ISSN 0026-8933, Molecular Biology, 2009, Vol. 43, No. 5, pp. 794–803. © Pleiades Publishing, Inc., 2009.

Original Russian Text © S.B. Gontcharova, A.A. Gontcharov, 2009, published in Molekulyarnaya Biologiya, 2009, Vol. 43, No. 5, pp. 856–865.

UDC 575:582

Molecular Phylogeny and Systematics of Flowering Plants

of the Family Crassulaceae DC1
S. B. Gontcharovaa and A. A. Gontcharovb
a Botanical garden-institute of the Far-Eastern Branch of Russian Academy of Sciences, Vladivostok, 690024 Russia
b Institute of Biology and Soil Science of the Far-Eastern Branch of Russian Academy of Sciences, Vladivostok, 690022 Russia;
e-mail: gontcharov@biosoil.ru
Received November 25, 2008
Accepted for publication December 24, 2008

Abstract—Crassulaceae (orpine or stonecrop family) is the most species-rich (ca. 1400 spp) family in the order
Saxifragales. Most members of the family are succulent plants. Phenotypic diversity and large number of spe-
cies complicates systematics of the family and obscures reconstruction of relationship within it. Phylogenetic
analyzes based on morphological and molecular markers placed Crassulaceae as one of the crown clades of
Saxifragales. In this contribution a review of phylogenetic studies on the family Crassulaceae, based on DNA
nucleotide sequence comparisons is presented; major clades established in the family are characterised; their
structure and polyphylesis of some genera are discussed. It is shown that the traditional taxonomic structure of
Crassulaceae contradicts pattern of phylogenetic relationships between its members. We critically analyzed
recent taxonomic systems of the family and stress that homoplasy of morphological characters does not allow
to use them to reconstruct relationships between crassulacean taxa even at the low taxonomic levels.
DOI: 10.1134/S0026893309050112

Key words: Crassulaceae, nucleotide sequences, molecular phylogenetics, systematics, homoplasy, DNA

1 Morphologically diverse and taxonomically com-
plex family Crassulaceae (orpines or stonecrops)
comprises ca. 1400–1500 species, classified in 33
genera [1]. Majority of these species are perennial
herbs, subshrubs or shrubs, sometimes tree-like
plants, adapted to xeric environment (have succulent
leafs, rarely stems, rhizomes, caudices or roots). Epi-
phytes and aquatic species (some members of the
genus Crassula) are also known in the Crassulaceae.
Representatives of this family are widely known and
popular as medicinal plants (Rhodiola rosea and some
others), ornamental outdoor and indoor plants.
The family has almost cosmopolitan distribution;
most often its members occur in arid and mountainous
habitats of temperate and sub-tropical regions. Cras-
sulaceae are particularly divers in southern Africa,
alleged center of their origin [2], in Mexico, Macaro-
nesia, Mediterranean region and Himalaya.
Crassulaceae are distinct in their physiology, it is
the only plant family whose representatives, both ter-
restrial and aquatic, are characterized by so-called
ëÄå metabolism (Crassulacean Acid Metabolism).
CAM is an ancient pathway of photosynthesis, pre-
sumably typical for early vascular plants inhabiting
seasonal pools in the Mesozoic era (200 million years
ago [3, 4]).
1 The article was translated by the authors.
Composition of the family has never been disputed
since its description and it was always regarded as nat-
ural. The only exception is the genus Penthorum that
was classified either within Crassulaceae [5], in Saxi-
fragaceae [6–8] or its own monogeneric family
Penthoraceae [9].
Traditionally the family Crassulaceae was consid-
ered as a primitive member of the Rosidae (because of
their floral structure and embryology), and the family
Saxifragaceae was regarded as its closest relative [6–-
9]. Molecular phylogeny data confirmed alliance of
these families and placed Crassulaceae in the clade of
the order Saxifragales, where the former compose a
clade together with the families Penthoraceae and
Haloragaceae [10-–15]. It was suggested that an
ancestor of these families diverged ca. 70 millions
years ago and the families are of approximately the
same age [16, 17].
Modern studies confirmed that the family Crassu-
laceae is a well circumscribed natural lineage, how-
ever, identification of monophyletic groups of all
ranks in the family is very difficult because of a great
diversity of their morphological and cytological fea-
tures [1, 2, 18].
By the end of 19th and the beginning of 20th cen-
turies, several family systems had been proposed
(reviewed by [19]), however, only that of Berger [20]

