Saxifragales

The Saxifragales (saxifrages) are an order of flowering plants (Angiosperms). They are an extremely diverse group of plants which include trees, shrubs, perennial herbs, succulent and aquatic plants. The degree of diversity in terms of vegetative and floral features makes it difficult to define common features that unify the order.
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 consist 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 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 (late Cretaceous) time, about 90 million years ago (Myr). However, molecular studies suggest an earlier origin in the early Cretaceous (102–108 Myr) with rapid early diversification to more modern forms.
The order Saxifragales consists of 15 families, about 100 genera and 2,470 species. Of the 15 families, many are small, with 8 having only a single genus, the largest family being the Crassulaceae (stonecrops) with about 35 genera. Saxifragales are found worldwide, though rarely in the tropics, and in a wide variety of habitats from desert to aquatic. They also have a wide variety of uses, from timber to foodstuffs and ornamental plants. Apart from ornamentals, the major economically important group is the Grossulariaceae (currants and gooseberries), particularly blackcurrant.
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.
With 15 families, about 100 genera and about 2,470 species, Saxifragales is a relatively small angiosperm order.
History.
Saxifragales was first described in 1820 by Berchtold and Presl in 1820 as a group of plants, Saxifrageae, with five genera, including "Saxifraga", and therefore bear 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 112–120 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 with the order Saxifragales: 
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.
In the clade Haloragaceae "sensu lato" "(s.l.)" + Crassulaceae the genera constituting Haloragaceae "s.l." are all small, and APG II (2003) proposed merging them into a single larger Haloragaceae "s.l.", but transferred "Aphanopetalum" from Cunoniaceae to this group. The Saxifragaceae alliance represents Saxifragaceae together with a number of woody members of the traditional Saxifragaceae "sensu" Engler (1930). Within this, APG II (2003) proposed placing the two species of "Pterostemon" that constitute Pterostemonaceae within Iteaceae, and all subsequent versions have maintained this practice. Thus Saxifragales "sensu" APG II consisted of only 10 families. The third version (2009) added Peridiscaceae (from Malpighiales), as sister to all other families, but re-expanded Haloragaceae to provide for a narrower circumscription, Haloragaceae "sensu stricto" ("s.s."), to give a total of 14 families. APG IV (2016) added the parasitic family Cynomoriaceae to provide a total of 15 families, although its placement within the order remained unclear.
Of the 15 families included in APG IV, the basal divergence Peridiscaceae underwent radical shifting and recircumscription from 2003 to 2009. Originally, it consisted of two closely related genera, "Peridiscus" and "Whittonia". The APG II system placed the family in Malpighiales, based on a DNA sequence for the "rbcL" gene from "Whittonia". This sequence turned out to be not from "Whittonia", but from other plants whose DNA had contaminated the sample. After placement in Saxifragales, it was expanded to include "Soyauxia" in 2007, and "Medusandra" in 2009.
In the first of the subclades of the remaining Saxifragales, Paeoniaceae possesses many unique features and its taxonomic position was controversial for a long time, and "Paeonia" was placed in Ranunculales, close to "Glaucidium", prior to transfer to Saxifragales as sister to the woody clade.
In the woody clade, the genus "Liquidamber" was included in Hamamelidaceae until molecular phylogenetic studies showed that its inclusion might make Hamamelidaceae paraphyletic, and was segregated as a separate monotypic family, Altingiaceae in 2008. Cercidiphyllaceae was for a long time associated with Hamamelidaceae and Trochodendraceae and was often thought to be closer to the latter, which is now in the basal eudicot order Trochodendrales. "Daphniphyllum" was always thought to have an anomalous combination of characters and was placed in several different orders before molecular phylogenetic analysis showed it to belong to Saxifragales.
In the core Saxifragales, Crassulaceae and Tetracarpaeaceae have been associated with Saxifragaceae, while "Penthorum" has been associated both with Crassulaceae and Saxifragaceae, before being placed here. "Aphanopetalum" was often placed in Cunoniaceae, a family in Oxalidales, even though there were good reasons to put it in Saxifragales, and it was subsequently transferred. Haloragaceae was included in Myrtales, before being placed in Saxifragales.
The other "core" group, the Saxifragaceae alliance comprises four families: Pterostemonaceae, Iteaceae, Grossulariaceae, and Saxifragaceae, which have long been known to be related to each other, but the circumscription of Saxifragaceae has been much reduced and Pterostemonaceae submerged as "Pterostemon" in Iteaceae.
