Saxifragales


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, 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. The largest family is the Crassulaceae, 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, 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, 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. However, molecular studies may suggest an older origin, from the early Cretaceous, with rapid and early diversification to more modern forms.

Description

The order Saxifragales is extremely morphologically diverse. It includes trees, fruit bearing shrubs, lianas, annual and perennial herbs, rock garden plants, ornamental garden plants, succulents and aquatics. The flowers demonstrate major variations in sepal, petal, stamen, and carpel number, as well as ovary position.
This degree of diversity makes defining synapomorphy for the group extremely difficult, the order being defined on the basis of molecular affinity rather than morphology. However, some characteristics that are prevalent represent potential or putative synapomorphies based on ancestral states. These include flowers that are usually radially symmetric and petals that are free. The gynoecium generally consists of two carpels that are free, at least toward the apex and possess a hypanthium. In the androecium, the stamen anthers are generally basifixed, sometimes dorsifixed . Other commonly occurring features are fruit that is generally follicular, seeds with abundant endosperm surrounding the embryo and leaves with glandular teeth at their margins. 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. At times, that authority has also been given to Dumortier, due to a later publication. Dumortier first used the word Saxifragaceae. By the time of John Lindley's The Vegetable Kingdom, 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 classification. They are identified as a strongly monophyletic group.
In the initial APG publication, 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, the latter representing about 70% of all angiosperms, with eight major lineages. Later, 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, placing Saxifragales as a sister group to the rosids, within the Pentapetalae clade. This large combination has subsequently been given the name superrosids, 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

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, 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, 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 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. 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 to early Miocene, to the cooler drier conditions of the mid-Miocene. 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 placed 13 families within the order Saxifragales:
This was subsequently revised to 15, in the fourth version. 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 and the "core" Saxifragales, with the latter subdivided into two further subclades, and the Saxifragaceae alliance.
In the clade Haloragaceae sensu lato '''' + Crassulaceae the genera constituting Haloragaceae s.l. are all small, and APG II 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. Within this, APG II 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 added Peridiscaceae, as sister to all other families, but re-expanded Haloragaceae to provide for a narrower circumscription, Haloragaceae sensu stricto, to give a total of 14 families. APG IV 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 Liquidambar 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, Saxifragaceae , Grossulariaceae, Haloragaceae, and Hamamelidaceae.
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. 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: