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Horticultural applications of jasmonates: A review

By C. L. ROHWER and J. E. ERWIN*

Department of Horticultural Science, University of Minnesota, 305 Alderman Hall, 1970 FolwellAvenue, St. Paul, MN 55108, USA(e-mail: erwin001@umn.edu) (Accepted 22 January 2008)

SUMMARYPlant growth and development are controlled, in part, by endogenous growth substances which are affected by bioticand abiotic signals and events. A particular class of growth regulators, collectively called jasmonates are involved inplant responses to such events and elicit unique responses. The effects of jasmonates on plant growth are varied andinclude storage organ formation,induction of plant defences against biotic (e.g., herbivores and pathogens) and abiotic(e.g., drought and ozone) stresses, and growth inhibition in tissues such as roots and young shoots. In addition,jasmonates can interact with other hormone pathways, especially ethylene, to affect growth and development.Detailed knowledge of jasmonate responses in models such as Arabidopsis is being put to use in a wide variety of

horticultural crops. This review summarises the impacts of jasmonates on plant growth and physiology, and howjasmonates may impact horticultural crop growth, physiology, protection from stresses, and/or handling.

Jasmonates are a class of endogenous plant growthregulators that have unique and potentiallycommercially useful properties that affect plant growthand development.As a class, these compounds generallyaide in defending a plant and possibly surrounding plantsfrom attack by pests and/or diseases. Here,we summarisejasmonate-related research on horticultural crops andpossibilities for future research related to the application

of this unique class of compounds in horticultural cropproduction. For the purposes of this review, jasmonatesinclude jasmonic acid (JA), methyl jasmonate (MeJA),and closely-related analogues. Octadecanoid precursorsto JA, or related products of fatty acid metabolism, areimplicated in some JA-independent responses (Stinziet al ., 2001; Farmer et al., 2003), but they will not bediscussed extensively here.

Jasmonate is a broad term covering numerouscompounds, but MeJA is particularly interesting becauseof the myriad of plant responses associated with itssynthesis and presence. Post-harvest application ofMeJA as a gas can activate defences and prevent post-harvest disorders in a number of horticultural crops (seePre- and post-harvest jasmonate application below).MeJA is emitted by wounded plants (Meyer et al., 2003)and, therefore, may represent a means of communicationbetween damaged plants. Jasmonate-induced volatileshave been shown to attract beneficial arthropods(Table I), a potentially useful response in the productionof horticultural crops. Numerous resources existdescribing the analysis of jasmonate-mediated responsesidentified by altered gene expression, but here we willfocus on the effects of exogenous jasmonates on plantresponses downstream from molecular responses. Here,we outline: (i) what jasmonates are; (ii) jasmonate-induced morphological and physiological responses in

plants; (iii) jasmonate research of relevance to

horticultural crops; and (iv) potential future directions injasmonate research related to horticultural applications.

WHAT ARE JASMONATES?Definition and distribution in plants

MeJA was discovered in 1962 as a sweet-smellingcompound inJasminium grandiflorum L. flower extracts

(Demole et al., 1962). After its discovery in jasmineflowers, JA was isolated from a pathogenic fungus,Lasiodiplodia theobromae (Aldridge et al., 1971). Thebiological activity of MeJA, extracted from Artemisiaabsinthium L., was reported nearly 10 years later (Uedaand Kato, 1980).Since then, jasmonates have been foundin many species and are considered ubiquitous (Meyeret al ., 1984; Hamberg and Gardner, 1992).

Jasmonates are defined as hormones because theyelicit cellular responses at low concentrations distantfrom their site of synthesis. For instance, long-distancewound-signalling is at least partially mediated by theinterplay of jasmonate and systemin throughout thevascular system, and likely involves H2O2 (Browse, 2006;Ryan and Moura, 2002; Schilmiller and Howe, 2005;Stratmann,2003;Wasternack et al., 2006).The quantity ofjasmonates in plants typically ranges from0.01 3.0 ng g1 fresh weight (FW), but up to 95 g g1

MeJA was detected inArtemisia tridentata ssp. tridentataNutt. (Preston et al., 2004). Jasmonate levels can behigher in some tissues than in others.As a percentage ofthe total JA and MeJA present in tomato flowers, MeJAcontent was 13% in pistils and 53% in petals (Mierschet al., 2004).

Jasmonates are synthesised via the octadecanoidpathway,beginning at linolenic acid and ending at (+)-7-epi-JA,and its conjugates and isomers [reviewed by Liechti and

Farmer (2006); Schaller et al. (2005); Wasternack (2006)].JA metabolite physiology has recently been discussedelsewhere (Delker et al., 2006;Wasternack, 2007).*Author for correspondence.

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Horticultural applications of jasmonates284

TABLE

I

Responsestoexogenousjasmonates

Reduced

Accumulation

Accumulation

D

ecreasedPerformance

Formationof

Abscissionor

Transpiration

ofNon-Jasmonate

ofAnthocyanins

ofArthropod

Enhanced

Attractionof

TubersorOther

Degradationof

orClosureof

Secondary

or

Herbivores

Resistanceto

Predatoryor

PlantSpecies

StorageOrgans

Chlorophyll

Stomata

Compounds

Carotenoids

(W

eight,Proliferation,etc.)

