl & H. Saedler. 1989. Molecular evidence for pre-Cretaceous angiosperm origin. Nature 339: 46-48.
  2. Wolfe, K.H., M. Gouy, Y.-W. Yang, P.M. Sharp & W.-H. Li. 1989. Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc. Natl. Acad. Sci. U.S.A. 86: 6201-6205.
recent studies suggest the first land plants arose some 450 mya; the ultimate angiosperm line diverged from the ultimate conifer line some 350 mya; monocots separated from dicots some 160 mya
  1. Chaw, S.-M., A. Zharkikh, H.-M. Sung, T.-C. Lau & W.-H. Li. 1997. Molecular phylogeny of gymnosperms and seed plant evolution: Analysis of 18S rRNA sequences. Molec. Biol. Evol. 14: 56-68.
  2. Goremykin, V.V., V.K. Bobrova, J. Pahnke, A.V. Troitsky, A.S. Antonov & W. Martin. 1996. Noncoding sequences from the slowly evolving chloroplast inverted repeat in addition to rbcL data do not support gnetalean affinities of angiosperms. Molec. Biol. Evol. 13: 383-306.
  3. --, S. Hansmann & W.F. Martin. 1997. Evolutionary analysis of 68 proteins encoded in six completely sequenced chloroplast genomes: Revised molecular estimates of two seed plant divergent times. Pl. Syst. Evol. 206: 337-351.
see articles in the first volume of Flora North America on flora of North America from the Cretaceous onward

br>Drimys winteri (Winteraceae), the basal angiosperm according to Cronquist

early angiosperm features: small woody plant with simple, entire, pinnately veined leaves with large, terminal and axillary solitary flowers on an elongated receptacle bearing a perianth of modified bracts, leaflike stamens bearing monosulcate pollen, and unsealed, conduplicate carpels (Cronquist)
early angiosperm features: small rhizomatous perennial herbs bearing broad simple, entire leaves with intermediate pinnate to palmate primary venation, the small flowers with diminutive reproductive organs arranged cymosely and subtended by a complex of numerous bracts, and spherical, reticulate, monosulcate pollen (Taylor & Hickey)

early true angiosperms had a condensed life cycle and a weedy nature arrayed in two types initially, a rare magnoliaceous, arborescent marginal forest dweller and a more common, and diverse piperoid herbaceous forest floor dweller; the latter adopted a shrubby habit that rapidly evolved in more arid regions, maintained a basic herbaceous aspect from which most subsequent angiosperms arose, and an aquatic habit characterized by significant reduction of structural complexity (Reveal)

"sneaky herbs among the feet of dinosaurs"
earliest flowers are most similar to Piperopsida

