Date post: | 19-Feb-2018 |
Category: |
Documents |
Upload: | sabrina-queiroz |
View: | 214 times |
Download: | 0 times |
of 21
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
1/21
PP66CH19-Lange ARI 12 January 2015 14:13
RE
V I E WS
I
N
AD V A
N
C
E
The Evolution of PlantSecretory Structures and theEmergence of TerpenoidChemical Diversity
Bernd Markus LangeInstitute of Biological Chemistry and M.J. Murdock Metabolomics Laboratory, WashingtonState University, Pullman, Washington 99164-6340; email: [email protected]
Annu. Rev. Plant Biol. 2015. 66:19.119.21
TheAnnual Review of Plant Biologyis online atplant.annualreviews.org
This articles doi:10.1146/annurev-arplant-043014-114639
Copyright c2015 by Annual Reviews.All rights reserved
Keywords
fossil record, glandular trichome, resin duct, secretory cavity
Abstract
Secretory structures in terrestrial plants appear to have first 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 epider-
mal 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 thatshaped plant-herbivore and plant-pathogen interactions. Although this re-
view 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.
19.1
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
2/21
PP66CH19-Lange ARI 12 January 2015 14:13
CGAs: charophyceangreen algae
Contents
EARLY TERRESTRIAL ALGAE: DEVELOPMENTAL
AND METABOLIC ADAPTATIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19.2BRYOPHYTES: 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 P HYTOCHEMICAL F ACTORIES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .19.16
Ultrastructural and Metabolic Specialization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .19.16
Jasmonates Regulate the Formation of Secretory Structures. . . . . . . . . . . . . . . . . . . . . . .19.17
EARLY TERRESTRIAL ALGAE: DEVELOPMENTALAND METABOLIC ADAPTATIONS
Land plants (embryophytes) evolved as a monophyletic group from multicellular algae calledcharophycean green algae (CGAs) (Figure 1). The reconstruction of ancestral CGAs prior to
the emergence of land plants is very difficult because (a) extant CGAs are phenotypically diverse,
ranging from microscopic unicellular flagellates to complex, branched filaments over a meter in
length, and (b) both elaborations (leading to increased complexity) and simplifications (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 fixation 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 autofluorescent material with properties similar
19.2 Lange
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
3/21
PP66CH19-Lange ARI 12 January 2015 14:13
Time (Mya)
Precambrian eon
4,600 2,500 540
ARCHEAN PROTEROZOIC
Paleozoic era
540 490 445 415 355355 300 250
TRIASSIC JURASSIC
Mesozoic era250 200 145 65
CRETACEOUS
CAMBRIAN SILURIANORDOVICIAN DEVONIAN CARBONIFEROUS PERMIAN
4,600Accretionof Earth
3,800Earliest life
(carbon isotopeevidence)
2,700Oldest oxygenicphotosynthetic
stromatolites
2,7202,470Oldest fossils
with hopanoids(prokaryotic tri-
terpene biomarker)
1,700Oldest fossilswith steranes
(eukaryotic tri-terpene biomarker)
1,200Oldest
unquestionedalgal fossils
~700Split of Chlorophyta
and Streptophyta(including CGAsthat gave rise to
land plants)
~470Oldest fossilsassignable to
bryophytes (spores)
Oil bodies (?)
450390Rhyniophytes
418407
Lycophyta(oldest extantvascular plants)
~365True
gymnosperms
360250Seed ferns
(Pteridospermatophyta)
~320
Oldest fossilswith diterpenoids(amber)
Resin ducts/blisters (?)
~300Glandulartrichomes
on seed fern ~250
Oldest fossilswith oleananes(angiosperm tri-
terpene biomarker)
136130Oldest
angiospermfossils
~100Angiosperm
radiation
Figure 1
Time line of land plant evolution based on fossil evidence. Green indicates the emergence of new plant lineages, blue indicates theoldest 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 definitive chemical and molecular evidence for the presence of sporopollenin
in CGAs is certainly needed, possible functions of the autofluorescent 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 (cy-
tokinin), salicylic acid, and jasmonic acid; seeFigure 2] were detected at low (in some cases very
low) levels in the filamentous CGAKlebsormidium flaccidum, a species regarded as still relativelyclosely 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 19.3
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
4/21
PP66CH19-Lange ARI 12 January 2015 14:13
Ethylene
Hormone class Biosynthetic precursors Distribution Comments
C B L M G A
Indole-3-acetic acid (auxin) C B L M G A
Abscisic acid CarotenoidsC B L M G A
?
?
?
Salicylic acid C B L M G A
?
Glycerolipid
C B L M G A? ?
CarotenoidsC B L M G A
B L M G A
SterolsL M G A
?
B
?
Zeatin (cytokinin) DMAPP and adenineC B L M G A
(+)-Orobanchol (strigolactone)
Jasmonic acid (oxilipin)
GA3(gibberellin)
Brassinolide (brassinosteroid)
ent-Kaurene (diterpene)
L-Methionine,
S-AdenosylmethionineCH2
OH
OHNH
COOH
COOH
COOH
COOH
OH
OH
OHH
HH
H
OC
HO
HO
HO
OH
O
OOO
O
O
O
O
OH
O
NH
O
NH
N
N
N
H2C
L-Trypothophanor indole
L-Phenylalanineor isochorismic acid
The presence of brassinosteroidsin bryophytes has beendemonstrated in a liverwort, butthe presence/absence of the signaltransduction pathway has not yet
been investigated
Bryophytes may produce onlyprecursors of gibberellins and donot have fully functionalcomponents of gibberellin signaltransduction
Very low concentration reported
in CGAs; several biosyntheticgenes and all signal transductioncomponents missing in CGAs;bryophytes produce precursors ofjasmonic acid
Some signal transductioncomponents missing in CGAs
CGAs and all lineages of landplants respond to exogenousstrigolactones
Some biosynthetic genes andsignal transduction componentsmissing in CGAs
Certain signal transductioncomponents possibly missing inCGAs
Some signal transductioncomponents missing in CGAs
Some signal transduction
components missing in CGAs
19.4 Lange
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
5/21
PP66CH19-Lange ARI 12 January 2015 14:13
D-GAP Pyruvate
PLASTID CYTOSOL MITOCHONDRIONPer
ER
Acetyl-CoA
MEP pathway
Isoprene
Monoterpenes
Sesquiterpenes[ ]
Diterpenes
Carotenoids
Phytol
TocopherolsPhylloquinone
Chlorophylls
DiterpenoidsGibberellins
Plastoquinone
F
MonoterpenoidsF
Abscisic acidStrigolactones
FC
C5 C5C5
C10
C20
C40
C45
C15C15
C15
C45C30
MVA pathway
?
