Rubiaceae

Most members of the Rubiaceae are zoophilous, pollinated mainly by insects. Entomophilous species produce nectar from an epigynous disk at the base of the corolla tube to attract insects. Ornithophily is rare and is found in red-flowered species of Alberta, Bouvardia, and Burchellia. Anemophilous species are found in the tribes Anthospermeae and Theligoneae and are characterized by hermaphroditic or unisexual flowers that exhibit a set of specialized features, such as striking sexual dimorphism, increased receptive surface of the stigmas and pendulous anthers.[5]

Although most Rubiaceae species are hermaphroditic, outbreeding is promoted through sequential hermaphroditism and spatial isolation of the reproductive organs. More complex reproductive strategies include secondary pollen presentation, heterostyly, and unisexual flowers.

Secondary pollen presentation (also known as stylar pollen presentation or ixoroid pollen mechanism) is especially known from the Gardenieae and related tribes. The flowers are proterandrous and the pollen is shed early onto the outside of the stigmas or the upper part of the style, which serve as a pollen receptacle. Increased surface area and irregularity of the pollen receptacle, caused by swellings, hairs, grooves or ridges often ensure a more efficient pollen deposition. After elongation of the style, animals transport the pollen to flowers in the female or receptive stage with exposed stigmatic surfaces. A pollen catapult mechanism is present in the genera Molopanthera and Posoqueria (tribe Posoquerieae) that projects a spherical pollen mass onto visiting hawk moths.[8]

Heterostyly is another mechanism to avoid inbreeding and is widely present in the family Rubiaceae.[9] The tribes containing the largest number of heterostylous species are Spermacoceae and Psychotrieae. Heterostyly is absent in groups that have secondary pollen presentation (e.g. Vanguerieae).

Unisexual flowers also occur in Rubiaceae and most taxa that have this characteristic are dioecious. The two flower morphs are however difficult to observe as they are rather morphologically similar; male flowers have a rudimentary pistil with the ovaries empty and female flowers sterile or rudimentary stamens with empty anthers.[5] Flowers that are morphologically hermaphrodite, but functionally dioecious occur in Pyrostria.[10]

The dispersal units in Rubiaceae can be entire fruits, syncarps, mericarps, pyrenes or seeds. Fleshy fruit taxa are probably all (endo)zoochorous (e.g. tribes Pavetteae, Psychotrieae), while the dispersal of dry fruits is often unspecialized (e.g. tribes Knoxieae, Spermacoceae). When seeds function as diaspores, the dispersal is either anemochorous or hydrochorous. The three types of wind-dispersed diaspores in Rubiaceae are dust seeds (rare, e.g. Lerchea), plumed seeds (e.g. Hillia), and winged seeds (e.g. Coutarea). Long-distance dispersal by ocean currents is very rare (e.g. the seashore tree Guettarda speciosa). Other dispersal mechanisms are absent or at least very rare. Some Spermacoceae having seeds with elaiosomes are probably myrmecochorous (e.g. Spermacoce hepperiana). Epizoochorous taxa are limited to herbaceous Rubiaceae (e.g. Galium aparine fruits are densely covered with hooked bristly hairs).

The genera Anthorrhiza, Hydnophytum, Myrmecodia, Myrmephytum, and Squamellaria are succulent epiphytes that have evolved a mutualistic relationship with ants. Their hypocotyl grows out into an ant-inhabited tuber.[11] Some shrubs or trees have ant holes in their stems (e.g. Globulostylis).[12] Some Rubiaceae species have domatia that are inhabited by mites (viz. acarodomatia; e.g. Plectroniella armata).[13]

An intimate association between bacteria and plants is found in three rubiaceous genera (viz. Pavetta, Psychotria, and Sericanthe).[14] The presence of endophytic bacteria is visible by eye because of the formation of dark spots or nodules in the leaf blades. The endophytes have been identified as Burkholderia bacteria. A second type of bacterial leaf symbiosis is found in the genera Fadogia, Fadogiella, Globulostylis, Rytigynia, Vangueria (all belonging to the tribe Vanguerieae), where Burkholderia bacteria are found freely distributed among the mesophyll cells and no leaf nodules are formed.[15][16][17] The hypothesis regarding the function of the symbiosis is that the endophytes provide chemical protection against herbivory by producing certain toxic secondary metabolites.[18]