Pathogens

ParasiticArthropods

Agrostem

magithago

52

Alliumsativum

61,64,93

Apiumg

raveolens

80

Arabidopsisthaliana

55,75

114

63

36

26,109

90,124126,137,153

136

Arachishypogaea

20

Artemisiavulgaris

50

Avenasa

tiva

52,95,129,130

95

111

Bellisperennis

52

Brassica

juncea

13

Brassica

napus

13,32

14

Brassica

oleracea

5

Brassica

rapa

13

109

Bryophy

llumcalycinum

101

Bupleurumfalcatum

4

Catharan

thusroseus

2

Chelidon

iummajus

52

Commelinabenghaensis

92

Crotolariacobalticola

44

Cucumis

melo

16,17

Cucumis

sativus

1,52

Cupressu

slusitanica

151,152

Dioscore

aopposita

62,64,65

Dolichoslablab

52

Dryopterisfilix-mas

52

Echinaceapallida

12

Eschscholziacalifornica

44,45

Forsythia

intermedia

106

Fragaria

ananassa

89

6

6

Fragaria

vesca

138

Gerbera

jamesonii

41

Ginkgobiloba

134

Glycinemax

43,44

37,55

Glycyrrh

izaglabra

47

Gossypiumhirsutum

86

Gossypiumspp.

52

Helianth

usannuus

25,33,52

Hordeum

vulgare

52,141

128

71

107

Hyoscya

musmuticus

110

Kalanchoeblossfeldiana

97

Lactuca

sativa

52

44

Larixdecidua

52

Liliumlongiflorum

52

Linuma

lbum

135

Lithospe

rmumerythrorhizon

83,144

Macaran

gatanarius

49,73

Malusbaccatamandschurica

54

54

Malussp

p.

88

88,94

Mangiferaindica

69

Narcissu

striandrus

102

Nicotianaattenuata

7,40,56,58,91,132

59,77,91,132,133

59

Nicotianarustica

52

Nicotianasylvestris

8

Nicotianatabacum

5

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Horticultural applications of jasmonates

Other jasmonates with biological activity includetuberonic acid (from the leaves of Solanum tuberosumL.; Yoshihara et al., 1989), dihydrojasmonic acid (fromVicia faba L.; Miersch et al., 1989), and cucurbic acid(from seeds of Cucurbita pepo L.; Fukui et al., 1977).Conjugation to isoleucine is necessary to elicit somejasmonate responses (Staswick and Tiryaki, 2004), and

many other conjugates exist (Gapper et al., 2002;reviewed by Hamberg and Gardner, 1992).Analogs of MeJA or JA have physiological activity.

For instance, N-propyl dihydrojasmonate (PDJ)increased the abscisic acid (ABA) and anthocyanincontent of apples (Kondo et al., 2000). Coronatine is aphytotoxin from Pseudomonas syringae pv. tomato withstructural similarities to octadecanoid precursors of JA.Within its structure is a 5-membered keto-ringcompound with stereochemistry similar to (3R-7S)-JA,which is thought to be the most active isomer of JA.Coronatine induced tendril coiling in Bryonia dioicaJacq. and alkaloid accumulation in Eschscholziacalifornica Cham. (Weiler et al., 1994). Coronatine isactive at lower concentrations than JA in inducing potato(S. tuberosum L.) tuber cell expansion (Koda, 1997).

HOW DO JASMONATES AFFECT PLANTMORPHOLOGY AND PHYSIOLOGY?Methods of application

Jasmonates can be applied to plants in a variety ofways. For instance, MeJA may be applied to plants as agas in an enclosed environment. In the gas phase, MeJAcan induce plant defence responses. MeJA (at 8 nl l1, orapprox. 8 g l1) saturated the promotion of proteaseinhibitor synthesis in tomato plants (Farmer and Ryan,

1990). Falkenstein et al. (1991) reported a 90 95%release of MeJA from cotton (Gossypium hirsutum L.)plugs sealed in a 13 l chamber. MeJA-induced responseswere detected in cotton treated with 18 mol MeJAvapour in 31.8 l ventilated chambers (Rodriguez-Saonaet al., 2001). The use of volatile MeJA as an applicationtechnique is worth more detailed study. Post-harvesttreatments with other gases are not uncommon; ripeningis often initiated and synchronised in bananas (Musaacuminata Colla) with ethylene (Reid, 1992), and1-methylcyclopropene (1-MCP) may be used to preventethylene damage to fruit, cut flowers, or potted floweringplants (Blankenship and Dole, 2003), for example.

In contrast to applying it as a gas, some researchersmix MeJA in a lanolin paste, and spread the paste onplant tissues [for example, Tulipa gesneriana L.(Saniewski et al., 1998a), Nicotiana attenuata Torr. ex.Watson (Kessler and Baldwin, 2001), and apples [Malus

pumila Mill. (Miszczak et al., 1995)]. In contrast, someresearchers applied MeJA in a liquid form to ahydroponic solution (Baldwin and Schmelz, 1996). Ifroots are the primary site of action for jasmonateresponses (e.g., nicotine synthesis in Nicotiana roots),this method of application reduces the effects ofjasmonate transport to the roots by exposing the site ofaction directly to the hormone.

Jasmonate sprays typically contain a surfactant (such

as polysorbate or Triton X-100

), and a small amount ofsolvent, such as acetone or methanol, to dissolve thejasmonate. Typical concentrations of jasmonates sprays

range from 107 103 M. It is important to recognise thatMeJA is volatile, and liquid application to one plant may,in effect, result in an application to neighbouring plants,as a gas. In addition, drying time affects plant responsesto MeJA (Janoudi and Flore, 2003).