Cytokinins CytokininsSesquiterpenes
Sterols
Triterpenes
Brassinosteroids
Sesquiterpenoids
F
F
Triterpenoids
ER
Ubiquinone
Polyterpenes (dolichols, rubber)
Figure 3
Overview of terpenoid biosynthesis in plants. The major terpenoid products of secretory structures are shown in blue. The exchange ofterpenoid pathway intermediates between subcellular compartments involves unidentified transporters ( yellow circle with question mark).The C box shows the plastidial localization of carotenoid cleavage enzymes involved in the biosynthesis of abscisic acid andstrigolactones; the F boxes show the locations of enzymes involved in the functionalization of terpenoid core structures (cytosol andER). Abbreviations: CoA, coenzyme A; ER, endoplasmic reticulum; GAP, glyceraldehyde 3-phosphate; MEP, 2C-methyl-D-erythritol4-phosphate; MVA, mevalonic acid; Per, peroxisome.
DMAPP:dimethylallyl
diphosphateIPP: isopentenyldiphosphate
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., strigolactone-controlled 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 briefly 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 con-
sists of reactions leading to the formation of dimethylallyl diphosphate (DMAPP) and isopen-
tenyl 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
Figure 2
Occurrence of hormones across different plant lineages. The boxed letters indicate the presence of a particular hormone incharophycean green algae (C), bryophytes (B), lycopods (L), monilophytes (M), gymnosperms (G), and angiosperms (A). A questionmark indicates that components of the biosynthetic and/or signal transduction pathway for a particular hormone are not detectable inrepresentative genomes. Abbreviations: CGAs, charophycean green algae; DMAPP, dimethylallyl diphosphate.
www.annualreviews.org Evolution of Plant Secretory Structures 19.5
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
6/21
PP66CH19-Lange ARI 12 January 2015 14:13
MVA: mevalonic acid
ER: endoplasmicreticulum
MEP: 2C-methyl-D-erythritol4-phosphate
mevalonic acid (MVA) pathway operates primarily in the cytosol and the endoplasmic reticu-
lum (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-specific prenyltransferases (Figure 3). The condensation of one
moleculeof DMAPPand onemoleculeof IPPto geranyl diphosphate (C10) is catalyzed by plastidial
geranyl diphosphate synthase (in the genusSolanum, neryl diphosphate synthase is a second C 10-
generating prenyltransferase) (55). A condensationof one moleculeof DMAPP withtwo molecules
of IPP generatesE,E-farnesyl diphosphate (C15), which is catalyzed by farnesyl diphosphate syn-
thase isoforms localized to the cytosol, plastids, mitochondria, or peroxisomes (the genusSolanum
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 syn-
thases generate the precursors for carotenoids (C40) and plastoquinone (C45). Sterols/triterpenes
and derived steroids are synthesized from C30precursors by ER-localized enzymes. Longer-chain
dolichols are synthesized bycis-prenyltransferase isoforms localized to the ER (61). A long-chaintrans-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
first 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 sidechain 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 LIVERWORTSCONTAIN A WEALTH OF TERPENOID STRUCTURES
The invasion of the land by plants (terrestrialization) was one of the most significant 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 earli-
est 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 importantto note that, based on multiplelines
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
19.6 Lange
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
7/21
PP66CH19-Lange ARI 12 January 2015 14:13
bryophyte-like plants at the base of the embryophyte clade (32). Important adaptations facil-
itating 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 promi-
nently included the production of novel secondary (or specialized) metabolites. They evolved the
ability to synthesize various soluble polyphenols, such as phenylpropanoid and bibenzyl deriva-
tives, flavonoids, coumarins, and lignans consisting of catechol units (although not all extant rep-
resentatives accumulate these metabolites; e.g., flavonoids and lignans are absent from hornworts
and mosses, respectively) (4, 5, 9, 76, 91). Various studies reported on the occurrence of lignin-
and 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 lack-
ing (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 inter-
preted with caution. Nitrogen-containing metabolites, such as alkaloids, are only rarely found in
bryophytes (46), although endosymbiotic nitrogen fixation, 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 bioticand abiotic stresses (79), butsignificant changes with regardto 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 synthesizingent-kaurene
andent-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 functionsduring 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 diver-
sity 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 bod-
ies of angiosperms (36). There is considerable debate about the organellar origin of bryophyte
oil bodies, in part because older studies employed fixation techniques that were inadequate forsubsequent microscopic studies. More recent investigations have indicated that the primary (if
not exclusive) mechanism of oil body formation in bryophytes involves an assembly from subdo-
mains of the ER (36). However, significantly more experimental evidence with a larger number
of species is required to even begin to understand the ontogeny of these important subcellular
structures.
www.annualreviews.org Evolution of Plant Secretory Structures 19.7
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
8/21
PP66CH19-Lange ARI 12 January 2015 14:13
O
O
O
O
OO
O
H
H
H
H
H
H
H
H
OAc
CHO
CHO
COOH
CHO
OAc
AcO
Bicyclohumulenone(woody)
Polygodial(pungent and insecticidal)
Plagiochiline A(nematocidal)
Anastreptine A(bitter)
ent-Kaurenoic acid(hormone precursor)
ent-Trachyloban-17-al(antimicrobial)
cis-Pinocarveylacetate
(turpentine-like)
aa b
c
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 precursorent-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 diphos-
phate (Figure 3), are present in both plastids and oil bodies. Further studies of plastidial andoil bodyspecific isoforms of these enzymes, should their presence be confirmed molecularly and
biochemically, would provide opportunities to investigate the role of paralogous gene duplicates
or alternative splicing as drivers of diversification.
