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12 January 2015
D V A
The Evolution of Plant

Secretory Structures and the
Emergence of Terpenoid
Chemical Diversity
Bernd Markus Lange
Institute of Biological Chemistry and M.J. Murdock Metabolomics Laboratory, Washington
State University, Pullman, Washington 99164-6340; email: lange-m@wsu.edu
Annu. Rev. Plant Biol. 2015. 66:19.119.21
Keywords
The Annual Review of Plant Biology is online at

plant.annualreviews.org
fossil record, glandular trichome, resin duct, secretory cavity
This articles doi:

10.1146/annurev-arplant-043014-114639
Abstract
c 2015 by Annual Reviews.

Copyright
All rights reserved
Secretory structures in terrestrial plants appear to have rst emerged as

intracellular oil bodies in liverworts. In vascular plants, internal secretory
structures, such as resin ducts and laticifers, are usually found in conjunction
with vascular bundles, whereas subepidermal secretory cavities and epidermal glandular trichomes generally have more complex tissue distribution
patterns. The primary function of plant secretory structures is related to
defense responses, both constitutive and induced, against herbivores and
pathogens. The ability to sequester secondary (or specialized) metabolites
and defense proteins in secretory structures was a critical adaptation that
shaped plant-herbivore and plant-pathogen interactions. Although this review places particular emphasis on describing the evolution of pathways
leading to terpenoids, it also assesses the emergence of other metabolite
classes to outline the metabolic capabilities of different plant lineages.
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Contents

EARLY TERRESTRIAL ALGAE: DEVELOPMENTAL

AND METABOLIC ADAPTATIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19.2
BRYOPHYTES: INTRACELLULAR OIL BODIES OF LIVERWORTS
CONTAIN A WEALTH OF TERPENOID STRUCTURES . . . . . . . . . . . . . . . . . . . 19.6
LYCOPODS: RELATIVELY LOW TERPENOID PRODUCTION BY A
LINEAGE MOSTLY DEVOID OF SECRETORY STRUCTURES . . . . . . . . . . . . 19.9
FERNS: THE PRESENCE OF GLANDULAR TRICHOMES CORRELATES
WITH SECRETION OF FARINOSE WAXES RICH IN FLAVONOIDS
BUT NOT IN TERPENOIDS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .19.10
THE EVOLUTION OF SECRETORY DUCTS AND CAVITIES
IS CORRELATED WITH A REMARKABLE EXPANSION
OF TERPENOID CORE STRUCTURES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .19.10
LATICIFERS: TUBES CONTAINING STICKY AND TOXIC
CONCOCTIONS OF METABOLITES AND PROTEINS . . . . . . . . . . . . . . . . . . . .19.13
GLANDULAR TRICHOMES: MODIFIED HAIRS
THAT TRAP VOLATILES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .19.15
SECRETORY STRUCTURES: COMMON FEATURES
OF PHYTOCHEMICAL FACTORIES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .19.16
Ultrastructural and Metabolic Specialization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .19.16
Jasmonates Regulate the Formation of Secretory Structures . . . . . . . . . . . . . . . . . . . . . . .19.17
EARLY TERRESTRIAL ALGAE: DEVELOPMENTAL

AND METABOLIC ADAPTATIONS
CGAs: charophycean
green algae
19.2
Land plants (embryophytes) evolved as a monophyletic group from multicellular algae called
charophycean green algae (CGAs) (Figure 1). The reconstruction of ancestral CGAs prior to
the emergence of land plants is very difcult because (a) extant CGAs are phenotypically diverse,
ranging from microscopic unicellular agellates to complex, branched laments over a meter in
length, and (b) both elaborations (leading to increased complexity) and simplications (resulting in
loss of characters) occurred independently during the enormous evolutionary divergence between
ancestral CGAs and extant embryophytes (11). Nevertheless, when combining morphological,
ultrastructural, chemical, and molecular evidence, one can infer which features of land plants were
likely inherited from CGA progenitors.
A common, but not universal, character of CGAs is the pyrenoid, a microcompartment
associated with a concentrating mechanism for carbon dioxide xation in chloroplasts, which has
been retained in only a single group of land plants, the hornworts (82). In the CGA ancestor of
land plants, starch likely served as a storage polysaccharide, whereas other polysaccharides, such
as cellulose, hemicelluloses, and pectins, served as building blocks of the cell wall (83). In addition,
small amounts of lignin-like material have been detected in some extant CGAs, indicating that
some parts of the biochemical machinery required to generate more complex cell walls may have
evolved early during their divergence (83). The cell walls of the zygote (the only diploid cell in an
organism with an otherwise haplontic life cycle) of various CGAs are highly resistant to chemical
and biochemical deconstruction and contain an autouorescent material with properties similar
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Precambrian eon
Time (Mya)
4,600
2,500
540
ARCHEAN
4,600
Accretion
of Earth
3,800
Earliest life
(carbon isotope
evidence)
PROTEROZOIC
2,700
Oldest oxygenic
photosynthetic
stromatolites
2,7202,470
Oldest fossils
with hopanoids
(prokaryotic triterpene biomarker)
1,200
~700
1,700
Oldest
Split of Chlorophyta
unquestioned
and
Streptophyta
Oldest fossils
algal fossils
(including CGAs
with steranes
that gave rise to
(eukaryotic triland plants)
terpene biomarker)
Paleozoic era
540
490

