rüdiger mues

Chemical constituents and biochemistry

Only 30 years ago the chemistry of bryophytes was virtually

unknown. Recent research on the biology of bryophytes and progress in
analytical techniques has resulted in a deeper knowledge about the chem-
ical constituents of bryophytes, although our understanding of their
biochemical processes, especially biosynthetic pathways, compared to
vascular plants, is still rather poor. In the first part of this chapter the
present state of the art regarding the chemistry of bryophytes will be pre-
sented, the second part deals with some aspects of chemosystematics, and
in the third part knowledge of the biochemistry of bryophytes is summar-
ized. A recent thorough and comprehensive review on the topic has been
published by Asakawa (1995). A further review, in 1997, on “heterocyclic
compounds in bryophytes” was published by the same author. He deals
mainly with secondary metabolites and does not mention inorganic com-
pounds. Primary metabolites are partly discussed, e.g., lipids, carbohy-
drates, and phaeophytins. Biochemistry was not a topic of his review; this
field of research was recently surveyed in Chopra and Bhatla (1990) and
Rudolph (1990).
In the section ‘Chemistry of bryophytes’, present knowledge about
inorganic compounds and primary metabolites, their structural ana-
logues, and other ubiquitous compounds in bryophytes will be discussed,
followed by the main classes of secondary products. The examples men-
tioned here are selected from recent original papers not cited in Asakawa
(1995, 1997); they are more or less confined to those compounds typical of
bryophytes in general. The following section on ‘Chemosystematics’ will
discuss marker components for at least the bryophyte classes. Examples
mentioned in the section on ‘Biochemistry’ will also focus on recent orig-
inal papers. Because of limited space in this chapter, only the most impor-

[150]

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 Chemical constituents and biochemistry 151

tant examples of each compound class and biochemical processes can be

discussed. Structures are drawn only for those compounds not illustrated
in Asakawa (1995, 1997) or in Huneck (1983).

5.1 Chemistry of bryophytes

5.1.1 Inorganic compounds

Among bryophytes there does not appear to be a general accumulation of
special inorganic compounds as known for example in lycopods with alu-
minium oxide, or in horsetails with silica (Hegnauer 1962). Inorganic ions
found in most bryophytes do not differ qualitatively and quantitatively
from those found in vascular plants (Huneck 1983). A few recent papers
deal with this topic and in an increased number of studies bryophytes are
used to monitor dispersion patterns of atmospheric pollutants (Muhle
1984, Steinnes 1995). It is frequently observed that certain bryophytes accu-
mulate potentially toxic levels of metal ions without apparent damage.
Some species show specific tolerance to metals present in their natural
environment (Wells & Brown 1995). There is one liverwort species with an
unusually high dry-weight content of 1.3% mercury: Jungermannia vulcani-
cola Steph. The mercury is deposited in the cell walls in a mercury–sulfur
component (Satake & Miyasaka 1984). Satake et al. (1984) found in some
water mosses in New Caledonia rather unusual high contents of inorgan-
ics. In the moss Ectropothecium subobscurum Thér. they detected high
contents of nickel (690 ␮g g⫺1 dry weight), manganese (470 ␮g g⫺1),
chromium (254 ␮g g⫺1), and bromine (210 ␮g g⫺1) and in the liverwort
Lopholejeunea sp. an incredibly high amount of manganese with 15300 ␮g
g⫺1. In general, according to those authors, the amounts of nickel, chro-
mium, and bromine in plants do not exceed 100 ␮g g⫺1 dry weight.

5.1.2 Primary metabolites, their structural analogues,

and other ubiquitous compounds
Primary metabolites are regarded as essential for almost all living organ-
isms and are derived from reactions of primary metabolism. Among them
should be noted carbohydrates, nucleotides, proteins, intermediates of the
tricarboxylic acid cycle, lipids, common pigments for photosynthetic pro-
cesses, and lignin. For a detailed introduction to “primary” and “secon-
dary” plant products see Mothes (1980). As bryophytes definitely belong
to the “green line” of land plants developing from early chlorophytes
(Graham et al. 1991, Hedderson et al. 1998), their primary metabolism is

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 152 rüdiger mues

very similar to that of vascular plants (Hegnauer 1962, 1986). This holds
true for such essential compounds as cellulose in the cell walls, chloro-
phylls a and b, main carotenoids, starch, nucleic acids, sugars, and certain
lipids. So far no real lignin has been found in the cell walls of bryophytes,
only “lignin-like” aromatic compounds (Wilson et al. 1989, Edelmann et al.
1998). Some of the few recent papers on carbohydrates in bryophytes are
discussed in Asakawa (1995). Konno et al. (1987) analyzed cell cultures of
the liverwort Marchantia polymorpha L. for its pectic polysaccharides in cell
walls and classified them as three types. According to these authors, carbo-
hydrates correspond in general to those of vascular plants, even in their
absolute configuration. The protein amino acids of bryophytes do not
seem to be significantly different from those of higher plants (Huneck
1983). In a survey of the occurrence of amino acids, Dutt (1996) found
common protein amino acids in 23 species of mosses and liverworts, and in
the liverwort Pellia epiphylla (L.) Corda also the two non-protein amino
acids: ␥-aminobutyric acid (GABA) and ornithine. Salm et al. (1998) isolated
the amino acid N-(4-hydroxy-3,5-dimethoxy-benzoyl)aspartic acid, called
fontinalin (1), from Fontinalis squamosa Hedw. Trennheuser et al. (1994)

