Leaf of Sagenopteris colpodes, from Taylor et al. (2006).

Belongs within: Spermatophyta.
Contains: Angiospermae.

The Pan-Angiospermae are the total clade of angiosperms, including flowering plants and all fossil taxa more closely related to them than any other modern plant lineage.

The origins of flowers
Published 4 July 2008
Reconstruction of the bennettitalean Williamsonia, a potential stem-angiosperm, from Turbo Squid.

The origin of the angiosperms (flowering plants) has long been considered one of the great unsolved questions of biology, and I must confess to having occassionally slipped into the hyperbole myself. However, we actually have some much better ground to stand on than the hyperbole might suggest.

First off, we need to ask what exactly makes flowering plants so distinct? What do they have that no other plant has? I bet some of you are fighting the urge to reply with, “They have flowers. Duh.” To which I have to reply—wrong! After all, you could debate to what extent the reproductive structures of many flowering plants can really be called ‘flowers’. Many flowering plants lack the petals and/or sepals of more classic flowers. They may have bracts (coloured leaves) instead, like poinsettias or bougainvilleas, while many wind-pollinated angiosperms simply do without ornamentation entirely. And if we argue that petals are not necessary to count as a flower—if those plants that surround their reproductive structures with bracts also count as having flowers—then flowers are not actually unique to angiosperms (as I’ll explain in a minute). No, the really significant feature of angiosperms is the carpel, the protective covering of two integuments that encloses the ovule of angiosperms. In other living seed plants, the gymnosperms, the ovules generally have only one integument and are produced exposed on the ends of short branches, often surrounded by a protective whorl of leaves or leaf-derived structures to form a structure called a strobilus (in many conifer groups, these protective leaves have become hard and woody to form the scales of a cone with an ovule at the base of each scale). Morphological and molecular phylogenetic analyses disagree significantly about the relationships between angiosperms and living gymnosperms (Friedman & Floyd 2001). Morphological analyses place angiosperms nested within gymnosperms, forming a clade with the Gnetales, while molecular analyses place the angiosperms as sister to all living gymnosperms, not closely related to Gnetales.

While there is a significant divide between the carpel-enclosed ovules of angiosperms and the exposed ovules of gymnosperms in living taxa, this divide (unsurprisingly) actually dwindles when we consider fossil taxa. Debate still rages about which fossil taxa are the closest relatives of angiosperms, but two taxa that pop up on a regular basis are the Bennettitales and Caytonia. These taxa are often closely related to angiosperms and the Gnetales in morphological analyses (Doyle 1998), while if morphological analyses are constrained to match the molecular trees the angiosperms form a clade with Bennettitales, Caytonia and glossopterids (Doyle 2006). The Bennettitales and Caytonia both put in an appearance during the Triassic and survived until the end of the Cretaceous, while angiosperms are first known from the early Cretaceous (Doyle 1998). Caytonia is generally described as a “seed fern”, which were usually trees, but articulated fossils are fairly rare. It produced multiple single-integument ovules reflexed and contained within a protective structure called a cupule. It does not take a significant leap to imagine the reduction to a single ovule per cupule and the cupule developing into the outer integument of the angiosperm carpel.

(From Frohlich & Chase 2007) Reproductive structures of fossil stem-angiosperm candidates. a, Glossopteris showing cupules borne on stalk above a leaf. b, Caytonia male (above) and female (below) reproductive units. c, Caytonia cupule. d, Corystosperm (Umkomasia) cupule containing one ovule. Cupule wall almost surrounds ovule, except for a slit facing the stalk. e, Bennettitales (Williamsoniella) bisexual reproductive unit; each oval pollen sac consists of several fused microsporangia. Ovules are borne among scales on the central stalk; in Vardekloftia each is enclosed by a cupule wall. Green, cupule wall; red, ovule; yellow, pollen organ.

