Lecture © Stefan Little
BIOL 606 Session, University of Alberta, March 21, 2001
The term plant defines members of what have been called 'green algae' and the embryophytes, or land plants (Kenrick and Crane, 1997). These members of the kingdom plantae share certain characters. They all possess the pigments chlorophylls a and b, xanthophylls and carotenoids, cellulose cell walls and the secondary compounds sporopollenin, cutin, lignin and suberin. They also produce starch as storage compound, display phragmoplast with cell plate formation during mitosis and have plasmodesmata as cell to cell connections. Plants are oogamous and have an 'alternation of generations, life cycle.
Plants all have an alternation of generation life cycle. This describes a life cycle that has a haploid phase (gametophyte) that produces gametes via mitosis. These gametes unite to form a diploid zygote that grows and develops into the diploid phase (sporophyte). The diploid sporophyte produces haploid spores via meiosis. These spores germinate, grow and develop into the haploid gametophyte phase. Land plants have developed three main syndromes, homospory, heterospory and the seed habit that modify this basic life cycle. In order to understand the evolution of angiosperm flowers, one must first understand the different patterns of reproduction that plants display.
Features of the homosporous and heterosporous habit are listed below for comparison and contrast.
·One size spore
·Exosporic gametophyte development
·Gametophytes produce both antheridia and archegonia
·H2O required for spore germination and fertilization
·Two types of sporangia
·Two sizes of spores
·Endosporic gametophyte development
·Separate megagameotphyes and microgametophytes
·H2O required for fertilization but not for spore germination or gameotphyte growth
The heterosporous habit is further elaborated upon by seed plants. The megasporangium is enclosed by integumentary tissue, and the megaspore develops into the megagametophyte within the megasporangium. This elaboration on the megasporangium and megagametophyte form the immature seed (ovule). The microgametophyte is now wind or insect dispersed, and germinates distally from the microspore wall (pollen). The seed habit further eliminates the need for water for fertilization through this transport of the pollen to the ovule micropyle for pollen tube growth and release of sperm to the egg.
Flowering plants (angiosperms) are seed plants that have their ovules enclosed by a carpel. The carpel is a leaf-like organ that has receptive tissue (stigma) for pollen germination. All the carpels in a flower, usually the center most set of floral parts, form the gynoecium. Extinct fossil taxa such as Caytonia and Lepidopteris have cupules that appear to approach angiospermy, but these taxa did not have pollination occur at the stigma, but rather at the micropyle. Pollination at the micropyle is the pollination feature of gymnosperms (naked seeded plants). Therefor the major reproductive innovation of the angiosperms is the presence of the fully enclosed carpel and the change from pollination at the stigma to pollination at the micropyle. The other major reproductive innovation of angiosperms is the reduction of the megagametophyte to only a few cells, with double fertilization, producing the zygote, and endosperm (nutritive tissue for the seed).
The concept of 'primitive' angiosperms began with assumptions on what are primitive characters for these plants, such as Bessey's dicta (Bessey, 1915). The plants that shared a lot of primitive features where considered to be a primitive group of plants, such as Ranales sensu Bessey (1915) or Magnoliids sensu Cronquist (1981). Late Cretaceous angiosperm fossils are often members of these 'primitive' groups, lending support to the idea that these angiosperms are in fact extant members of this early lineage. Some important features of primitive angiosperms: an apocarpous gynoecium, granular monocolpate pollen, a lack of vessels, numerous floral parts, large showy flowers, laminar stamens, and a shrub or tree habit.
Some early morphological cladistic analyses of the flowering plants agreed with the morphology based assumptions of what is a primitive angiosperm (Donoghue and Doyle, 1989). These analyses had the Magnoliales and the Laurales as first branching lineages in the angiosperm phylogeny.
More recent analyses using molecular characters found that these 'primitive' groups are not first branching groups (Doyle and Endress, 2000). A basal grade below the Magnoliales has been found in several analyses using different DNA regions. This grade has been called the ANITA grade, an acronym using the first letters of the names of these basal plant families, Amborellaceae, Nymphaeaceae, Illiciaceae, Trimeniaceae, Austrobaileyaceae.
