Of the 15 families, many are small, with eight of them beingmonotypic (having only a single genus). The largest family is theCrassulaceae (stonecrops), a diverse group of mostlysucculent plants, with about 35 genera. Saxifragales are found worldwide, primarily intemperate tosubtropical zones, rarely being encountered growing wild in thetropics; however, many species are nowcultivated throughout the world as knowledge of plant husbandry has improved. They can be found in a wide variety of environments, fromdeserts to fullyaquatichabitats, with species adapted toalpine, forested or fully-aquatic habitats. Many areepiphytic orlithophytic, 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 fromtextiles andtimber 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 asornamental plants. Apart from ornamentals, another highly-prized group are theGrossulariaceae (currants andgooseberries), particularlyblackcurrants,redcurrants andwhite currants.
Overall, the order is extremelydiverse, encompassing numeroustrees,shrubs,perennial herbs andsucculent plants, as well asaquatic andsemi-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 theAngiosperm Phylogeny Group classification system, the Saxifragales are placed within the majordivision of flowering plants referred to aseudicots, specifically thecore eudicots. This subgroup consists of theDilleniaceae,superasterids andsuperrosids. The superrosids, in turn, have two components,rosids and Saxifragales. The Saxifragales order has undergone considerable revision since its originalclassification, which had been based purely onplant characteristics. The modern classification is based on genetic studies, usingmolecular phylogenetics. There is an extensivefossil record from theTuronian-Campanian phase of the lateCretaceous, 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.
This degree of diversity makes definingsynapomorphy (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 includeflowers that are usuallyradially symmetric andpetals that are free. Thegynoecium (female reproductive part) generally consists of twocarpels (ovary, style and stigma) that are free, at least toward the apex (partially fused bicarpellate gynoecium) and possess ahypanthium (cup shaped basal floral tube). In theandroecium (male reproductive part), the stamen anthers are generally basifixed (attached at its base to the filament), sometimes dorsifixed (attached at centre) (seeCarlsward et al (2011) Figure 2). Other commonly occurring features arefruit that is generallyfollicular (formed from a single carpel),seeds with abundantendosperm surrounding theembryo andleaves with glandularteeth at their margins (glandular dentate,seeimage). Within the Saxifragales, while the families of the woody clade are primarily woody, the primarilyherbaceous families of Crassulaceae and Saxifragaceae exhibit woody features as a secondary transition.[5][6][7]
Saxifragales was first described in 1820 byBerchtold and Presl as a group of plants, Saxifrageae, with five genera, includingSaxifraga, lending their names as thebotanical authority (Bercht. & J.Presl).[8] At times, that authority has also been given toDumortier, due to a later publication (1829). Dumortier first used the word Saxifragaceae.[9] By the time ofJohn Lindley'sThe Vegetable Kingdom (1853), the term Saxifragales was in use, which Lindley called an Alliance, containing five families.[10] Later, the Saxifragales were placed in theangiospermclassDicotyledons, also calledMagnoliopsida.[11]
In the initial APG publication (1998), the Saxifragales were identified within thecore eudicotsclade but its relationship to other clades was uncertain. The core eudicots consist of the orderGunnerales and a large clade ofPentapetalae (so named for having asynapomorphy ofpentamerous (5 part) perianths), the latter representing about 70% of all angiosperms, with eight major lineages.[14][15] 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.[16][3] This was eventually resolved in the third APG system (2009), placing Saxifragales as asister group to therosids (Rosidae), within the Pentapetalae clade.[17][18][19] This large combination has subsequently been given the namesuperrosids (Superrosidae), representing part of an early diversification of theangiosperms.[3][1][20] Among the rosids, they share a number of similarities with theRosales, particularlyRosaceae, including a hypanthium, five part flowers and free floral parts.[21] As circumscribed, Saxifragales account for 1.3% of eudicot diversity.[22]
Cladogram of Saxifragales relationships among core eudicots[1][12][23]
Diversification among Saxifragales was rapid, with the extensivefossil record[24][25][26][27][28][29] indicating that the order was morediverse and morewidespread than an examination of theextant members suggests, with considerablephenotypic diversity occurring early.[2] The earliest fossil evidence is found in theTuronian-Campanian (late Cretaceous), suggesting a minimum age of 89.5 Myr. However, moleculardivergence time estimation suggest an earlier time of 102–108 Myr, into the early Cretaceous, for thecrown andstem 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.[30][3][31]