  1. Friis, E.M., P.R. Crane & K.R. Pedersen. 1986. Floral evidence for Cretaceous chloranthoid angiosperms. Nature 320: 163-164.
from the late Albian (Cretaceous) in Maryland
  1. Taylor, D.W. & L.J. Hickey. 1990. An Aptian plant with attached leaves and flowers: Implications for angiosperm origin. Science 247: 702-704.
from Australia
Clavatipollenites, a common fossil pollen is most similar to that found in Piperopsida
place of origin probably in northern Gondwana or what is now northern Africa and South America in an arid or semiarid region
  1. Archangelsky, S. & T.N. Taylor. 1993. The ultrastructure of in situ Clavatipollenites pollen from the Early Cretaceous of Patagonia. Amer. J. Bot. 80: 879-885.
  2. Doyle, J.A. 1984. Evolutionary, geographic, and ecological aspects of the rise of angiosperms. Proc. 27th Int. Geol. Congr., Palaeontol. 2: 23-33.
if first angiospermous plants were of arid regions then the group likely of shrubby perennials with small, simple, alternately arranged leaves, cymose inflorescences of small flowers composed of numerous undifferentiated tepals (bracts to petaloid filaments) supporting a single unsealed, conduplicate carpel and a whorl of few to many cyclic stamens on shortened filaments, and a leathery or hardened fruit.
the probable key to the differentiation of angiosperms from gymnosperms was the evolution of a bisexual flower (androecium and gynoecium on same flower); the trend of small flower continued in the Piperopsida but changed to larger flowers to advertise in a more crowded environment (e.g., forests) in the Magnoliopsida; the Nymphaeidae are a specialized aquatic group of Magnoliopsida, not paleoherbs (Piperopsida); the understory plants evolved rapidly in association with insects forming Ranunculopsida.
Three basal groups of angiosperms, the magnolioids (an evolutionary dead-end), the paleoherbs (from which the monocots arose), and the ranunculoids (from which the remaining groups of dicots evolved) all of these three mainly groups were basically "sneakers" existing under the fern and gymnosperm canopy, on top of the canopy, or on its very edge; only in arid regions were the members likely shrubby and more common, but it was the general development of drier conditions that stressed the ferns and gymnosperms to the point the angiosperms to successfully radiate and claim dominancy.
  1. Endress, P.K. 1990. Evolution of reproductive structures and functions in primitive angiosperms (Magnoliidae). Mem. New York Bot. Gard. 55: 5-34.
  2. --.1994. Floral structure and evolution of primitive angiosperms: Recent advances. Pl. Syst. Evol. 192: 79-97.
traditional view of early angiosperms: early flowers are mostly mid-Cretaceous and magnolioid in nature: Lesqueria, Archaeanthus, Prisca
  1. Crane, P.R. & D.L. Dilcher. 1984. Lesqueria: An early angiosperm fruiting axis from the mid-Cretaceous. Ann. Missouri Bot. Gard. 71: 384-402.
  2. Dilcher, D.L. & P.R. Crane. 1984. Archaeanthus: An early angiosperm from the Cenomanian of the western interior of North America. Ann. Missouri Bot. Gard. 71: 371-383.
  3. Drinnan, A.N., P.R. Crane, E.M. Friis & K.R. Pedersen. 1990. Lauraceous flowers from the Potomac Group (mid-Cretaceous) of eastern North America. Bot. Gaz. 151: 370-384.
  4. ----. 1991. Angiosperm flowers and tricolpate pollen of buxaceous affinity from the Potomac Group (mid-Cretaceous) of eastern North America. Amer. J. Bot. 78: 153-176.
  5. Labandeira, C.C., D.L. Dilcher, D.R. Davis & D.L. Wagner. 1994. Ninety-seven million years of angiosperm-insect association: Paleobiological insights into the meaning of coevolution. Proc. Natl. Acad. Sci., U.S.A. 91:12278-12282.
  6. Retallack, G.J. & D.L. Dilcher. 1981. Early angiosperm reproduction: Prisca reynoldsii, gen. et sp. nov. from mid-Cretaceous coastal deposits in Kansas, U.S.A. Palaeontographica 179B: 103-137.
diversification and adaptative radiation, able to exploit new habitats
  1. Retallack, G.J. & D.L. Dilcher. 1986. Cretaceous angiosperm invasion of North America. Cretaceous Rev. 7: 227-252.
Phylogenetic systems of classification
Jussieu, Candolle, Bentham and Hooker
Darwin
Engler and Prantl (works: 1887-1915)
amentiferous, Amentiferae
Betulaceae, Fagaceae, Juglandaceae
Cronquist
Bessey
ranalian school (1915)
cycadeoid ancestor with a bisexual strobli
dicta
Besseyan cactus (1914)
monophyletic
Hutchinson (work: 1926-1973)
herbaceous and woody groups
Cronquist and Takhtajan
Dahlgren and Thorne
Reveal additional subclasses now often recognized: Nymphaeidae, Piperidae, Ranunculidae, Nelumbonidae, Cornidae, Lamiidae and Triurididae
Aridae newly established for Acoraceae and Araceae
Cronquist: 83 orders and 388 families
Takhtajan: ca 166 orders and 533 families
Dahlgren: 111 orders and 479 families
Thorne: 74 orders and 437 families
Reveal: 202 orders and 551 families
superorder: all but Cronquist
monocots vs. dicots [REQUIRED READING]
monocot characters
    1. stems herbaceous; lack cambial ring
    2. vessels with scalariform pits in roots
    3. cuneate protein in sieve-tube plastids
    4. flowers trimerous
    5. perianth yellowish
    6. stamens basifixed
    7. anther wall monocot type
    8. pollen grain monosulcate
    9. ovules crassinucellate
    10. endosperm formation helobial
    11. linear embryo in endosperm
    12. embryo monocotyledonous
chicken versus egg: monocots or dicots
vesselless angiosperms
  1. Young, D. 1981. Are the angiosperms primitively vesselless? Syst. Bot. 6: 313-330.
Nymphaeales
William C. Burger (1932- )
  1. Burger, W.C. 1977. The Piperales and the monocots: Alternative hypotheses for the origin of monocotyledonous flowers. Bot. Rev. 43: 345-393.
  2. --. 1981. Heresy reviewed: The monocot theory of angiosperm origin. Evol. Theory 5: 189-225. two classes vs. five classes
    para-monophylletic
    alternative classification with five classes outlined according to the linear sequence of classes and superorders proposed by Reveal
    1. Reveal, J.L. 1994. New supraordinal names and recognition of five classes in Magnoliophyta. Phytologia 76: 1-7.
    Magnoliophyta Cronquist, Takht. & Zimmerm. ex Reveal, Phytologia 79: 70. 1996 (angiosperms)

    For the latest consensus tree for the flowering plants, see treezilla from Harvard University and TreeBase. For a modified presentation whereby family names are added, see this version of treezilla.

    Other Sites of Interest:

    Review of flower parts
    Review of floral morphology

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    Last revised: 8 Feb 1999