Morphogenesis of Flowers—Our Evolving View

In this essay, the time course of our understanding of the structure and function of flowers will first be outlined from prehistoric times to the mid-twentieth century. Information is taken mostly from Sachs (1875), Arber (1950), and especially Morton (1981). More recent studies on the genetic basis of flower development will then be reviewed, focusing on floral organs rather than ovules, seeds, or fruits. Finally, major gaps in our present understanding and possible future advances will be discussed. Until ∼12,000 years ago, humankind survived by exploiting wild plants and animals for food and shelter. Since then, domestication of many species led to major population increases, urbanization, and the availability of time for creative pursuits. These changes have been associated with the rise of mechanical invention, literacy, and ultimately modern civilization. The domestication of plants required knowledge of how to cultivate them successfully. However, the initial choice of species and the improvement of strains were rather haphazard and empirical processes. Improvement mostly relied on early farmers selecting seeds from the best performing plants of the current crop to grow in the next season. Occasionally, rare genetic variants or hybrids would arise that were seized on as offering major benefits in quality and yield. For example, domesticated maize differs from its wild Mexican ancestor teosinte by several major genetic variants that result in reduced branching and larger, nonshattering ears (Doebley, 2004). Also, the domestication of bread wheat in the Middle East included the selection of two sequential interspecies hybrids that apparently arose after spontaneous hybridization events between cultivated and weedy species (Feldman et al., 1995). Ancient civilizations did not know about plant sexual reproduction. The closest they got was to realize that there are two forms of date palm and that fruit set could be promoted if dust of a flowering shoot of a sterile tree was shaken over the flowering shoots of potentially fertile trees. The first historical records of attempts to comprehend the general properties of plants are the writings of the Greek philosopher Theophrastus (∼370–285 BCE). The father of botanical science, Theophrastus was a colleague of Aristotle, whom he succeeded as leader of the Lyceum. Theophrastus considered plants to be made up of persistent parts (roots, stems, branches, and twigs) and ephemeral parts (leaves, flowers, fruits, including seeds, and the stalks of these organs). In his view, flowers were basically defined by the petals, although they did include stamens and the styles of carpels. Sepals were considered small leaves, and the ovary seemed to be viewed not as a floral part but as the future fruit case. Thus, the flower represented only those organs that abscised from the developing fruit. Sexual reproduction was not understood or distinguished from vegetative reproduction. The role of stamens, the fertilization of ovules, and the universal occurrence of seeds as a stage in the life cycle were not comprehended. For the next 1800 years, interest in the study of plants was mostly limited to their role in medicine, with descriptions of useful species being reproduced down the generations in compendia called herbals. In Oriental cultures, plant descriptions were particularly accurate, and they also included species of aesthetic attraction such as peonies, lilies, and chrysanthemums in addition to medicinal plants. In Europe from the sixteenth century on, attempts were renewed to understand the basic principles of plant structure, function, and classification. An Italian physician, Andrea Cesalpino (1519–1603), proposed the first natural system of plant classification (i.e., one in which plants are grouped by their degree of relationship) using their fructification properties. These included the position of the abscising floral organs on the seed case (i.e., whether the ovary is superior with the outer organs at its base or inferior [organs at its apex]), the number of seeds in a fruit, and the number of cavities (locules) per fruit. Joachim Jung (1587–1657), a professor of Natural Sciences in Hamburg, clarified the distinction between petals and the organs that surround the flower (which Jung called the perianthium and which includes what we now call floral bracts as well as sepals). He also noted that stamens are often divisible into a pediculus (filament) and a capitulus (head or anther). The invention of the microscope allowed two major contributions to plant anatomy soon after. Italian Marcello Malpighi (1628–1694) and Englishman Nehemiah Grew (1641–1712) observed not only plant morphology, but they linked mature structures with their development for the first time. They recognized the generality of properties of different floral organs across species. For example, they observed that what we now call perianth organs (sepals and petals) are usually essentially leaf like and that stamens, almost universal components of flowers, always released dust from their upper regions. The Englishman John Ray (1623–1705) subsequently named this dust pollen and also distinguished between the calyx (now called sepals) and the internal corolla made up of showy “petals,” a name he popularized and which came into common use. Thus, the components of the flower were now defined almost as in current usage except that the ovary was still not recognized as a floral component, only the style. Surprising as it now seems, it wasn't until the end of the seventeenth century that the role of pollen in fertilization was established and that sexual reproduction was confirmed in plants. Rudolph Jacob Camerarius (1665–1721), director of the Botanic Garden in Tübingen, Germany, observed that most flowers had stamens positioned close to the style that topped the future seed case. He proposed that such flowers were hermaphrodite and that pollen released from the anthers landed on the style and ensured that seeds subsequently developed. He concluded that petals were not involved because many flowers lack petals but set seeds (e.g., vines and cereals), and also some garden plant variants had extra petals at the expense of stamens (double flowers), and even though these may have styles, fruit was not usually set. Camerarius then performed experiments to test the role of pollen. He used plant species in which flowers of two types occurred: male (stamens only) and female (styles only). These were present either on separate plants (dioecious, including the mulberry Morus and dog's mercury Mercurialis) or on the same plant (monoecious, castor oil plant Ricinus and maize Zea). By preventing any pollen from landing on styles in each case, in 1694, he confirmed the necessary role of pollen in fruit and seed set. Again, it is surprising in hindsight how long it took for this conclusion to be extended to understanding the role of insects in transfer of pollen between anthers and styles (the 1760s by Joseph Gottlieb Koelreuter [1733–1806] in Karlsruhe) and the adaptation of many flowers to insect-driven cross-pollination rather than self-fertilization (in 1793 by Christian Konrad Sprengel [1750–1816] in Berlin). The mechanics of fertilization were not fully defined until even later. 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