Morphological responses

Changes in plant development and structure areassociated with the presence of jasmonates. Most notableis the promotion of storage organ formation byjasmonates (Table I). For instance, tuberisation inChinese yam (Dioscorea opposita Thunb.) was promotedby jasmonates (Koda and Kikuta, 1991). Sprayingfield-grown Chinese yam with 5 10 mg l1 of a JAanalogue increased tuber yield by 15 40% (Kim et al.,2005). JA was able to enhance tuber formation inPterostylis sanguinea D. Jones and M. Clements in vitro,but this response also had an optimal concentration, andthe response was dependent on the sucrose content ofthe medium (Debeljak et al. , 2002). The need forjasmonates for tuberisation in soil-grown potato is notcertain (Jackson, 1999), and a recent study showed noeffect or inhibition of tuberisation in vitro (Zhang et al.,2006). Other results contradict this finding. JA (5 M)was more effective at inducing potato tuberisation thankinetin (11.6 M) in vitro (Pelacho and Mingo-Castel,1991). Theobroxide, a metabolite from the fungusLasiodiploidia theobromae (Patouillard) Griffon &Maubl., is structurally similar to jasmonates.Theobroxide had tuber-inducing activity in S. tuberosum(Yang et al., 2004; Yoshihara et al., 2000), similar tojasmonates (Koda et al., 1991). Bulblet formation ingarlic (Allium sativum L.) and onion (Allium cepa L.)was affected by jasmonates. JA (0.01 10 M) in the

culture medium increased garlic bulb number (Ravnikaret al., 1993), and 10 M JA stimulated bulbing in onionplantlets (Koda, 1997). In vitro culture of Narcissustriandrus L. shoots on medium containing JA enhancedbulb number and quality (Santos and Salema, 2000).Gaseous MeJA reduced FW and bulblet number inLilium longiflorum Thunb. and Asiatic hybrid LiliumConnecticut King explants, but the effects on Lilium

speciosum Thunb. were minimal. Interestingly, MeJAreduced the cold requirement for bulblet sprouting(breaking of dormancy) in these lily species (Jsik and deKlerk, 2006).

In some cases, flowering may be influenced byjasmonates. JA (106 M) inhibited flower bud formationin thin-layer explants of day-neutral N. tabacum L.(Barendse et al., 1985). Cultures of another day-neutralplant, Spirodela polyrrhiz (L.) Schleiden, showedenhanced flowering when JA was included in the culturemedium (Krajni and Nemec, 1995). Theobroxidereduced flowering and stem elongation in spinach(Spinacia oleracea L.), a long-day plant, through areduction in gibberellic acid content (Kong et al., 2006).MeJA also reduced or inhibited flowering in the long-day plant Chenopodium rubrum L. (Albrechtov andUllmann, 1994). Theobroxide induced flowering in theshort-day plant Pharbitis nil Chois. under 18-h(non-inductive) photoperiods, but downstream signals,

including jasmonates, may be the final signal oftheobroxide effects (Yang et al., 2004; Yoshihara et al.,2000). Treating Pharbitis with MeJA before an inductive

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8-h photoperiod inhibited flowering (Maciejewska andKopcewicz, 2002), but theobroxide treatment duringinductive photoperiods increased flower number (Yanget al., 2004; Yoshihara et al., 2000). It is difficult tocompare these results directly due to the differentchemical treatments and experimental conditions, butjasmonates appeared to have an effect on P. nil

flowering. JA promoted flowering in a long-short-dayplant, Wolffia arrhiza (L.) Horkel ex Wimm. whenapplied during the second photo-inductive period(Krajni and Cenci, 2000). JA also promoted floweringin the long-day plant Lemna minor L. (Krajni et al.,2006). It may be possible to use jasmonates forornamental plant production, or for breeding purposes,to induce uniform flowering in some plants that flowerunreliably or non-uniformly. Wasternack (2006) outlinedother variable roles of jasmonates in flowering, includinganther development and dehiscence, female organdevelopment, chemical defence production, colourproduction (discussed later), and the attraction ofpollinators.

Many other morphological responses are notflowering- or storage organ-related. Shoot growth, fruitnumber, inflorescence number, and development rate ofPhaseolus lunatus L. were enhanced by 1 mM JA (Heil,2004b). More nodes and greater internode length werefound on Vitis vinifera L. stems in tissue culture when0.5 M JA was added to the culture medium (Ravnikaret al., 1990). Parenchyma cell diameter was smaller, andmetaxylem vessel diameter and number were larger inGloriosa rothschildiana OBrien grown in a culturemedium with 25 mg l1 MeJA (Weryszko-Chmielewskaand Kozak, 2002). MeJA generally inhibited root andshoot growth in P. nil, although a very low concentration

(107

M) enhanced elongation (Maciejewska andKopcewicz, 2002). Four or six applications of MeJA to5-year-old peach (Prunus persica L. Batsch) treesreduced shoot growth, and 14 applications of MeJAreduced branch length,canopy density, leaf area,and leafFW in Malus baccata mandschurica (Janoudi and Flore,2003). Delayed development of S. lycopersicum plantswas noted after treating plants with 5 10 mM MeJA,butthis effect was temporary (Boughton et al., 2006). MeJAand JA promoted the germination of dormant Malusembryos (Ranjan et al., 1994). This may be a usefulresponse to promote germination in difficult-to-germinate plants.

Some responses are morpho-physiological. Rapidchanges in the shape or structure of a plant part oftenrequire rapid changes in cell physiology. For example,Mimosa pudica L. pulvinules closed in response to thepresence of JA in darkness in the presence of indole-3-acetic acid (IAA) and in the light without IAA (Tsurumiand Asahi, 1985). IAA caused tendril coiling in B. dioica,but higher concentrations of IAA were necessary for asimilar response induced by MeJA (Falkenstein et al.,1991).