CAMBRIAN
445
ORDOVICIAN
~470
Oldest fossils
assignable to
bryophytes (spores)
Oil bodies (?)
415
SILURIAN
450390
Rhyniophytes
418407
Lycophyta
(oldest extant
vascular plants)
355
DEVONIAN
300
250
CARBONIFEROUS
PERMIAN
360250
Seed ferns
~365
~300
)
(Pteridospermatophyta
True
Glandular
gymnosperms
trichomes
~250
~320
on seed fern
Oldest fossils
Oldest fossils
with oleananes
with diterpenoids
(angiosperm tri(amber)
terpene
biomarker)
Resin ducts/blisters (?)
Mesozoic era
250
200
TRIASSIC
145
65
CRETACEOUS
JURASSIC
136130
Oldest
angiosperm
fossils
~100
Angiosperm
radiation
Figure 1
Time line of land plant evolution based on fossil evidence. Green indicates the emergence of new plant lineages, blue indicates the
oldest fossils containing signature metabolites, and purple indicates the emergence of secretory structures. Crosses indicate extinct
groups. Abbreviation: CGAs, charophycean green algae.
to those of sporopollenin, a biopolymer derived from hydroxylated fatty acids and phenolics
that is characteristically present in the outer walls of spores and pollen of land plants (22, 53).
Although more denitive chemical and molecular evidence for the presence of sporopollenin
in CGAs is certainly needed, possible functions of the autouorescent polymeric material may
involve protection from environmental extremes (e.g., water loss, digestion, and UV irradiation)
(31). Flavonoids and phlorotannins have been described as products of metabolism in certain
algae (30, 66), but the available evidence does not allow inferences regarding the likelihood of an
occurrence in ancestral CGAs.
Several plant hormones [indole-3-acetic acid (auxin), abscisic acid, isopentenyladenine (cytokinin), salicylic acid, and jasmonic acid; see Figure 2] were detected at low (in some cases very
low) levels in the lamentous CGA Klebsormidium accidum, a species regarded as still relatively
closely related to the common ancestor of land plants (40). The genome sequence of this alga
indicated the presence of some, but not all, genes that encode enzymes known to be involved
in hormone biosynthesis and perception (including those related to the formation of ethylene,
which was not assayed chemically) (40). Strigolactones were reported to be present in several
CGAs (21), whereas gibberellins and brassinosteroids were not detectable (85) (Figure 2). The
www.annualreviews.org Evolution of Plant Secretory Structures
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Hormone class
Biosynthetic precursors
Distribution
Comments
Ethylene
L-Methionine,
S-Adenosylmethionine
C B L M G A
?
Some signal transduction

components missing in CGAs
L-Trypothophan
or indole
C B L M G A
?

DMAPP and adenine
C B L M G A
Certain signal transduction

components possibly missing in
CGAs
Carotenoids
C B L M G A
?
Some biosynthetic genes and

signal transduction components
missing in CGAs
Carotenoids
C B L M G A
CGAs and all lineages of land

plants respond to exogenous
strigolactones
C B L M G A
?

C B L M G A
? ?
Very low concentration reported

in CGAs; several biosynthetic
genes and all signal transduction
components missing in CGAs;
bryophytes produce precursors of
jasmonic acid
CH2
H2C
Indole-3-acetic acid (auxin)

O
OH
N
H
Zeatin (cytokinin)
N
NH

N
NH
OH
Abscisic acid
COOH
(+)-Orobanchol (strigolactone)
O
OH
Salicylic acid
L-Phenylalanine
or isochorismic acid
COOH
OH
Jasmonic acid (oxilipin)
Glycerolipid
COOH
ent-Kaurene (diterpene)
GA3 (gibberellin)
OH
B L M G A
?
Bryophytes may produce only

precursors of gibberellins and do
not have fully functional
components of gibberellin signal
transduction
B L M G A
?
The presence of brassinosteroids

in bryophytes has been
demonstrated in a liverwort, but
the presence/absence of the signal
transduction pathway has not yet
been investigated
OC
HO
COOH
Brassinolide (brassinosteroid)
OH
H
HO
H
HO
OH
Sterols
O
H
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D-GAP
Acetyl-CoA
MEP pathway
PLASTID
Isoprene
Cytokinins
[ Sesquiterpenes
Tocopherols
Phylloquinone
Chlorophylls
Pyruvate
CYTOSOL
C5
C10
MVA pathway
Monoterpenes
E Pe
R r
MITOCHONDRION
C5
F
Monoterpenoids
C15
C5
Cytokinins
Sesquiterpenes
C15
C15 ]
C20
Diterpenes
Diterpenoids
Gibberellins
Phytol
C40
Carotenoids
Abscisic acid
Strigolactones
C30
E
R
Sesquiterpenoids
C45
Triterpenes
F
Sterols
Ubiquinone

Triterpenoids
C45
Brassinosteroids
Plastoquinone
Polyterpenes (dolichols, rubber)
Figure 3
Overview of terpenoid biosynthesis in plants. The major terpenoid products of secretory structures are shown in blue. The exchange of
terpenoid pathway intermediates between subcellular compartments involves unidentied transporters ( yellow circle with question mark).
The C box shows the plastidial localization of carotenoid cleavage enzymes involved in the biosynthesis of abscisic acid and
strigolactones; the F boxes show the locations of enzymes involved in the functionalization of terpenoid core structures (cytosol and
ER). Abbreviations: CoA, coenzyme A; ER, endoplasmic reticulum; GAP, glyceraldehyde 3-phosphate; MEP, 2C-methyl-D-erythritol
4-phosphate; MVA, mevalonic acid; Per, peroxisome.
distribution of hormones across extant CGAs requires further investigation before more reliable
inferences about the hormone content of ancestral CGAs can be attempted. The scant molecular
and experimental evidence available to date suggests that some hormone responses may have been
assembled gradually during the adaptation of CGAs to a terrestrial environment. The primary
roles of hormones in ancestral CGAs were most likely to facilitate growth [e.g., strigolactonecontrolled rhizoid elongation (21)] and orchestrate responses to environmental stresses, whereas
more complex roles in plant development and interactions with the environment (including the
requisite signal transduction network) emerged later during embryophyte evolution.
Terpenoids involved in primary metabolism and photosynthetic energy capture and transfer
were likely present in the CGAs that gave rise to land plants. Here, I briey outline the biosynthesis
of the different classes of terpenoids, including some that may or may not have been produced by
ancestral CGAs but are important for the discussion further below in this article.
The biosynthesis of terpenoids is modular and can be divided into four stages. Stage 1 consists of reactions leading to the formation of dimethylallyl diphosphate (DMAPP) and isopentenyl diphosphate (IPP), the universal C5 building blocks of terpenoids (Figure 3). In CGAs
and all land plants, DMAPP and IPP are synthesized via two compartmentalized pathways. The
DMAPP:
dimethylallyl
diphosphate
IPP: isopentenyl
diphosphate
Figure 2
Occurrence of hormones across different plant lineages. The boxed letters indicate the presence of a particular hormone in
charophycean green algae (C), bryophytes (B), lycopods (L), monilophytes (M), gymnosperms (G), and angiosperms (A). A question
mark indicates that components of the biosynthetic and/or signal transduction pathway for a particular hormone are not detectable in
representative genomes. Abbreviations: CGAs, charophycean green algae; DMAPP, dimethylallyl diphosphate.
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MVA: mevalonic acid