(1)

detected six glutamic acid amides in Anthoceros agrestis Paton. Hegewald

and Kneifel (1987) investigated three liverwort and nine moss species for
their polyamine content. They found nine polyamines, spermidine
being the dominant one. Kraut et al. (1997a) isolated and synthesized
the oligopeptide rufulamide (2) from Metzgeria rufula Spruce. Adam and
Becker (1993) screened 13 liverwort, one hornwort and seven moss species
for the occurrence of lectins. From Marchantia polymorpha they purified the
first bryophyte lectin and showed it to be a monomeric protein of around
16 kDa. Among the lipids one may distinguish between n-alkanes and
their derivatives, and fatty acids, either free or bound as triglycerides. The
occurrence of aliphatic compounds in liverworts and mosses was sum-
marized by Asakawa (1995), whereas no report of compounds of this class
seems to have been published for hornworts. A few additional aliphatic
compounds have since been reported. According to Asakawa et al. (1996)

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 Chemical constituents and biochemistry 153

(2)

the liverwort Chiloscyphus pallidus Mitt. in Hook. f. emits a “very strong

stink bug smell” from crushed fresh material. The authors found as com-
pounds responsible for the odor simple aliphatic aldehydes, of which (E)-
dec-2-enal (3) is the major one. Nissinen and Sewón (1994) studied

(3)

hydrocarbon patterns in different tissues of Polytrichum commune Hedw.

Neinhuis and Jetter (1995) found n-alkanes, n-alkyl esters, n-alkanals,
primary n-alkanols, and n-alkanoic acids, closely resembling those of
moss gametophytes and higher plants, in waxes of the sporophytes of Pog-
onatum belangeri (C. Muell.) Jaeg. and P. urnigerum (Hedw.) P. Beauv. The
dominant compound was nonacosan-10-ol. In addition to the common
fatty acids ubiquitous in green land plants, mosses and liverworts contain
typical unsaturated ones, most of them mentioned by Asakawa (1995).
Examples for other recent papers on lipids in bryophytes are those of
Kohn et al. (1994), Dembitsky and Rezanka (1995), and Toyota et al. (1997b).
Further primary compounds, including enzymes, will be discussed under
Biochemistry.

5.1.3 Secondary products

Table 5.1 shows the classes of secondary compounds and their distribu-
tion in bryophytes.

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 154 rüdiger mues

Table 5.1. Secondary compounds from bryophytes

Compound class Liverworts Hornworts Mosses

Terpenoids ⫹⫹ (⫹) ⫹
Aromatic compounds ⫹⫹ ⫹ ⫹⫹
Nitrogen-containing compounds ⫹ (⫹) (⫹)
Sulfur-containing compounds (⫹) (– (–
Chlorine-containing compounds ⫹ (– (–

Notes: ⫹⫹ ⬎100 compounds; ⫹10–100 compounds; (⫹) ⬍10 compounds.

Table 5.2. Terpenoids from bryophytes

Terpenoid-class Liverworts Hornworts Mosses

Monoterpenes ⬃060 — 03
Sesquiterpenes ⬃600 5 09
Diterpenes ⬃300 — 04
Triterpenes ⬃018 2 25
Steroids ⬃017 4 10
Tetraterpenes ⬃026 ? 28
Polyterpenes ⬃ ⫹ ? 0⫹

Terpenoids
The distribution of terpenoids in bryophytes and the approximate
numbers of single compounds of the different terpenoid classes known
from bryophytes are shown in Table 5.2.

Monoterpenes and related compounds Besides aliphatic compounds (see

above) and certain sesquiterpenes (see below), monoterpenes are mainly
responsible for the characteristic odour of many liverworts. They are typ-
ically stored in the oil bodies and are therefore almost limited to liver-
worts. Examples of monoterpenes responsible for this odour are given by
Asakawa (1995). Only a few additional species have been investigated for
the occurrence of monoterpenes and a few new compounds have been iso-
lated. Toyota et al. (1997d) reinvestigated the fragrant liverwort Conoceph-
alum conicum (L.) Underw., one of the chemically best-known liverwort
species. Nevertheless, they succeeded in detecting three new monoter-
pene esters, the main one being (⫹)-bornyl cis-ferulate (4). In hornworts
monoterpenes have so far not been detected and in mosses they have up to
now been found only in the two Splachnaceae species, Splachnum luteum
Hedw. and S. rubrum Hedw. (Asakawa 1995). For most monoterpenes the

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 Chemical constituents and biochemistry 155

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absolute configuration has not been determined, since almost all of them
were detected by GC-MS (gas chromatography – mass spectroscopy) anal-
ysis (Asakawa 1995).

Sesquiterpenes and related compounds Sesquiterpenes are by far the

largest class of secondary metabolites in bryophytes, although they
mainly occur in liverworts (Table 5.2). Liverworts synthesize both the
same sesquiterpenes as higher plants and others with characteristic liver-
wort skeletons. In some cases the compounds correspond to the same
enantiomers as in higher plants, in others they represent the optical anti-
podes. So far acyclic, mono-, di-, tri-, and tetracyclic sesquiterpenes have
been detected. Asakawa (1995, 1997) gave a detailed discussion of the ses-
quiterpene types found up to the middle of the 1990s. He listed no fewer
than 61 types of sesquiterpenes from liverworts, eudesmane types being
most frequent. Many of them show remarkable biological activities
(Asakawa 1995, 1997). Among the sesquiterpene skeletons found to be
unique to liverworts are those shown in Fig. 5.1. Since 1994 about 70
papers have reported on the isolation and identification of sesquiterpenes
from liverworts. Only a few of those papers can be discussed here.
Since their detection in liverworts, the barbatane- and bazzanane-type
sesquiterpene skeletons had been regarded as liverwort-specific. König et
al. (1996) identified the sesquiterpene hydrocarbons ␤-bazzanene, ␣- and
␤-barbatene, and isobazzanene for the first time as constituents of the
roots of Meum athamanticum (L.) Jacq. (Umbelliferae). For ␣- and ␤-bar-
batene the authors determined the opposite configurations to those in
liverworts. In other cases both enantiomers of one sesquiterpene may
occur in one liverwort species (e.g., Saritas et al. 1998). In a first study on
the chemistry of the liverwort family Cephaloziellaceae, Wu et al. (1996)
detected in Cephaloziella recurvifolia Hatt. the aromadendrane-type sesqui-
terpene alcohol (-)-ledol and other oxygenated sesquiterpenes as major
constituents. Toyota et al. (1997a) isolated two sesquiterpene alcohols
belonging to the new “dumortane-type” sesquiterpene skeleton from