Physiological responsesPlants have a variety of defences against stress. Some

of these are physical or morphological in nature, andsome are chemical. Constitutive plant defences include

glandular trichomes, cuticular waxes, and other structuraland chemical defences (Wittstock and Gershenzon,2002). Inducible chemical defences include a wide

variety of compounds that are toxic, anti-nutritive, orinjurious to attacking organisms, including alkaloids,phenolic compounds, chitinases, and protease inhibitors,among others.

Plant enzyme systems or inhibitors can be defensiveand can be jasmonate-induced. Polyphenol oxidase(PPO) is anti-nutritive to herbivores by promoting

quinine formation, which binds amino acids in food,making the food nutritionally useless (Felton et al.,1992). PPO also promotes the synthesis of stickypolyphenolic compounds that may entangle arthropodherbivores as they move past glandular trichomes(Kennedy, 2003). PPO activity is inducible by volatile orliquid jasmonates in many plants (Alba-Meraz andChoe, 2002; Doan et al., 2004; Constabel and Ryan, 1998;Constabel et al., 2000). Peroxidases function in numerousbiochemical processes, but they may be related to theproduction of reactive oxygen species or structuraldefences (e.g., lignin, cell wall crosslinks). Peroxidase andPPO were induced in tomato plants 36 h after a 12-htreatment with gas-phase MeJA (Thaler et al.,1996), 48 hafter 0.5 10 mM JA treatment (Cipollini and Redman,1999; Thaler, 2002; Thaler et al., 1996), or 72 h afterspraying plants with 7.5 mM or 10 mM MeJA (Boughtonet al., 2006). Treating Cucurbita melo L. seeds withgaseous MeJA induced defences against soil-borneseedling pathogens, but did not induce peroxidase (Buziet al., 2004b). However, soaking seeds in 45 M MeJAinduced both lipoxygenase and peroxidase synthesis(Buzi et al., 2004a). PPO and protease inhibitors wereinduced systemically in S. lycopersicum after treatmentof one leaflet with 0.5 mM JA, and lipoxygenase wasinduced locally (Thaler et al., 1996).

Protease inhibitors block the function of proteolytic

enzymes in the gut of herbivores, but the mode oftoxicity may also involve the stimulation or over-production of digestive enzymes, leading to amino acidstarvation (Broadway and Duffey, 1986). AS. lycopersicum protease inhibitor mRNA wassystemically induced 3 h after an application of 1 mM JA(Fidantsef et al., 1999). JA, and intermediates in JAsynthesis, induced the accumulation of proteaseinhibitors in S. lycopersicum. Less than 10 nmol per plantof 13(S)-hydroperoxylinoleic acid (a JA precursor)promoted the accumulation of protease inhibitor in15-d-old plants (Farmer and Ryan, 1992). Gas-phaseMeJA (80 nl l1) induced inhibitors in less than 1 h, andthe response to constant MeJA application was saturatedafter 40 h (Farmer and Ryan, 1990). Less than 1 nl l1MeJA induced inhibitors after 24 h of treatment (Farmerand Ryan, 1990). Artemisia tridentata (sagebrush)clippings, when put in an enclosed chamber withS. lycopersicum, induced protease inhibitor activity inS. lycopersicum. MeJA was isolated as the activecomponent of the sagebrush (Farmer and Ryan, 1990).MeJA also induced protease inhibitor accumulation inMedicago sativa L. and N. tabacum cv. Xanthi NC(Farmer and Ryan,1990). Jasmonate treatment increasedprotease inhibitor activity in a wide variety of genera,including Alnus (Tsharntke et al., 2001), Capsicum(Moura and Ryan, 2001), Nicotiana (Glawe et al., 2003;

Lou and Baldwin, 2003; Pohlon and Baldwin, 2001; vanDam et al., 2001a, b), and Solanum (Bolter, 1993; Thaleret al., 1996, 2001; Stout et al., 1998).

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The induction of anti-nutritive compound synthesisusing jasmonates is a promising area of research for pestcontrol (discussed below), and there is potential forspecifically creating protease inhibitor-enforced plants toresist pests (Lawrence and Koundal, 2002). For instance,mortality in the first and second generation of potatoaphid (Macrosiphium euphorbiae Thomas) was

increased when they fed on S. lycopersicum treated with1.5 mM JA, presumably due to anti-nutritive defencecompounds induced in the plants, including proteaseinhibitors (Cooper and Goggin, 2005). Other researchshowed that jasmonate-induced deaminase enzymes intomato plants caused the catabolism of essential aminoacids in insects, further rendering the plant less nutritious(Chen et al., 2005).

Some researchers have proposed undesirable effectson non-target organisms or predatory or parasiticarthropods following jasmonate-induced plant defences.One proposed mechanism for these effects is theaccumulation of toxic compounds in the herbivore(Malone and Burgess, 2000). When S. lycopersicum wastreated with JA, a reduction in the number of syrphid fly(a predator of aphids) eggs was noted.However, this wasalso correlated with a reduction in the number of aphids,suggesting that predator number differences could havebeen affected by aphid density (Thaler, 2002). Thenumber of Aphelinid-parasitised aphids onS. lycopersicum was unaffected by JA treatment (Thaler,2002). Survivorship of Spodoptera exigua Hbnercaterpillars was reduced when they fed on JA-treatedS. lycopersicum, but parasitism by Hyposoter exiguaewasps was less effective on caterpillars fed jasmonate-treated tissue (Thaler, 2002). This was explained by alower body weight per caterpillar when reared on

jasmonate-treated leaves. The negative effects ofexogenous jasmonates on parasitoids or predators couldresult from the reduced performance of the host, or foodsource for these arthropods. Interestingly, it has beensuggested that low doses of protease inhibitors may bemore useful than high doses in biologically-orientedintegrated pest management (IPM) programmes(Cloutier and Michaud, 2000). Low doses of toxiccompounds would theoretically reduce pest performancewithout affecting predator or parasitoid survival orfecundity. If true, this means the that fine control ofprotease inhibitor induction with jasmonates is moreuseful than maximum induction.