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 Haloragaceaes.l. remaining woody), while other taxa reverted to a woody habit, especially Crassulaceae. Most of Saxifragales have a superiorovary, 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 ancestralcarpel number is two, with transition to higher numbers, such as four in Haloragaceaes.l. and Peridiscaceae with five in Penthoraceae. The ancestral carpel number for Crassulaceae is five, decreasing to four inKalanchoe, where it is synapomorphic for the genus, though the most frequent transition in this family is 6–10, but only wherestamen number is increased above five. SomeMacaronesian taxa (Aeonieae) have 8–12, with up to 32 carpels forAeonium.[3]
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 andAltingia 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 (butCrassula 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.[3] The ancestral habitat appears to be forests, followed by early diversification into desert and aquatic habitats, with shrubland the most recent colonization.[2]
Species diversification was rapid following a transition from a warmer, wetter Earth in theEocene (56–40 Myr) to earlyMiocene (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.[32]
This was subsequently revised to 15, in the fourth version (2016).[1] The Saxifragales families have been grouped into a number of informally named suprafamilial subclades, with the exception of thebasal split of Peridiscaceae, which thus forms asister 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, (Haloragaceaesensu lato + Crassulaceae) and the Saxifragaceae alliance.[3]
In the clade Haloragaceaesensu lato(s.l.) + Crassulaceae the genera constituting Haloragaceaes.l. are all small, and APG II (2003) proposed merging them into a single larger Haloragaceaes.l., but transferredAphanopetalum fromCunoniaceae to this group.[16] The Saxifragaceae alliance represents Saxifragaceae together with a number of woody members of the traditional Saxifragaceaesensu Engler (1930).[34] Within this, APG II (2003) proposed placing the two species ofPterostemon that constitute Pterostemonaceae withinIteaceae, and all subsequent versions have maintained this practice.[16] Thus Saxifragalessensu APG II consisted of only 10 families. The third version (2009) addedPeridiscaceae (fromMalpighiales), as sister to all other families, but re-expanded Haloragaceae to provide for a narrower circumscription, Haloragaceaesensu 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.[35][1]
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 andWhittonia. TheAPG II system placed the family inMalpighiales, based on aDNA sequence for therbcLgene fromWhittonia. This sequence turned out to be not fromWhittonia, but from other plants whoseDNA had contaminated the sample.[36] After placement in Saxifragales, it was expanded to includeSoyauxia in 2007,[37] andMedusandra in 2009.[38]
In the first of the subclades of the remaining Saxifragales, Paeoniaceae possesses manyunique features and its taxonomic position was controversial for a long time,[39] andPaeonia was placed inRanunculales, close toGlaucidium,[40][41] prior to transfer to Saxifragales as sister to the woody clade.[30][42]
In the woody clade, the genusLiquidambar was included in Hamamelidaceae untilmolecular phylogenetic studies showed that its inclusion might make Hamamelidaceaeparaphyletic, and was segregated as a separate monotypic family, Altingiaceae in 2008.[30] Cercidiphyllaceae was for a long time associated with Hamamelidaceae andTrochodendraceae and was often thought to be closer to the latter,[43] which is now in the basaleudicot orderTrochodendrales.[44]Daphniphyllum was always thought to have an anomalous combination of characters[45][45] and was placed in several different orders before molecular phylogenetic analysis showed it to belong to Saxifragales.[46]
In the core Saxifragales, Crassulaceae[47] and Tetracarpaeaceae[48] have been associated with Saxifragaceae, whilePenthorum has been associated both with Crassulaceae and Saxifragaceae,[49] before being placed here.Aphanopetalum was often placed inCunoniaceae, a family inOxalidales, even though there were good reasons to put it in Saxifragales,[50] and it was subsequently transferred.[51] Haloragaceae was included inMyrtales,[52] before being placed in Saxifragales.[53]
The other "core" group, the Saxifragaceae alliance comprises four families: Pterostemonaceae, Iteaceae, Grossulariaceae, and Saxifragaceae,[30] which have long been known to be related to each other, but thecircumscription of Saxifragaceae has been much reduced and Pterostemonaceae submerged asPterostemon in Iteaceae.[54]
The relationships of the Saxifragales families to each other is shown in the followingcladogram. Thephylogeny in this cladogram still has some uncertainty as to the exact relationships, and the phylogenetic tree is subject to further revision.[59][60]Cynomoriaceae, previously placed inSantales orRosales 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+Haloragaceaes.l. tree, i.e. as sister to those two families.[31] The number of genera in each family is shown in parentheses:
100%maximum likelihoodbootstrap support except where labeled with bootstrap percentage Monogeneric families are represented by genus names, otherwise the number of genera is in (parentheses) Cynomorium (Cynomoriaceae) remains unplaced within this tree