Most of the families are monogeneric. "Choristylis" is now considered a synonym of Itea, but the addition of "Pterostemon", gives Iteaceae two genera. "Liquidambar" and "Semiliquidambar" are also submerged into "Altingia", making Altingiaceae monogeneric. About 95% of the species are in five families: Crassulaceae (1400), Saxifragaceae (500), Grossulariaceae (150–200), Haloragaceae (150), and Hamamelidaceae (100).
The relationships of the Saxifragales families to each other is shown in the following cladogram. The phylogeny in this cladogram still has some uncertainty as to the exact relationships, and the phylogenetic tree is subject to further revision. Cynomoriaceae, previously placed in Santales or Rosales is included in Saxifragales, but unplaced within it. Li et al. (2019) have slightly different relationships, and also place Cynomoriaceae as the first branch in the Crassulaceae+Haloragaceae "s.l." tree, i.e. as sister to those two families. The number of genera in each family is shown in parentheses:
Distribution and habitat.
Saxifragales are found worldwide, though primarily in temperate zones and rarely in the tropics. They occupy a wide variety of habitats from arid desert (Crassulaceae) to aquatic conditions (Haloragaceae), with 6 families, including North American species, that are obligate aquatic (fully dependent on an aquatic environment), and including forests, grasslands and tundra. Saxifragales exceeds all other comparably sized clades in terms of diversity of habitats. Most of the diversity occurs in temperate (including montane and arid) conditions that expanded globally during cooling and drying trends in the last 15 My.
The most common habitats are forests and cliffs, with about 300 species occupying each, but with forests being the most diverse phenotypically, where nearly all families are represented. In contrast desert and tundra, with only two families each, contain only about 10% of species. About 90% of species can be assigned to a single habitat.
Conservation.
"Whittonia" (Peridiscaceae) is thought to be extinct. the IUCN lists 9 critically endangered, 12 endangered, 19 vulnerable and 7 near threatened species. Among the most threatened Saxifragales are "Aichryson dumosum" and "Monanthes wildpretii" (Crassulaceae), "Haloragis stokesii" and "Myriophyllum axilliflorum" (Haloragaceae), "Ribes malvifolium" and "R. sardoum" (Grossulariaceae), "Saxifraga artvinensis" (Saxifragaceae) and "Molinadendron hondurense" (Hamamelidaceae).
Uses.
Plants in the order Saxifragales have found a wide variety of uses, including traditional medicines, ornamental, household, aquarium, pond and garden plants, spices, foodstuffs (fruit and greens), dyestuffs, smoking, resin, timber and roof coverings (see Families).
Cultivation.
A number of Saxifragales genera are commercially cultivated. "Paeonia" are cultivated both as ornamental shrubs (generally sold as root stock) and for cut flowers, with the Netherlands representing the largest production, other more minor producers are Israel, New Zealand, Chile and the United States. "Liquidamber" is used for hardwood, with the American Sweetgum ("Liquidambar styraciflua") being among the most important sources of commercial hardwood in the Southeast United States, with one of its uses being veneer for plywood. "Hamamelis" is cultivated in New England for distilleries extracting witch-hazel, widely used in skincare, and is the largest source of this medicament in the world. Among the Crassulaceae, economic importance is limited to horticulture, with many species and cultivars important as ornamentals, including "Crassula ovata" (jade plant) and "Jovibarba" (hen and chicken). "Hylotelphium", "Phedimus", "Sedum" and "Sempervivum" are cultivated for rock gardens and for "green roofs". In particular, cultivars of the Madagascan "Kalanchoe blossfeldiana", e.g. 'Florists kalanchoe' have achieved commercial success throughout the world, being popular Christmas decorative plants. The Haloragaceae aquatic genus "Myriophyllum" and the closely related "Proserpinaca" are cultivated for the commercial aquarium trade. "Myriophyllum" is also economically important for purification of water and as feed for pigs, ducks, and fish, and polishing wood. 
A number of "Ribes" (Grossulariaceae) are in commercial production, concentrated in Europe and the USSR from species native to those areas. "R. nigrum" (blackcurrant) was first cultivated in monastery gardens in Russia in the 11th century, and currant cultivation more generally later in Western Europe, "R. uva-crispa" (gooseberry) production began around 1700. The first colonists in N America began cultivating currants in the late 1700s. "R. nigrum" is the most important commercial currant crop, being produced in more than 23 countries, with the major centres being Russia (more than 63 thousand hectares), Poland, Germany, Scandinavia and the UK. An important source of Vitamin C, black currants are used in the manufacture of jam, fruit jelly, compote, syrup, juice and other drinks, including the cordial Ribena and the liqueur Cassis. Other commercial crops include "R. rubrum" (red currant). World "Ribes" crop production was over 750,000 tons in 2002, of which about 150,000 tons were gooseberries, and the largest group blackcurrants.