ER: endoplasmic
reticulum

MEP: 2C-methyl-Derythritol
4-phosphate
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mevalonic acid (MVA) pathway operates primarily in the cytosol and the endoplasmic reticulum (ER) (the involvement of peroxisomes has been demonstrated in some higher plants but has
not been investigated in other organisms), whereas the enzymes of the 2C-methyl-D-erythritol
4-phosphate (MEP) pathway are localized to plastids (55, 61).
Stage 2 of terpenoid biosynthesis involves condensation reactions of DMAPP and IPP that
are catalyzed by chain-length-specic prenyltransferases (Figure 3). The condensation of one
molecule of DMAPP and one molecule of IPP to geranyl diphosphate (C10 ) is catalyzed by plastidial
geranyl diphosphate synthase (in the genus Solanum, neryl diphosphate synthase is a second C10 generating prenyltransferase) (55). A condensation of one molecule of DMAPP with two molecules
of IPP generates E,E-farnesyl diphosphate (C15 ), which is catalyzed by farnesyl diphosphate synthase isoforms localized to the cytosol, plastids, mitochondria, or peroxisomes (the genus Solanum
also contains a plastidial Z,Z-farnesyl diphosphate synthase). E,E,E-Geranylgeranyl diphosphate
(C20 ) is generated by catalysis of several geranylgeranyl diphosphate synthase isoforms present in
plastids, the ER, and mitochondria (55). In plastids, longer-chain trans-prenyl diphosphate synthases generate the precursors for carotenoids (C40 ) and plastoquinone (C45 ). Sterols/triterpenes
and derived steroids are synthesized from C30 precursors by ER-localized enzymes. Longer-chain
dolichols are synthesized by cis-prenyltransferase isoforms localized to the ER (61). A long-chain
trans-prenyltransferase in mitochondria is responsible for the biosynthesis of the C45 side chain
of ubiquinone.
In stage 3 of terpenoid biosynthesis, reactions catalyzed by terpene synthases result in the
assembly of the structural core of each terpenoid class (Figure 3). In general, terpene synthases
for hemiterpenes (C5 ), monoterpenes (C10 ), diterpenes (C20 ), and tetraterpenes/carotenoids (C40 )
are localized to plastids, whereas sesquiterpene (C15 ) and triterpene (C30 ) synthases are localized
to the cytosol (with some exceptions, mentioned below) (18, 87, 93).
During stage 4, terpenoid skeletons are further functionalized through redox, conjugation,
and other modifying reactions to yield a wide range of end products. For example, abscisic acid
and strigolactones (plant hormones) are derived from plastidial carotenoid precursors, which are
rst processed by plastidial cleavage enzymes and then decorated by various cytosol/ER-localized
enzymes (Figure 3). Although some terpenoid end products are usually derived entirely from
precursors of the MVA pathway (e.g., sterols) or MEP pathway (e.g., carotenoids and the side
chain of chlorophylls), there is also evidence for a contribution of building blocks from both
precursor pathways to a given terpenoid (metabolic crosstalk) under certain conditions or in
certain cell types (37).
BRYOPHYTES: INTRACELLULAR OIL BODIES OF LIVERWORTS

