Family Crassulaceae

Crassulaceae is a middle-sized family of dicots, which includes about 1400 to 1500 species classified in 35 genera. It has been suggested that this family arose in South Africa 80 million years ago. There was a heavy diversity period about 40 millions years ago. Crassulaceae encompasses three subfamilies: Crassuloideae, Kalanchoideae, and Sempervivoidae. They include genera such as Crassula, Kalanchoe, and Sedum. Plants are characterized by featuring succulent leaves and, frequently, stems and performing the CAM metabolism (CAM: "crassulacean acid metabolism").

Crassulaceae are specialized in storing water in their cells, which is why their tissues are fleshy—that is, they have succulent leaves and stems. In addition to CAM metabolism, they have vacuoles that occupy more than 90% of the cell volume, rather than 70–80%, as is the case in other plants. Their epidermis is adapted to conserve water by developing a thick, hydrophobic cuticle. Many species have developed hydathodes on their leaves. Furthermore, the leaves of Crassulaceae have a lower stomatal density.

Crasulaceae are succulent plants. Contrary to what one might think, succulent plants are not found in the driest deserts. They are abundant in semi-arid areas where there are regular, though infrequent, periods of rainfall. Although some succulents can absorb water from the atmosphere, most of their water is taken in through their roots, which are thin and shallow. Interestingly, there is one species that is aquatic: Crassula helmsii. The phenomenon of succulence is considered an example of convergent evolution. All succulent plants share the presence of very large cells that store water. However, there are additional characteristics related to ecophysiological traits. Succulence is not an all-or-nothing trait, but rather a continuum ranging from normal tissues to clearly succulent ones; in other words, there is a spectrum of succulence. Between 3 and 5 percent of flowering plants have been classified as succulents. These include the families Crassulaceae, Apocynaceae, Cactaceae, Aizoaceae, Asparagaceae, Asphodelaceae, Archidaceae, and Euphorbiaceae.

Crasulaceae are perennials; they are rarely annuals. They are mostly herbaceous, and less commonly shrubby, climbing, or tree-like; some are epiphytes, and very rarely aquatic. As we have mentioned, most of them are succulents.

Stem

The stem may be succulent, usually due to the specialization of the parenchyma and cortical or medullary collenchyma. Rhizomes or underground stems sometimes develop.

The epidermis of the stem is often unicellular in heigh, but there are also examples of multilayered epidermis.

The cortical zone of the stem is parenchyma or collenchyma, and sometimes contains chloroplasts.

Vascular components are not usually arranged in bundles, except in tree species. Bundles are observed only in the leaf rays. The xylem in the stems is not usually separated by parenchymatous rays, and its organization is typically irregular, although it is often arranged in a cylinder or takes on other shapes. It has very short vessel elements (xylem) (100–229 µm), with no morphological variations from the inside to the outside, and thickenings similar to those found during primary growth. The thickenings are annular, heliocoidal, and sometimes scale-like. The perforated plates are simple, rarely reticulate. No areolate (rimmed) pores have been detected. The phloem is poorly developed and difficult to distinguish. In any case, cambial activity is not very intense, and growth rings are not usually recognizable.

The wood consists mainly of libriform xylary sclerenchyma fibers (unseptate, with simple pores, and with relatively thin walls). The axial parenchyma is sparse.

It contains pigment cells containing anthocyanins

When secondary growth occurs, the periderm (or multiseriate epidermis) arises from the subepidermal cells of the cortex or from the epidermis itself. This periderm is composed of layers of cells with thin cell walls.

Rhizomes are usually sympodial, rarely monopodial.

