Class Magnoliopsida

The dicots, class Magnoliopsida, constitute a much larger group than the monocots and are divided into six subclasses: (1) Magnoliidae, (2) Hamamelidae, (3) Caryophyllidae, (4) Dilleniidae, (5) Rosidae, and (6) Asteridae (Fig. 1). They are more difficult to characterize than are the monocots because they are so diverse. Virtually every type of organ, tissue, and metabolism has several or many variations, resulting in hundreds of thousands of species of dicots. A simple description would be both inaccurate and misleading, so each subclass is described below in some detail.

FIGURE 1: Diagram of a widely accepted classification of the dicots, class Magnoliopsida

Subclass Magnoliidae. Subclass Magnoliidae is made up of those dicot species that (1) have relictual characters we associate with early angiosperms and (2) are apparently not related to more derived groups (Table 1). For example, family Magnoliaceae contains trees with wood similar to that of gymnosperms in that it lacks vessels, fibers, and axial parenchyma; magnolia flowers have many of each organ, and the numerous stamens and carpels are arranged in spirals as leaves usually are. The carpels are not fused together into a compound gynoecium. Another important feature is that their pollen grains have only a single germination pore: They are uniaperturate, as are monocots. More derived dicots have three germination pores (Fig. 2). Other members of the Magnoliidae are the laurels and avocado (Tauraceae), star anise (Illiciaceae), buttercups and anemones (Ranunculaceae), peperomias (Piperaceae), and water lilies (Nymphaeaceae in the order Nymphaeales, which may be related to the ancestors of monocots.

FIGURE 2:  (a) All early fossil pollen has only one aperture, but almost all living dicots with many derived features have three apertures. Therefore, uniaperturate pollen in living angiosperms, such as this Siphonoglossa, is considered a relictual feature. Other features of this genus are derived (X 300). (b) This pollen of Lophospermum has three germination pores; the pores are located in grooves, something that does not occur in any early fossil pollen (X 300). (a, courtesy of R. A. Hilsenbeck, Sul Ross State University; b, W. ]. Elisens, University of Oklahoma)

Several member groups are important medicinally: Papaveraceae (poppies) is the source of milky latex harvested for opium. Morphine, a strong analgesic (pain killer) that depresses the cerebral cortex, is extracted from opium, as is codeine. Chondodendron (Menispermaceae) produces curare, a drug that blocks nerve transmission and causes temporary paralysis; it is used in surgery to relax muscles without the need for deep anesthesia.

Subclass Magnoliidae is unusual in that some of its member families consist of woody tree species (Magnoliaceae, Degeneriaceae, Lauraceae), whereas others are aquatic or semi- aquatic herbs (Nymphaeaceae and many Ranunculaceae). Although the overall aspects of these two types of plant are so different that one would not immediately place magnolias and water lilies together, they have numerous anatomical, chemical, and reproductive similarities. Not long after dicots evolved from gymnosperms to a state somewhat like that of magnolias, they may have divided into two evolutionary lines, one adapting to marshy or aquatic habitats and becoming less woody and more herbaceous. This line may have resulted in water lilies and monocots. The other line would have remained terrestrial and woody, giving rise to the rest of the flowering plants.

Subclass Hamamelidae. Some of the more common members of the subclass Hamamelidae are the sycamores (Platanaceae); walnut, hickory, and pecan (Juglandaceae); oak, chestnut, and beech (Fagaceae); marijuana and hops (Cannabaceae); alders and birches (Betulaceae); and stinging nettles (Urticaceae) (3; Table 2). Subclass Hamamelidae consists of an evolutionary line of plants that began to differentiate about 120 million years ago, during the Lower Cretaceous Period, in areas that had alternating wet and dry seasons. In adapting to such a climate, they became deciduous, their leaves abscising each autumn, as opposed to remaining evergreen like members of subclass Magnoliidae. They produce flowers early in spring, before their new leaves expand, so the flowers are exposed to wind; it has been possible for these species to revert to wind pollination. This combination of characters permitted them to migrate out of the tropics into drier, colder temperate regions. At that time, temperate regions were sparsely populated and the members of Hamamelidae expanded their range and diversified rapidly, dominating the regions. However, by the Upper Cretaceous Period, about 80 million years ago, insect-pollinated members of subclasses Rosidae and Dilleniidae began to adapt to temperate climates and to outcompete the Hamamelidae, causing a decline in their timbers and diversity. As insects and Rosidae continue to co-evolve, the Hamamelidae may become even more restricted.