CONTAIN A WEALTH OF TERPENOID STRUCTURES
The invasion of the land by plants (terrestrialization) was one of the most signicant evolutionary
events in the history of life on Earth. The development of a vegetation cover on the previously
barren land surfaces impacted the global biogeochemical cycles (including causing a dramatic
decline of atmospheric carbon dioxide concentrations) and the geological processes of erosion
and sediment transport. Based on the microfossil record (spores and tissue fragments), the earliest colonization of terrestrial habitats occurred during the Ordovician and early Silurian periods
(480430 Mya) (Figure 1) (96). The oldest lineage of land plants is often referred to as the
bryophytes (nonvascular land plants). However, it is important to note that, based on multiple lines
of evidence, bryophytes are considered a paraphyletic grade, consisting of three phylaliverworts
(Marchantiophyta; 6,000 extant species), mosses (Bryophyta; 14,000 species), and hornworts
(Anthocerotophyta; 300 species)with controversy still persisting regarding the properties of
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bryophyte-like plants at the base of the embryophyte clade (32). Important adaptations facilitating the transition from an aquatic to a terrestrial environment included the emergence of a
cutinized epidermis to limit water loss (not present in all bryophytes), the emergence of a life cycle
with alternating generations (diploid asexual sporophyte and haploid sexual gametophyte, which
resulted in an enhanced capacity for gradual increase in size and complexity), and the origin of
stomata for gas exchange (note that liverworts do not have stomata but rather have potentially
homologous air pores) (70).
Despite the tremendous success of the terrestrialization by ancestral species, the nonvascular
body plan of modern-day bryophytes has restricted their distribution to moist habitats. With
the emergence of better-adapted (preexisting) microorganismic and novel invertebrate (and later
vertebrate) biotic challengers, bryophytes required improved defense mechanisms, which prominently included the production of novel secondary (or specialized) metabolites. They evolved the
ability to synthesize various soluble polyphenols, such as phenylpropanoid and bibenzyl derivatives, avonoids, coumarins, and lignans consisting of catechol units (although not all extant representatives accumulate these metabolites; e.g., avonoids and lignans are absent from hornworts
and mosses, respectively) (4, 5, 9, 76, 91). Various studies reported on the occurrence of ligninand sporopollenin-like materials in cell walls of extant and, by inference, ancestral bryophytes
(32). However, because lignin-enforced transport tissues such as xylem and phloem are lacking (although some mosses contain hydroids and leptoids for short-distance water and nutrient
conduction, respectively), the structures and functions of these biopolymers need to be interpreted with caution. Nitrogen-containing metabolites, such as alkaloids, are only rarely found in
bryophytes (46), although endosymbiotic nitrogen xation, by association with cyanobacteria,
evolved as an important process for surviving under nitrogen-limiting conditions (24).
Ethylene, auxins, abscisic acid, cytokinins, oxylipins (precursors of jasmonic acid), salicylic acid,
strigolactones, and brassinosteroids are produced by extant bryophytes, in particular as a response
to various biotic and abiotic stresses (79), but signicant changes with regard to the capacity for the
biosynthesis and perception of these plant hormones occurred during the evolution of land plants.
The moss Physcomitrella patens (Hedw.) Bruch & Schimp. is capable of synthesizing ent-kaurene
and ent-kaurenoic acid (35, 67) (Figure 4c), which are precursors of gibberellins in more recently
diverged land plant lineages. These metabolites appear to serve unique hormone-like functions
during germination (3, 34). However, DELLA and GID1-like proteins, which are essential for
gibberellin signal transduction, are likely not able to interact in bryophytes (39, 99), and how
hormone perception occurs in this lineage thus remains to be investigated.
One of the most striking phytochemical characteristics of liverworts is the remarkable diversity of terpenoids (more than 700 unique structures have been reported to date) (6); by contrast,
mosses and hornworts (the other bryophyte clades) are more limited terpenoid producers (4, 5).
Liverwort terpenoids include various monoterpenes, more than 60 classes of sesquiterpenes, and
close to 20 classes of diterpenes (Figure 4b). Terpenoid (and polyphenolic) structural variety in
bryophytes correlates with the presence of oil bodies (Figure 4a), an evolutionary innovation
unique to the liverworts (Figure 1). These subcellular structures, which can vary greatly in size
and abundance, are surrounded by a single-layer membrane and are distinct from seed oil bodies of angiosperms (36). There is considerable debate about the organellar origin of bryophyte
oil bodies, in part because older studies employed xation techniques that were inadequate for
subsequent microscopic studies. More recent investigations have indicated that the primary (if
not exclusive) mechanism of oil body formation in bryophytes involves an assembly from subdomains of the ER (36). However, signicantly more experimental evidence with a larger number
of species is required to even begin to understand the ontogeny of these important subcellular
structures.
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CHO
CHO
OAc
cis-Pinocarveyl
acetate
(turpentine-like)
Bicyclohumulenone
(woody)
O
OAc
H
CHO
H
H

Polygodial
(pungent and insecticidal)
O O
H
H
H
COOH
AcO
ent-Kaurenoic acid
(hormone precursor)
Plagiochiline A
(nematocidal)
O Anastreptine A
O
(bitter)
ent-Trachyloban-17-al
(antimicrobial)
Figure 4
Terpenoid accumulation in liverworts. (a) Schematic representation of oil bodies ( yellow) in a liverwort cellular unilayer.
(b) Representative structures of terpenoids occurring in liverwort oil bodies. (c) The structure of the gibberellin biosynthetic precursor
ent-kaurenoic acid, which is present in the moss Physcomitrella patens.
Based on immunolocalization studies with the liverwort Marchantia polymorpha, Suire et al.
(86) concluded that certain enzymes of the terpenoid biosynthetic pathway, in particular those
responsible for chain elongation reactions (C5 C10 C20 ) and the reduction to phytyl diphosphate (Figure 3), are present in both plastids and oil bodies. Further studies of plastidial and
oil bodyspecic isoforms of these enzymes, should their presence be conrmed molecularly and
biochemically, would provide opportunities to investigate the role of paralogous gene duplicates
or alternative splicing as drivers of diversication.
When liverwort tissue is injured or dried, characteristic mixtures of volatile terpenoids (mostly
mono- and sesquiterpenoids) are released from ruptured or degrading oil bodies. Depending on
the species under investigation, these scents have been described as woody, turpentine-like, mossy,
carrot-like, or seaweed-like (6). Humans characterize the taste of ingested liverworts as pungent
and/or bitter, which is due to the occurrence of sesquiterpene lactones as well as glycosylated and
highly oxygenated diterpenoids (Figure 4b). Cytotoxic activities of liverwort-derived terpenoids
have been demonstrated against bacteria, fungi, insects, nematodes, sh, other plants, and animal
cell lines (6). Although high terpenoid levels are certainly not a prerequisite for success, as evidenced by the ascendance of mosses and hornworts (which accumulate only low concentrations),
the appearance of oil bodies as a secretory (storage) structure in liverworts likely facilitated
the evolution of terpenoid (and polyphenolic) chemical diversity. The earliest macrofossils of
liverworts, dated to the Middle Devonian period (388 Mya) (Figure 1), contain circumstantial
evidence, in the form of undigested, darkly stained cells with a conspicuous distribution, that
antiherbivore defenses involved strategies similar to those enabled by terpenoid-containing oil
bodies of modern liverworts (54).
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LYCOPODS: RELATIVELY LOW TERPENOID PRODUCTION BY A