Leaves

They are commly alternate and is spirals, decusate-opposite, or rarely verticiliate. They are sesil, subsesil, or not frequently petiolates, lacking stipules. Leaves are simple, rarely pinnate. Leaves are generally entire, crenate (like those of the Umbilicaceae), or lobed, simple (rarely compound), frequently grouped in basal rosettes, with highly diverse morphologies. The arrangement of leaves in more or less dense rosettes has evolved independently many times in numerous genera of the major clades (except in Umbilicus), especially within the Sempervivoideae. In some rosettes, stolons are present as a means of vegetative propagation. The rosettes may close up to form a bulbous structure during periods of drought.

Heterophily (different leaf morphologies on the same plant) has been observed in some species. The leaves are more or less flat to tapered, awl-shaped, fairly flat on top and slightly rounded on the underside, and some develop a partial keel. They are usually thick and fleshy, with a distinct waxy layer on their cuticle, which is typically thick. This waxy layer often gives many species a bluish-whitish color. The surface-to-volume ratio is lower than in other plants, which facilitates water retention. Sometimes they have long trichomes called cilia, as in Aenoium.

The leaves are bifacial, centric, or intermediate between centric and dorsiventral.

In most perennials, the stem and at least some of the leaves survive adverse conditions, such as freezing or drought. The leaves may fall off when other parts of the plant serve as storage organs.

The epidermis is usually composed of cells arranged in a single layer, sometimes two or three layers, and elongated transversely to the main axis of the leaf. Their cell walls can range from wavy to straight. The cuticle is usually smooth or has fine striations or grooves.

Stomata typically appear across the entire leaf surface (homostomatic), meaning they are found on both the upper (adaxial) and lower (abaxial) surfaces. They can be superficial or raised (in Sedum), and sometimes sunken. Stomatal density is low and typically ranges from 5–80 mm², which is similar to other succulents but lower compared to the leaves of other species. The stomata are of the asynocytic type, meaning that the accessory cells are arranged around the guard cells, usually in groups of 3, although up to 8 may be present. The accessory cells usually share a common origin with the guard cells. They are therefore called mesogenous.

The mesophyll may contain photosynthetic cells and water-storing cells (hydrenchym) or a single cell type that performs both functions. The presence of palisade parenchyma is rare, although there may be mesophyll arrangements on the adaxial side that resemble palisade parenchyma. Most leaves are thick, with transitions in the mesophyll from chlorenchyma in the peripheral zone to hydrenchyma in the central zone, where there are large parenchymatous cells without chloroplasts. Thinner leaves lack this organization, and virtually the entire mesophyll consists of chlorenchyma.

The vascular bundles are collateral. The venation of the leaves is typically less dense than in other groups of plants with non-succulent leaves. The distribution of the vascular bundles is three-dimensional and adapts to the thickness of the leaf. The venation is pinnate or palmate and camptodromous or reticulate, typically with a submarginal vein. In flat leaves, the midrib usually protrudes from the abaxial surface.

Trichomes are rare on the leaves. The petioles typically have vascular bundles arranged in a crescent shape. The tissues contain abundant tannins. Solitary druses are common.

Epithema-type hydathodes are present on the leaves of virtually all species, ranging from many to just one.

Flor

They typically have terminal inflorescences with many flowers. These are usually thyrse-type inflorescences, with terminal, semi-, di-, or monocasiose flowers. The flowers are erect on the inflorescence. They are generally pentamerous and actinomorphic. They have bracts. They are hermaphroditic, rarely unisexual, and commonly proterandrous, that is, the stamens mature before the pistil. Their flowers are generally small. They lack stipules.

The sepals are usually green and shorter than the petals, fused at the base. During flower development, the sepals develop much earlier than the petals. The petals have a very fine texture and may be free or form tubes of varying sizes. They may have a central keel. Sympetalous flowers (fused petals) are common in some groups. They are usually one or two colors—rarely three—ranging from yellow to red, white, greenish, or brown.

The stamens are arranged in 1 or 2 whorls, with a number equal to or double that of the petals. The filaments may be free or fused to the tubular corolla and are usually about 1 mm long. The anthers are basifixed (attached to the filament at the base) and contain four sporangia. The anthers have a persistent epidermis, a layer of fibrous endothecium, two intermediate layers, and a secretory, uninucleate tapetum. Pollen is usually released first from the innermost anthers, those closest to the petals.

