Both the stamens and the carpels are of a unique structure, distinct from the pol- len- and ovule-bearing organs of any other seed plants. The ovules are also highly distinctive, with several unique adaptations that can be tied to the shortening of the life cycle, and some other peculiarities with no obvious adaptive value. These highly distinctive reproductive organs are fundamentally the same throughout the angiosperm crown group, so they were probably standardized prior to the common ancestor.
In addition, carpels, as closed ovule-containing chambers, most likely evolved before they became part of the bisexual flower. In some of the oldest angiosperm fossils, such as Archaefructus, the carpels and stamens appear to be located on different parts of branching systems, without evident sepals or petals (Sun et al. 2002), though this structure can also be interpreted as a specialized inflorescence of small flowers (Friis et al. 2003). In any case, it is possible that “angiosperms”
evolved before “flowering plants,” and that these two names are not exactly synonymous.
Tepals (or the perianth) are the more-or-less leaflike organs that surround the reproductive organs in bud and typically spread out when the flower opens, forming a display to attract animal pollinators. Archaic angiosperms mostly have spirally arranged tepals that sometimes grade from outer, green, protective units into inner colored units. In most modern flowers tepals are divided into two spe- cialized sets: inconspicuous green sepals and showy petals. The sepals are usually specialized for protection of the unopened flower buds, while the typical petals are colored and sometimes also produce fragrances and nectar, as required to attract particular kinds of pollinators. The numerous exceptions to these gener- alities will be explored in Chapter 7.
Tepals do not necessarily have a single common origin. Any nearby leaves can be recruited either for protection or for display, and this has happened multiple times in the evolution of modern angiosperms. A most extravagant example is found in the familiar poinsettia. The bright red structures that attract pollinators are actually colored leaves that surround clusters of tiny, inconspicuous flowers. It appears on the other hand that petals in some families of flowering plants (e.g., the carnation family and rose family) evolved from the modification of some of the stamens rather than from ancient tepals.
The stamens typically consist of four parallel pollen sacs, usually packed like a bundle of sausages into a compact anther (Fig. 6.5A) and attached to the flower axis by a long, slender stalk (the filament). The four pollen sacs are distinctively borne on two sides of a flattened central ribe (Fig. 6.5B), suggesting an origin from a flat blade. Anthers in several archaic families, moreover, are more bla- tantly flat and leaflike (Fig. 6.5B–E), as if they had evolved directly from earlier pollen-bearing seed fern fronds. This interpretation is controversial, however, and we’ll see shortly that there are some other possibilities.
The carpels are specialized chambers within which the ovules develop and mature into seeds. The angiosperms get their name (“hidden seeds”) from this unique arrangement. Pollen tubes must enter the carpel to bring sperm to egg. A specialized region at the tip of the carpel, called the stigma, becomes sticky when eggs are ready for fertilization. This not only catches the pollen, but also secretes chemicals that stimulate the pollen tube to begin its growth. An elongate section of the carpel, called the style, provides a soft-tissued conduit for the pollen tubes to reach the ovule chamber, or ovary, below.
The classic model of the carpel is something like a modern peapod, or the similar multiseeded follicles seen in some members of the Ranunculaceae. Such a carpel is considered a seed leaf (megasporophyll), folded along its midrib (or “backbone”), with the margins joined together and the ovules brought inside (Fig. 6.6). Though there is some controversy about the form of the very earli- est carpels (which we’ll get to later), most modern carpels can be viewed as
Figure 6.5 Although there is much variation, typical stamens, like those in Plantago (A),
consist of a slender stalk, or filament, and a slightly flattened anther with four pollen sacs (B). In some archaic angiosperms (C), stamens are flat and leaflike, suggesting ancestry
from a pollen-bearing leaf. Drawings from Brown 1935 (A, B) and Mauseth 2014 (C).
