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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 such as conifers) 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 ovum 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]

Contents

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. In flowers which possess indistinguishable calyx and corolla, the individual units are then called "tepals". The stamens collectively are called the androecium 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
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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.

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 versus the larger plant population. 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.[4] Other plant populations 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 either male or female.

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

  • 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 - an individual that has both 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.
  • Dioecious - refers to a plant population having separate male and female plants. That is, no individual plant of the population produces both microgametophytes (pollen) and megagametophytes (ovules); individual plants are either male or female.[5] From Greek for "two households". [Individual plants are not called dioecious; they are either gynoecious (female plants) or androecious (male plants).]
    • Androecious - plants producing male flowers only, produce pollen but no seeds, the male plants of a dioecious population.
    • Gynoecious - plants producing female flowers only, produces seeds but no pollen, the female of a dioecious population. In some plant populations, all individuals are gynoecious with non sexual reproduction used to produce the next generation.
  • Subdioecious, a tendency in some dioecious populations 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 vice versa. The condition is thought to represent a transition between hermaphroditism and dioecy.[6].
    • 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.
  • Polygamy - Plants with male, female and perfect (hermaphrodite) flowers on the same plant, called trimonoecious or polygamomonoecious plants, (see next section for use for plant populations).[7] A polygamous inflorescence has both unisexual and bisexual flowers.[8]
    • Trimonoecious (polygamous) - male, female, and hermaphrodite floral morphs 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 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 population 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. The American Holly (Ilex opaca) is a famous example.
  • Androdioecious - both male and hermaphrodite plants present.
  • 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]
  • Gynoecy - plants are all females in a population, often regulated by environmental factors like temperature, photo period or water availability.
  • Polygamous - when there is a mix of hermaphrodite and unisexual plants in the natural population.[13]
    • Subdioecious - population of unisexual (dioecious) plants, with monoecious individuals too.[14]
    • Trioecious - sometimes used in place of subdioecious when male, female, and hermaphrodite plants are more equally mixed within the same population.
  • Polygamodioecious, - having bisexual and male flowers on some plants, and bisexual and female flowers on others.[15]

About 11% of all angiosperms are strictly dioecious or monoecious. Intermediate 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.

Dichogamy is common in flowering plants, and occurs when bisexual (perfect) flowers (or sometimes entire plants) produce pollen when the stigmas of the same flower is not receptive of the pollen, this promotes outcrossing by limiting what is called autopollination or self pollination or selfing.[17] These plants are called dichogamous. Some plants have bisexual flowers but the pollen is produced before the stigma of the same flower is receptive of pollen, these are described as protandrous flowers; in a similar way, protogyny describes flowers that have stigmas that can accept pollen before the same flower or plant sheds its pollen.[7]

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.

The Asteraceae or sunflower family with close to 22,000 species,[18] 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.

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.[19][20]

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.[21]

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

  1. ^ Barrett, S. C. H. (2002). The evolution of plant sexual diversity. Nature Reviews Genetics 3(4): 274-284.
  2. ^ Costich, D. E. (1995). Gender specialization across a climatic gradient: experimental comparison of monoecious and dioecious Ecballium. Ecology 76 (4): 1036-1050.
  3. ^ Molnar, S. (2004). Plant Reproductive Systems, internet version posted February 17, 2004.
  4. ^ Ewing, J. W., & Klein, R. M. (1982). Sex Expression in Jack-in-the-Pulpit. Bulletin of the Torrey Botanical Club 109 (1): 47-50. doi:10.2307/2484467
  5. ^ Angiosperm sexual systems
  6. ^ Correlation between male and female reproduction in the subdioecious herb Astilbe biternata (Saxifragaceae) - Olson and Antonovics 87 (6): 837 - American Journal of Botany
  7. ^ a b Geber, Monica A. (1999), Gender and sexual dimorphism in flowering plants : with 29 tables, Berlin: Springer, pp. 4, ISBN 3540645977, http://books.google.com/books?id=pUo2T34ppKUC&pg=PA4&dq=polygamy+plants&ei=2aFlSfeVBqTmyASxoeyTAw&client=firefox-a#PPA4,M1 
  8. ^ Davis, P.H.; Cullen, J. (1979), The identification of flowering plant families, including a key to those native and cultivated in north temperate regions, Cambridge: Cambridge University Press, pp. 106, ISBN 0521293596 
  9. ^ Kiesselbach, T.A. (1999), The structure and reproduction of corn, Cold Spring Harbor, N.Y: Cold Spring Harbor Laboratory Press, pp. 3, ISBN 9780879695569, OCLC 245875754 
  10. ^ http://www.ext.vt.edu/departments/envirohort/factsheets2/landsnurs/feb88pr6.html
  11. ^ Waldbauer, Gilbert (2003), What good are bugs? : insects in the web of life, Cambridge, Mass.: Harvard University Press, pp. 33–34, ISBN 9780674010277, OCLC 50198798 
  12. ^ Delannay, Xavier (1979), "Evolution of male sterility mechanisms in gynodioecious and dioecious species ofCirsium (Cynareae, Compositae)", Plant Systematics and Evolution 132: 327, doi:10.1007/BF00982395 
  13. ^ Males outcompete hermaphrodites for seed siring success in controlled crosses in the polygamous Fraxinus excelsior (Oleaceae) - Morand-Prieur et al. 90 (6): 949 - American Journal of Botany
  14. ^ Barrett S.C.H.; Case A.L.; Peters G.B. Gender modification and resource allocation in subdioecious Wurmbea dioica (Colchicaceae) Journal of Ecology, Volume 87, Number 1, January 1999 , pp. 123-137(15)
  15. ^ Gleason & Cronquist (1963), Manual of vascular plants of Northeastern United States and adjacent Canada, Princeton, N.J., pp. XX, ISBN 0442027222 
  16. ^ S. L. Dellaporta, and A. Calderon-Urrea. Sex Determination in Flowering Plants Plant Cell 5: Pages 1241-1251.
  17. ^ http://www.publish.csiro.au/?act=view_file&file_id=BT9950451.pdf
  18. ^ Asteraceae in Flora of North America @ efloras.org
  19. ^ Rieger, R., A. Michaelis, and M.M. Green (1991). Glossary of Genetics, Fifth Edition. Springer-Verlag. ISBN 0-387-52054-6
  20. ^ Heilbuth, J.C. (2000). Lower species richness in dioecious clades. American Naturalist 156: 221-241
  21. ^ Vamosi, J.C., & Vamosi, S.M. (2004). The role of diversification in causing the correlates of dioecy. Evolution 58: 723-731

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