Plant sexuality

Close-up of an Echinopsis spachiana flower, showing both carpels (only the styles and stigmas are visible) and stamens, making it a complete flower.

Plant sexuality covers the wide variety of sexual reproduction systems found across the plant kingdom. This article describes morphological aspects of sexual reproduction of plants.

Among all living organisms, flowers, which are the reproductive structures of angiosperms, are the most varied physically and show the greatest diversity in methods of reproduction of all biological systems.^[1] Carolus Linnaeus (1735 and 1753) proposed a system of classification of flowering plants based on plant structures, since plants employ many different morphological adaptations involving sexual reproduction, flowers played an important role in that classification system. Later on Christian Konrad Sprengel (1793) studied plant sexuality and called it the "revealed secret of nature" and for the first time it was understood that the pollination process involved both biotic and abiotic interactions (Charles Darwin's theories of natural selection utilized this work to promote his idea of evolution). Plants that are not flowering plants (green alga, mosses, liverworts, hornworts, ferns and gymnosperms) also have complex interplays between morphological adaptation and environmental factors in their sexual reproduction. The breeding system, or how the sperm from one plant fertilizes the ovals of another, is the single most important determinant of the mating structure of nonclonal plant populations. The mating structure or morphology of the flower parts and their arrangement on the plant in turn controls the amount and distribution of genetic variation, a central element in the evolutionary process.^[2]

Flower, showing both carpels (only the styles and stigmas are visible) and stamens, making it a complete flower.

History

Unlike animals, plants are immobile and cannot seek out sexual partners for reproduction. The first plants used abiotic means to transport sperm for reproduction, utilizing water and wind. The first plants were aquatic and released sperm freely into the water to be carried by the currents. As plants moved onto land they used a thin film of water or water droplets like liverworts and ferns, in which mobile sperm swam from the male reproduction organs to the female organs. As plants became more complex and developed vascular systems enabling them to grow taller, they used alternation of generations like in ferns or the wind to move spores. In the Paleozoic era progymnosperms reproduced by using spores dispersed on the wind, 350 million years ago the seed plants evolved, including seed ferns, conifers and cordaites all were gymnosperms. Pollen grains, the male gametophyte, developed for protection of the sperm during the process of transfer from male to female parts. It is believed that insects feed on the pollen and plants evolved to use insects to actively carry pollen from one plant to the next. Seed producing plants, which include the angiosperms and the gymnosperms, have hetromorphic alternation of generations with large sporophytes containing much reduced gametophytes. Angiosperms have distinctive reproductive organs called flowers with carpels and the gametophyte is greatly reduced to a female embryo sac with as few as eight cells and the male gametophyte develop from the pollen grains. The sperm of seed plants are non motile except for two older groups of plants the Cycadophyta and the Ginkgophyta which have flagellated sperm.

Terminology

The flowers of angiosperms are determinate shoots that have sporophylls. The parts of flowers are named by scientists and show great variation in shape, these flower parts include sepals, petals, stamens and carpels. As a group the sepals form the calyx and as a group the petals form the corolla, together the corolla and the calyx is called the perianth. The stamens collectively are called the androecuim and the carpels collectively are called the gynoecium.

The complexity of the systems and devices used by plants to achieve sexual reproduction has resulted in botanists and evolutionary biologists using numerous terms to describe physical structures and functional strategies. Dellaporta and Calderon-Urrea (1993) list and define a variety of terms used to describe the modes of sexuality at different levels in flowering plants. This list is reproduced here ^[3], generalized to fit more than just plants that have flowers, and expanded to include other terms and more complete definitions.

The Alder is monoecious. Shown here: maturing male flower catkins on right, last year's female catkins on left

Individual reproductive unit (a flower in angiosperms)

• Bisexual - or perfect flowers have both male (androecium) and female (gynoecium) reproductive structures, including stamens, carpels, and an ovary. Flowers that contain both androecium and gynoecium are called androgynous or hermaphroditic. Examples of plants with perfect or bisexual flowers include the lily, rose, and most plants with large showy flowers, though a perfect flower does not have to have petals or sepals. Other terms widely used are hermaphrodite, monoclinous, and synoecious. A complete flower is a perfect flower with petals and sepals.
• Unisexual - Reproductive structure that is either functionally male or functionally female. In angiosperms this condition is also called diclinous, imperfect or incomplete.