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 156 rüdiger mues

Fig. 5.1. Sesquiterpene skeletons unique to liverworts.

Argentinian Dumortiera hirsuta (Sw.) Nees and determined the structure of

one “dumortenol” as 3,4,11-trimethyl-7-methylenebicyclo[6.3.0]undec-2-
en-11␣-ol (5). Other interesting new sesquiterpenes have been reported by

(5)

Liu et al. (1996) and Hashimoto et al. (1998a). Toyota et al. (1996a) discov-
ered (-)-ent-spathulenol isolated from liverworts to be an artefact. Only
three sesquiterpenes are so far known from hornworts (Asakawa 1995).
Sesquiterpenes had not been recorded in mosses until Takakia was recog-
nized to be a moss rather than a liverwort (Smith & Davison 1993, Renza-
glia et al. 1997). From both Takakia species, sesquiterpenes were identified
by GC-MS analysis (Asakawa 1995).

Diterpenes Diterpenes detected in bryophytes are the second largest

terpenoid class in bryophytes. As with sesquiterpenes, almost all diter-
penes have been detected in liverworts. They are unknown for hornworts
and except for phytol, which is a ubiquitous part of chlorophylls a and b
in all green bryophytes, only four are known from mosses (Table 5.2).

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 Chemical constituents and biochemistry 157

Fig. 5.2. Diterpene skeletons unique to liverworts.

Regarding the absolute configuration of diterpenes, as for sesquiter-

penes, both enantiomers may occur, either the same as or opposite to
those found in higher plants. So far, acyclic, di-, tri-, tetra-, and pentacyclic
diterpenes have been detected. Asakawa (1995, 1997) mentioned at least 18
diterpene types found in liverworts, labdanes, clerodanes, and kauranes
being the most common ones. Typical diterpene skeletons for liverworts
are shown in Fig. 5.2. Since 1994, more than 40 additional papers have
reported diterpenes in liverworts, some of them exhibiting remarkable
biological activities. Thus Perry et al. (1999) isolated four new 8,9-secokau-
ranes and three new kauren-15-ones from Lepidolaena taylorii (Gott.) Trev.,
which is endemic to New Zealand. Some of these compounds showed dif-
ferential cytotoxic activity against human tumor cell lines with 8,9-seco-
kaurane (6) being the main cytotoxin. Cullmann and Becker (1998a)

(6)

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 158 rüdiger mues

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reported the isolation of pellialactone (7), a new nor-diterpenoid with an

unusual skeleton from Pellia epiphylla. Other new diterpenes have been
reported by Nagashima et al. (1997), Yoshida et al. (1997), and Hashimoto et
al. (1998b). The four diterpenes so far known from mosses are cited in
Asakawa (1995).

Triterpenes Triterpenes are found in species of all three bryophyte

classes, but only two are known from hornworts (Table 5.2). So far no
bryophyte-specific triterpenoid skeleton has been detected. About 40 dif-
ferent triterpenes are known from bryophytes, with around 20 from
mosses only. Four have been found in both liverworts and mosses.
Asakawa (1995) reported on GC-MS investigations of about 700 liverwort
species. These studies documented the presence of squalene in almost all
species, whereas it was only once found in a moss: Racomitrium japonicum
Dozy & Molk. (Asakawa 1995). The most common triterpenoid in mosses
is diploptene (⫽hop-22(29)-ene) (Asakawa 1995). Grammes et al. (1994)
isolated 22-hydroxy-29-methylhopanoate, 20-hydroxy-22(29)-hopene,
22(30)-hopene-29-oic acid, adianton (⫽30-nor-21␤-hopane-22-one), and
tetrahymenol (⫽3␤-hydroxy-gammaceran) from in vitro cultures of Fos-
sombronia alaskana Steere & Inoue and F. pusilla (L.) Nees. Cullmann and
Becker (1998a) and Sanders (1996) detected betulin (⫽20(29)-lupen-3␤,28-
diol) in Pellia epiphylla and Lepidozia reptans (L.) Dum. respectively. Toyota
et al. (1998) isolated the new dammarane-type triterpenoid dammara-
17Z,21-diene (8) from the moss Floribundaria aurea subsp. nipponica (Nog.)

(8)

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 Chemical constituents and biochemistry 159

Nog. This was the first record of this triterpene type for bryophytes. From
the hornwort Phaeoceros laevis (L.) Prosk. Trennheuser (1992) isolated the
triterpenoid acids betulic and ursolic acid, both common in higher
plants. Ursolic acid is also known from mosses (Asakawa 1995) and liver-
worts (Schmidt 1996).

Steroids The main phytosteroids, campesterol, sitosterol, and stig-

masterol, are found in almost all bryophytes investigated (Table 5.2). In
some mosses and liverworts, Patterson et al. (1990) found only the 24␣-
ethyl epimer (sitosterol), whereas in other moss and liverwort species
mixtures with the 24␤ epimer (clionasterol) occur. In higher plants only
the 24␣ epimers (sitosterol and campesterol) have been detected, in algae
always the 24␤ ones (clionasterol and dihydrobrassicasterol). Regarding
the epimers of phytosteroids, bryophytes take an intermediate position
between algae and tracheophytes. Besides the steroids listed in Asakawa
(1995) a range of others, new for bryophytes, was later detected in several
liverwort species and in Hypnum cupressiforme Hedw. (e.g., Sievers 1992,
Martini 1996, Sanders 1996, Schmidt 1996, Cullmann & Becker 1998a,
Hashimoto et al. 1998b). One new phytosteroid, stigmast-5,28-dien-3␤-ol
(9), was isolated by Martini (1996) from Riella helicophylla (Bory & Mont.)
Mont.

(9)

Tetraterpenes (carotenoids) For the distribution of carotenoids in bryo-

phytes see Table 5.2. Besides the 12 carotenoids mentioned by Asakawa
(1995) for mosses and liverworts, Czeczuga (1980, 1985a, b) and Czeczuga et
al. (1982) found an additional 22 carotenoids in 10 liverwort and 32 moss
species. Among them seven are found only in liverworts and nine only in
mosses. There seem to be no reports of carotenoids in hornworts.

Polyterpenes Such polyterpenes as rubber and gutta-percha from

certain higher plants are unknown from bryophytes, but according to

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 160 rüdiger mues

Table 5.3. Aromatic compounds from bryophytes

Compound class Liverworts Hornworts Mosses

Benzoic and cinnamic acid derivatives (⫹ (⫹) (⫹

Phenolethers, alkylphenols, phenylglycosides (⫹ (– (–
Bibenzyls, bisbibenzyls, bisbibenzyl dimers, (⫹⫹ (– (⫹)
stilbenes, and related compounds
Phenanthrenes (⫹ (– (–
Naphthalenes (⫹) (– (–
Acetophenones (⫹) (– (–
Lignans (⫹ (⫹) (–
Flavonoids (⫹⫹ (– (⫹⫹
Coumarins, isocoumarins, coumestans (⫹) (– (⫹
Benzonaphthoxanthenones (– (— (⫹)

Notes: ⫹⫹ ⬎100 compounds; ⫹ 10–100 compounds; (⫹) ⬍10 compounds.

Rezanka and Dembitsky (1993), polyisoprenoid alcohols appear to be

universally present in bacteria, plants, and animals. They investigated
eight mosses and Marchantia polymorpha for the occurrence of prenols in
bryophytes. The mosses contain mainly betulaprenols with an average
chain length of C§º, M. polymorpha had two maxima of chain lengths, the
first at C¶º and the second at C¡¡∞, and contained predominantly ficapre-
nols with up to 5% betulaprenols.

Aromatic compounds
Besides the terpenoids, aromatic compounds constitute the most impor-
tant secondary products of bryophytes. They occur as a wide range of dif-
ferent types, but rather unequally distributed among the bryophyte
classes (Table 5.3). Only one type has been found in species of each class;
most types are known only from liverworts, others only from mosses. No
type is found exclusively in hornworts. Most of these types are also
known from vascular plants. Only the sphagnorubins from peat mosses,
the benzonaphthoxanthenones from Polytrichum, and with very few
exceptions also the bisbibenzyls and bisbibenzyl dimers of liverworts are
regarded as bryophyte-specific.

Benzoic and cinnamic acid derivatives Asakawa (1995) recorded about 30

compounds of this class. Only a few more papers have reported such com-
pounds in bryophytes. Perry et al. (1996) found the new cytotoxic mono-
terpene phenyl ether (10) in Trichocolea mollissima (Hook. f. & Tayl.) Gott.
They also corrected the structures of benzoates earlier reported from Tri-

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 Chemical constituents and biochemistry 161

(10)

chocolea tomentella (Ehrh.) Dum. Kraut et al. (1993) isolated from two Frulla-
nia species (one of them at that time still known as F. muscicola Steph., now
confirmed to be a new species and renamed F. azorica Sim-Sim, Sérgio,
Mues & Kraut [Sim-Sim et al. 1995]) three glycerol glucosides acylated with
caffeic acid, the main compound being (11). Schoeneborn (1996) detected
the isocitric acid esters of caffeic (12) and ferulic acid, respectively, in Mar-

(11)

(12)

chesinia bongardiana (Lehm. & Lindenb.) Trev. Further benzoic and cin-
namic acid derivatives have been reported by Trennheuser (1992), Brink-
meier (1996), and Kraut and Mues (1999).

Phenylethers, alkylphenols, phenylglycosides Asakawa (1995) mentioned

a few examples of this type of aromatic compounds in liverworts. Accord-
ing to Toyota et al. (1997c), the intensely fragrant odour of crushed Leptole-
jeunea elliptica (Lehm. & Lindenb.) Schiffn. is due to 1-ethyl-4-hydroxy-,
-4-methoxy- and -4-acetoxybenzene. The first allopyranosyl aromatic

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 162 rüdiger mues

glycoside for bryophytes was isolated by Toyota et al. (1996b) from Cono-
cephalum conicum: 2–(3,4-dihydroxyphenyl)-ethyl-O-␤-allopyranoside.

Bibenzyls, bisbibenzyls, bisbibenzyl dimers, stilbenes, and related compounds

After flavonoids this class of aromatic compounds is the second most
important one in liverworts, still unknown from hornworts and mosses
with the exception of pallidisetins A [13, 2–(E)] and B [13, 2–(Z)], two novel

(13)

cinnamoyl bibenzyls isolated by Zheng et al. (1994) from Polytrichum pallid-

isetum Funck. Both have cytotoxic activities against the human tumor cell
lines RPMI-7951 melanoma and U-251 glioblastoma multiforme. Biben-
zyls also occur regularly in species of certain angiosperm families, e.g.,
Cannabaceae, Dioscoreaceae, and Orchidaceae. Until recently bisbiben-
zyls and dimeric bisbibenzyls had been regarded as liverwort-specific, but
Bai et al. (1996) isolated a bibenzyl-dihydrophenanthrene dimer, biogen-
etically related to the bisbibenzyls, from tubers of the orchid Pleione bul-
bocodioides (Franch.) Rolfe. Asakawa (1995, 1997) recorded more than 90
bibenzyls and their derivatives, including about 50 bisbibenzyls and
seven bisbibenzyl dimers. Since then about 30 papers describing this class
of compounds from liverworts have appeared. Kunz and Becker (1994) iso-
lated the new 2,5,4⬘-trihydroxybibenzyl from Ricciocarpos natans (L.) Corda
and Cullmann et al. (1997) found the new 7-hydroxypellepiphyllin (14) in

(14)

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 Chemical constituents and biochemistry 163

Pellia epiphylla. Other new bibenzyls have been reported by Kraut et al.
(1997b), Rycroft et al. (1998a), and Schoeneborn (1996). A new bisbibenzyl
was detected by Kraut et al. (1997b) in Lethocolea glossophylla (Spruce) Grolle,
the bisprenylated glossophyllin (15) with a chromene and a chromane

(15)

moiety. Anton et al. (1997) found the two new bisbibenzyls isoplagiochins
E (16) and F (17). Nabeta et al. (1998) isolated from cell cultures of Heteroscy-

(16/17)

phus planus (Mitt.) Schiffn. two bisbibenzyls, the known isoplagiochin A

and the structurally related planusin A (18). Cullmann et al. (1997) revised
the structures of some perrottetin E-type bisbibenzyls from Pellia epiphylla

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 164 rüdiger mues

(18)
and isolated the new bisperrottetin, 13⬘, 13⵮-bis-(10⬘-hydroxy-perrottetin
E) (19). The first and still the only monomeric stilbene from bryophytes,

(19)

3,4-dihydroxy-3⬘-methoxystilbene, was isolated by Speicher and

Schoeneborn (1997) from Marchesinia bongardiana, its structure being con-
firmed by independent synthesis.

Phenanthrenes Although biogenetically related to the bibenzyls via

the dihydro derivatives, phenanthrenes are treated separately here.
Asakawa (1995) recorded only three dihydrophenanthrenes and three
phenanthrenes. Subsequently, a few papers have reported this compound
type: Adam and Becker (1994), Anton et al. (1997), and Connolly (1997).

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 Chemical constituents and biochemistry 165

Naphthalenes Besides naphthalene itself, only 2,4,7-trimethoxy-

naphthalene and the methylene-dioxy substituted naphthalenes wett-
stein A–C were discussed in Asakawa (1995, 1997). Later, Rycroft et al.
(1998b) isolated the new naphthalenes 1,2,4-trimethoxy- and 1,2,3,4-
tetramethoxynaphthalene from Adelanthus decipiens (Hook.) Mitt.

Acetophenones Acetophenones are reported by Asakawa (1995) only

from Trocholejeunea sandvicensis (Gott.) Mizut. Lorimer and Perry (1994) iso-
lated two antifungal acetophenones (20, 21) from Plagiochila fasciculata

(20–24)

Lindenb. These were also detected by Rycroft et al. (1998b) in Adelanthus

decipiens, which also contained additionally the new acetophenones
22–24. Cullmann and Becker (1999) detected the first acetophenone C-gly-
coside from bryophytes, the 2,4,6-trihydroxyacetophenone-3,5-di-C-␤-D-
glucopyranoside, in Lepicolea ochroleuca (Spreng.) Spruce.

Lignans The lignans are a class of phenolics of which at the time of

Asakawa’s reviews (1995, 1997) only a few compounds were known from
bryophytes. Among them the cyclolignan 2,3-dicarboxy-6,7-dihydroxy-
1-(3,4-dihydroxy)-phenyl-1,2-dihydronaphthalene (25), first isolated by

(25)

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 166 rüdiger mues

Cullmann et al. (1993) from Pellia epiphylla, seems to be a common basic

element of this class. This compound was later detected in other liverwort
species. Lignans of this type are still limited to liverworts, whereas other
lignan types are typical phenolics of hornworts. They are yet unknown in
mosses (Asakawa 1995). The 1,2-dehydro derivative of 25 was first detected
by Tazaki et al. (1995) in Jamesoniella autumnalis (DC.) Steph. The 1,2-
dehydro-2-decarboxy derivative of 25 was the first compound of this type
found as a natural product, first isolated from Pellia epiphylla by Risch-
mann et al. (1989), and later from other liverworts, e.g., Bazzania trilobata
(L.) S. Gray (Martini et al. 1998a), Lepidozia incurvata Lindenb., Chiloscyphus
polyanthos (L.) Corda, and Jungermannia exsertifolia Steph. subsp. cordifolia
(Dum.) Vána (Cullmann et al. 1999). Other new lignans have been reported
by Martini et al. (1998a). Cullmann and Becker (1999) isolated the first gly-
cosides and further esters of 25 from Lepicolea ochroleuca. Because of its
wide occurrence, they proposed for 25 the trivial name “epiphyllic acid.”

Flavonoids Flavonoids are the most widespread phenolics in bryo-

phytes, although still unknown from hornworts. Since Asakawa’s review
(1995), about 30 papers on the occurrence of flavonoids in mosses and
liverworts have appeared, among them some reports of other flavonoid
monomeric aglycones, e.g., Morais and Becker (1991), Cullmann and
Becker (1998b), and Hashimoto et al. (1998b). Sievers et al. (1994) found
traces of kaempferol in Hypnum cupressiforme, the first time for a moss as a
free aglycone. They detected the new dihydroflavonol derivatives,
hypnum acid (26) and its methyl ester. About 15 new flavone glycosides

(26)

have since been isolated, e.g., by Anhut et al. (1992), Kraut et al.
(1993,1995,1996), and Brinkmeier et al. (1998). From in vitro cultures Kunz
et al. (1994) isolated the red cell-wall pigments of Ricciocarpos natans. The
main compound, riccionidin A (27), is the first natural anthocyanidin
derivative with an additional connection betweeen the B- and C-ring and
with a hydroxylation pattern, unusual for flavonoids. The second
pigment, riccionidin B, is a dimer of A. As cell-wall pigments, both

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 Chemical constituents and biochemistry 167

(27)

compounds are not glycosylated like the common anthocyanins of vascu-

lar plants. They were also detected as red pigments of Marchantia polymor-
pha, Riccia duplex Lorbeer, and Scapania undulata (L.) Dum. The typical red
pigments reported from certain Sphagnum species, the sphagnorubins
A–C, may have a chemical relation to 3-deoxyanthocyanidins. They were
discussed by Asakawa (1995) and no other compounds of this type have
since been isolated. Much progress has been made in the field of biflavo-
noid research in bryophytes since Asakawa’s review (1995). Almost 20
papers reported biflavonoids in mosses and the first paper on a biflavone
in a liverwort was published by Kraut and Mues (1999). They found dicra-
nolomin in Chandonanthus hirtellus (Web.) Mitt. subsp. giganteus (Steph.)
Vanden Berghen. Geiger et al. (1997) published a review on the occurrence
of flavonoids in arthrodontous mosses. They recorded eight biflavonoids
and five triflavonoids not listed in Asakawa (1995), provided new refer-
ences, and drew the structures of all bi- and triflavonoids from mosses
known up to the publication of their paper. They also presented a table
with the known flavonoid glycosides reported from mosses. Later Brink-
meier (1996) and Brinkmeier et al. (1999) reported six new biflavonoids
from Mnium hornum Hedw. and Pilotrichella flexilis (Hedw.) Angstr. The
actual flavonoid types and their numbers in bryophytes are presented in
Table 5.4. Altogether 356 different flavonoids have been reported from
bryophytes.

Coumarins, isocoumarins, coumestans The first coumarins isolated and

identified from bryophytes were reported by Jung et al. (1994, 1995) from
Atrichum undulatum (Hedw.) P. Beauv., Polytrichum formosum Hedw., and
Tetraphis pellucida Hedw. These authors characterized 11 highly oxygen-
ated new coumarins found to be unique to nematodontous mosses; the
structures of most of these compounds are shown in Asakawa (1997).
Besides these new coumarins, Jung et al. (1994) detected daphnin, the 7,8-
dihydroxy-7–O-␤-D-glucopyranosylcoumarin, in P. formosum, also known
from higher plants. This is the only coumarin so far to be found also in
some liverworts; e.g., Lepidozia reptans (Sanders 1996) and Bazzania trilobata
(Martini 1996). Raubuch (1998) investigated other nematodontous mosses

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 168 rüdiger mues

Table 5.4. Flavonoids from bryophytes

Flavonoid type Liverworts Mosses

Flavone aglycones and glycosides 218 77

Flavonol aglycones and glycosides 210 29
Anthocyanins and derivatives 212 25
Aurones 211 63
Biflavonoids 211 36
Flavanones 214 2—
Dihydrochalcones 212 2—
Dihydroflavonols 21— 23
Isoflavones 21— 27
Triflavones 21— 25

and Encalypta streptocarpa Hedw. for the occurrence of coumarins and iso-
lated 13 different coumarin glycosides, among them five new ones, but of
a similar type as those reported from Jung et al. (1994, 1995). Thus, until
now 16 different coumarins have been reported from mosses. The few iso-
coumarins known from bryophytes are listed by Asakawa (1995, 1997).
Brinkmeier (1996) found the first coumestans as derivatives of 4,2⬘-epoxy-
3-phenylcoumarins in a bryophyte: she isolated six different hydroxy-
lated and methoxylated compounds of this type from Mnium hornum, the
main one being 4,2⬘-epoxy-4⬘-hydroxy-5,7,5⬘-trimethoxy-3-phenyl-
coumarin (28).

(28)

Benzonaphthoxanthenones The only known compounds of this type

from bryophytes mentioned by Asakawa (1995, 1997) are the ohioensins
A–E from Polytrichum ohioense Ren. & Card., based on the novel benzo-
naphthoxanthenone skeleton. They exhibited cytotoxicity against 9 PS
murine leukemia cells and certain human tumor cells in culture. Zheng et
al. (1994) isolated three other novel benzonaphthoxanthenones from Poly-
trichum pallidisetum, of which 1-O-methyl-ohioensin B (29) was the main
compound. They also showed cytotoxic activity against several human
tumor cell lines.

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 Chemical constituents and biochemistry 169

(29)

Nitrogen-containing compounds
Bryophytes do not regularly produce nitrogen-containing secondary
products, e.g. alkaloids. Thus, Asakawa (1995, 1997) recorded only two
alkylindols, skatol and indoleacetic acid (IAA) from liverworts, the new
alkaloid anthocerodiazonin from Anthoceros agrestis, four maytansinoids
from Isothecium subdiversiforme Broth. and Thamnobryum sandei (Besch.)
Iwats., an alkylamide from Thuidium kanedae Sak., and indole and pyr-
rolidine from Splachnum rubrum. Only one other paper on nitrogen-
containing compounds has since been reported for bryophytes. Besides
the known harmane alkaloid, 7-hydroxyharmane (⫽harmol), Salm et al.
(1998) found for the first time in a bryophyte, the new harmol propionic
acid ester (30) in Fontinalis squamosa.

(30)

Sulfur-containing compounds
The only sulfur-containing compounds reported from bryophytes are
dimethyl sulfide and the thioacrylates isotachins A–C from Isotachis and
Balantiopsis species (Asakawa 1995).

Chlorine-containing compounds
Asakawa (1995, 1997) recorded as the only chlorine-containing com-
pound from bryophytes the drimane-type sesquiterpene 7␣-chloro-6␤-
hydroxyconfertifolin detected in Makinoa crispata (Steph.) Miyake. Two
other papers reported chlorine-containing compounds in liverworts.
Anton et al. (1997) isolated 12-chloro-isoplagiochin D from a Plagiochila
species. Martini et al. (1998b) detected 10 cyclic bisbibenzyls substituted
with one to six chlorine atoms and bazzanin K (31), a new dichlorinated

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 170 rüdiger mues

(31)

macrocycle consisting of a phenanthrene and a bibenzyl moiety, in Bazza-

nia trilobata.

5.2 Chemosystematics

As mentioned above, most compounds of primary and secondary metabo-

lism synthesized by bryophytes are comparable to those produced by vas-
cular plants. Liverworts are clearly the chemically best investigated
bryophyte class. Asakawa (1995, 1997) did not give a precise number of
chemically investigated liverwort species, but estimated that about “6%
of all liverwort species and less than 2% of all mosses have been studied
chemically.” This does not mean that each “chemically examined” species
has been investigated for all classes of natural products. In some cases,
only the lipophilic extract and its main compound(s) has been character-
ized. Therefore, although it is difficult to give a precise number of chemi-
cally investigated species, at least one compound has been detected in
approximately 700–900 liverworts and about 400 mosses. For the occur-
rence of flavonoids only, Geiger et al. (1997) counted nearly 300 moss
species from 59 different families. From hornworts fewer than 10 species
in five genera have been studied; therefore knowledge about the chemis-
try of hornworts is only fragmentary. Significant differences in the chem-
istry of the bryophyte classes are summarized in Tables 5.2 and 5.3. Aside
from mono- and diterpenes, which are definitely unknown for horn-
worts, all other terpenoid types occur in each bryophyte class. The marker
components for liverworts are the sesqui- and diterpenes. Certain liver-
wort-typical sesqui- and diterpene skeletons have been detected, but the
majority exhibit similar structural types to those found in vascular
plants. For aromatic compounds (Table 5.3) only the benzoic and cin-

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 Chemical constituents and biochemistry 171

namic acid derivatives are known from all three groups; all others are
either limited to liverworts or have been found only in liverworts and
mosses. Only the coumestans and benzonaphthoxanthenones appear to
be restricted in bryophytes to mosses. The typical aromatic compounds of
liverworts are the bisbibenzyls and bisbibenzyl dimers. The liverwort and
hornwort lignans are characteristic for each class, absent from mosses and
different from the lignans of vascular plants. Flavonoids are common
compounds in the green land plants. Thus, their absence in hornworts is
somewhat surprising and might be due to the unsufficient chemical
investigation of this class. Among the flavonoids, only the tricetin 6,8-di-
C-glycosides, especially tricetin 6,8-di-C-␤-D-glucopyranoside (32), are

(32)

unique for liverworts in the plant kingdom. Most other flavone mono-
meric aglycones and glycosides are found in higher plants as well. All bi-
and triflavonoids of mosses (included dicranolomin from Chandonanthus)
are unique and differ from those of pteridophytes and seed plants. Other
flavonoid types unique to bryophytes are the riccionidins from liverworts
and the sphagnorubins from Sphagnum. The highly oxygenated coumar-
ins of mosses are aromatics reported only for nematodontous groups and
for Encalypta streptocarpa. Primary and secondary metabolites of bryophy-
tes are most variable in the liverworts. This is true of both structure types
and of single compounds. The lowest diversity is found in hornworts,
probably due to poor knowledge of their chemistry in general.
Differences in chemistry between the bryophyte classes, and between
bryophytes and vascular plants, are by far less substantial than the differ-
ences between the different groups of algae (excluding the green algae) on
one hand, and bryophytes and tracheophytes on the other hand. There-
fore, chemistry clearly supports the evolution of bryophytes and tracheo-
phytes as being monophyletic from the green line of land plants.

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 172 rüdiger mues

5.3 Biochemistry

The biochemistry of bryophytes has been recently reviewed, e.g., by

Chopra and Bhatla (1990) and Rudolph (1990).

5.3.1 Enzyme activities in primary metabolism

Most of the papers on enzyme activities in the primary metabolism of
bryophytes deal with nitrogen metabolism. Thus the nitrogen metabo-
lism of Sphagnum was discussed in detail by Rudolph et al. (1993). Studies
on the in vivo activity of nitrate reductase, an enzyme catalyzing the con-
version of nitrate to nitrite, were carried out by Marschall (1998). The
enzyme aspartate aminotransferase (AspAT) plays a key role in nitrogen
and carbon metabolism of plants, animals, and microorganisms, catalyz-
ing the reversible transfer of the amino group from aspartate to gluta-
mate. Heeschen et al. (1996) separated four AspAT isoforms from extracts
of Sphagnum fallax (Klinggr.) Klinggr., each exhibiting identical molecu-
lar weights. Heeschen et al. (1997) purified the glutamate dehydrogenase
of S. fallax, the enzyme catalyzing the reversible reductive amination of 2-
oxoglutarate to l-glutamate. Kahl et al. (1997, 1998) worked on the purifi-
cation and characterization of l-glutamine synthetase from S. fallax.
Only a few papers have reported on other aspects of primary metabolism
in bryophytes. Lipoxygenase catalyzes the oxidation of linoleic acid and
certain other polyunsaturated fatty acids to form conjugated diene
hydroperoxides. Fatty acid hydroperoxides (HPOs) thus formed are
further converted to various lipid breakdown compounds in plant
tissues. HPOlyase cleaves the HPOs to form C§-aldehydes and C¡™-oxo
acids. Matsui et al. (1996) found HPOlyase activity in cultured cells of Mar-
chantia polymorpha and they succeeded in isolating and characterizing the
HPOlyase partially, the first time for a bryophyte. They also isolated and
identified n-hexanal and 12-oxo-(9Z)-dodeceonoic acid, products of
HPOlyase activity. Matlok et al. (1989) described a method for the isola-
tion of cell-wall-bound peroxidase isozymes of Sphagnum magellanicum
Brid.

5.3.2 Biosynthesis and metabolism of secondary

products
Substantial progress has been made during the last three years in the
research on the biosynthesis of terpenoids in liverworts. In the past, the
mevalonic acid pathway leading to the biosynthesis of isopentenyldiph-

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 Chemical constituents and biochemistry 173

osphate (IPP) had been accepted as the only biosynthetic route for all terp-
enoid producing organisms. Only recently, an alternative nonmevalonoid
pathway of IPP biosynthesis, the “glyceraldehyde–pyruvate” pathway,
has been discovered in bacteria and plants (Rohmer 1998). Adam et al.
(1998) studied the incorporation of 13C-labeled glucose into the monoter-
penes borneol and bornyl acetate, the sesquiterpenes cubebanol and ric-
ciocarpin A, the diterpene phytol, and the phytosteroid stigmasterol in
axenic cultures of Ricciocarpos natans and Conocephalum conicum. They
showed that the isoprene building blocks of sesquiterpenes and stigmas-
terol are made via the mevalonic acid pathway, whereas isoprene units of
the monoterpenes and phytol are exclusively derived from the glyceralde-
hyde–pyruvate pathway. Other papers on terpenoid biosynthesis in liver-
worts were published by Adam et al. (1996), Adam and Croteau (1998), and
Nabeta et al. (1994).
Some progress has also been made in research on biosynthesis and
metabolism of phenolics in bryophytes. Rasmussen et al. (1995) worked on
biosynthesis of the Sphagnum-specific trans-sphagnum acid, and Rasmus-
sen et al. (1996) on the biosynthesis and accumulation of 4⬘-O-␤-D-
glucosyl-cis-p-coumaric acid in axenic cultures of S. fallax. Later
Rasmussen and Rudolph (1997) isolated a stereospecific glucosyltransfer-
ase from S. fallax, that catalyzes the transfer of glucose from UDP-glucose
to the 4⬘-hydroxy group of cis-p-coumaric acid. Fischer et al. (1995) clearly
showed activity of the key enzyme in flavonoid biosynthesis, chalcone
synthase, in Marchantia polymorpha and identified naringenin as the
typical cyclization product of the corresponding chalcone. The first paper
dealing with the biosynthesis of cyclic bisbibenzyls of liverworts was pub-
lished by Friederich et al. (1999), using sterile thallus tissue of Marchantia
polymorpha. Feeding experiments with 13C-labeled precursors showed
that the rings A and C of the marchantin A molecule (33) are derived from

(33)

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 174 rüdiger mues

the benzene ring of l-phenylalanine via trans-cinnamic acid and p-

coumaric acid. A phenylpropane–polymalonate pathway using dihydro-
p-coumaric acid and acetate/malonate was proposed for the biosynthesis
of the bibenzyl monomers which were confirmed to be the building
blocks of the marchantin molecule. The bibenzyls in turn are coupled to
form the bisbibenzyl structure, but the mechanism of this final coupling
step is unknown.

Closing remarks

Substantial progress has been made on the chemistry of bryophytes in the

last two decades, but still fewer than 10% of all bryophyte species have
been thoroughly studied. Almost all papers deal with the chemistry of the
gametophyte, while only a few compare the chemistry of the gameto-
phyte and the sporophyte of a given species, one of the most impressive
examples being the dissertation of Cullmann (1996) and the papers result-
ing from that dissertation mentioned in this review. The biological activ-
ity of bryophyte compounds has been documented in several papers, e.g.,
Asakawa (1995, 1998). Numerous bryophyte species, especially liverworts,
are now cultivated under axenic conditions (e.g., Becker 1994) and a
substantial number of bryophyte compounds have been synthesized
(Asakawa 1995, Eicher et al. 1996, 1998). Bryophytes are chemically rich
and their chemistry and biochemistry are active areas of research.

Acknowledgments

My sincere thanks are given to my colleague, Professor Dr H. Rudolph,

Kiel, for valuable help with references to the section on Biochemistry, and
to my co-workers, Mrs C. Zehren and Dr U. Lion, for drawing the struc-
tures presented in this review.

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