794
 MOLECULAR PHYLOGENY AND SYSTEMATICS OF FLOWERING PLANTS
was widely adopted by specialists. According to this
system, six subfamilies and 33 genera were recog-
nized in the family. The subfamilies were grouped into
two lines: Crassula-line (Crassuloideae, Kalanchoid-
eae, and Cotyledonoideae), that included taxa from
the Southern Hemisphere, mostly from the southern
Africa, and Sedum-line (Sempervivoideae, Sedoideae,
and Echeveroideae) comprising crassulaceae from the
Northern Hemisphere. To distinguish the families
within each line, the number of floral parts and pattern
of their arrangement as well as the degree of sym-
petaly and phyllotaxis were used. For example, Cras-
suloideae included species having four-merous flow-
ers with unfused corollas and a single whorl of sta-
mens (haplostemonous), while Kalanchoideae and
Cotyledonoideae comprised species having four-mer-
ous obdiplostemonous flowers and fused corollas.
Echeverioideae were characterised by five-merous
more or less fused corollas, and Sempervivoideae
were distinct in unfused, polymerous flowers. These
five subfamilies were seen distinct morphologically
and geographically, however, diagnosis of the remain-
ing subfamily Sedoideae was always uncertain. It was
noted [21], that Sedoideae is an artificial taxon that
comprises all genera not fitting diagnoses of other
subfamilies and its core genus Sedum (ca. 500 spp.)
comprises species, not fitting diagnoses of other gen-
era. This artificiality was a reason of all further prob-
lems in taxonomy of the subfamily and Sedum. Defi-
ciency of Berger’s system and particularly his subfam-
ily Sedoideae has been acknowledged by many
specialists, nevertheless, the system was widely used
[22–24].
At the end of the last and beginning of the new cen-
turies in the classification systems of flowering plants
based on phenotypic features, number of subfamilies
of Crassulaceae was reduced to four (Echeveroideae,
Crassuloideae, Kalanchoideae, and Sedoideae [24]),
than to three (Crassuloideae, Kalanchoideae Ë
Sedoideae, [25]) and finally to two (Crassuloideae and
Sempervivoideae [9]). However, these classifications
yet to be commonly accepted.
In the past two decades molecular phylogenetic
studies significantly changed our view on the relation-
ships between taxa at different taxonomic levels.
These studies prompted a number of new hypotheses
of plants evolution that extensively affected systemat-
ics of many groups including Crassulaceae. However,
despite the fact that the first nucleotide sequence of
Crassulaceae was deposited in GenBank as early as in
1992 [26], relationships within the family are far from
being fully understood.
In the present contribution we critically review
studies on evolution and taxonomy of the family Cras-
sulaceae from the point of view of molecular phylog-
eny. Closest relatives of the family, types of molecular
data used to analyze relationships within it, major
MOLECULAR BIOLOGY Vol. 43 No. 5 2009
795
clades established in the family are described and a
discrepancy between molecular phylogenetic data and
morphology-based system of the family is discussed.
Closest Relatives of the Family Crassulaceae
An alliance of Crassulaceae to the order Saxi-
fragales and its close relationship with the family Sax-
ifragaceae has been clamed by many authors [8, 24]
and was confirmed in analyzes of phenotypic data [27,
28], as well as by molecular phylogenetic studies [29–
-33]. However, exact position of Crassulaceae in the
tree of the order remains uncertain. Different data sets
and markers resolved the family Podostemaceae [34],
Cynomoriaceae [35] and Haloragaceae [30, 32] as a
sister of Crassulaceae. The late sistership received the
strongest bootstrap support. Close relationship
between Crassulaceae and Podostemaceae, resolved
in rbcL sequence comparisons with strong support as
well, was later refuted in a combined analyzes of SSU
rDNA and rbcL genes [36] and attributed to the long-
branch attraction artifact and insufficient taxon sam-
pling.
Affinity of aquatic Haloragaceae to Saxifragales
and their close relationship with the family Crassu-
laceae was established only with molecular phyloge-
netic data and can’t be substantiated at present by any
morphological [37]. Recent multigene analyzes
resolved Haloragaceae and Crassulacea as sisters with
high significance [14, 15] and thus corroborated data
obtained with of rbcL gene [33]. It was shown that the
clade Haloragaceae-Crassulaceae occupies a crow
position in the tree of Saxifragales, often as a sister of
the clade of the family Saxifragaceae [10, 13−15]. The
same studies resolved the genus Penthorum (the fam-
ily Penthoraceae or Haloragaceae s. l.), earlier a mem-
ber of Crassulaceae very similar to them morphologi-
cally, has no affinity to Crassulaceae. Instead, this
genus was placed as one of the crown branches of
Haloragaceae. Taking into account that Aphanopeta-
lum and Tetracarpaea, distinct from each other and
Crassulaceae phenotypically, occupy basal position in
the clade of the family Haloragaceae, these genera
could be regarded as the closest to Crassulaceae suc-
cessors of a common ancestor.
Types of Molecular Data
Although complexity of relationships in the family
Crassulaceae has been noted by all students there were
very few attempts to resolve these relationships with
molecular tools. The first assessment of crassulacean
phylogeny based on chloroplast DNA restriction-site
data (44 species from 19 genera) and trnL-F intergenic
spacer sequence comparisons (49 species from 26
genera), highlighted this problem and identified a
direction for further research [2, 38, 39]. These studies
were followed by a comparison of 112 sequences of
796 GONTCHAROVA AND GONTCHAROV

Clades Subtribes Tribes Subfamily

Cremnophyla, Echeveria,
Graptopetalum,
Lenophyllum, Thompsonella, Acre
Villadia,
Sedum subgenus Sedum Sedeae
Dudleya, Pistorinia
Prometheum, Rosularia,

Sedinae
Sedella, Leucosedum
Sedum subgenus Gormania
Sempervivum
Sedum Sempervivum Sempreviveae
cep. Rupestria
Aichryson
Aeonium
Aeonium Aeonieae

Sedeae
Monanthes
Sempervivo-
ideae

Sedinae
Sedum p.p.
Hylotelephium+
Orostachys subcection
Orostachys
Orostachus subcection Telephieae
Appendiculatae

Telephiinae
Meterostachys
Sinocrassula
Umbilicus
Rhodiola
Pseudosedum Telephium Umbilicieae
Phedimus
Aizopsis
Kalanchoe
Cotyledon Kalancho-
Tylecodon Kalanchoe Kalanchoeae ideae
Adromischus
Crassula Crassula Crassulo-
ideae

Generalized scheme of phylogenetic relationships in the family Crassulaceae, based on results of restrict analyzes of chloroplast
DNA [2, 38] and nucleotide sequence comparisons of chloroplast matK gene, trnL-F intergenic spacer and nuclear ITS rDNA [18,
40, 41], showing common for all analyzes features. Names of clades of Crassulaceae correspond the first molecular phylogeny of
the family [38], taxonomic structure − to the system proposed by Thiede and Eggli [62]. Taxa proposed by t’ Hart [39] and discussed
in the text are shown by grey.

chloroplast matK gene [18]. The tree obtained was
more detailed and improved understanding of evolu-
tionary relationships in the family Crassulaceae. Most
clades of this tree were supported by high bootstrap
values, however, branching pattern between the clades
remained largely unresolved (figure). Likely, still
insufficient taxon sampling in some clades and rela-
tively low phylogenetic resolution of matK gene neg-
atively affected results of the analysis.
There was also an attempt to resolve phylogeny of
Eastern Asian branch of the family Crassulaceae (the
subfamily Sedoideae, mostly from Telephium clade,
see below) based on individual and combined ana-
lyzes of sequences of trnL-F intergenic spacer of chlo-
roplast DNA (103 species) and ITS region of nuclear
ribosomal DNA (74 species) [40].
The most problematic member of the family, the
genus Sedum, was represented in the analyzes
described above by a limited number of taxa therefore
relationships between its members remained largely
unknown. To close this gap Gontcharova et al. [41]
created a data set that included 158 sequences of ITS
region of nuclear rDNA. The genus Sedum was repre-
sented in this data set by 65 species (14% from the
total number). Their sequences alignment was based
on ITS1 and ITS2 secondary structure models pro-
posed earlier for the family Crassulaceae [42] that sig-
nificantly eased a search for homologous positions
between rather divergent sequences.
Thus, to date only four studies aimed analyzes of
phylogenetic relationships in Crassulaceae at the fam-
ily level. They similarly resolved pattern of relation-
ships in the family, however, composition of some
clades, particularly those comprising a crown group,
and their branching order, remained unclear. Compar-
ison of phylogenetic trees based on coding (matK,
[18]) and non-coding (trnL-F and ITS rDNA [39, 40])
regions of nuclear and chloroplast genomes revealed
that their informativeness is not sufficient to recon-
struct a fully resolved crassulacean phylogenetic tree.
Noteworthy, the results based on different markers
independently revealed the same problematic assem-
blages (clades [37]), namely Telephium, Leucosedum
and Sempervivum [18, 40, 41] (figure). It is not clear
yet whether this congruence is a result of a relatively
recent but fast divergence or still insufficient taxon
sampling in these assemblages.

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 MOLECULAR PHYLOGENY AND SYSTEMATICS OF FLOWERING PLANTS
Undoubtedly, still a limited number of the
sequences analyzed reduces resolution of the phyloge-
netic tree of Crassulaceae [43, 44]. In studies men-
tioned above only 28 out of 33 crassulacean genera of
presumably non-hybrid origin [1] were sampled, how-
ever, in some clades/genera, particularly those spe-
cies-rich and therefore difficult for study, the number
of studied representatives was not enough to resolve
internal relationships with high significance. Remain-
ing five genera are oligotypic and generally poor stud-
ied. Some assumptions on their relationship to the rest
of the family were made based on morphology [1, 22,
39], that, however, is highly homoplasious in the fam-
ily, therefore these assumptions require conformation
by molecular data. It could be expected that extended
taxon sampling and greater number of characters in
the data sets could increase robustness of phyloge-
netic inference in the Crassulaceae.
A range of molecular markers, used to analyze
phylogenetic relationships in the family, was recently
supplemented by the external transcribed spacer
(ETS) of nuclear DNA and chloroplast rps16 gene
[45]. These markers were used to resolve relationships
between endemic American taxa of Crassulaceae
(Acre clade, see below). Resolving power of the gene
rps16 was low and only 5.78% of its nucleotides were
parsimony-informative. ETS sequences were notably
more divergent (33.4% of informative positions),
however, this high divergence also negatively affected
bootstrap support of the tree.
Combined analyzes of several molecular markers
have been used to infer relationships within some
crassulacean genera and clades [40, 47−50]. These
studies generally improved phylogeneti resolution but
also revealed incongruence between chloroplast and
nuclear markers in some instances that was explained
by a cpDNA-capture and/or hybridization [49, 50].
This result confirms that hybridization and introgres-
sion may have played a certain role in shaping the
family structure, as it was hypothesized by some
researchers [1, 18, 51–-55], however, the extent of
these processes in Crassulaceae remains poorly stud-
ied with molecular tools. It should be noted that phy-
logenetic analyzes of the genus Graptopetalum and its
close relatives with several markers from nuclear and
chloroplast genomes [56], did not produce any evi-
dence of hybridization that was expected in these taxa
[57].
The Current Status of Phylogeny and Systematics
of Crassulaceae
Already the first attempt to analyze relationships
between crassulacean species with molecular phylo-
genetic methods [38] revealed significant discrepan-
cies between the results obtained and traditional sys-
tem of the family [20]. Restrict analyzes of chloro-
MOLECULAR BIOLOGY Vol. 43 No. 5 2009
797
plast DNA established seven clades in the family,
Crassula, Kalanchoe, Telephium, Sempervivum, Aeo-
nium, Leucosedum and Acre [2, 38] (figure). Of these,
only Crassula clade corresponded subfamily Crassu-
loideae in Berger’s system while all other included
members of at least two traditional subfamilies.
Although further studies, based on DNA nucleotide
sequence comparisons, refuted entity of some of these
clades, the new hypothesis on relationships in the fam-
ily Crassulaceae became popular among researchers
[18, 40].
The Crassula clade was identified as the basal
divergence of the family tree [2, 14, 15, 18, 58], and
this placement as well as the clade monophyly was
supported not only by high bootstrap values but also
by indels in the matK sequences that, however, are
homoplasious [18]. As it was mentioned above, mor-
phologically Crassuloideae is characterized by four-
merous flowers and haplostemonous androecia, how-
ever, these features are homoplasious as well and typ-
ical for the distantly related genus Sinocrassula [40].
Most members of the Crassula clade occur in southern
Africa, except for aquatic species having almost a cos-
mopolitan distribution.
In Berger’s system the subfamily included five
genera while in the current classification four of them
(Dinacria, Pagella, Rochea, Vauanthes and Vauanthes)
are merged with Crassula [23, 59]. The validity of this
rearrangement has yet to be significantly confirmed by
molecular data. Crassula s.l. is a species rich and mor-
phologically diverse genus with ca. 200 species clas-
sified in 20 sections [59]. Although, some of these sec-
tions are distinct in characters of vegetative morphol-
ogy and reproduction, as well as in habit and
distribution, phylogenetic significance of these fea-
tures yet to be evaluated. The status of one section
comprising dwarf, mostly annual aquatic plants, that
was formerly regarded as an independent genus
Tillaea, has been already changed. At present Tillaea
is recognized as a sister group of the rest of Crassula
[2, 38] with a high divergence between the two
branches. This result was acknowledged as a possible
argument for restoring Tillaea to the generic rank and
recognising it as the first divergence in the family tree,
supporting earlier phylogenetic hypotheses [2, 22,
39]. In our opinion, sister relationship between Tillaea
and Crassula only confirms the monophyly of two
clades but it does not establish their taxonomic rank.
The clade Kalanchoe comprises genera of two tra-
ditional subfamilies, all of Kalanchoideae sensu
Berger (the genus Kalanchoe s. l.) and a portion of the
Cotyledonoideae. Fused corollas, base chromosome
number (x = 9), chromosome morphology and mostly
southern African distribution are characterise the
clade members [18, 60, 61]. The clade monophyly is
generally supported by all molecular markers, how-
ever, its position in the tree is still under the question.
798 GONTCHAROVA AND GONTCHAROV
Results of restriction analyzes and chloroplast mark-
ers significantly positioned clade as the second diver-
gence in the family tree [2, 18, 38, 40], while in phy-
logeny based on nuclear markers, the clade Kalanchoe
was placed after three branches belonging to Telephi-
inae, although with low significance [41]. The clade
was recognized as the tribe Kalanchoeae [39] or the
subfamily Kalanchoideae [25, 62] (figure).
Monophyly of genera comprising this clade
appears to be rather well established [18, 41, 49, 63].
Adromischus was resolved as its basal branch, fol-
lowed by the genus Kalanchoe, having a pair Cotyle-
don/Tylecodon as a sister group [18]. Molecular data
confirmed hypotheses based on cytology [60] on a
close affinity between morphologically distinct Kal-
anchoe, Adromischus and Cotyledon. However, it is
rather unlikely that Kalanchoe has an allopolyploid
origin from Cotyledon and Crassula as has been sug-
gested earlier [60]. Although the latter assertion has
not been rigorously tested, comparison of the topolo-
gies, based on nuclear (ITS rDNA, [41]) and chloro-
plast (matK, [18]) markers, revealed no discrepancy
between them in branching pattern within the clade,
suggesting evolution from a single ancestor.
To date phylogenetic relationships were studied in
detail only in two of the four genera composing the
clade Kalanchoe. ITS rDNA sequence comparisons in
the third species-rich genus in the family, Kalanchoe,
confirmed its monophyly and established three major
lineages in it, each characterized by a distinct distribu-
tion and partly morphology [63]. Accelerated evolu-
tionary rates in ITS rDNA sequences are typical for
the representatives the genus Kalanchoe, where an
average sequence divergence (p-distance) accounts
for ca. 10% [41]. Numerous extensive indels in ITS
and a somewhat elevated GC content (> 60%) are also
characteristic for Kalanchoe. In contrast to that, ITS
sequence divergence in Adromischus, Cotyledon and
Tylecodon was significantly lower (≤1%), and the
same could be expected for the chloroplast markers as
well. Mort et al. [49] analyzed a large data set
(1931 nt), that combined sequences from chloroplast
(psbA-trnH and trnL-trnF) and nuclear (ITS rDNA)
genomes of representatives of the genus Cotyledon but
they were unable to resolve significantly branching
pattern in the generic clade.
The putative clade Telephium comprises crassu-
lacean genera (former section and subsection of
Sedum), distributed mostly and Eastern Asia and the
clade Umbilicus, confined to Mediterranean Sea [2,
38]. Although the clade was resolved with a very low
significance (25%), it was readily accepted by namy
specialists and formally described as the subtribe
Telephiinae (figure). Five-merous flowers with free
petals, flat, dentate leaves and tuberous roots or thick-
ened rhizomes are synapomorphic morphological fea-
tures of the subtribe members [39]. However, this
statement is difficult to agree with taking into account
that these features occur in other clades/taxa. Further
studies based on sequence comparisons of chloroplast
gene matK [18], intergenic spacer trnL-F [39, 40] and
nuclear ITS rDNA region [40, 64] fail to confirm
monophyly of this taxon. In contrast, in all analyzes
genera assigned to the Telephiinae were distributed
between three or four robust clades of the tree. Only
two of them, Rhodiola and Phedimus, showed affinity
to each other [40] and were recognised as an informal
group Rhodiola [64]. Weakly supported sister rela-
tionships were established also between this pair and
the genus Umbilicus but only in cases when datasets
did not include the genus Crassula, most basal crassu-
lacean clade [40, 64]. In analyzes of the extended set
of ITS rDNA sequences affinity between Umbilicus
and the clade Rhodiola/Phedimus was not significant
because it was supported by low bootstrap values [41].
Thus, monophyly of the tribe Umbilicieae [62]
appears to be doubtful (figure).
Exact position of one more clade of Telephiinae in
the tree, Hylotelephium (tribe Telephieae [62]), com-
posed by the genera Hylotelephium, Orostachys,
Meterostachys and Sinocrassula, also remains uncer-
tain because in all phylogenies the clades Hyloteleph-
ium and Rhodiola form a polytomy [18, 40, 64, 65].
We have no reason to deny possible origin of these
clades from a common ancestor completely, however,
even in this case it is very likely that their divergence
was fast and could not be traced with the markers used
to date.
Molecular data fully confirmed the distinctness of
the genera Hylotelephium, Orostachys, Rhodiola,
Phedimus and Aizopsis from Sedum, which they tradi-
tionally belonged to. At the same time, pattern of rela-
tionships between these genera (existence of robust
polyphyletic clades Hylotelephium + Orostachys and
Rhodiola + Pseudosedum) as well as within the gen-
era (polyphyly of sections and subsections of
Hylotelephium and Rhodiola), established in phyloge-
netic analyzes, is rather unexpected and could not be
explained from the point of view of morphology
[40, 64].
Significant in most analyzes crown assemblage of
crassulacean phylogenetic tree, currently recognised
as the subtribe Sedinae [1, 39] or three tribes [62], is
composed of four large clusters/clades, Aeonium,
Sempervivum, Leucosedum and Acre (figure). The
genus Sedum s.str. is represented in each of these
clades and constitutes a bulk of the clades Acre and
Leucosedum. This fact clearly demonstrates poly-
phyletic nature of this genus. Beside Sedum the sub-
tribe includes ca. 16 genera more and comprises more
than 50% of the total species number of the family [1,
39]. Although composition of this assemblage is
beyond doubt in general, branching order of its major
clades remains tentative. Non-coding sequences from
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 MOLECULAR PHYLOGENY AND SYSTEMATICS OF FLOWERING PLANTS
chloroplast (trnL-F spacer; [40]) and nuclear (ITS
rDNA; [41]) genomes placed the clade Aeonium in the
most basal position in the assemblage, followed by the
clade Sempervivum and than by a paraphyletic or
non-supported in most analyzes artificial group Leu-
cosedum and its sister, the most species-rich clade
Acre.
Although monophyly of Sedinae is well supported
by molecular data, morphologically this taxon is
extremely heterogeneous and it is almost impossible
to find synapomorphic phenotypic features that distin-
guish the subtribe from the rest of the family. The
same problem is also characteristic for the major
clades composing Sedinae. Perhaps, only the clade
Aeonium is defined best of all because the molecular
data (significance thresholds and indels in matK gene
and ITS rDNA sequences [18, 40, 41]), distribution
(mostly Macaronesia) and polymerous flowers distin-
guish its members from other crassulaceae.
Likely this fact prompted recognition of the clade
as the tribe Aeonieae [62]. It should be mentioned,
however, that polymerous flowers are also typical for
the distantly related representatives of the clade Sem-
pervivum. Molecular phylogenetic studies allowed to
clarify the relationship within Aeonium clade, ana-
lyzed the evolution of morphological traits and diver-
sification in the genera composing the clade and con-
firmed Macaroneaian origin of the clade from a north
African predecessor [18, 47, 48, 66]. Several north-
African Sedum species belonging to three presumably
related series could have played this role [67, 68].
However, exact relationships between these taxa and
Macaroneaian genera remain unresolved.
The Sempervivum clade is another crassulacean
group that could not be unambiguously characterised
phenotypically and its composition has yet to be
defined. Nevertheless, the clade has been recognized
by some authors as the tribe Semperviveae [62]. Its
nominant genus Sempervivum is rather distinct from
other family members morphologically, by habit and
distribution and undoubtedly represent a monophyl-
etic lineage of Sedinae [69]. Some contradiction
relates to the taxonomic status of Jovibarba, a section
of Sempervivum or a separate genus [70, 71]. In any
case these two taxa are closely related and form a
robust common clade [18]. Less defined are relation-
ships between Sempervivum and some species of
Sedum. It was suggested that Sempervivum originated
from a polyploid group of Sedum [70], and a species
of Sedum series Rupestria was seen as the closest rel-
ative of Sempervivum [71]. This alliance was con-
firmed in DNA restriction analysis as well as ITS
rDNA sequence comparisons although with low boot-
strap support [2, 41]. However, matK gene failed to
confirm close relationship between Sempervivu and
Sedum ser. Rupestria [18]. Morphological similarity
between the two groups is not pronounced except for
MOLECULAR BIOLOGY Vol. 43 No. 5 2009
799
common for them polymerous flowers, feature that
likely arose several times in the family.
The polygeneric clade Leucosedum was one of the
best supported in the analysis of chloroplast DNA
restriction site data [2, 38], however, in all further
studies based on nucleotide sequence comparisons it
was resolved without bootstrap support [18] or as a
paraphyletic entity [40, 41]. Species of Sedum subge-
nus Gormania and some taxa presumably originating
from Gormania in Northern America (Dudleya,
Sedella) as well as in Eurasia (Rosularia, Prometheum
and Pistorinia) belong to this assemblage. It accounts
for ca. 200 species classified in 5–-7 genera that are
poorly studied with molecular methods. In addition to
Gormania species, the assemblage may include some
representatives of the subgenus Sedum as well [18,
41], therefore only an assumption could be made
regarding species composition of the clade Leucose-
dum, its structure, and morphology and distribution of
species belonging to the clade.
In species composing Leucosedum assemblage
ITS rDNA sequences were characterised by high
divergence (an average p-distance > 15%) that may
reflect either accelerated evolutionary rate in this
marker in the group or only distant relationships
between its members [41].
Acre clade is the most species and genera rich
among major the clades composing the family Crassu-
laceae. It is expected to accommodate ca. 500 species
traditionally classified in 7 genera [1]. These are rep-
resentatives of Sedum subgen. Sedum and most Amer-
ican endemic crassulacean genera formerly classified
in the subfamily Echeverioideae [20]. Monophyly of
this clade was well supported in all phylogenetic ana-
lyzes [2, 18, 38, 40, 41], however, affinity of some
non-American species of the subgenus Sedum to the
clade is questionable since they may belong to the
clade Leucosedum (see above). At the same time there
is no indication that any species of the subgen. Gor-
mania may ally to the clade Acre.
Until recently, structure of the clade Acre had been
little studied. It was established that the genera for-
merly belonging to the Echeverioideae, form several
lineages, however, their relationships with Sedum spe-
cies were not analyzed because of a limited taxon
sampling [18, 56]. Comparisons of a large number of
ITS rDNA sequences of Sedum allowed to clarify rela-
tionships in this genus in general and in the clade Acre
in particular [41]. It was shown, that the clade is split
into two clusters, one composed by species occurring
only in Southern and Northern Americas, and the sec-
ond include Eurasian species. Macaronesian Sedum
farinosum was resolved as a sister branch of the sig-
nificantly supported subclade of American crassu-
laceae. In this subclade Sedum species formed several
supported basal clusters with unresolved branching
pattern, while genera earlier composing Echeverio-
800 GONTCHAROVA AND GONTCHAROV
ideae, were placed in a large crown polygeneric
assemblage again having Sedum species at the base.
Eurasian species of the genus were also arranged into
several supported lineages, however, their common
cluster gained no bootstrap support [41]. It is likely
that accelerated evolutionary rates in their ITS rDNA
sequences (an average p-distance 15%) and still insuf-
ficient taxon sampling (21 species) reduced support
for the Eurasian cluster. Noteworthy, the sequence
divergence in the American subclade was twice as low
as that in Eurasian cluster, although the former
included representatives of seven traditional genera of
Crassulaceae. High sequence similarity [41, 56] and
presence of numerous intergeneric hybrids in Ameri-
can genera [1] questions applicability of traditionally
used morphological characters for the taxonomy of
these genera.
Thus, phylogenetic structure of the family Crassu-
laceae is still far from being fully elucidated. Only
four out of the seven clades, established in the first
analysis of chloroplast DNA restriction-site data,
were confirmed by further studies based on results of
nucleotide sequence comparisons, Crassula, Kalan-
choe, Aeonium and Acre (figure). In three “clades”,
Telephium, Sempervivum and Leucosedum, several
monophyletic lineages were identified (Hyloteleph-
ium, Rhodiola, Umbilicus, Sempervivum and other,
see above). These lineages showed little affinity to
each other and it is unlikely that they originated from
a common ancestor. The question, whether we deal
with a “hard” or “soft” polytomy in this case, remains
without an answer yet and requires further study using
more taxa and molecular markers.
Although molecular phylogenetic studies convinc-