The epidermis of the anthers lacks stomata. Dehiscence occurs through longitudinal slits. Pollen grains are typically trilobate, subspherical, and more or less triangular when viewed from the pole. They measure approximately 13 to 38 µm in length. Pollen morphology can vary even within the same inflorescence and is therefore of limited taxonomic value. Microsporogenesis is simultaneous, and pollen is released in monads. Pollen grains are binucleate, sometimes with starch inclusions.

The ovary is superior (rarely semi-inferior), with the same number of carpels as sepals or petals (isomerous with the perianth), each developing a style. The carpels appear open during some early stages of their development, but later fuse postgenitally and are plicated. The carpels of a flower are initially fused at the base and later in more apical regions. No completely free carpels have been found. The stigma is small, apical or subapical, and often poorly differentiated. There are usually many ovules, which are bitegmic on parietal or marginal placentas. As in most angiosperms, the ovules are anatropous, that is, with the micropyle closest to the placenta. The micropyle of the ovules is formed by the two teguments, which are bilaminate. The embryo sac is of the Polygonum type and generally contains starch granules. The carpels usually have nectary scales at their dorsal base (although these may be absent); they release the liquid through stomata.

Pollination is carried out by hymenopterans (many Sedum species), butterflies, moths, flies, and birds.

Seed / Fruit

The fruit is a follicle, typically dehiscent along its ventral suture. Non-dehiscent or nut-like fruits are rare. Each follicle usually contains many seeds, which are gradually released as the fruit dries out. The fruit dehiscence occurs along the ventral suture. The seeds are small, typically between 0.5 and 1 mm long and weighing about 0.02 g. They are elongated and have longitudinal ridges (ribs) or papillae. They are brown in color. The embryo is small, long, and straight, lacking a plumule, and stores aleurone and oil. The endosperm is cellular and sparse, reduced to a single-celled layer surrounding the hypocotyl. The epicotyl is usually well developed; it rarely remains small. The seed coat consists of 4 layers.

The seeds are dispersed by gravity and wind. They remain viable for a few years. Germination is epigeal, and the cotyledons are fleshy, usually petiolate, and long-lasting.

They have a great capacity for vegetative reproduction, which occurs from any broken-off part of the plant that comes into contact with the growing medium, often from the edges of the leaves. This ability is a trait that enables them to survive in extreme environments. Fallen parts usually sprout easily to form a new plant. Another common form of asexual reproduction in Crassulaceae is propagation by rhizomes.

Hybridization and polyploidization also appear to be common during evolution.

The Crasulaceae family exhibits great variation in chromosome number among groups, genera, and even within the same species. It may be one of the most diverse families among angiosperms. The base number for the Crassuloidea and Sempervioideae is 8. Many species are polyploid.

Root

The roots are usually small and diffuse, which gives them a great ability to absorb water quickly. Their tips are often reddish in color, which may indicate the presence of anthocyanin. Root hairs are usually unicellular, but those on adventitious roots may be multicellular.

The roots are generally fibrous, rarely conical or tuberous. In some species, they may be succulent. Secondary growth has been described in the roots of Sedum. Adventitious roots form easily, a trait that is exploited for propagation in gardening.

Habitat, distribution

They generally grow in rocky areas in humid environments or in arid mountainous regions, but are virtually absent from deserts and low-altitude arid lands. Some species are epiphytes, and one species has been found to be aquatic.

These species are adapted to arid (hot or cold) and mountainous environments, growing on rocks with little water and organic matter. Their roots are well-suited for anchoring the plant. They can thrive in extreme environments. Some species can withstand temperatures ranging from -25 °C to 60 °C. They are cosmopolitan and are distributed primarily in the Northern Hemisphere; the greatest diversity is found in Mexico (325 species) and South Africa (over 250 species). They are scarce on the Qinghai-Tibetan Plateau, in South America, and in tropical Africa, and are also found in Australia. Southern Africa is believed to be their place of origin, from where they may have spread to the rest of the world, beginning with the Mediterranean, and from there to Asia and the Americas.

Society

The Crassulaceae family does not include edible species, but it does include ornamental ones. Because of their hardiness, they are widely used in gardening, and they can sometimes become naturalized. Due to the Crassulaceae's ability to thrive in extreme environments, they are used to prevent soil erosion or as green roofs on buildings.

Some species have been used in traditional medicine because of their ability to synthesize metabolites with medicinal properties. The most important types of metabolites with potential medical applications include more than 55 types of phenolic compounds and flavonoids, 8 steroid and terpene compounds, as well as others such as cardenolides and bufadienolides. Some of these compounds exhibit antioxidant, antimicrobial, anti-inflammatory, and analgesic activity, among others.

The ability to produce nitrogenous metabolites appears to have been acquired following the split of the genus Crassula. Crassulaceae accumulate large amounts of sedoheptulose, which is the most abundant sugar in most species. In addition, nearly all of them contain isocitrate, which is not the case in other succulents.

Phylogeny

Taxonomy / NBCI (↗): Viridiplantae; Streptophyta; Streptophytina; Embryophyta; Tracheophyta; Euphyllophyta; Spermatophyta; Magnoliopsida; Mesangiospermae; eudicotyledons; Gunneridae; Pentapetalae; Saxifragales; Crassulaceae.

WFO (↗): Plantae / Pteridobiotina / Angiosperms / Saxifragales / Crassulaceae

GBIF (↗): Plantae / Tracheophyta / Magnoliopsida / Saxifragales / Crassulaceae

Bremer et al., 2016: Angiosperms / eudicots / core-dicots / Saxifragales / Crassulaceae

The Crassulaceae are monophyletic, with characteristics such as succulent leaves, anisocytic stomata, and carpel scales in the nectaries. Genetic studies have shown that the Crassulaceae family can be subdivided into 7 clades: Crassula, Kalanchoe, and 5 others belonging to the Sempervivoidae subfamily (Telephium; Sempervivum, Aeonion, Leucosedum, and Acre). All of these are monophyletic, and the Acre and Leucosedum clades form a clade called Sedeae. The Crassula and Kalanchoe clades have diverged morphologically.

It appears that the Crasulaceae family emerged about 80 million years ago, and phylogenetic studies place the period of greatest divergence around 64 million years ago, likely for two reasons. Following the mass extinction at the K-Pg boundary, many habitats became available. In addition, they developed CAM metabolism, which enabled them to colonize more hostile environments. The Crassula clade was the first to diverge (about 39 to 4 million years ago), followed by Kalanchoe (about 25 to 29 million years ago), and then by Telephium (from the Sempervioideae group). The separation of Acre and Leucosedum occurred about 13 to 18 million years ago.

Within the clade Sempervivoideae, the first group to diverge was Telephium, which is monophyletic. Within Telephium are the clades Rhodiola, Phedimus, and Pseudosedum.

Otra información

The typical plastome of the Crassulaceae family contains 85 protein-coding genes, 36 to 37 tRNA genes, 8 rRNA genes, and 4 pseudogenes.

Bibliografía

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Eid O, Ezzat S, Gonaid M, Choucry M. 2018. Crassulaceae (chemistry and pharmacology) - A review. Future Journal of Pharmaceutical Sciences. 2: 234-240. DOI: 10.1016/j.fjps.2018.07.003.

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Thiede J. Eggli U. 2007. Crassulaceae. In: Kubitzki, K. (eds) Flowering Plants · Eudicots. The Families and Genera of Vascular Plants, vol 9. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-32219-1_12.