Bennettitales were plants fairly similar in appearance to modern cycads that lacked any such carpel-like arrangement and had ovules born along scales in the strobilus. What Bennettitales did have, however, were flowers (of a sort). The leaves of the strobilus were expanded into flower-like bracts that were quite large (and possibly quite colourful) in a number of taxa. Certain features of the bennettitalean bracts suggest that they had a role in attracting insect pollinators, just as modern flowers do today (Gottsberger 1988). The largest bennettitalean “flowers” were found in Cycadeoidea, which had the bracts recurved to enclose a central chamber containing the reproductive organs. This is of great significance because similar arrangements are found in modern beetle-pollinated flowers, which are believed to be among the more basal flower forms. Also significant is the presence in bennettitalean fossils of the chemical oleanane, derived from a secondary metabolite that is only produced by angiosperms among living taxa, further supporting their relationship (Taylor et al. 2006).

The earliest major pollinators of flowers were probably beetles and flies (Kevan & Baker 1983). Beetles in particular are the major pollinators of members of basal angiosperm orders such as Magnoliales and Nymphaeales. The two insect groups most commonly associated with pollination in most peoples minds, butterflies and bees, were unlikely to have been significant players in the origin of flowers for the simple reason that neither had come into existence yet—Lepidoptera as a whole only started making an appearance during the Cretaceous, while bees were not to appear until the Tertiary. As already noted, many of the basal angiosperm groups show adaptations towards beetle pollination (this is why magnolias, for instance, produce such a powerful perfume and white flowers—nocturnal beetles use smell more in finding food, while white stands out more at night than colour would). Many beetle-pollinated flowers have some sort of enclosed chamber, or close during the day, providing their pollinators with a safe haven from predators as well as providing food in the form of nectar or pollen (it is quite alright if the pollinator eats some of the pollen so long as the flower produces far more than the pollinator can eat – indeed, if the pollinator is actually going for the pollen then it will almost certainly be rooting around in it and getting covered with it), and this may have been the approach Cyacadeoidea was going for. On the other hand, another basal angiosperm family, the Winteraceae, has open and unspecialised flowers that attract a wide range of pollinators such as beetles, moths, flies and thrips.

Arabidopsis with induced mutation causing leaves to be partially converted into petals, from University of California, San Diego.

Insect-attracting strobili such as found in Bennettitales could have quite easily given rise to the first flowers. Developmental genetics has confirmed the theory put forward many years previously that petals and sepals represent modified leaves, and by affecting the expression of the genes involved it has proved possible to make leaves grow instead of petals, and petals grow instead of leaves (Goto et al. 2001). So while we have still not entirely solved what Darwin so overquotedly referred to as the “abominable mystery”, the answer has drawn tantalisingly close.

Systematics of Pan-Angiospermae
<==Pan-Angiospermae [Magnoliophyta]CD07
    |    |--AngiospermaeFC07
    |    `--Archaefructus [Archaefructaceae]SJ02
    |         |--*A. liaoningensisSJ02
    |         |--A. eofloraSD11
    |         `--A. sinensis Sun, Ji et al. 2002SJ02
    |--Czekanowskiaceae [Czekanowskiales, Iraniales, Leptostrobaceae, Leptostrobales]RL09
    |    |--Czekanowskia rigida Heer 1876C93
    |    |--IxostrobusRL09
    |    |--Solenites vimineusRL09
    |    |--Irania hermaphroditica Schweitzer 1977C93
    |    |--Phoenicopsis sttenstrupiiC93
    |    `--LeptostrobusFC07
    |         |--L. cancerRL09
    |         |--L. laxiflorus Heer 1876C93
    |         `--L. longus Harris 1935C93
    `--Caytoniaceae [Caytoniales]RL09
         |--Mexiglossa varis Delevoryas & Person 1975C93
         |--Perezlaria oaxacensis Delevoryas & Gould 1971C93
         |--Pramelreuthia halberfelneri Krasser 1909C93
         |    |--C. nathorstii (Thomas) Harris 1940C93
         |    `--C. sewardiRL09
         |    |--C. arberiRL09
         |    `--C. kochii Harris 1932C93
         |    |--A. ellipticum Harris 1932C93
         |    |--A. major Harris 1932C93
         |    `--A. rotundum Harris 1932C93
         |    |--S. colpodesRL09
         |    |--S. halleiC93
         |    |--S. rhoifoliaF71
         |    |--S. salisburoidesR87
         |    `--S. variabilisC93