Adaptations

Plants with wind pollinated flowers tend to have flowers without petals or sepals. Typically large amounts of pollen are produced and pollination often occurs early in the growing season before leaves can interfere with the dispersal of the pollen. Many trees and all grasses and sedges are wind pollinated, as such they have no need for large fancy flowers. In plants that use insects or other animals to move pollen from one flower to the next, plants have developed greatly modified flower parts to attract pollinators and to facilitate the movement of pollen from one flower to the insect and from the insect back to the next flower. Plants have a number of different means to attract pollinators including color, scent, heat, nectar glands, eatable pollen and flower shape. Along with modifications involving the above structures two other conditions play a very important role in the sexual reproduction of flowering plants, the first is timing of flowering and the other is the size or number of flowers produced. Often plant species have a few large, very showy flower while others produce many small flower, often flowers are collected together into large inflorescences to maximize their visual effect, becoming more noticeable to passing by pollinators. Flowers are attraction strategies and sexual expressions are functional strategies used to produce the next generation of plants, with pollinators and plants having co-evolved, often to some extraordinary degrees, very often mutually benefiting both.

The largest family of flowering plants is the orchids (Orchidaceae), estimated by some specialists to include up to 35,000 species,^[4] which often have highly specialized flowers used to attract insects and facilitate pollination. The stamens are modified to produce pollen in clusters called pollinium, which are attached to insects when crawling into the flower. The flower shapes are modified to force insects to pass by the pollen, which is "glued" to the insect. Some orchids are even more highly specialized, with flower shapes that mimic the shape of insects to attract them to 'mate' with the flowers, a few even have scents that mimic insect pheromones.

Flower heads showing disk and ray florets.

Another large group of flowering plants is the Asteraceae or sunflower family with close to 22,000 species,^[5] which also have highly modified inflorescences that are flowers collected together in heads composed of a composite of individual flowers called florets. Heads with florets of one sex, when the flowers are pistillate or functionally staminate, or made up of all bisexual florets, are called homogamous and can include discoid and liguliflorous type heads. Some radiate heads may be homogamous too. Plants with heads that have florets of two or more sexual forms are called heterogamous and include radiate and disciform head forms, though some radiate heads may be heterogamous too.

Individual plant sexuality

Many plants have complete flowers that have both male and female parts, others only have male or female parts and still other plants have flowers on the same plant that are a mix of male and female flowers. Some plants even have mixes that include all three types of flowers, where some flowers are only male, some are only female and some are both male and female. A distinction needs to be made between arrangements of sexual parts and the expression of sexuality in single plants verses the species. Some plants also undergo what is called Sex-switching, like Arisaema triphyllum which express sexual differences at different stages of growth. In some arums smaller plants produce all or mostly male flowers and as plants grow larger over the years the male flowers are replaced by more female flowers on the same plant. Arisaema triphyllum thus covers a multitude of sexual conditions in its life time; from nonsexual juvenile plants to young plants that are all male, as plants grow larger they have a mix of both male and female flowers, to large plants that have mostly female flowers.^[6] Other species have plants that produce more male flowers early in the year and as plants bloom later in the growing season they produce more female flowers. In plants like Thalictrum dioicum all the plants in the species are ether male or female.

Specific terms are used to describe the sexual expression of individual plants within a population.

• Androecious - plants producing male flowers only, produce pollen but no seeds, the male plants of a Dioecious species.
• Dioecious - refers to a species having separate male and female plants. That is, no individual plant of the species produces both microspores and megaspores; individual plants are either male (producing microspores) or female (producing megaspores). ^[7] From Greek for "two households". [Individual plants are not called dioecious; they are either gynoecious (female plants) or androecious (male plants).]
• Gynoecious - plants producing female flowers only, produces seeds but no pollen, the female of a Dioecious species. In some plant species or populations all individuals are gynoecious with non sexual reproduction used to produce the next generation.
• Hermaphrodite - A plant that has only bisexual reproductive units (flowers, conifer cones, or functionally equivalent structures). In angiosperm terminology a synonym is monoclinous from the Greek "one bed".
• Monoecious - having separate male and female reproductive units (flowers, conifer cones, or functionally equivalent structures) on the same plant; from Greek for "one household". Individuals bearing separate flowers of both sexes at the same time are called simultaneously or synchronously monoecious. Individuals that bear flowers of one sex at one time are called consecutively monoecious; Plants may first have single sexed flowers and then later have flowers of the other sex. Protoandrous describes individuals that function first as males and then change to females; protogynous describes individuals that function first as females and then change to males.
• Subdioecious, a tendency in some dioecious species to produce monoecious plants. The population produces normally male or female plants but some are hermaphroditic, with female plants producing some male or hermaphroditic flowers or vise versa. The condition is thought to represent a transition between hermaphroditism and dioecy. ^[8].
  • Gynomonoecious - has both hermaphrodite and female structures.
  • Andromonoecious - has both hermaphrodite and male structures.
  • Subandroecious - plant has mostly male flowers, with a few female or hermaphrodite flowers.
  • Subgynoecious - plant has mostly female flowers, with a few male or hermaphrodite flowers.
• Trimonoecious (polygamous) - male, female, and hermaphrodite structures all appear on the same plant.
• Diclinous ("two beds"), an angiosperm term, includes all species with unisexual flowers, although particularly those with only unisexual flowers, i.e. the monoecious and dioecious species.