LINEAGE MOSTLY DEVOID OF SECRETORY STRUCTURES
The plants with the rst branched stems containing sporangia as spore-forming terminal organs
(collectively called polysporangiophytes) were the extinct Horneophytopsida (rst evidence in the
mid-Silurian period, 430 Mya) and the genus Aglaophyton (rst evidence in the Early Devonian
period, 410 Mya), both of which consisted of nonvascular plants. The earliest plants with simple
vascular tissue were those from the genus Cooksonia (rst evidence in the mid-Silurian period,
433427 Mya) and the rhyniophytes (rst evidence in the Early Devonian period, 410 Mya),
which are also both extinct (Figure 1). The oldest division of extant vascular plants (tracheophytes)
are the lycopods (or, more formally, Lycopodiophyta; rst evidence in the Early Devonian period, 410 Mya), comprising approximately 1,200 modern-day species divided into three orders:
Lycopodiales (club mosses), Isoetales (quillworts), and Selaginellales (spike mosses). During the
Carboniferous period, tree-like lycopods formed large forests that dominated the landscape until
a change in climate caused their collapse during the mid-Pennsylvanian. Their remains formed
massive fossil coal deposits. The lycopods have roots and stems with a central core of vascular tissue
consisting of a cylindrical strand of xylem surrounded by a region of phloem (prostele). The leaves
(microphylls) have only a single, unbranched vein. At the phytochemical level, the transition from
bryophytes to lycopods is characterized by the occurrence of abundant polyphenols: biavonoids,
lignans and lignins derived from sinapyl alcohol (bryophyte lignans characterized thus far contain
exclusively catechol units), selaginellins (uniquely found in the genus Selaginella), anthraquinones,
and chromones (97) (Figure 5). Alkaloids are fairly rare in the genera Selaginella and Isoetes, but
more than 200 representatives of this class of secondary (or specialized) metabolites have been
described in the genus Lycopodium (62).
Recent studies of the spike moss Selaginella moellendorfi have established the presence of gibberellins (39), indicating that lycopods were the rst lineage that evolved the ability to synthesize
these terpenoid hormones. The DELLA and GID1 proteins were demonstrated to interact properly, and this interaction was enhanced by gibberellins (99); one can thus conclude that gibberellin
OH
OCH3
H3CO
HO
OH
HO
HO
OCH3
O
OH
CHO
COOH COOH
H3CO
2', 8''-Biagigenin
(biflavonoid)
OH
Gibberellin A4
(diterpenoid hormone)
()-Lirioresinol
(lignan)
O
OH
HO
OH
HO
HO
HO
O
O
Selaginellin L
Emodin
(anthraquinone)
Umbelliferone
(coumarin)
8-Methyleugenitol
(chromone)
OH
Figure 5
Representative structures for different classes of secondary (or specialized) metabolites in lycopods.
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perception evolved after the divergence of mosses. Although the development of a gibberellin
response system was an important innovation, the lycopods do not appear to be prolic producers of other (non-gibberellin) terpenoids (97). Interestingly, the genome of S. moellendorfi
contains a large family of terpene synthase genes (59), and one would thus expect a more diverse
spectrum of terpenoids. Among the representatives of the terpene synthase family, 18 members
share a common ancestry with typical terpene synthases of higher plants, whereas 48 members
are more closely related to microbial terpene synthases (and have not yet been found in other
plants). Li et al. (59) analyzed the functions of six genes belonging to the microbial terpene
synthaselike clade and demonstrated that the encoded enzymes are indeed mono- and sesquiterpene synthases with diverse product proles. When S. moellendorfi plants were treated with
alamethicin, a peptide antibiotic produced by the phytopathogenic fungus Trichoderma viride
Pers., a fairly complex bouquet of terpenoids and other volatiles was released. These results indicate that terpenoid structural diversity in the lycopods may have been underestimated, and further
experiments to induce the full array of lycopoid terpenoid products remain to be undertaken.

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FERNS: THE PRESENCE OF GLANDULAR TRICHOMES CORRELATES

WITH SECRETION OF FARINOSE WAXES RICH IN FLAVONOIDS
BUT NOT IN TERPENOIDS
Ferns (monilophytes) rst appeared in the fossil record of the Late Devonian period (360 Mya),
but the diversication leading to the genera found today (approximately 1,200 species) likely
occurred much later, during the Cretaceous period, in parallel with the emergence of dominant
angiosperms (81). True leaves with a branched vascular system (macrophylls) rst evolved in the
fern lineage. A short stalk connects the frond (a large, divided leaf ) to the rhizome (a stem that is
often found underground and retains the ability to send out roots and new shoots). The lower leaf
surface of a number of fern species, belonging to several genera of the Pteridaceae, is characterized
by the appearance of a white exudate referred to as farinose wax. The secretion of this material
correlates with the presence of modied multicellular hairs called glandular trichomes. The main
constituents of farinose wax are avonoid aglycones, whereas kaurene-type diterpenoids are only
minor components (98).
The earliest evidence for the occurrence of modied trichomes comes from fossils of the late
Carboniferous (Stephanian stage, 290 Mya). Fronds of Blanzyopteris praedentata and Barthelopteris
germarii, members of the seed ferns (Pteridospermatophyta, comprising seed plants with fern-like
fronds known only from the fossil record), possess several types of trichomes, including glandular
trichomes up to 1 mm in length, with a uniserate stalk of 310 cells, an enlarged apical secretory
cell, and a small-celled lament (Figure 6). It has been hypothesized that a mechanical stimulus
to the lamentfor example, when touched and ruptured by an insectwould release a sticky
exudate from the secretory cell, thereby impeding insect movement (4850, 52). A much greater
diversity of glandular trichomes evolved later within the angiosperm lineage, as discussed in more
detail below.
THE EVOLUTION OF SECRETORY DUCTS AND CAVITIES