FIGURE 3: American sycamore (Platanus occidentalis) is a member of the Hamamelidae, a wind-pollinated tree. (L. Lefever from Grant Heilman)

At present, Hamamelidae contains 11 orders, 24 families, and about 3400 species. Many of the families are small and well defined, quite distinct from other families; such characters lead us to suspect that the families are old and relictual, having originated and diversified early. They are not changing rapidly now and are not producing many new species. A large number of species, especially in the orders Fagales, Hamamelidales, and Juglandales, consist of large woody trees, similar to those of Magnoliidae. Only in the order Urticales has there been a marked evolutionary trend toward herbaceousness.

Subclass Caryophyllidae. Examples of Caryophyllidae are pokeweed (Phytolaccaceae), cacti (Cactaceae), iceplant (Aizoaceae), sorel and buckwheat (Polygonaceae), portulaca (Portulacaceae), bougainvillea and four-o'clocks (Nyctaginaceae), spinach, beets, and Rus­sian thistle (Chenopodiaceae), and carnations and chickweed (Caryophyllaceae) (Table 3). The order Caryophyllales, containing 14 families, is held together strongly by many derived characters, but one is especially important. Whereas other flowering plants have anthocyanin pigments in their flowers, almost all Caryophyllales instead produce a group of water-soluble pigments called betalains (Fig. 4). The ancestral group may have lacked petals in their flowers, a condition common in Ranunculaceae (subclass Magnoliidae) and many Caryophyllidae. Many species of this subclass do have petals now, but their petals are thought not to be homologous with petals of other angio­sperms. Instead, in some they appear to be modified sepals, in others modified stamens.

FIGURE 4: The order Caryophyllales is characterized by the presence of betalain pigments in flowers and fruits. There are two basic types: betacyanins (red to violet) and betaxanthins (yellow).

Another unifying character of the order Caryophyllales is that the endosperm develops little if at all, and a different nutritive tissue (perisperm) develops by the proliferation of the nucellus (Fig. 5).

FIGURE 5: In Caryophyllales, endosperm develops for only a short while or not at all and is not sufficient to nourish the embryo. Instead, the nucellus (megasporangium) cells proliferate and act like endosperm, forming a tissue called perisperm. Which do you think probably occurred first in evolution—the mutations that caused the lack of formation of endosperm or those that caused the formation of perisperm?

A third feature that unites the members of this order and distinguishes them from all other taxa is the nature of the plastids in their sieve tube members. In Caryophyllales, phloem plastids contain deposits of fibrous protein located as a ring just interior to the plastid membrane (Fig. 6). In other subclasses, plastids contain either starch or crys­talline protein with a different structure.

FIGURE 6: The plastids in sieve tube members are simple, but they may accumulate particles of starch or protein or both. The nature of the accumulated material is highly specific with regard to the family of the organism, and phloem plastid analysis is important in studying the evolution of flowering plants. Sieve tube plastids of Monococcus (a) lack a central cubic protein crystal, but those of Macarthuria have one (b). Both are members of order Caryophyllales, so both have a peripheral ring of protein filaments. (Both X 40,000) (Courtesy of H.-Dietmar Behnke, University of Heidelberg)

The Caryophyllidae are postulated to have arisen from ancestors to the family Ranunculaceae or a similar group, about 70 to 80 million years ago. The members of Caryophyllidae are mostly herbaceous, with either no wood, very little wood, or unusual, anomalous wood (Figs. 7). The ancestral group is therefore suspected to have been herbaceous or shrubby, having lost the capacity for extended, massive secondary growth. Those members of Caryophyllidae that are now large trees typically have anomalous sec­ondary growth; because these woody plants evolved from an herbaceous ancestor, their wood is not strictly homologous with that of other angiosperms. All the cell types are the same, but often the organization of the wood is different.