The name Rubiaceae (nomen conservandum) was published in 1789 by Antoine Laurent de Jussieu,[20] but the name was already mentioned in 1782.[21]

Several historically accepted families are since long included in Rubiaceae: Aparinaceae, Asperulaceae, Catesbaeaceae, Cephalanthaceae, Cinchonaceae, Coffeaceae, Coutariaceae, Galiaceae, Gardeniaceae, Guettardaceae, Hameliaceae, Hedyotidaceae, Houstoniaceae, Hydrophylacaceae, Lippayaceae, Lygodisodeaceae, Naucleaceae, Nonateliaceae, Operculariaceae, Pagamaeaceae, Psychotriaceae, Randiaceae, Sabiceaceae, Spermacoceaceae.[1]

More recently, the morphologically quite different families Dialypetalanthaceae,[22] Henriqueziaceae,[23] and Theligonaceae[24][25][26] were reduced to synonymy of Rubiaceae.

The classical classification system of Rubiaceae distinguished only two subfamilies: Cinchonoideae, characterized by more than one ovule in each locule, and Coffeoideae, having one ovule in each locule.[27][28] This distinction, however, was criticized because of the distant position of two obviously related tribes, viz. Gardenieae with many ovules in Cinchonoideae and Ixoreae with one ovule in Coffeoideae, and because in species of Tarenna the number of ovules varies from one to several in each locule.[29][30] During the twentieth century other characters were used to delineate subfamilies, e.g. stylar pollen presentation, raphides, endosperm, heterostyly, etc. On this basis, three[31] or eight[32] subfamilies were recognised. The last subfamilial classification solely based on morphological characters divided Rubiaceae into four subfamilies: Cinchonoideae, Ixoroideae, Antirheoideae, and Rubioideae.[5] In general, problems of subfamilies delimitation in Rubiaceae based on morphological characters are linked with the extreme naturalness of the family, hence a relatively low divergence of its members.[5]

The introduction of molecular phylogenetics in Rubiaceae research has corroborated or rejected several of the conclusions made in the pre-molecular era. There is support for the subfamilies Cinchonoideae, Ixoroideae, and Rubioideae, although differently circumscribed, and Antirheoideae is shown to be polyphyletic.[33] The tribe Coptosapelteae including the genera Acranthera and Coptosapelta, and the monogeneric tribe Luculieae have not been placed within a subfamily and are sister to the rest of Rubiaceae.[34] Currently, in most molecular research concerning the family Rubiaceae, the classification with three subfamilies (Cinchonoideae, Ixoroideae, and Rubioideae) is followed.[35] However, an alternative view is proposed where only two subfamilies are recognized, an expanded Cinchonoideae (that includes Ixoroideae, Coptosapeltaeae and Luculieae) and Rubioideae.[26] The adoption of the Melbourne Code for botanical nomenclature had an unexpected impact on many names that have been long in use and are well-established in literature. According to the Melbourne Code, the subfamilial name Ixoroideae should be replaced by Dialypetalanthoideae.[36] However, Dialypetalanthus is morphologically quite aberrant in Rubiaceae and if it should be excluded from Rubiaceae, the subfamilial name remains Ixoroideae. Molecular studies also have substantial impact on tribal delimitations and taxonomic changes are still being made.[37][38] Also here, according to the Melbourne Code, the tribe Condamineeae should be renamed to Dialypetalantheae. The following list contains the validly published tribe names, however, some tribes might be disputed. The approximate number of species is indicated between brackets,[39] however, several genera and species are not yet placed in a tribe.