IS CORRELATED WITH A REMARKABLE EXPANSION
OF TERPENOID CORE STRUCTURES
Numerous types of secretory structures for lipophilic, terpenoid-containing materials, with sizes
from the micrometer to meter scale, occur in extant gymnosperms and angiosperms. In the context
of a paleobotanical analysis, it is important to note that identifying endogenous secretions into
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Figure 6
Schematic representation of a suggested mechanism for the function of touch-sensitive glandular trichomes
in seed ferns. A glandular trichome is shown (a) before an attack, (b) during the initial opening after insect
contact, (c) during the exudation of secreted contents, and (d ) at the postsecretory stage. Figure adapted from
Reference 50 with permission.
intercellular cavities in fossilized plant remains is technically challenging, with dark dots among
the most frequently misinterpreted features (51). The earliest credible fossil evidence was obtained
with specimens dated to the late Carboniferous (300 Mya) (Figure 1), which had preserved seed
ferns containing secretory cavities in the pinnules (one of the ultimate divisions of the compound
fern leaf) (47, 84) (Figure 7a). Although the chemical composition and ecological roles of these
secretions are unknown, Krings et al. (51) have hypothesized that these secretions may have originated in a physiological process that incidentally provided adaptive benets, including protection
against phytopathogenic microorganisms and/or animals.
The issue of potentially misidentifying secretory structures in the fossil record is avoided when
known contents give rise to fossilized deposits. This is the case for terpenoid oleoresins, which,
under high pressures and temperatures generated by overlying sediments, can polymerize to a solidied, degradation-resistant material widely known as amber. Recent mass spectrometric analyses
have suggested that amber is present in the form of macroscopic blebs in Carboniferous sediments
that formed approximately 320 Mya (12). These results indicate that oleoresins were synthesized
by early gymnosperms, even before the emergence of conifers, the most prolic modern-day producers of secreted terpenoids (the oldest fossils date to the late Carboniferous period, 300 Mya)
(Figure 1). The oleoresins in stems of the conifer genera Abies, Cedrus, Tsuga, and Pseudolarix accumulate in sac-like structures called resin blisters, whereas tube-like resin ducts are present in the
vascular tissues of stems and needles of the genera Pinus, Picea, Larix, and Pseudotsuga (Figure 7b,c).
When the cell layers surrounding such secretory structures are signicantly damagedfor example, by woundingoleoresin is exuded and, when exposed to air, dries down to a highly viscous
and eventually solid exudate, thus forming a physical and chemical barrier. Leaf subdermal secretory cavities are found mostly in the rosids [Rosaceae (e.g., Rosa spp.), Rutaceae (e.g., Citrus spp.),
and Malvaceae (e.g., Eucalyptus spp.)] (Figure 7d ), but their role in stress responses is less well
understood (26).
Conifer oleoresins generally consist of liquid volatiles (mostly monoterpene olens, with
smaller amounts of sesquiterpenes) and dissolved solids (primarily diterpenoids, with very small
amounts of triterpenoids). More than 50 different monoterpenes, with bicyclic pinenes often
the most abundant, have been characterized from volatile distillates of modern-day conifers.
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-Farnesene
(acrylic)
Bisabolene
(monocyclic)
-Bergamotene
(bicyclic)
-Copaene
(tricyclic)
(+)-Cyclosativene
(tetracyclic)
Figure 7
(ad ) Schematic representations of secretory ducts and cavities: secretion bodies in fossilized pinnules of seed ferns (panel a), a conifer
resin blister (panel b), a conifer resin duct (panel c), and a secretory cavity of Citrus peel (panel d ). (e) Structures of different classes of
sesquiterpenes that occur in gymnosperm oleoresins. Panel a adapted from Reference 47 with permission; panel c adapted from
Reference 57 with permission; panel d drawn based on a microscopic image taken by Dr. Glenn W. Turner.
However, the greatest structural diversity, represented by several hundred unique metabolites,
is found within the sesquiterpenes and diterpenoids (>40 and >15 different structural classes, respectively) (71) (Figure 7e). Voluminous oleoresin production, again associated with tremendous
terpenoid structural diversity, also occurs in more recently evolved angiosperms, particularly in
tropical members of the Fabaceae and Dipterocarpaceae (73). A noteworthy example is the diesel
tree (Copaifera langsdorfi Desf.), which contains an oleoresin rich in sesqui- and diterpenes (>100
and >40 different structures, respectively) that can be tapped from tree trunks at a yield of >40 L
per tree per year (14).
Resin ducts and blisters are lined by thin-walled, unlignied, secretory (epithelial) cells, which
are responsible for the biosynthesis and secretion of oleoresins (100), and sheath cells with thicker,
but also unlignied, cell walls (Figure 7b,c). Epithelial cells are characterized by an abundance
of nonphotosynthetic leucoplasts that are associated with membranes of the ER (20). These leucoplasts contain the entire set of enzymes required to synthesize mono- and diterpene core skeletons of oleoresins. Precursors (C5 ) are derived from the MEP pathway and, following elongation
reactions, are converted to terpene hydrocarbons by terpene synthases (Figure 2). Genome-scale
analyses of conifer terpene synthases have not yet been published; however, based on the available transcriptome and other experimental evidence, it is clear that conifer genomes harbor large
families of terpene synthase genes (18, 44). Terpene synthases are also notorious for producing
multiple products, which further increases the capacity to generate terpenoid diversity. Resin acids
are synthesized from C20 hydrocarbon precursors by cytochrome P450dependent oxygenases,
which are also encoded by a very large gene family with hundreds of members in higher plants (68).
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Adaptations to environmental challenges are among the most important mechanisms leading to
the evolution of chemical diversity, and here I briey discuss the interaction between conifers, bark
beetles, and microbial symbionts as an example of the importance of secretory structures in this
process. Wounding, pathogen exposure, or insect attack often leads to the de novo formation of
resin ducts, in addition to those formed constitutively (100). To avoid potentially lethal oleoresinbased defenses (25), most species of bark beetles attack only trees that are already severely stressed.
However, bark beetles can overcome chemical defenses of healthy conifers by mass attack, which
is mediated by terpenoid-based aggregation pheromones (some of which are synthesized from
host terpenes) (8, 89). Interestingly, the emission of host volatiles and bark beetle pheromones can
attract predators, thus leading to a reduction in beetle population (78). Microbial symbionts of
bark beetles (bacteria and fungi) are often able to metabolize the hosts defense terpenoids, thereby
contributing to the complexity of the interaction, which requires adjustments of chemical defenses
for the survival of the plant. Raffa (77) pointed out the importance of scale, with terpenoids playing
roles ranging from defense against an individual bark beetle in a gallery (oleoresin in secretory
structures) to ecological interactions in an entire stand (released plant and bark beetle terpene
volatiles).
LATICIFERS: TUBES CONTAINING STICKY AND TOXIC