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 beendescribed 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, fish, other plants, and animal
cell lines (6). Although high terpenoid levels are certainly not a prerequisite for success, as evi-
denced 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 facilitatedthe 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).
19.8 Lange
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
9/21
PP66CH19-Lange ARI 12 January 2015 14:13
LYCOPODS: RELATIVELY LOW TERPENOID PRODUCTION BY ALINEAGE MOSTLY DEVOID OF SECRETORY STRUCTURES
The plants with the first branched stems containing sporangia as spore-forming terminal organs
(collectively called polysporangiophytes) were the extinct Horneophytopsida (first evidence in themid-Silurian period,430 Mya) and the genusAglaophyton(first 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 genusCooksonia (first evidence in the mid-Silurian period,
433427 Mya) and the rhyniophytes (first evidence in the Early Devonian period, 410 Mya),
which are also both extinct (Figure 1). The oldest divisionof extant vascular plants (tracheophytes)
are the lycopods (or, more formally, Lycopodiophyta; first evidence in the Early Devonian pe-
riod,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 fossilcoaldeposits. Thelycopods have roots andstemswitha 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 frombryophytes to lycopods is characterized by the occurrence of abundant polyphenols: biflavonoids,
lignans and lignins derived from sinapyl alcohol (bryophyte lignans characterized thus far contain
exclusively catechol units), selaginellins (uniquely found in the genusSelaginella), anthraquinones,
and chromones (97) (Figure 5). Alkaloids are fairly rare in the genera Selaginellaand Isoetes, but
more than 200 representatives of this class of secondary (or specialized) metabolites have been
described in the genusLycopodium(62).
Recent studies of the spike moss Selaginella moellendorffiihave established the presence of gib-
berellins (39), indicating that lycopods were the first lineage that evolved the ability to synthesize
these terpenoid hormones. The DELLA and GID1 proteins were demonstrated to interact prop-
erly, and this interaction was enhanced by gibberellins (99); one can thus conclude that gibberellin
OH
OH
OH OHO
O
O
O
O
O
OH
OH
OH O
O
O
OO
2', 8''-Biagigenin(biavonoid)
Emodin(anthraquinone)
()-Lirioresinol(lignan)
Umbelliferone(coumarin)
8-Methyleugenitol(chromone)
Gibberellin A4(diterpenoid hormone)
Selaginellin L
OHO
HO
HO
HO
HOHO
H3CO
OCH3
OCH3
CHO
COOH COOH
H3CO
HO
Figure 5
Representative structures for different classes of secondary (or specialized) metabolites in lycopods.
www.annualreviews.org Evolution of Plant Secretory Structures 19.9
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
10/21
PP66CH19-Lange ARI 12 January 2015 14:13
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 prolific pro-
ducers of other (non-gibberellin) terpenoids (97). Interestingly, the genome of S. moellendorffii
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 sesquiter-
pene synthases with diverse product profiles. When S. moellendorffiiplants 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 indi-
cate 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.
FERNS: THE PRESENCE OF GLANDULAR TRICHOMES CORRELATESWITH SECRETION OF FARINOSE WAXES RICH IN FLAVONOIDSBUT NOT IN TERPENOIDS
Ferns (monilophytes) first appeared in the fossil record of the Late Devonian period (360 Mya),
but the diversification 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) first 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, belongingto several generaof 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 modified multicellular hairs called glandular trichomes. The main
constituents of farinose wax are flavonoid aglycones, whereas kaurene-type diterpenoids are only
minor components (98).The earliest evidence for the occurrence of modified trichomes comes from fossils of the late
Carboniferous (Stephanianstage,290Mya). FrondsofBlanzyopterispraedentataand 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 filament (Figure 6). It has been hypothesized that a mechanical stimulus
to the filamentfor 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 CAVITIESIS CORRELATED WITH A REMARKABLE EXPANSIONOF TERPENOID CORE STRUCTURES
Numerous types of secretory structures for lipophilic, terpenoid-containing materials, with sizes
from themicrometer to meter scale, occurin extantgymnospermsand angiosperms.In thecontext
of a paleobotanical analysis, it is important to note that identifying endogenous secretions into
19.10 Lange
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
11/21
PP66CH19-Lange ARI 12 January 2015 14:13
a b c d
Figure 6
Schematic representation of a suggested mechanism for the function of touch-sensitive glandular trichomesin 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 fromReference 50 with permission.
intercellular cavities in fossilized plant remains is technically challenging, with dark dots among
the mostfrequentlymisinterpreted 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 origi-
nated in a physiological process that incidentally provided adaptive benefits, 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 so-lidified,degradation-resistant materialwidelyknown as amber. Recent massspectrometric 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 prolific modern-day pro-
ducers of secreted terpenoids (the oldest fossils date to the late Carboniferous period,300 Mya)
(Figure 1). The oleoresins in stems of the conifer generaAbies,Cedrus,Tsuga, andPseudolarixac-
cumulate in sac-like structures called resin blisters, whereas tube-like resin ducts are present in the
vasculartissues of stems and needles of the generaPinus,Picea,Larix,andPseudotsuga (Figure7b,c).