FIGURE 7: Members of subclass Caryophyllidae: (a) Portulaca (Portulaca grandiflora), (b) Carpobrotus (a, B. Head/Earth Scenes').

Subclass Dilleniidae Examples of Dilleniidae are Paeonia (Paeoniaceae), Camellia (both the ornamental and the plant from which tea is produced; Theaceae); Hypericum (St. John's wort; Clusiaceae); linden tree (Tiliaceae); Theobroma cacao (source of chocolate; Sterculiaceae); balsa wood (Bombacaceae); cotton, Hibiscus, and mallows (Malvaceae); insect-catching pitcher plants (Sarraceniaceae and Nepenthaceae) and sundews (Droseraceae); violets (Violaceae); passion flowers (Passifloraceae); pumpkins, watermelons, and squash (Cucurbitaceae); Rhododendron, cranberries, blueberries, heather, and mountain laurel (Ericaceae); and cyclamen and primroses (Primulaceae) (Table 4). Subclass Dilleniidae evolved from subclass Magnoliidae. Their most striking evolutionary modifications are fusions of the flower parts and several technical features. Whereas the most relictual flowering plants have numerous flower parts, all separate and free of each other as in Magnolia, in Dilleniidae there are strong trends of fusion. Carpels are most commonly fused together into one compound gynoecium, and in about one third of the species, petals are fused together (Fig. 8). The most relictual group within the subclass Dilleniidae is the order Dilleniales (which contains peonies), especially the family Dilleniaceae. It does not have many of the characters of the subclass and could be placed rather easily into subclass Magnoliidae; it has been suggested that the Dilleniidae diverged from the Magnoliidae about 75 million years ago.

FIGURE 8: ((a)) These flowers of Cavendishia in the Ericaceae show the derived feature of sympetally—petals fused together as one unit, except at their tips. Fused parts are common in recently evolved flowers, rare in ancient ones, (b to e) Members of subclass Dillemidae (b) swamp rose-mallow (Hibiscus palustris); (c) St John's wort (Hypericum spathulatum); (d) pitcher plant (Sarracenia alabamense); (e) Theobroma cacao, the source of chocolate. Flowers and fruits are borne on the trunk and large branches, not on twigs. The seeds are harvested, fermented, roasted, and ground into cocoa powder. (b, S. Rannels from Grant Heilman; john Lynch, PHOTO/NATS; d, William E. Ferguson; e, JamesL. Castner))

The central order of Dilleniidae is Theales, which contains camellias, tea, and Hypericum. The rest of the subclass seems to have diversified from this group. During the later evolution into the various orders, numerous modifications occurred, leaving few dominant similarities. Instead, this is a diverse group, occupying many habitats and having numerous types of structure, metabolism, and reproductive biology. Dilleniidae contains 13 orders, 78 families, and about 25,000 species.

Subclass Rosidae. Subclass Rosidae is the largest in terms of the number of families it contains (114), and it seems to be a natural group, although it is difficult to give any universal characters (Table 5). As a group, the members of Rosidae are more derived than those of subclass Magnoliidae, from which they arose (probably beginning about 115 million years ago), but have none of the specialized characters of the Hamamelidae (wind pollination) or Caryophyllidae (betalains and perisperm). It is difficult to distinguish between the Rosidae and the Dilleniidae, and one theory postulates that they constitute a single group. The Rosidae are especially interesting in that none of them has any of the highly relictual features found in some of the Magnoliidae.

One important character in Rosidae is the presence of pinnately compound leaves. This is believed to have been the ancestral condition for the subclass, the Rosidae having evolved from some member of the Magnoliidae that had pinnately compound leaves. Although some living species have simple leaves, these apparently have arisen from com-pound leaves, perhaps by suppression of all the leaflets except one. Whereas simple leaves are an early, relictual condition of the division Magnoliophyta, they are a later, derived condition for subclass Rosidae.