Holly (Ilex aquifolium) is dioecious: (above) shoot with flowers from male plant; (top right) male flower enlarged, showing stamens with pollen and reduced, sterile stigma; (below) shoot with flowers from female plant; (lower right) female flower enlarged, showing stigma
and reduced, sterile stamens with no pollen

Plant population

Most often plants show uniform strategies across the species or in populations in their sexual expression and specific terms are used to describe the sexual expression of the species or population.

• Hermaphrodite - only hermaphrodite plants with flowers that have both male and female parts.
• Monoecious - only monoecious plants, that is plants have separate male and female flowers on the same plant. A plant species where the male and female organs are found in different flowers on the same plant. These plants are often wind pollinated. Examples of monoecious plants include corn,^[9] birch and pine trees,^[10] and most fig species.^[11]
• Dioecious - only dioecious plants, all plants are either female or male.
• Gynodioecious - both female and hermaphrodite plants present. In some plants, strictly female plants are produced by the degeneration of the tapetum, a shell-like structure in the anther of a flower where the pollen cells form,^[12] producing male sterility.^[13]
• Gynoecy - plants are all females in a population, often regulated by environmental factors like temperature, photo period or water availability.
• Androdioecious - both male and hermaphrodite plants present.
• Polygamous - when there is a mix of hermaphrodite and unisexual plants in the natural population.^[14]
• Subdioecious - population of unisexual (dioecious) plants, with monoecious individuals too.^[15]
• Trioecious - sometimes used in place of subdioecious when male, female, and hermaphrodite plants are more equally mixed with in the same population.

About 11% of all angiosperms are strictly dioecious or monoecious, lntermediate forms of sexual dimorphism, including gynodioecy and androdioecy, represent 7% of the species examined of a survey of 120,000 plant species. In the same survey, 10% of the species contain both unisexual and bisexual flowers.^[16]

The majority of plant species use allogamy - also called cross-pollination, as a means of breeding. Many plants are self fertile and the male parts can pollinate the female parts of the same flower and/or same plant. Some plants use a method known as self-incompatibility to promote outcrossing. In these plants, the male organs cannot fertilize the female parts of the same plant, other plants produce male and female flowers at different times to promote outcrossing. Some plants have bisexual flowers but the pollen is produced before the stigma of the same flower is receptive of pollen, this promotes out crossing by greatly limiting self pollination and these types of flowers are called protandrous.

Flower morphology

A species such as the ash tree (Fraxinus excelsior L.), demonstrates the possible range of variation in morphology and functionality exhibited by flowers with respect to gender. Flowers of the ash are wind-pollinated and lack petals and sepals. Structurally, the flowers may be either male or female, or even hermaphroditic, consisting of two anthers and an ovary. A male flower can be morphologically male or hermaphroditic, with anthers and a rudimentary gynoecium. Ash flowers can also be morphologically female, or hermaphroditic and functionally female.

Evolution

Angiosperms

It is thought that flowering plants evolved from a common hermaphrodite ancestor, and that dioecy evolved from hermaphroditism. Hermaphroditism is very common in flowering plants; over 85% are hermaphroditic, whereas only about 6-7% are dioecious and 5-6% are monoecious. ^{[17] [18]}

A fair degree of correlation (though far from complete) exists between dioecy/sub-dioecy and plants that have seeds dispersed by birds (both nuts and berries). It is hypothesized that the concentration of fruit in half of the plants increases dispersal efficiency; female plants can produce a higher density of fruit as they do not expend resources on pollen production, and the dispersal agents (birds) need not waste time looking for fruit on male plants. Other correlations with dioecy include: tropical distribution, woody growth form, perenniality, fleshy fruits, and small, green flowers.^[19]

Plant growth regulators can be used to alter flower and plant sexuality, in cucumbers ethephon is used to delay staminate flowering and transforms monoecious lines into all-pistillate or female lines. Gibberellins also increase maleness in cucumbers. Cytokinins have been used in grapes that have undeveloped pistils to produce functional female organs and seed formation.

References

• Binggeli, P., & Power, J. (1999). Gender variation in ash (Fraxinus excelsior L.)
• Darwin, C. (1877). The Different Forms of Flowers on Plants of the Same Species.
• Dellaporta, S.L. and A. Calderon-Urrea. (1993). Sex determination in flowering plants. The Plant Cell 5: 1241-1251.
• Linnaeus, C. (1735). Systema Naturae.
• Renner, S.S., & Ricklefs, R.E. (1995). Dioecy and its correlates in the flowering plants. American Journal of Botany 82: 596-606.

External links

• Images of sexual systems in flowering plants at bioimages.vanderbilt.edu