Structural defences also may be jasmonate-inducible,or require jasmonate signalling. For instance, trichomenumber and density increased after jasmonateapplication to Arabidopsis (Traw and Bergelson, 2003)or tomato (Boughton et al., 2005). An S. lycopersicumjasmonate signalling mutant had fewer trichomes, andglandular trichomes that had a lower terpenoid content(Li et al., 2004). MeJA induced phenolic- or resinduct-related structural defence responses in 16 speciesrepresenting five gymnosperm families (Franceschi et al.,2002; Hudgins et al., 2003; 2004; Martin et al., 2002).

Mutants and mechanisms of jasmonate actionA number ofA. thaliana mutants related to jasmonate

synthesis and action have been identified [reviewed byBerger (2002); Rosahl and Feussner (2005); Beckers andSpoel (2006); Delker et al. (2006); Wasternack (2006)].

Mutants unable to synthesise trienoic fatty acids (JAprecursors),or an enzyme necessary for JA synthesis, weremale-sterile because of unsuccessful pollen development(McConn and Browse, 1996; Stinzi and Browse, 2000). Atomato mutant (JL5) incapable of synthesising jasmonateshas also been used in some studies (Howe et al., 1996).Further discussion of signalling and response mutants can

be found in the previously cited references.Recent reviews on the jasmonate signalling pathwayare abundant (Devoto and Turner, 2003, 2005;Glazebrook et al., 2003; Liechti et al., 2006; Gfeller et al.,2006). Genes specifically involved in jasmonate-induceddefences in tomato and A. thaliana have also beenreviewed (Walling, 2000). The jasmonate responsepathway utilises a protein turnover mechanism, similarto other hormone response pathways (Browse, 2006). Askp-like/cullin/F-box (SCF) ubiquitin ligase, inconjunction with a proteasome, controls jasmonate-regulated protein turnover (reviewed by Wasternack,2006). In A. thaliana, COI1 is the F-box protein in thejasmonate response complex SCFCOI1 (Xu et al., 2002). Intomato, JAI1 is the COI1 homolog (Li et al., 2004).

No discussion of jasmonate responses can occurindependently of a discussion of ethylene responses(Arimura et al., 2005; Campbell et al., 2003; Xu et al.,1994; Zhao et al., 2004). Microarray analysis showed thatjasmonate- and ethylene-responsive gene expressionpatterns cluster together in defence signalling(Glazebrook et al, 2003). In pathogen defence responses,PDF1.2 gene activation required simultaneousperception of jasmonate and ethylene (Penninckx et al.,1996; 1998; Ellis et al., 2002). Ethylene (at 1 l l1)enhanced the sensitivity of Z. mays to JA application at5 nmol and 50 nmol JA plant1 (Schmelz et al., 2003b).

MeJA-induced gum formation in Prunus persica Batschwas proposed to act through the induction of ethylene(Saniewski et al., 1998b). Ethylene perception wasnecessary for jasmonate-induced accumulation ofprotease inhibitor transcripts in S. lycopersicum(ODonnell et al., 1996), and simultaneous ethylene andMeJA treatment enhanced protease inhibitor transcriptaccumulation in N. sylvestris Speg., more than eitherMeJA or ethylene treatment alone (Shoji et al., 2000).Similar results were noticed in the induction of -thujaplicin in Cupressus lusitanica Mill. cell cultures(Zhao et al., 2004).

On the other hand, several ethylene-independent orethylene-antagonised jasmonate responses have beendiscovered. Ethylene blocked MeJA-induced vegetativestorage protein accumulation inA. thaliana (Matsushimaet al., 2002). A. thaliana ethylene response mutantsshowed enhanced accumulation of jasmonate-responsivetranscripts compared to wild-type plants (Rojo et al.,1999).An S. lycopersicum mutant impaired in jasmonatesynthesis (def1) could be made resistant to Botrytiscinerea Pers. ex Fr. by treating plants with ethylenebefore inoculation. However, an S. lycopersicum lineover-expressing pro-systemin, which activates jasmonatesignalling, was more resistant to B. cinerea and did notrequire ethylene perception (Daz et al., 2002).Simultaneous perception of MeJA and ethylene was also

not required for Botrytis resistance in A. thaliana.Ethylene-insensitive A. thaliana was protected fromBotrytis by gas-phase MeJA (Thomma et al., 1999a).

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Ethylene blocked jasmonate-inducible nicotineaccumulation, or biosynthesis, in N. attenuata (Kahl et al.,2000;Winz and Baldwin, 2001) and in N.sylvestris (Shoji etal., 2000). Jasmonate signalling is required for thecontainment of cell death in ozone-treatedA. thaliana;butethylene signalling plays an opposite role (Overmyer et al.,2000;Tuominen et al., 2004).MeJA (100 M) did not cause

leaf abscission in Vigna radiata (L.) R. Wilczek explants,but enhanced petiole abscission in AgNO3-treated plantscompared to plants treated with AgNO3, without MeJA(Curtis,1984), suggesting ethylene-independent abscission.It is clear that ethylene and jasmonates are involved ininduced defence responses, and that the signallingpathways needed for resistance responses are specific toparticular species and stress systems.