When the cell layers surrounding such secretory structures are significantly damagedfor exam-
ple, 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 secre-
tory cavities are found mostly in the rosids [Rosaceae (e.g.,Rosaspp.), Rutaceae (e.g.,Citrusspp.),
and Malvaceae (e.g.,Eucalyptusspp.)] (Figure 7d), but their role in stress responses is less well
understood (26).
Conifer oleoresins generally consist of liquid volatiles (mostly monoterpene olefins, 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.
www.annualreviews.org Evolution of Plant Secretory Structures 19.11
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
12/21
PP66CH19-Lange ARI 12 January 2015 14:13
cba d
e
-Farnesene(acrylic)
-Copaene(tricyclic)
(+)-Cyclosativene(tetracyclic)
Bisabolene(monocyclic)
-Bergamotene(bicyclic)
H
H
H
Figure 7
(ad) Schematic representations of secretory ducts and cavities: secretion bodies in fossilized pinnules of seed ferns (panel a), a coniferresin blister (panelb), a conifer resin duct (panelc), and a secretory cavity ofCitruspeel (paneld). (e) Structures of different classes ofsesquiterpenes that occur in gymnosperm oleoresins. Panelaadapted from Reference 47 with permission; panelcadapted fromReference 57 with permission; panelddrawn 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, re-
spectively) (71) (Figure 7e). Voluminous oleoresin production, again associated with tremendousterpenoid 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 langsdorffiiDesf.), 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, unlignified, secretory (epithelial) cells, which
areresponsible for the biosynthesis and secretion of oleoresins (100), and sheath cells with thicker,
but also unlignified, 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 leu-
coplasts contain the entire set of enzymes required to synthesize mono- and diterpene core skele-
tons 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 avail-able 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).
19.12 Lange
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
13/21
PP66CH19-Lange ARI 12 January 2015 14:13
Adaptationsto environmentalchallenges are among the most important mechanismsleading to
the evolutionof chemicaldiversity,and here I brieflydiscuss theinteraction 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 oleoresin-
based 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 (bacteriaand fungi) areoften able to metabolize thehosts defense terpenoids, thereby
contributing to the complexity of the interaction, which requires adjustments of chemical defenses
for the survivalof 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 TOXICCONCOCTIONS OF METABOLITES AND PROTEINS
A milky-white latex has been estimated to be present in more than 10% of all flowering plants
(angiosperms)corresponding to approximately 20,000 species (33)with isolated reports of the
occurrence of latex in ferns (genusRegnellidium) (28) and gnetophytes (genusGnetum) (7). Upon
tissue damage, latex is exuded, driven initially by internal pressure and then by osmotic flow (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 secretorystructure 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 defined as secretorycell types that accumulate intracellular latex as
an emulsion of lipopolymeric microparticles (containing generally linearcis-1,4-polyisoprene, orrubber) 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 char-
acteristics 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, multinucle-
ated 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 genusLactuca, the diterpenoid phorbol in the genusEuphorbia, or triterpenoid car-
denolides in the Apocynaceae), alkaloids (e.g., morphine in opium poppy), and phenolics (esters
ofp-coumaric acid with longer-chain hydrocarbons in sweet potato) (Figure 8b). Several pro-
teins with putative defense functions (e.g., cysteine proteases, proteinase inhibitors, polyphenol
www.annualreviews.org Evolution of Plant Secretory Structures 19.13
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
14/21
PP66CH19-Lange ARI 12 January 2015 14:13
ba
OH
OH
OAc
O
OO
OH
H
H
HH
O
O
O
Lactucin(sesquiterpene lactone)
Oleandrin(cardenolide)
HO
HO
OCH3
Figure 8
Laticifers. (a) Schematic representation of an articulated laticifer (red) in the genusLactuca(Asteraceae). (b) Representative structures ofterpenoid 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 pos-
sible correlation between latex production and plant fitness, 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 significant 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 num-
ber 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 mostcommonly observed in tropical habitats (58). Two hypotheses (or a combination of both) are con-
sistent 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, con-
vincing 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 briefly present one example to illustrate
the importance of latex for plant-insect interactions. The latex of the Apocynaceae (in particular
milkweeds in the genusAsclepias) 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 butter-fly (Danaus plexippusL.), 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 affinity, but might be even more important for facil-
itating sequestration to the exoskeleton. Accumulated cardenolides render butterflies both toxic
and distasteful to predators, but sequestration of these metabolites by specialist butterflies is most
19.14 Lange
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
15/21
PP66CH19-Lange ARI 12 January 2015 14:13
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 HAIRSTHAT 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 modified (glandular) trichomes that are generally not well preserved in fossils, and their
earliestappearances have thus beena matter of speculation (88).As mentioned above, glandular tri-
chomes 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
(comprisingAmborella, Nymphaeales, Illiciales, Trimeniaceae, and Austrobaileyaceae) (17, 94).