The family Rubiaceae contains about 13,500 species in 619 genera. This makes it the fourth-largest family of flowering plants by number of species and fifth-largest by number of genera. Although taxonomic adjustments are still being made, the total number of accepted genera remains stable. In total, around 1338 genus names have been published, indicating that more than half of the published names are synonyms. Psychotria, with around 1530 species, is the largest genus within the family and the third-largest genus of the angiosperms, after the legume Astragalus and the orchid Bulbophyllum. However, the delimitation of Psychotria remains problematic and its adjustment might reduce the number of species. In total, 30 genera have more than 100 species. However, 138 genera are monotypic, which account for 22% of all genera, but only for 1.1% of all species.[7]

Molecular studies have demonstrated the phylogenetic placement of Rubiaceae within the order Gentianales and the monophyly of the family is confirmed.[40][41] The relationships of the three subfamilies of Rubiaceae together with the tribes Coptosapelteae and Luculieae are shown in the phylogenetic tree below. The placement of these two groups relative to the three subfamilies has not been fully resolved.[41]

The fossil history of the Rubiaceae goes back at least as far as the Eocene. The geographic distribution of these fossils, coupled with the fact that they represent all three subfamilies, is indicative of an earlier origin for the family, probably in the Late Cretaceous or Paleocene. Although fossils dating back to the Cretaceous and Palaeocene have been referred to the family by various authors, none of these fossils has been confirmed as belonging to the Rubiaceae.[42]

The oldest confirmed fossils, which are fruits that strongly resemble those of the genus Emmenopterys, were found in the Washington and are 48–49 million years old. A fossil infructescence and fruit found in 44 million-year-old strata in Oregon was assigned to Emmenopterys dilcheri, an extinct species. The next-oldest fossils date to the Late Eocene and include Canthium from Australia, Faramea from Panama, Guettarda from New Caledonia, and Paleorubiaceophyllum, an extinct genus from the southeastern United States.[42]

Fossil Rubiaceae are known from three regions in the Eocene (North America north of Mexico, Mexico-Central America-Caribbean, and Southeast Pacific-Asia). In the Oligocene, they are found in these three regions plus Africa. In the Miocene, they are found in these four regions plus South America and Europe.[42]

No staple foods are found in the Rubiaceae, but some species are consumed locally and fruits may be used as famine food. Examples are African medlar fruits (e.g. V. infausta, V. madagascariensis), African peach (Nauclea latifolia), and noni (Morinda citrifolia).

The most economically important member of the family is the genus Coffea used in the production of coffee. Coffea includes 124 species, but only three species are cultivated for coffee production: C. arabica, C. canephora, and C. liberica.[7]

The bark of trees in the genus Cinchona is the source of a variety of alkaloids, the most familiar of which is quinine, one of the first agents effective in treating malaria. Woodruff (Galium odoratum) is a small herbaceous perennial that contains coumarin, a natural precursor of warfarin, and the South American plant Carapichea ipecacuanha is the source of the emetic ipecac. Psychotria viridis is frequently used as a source of dimethyltryptamine in the preparation of ayahuasca, a psychoactive decoction.[43] The bark of the species Breonadia salicina have been used in traditional African medicine for many years.[44] The leaves of the Kratom plant (Mitragyna speciosa) contain a variety of alkaloids, including several psychoactive alkaloids and is traditionally prepared and consumed in Southeast Asia, where it has been known to exhibit both painkilling and stimulant qualities, behaving as a μ-opioid receptor agonist, and often being used in traditional Thai medicine in a similar way to and often as a replacement for opioid painkillers like morphine.

Originally from China, the common gardenia (Gardenia jasminoides) is a widely grown garden plant and flower in frost-free climates worldwide. Several other species from the genus are also seen in horticulture. The genus Ixora contains plants cultivated in warmer-climate gardens; the most commonly grown species, Ixora coccinea, is frequently used for pretty red-flowering hedges. Mussaenda cultivars with enlarged, colored calyx lobes are shrubs with the aspect of Hydrangea; they are mainly cultivated in tropical Asia. The New Zealand native Coprosma repens is a commonly used plant for hedges. The South African Rothmannia globosa is seen as a specimen tree in horticulture. Nertera granadensis is a well-known house plant cultivated for its conspicuous orange berries. Other ornamental plants include Mitchella, Morinda, Pentas, and Rubia.

Rose madder, the crushed root of Rubia tinctorum, yields a red dye, and the tropical Morinda citrifolia yields a yellow dye.