PRACTICAL APPLICATIONS ANDHORTICULTURAL RELEVANCEUse of other compounds for defence induction

Commercial applications of materials that induceplant defences are just beginning to be appreciated as ameans to reduce pest and disease infestation. Suchcompounds are often called plant activators. To ourknowledge, all available products are activators ofsystemic acquired resistance (SAR) and are appliedpreventatively to control disease. SAR is a plant defenceresponse that requires salicylic acid (SA) for within-plant defence activation against viruses and pathogens(Mtraux et al., 2002). The use of plant activators is notwidespread in commercial horticulture. For instance,harpin protein, an activator of SAR (Dong et al., 1999),was applied commercially to 3% of the U.S. strawberrycrop in 2006 (USDA, 2007) for disease prevention.

Harpin slowed the development of blue mould(Penicillium expansum Link) in apple (Malus domestica Borkh; de Capdeville et al., 2003). Harpinalone, or in rotation with chemical fungicides, reducedthe incidence and severity of disease in tomatoes inFlorida, but acibenzolar-S-methyl benzothiadiazole;(BTH) provided better prevention (Pernezny et al.,2002). BTH is an analog of SA, and is anothercommercially available (Actigard or Blockade)inducer of SAR, labelled in the United States forpreventative disease resistance in cole crops, tomatoes,leafy vegetables, and tobacco (Syngenta CropProtection, Greensboro, NC, USA). BTH can alsoprotect plants against some piercing-sucking insects, asseen in M. persicae-tomato (Boughton et al., 2006),Macrosiphium euphorbiae-tomato (Cooper et al., 2004),Bemisia tabaci-cotton (Inbar et al., 2001), and to a lesserextent in Bemisia argentifolii-tomato (Inbar et al., 1998)interactions. No effect, or variable effects of BTH weredetected against Helicoverpa armigera on cotton plants(Inbar et al., 2001), but Liriomyza spp. (leafminer)preferred control tomato leaves over leaves treated withBTH (Inbar et al., 1998). Harpin is also being studied forinduced insect defences. For instance, reduced feeding ofthe striped cucumber beetle [Acalymma vittatum (F.)] onCucumis sativus L. was noted when insects were applied7 d after treating plants with harpin (Zitter and Beer,

1998). Aphids (Myzus persicae Sulzer) applied to A.thaliana plants 5 d after treating the plants with harpinhad a reduced rate of reproduction (Dong et al., 2004).

The utility of commercial inducers of plant defences hasbeen established by these examples. The impact of SARon jasmonate-regulated responses is varied and will bediscussed in the next section.

Use of jasmonates in induced defences against pests andpathogens

Jasmonates are an integral part of plant biotic defencesignalling. Resistance to plant pests can be enhanced byjasmonate treatment (Table I), and jasmonate synthesisor response mutants have helped to explain possiblemechanisms (Halitschke and Baldwin, 2006; van Poecke,2007). Stout and others (2002) noted that the utility ofeliciting multiple defences within a single plant, includingdirect and indirect defences, is inherently resilient to thedevelopment of pest resistance. Much of the work in thisarea has focussed on the inhibition of feeding bylepidopteran larvae; but Thaler et al. (2001) showed thatFrankliniella occidentalis Pergande (thrips, a cellcontent-feeding insect) and aphid (a phloem-feedinginsect) populations were reduced in field plots oftomatoes treated with JA. JA (1 mM) sprayed on field-grown S. lycopersicum reduced the survivorship ofS. exigua placed on the plants, and reduced the numberof naturally-occurring F. occidentalis found 3 weeks aftertreatment (Thaler et al., 1999). In a separate study, thripssurvivorship on tomatoes was not affected by JAtreatment, but thrips damage was reduced by JAtreatment (Thaler et al., 2002c). M. persicae populationswere reduced in tomato plants treated with 5 10 mMMeJA (Boughton et al., 2006). Jasmonate signalling wasrequired for defence against T. urticae in S. lycopersicum(Li et al., 2002; 2004), and exogenous JA reducedTetranychus pacificus McGregor (Pacific spider mite)

performance on grapevines (Omer et al., 2000) andT. urticae performance on tomato (Thaler et al., 2002c).MeJA reduced T. urticae preference for, andperformance on Viola wittrockiana Gams and

Impatiens walleriana Hook.f. (Rohwer and Erwin,unpublished). Other studies suggest varied, yet specific,responses to particular pests. Defence responsestherefore seem to be specific and tightly controlled. Ajasmonate-inducible metallopeptidase-like gene inCucurbita pepo (SLW1) was induced by Bemisiaargentifolii Bellows and Perring (silverleaf whitefly)nymphs, but not by B. argentifolii adults or B. tabaciGennadius (sweetpotato whitefly; van de Ven et al.,2000). Even within a feeding guild, jasmonate responsesmay vary.As the feeding mechanisms of these insects arevery similar, this response is probably a result of uniquecomponents in the saliva, or different concentrations ofsalivary constituents (Thompson and Goggin, 2006).