Although glandular trichomes are present on the aerial surfaces of certain families of monocotyle-dons, 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 terpenoid-
containing oils or resins (e.g., tobacco), whereas others are covered with a thick cuticle and accu-
mulate terpenoidvolatiles in a subcuticularcavity (e.g., members of the Lamiaceae). The plastidsofsecretorycellsare often (but notalways) unpigmented, have an amoeboid shape,and lack thylakoid
membranes (16, 20), which is a common feature of terpenoid-producing cells in secretory struc-
tures. Leucoplasts are the exclusive source of precursors for mono- and diterpenoids in glandular
trichomes (15, 45). In tomato, sesquiterpenes derived from aZ,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 be-
come more widely available for certain glandular trichomebearing plants, definitive 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 functionalizedmetabolites with terpenoid cores or moieties (56) (Figure 9c). Although terpenoids are common
constituents of glandular trichomes, various other classes of metabolites (e.g., phenylpropenes,
flavonoids, 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
www.annualreviews.org Evolution of Plant Secretory Structures 19.15
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
16/21
PP66CH19-Lange ARI 12 January 2015 14:13
c
b
a
OH
COOCH3
AcO
O
O
O
O
O
O O
O
O
O
H H
H
H
H
H
H
OH
()-Menthol(monoterpene of peppermint)
()-trans-9-Tetrahydrocannabinol(psychoactive meroterpene of Cannabis)
Salvinorin A(psychoactive diterpene
of diviners sage)
Subcuticular cavity
Cuticle
Artemisinin(antimalarial sesquiterpene
of sweet wormwood)
Secretorycell
Stalk cell
Basal cell
Secretorycell
Stalk cell
Basal cell
Figure 9
(a,b) Schematic representations of a peppermint glandular trichome at presecretory (panela) and postsecretory (panelb) stages.Terpenoid essential oil (yellow) is deposited in a subcuticular cavity formed after the thick cuticle separates from the biosyntheticallyactive secretory cells (gray). (c) Representative classes of terpenoids accumulated in glandular trichomes of different angiosperms.
Panelsaandb adapted from Reference 56 with permission.
certain level of resistance against pests and are therefore important contributors to the enormous
diversification of angiosperms (29).
SECRETORY STRUCTURES: COMMON FEATURESOF 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 in-volving 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 as-
sociated 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
19.16 Lange
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
17/21
PP66CH19-Lange ARI 12 January 2015 14:13
secreted lipophilic metabolites from imported carbohydrate precursors, whereas pathways leading
to other metabolicend products areexpressed only at very lowlevels duringsecretion (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 ap-
plication also induces the emergence of an increased number of glandular trichomes on tomato
leaves (10, 90). In the liverwortPlagiochasma 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 biosyn-
thetic or signal transduction pathways, the number of glandular trichomes is significantly reduced
(9, 60). Henery et al. (38) did not find 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 de-
termined. 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 affiliations, memberships, funding, or financial holdings that might
be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTSI 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, Office of Science, Office of Basic Energy Sciences, under award number
DE-FG02-09ER16054.
LITERATURE CITED
1. Agrawal AA. 2005. Natural selection on common milkweed (Asclepias syriaca) by a community of special-
ized insect herbivores.Evol. Ecol. Res. 7:65167
2. Agrawal AA, Petschenka G, Bingham RA, Weber MG, Rasmann S. 2012. Toxic cardenolides: chemical
ecology and coevolution of specialized plantherbivore interactions.New Phytol.194:2845
3. Anterola A, Shanle E, Mansouri K, Schuette S, Renzaglia K. 2009. Gibberellin precursor is involved in
spore germination in the mossPhyscomitrella patens.Planta229:100374. Asakawa Y, Ludwiczuk A, Nagashima F. 2013. Chemical constituents of Anthocerotophyta. InChemical
Constituents of Bryophytes: Bio- and Chemical Diversity, Biological Activity, and Chemosystematics, pp. 60717.
Prog. Chem. Org. Nat. Prod. Vol. 95. Vienna: Springer
5. Asakawa Y, Ludwiczuk A, Nagashima F. 2013. Chemical constituents of Bryophyta. In Chemical Con-
stituents of Bryophytes: Bio- and Chemical Diversity, Biological Activity, and Chemosystematics, pp. 563605.
Prog. Chem. Org. Nat. Prod. Vol. 95. Vienna: Springer
www.annualreviews.org Evolution of Plant Secretory Structures 19.17
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
18/21
PP66CH19-Lange ARI 12 January 2015 14:13
6. Asakawa Y, Ludwiczuk A, Nagashima F. 2013. Chemical constituents of Marchantiophyta. InChemical
Constituents of Bryophytes: Bio- and Chemical Diversity, Biological Activity, and Chemosystematics, pp. 25561.
Prog. Chem. Org. Nat. Prod. Vol. 95. Vienna: Springer
7. Behnke HD, Herrmann S. 1978. Fine structure and development of laticifers in Gnetum gnemon L.
Protoplasma94:371848. Blomquist GJ, Figueroa-Teran R, Aw M, Song M, Gorzalski A, et al. 2010. Pheromone production in
bark beetles.Insect Biochem. Mol. Biol. 40:699712
9. Bosch M, WrightLP, Gershenzon J, Wasternack C, Hause B, et al. 2014. Jasmonic acid andits precursor
12-oxophytodienoic acid control different aspects of constitutive and induced herbivore defenses in
tomato.Plant Physiol.166:396410
10. Boughton AJ, Hoover K, Felton GW. 2005. Methyl jasmonate application induces increased densities
of glandular trichomes on tomato, Lycopersicon esculentum.J. Chem. Ecol.31:221116
11. Bowman JL. 2013. Walkabout on the long branches of plant evolution.Curr. Opin. Plant Biol.16:7077
12. Bray PS, Anderson KB. 2009. Identification of Carboniferous (320 million years old) class Ic amber.
Science326:13234
13. Call V, Dilcher D. 1997. The fossil record ofEucommia(Eucommiaceae) in North America.Am. J. Bot.
84:798
14. Calvin M. 1980. Hydrocarbons from plants: analytical methods and observations. Naturwissenschaften
67:5253315. Carde JP. 1984. Leucoplasts: a distinct kind of organelles lacking typical 70S ribosomes and free thy-
lakoids.Eur. J. Cell Biol.34:1826
16. Carpenter KJ. 2006. Specialized structures in the leaf epidermis of basal angiosperms: morphology,
distribution, and homology.Am. J. Bot.93:66581
17. Charon J, Launay J, Card e JP. 1985. Spatial organization and volume density of leucoplasts in pine
secretory cells.Protoplasma138:4553
18. Chen F, Tholl D, Bohlmann J, Pichersky E. 2011. The family of terpene synthases in plants: a mid-size
family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J.
