the evolution of plant secretory structures. 2014.pdf

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PP66CH19-Lange ARI 12 January 2015 14:13

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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.

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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

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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


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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

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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.



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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

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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.



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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).

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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.



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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 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


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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.



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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).

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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



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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


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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 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



16/21


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


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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.

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