CONCOCTIONS OF METABOLITES AND PROTEINS
A milky-white latex has been estimated to be present in more than 10% of all owering plants
(angiosperms)corresponding to approximately 20,000 species (33)with isolated reports of the
occurrence of latex in ferns (genus Regnellidium) (28) and gnetophytes (genus Gnetum) (7). Upon
tissue damage, latex is exuded, driven initially by internal pressure and then by osmotic ow (75);
it is often (but not always) sticky and viscous, thereby impeding the movement of herbivores, and
can contain toxic metabolites and defense-related proteins (46). The secretory structure associated
with the production of latex is called a laticifer, which is a common feature only in the angiosperm
fossil record beginning in the Eocene epoch (50 Mya) (13, 63).
Laticifers were traditionally dened as secretory cell types that accumulate intracellular latex as
an emulsion of lipopolymeric microparticles (containing generally linear cis-1,4-polyisoprene, or
rubber) in conjunction with small molecules and proteins, which is fundamentally different from
the intercellular collection of lipophilic materials in secretory ducts and cavities (26). However,
it is noteworthy that the chemical composition of latex sap is complex and highly variable (and is
thus not a suitable descriptor); its origins and developmental anatomy are more consistent characteristics of laticifers. Nonarticulated laticifers originate from a single cell, elongate during plant
growth, proceed through nuclear divisions without cytokinesis (resulting in multinucleated cells),
and sometimes fuse later to form a branched network, which then continues to enlarge (again,
concomitantly with plant growth). Articulated laticifers, by contrast, have multiple origins within
rows of cells, with a subsequent perforation of cell walls (leading to a continuous, multinucleated cytoplasm), and sometimes form branched structures (following more cell wall degradation)
(Figure 8a). Like secretory ducts and cavities, both types of laticifers are usually associated with
vascular tissues, and they can occur in any organ (although stems and leaves are most commonly
investigated) (33).
Low-molecular-weight constituents of plant latex can include terpenoids (e.g., sesquiterpene
lactones in the genus Lactuca, the diterpenoid phorbol in the genus Euphorbia, or triterpenoid cardenolides in the Apocynaceae), alkaloids (e.g., morphine in opium poppy), and phenolics (esters
of p-coumaric acid with longer-chain hydrocarbons in sweet potato) (Figure 8b). Several proteins with putative defense functions (e.g., cysteine proteases, proteinase inhibitors, polyphenol
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HO
O
O
H
OCH3
H
H
OH
Lactucin
(sesquiterpene lactone)
OAc
H
HO
OH
Oleandrin
(cardenolide)

Figure 8
Laticifers. (a) Schematic representation of an articulated laticifer (red ) in the genus Lactuca (Asteraceae). (b) Representative structures of
terpenoid classes commonly found in laticifers.
oxidases, and lectins) have been described as latex components as well (46). Latex components
can occur in various combinations or as a single, dominant class of metabolites. To assess a possible correlation between latex production and plant tness, Agrawal (1) employed a common
garden study design, in which he collected different populations of a species, grew them at a single
location, and evaluated the impact of the environment on trait expression. This study provided
weak but statistically signicant genetic evidence that natural selection leads to an increase in
latex secretion in common milkweed (Asclepias syriaca L.) (1). Based on a comprehensive analysis
of plants bearing resin ducts or laticifers with their nonsecretory taxonomic sister groups, Farrell
et al. (27) concluded that lineages with secretory canals are much more diverse (in terms of number of species) than their sister groups. Plant families known to contain larger numbers of genera
with laticifers are widely distributed across the angiosperm lineage, but even within a genus, there
are usually species with and without laticifers (33). The chemical composition of latex within a
given laticiferous family also varies (46). The only generalizable trend is that laticifers are most
commonly observed in tropical habitats (58). Two hypotheses (or a combination of both) are consistent with these observations: (a) Laticifers existed in the last common ancestor of laticiferous
clades but were lost in some species (divergent evolution), or (b) laticifers emerged multiple times
in independent lineages (convergent evolution).
Although various hypotheses to explain latex secretions have been discussed historically, convincing experimental evidence is available only for a role in plant defense (although this is not
equally true for all constituents). Several excellent reviews have covered this topic recently (2, 33,
46, 75), and owing to space constraints, I therefore only briey present one example to illustrate
the importance of latex for plant-insect interactions. The latex of the Apocynaceae (in particular
milkweeds in the genus Asclepias) contains high concentrations (up to 30% of latex dry weight)
of cardenolides. Cardenolides are potent inhibitors of Na+ /K+ -ATPases, which are essential for
many physiological processes in animals, including nervous system function. These metabolites
are highly toxic to generalist herbivores (23), but there are specialists, such as the monarch buttery (Danaus plexippus L.), that are largely insensitive to cardenolides. Petschenka et al. (74) recently
provided evidence that amino acid substitutions in the Na+ /K+ -ATPase not only contribute to
cardenolide tolerance by lowering binding afnity, but might be even more important for facilitating sequestration to the exoskeleton. Accumulated cardenolides render butteries both toxic
and distasteful to predators, but sequestration of these metabolites by specialist butteries is most
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effective when feeding on milkweed species with intermediate cardenolide content, indicating a
trade-off between defense and growth (64). The milkweed-monarch interaction is an excellent
example of reciprocal natural selection, in which the plant synthesizes defensive metabolites and
the insect evolves adaptations that allow it to overcome toxicity.