66:21229
19. Cheng A, Wang L, Sun Y, Lou H. 2012. Identification and expression analysis of key enzymes of the
terpenoids biosynthesis pathway of a liverwortPlagiochasma appendiculatumby EST analysis.Acta Physiol.
Plant.35:10718
20. Cheniclet C, Carde JP. 1985. Presence of leucoplasts in secretory cells and of monoterpenes in the
essential oil: a correlative study.Israel J. Bot.34:2193821. Delaux PM, Xie X, Timme RE, Puech-Pages V, Dunand C, et al. 2012. Origin of strigolactones in the
green lineage.New Phytol.195:85771
22. Delwiche CF,GrahamLE, Thomson N. 1989. Lignin-like compoundsand sporopollenin in Coleochaete,
an algal model for land plant ancestry. Science245:399401
23. Dussourd DE, Hoyle AM. 2000. Poisoned plusiines: toxicity of milkweed latex and cardenolides to some
generalist caterpillars.Chemoecology10:1116
24. Elbert W, Weber B, Burrows S, Steinkamp J, Budel B, et al. 2012. Contribution of cryptogamic covers
to the global cycles of carbon and nitrogen. Nat. Geosci.5:45962
25. Everaerts C, Gregoire JC, Merlin J. 1988. The toxicity of Norway spruce monoterpenes to two bark
beetle species and their associates. In Mechanisms of Woody Plant Defenses Against Insects, ed. WJ Mattson,
J Levieux, C Bernard-Dagan, pp. 33544. New York: Springer
26. Fahn A. 1988. Secretory tissues in vascular plants.New Phytol.108:22957
27. Farrell BD, Dussourd DE, Mitter C. 1991. Escalation of plant defense: Do latex and resin canals spur
plant diversification?Am. Nat.138:88190028. Foster AS Gifford EM. 1974.Comparative Morphology of Vascular Plants. San Francisco: Freeman
29. Glas JJ, Schimmel BC, Alba JM, Escobar-Bravo R, Schuurink RC, Kant MR. 2012. Plant glandular
trichomes as targets for breeding or engineering of resistance to herbivores. Int. J. Mol. Sci. 13:17077
103
30. Goiris K, Muylaert K, Voorspoels S, Noten B, De Paepe D, et al. 2014. Detection of flavonoids in
microalgae from different evolutionary lineages. J. Phycol.50:48392
19.18 Lange
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
19/21
PP66CH19-Lange ARI 12 January 2015 14:13
31. Graham LE, Gray J. 2001. The origin, morphology, and ecophysiology of early embryophytes: neon-
tological and paleontological perspectives. In Plants Invade the Land: Evolutionary and Environmental
Perspectives, ed. PG Gensel, D Edwards, pp. 14058. New York: Columbia Univ. Press
32. Graham LE, Lewis LA, Taylor W, Wellman C, Cook M. 2014. Early terrestrialization: transition from
algal to bryophyte grade. InPhotosynthesis in Bryophytes and Early Land Plants, ed. DT Hanson, SK Rice,pp. 928. Adv. Photosynth. Respir. Vol. 37. Amsterdam: Springer
33. Hagel JM, Yeung EC, Facchini PJ. 2008. Got milk? The secret life of laticifers.Trends Plant Sci.13:631
39
34. Hayashi K, Horie K, Hiwatashi Y, Kawaide H, Yamaguchi S, et al. 2010. Endogenous diterpenes de-
rived froment-kaurene, a common gibberellin precursor, regulate protonema differentiation of the moss
Physcomitrella patens.Plant Physiol.153:108597
35. Hayashi K, Kawaide H, Notomi M, Sakigi Y, Matsuo A, Nozaki H. 2006. Identification and functional
analysis of bifunctional ent-kaurene synthase from themossPhyscomitrella patens.FEBS Lett. 580:617581
36. He X, SunY, ZhuRL. 2013.The oilbodies of liverworts: uniqueand importantorganelles in land plants.
Crit. Rev. Plant Sci.32:293302
37. Hemmerlin A, Harwood JL, Bach TJ. 2012. A raison detre for two distinct pathways in the early steps
of plant isoprenoid biosynthesis?Prog. Lipid Res.51:95148
38. HeneryML, WallisIR, StoneC, Foley WJ.2008. Methyljasmonate does notinduce changes inEucalyptus
grandisleaves that alter the effect of constitutive defense on larvae of a specialist herbivore. Oecologia156:84759
39. Hirano K, Nakajima M, Asano K, Nishiyama T, Sakakibara H, et al. 2007. The GID1-mediated gib-
berellin perception mechanism is conserved in the lycophyte Selaginella moellendorffiibut not in the
bryophytePhyscomitrella patens.Plant Cell19:305879
40. Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N, et al. 2014.Klebsormidium flaccidum genome
reveals primary factors for plant terrestrial adaptation. Nat. Commun.5:3978
41. Hudgins JW, Christiansen E, Franceschi VR. 2003. Methyl jasmonate induces changes mimicking
anatomical defenses in diverse members of the Pinaceae. Tree Physiol.23:36171
42. Hudgins JW, Christiansen E, Franceschi VR. 2004. Induction of anatomically based defense responses
in stems of diverse conifers by methyl jasmonate: a phylogenetic perspective. Tree Physiol.24:25164
43. Ishida T, Kurata T, Okada K, Wada T. 2008. A genetic regulatory network in the development of
trichomes and root hairs. Annu. Rev. Plant Biol.59:36586
44. Keeling CI, Bohlmann J. 2006. Diterpene resin acids in conifers.Phytochemistry67:241523
45. Keene CK, Wagner GJ. 1985. Direct demonstration of duvatrienediol biosynthesis in glandular headsof tobacco trichomes.Plant Physiol.79:102632
46. KonnoK. 2011.Plantlatexand other exudates as plant defense systems: roles ofvarious defense chemicals
and proteins contained therein.Phytochemistry72:151030
47. Krings M. 2000. Remains of secretory cavities in pinnules of Stephanian pteridosperms from Blanzy-
Montceau (Central France): a comparative study. Bot. J. Linn. Soc.132:36983
48. KringsM, Kellogg DW,Kerp H, TaylorTN. 2003. Trichomes of theseed fern Blanzyopteris praedentata:
implications for plantinsect interactions in the Late Carboniferous. Bot. J. Linn. Soc.141:13349
49. Krings M, Kerp H. 1998. Epidermal anatomy ofBarthelopteris germariifrom the Upper Carboniferous
and Lower Permian of France and Germany. Am. J. Bot.85:55362
50. Krings M, Kerp H. 1999. Morphology, growth habit, and ecology ofBlanzyopteris praedentata(Gothan)
nov.comb., a climbing neuropteroid seed fern from the Stephanian of central France.Int. J. Plant Sci.