Although the subclass is named for the Order Rosales, roses should not be considered typical because Rosales is the most relictual order, the one closest to the Magnoliidae. The members of the rest of subclass Rosidae are much more derived and modified (Fig. 9). Because Rosidae contains 18 orders, 114 families, and 58,000 species, only a few can be mentioned here. Five of the orders contain almost 75 percent of the species: Fabales (legumes) 14,000 species; Myrtales {Eucalyptus, evening primrose) 9000; Euphorbiales (poinsettia, rubber tree) 7600; Rosales (roses, saxifrages) 6600; and Sapindales (maples, horse chestnuts, creosote bush, and the species whose resins are valued as frankincense— Boswellia—and myrrh—Commiphora) 5400. Members of this subclass include roses, of course, and legumes (peas, beans, peanuts, Mimosa, redbud, and clover; Fabaceae = Leguminosae); Fuchsia, evening primrose (Onagraceae); dogwood (Cornaceae); mistletoes and some of the other parasites (Santalaceae, Loranthaceae, Viscaceae, and Balanophoraceae); the spurges that look like cacti and often have an extremely poisonous milky latex (Euphorbiaceae); grapes (Vitaceae); maples (Aceraceae); geraniums (Geraniaceae); dill, celery, carrot, parsley, and hemlock (Apiaceae = Umbelliferae).

FIGURE 9: Members of subclass Rosidae: (a) lupine (Lupinus latifolius), (b) horse chestnut (Aesculus hippocastanum), (c) Mexican plum (Prunus mexicana), (d) strawberry (Fragaria). (b, Kent and Donna Dannen/Photo Researchers, Inc.)

The rose family is important not only in an evolutionary sense but also economically. Rosaceae contains numerous ornamental genera, including Rosa, Crategus (hawthorn), Spiraea, Cotoneaster, Pyracantha, Photinia, Potentilla, Chaenomeles (flowering quince), and Sorbus (mountain ash). The family also provides most of the fruits that can be grown in temperate climates: Malus (apple), Pyrus (almond, apricot, cherry, nectarine, peach, plum, prune), Eriobotrya (loquat), Fragaria (strawberry), and Rubus (blackberry, loganberry, and raspberry).

Subclass Asteridae. The most derived subclass of dicots is the Asteridae (Table 6), which contains plants such as sunflower, periwinkle, petunia, and morning glory. The Asteridae, having evolved out of the Rosidae perhaps as recently as 60 million years ago, are now far removed from the relictual subclass Magnoliidae. The majority of Asteridae can be easily distinguished from all other flowering plants on the basis of three features: (1) They have sympetalous flowers (their petals are fused together into a tube); (2) they always have just a few stamens, never more than the number of petal lobes; and (3) stamens alternate with petals (Fig. 10). The Asteridae exploit very specialized pollinators that recognize complex floral patterns, and such plants could not evolve before derived, sophisticated insects appeared.

FIGURE 10: Flowers of potato (Solanum tuberosum) have stamens that alternate with the fused petals.

Many chemical differences exist between this group and all others. It lacks many specialized chemicals found in other subclasses: betalains present in the Caryophyllidae, benzyl-isoquinoline alkaloids common in Magnoliidae, and ellagic acid (Fig. 11a) or proanthocyanins common in Rosidae, Dilleniidae, and Hamamelidae. Instead, many as teridae have iridoid compounds (Fig. 11b), which occur only rarely outside this subclass.

FIGURE 11:  (a) The presence or absence of certain classes of chemicals is an important character in studying the relationships of plants (chemotaxonomy). This is ellagic acid, which is common in three dicot subclasses but absent from one of the most derived, the Asteridae. Its presence deters many insects from eating the plants, but by about 50 million years ago, many types of insects had evolved a tolerance to it. (b) Many Asteridae produce iridoid compounds such as this cornin. They are a relatively new class of chemical defense compounds, so new that few insects tolerate them; iridoid compounds may be partly responsible for the success of the Asteridae by keeping herbivory to a minimum.