The Peridiscaceae (Ringflower family) are a small tropical family of 4 genera and 11–12 species of small trees and shrubs found in theGuiana Shield of S America (2 genera, one of which,Whittonia, is thought to beextinct) and West and Central Africa (2 genera). The majority of species occur in the African genusSoyauxia. The name comes from theGreek,peri (around)discos (ring).[6][61][21]
The Paeoniaceae (Peony family) consist of a single genus (Paeonia) with about 33 species of perennial herbs and small shrubs with showy flowers, found from the Mediterranean to Japan, but two species occur in western N America. They are commercially important as popular garden ornamentals, cultivated since antiquity, and have been used medicinally. The herbaceous varieties are derived fromP. lactiflora, while the shrubs are derived fromP. suffruticosa (tree peony), both Asian species. The botanical name comes from its Greek name,paionia, named in turn for the GodPan.[6][61][21]
The Altingiaceae (Sweetgum family) consist of a single genus (Liquidambar) with 15 species of trees with unisexual flowers found in Eurasia, but with one species in North and Central America,Liquidambar styraciflua (American sweetgum).Liquidambar is used for itsresin and timber, as well being ornamental trees. The nominative genus and family are named afterWillem Alting, and Liquidambar for liquidambar, Arabic for the resin.[6][61][21]
The Hamamelidaceae (Witch-hazel family) consists of trees and shrubs with a widespread distribution, but main centres in East Asia and Malaysia. They are found in wet woodlands and forested slopes. The family has 26 genera and about 80–100 species, in five subfamilies, of which the nominative, Hamamelidoideae, contains over 75% of the genera. The species have uses as medicaments, timber and ornamental plants for their flowers, such asHamamelis (witch hazel) or leaves, such asParrotia persica (Persian ironwood). The family and nominative genus is named for the Greekhamamelis, the wych elm.[61][21][6]
The Cercidiphyllaceae (Caramel-tree family) are a small family of deciduous trees found in China and Japan, with a single genus,Cercidiphyllum and two species,C. japonicum andC. magnificum. The trees are valued for their wood (katsura) and as ornamentals.C. japonicum is the largest deciduous tree in Japan. The name is derived from the Greek wordskerkis (poplar) andfyllon (leaf), from a supposed similarity in leaves.[61][21]
The Daphniphyllaceae (Laurel-leaf family) consist of a single genus,Daphniphyllum, with about 30 species. They are evergreen unisexual trees and shrubs distributed in SE Asia and the Solomon Islands. The dried leaves ofDaphniphyllum macropodum[a] have been used for smoking in Japan and Siberia. The name is derived from the Greek wordsdafne (laurel) andfyllon (leaf), from a supposed resemblance to the leaves of the former (Laurus nobilis).[61][21]
The Crassulaceae (Orpine and Stonecrop family) are a medium size diverse and cosmopolitan family, that form the largest family within Saxifragales. They are mainlysucculent, rarely aquatic, with a specialised form ofphotosynthesis (Crassulacean Acid Metabolism). Genera vary from 7 to 35, depending on the circumscription of the large genusSedum, and there are about 1,400 species. Uses are diverse, including spices, medicaments and roof coverings as well as ornamentalrock garden and household plants such as the S AfricanCrassula ovata, the jade or money plant. The name is derived from the Latin,crassus (thick), referring to the fleshy leaves.[61][21][6]
The Aphanopetalaceae (Gum-vine family) consists of a single genus of Australian climbing shrubs,Aphanopetalum, which has two species,A. clematidium (SW Australia) andA. resinosum (Queensland, NSW). The name is derived from the Greek wordsafanos (inconspicuous) andpetalon (petal).[61][21]
The Tetracarpaeaceae (Delicate-laurel family) is a very small evergreen Australian shrub family with a single genus,Tetracarpaea and a single species,T. tasmannica, confined to subalpine Tasmania. The name is derived from the Greek wordstetra (four) andcarpos (fruit), referring to the ovaries which have four carpels.[61][21][6]
The Penthoraceae (Ditch-stonecrop family) is a very small family of rhizomatous perennial herbs found in eastern N America and E Asia, in mainly wet environments. It consists of a single genus,Penthorum with two species,P. sedoides in N America andP. chinense from Siberia to Thailand.P. sedoides is used in aquaria and water gardens.[62] The name is derived from the Greek wordpente (five) referring to the five-part fruit.[61][21][6]
The Haloragaceae (Water-milfoil family) is a small family of trees, shrubs, perennial, annual terrestrial, marsh and aquatic herbs with global distribution, but especially Australia. It consists of 9–11 genera and about 145 species. The largest genus isGonocarpus with about 40 species. The major horticultural genus isMyriophyllum (watermilfoil) whose species are valued as aquaria and pond plants but may escape and naturalise, becoming invasive. Some cultivars ofHaloragis are valued as ornamentals.[62] Only one genus,Haloragodendron, is a shrub and is confined to S Australia. The family and nominative genus,Haloragis are named from the Greek wordshalas (salt) andrhoges (berries).[61][21][6]