*Type species of generic name indicated


[CD07] Cantino, P. D., J. A. Doyle, S. W. Graham, W. S. Judd, R. G. Olmstead, D. E. Soltis, P. S. Soltis & M. J. Donoghue. 2007. Towards a phylogenetic nomenclature of Tracheophyta. Taxon 56 (3): E1–E44.

[C93] Cleal, C. J. 1993. Gymnospermophyta. In: Benton, M. J. (ed.) The Fossil Record 2 pp. 795–808. Chapman & Hall: London.

Doyle, J. A. 1998. Molecules, morphology, fossils, and the relationship of angiosperms and Gnetales. Molecular Phylogenetics and Evolution 9 (3): 448–462.

Doyle, J. A. 2006. Seed ferns and the origin of angiosperms. Journal of the Torrey Botanical Society 133 (1): 169–209.

[F71] Fletcher, H. O. 1971. Catalogue of type specimens of fossils in the Australian Museum, Sydney. Australian Museum Memoir 13: 1–167.

Friedman, W. E., & S. K. Floyd. 2001. Perspective: The origin of flowering plants and their reproductive biology—a tale of two phylogenies. Evolution 55(2): 217–231.

[FC07] Friis, E. M., P. R. Crane, K. R. Pedersen, S. Bengtson, P. C. J. Donoghue, G. W. Grimm & M. Stampanoni. 2007. Phase-contrast X-ray microtomography links Cretaceous seed with Gnetales and Bennettitales. Nature 450: 549–552.

Frohlich, M. W., & M. W. Chase. 2007. After a dozen years of progress the origin of angiosperms is still a great mystery. Nature 450: 1184–1189.

[G10] Gordenko, N. V. 2010. Vladimariales ordo nov. (Gymnospermae) from the Middle Jurassic deposits of the Mikhailovskii rudnik locality (Kursk Region, European Russia). Paleontological Journal 44 (10): 1281–1307.

Goto, K., J. Kyozuka & J. L. Bowman. 2001. Turning floral organs into leaves, leaves into floral organs. Current Opinion in Genetics and Development 11 (4): 449–456.

Gottsberger, G. 1988. The reproductive biology of primitive angiosperms. Taxon 37 (3): 630–643.

Kevan, P. G., & H. G. Baker. 1983. Insects as flower visitors and pollinators. Annual Review of Entomology 28: 407–453.

[R87] Ratte, F. 1887. Notes on Australian fossils. Proceedings of the Linnean Society of New South Wales, series 2, 1 (4): 1065–1084, pls 15–17.

[RL09] Ren, D., C. C. Labandeira, J. A. Santiago-Blay, A. Rasnitsyn, C. Shih, A. Bashkuev, M. A. V. Logan, C. L. Hotton & D. Dilcher. 2009. A probable pollination mode before angiosperms: Eurasian, long-proboscid scorpionflies. Science 326: 840–847.

[SD11] Sun, G., D. L. Dilcher, H. Wang & Z. Chen. 2011. A eudicot from the Early Cretaceous of China. Nature 471: 625–628.

[SJ02] Sun, G., Q. Ji, D. L. Dilcher, S. Zheng, K. C. Nixon & X. Wang. 2002. Archaefructaceae, a new basal angiosperm family. Science 296: 899–904.

Taylor, D. W., H. Li, J. Dahl, F. J. Fago, D. Zinniker & J. M. Moldowan. 2003. Biogeochemical evidence for the presence of the angiosperm molecular fossil oleanane in Paleozoic and Mesozoic non-angiospermous fossils. Paleobiology 32: 179–190.

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