160:60319
51. Krings M, Kerp H, Taylor TN, Taylor EN. 2003. How Paleozoic vines and lianas got off the ground:
on scrambling and climbing Carboniferous-Early Permian pteridosperms. Bot. Rev.69:2042452. Krings M, Taylor TN, Kellogg DW. 2002. Touch-sensitive glandular trichomes: a mode of defence
against herbivorous arthropods in the Carboniferous.Evol. Ecol. Res.4:77986
53. Kroken SB, Graham LE, Cook ME. 1996. Occurrence and evolutionary significance of resistant cell
walls in charophytes and bryophytes. Am. J. Bot.83:124154
54. Labandeira CC, Tremblay SL, Bartowski KE, VanAller Hernick L. 2014. Middle Devonian liverwort
herbivory and antiherbivore defence.New Phytol.202:24758
www.annualreviews.org Evolution of Plant Secretory Structures 19.19
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
20/21
PP66CH19-Lange ARI 12 January 2015 14:13
55. Lange BM, Ahkami A. 2013. Metabolic engineering of plant monoterpenes, sesquiterpenes and
diterpenescurrent status and future opportunities. Plant Biotechnol. J.11:16996
56. Lange BM, Turner GW. 2013. Terpenoid biosynthesis in trichomescurrent status and future oppor-
tunities.Plant Biotechnol. J.11:222
57. LangenheimJH. 2003.Plant Resins: Chemistry, Evolution, Ecology, and Ethnobotany. Portland,OR: Timber58. Lewinsohn E, Gijzen M, Savage TJ, Croteau R. 1991. Defense mechanisms of conifers: relationship
of monoterpene cyclase activity to anatomical specialization and oleoresin monoterpene content. Plant
Physiol.96:3843
59. Li G, Kollner TG, Yin Y, Jiang Y, Chen H, et al. 2012. Nonseed plantSelaginella moellendorffihas both
seed plant and microbial types of terpene synthases. PNAS109:1471115
60. Li L, McCraig BC, Wingerd BA, Wang J, Whalon ME, et al. 2003. The tomato homolog of
CORONATINE-INSENSITIVE 1 is required for the maternal control of seed maturation, jasmonate-
signaled defense responses, and glandular trichome development.Plant Cell16:12643
61. Lohr M, Schwender J, Polle JE. 2012. Isoprenoid biosynthesis in eukaryotic phototrophs: a spotlight on
algae.Plant Sci.18586:922
62. Ma X, Gang DR. 2004. The Lycopodium alkaloids.Nat. Prod. Rep.21:75272
63. MahlbergPG, FieldDW, Frye JS.1984. FossillaticifersfromEocene browncoaldepositsof theGeiseltal.
Am. J. Bot.71:1192200
64. Malcolm SB, Brower LP. 1989. Evolutionary and ecological implications of cardenolide sequestrationin the monarch butterfly.Experientia45:28495
65. Martin D, Tholl D, Gershenzon J, Bohlmann J. 2002. Methyl jasmonate induces traumatic resin ducts,
terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway spruce stems.
Plant Physiol.129:100318
66. Meslet-Cladiere L, Delage L, Leroux CJ, Goulitquer S, Leblanc C, et al. 2013. Structure/function
analysis of a type III polyketide synthase in the brown alga Ectocarpus siliculosus reveals a biochemical
pathway in phlorotannin monomer biosynthesis.Plant Cell25:3089103
67. Miyazaki S, Katsumata T, Natsume M, Kawaide H. 2011. The CYP701B1 ofPhyscomitrella patensis an
ent-kaurene oxidase that resists inhibition by uniconazole-P.FEBS Lett.585:187983
