Saxifragales is an order of flowering plants in the superrosid clade of the eudicots. It contains 15 families and around 100 genera, with nearly 2,500 species. Well-known and economically important members of this order include saxifrages (after which the order is named), blackcurrants, redcurrants, gooseberries, peonies, liquidambars, witch-hazel, Persian ironwood, katsura, jade plant, houseleeks, and water milfoil.
Of the 15 families, many are small, with eight of them being monotypic (having only a single genus). The largest family is the Crassulaceae (stonecrops), a diverse group of mostly succulent plants, with about 35 genera. Saxifragales are found worldwide, primarily in temperate to subtropical zones, rarely being encountered growing wild in the tropics; however, many species are now cultivated throughout the world as knowledge of plant husbandry has improved. They can be found in a wide variety of environments, from deserts to fully aquatic habitats, with species adapted to alpine, forested or fully-aquatic habitats. Many are epiphytic or lithophytic, growing on exposed cliff faces, on trees or on rocks, and not requiring a highly organic or nutrient-dense substrate to thrive.
Globally, the saxifrages have a wide variety of uses by humans, ranging from textiles and timber to foodstuffs. Several families—such as the aforementioned Crassulaceae—and genera are of significant commercial importance in some countries and economies, being cultivated on a large scale for sale as ornamental plants. Apart from ornamentals, another highly prized group are the Grossulariaceae (currants and gooseberries), particularly blackcurrants, redcurrants and white currants.
Overall, the order is extremely diverse, encompassing numerous trees, shrubs, perennial herbs and succulent plants, as well as aquatic and semi-aquatic species. The order's high degree of diversity, in terms of vegetative and reproductive traits (and sheer amount of species), can make it challenging to find any common or unifying features amongst the respective genera.
In the Angiosperm Phylogeny Group classification system, the Saxifragales are placed within the major division of flowering plants referred to as eudicots, specifically the core eudicots. This subgroup consists of the Dilleniaceae, superasterids and superrosids. The superrosids, in turn, have two components, rosids and Saxifragales. The Saxifragales order has undergone considerable revision since its original classification, which had been based purely on plant characteristics. The modern classification is based on genetic studies, using molecular phylogenetics. There is an extensive fossil record from the Turonian-Campanian phase of the late Cretaceous, dating to about 90 million years ago (Myr). However, molecular studies may suggest an older origin, from the early Cretaceous (102–108 Myr), with rapid and early diversification to more modern forms.
Description
The order Saxifragales is extremely morphologically diverse (hyper-diverse). It includes trees (e.g. witch hazel, witch alder in Hamamelidaceae), fruit bearing shrubs (e.g. currants, gooseberries in Grossulariaceae), lianas, annual and perennial herbs, rock garden plants (e.g. saxifrage in Saxifragaceae), ornamental garden plants (e.g. peonies in Paeoniaceae), succulents (e.g. stonecrop in Crassulaceae) and aquatics (e.g. watermilfoil in Haloragaceae). The flowers demonstrate major variations in sepal, petal, stamen, and carpel number, as well as ovary position (see Biogeography and evolution).
This degree of diversity makes defining synapomorphy (derived common characteristics) for the group extremely difficult, the order being defined on the basis of molecular affinity rather than morphology. However, some characteristics that are prevalent (common traits) represent potential or putative synapomorphies based on ancestral states. These include flowers that are usually radially symmetric and petals that are free. The gynoecium (female reproductive part) generally consists of two carpels (ovary, style and stigma) that are free, at least toward the apex (partially fused bicarpellate gynoecium) and possess a hypanthium (cup shaped basal floral tube). In the androecium (male reproductive part), the stamen anthers are generally basifixed (attached at its base to the filament), sometimes dorsifixed (attached at centre) (see Figure 2). Other commonly occurring features are fruit that is generally follicular (formed from a single carpel), seeds with abundant endosperm surrounding the embryo and leaves with glandular teeth at their margins (glandular dentate, see image). Within the Saxifragales, while the families of the woody clade are primarily woody, the primarily herbaceous families of Crassulaceae and Saxifragaceae exhibit woody features as a secondary transition.
Taxonomy
Saxifragales is a relatively small angiosperm order, having only 15 families, about 100 genera and about 2,470 species.
History
Saxifragales was first described in 1820 by Berchtold and Presl as a group of plants, Saxifrageae, with five genera, including Saxifraga, lending their names as the botanical authority (Bercht. & J.Presl). At times, that authority has also been given to Dumortier, due to a later publication (1829). Dumortier first used the word Saxifragaceae. By the time of John Lindley's The Vegetable Kingdom (1853), the term Saxifragales was in use, which Lindley called an Alliance, containing five families. Later, the Saxifragales were placed in the angiosperm class Dicotyledons, also called Magnoliopsida.