ingly demonstrated artificial nature of the traditional sys-
tem of the family Crassulaceae, its recent revisions [39,
62] are deficient as well because monophyly of some
intrafamiliar taxa, adopted by authors of these revisions is
questionable. First of all, this applies to the tribe Sedeae
[39] or the subfamily Sempervivoideae equivalent to it, as
well as the tribes Sedeae, Semperviveae and Umbilicieae
[62]. Beside unclear phylogenetic status, neither of these
taxa could be explicitly characterized by any synapomor-
phic morphological character or even a unique set of char-
acters. Neither flower and inflorescence morphology nor
morphology of vegetative organs could be used to diag-
nose suprageneric taxa of Crassulaceae or their clades,
because it has been shown earlier that these features
evolved independently several times in the family [2, 18,
40, 41].
Only partly resolved phylogenetic relationships
and a high level of homoplasy of phenotypic features
complicate reconstruction of trends of morphological
evolution in Crassulaceae. Autapomorphic characters
are known at least for some crassulacean genera, how-
ever, even at this relatively low taxonomic level,
homoplasy occurs in the family. The genus Sedum is
particularly notorious in this respect. This genus
included species mostly not fitting diagnoses of other
genera [21], and it was further extended recently with
morphologically distinct taxa (e. g., former members
of Echiverioideae and Sempervivoideae sensu Berger
[18, 40, 41]. At present the genus represents a con-
glomerate including ca. 50% of total number of spe-
cies in the family.
One more group characterized by an obvious con-
tradiction between the traditional genus concept and
molecular phylogeny data is the subtribe Telephiinae.
Recent studies revealed unexpectedly close relation-
ships between the genera Hylotelephium and
Orostachys, as well as between Rhodiola and Pseu-
dosedum. Members of these pairs differ well from
each other morphologically nevertheless they form
common clades with branching pattern rejecting their
generic statuses [40, 64, 65]. Similar ovary morphol-
ogy suggested possible kinship between Hyloteleph-
ium and Orostachys [22, 72], however, these genera
were seen well separated from each other because of
differences in habit and inflorescence morphology.
Homoplasy of morphological features is character-
istic for Crassulaceae at the lower taxonomic levels as
well. It was shown that the subgenera and sections of
the genera Hylotelephium and Rhodiola are not mono-
phyletic [40, 64], and it could be expected that more
detailed analyzes of other genera will lead to the same
result. The studies mentioned above also convincingly
demonstrated that importance of characters tradition-
ally regarded important for taxonomy of the family
should be re-evaluated based on molecular phyloge-
netic data. Mausumia and Ohba [40] found that the
subsections Appendiculatae and Orostachys of the
genus Orostachys, distinct only in a shape of the leaf
apex (cuspidate and blunt, respectively), in fact are
distantly related [40]. These authors revealed that the
subsection Orostachys is a part of the generic clade of
Hylotelephium while the subsection Appendiculatae
is allied to the genus Meterostachys. Leafs with a cus-
pidate apex is a common feature of Orostachys sub-
section Appendiculatae and Meterostachys, however,
the latter differs in spadix-like inflorescence (cymose-
paniculate in Orostachys subsection Appendiculatae).
Flower and inflorescence morphology was always
regarded as an important feature in taxonomy of flow-
ering plants but it becomes obvious that in Crassu-
laceae it is more labile, perhaps even at the genus
level.
CONCLUSIONS
Our knowledge of phylogenetic relationships in
the family Crassulaceae remains fragmentary and
incomplete after almost 15 years of studies with
molecular tools. Further detailed investigations are
needed to clarify status of some suprageneric taxa
MOLECULAR BIOLOGY Vol. 43 No. 5 2009
 MOLECULAR PHYLOGENY AND SYSTEMATICS OF FLOWERING PLANTS
(e.g. Sedeae, Semperviveae and Umbilicieae), puta-
tive clades (e.g. Leucosedum and Telephium) and
most crassulacean genera. Establishment of their
monophyletic cores will facilitate successful recon-
struction of a complex process of evolution and diver-
sification in the family and eventually will lead to a
classification system of Crassulaceae that adequately
reflects relationships in the group.
ACKNOWLEDGMENTS
This work was supported by the Russian Founda-
tion for Basic Research, project no. 9-04-00270a and
9-04-00621a, FEB RAS, project no. 09-III-A-06-167
and 09-III-A-06-188 and Grant-in-Aid for the Scien-
tific Program (A) 19255004 (Representative: Katsu-
hiko Kondo) of JSPS.
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