There is also evidence for the involvement ofjasmonates in resistance to root pests. Jasmonate-deficient A. thaliana were sensitive to fungus gnat(Bradysia impatiens) infestation (McConn et al., 1997),and fungus gnat survivorship was lower on MeJA-treated spinach compared to control-treated plants(Schmelz et al., 2002). The performance of Daktulosphaira vitifoliae Fitch (grape phylloxera) ongrapevines was reduced by treating the plants with JA

(Omer et al., 2000). Partial resistance to the avirulentnematode Meloidogyne javanica isolate VW4 wasimparted to S. lycopersicum by treating the foliage with

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JA, but resistance to a virulent nematode was not seen(Cooper et al., 2005). Nematode resistance in Avena

sativa and S. oleracea was imparted by the application ofMeJA to the roots (Soriano et al., 2004a, b).

Specialist and generalist herbivores typically behavedifferently on jasmonate-treated plants. This supportsthe theory that generalist herbivores are more strongly

affected by host plant defences than specialist herbivores(Strauss and Zangerl, 2002). Two generalist lepidopteranherbivores (S. exigua and Trichoplusia ni Hbner)performed less well on JA-treated tomato than onuntreated plants, but the results were somewhat variableand may depend on host genotype (Thaler et al., 1996;1999; 2001; 2002b; c). Feeding of a specialist herbivore ofsolanaceous plants (Epilachna vigintioctopunctata) ontomato was unaffected by jasmonate treatment, butfeeding was reduced on non-host brassicas such asBrassica rapa L. ssp.pekinensis andA. thaliana (Shinogiet al., 2005).The relative growth rate of another specialistlepidopteran (Manduca sexta L.) on tomato wasunaffected by treating the plants with 1.5 mM JA (Thaleret al., 2002c). Conflicting results have been reported forthis response (Iverson et al., 2001); but, in this case,0.45 mM MeJA was used for elicitation of defenses and adifferent tomato cultivar was used.An undesirable effectof using jasmonate treatment to reduce generalistherbivore damage under field conditions might be thegreater potential for proliferation, or at least minimalcontrol of specialist herbivores (Cipollini et al., 2003).

Exogenous jasmonates increased resistance to pests inNicotiana species, including tobacco hornworm(Manduca sexta L.). The nicotine defence system of thehost was effective and induction was measurable.Feeding by 2nd-instar tobacco hornworm larvae on

N. tabacum leaf discs was reduced when whole plantswere treated for 5 d with 0.5 l MeJA. Similar resultswere noticed when plants were grown free of MeJA for6 d after treatment (Avdiushko et al., 1997). The growthand feeding of larvae fed on MeJA-treated leaves werealso reduced. Hornworm egg hatching was not affected,but feeding of newly-hatched larvae was reduced(Avdiushko et al., 1997). Herbivore (Manducaquinquemaculata) oviposition on N. attenuata Torr ex. S.Watts was reduced when the plants were treated withMeJA, or when plants were under attack by caterpillars(Kessler and Baldwin, 2001). Both herbivory andflorivory were reduced in N.attenuata treated with MeJA(McCall and Karban, 2006). Manduca sexta larvae grewmore rapidly on lipoxygenase-impaired (and thereforejasmonate-deficient) N. attenuata compared to wild-typeplants,and MeJA restored native defences (Kessler et al.,2004). Native herbivores also attacked jasmonate-deficient plants more than wild-type plants (Kessler etal., 2004). A correlative relationship between MeJAreleased from damaged sagebrush (A. tridentata Nutt.)and reduced feeding by grasshoppers on natural standsof neighbouring N. attenuata has been established(Karban et al., 2000),and may be a result of the emissionof MeJA from the sagebrush (Farmer and Ryan, 1990).Recent results suggest that the enhanced resistance inthe tobacco was not directly due to the immediate

induction of defensive compounds, but rather toenhanced induction of defensive compounds once theNicotiana was attacked (Kessler et al., 2006). In addition,

other volatiles, such as (E)-2-hexenal and methacrolein,may be the compounds active in priming in Nicotiana(Kessler et al., 2006; Preston et al., 2004). Although thenicotine production rate increased in N. sylvestris afterMeJA application, the production rate returned to thesame as in untreated plants 6 d after elicitation. Therewas no ultimate difference in nicotine content between

plants that were treated several times with MeJA, andplants that were treated once. However, prior elicitationof plants caused a more rapid accumulation of nicotinethan in plants with no history of elicitation (Baldwin andSchmelz, 1996). This supports the theory that more rapidinduction of defenses is a mechanism for enhancedresistance in MeJA-treated plants when jasmonate-mediated defenses are subsequently elicited by a bioticor abiotic challenge. Priming plants, rather than inducingdefenses directly, may incur fewer energy costs and resultin similar benefits, as seen in the defense againstpathogens inArabidopsis (van Hulten et al., 2006).

Some physiological responses to jasmonates are notdirectly defensive, but can also serve to defend plantsindirectly. Jasmonate-treated plants have attractedpredators or parasitoids in at least eight plant species(Table I). Jasmonate signalling within the plant isrequired to attract the parasitoid Cotesia rubeculaMarshall to A. thaliana under attack by the herbivorePieris rapae L. (van Poecke and Dicke, 2002). Similarly,S. lycopersicum infested with T. urticae, and defective inJA synthesis, failed to attract predatory mites(Phytoseiulus persimilis Athias-Henriot) or to emitpredator-attractive volatiles to the same extent as wild-type plants (Ament et al., 2004). Parasitoids preferred

A. thaliana plants treated with exogenous JA overuntreated plants, 24 h after a JA treatment (van Poecke

and Dicke, 2002). Hyposoter exiguae parasitoids werepreferentially attracted to Spodoptera exigua Viereckcaterpillars placed in a field of S. lycopersicum treatedwith JA, compared to caterpillars in plots of untreatedplants (Thaler,1999a). P. lunatus treated with 1.0 mM JA,but not 0.1 mM, attracted P. persimilis better than plantstreated with water, but not as well as plants infested withprey (T. urticae; Dicke et al., 1999). Water-treatedP. lunatus plants with T. urticae damage were lessattractive to P. persimilis than 0.1 mM JA-treated plantsdamaged by T. urticae (Gols et al., 2003). Interestingly,JA-elicited volatiles from P. lunatus were similar toS. exigua-elicited volatiles, but applications of JAfollowed by methyl salicylate (MeSA) to plants wereneeded for terpenoid emissions similar to emissions fromT. urticae-treated plants (Ozawa et al., 2000).