GLANDULAR TRICHOMES: MODIFIED HAIRS

THAT TRAP VOLATILES
The aerial surfaces of land plants often contain epidermal outgrowths called trichomes, the most
common of which are hairs of different kinds and shapes. Terpenoid accumulation is commonly
found in modied (glandular) trichomes that are generally not well preserved in fossils, and their
earliest appearances have thus been a matter of speculation (88). As mentioned above, glandular trichomes were present in fossils of seed ferns dated to the late Carboniferous period (4752) and are
also common features of extant ferns (98). However, these secretory structures are rare in all other
lineages that emerged before angiosperms (69), including the ANITA group of basal angiosperms
(comprising Amborella, Nymphaeales, Illiciales, Trimeniaceae, and Austrobaileyaceae) (17, 94).
Although glandular trichomes are present on the aerial surfaces of certain families of monocotyledons, they are much more common in the eudicots (56). The available evidence suggests that
terpenoid-storing glandular trichomes are a more recent evolutionary invention compared with
the earliest demonstrated appearances of other secretory structures. The distribution patterns
of glandular trichomes across the angiosperm lineage indicate multiple independent emergences
(convergent evolution) (88), but analyses with molecular markers would be highly informative.
Although much progress has been made in understanding nonglandular trichome patterning in
model plant species (43), whether conserved mechanisms exist for glandular trichome initiation is
unknown.
Glandular trichomes generally consist of a basal cell in the epidermal cell layer, one or more
stalk cells, and secretory cells at the apex, with the latter being responsible for the biosynthesis
of terpenoids and other metabolites (Figure 9a,b). Some glandular trichomes secrete terpenoidcontaining oils or resins (e.g., tobacco), whereas others are covered with a thick cuticle and accumulate terpenoid volatiles in a subcuticular cavity (e.g., members of the Lamiaceae). The plastids of
secretory cells are often (but not always) unpigmented, have an amoeboid shape, and lack thylakoid
membranes (16, 20), which is a common feature of terpenoid-producing cells in secretory structures. Leucoplasts are the exclusive source of precursors for mono- and diterpenoids in glandular
trichomes (15, 45). In tomato, sesquiterpenes derived from a Z,Z-farnesyl diphosphate precursor
are also synthesized entirely in leucoplasts (80). E,E-Farnesyl diphosphatederived sesquiterpenes
can be formed from plastidial or cytosolic precursors, or a combination of both (37). Secretory
cell plastids are connected to abundant smooth ER through membrane contact sites. Based on
correlative ultrastructural evidence, Lange & Turner (56) hypothesized that the smooth ER may
play a role in terpenoid secretion; however, in part because genetic tools have only recently become more widely available for certain glandular trichomebearing plants, denitive evidence for
transport mechanisms is still lacking.
The structures of terpenoid metabolites synthesized in glandular trichomes across the
angiosperm lineage are remarkably diverse, ranging from hydrocarbons to highly functionalized
metabolites with terpenoid cores or moieties (56) (Figure 9c). Although terpenoids are common
constituents of glandular trichomes, various other classes of metabolites (e.g., phenylpropenes,
avonoids, methyl ketones, and acyl sugars) are also synthesized in these secretory structures in
some angiosperm lineages. Numerous studies of plant-herbivore and plant-pathogen interactions
have demonstrated that the various cocktails of metabolites in glandular trichomes confer a
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Cuticle
H
O
Secretory
cell
Stalk cell
OH
Basal cell
O
()-Menthol
(monoterpene of peppermint)
Artemisinin
(antimalarial sesquiterpene
of sweet wormwood)

Subcuticular cavity
O
H
OH
AcO
O
H
Secretory
cell
Stalk cell
O
COOCH3
Basal cell
Salvinorin A
(psychoactive diterpene
of diviners sage)
()-trans-9-Tetrahydrocannabinol
(psychoactive meroterpene of Cannabis)
Figure 9
(a,b) Schematic representations of a peppermint glandular trichome at presecretory (panel a) and postsecretory (panel b) stages.
Terpenoid essential oil ( yellow) is deposited in a subcuticular cavity formed after the thick cuticle separates from the biosynthetically
active secretory cells ( gray). (c) Representative classes of terpenoids accumulated in glandular trichomes of different angiosperms.
Panels a and b adapted from Reference 56 with permission.
certain level of resistance against pests and are therefore important contributors to the enormous
diversication of angiosperms (29).
SECRETORY STRUCTURES: COMMON FEATURES

OF PHYTOCHEMICAL FACTORIES
Ultrastructural and Metabolic Specialization
Terpenoids and other constituents of secretory structures are synthesized in specialized, mostly
nonphotosynthetic, cells. These epithelial (secretory) cells generally contain large numbers of
leucoplasts ensheathed with abundant smooth ER. Although the transport of lipophilic secondary
(or specialized) metabolites into secretory structures is still poorly understood, a mechanism involving the Golgi secretory pathway, which is known to be involved in the biosynthesis and
translocation of cell wall building blocks (72), is unlikely owing to the lack of Golgi bodies and associated vesicles (56). Evidence for the remarkable metabolic specialization of glandular trichomes
and secretory cavities comes from transcriptomic and proteomic data sets obtained with isolated
epithelial (secretory) cells. These cells express at high levels genes involved in the biosynthesis of
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secreted lipophilic metabolites from imported carbohydrate precursors, whereas pathways leading
to other metabolic end products are expressed only at very low levels during secretion (56, 92). The
biosynthesis of larger amounts of terpenoids in plants appears to require cells with a dedicated
biochemical machinery and intra- or extracellular structures to facilitate the sequestration and
accumulation of these biologically active metabolites. Terpenoid chemical diversity in secretory
structures results from reactions catalyzed by families of (often promiscuous) terpene synthases to
form core structures and modifying enzymes to decorate these structural cores (18, 44, 68).

Jasmonates Regulate the Formation of Secretory Structures

Jasmonate application to conifer stems causes the formation of traumatic resin ducts in certain
species, concomitant with an induction of terpenoid resin secretion (41, 42 65). Jasmonate application also induces the emergence of an increased number of glandular trichomes on tomato
leaves (10, 90). In the liverwort Plagiochasma appendiculatum, which contains abundant oil bodies,
jasmonate treatment increases terpenoid biosynthesis at the transcriptional level (19). Conversely,
in transgenic tomato plants with impaired expression of components of the jasmonate biosynthetic or signal transduction pathways, the number of glandular trichomes is signicantly reduced
(9, 60). Henery et al. (38) did not nd evidence for jasmonate-induced terpenoid production in
Eucalyptus leaves that contain fairly large numbers of secretory cavities. However, whether the
constitutive formation of these secretory structures might involve jasmonates remains to be determined. The role of jasmonates in triggering diverse defense responses is well established (95),
and the jasmonate-regulated accumulation of terpenoids in secretory structures is an integral part
of plant-insect and plant-pathogen interactions in many plant lineages.
DISCLOSURE STATEMENT
The author is not aware of any afliations, memberships, funding, or nancial holdings that might
be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
I apologize for the fact that, owing to length restrictions, not all relevant original papers and
review articles could be considered and cited. This material is based on work supported by the US
Department of Energy, Ofce of Science, Ofce of Basic Energy Sciences, under award number
DE-FG02-09ER16054.
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