Figure 6.6 A follicle (A, B) is a simple carpel with edges rolled together and sealed along a suture. The ovules are lined up along each margin of the leaflike ancestral structure. In
Eranthis (Ranunculaceae) (C), the separate carpels are maturing into follicles; petals and
stamens have fallen off. The capsule of a Colchicum (lily order) (D) develops from carpels
modifications of this fundamental design. Many carpels become dry and split open to release the mature seeds. The splitting occurs most often along the joined margins, essentially “unfolding” the original leaf, though many other ways of opening have evolved among specialized fruit types.
In archaic angiosperms, carpels are separate from each other and often variable in number. In most modern angiosperms, however, the carpels are fused together, creating a multichambered pistil. An advantage of this arrangement is that several carpels then share a common stigma, or have their stigmas close together. That in turn results in quicker and more efficient visits by pollinators. The pistil or the individual carpels become fruits as the ovules within them ripen into seeds.
As the angiosperms diversified, carpels became both simpler and more com- plex. Some may harbor a single ovule (as in a plum), or at the other extreme, a million or more (as in an orchid pod). In many angiosperms when the carpels are fused together into a pistil, the chambers of the carpels remain distinct from one another, and in each chamber, the two rows of ovules associated with the ancient carpel edges are lined up along a central axis. The capsule of a lily illus- trates this nicely (Fig. 6.6D). In others, the carpels join edge to edge, creating a single chamber.
Hiding ovules within closed carpels contributed to the early angiosperms’ ability to grow and reproduce in varied climates, particularly dry ones. It pro- tected young ovules from drying out or being eaten by animals. Since they no lon- ger had to provide their own armor, ovules then became smaller and lighter than their gymnosperm ancestors, could develop more quickly, and could be fertilized while they were still quite small and soft. This greatly accelerated the reproductive cycle. Gymnosperm pollen tubes have to eat their way slowly through the thick outer tissues of the ovule, a process that can take months.
Animal pollination, simpler stamens, and chambers for the protection of ovules all contributed to the angiosperms’ success in environments with short growing seasons, but the ovules themselves underwent the most extraordinary changes. Remember that a haploid, egg-bearing gametophyte must develop within the ovule before fertilization can take place. In gymnosperms, a female gametophyte consists of hundreds of cells and much stored food, in addition to the eggs waiting to be fertilized (Fig. 6.7A). These large ovules take much time and energy to develop, and if they are not fertilized, they drop off, wasting the food stored within them.
In the small soft ovules of angiosperms, however, the gametophyte itself remains in an embryonic state until it is fertilized. It consists of only seven cells (Fig 6.7B) and contains virtually no stored food. One of the cells, located near the ovule tip, serves as the egg, but the oddest part of the story concerns the large central cell, which contains two nuclei.
During fertilization, two sperm cells migrate down each pollen tube, the same as in gymnosperms. One sperm fertilizes the egg, as expected, but the second
sperm is not just a spare in case something happens to the first. It proceeds into the large central cell, where it combines with the two nuclei, creating a triploid cell (one that contains three complete sets of chromosomes), something unheard of in the rest of the living world. This unique process is called double fertilization. The triploid cell then begins dividing rapidly, and nutrients flow into it from the parent plant, forming a specialized food storage tissue called endosperm. Note that the endosperm does not begin to form until fertilization takes place, and in this way, angiosperms don’t waste material or energy on ovules that never get fertilized.
The ovules of angiosperms are also peculiarly different from those of gymno- sperms in two ways that have no obvious adaptive value. First, each angiosperm ovule (with a few exceptions) is wrapped in not one but two distinct integu- ments. The two integuments are thin, providing no apparent benefit compared to a single one, so the origin of the second integument is hard to explain. Second, most angiosperm ovules are bent over (anatropous) so that the tip faces back to the base (Fig. 6.7B). A typical gymnosperm ovule stands straight, with its tiny opening (micropyle) at its tip facing straight up (Fig. 6.7A). Though these features seem to have no significance, they may be clues as to who their ancestors were.
Figure 6.7 Ovules of gymnosperms (A) have one integument and are oriented straight up; those of angiosperms (B) have two integuments and are bent to face downward. The female gametophyte of angiosperms consists of only seven cells; one cell near the ovule opening serves as an egg, and the binucleate central cell will become the endosperm.