The Iteaceae (Sweetspire family) is a widespread small family of trees and shrubs, with 2 genera, and 18–21 species, found in tropical to northern temperate regions. The larger genus,Itea (c. 16 spp.) is more widespread, from the Himalayas to Japan and westernMalesia and one species in eastern N America (I. virginica) whereasPterostemon (c. 2 spp) is confined toOaxaca, Mexico.I. virginica andI. ilicifolia, from China, are valued as ornamental shrubs. The name is derived from the Greek worditea (willow) for its rapid growth and similar leaf form.[61][21][6]
The Grossulariaceae (Gooseberry family) are shrubs that are usually deciduous. The single genus,Ribes, has about 150 species that are commercially important and widely cultivated for their fruit and also grown as ornamentals, such asR. uva-crispa (gooseberry) andR. nigrum (blackcurrant). They are found in temperate northern hemisphere regions but extending through the Andes into S America. The family name is derived from the Latin wordgrossulus (an unripe fig), andRibes is Latinised from thesemitic wordribas (acid taste).[61][21][6]
The Saxifragaceae (Saxifrage family) are mainly perennial herbs distributed throughout the Northern Hemisphere and Andes, and New Guinea, in damp woodlands and cooler northern regions, rarely aquatic, but are adapted to a wide range of moisture conditions. The family, greatly reduced, includes 35 genera and about 640 species, in two lineages, saxifragoids (e.g.Saxifraga, rockfoil) and heucheroids (e.g.Heuchera, coral bells). The largest genus isSaxifraga, the type genus (370 species), though several genera are monotypic. Saxifragaceae are the most horticulturally important of the herbaceous Saxifragales. They provide foodstuffs and medicaments and include many ornamentals, particularly of border, rock and woodland gardens, such asAstilbe, though the largest number of cultivated species belong toSaxifraga. The family and type genus name are derived from the two Latin wordssaxum (rock), andfrango (to break), but the exact origin is unknown, although surmised to be either because of the ability ofSaxifraga to grow in crevices in rocks or medicinal use forkidney stones.[61][21][6]
The Cynomoriaceae (Tarthuth or Maltese Mushroom family) consists of a single genus,Cynomorium with one or two species,C. coccineum (Mediterranean basin) andC. songaricum (central Asia and China; sometimes treated as a variety ofC. coccineum). They are perennial bisexual herbaceous parasitic plants lacking chlorophyll, from deserts and arid regions. They have been harvested for food, as a dye and in traditional medicine. The name is derived from two Greek wordskynos (dog), andmorion (penis), for its shape.[61][21]
Saxifragales are found worldwide,[6] though primarily in temperate zones and rarely in the tropics.[61] 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),[63] and including forests, grasslands and tundra. Saxifragales exceeds all other comparably sized clades in terms of diversity of habitats.[2] 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.[32]
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.[2]
A number of Saxifragales genera are commercially cultivated.[61]Paeonia are cultivated both as ornamental shrubs (generally sold asroot stock) and forcut flowers, with the Netherlands representing the largest production, other more minor producers are Israel, New Zealand, Chile and the United States.[65]Liquidambar is used for hardwood, with the American Sweetgum (Liquidambar styraciflua) being among the most important sources of commercialhardwood in the Southeast United States, with one of its uses beingveneer forplywood.[66]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.[67] Among the Crassulaceae, economic importance is limited tohorticulture, with many species and cultivars important as ornamentals, includingCrassula ovata (jade plant) andJovibarba (hen and chicken).Hylotelphium,Phedimus,Sedum andSempervivum are cultivated forrock gardens and for "green roofs".[68][47] In particular, cultivars of the MadagascanKalanchoe blossfeldiana, e.g. 'Florists kalanchoe' have achieved commercial success throughout the world, being popular Christmas decorative plants.[69][70] The Haloragaceae aquatic genusMyriophyllum and the closely relatedProserpinaca are cultivated for the commercialaquarium trade.[71]Myriophyllum is also economically important for purification of water and as feed for pigs, ducks, and fish, and polishing wood.[72]
Blackcurrant crops, UK
A number ofRibes (Grossulariaceae) are in commercial production, concentrated in Europe and the USSR from species native to those areas.R. nigrum (blackcurrant) was first cultivated inmonastery 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 North 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 thousandhectares), Poland, Germany, Scandinavia and the UK.[73] An important source ofVitamin C, black currants are used in the manufacture of jam, fruit jelly, compote, syrup, juice and other drinks, including thecordialRibena and theliqueurCassis. Other commercial crops includeR. rubrum (red currant).[74][75] WorldRibes crop production was over 750,000 tons in 2002, of which about 150,000 tons were gooseberries, and the largest group blackcurrants.[76]
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.[61]
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