Phylogeny
The order Saxifragales has undergone considerable revision in both placement and composition, since the use of molecular phylogenetics, and the use of the modern Angiosperm Phylogeny Group (APG) classification. They are identified as a strongly monophyletic group.
In the initial APG publication (1998), the Saxifragales were identified within the core eudicots clade but its relationship to other clades was uncertain. The core eudicots consist of the order Gunnerales and a large clade of Pentapetalae (so named for having a synapomorphy of pentamerous (5 part) perianths), the latter representing about 70% of all angiosperms, with eight major lineages. Later (2003), the order was described as "one of the major surprises of molecular phylogenetic analyses of the angiosperms", having elements previously placed in three or four separate subclasses based on morphology. This was eventually resolved in the third APG system (2009), placing Saxifragales as a sister group to the rosids (Rosidae), within the Pentapetalae clade. This large combination has subsequently been given the name superrosids (Superrosidae), representing part of an early diversification of the angiosperms. Among the rosids, they share a number of similarities with the Rosales, particularly Rosaceae, including a hypanthium, five part flowers and free floral parts. As circumscribed, Saxifragales account for 1.3% of eudicot diversity.
Biogeography and evolution
Diversification among Saxifragales was rapid, with the extensive fossil record indicating that the order was more diverse and more widespread than an examination of the extant members suggests, with considerable phenotypic diversity occurring early. The earliest fossil evidence is found in the Turonian-Campanian (late Cretaceous), suggesting a minimum age of 89.5 Myr. However, molecular divergence time estimation suggest an earlier time of 102–108 Myr, into the early Cretaceous, for the crown and stem groups respectively. Within the order Saxifragales, the molecular data imply a very rapid initial diversification time of about 6–8 Myr, between 112 and 120 Myr, with major lineages appearing within 3–6 Myr.
The ancestral state appears to be woody, as in Peridiscaceae and the woody clade, but is also ancestral to Grossulariaceae. A number of independent transitions to a herbaceous habit occurred in the ancestors of Crassulaceae, Saxifragaceae and the base of the Haloragaceae-Penthoraceae clade (the other two families in Haloragaceae s.l. remaining woody), while other taxa reverted to a woody habit, especially Crassulaceae. Most of Saxifragales have a superior ovary, but some families show frequent transition with inferior or subinferior position, particularly Saxifragaceae and to a lesser extent Hamamelidaceae. Almost all Grossulariaceae have an inferior ovary. The ancestral carpel number is two, with transition to higher numbers, such as four in Haloragaceae s.l. and Peridiscaceae with five in Penthoraceae. The ancestral carpel number for Crassulaceae is five, decreasing to four in Kalanchoe, where it is synapomorphic for the genus, though the most frequent transition in this family is 6–10, but only where stamen number is increased above five. Some Macaronesian taxa (Aeonieae) have 8–12, with up to 32 carpels for Aeonium.
The ancestral petal number is five, with three major transitions; 5 to 0, 5 to 4, 5 to 6–10. Increased petal number is seen in Paeoniaceae and Crassulaceae, particularly where stamen number is also increased. Cercidiphyllum + Daphniphyllum, Chrysosplenium and Altingia are examples of the complete loss of petals. The ancestral stamen:petal ratio is 1, with transitions characterising several clades, e.g. Paeonicaceae+woody clade >2, Crassulaceae 2 (but Crassula 1). Overall there has been a decrease over evolution, but independent of a decrease in petal number, so that it is the stamen number that has decreased. The ancestral habitat appears to be forests, followed by early diversification into desert and aquatic habitats, with shrubland the most recent colonization.
Species diversification was rapid following a transition from a warmer, wetter Earth in the Eocene (56–40 Myr) to early Miocene (23–16 Myr), to the cooler drier conditions of the mid-Miocene (16–12 Myr). However, this appears to not have coincided with ecological and phenotypic evolution, which are themselves correlated. There is a clear lag, whereby increase in species diversification was followed later by increases in niche and phenotypic lability.
Subdivision
The first APG classification (1998) placed 13 families within the order Saxifragales:
Altingiaceae Cercidiphyllaceae Crassulaceae Daphniphyllaceae Grossulariaceae Haloragaceae Hamamelidaceae Iteaceae Paeoniaceae Penthoraceae Pterostemonaceae Saxifragaceae Tetracarpaeaceae
This was subsequently revised to 15, in the fourth version (2016). The Saxifragales families have been grouped into a number of informally named suprafamilial subclades, with the exception of the basal split of Peridiscaceae, which thus forms a sister group with the rest of Saxifragales. The two major ones are (Paeoniaceae + the woody clade of primarily woody families) and the "core" Saxifragales (i.e. the primarily herbaceous families), with the latter subdivided into two further subclades, (Haloragaceae sensu lato + Crassulaceae) and the Saxifragaceae alliance.