The focal paper investigates the gynoecium characters in terms of the new phylogenetic hypothesis presented by this recent molecular work (Endress and Igersheim, 2000). Some ANITA have not had much or any previous work published on their detailed gynoecial anatomy, so the paper was also collecting basic data on some of these taxa. The gynoecium data is used in a comparative way in order to begin to infer evolutionary trends in gynoecium structure.
It was found that there is a lack of complete postgenital fusion among ANITA. The authors made four classes of angiospermy:
ANITA tend to have type I or type II angiospermy. Magnoliids tend to have Type III or IV with some occasional Type II. Carpels tend to be pronouncedly ascidiate in ANITA and correlated with Type I angiospermy. Magnoliids tend to have less ascidiate carpels.
The authors observed the presence of an extragynoecial compitum in the basal angiosperms. An extragynoecial compitum is a zone of secretion that allows pollen tubes to move between apocarpous carpels. This allows pollen tubes to be evenly distributed between carpels. This feature is found in every family in the basal angiosperm grade, except for Trimeniaceae that has unicarpellate flowers, and Cabombaceae that does not appear to have contiguous stigmas at the first (female) phase of anthesis.
Some other features of carpel structure were found to be less prominent in ANITA. Oil cells and mucilage cells at the stigmatic surface were observed in some ANITA, but it was not found too commonly. The Magnoliids often posses these cells throughout their tissues. The Authors observed a overall anatropous ovule position in ANITA, but Amborellaceae (the basal most family) has orthotropous ovules, as well as some other important families. Although not a obvious trend, the authors argue that anatropous ovules are the plesiomorphic state in angiosperms. The presence of a lobed inner integument was also seen in some ANITA, but not consistently, and this feature is found in some higher branching taxa as well.
Discussion touched on the theories of carpel evolution (i.e. is the carpel equivalent to an inrolled leaf?). There was also discussion on the fossil record and if it conflicts with the present hypothesis that ANITA represents basal angiosperms. Recent papers findings show many members of ANITA in the early Cretaceous, but also members of the Magnoliids and some extinct groups. The idea that earlier aged sites may yield angiosperms was brought up, and that present molecular studies can be predictive, with the potential for the fossils to be used as evidence for or against the projected 'primitive' or early angiosperms. It would be difficult to find appropriate specimens to test these molecular trees, due to many of these characters being rare or impossible to find in the fossil record. The best option would be to look for Jurassic and Cretaceous cherts that may preserve the cellular detail needed, while being of the right age to find early angiosperms.
Cronquist, A. 1981. An Integrated system of classification of flowering plants. Columbia University Press, New York.
Bessey, C.E. 1915. The Phylogenetic Taxonomy of Flowering Plants. Annals of the Missouri Botanical Gardens. 2:108-164
Donoghue, M.J., J.A. Doyle. 1989. Phylogenetic analysis of angiosperms and the relationships of Hamamelidae. Pages 17-45 in P.R. Crane, S. Blackmore, eds. Evolution, systematics, and fossil history of the Hamamelidae. Vol. 1. Claredon, Oxford.
Doyle, J.A and P.K. Endress. 2000. Morphological phylogenetic analysis of basal angiosperms: comparison and combination with molecular data. International Journal of Plant Sciences. 161(6 Suppl.) S121-S153.
Endress, P.K. and A. Ingersheim. 2000. Gynoecium structure and evolution in basal angiosperms. International Journal of Plant Sciences. 161(6 Suppl.): S211-S223.
Kenrick, P. and P.R. Crane. 1997. The origin and early diversification of land plants, and Cladistic study. Smithsonian Institution Press, Washington, U.S.A.
Renner, S.S. 1999. Circumscription and phylogeny of the Laurales: evidence from molecular and morphological data. American Journal of Botany. 86(9): 1301-1325