At present, this subclass has the greatest number of species (about 60,000), but they are grouped into a small number of large families. One family (sunflowers, daisies; Asteraceae = Compositae) contains fully one third of all the species and is the largest family of dicots. Examples of this subclass are milkweeds (Asclepiadaceae); potato, tomato, red peppers, eggplant, tobacco, deadly nightshade, and petunia (Solanaceae); morning glory (Convolvulaceae); thyme, mints, and lavender (Lamiaceae); and Asteraceae with sunflowers, dandelions, lettuce, Chrysanthemum, ragweed, and thistle (Fig. 12).).

Many members of this subclass are extremely important medicinally: Apocynaceae (oleander family) contains periwinkle, Vinca, from which are extracted vinblastine and vincristine, two of our most potent anticancer drugs. Rubiaceae contains, in addition to coffee (Coffea), Cinchona, from which we derive the antimalaria drug quinine. Another rubiaceous genus, Cephaelis, provides us with ipecac, an emetic used to induce vomiting in cases of oral poisoning. Heart disease is treated with cardiac glycosides extracted from Digitalis (Scrophulariaceae, the snapdragon family); these compounds make heart muscle beat more slowly and strongly, increasing output of blood from the heart and improving circulation.

The most basal orders of subclass Asteridae, such as Gentianales (gentian and milkweed families) and Solanales (families of potato, morning glory, dodder, phlox), tend to be only moderately specialized compared with the rest of the subclass. They do have the fused petals and reduced number of stamens, but they show no major, distinctive evolutionary trends. They have many body types ranging from herbs to water plants to vines and occasionally small trees.

FIGURE 12: Members of subclass Asteridae: (a) potato (Solanum tuberosum), (b) milkweed (Asclepias viridis), (c) goatsbeard (Tragopogon species). Each outer "petal" is a ray floret and each central flower is a disk floret. The dark cylinders are anthers that have fused around styles. The innermost disk florets have not yet opened.

The order ScrophulHelveticaes (families of olive, Penstemon and snapdragon, gesneriads, acanths, and trumpet-creeper) is more derived in its floral characters; the flowers tend to be bilaterally symmetrical and of sizes and shapes that permit only certain insects to enter and effect pollination. The floral bilateral symmetry further forces the insect to enter in ore particular orientation. Pollinators capable of doing this tend to be sophisticated and able to recognize different flowers easily. They learn which flowers provide the greatest rewards, then search for other flowers of identical shape, color pattern, and fragrance, thus providing efficient pollination for the plant species.

The order Asterales consists of the single giant family Asteraceae. It contains 1100 genera and 20,000 species distributed worldwide in almost all habitats except dense, dark forests. They range from important food plants (Lactuca—lettuce) to ornamentals to weeds. The characteristic daisy/sunflower type of inflorescence makes them instantly recognizable. Members of Asteraceae have a wide range of unique chemical defenses against herbivores: sesquiterpene lactones, monoterpenes, terpenoids, and latex canals that contain polyacetylene resins (Fig. 13). The presence of these chemicals makes composites extremely resistant to animals that eat plants or lay eggs in them; it also causes them to be irritating to human skin, resulting in numerous cases of contact dermatitis. The Asteraceae is a young family, perhaps no more than 36 million years old, which probably originated in the Oligocene Epoch of the Tertiary Period.

FIGURE 13:  (a) This is hymenoxon, a sesquiterpene lactone, a member of the chemical arsenal of the Asteridae. This particular compound occurs in bitterweed (Hymenoxys odorata) of the southwestern United States; the plant is eaten by sheep only during droughts when no other plants are available. Sesquiterpene lactone causes hemorrhaging of all internal organs of the sheep. (b) Many members of Asteraceae contain secretory canals lined with cells that produce a variety of toxic compounds. This canal is in the style of sunflower (Helianthus)