68. Mizutani M, Ohta D. 2010. Diversification of P450 genes during land plant evolution.Annu. Rev. Plant
Biol.61:291315
69. Napp-Zinn K. 1966.Anatomie des Blattes, Teil 1: Blattanatomie der Gymnospermen . Handb. Pflanzenanat.
Vol. 8. Berlin: Gebruder Borntraeger
70. Niklas KJ, Kutschera U. 2010. The evolution of the land plant life cycle.New Phytol.185:274171. Otto A, Wilde V. 2001. Sesqui-, di-, and triterpenoids as chemosystematic markers in extant conifersa
review.Bot. Rev.67:141238
72. Parsons HT, Christiansen K, Knierim B, Carroll A, Ito J, et al. 2012. Isolation and proteomic charac-
terization of the Arabidopsis Golgi defines functional and novel components involved in plant cell wall
biosynthesis.Plant Physiol.159:1226
73. Patten AM, Vassao DG, Wolcott MP, Davin LB, Lewis NG. 2010. Trees: a remarkable biochemical
bounty. InComprehensive Natural Products II: Chemistry and Biology, Vol. 3:Development and Modification
of Bioactivity, ed. L Mander, Liu HWB, pp. 1173296. Oxford, UK: Elsevier
74. Petschenka G, Fandrich S, Sander N, Wagschal V, Boppre M, Dobler S. 2013. Stepwise evolution of
resistance to toxic cardenolides via genetic substitutions in the Na+/K+-ATPase of milkweed butterflies
(Lepidoptera: Danaini).Evolution67:275361
75. Pickard WF.2008.Laticifers and secretory ducts:two other tube systems in plants.New Phytol. 177:877
88
76. Pollastri S, Tattini M. 2011. Flavonols: old compounds for old roles.Ann. Bot.108:12253377. Raffa KF. 2014. Terpenes tell different tales at different scales: glimpses into the chemical ecology of
coniferbark beetlemicrobial interactions.J. Chem. Ecol.40:120
78. Raffa KF, Hobson KR, LaFontaine S, Aukema BH. 2007. Can chemical communication be cryptic?
Adaptations by herbivores to natural enemies exploiting prey semiochemistry.Oecologia153:100919
79. Sabovljevic M, Vujicic M, Sabovljevic A. 2014. Plant growth regulators in bryophytes. Bot. Serb.38:99
107
19.20 Lange
7/23/2019 The Evolution of Plant secretory structures. 2014.pdf
21/21
PP66CH19-Lange ARI 12 January 2015 14:13
80. Sallaud C, Rontein D, Onillon S, Jabes F, Duff e P, et al. 2009. A novel pathway for sesquiterpene
biosynthesis from Z,Z-farnesyl pyrophosphate in the wild tomato Solanum habrochaites.Plant Cell21:301
17
81. Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magall on S, Lupia R. 2004. Ferns diversified in the
shadow of angiosperms.Nature428:5535782. SmithEC, Griffiths H. 1996. A pyrenoid-based carbon-concentrating mechanism is present in terrestrial
bryophytes of the class Anthocerotae.Planta200:20312
83. Srensen I, Pettolino FA, Bacic A, Ralph J, Lu F, et al. 2011. The charophycean green algae provide
insights into the early origins of plant cell walls. Plant J.68:20111
84. Stidd BM, Phillips TL. 1973. The vegetative anatomy of Schopfiastrum decussatum from the Middle
Pennsylvanian of the Illinois Basin. Am. J. Bot.60:46374
85. Stirk WA, B alint P, Tarkowsk a D, Nov ak O, Strnad M, et al. 2013. Hormone profiles in microalgae:
gibberellins and brassinosteroids.Plant Physiol. Biochem. 70:34853
86. SuireC,BouvierF,BackhausRA,BeguD, Bonneu M, Camara B. 2000. Cellular localizationof isoprenoid
biosynthetic enzymes in Marchantia polymorpha. Uncovering a new role of oil bodies. Plant Physiol.
124:97178
87. Thimmappa R, Geisler K, Louveau T, OMaille P, Osbourn A. 2014. Triterpene biosynthesis in plants.
Annu. Rev. Plant Biol.65:22557
88. Tissier A. 2012. Glandular trichomes: What comes after expressed sequence tags?Plant J.70:5168
89. Tittiger C. 2010. Pheromone production in bark beetles.Insect Biochem. Mol. Biol. 40:699712
90. Van Schie CCN, Haring MA, Schuurink RC. 2007. Tomato linalool synthase is induced in trichomes
by jasmonic acid.Plant Mol. Biol.64:25163
91. Vassao DG, Kim KH, Davin LB, Lewis NG. 2010. Lignans (neolignans) and allyl/propenyl phenols:
biogenesis, structural biology, and biological/human health considerations. In Comprehensive Natural
Products II: Chemistry and Biology, Vol. 1: Natural Products Structural DiversityI: Secondary Metabolites:
Organization and Biosynthesis, ed. L Mander, HWB Liu, pp. 815928. Oxford, UK: Elsevier
92. Voo SS, Grimes HD, Lange BM. 2012. Assessing the biosynthetic capabilities of secretory glands in
Citruspeel.Plant Physiol.159:8194
93. Walter MH, Strack D. 2011. Carotenoids and their cleavage products: biosynthesis and functions.Nat.
Prod. Rep. 28:66392
94. WarnerKA, Rudall PJ,FrohlichMW. 2009. Environmental control of sepalnessand petalness in perianth
organs of waterlillies: a new mosaic theory for the evolutionary origin of a differentiated perianth.J. Exp.
Bot.60:355974
95. Wasternack C, Hause B. 2013. Jasmonates: biosynthesis, perception, signal transduction and action in
plant stress response, growth and development. An update to the 2007 review in Annals of Botany.Ann.
Bot.111:102158
96. Wellman CH, Osterloff PL, Mohiuddin U. 2003. Fragments of the earliest land plants.Nature425:282
85
97. Weng JK, Noel JP. 2013. Chemodiversity in Selaginella: a reference system for parallel and convergent
metabolic evolution in terrestrial plants. Front. Plant Sci.4:119
98. Wollenweber E, Schneider H. 2000. Lipophilic exudates of Pteridaceaechemistry and chemotaxon-
omy.Biochem. Syst. Ecol. 28:75177
99. Yasumura Y, Crumpton-Taylor M, Fuentes S, Harberd NP. 2010. Step-by-step acquisition of the
gibberellin-DELLA growth-regulatory mechanism during land-plant evolution. Curr. Biol. 17:1225
30
100. Zulak KG, Bohlmann J. 2010. Terpenoid biosynthesis and specialized vascular cells of conifer defense.
J. Integr. Plant Biol. 52:8697
www.annualreviews.org Evolution of Plant Secretory Structures 19.21