An understanding of the role of jasmonates intritrophic interactions may permit more effective use ofnatural enemies in horticultural crop production. Otherunique means of jasmonate-induced tritrophic defenceresponses have been noted. Natural herbivory onMacaranga tanarius Mll. Arg. was reduced by theapplication of JA. Extrafloral nectaries, induced by JA,attracted beneficial insects to plants, with an associatedreduction in herbivore numbers and damage (Arimuraet al ., 2005; Heil et al., 2001; Linsenmair et al., 2001).Similar results were observed in P. lunatus (Heil, 2004b).

Changes in the volatiles emitted by plants afterjasmonate application were the primary attractants inpredator or parasite-attracting olfactometer experiments.

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Jasmonates can induce the emission of a myriad volatilesfrom plants, often similar to responses induced duringherbivore feeding. The release of stored compounds andde novo synthesis of volatiles are probably bothresponsible for enhanced volatile production(Degenhardt and Lincoln, 2006). Volatile compounds,including indole, (Z)-3-hexenyl acetate, (E)--ocimene,

and (E,E)--farnesene, were produced by cotton plantsafter exposure to 18 mol MeJA vapour for 18 h(Rodriguez-Saona et al., 2001). Volatile MeJA inducedlocal, but not systemic, emission of monoterpenes andsesquiterpenes in Z. mays (Farag and Par, 2002).Interestingly, MeJA emission, following JA treatment,wasnoted in seven species representing the Dryopteridaceae(wood ferns), Ginkgoaceae, Solanaceae, Fabaceae, andPoaceae; but JA did not induce MeJA emission in fourother species representing the Brassicaceae, Myrtaceae,Asteraceae,and Salicaceae (Boland et al., 1995).The basisfor differences in the inducibility of MeJA emission wasnot addressed,but the ecological purpose of this responseposes a fascinating question.

In addition to their indirect effects, jasmonates mayhave direct effects on insect predators. MeJA andcis-jasmone attracted members of two families of insectparasitoids (Braconidae and Sarcophagidae) in hop(Humulus lupulus L.) cultivation (James, 2005).MeJA-baited traps attracted more Anagrus andMetaphycus parasitic wasps than untreated traps amonggrapevines (Vitis labrusca L.), but this study contradictedprevious research and could have resulted fromMeJA-elicited volatiles from the grapes (James et al.,2005). Interestingly, minimal induction of volatileemission in P. lunatus by JA attracted herbivores,whereas stronger induction repelled herbivores (Heil,

2004a).A similar experiment showed a herbivorous mite(T. urticae) was attracted to P. lunatus that were alreadylightly infested with T. urticae, but the mites wererepelled from heavily infested plants. Predatory mites(P. persimilis) were only attracted to plants moderatelyor heavily infested with their prey (Horiuchi et al., 2003).Therefore, in horticultural situations, it may be importantto fully induce volatile emissions to attract predators orparasitoids and to repel herbivores.

The importance of jasmonate signalling in repellingherbivores through volatile emissions was recentlydemonstrated in tomato, using a jasmonate synthesismutant. JA-deficient tomato plants showed reducedvolatile emissions and corresponding enhancedpreference by B. tabaci and M. sexta for oviposition(Snchez-Hernndez et al., 2006). Jasmonate-treatedB. rapa were less attractive to the herbivorous insectPlutella xylostella L.; but jasmonate-treated B. oleraceaL. var. capitata was more attractive to the herbivore(Lu et al., 2004). It is obviously undesirable to attractpests to crop plants, so further investigation seemsnecessary for specific host-herbivore interactions.

Jasmonates have shown no direct activity againstarthropods (Avdiushko et al., 1997). However, MeJA caninhibit spore germination and germ tube elongation inB. cinerea (Meir et al., 1998), but promote sporegermination in Botrytis (Darras et al., 2005) or Pythium

ultimum (Kozlowski et al., 1999). Jasmonates had nonegative effect on spore germination or growth inPenicillium digitatum Wehmer (green mould; Droby

et al., 1999),but MeJA (100 600 M) inhibited mycelialgrowth in Botrytis (Darras et al.,2005;Moline et al.,1997)and Penicillium expansum (Yao and Tian, 2005) in vitro.Mycelial growth of Phytophthora infestans (Mont.) deBary was either inhibited or promoted, depending on thegrowth medium, the concentration of MeJA and JA, andthe isolate (Cohen et al., 1993). MeJA and JA inhibited

zoospore discharge and germination in P. infestans, butenhanced germ tube formation directly from sporangia(Cohen et al., 1993). MeJA had no effect on mycelialgrowth in vitro in Pythium mastophorum Drechsler(Vijayan et al., 1998).

Regardless of whether jasmonates act directly onpathogens or not, it is clear that there is jasmonatesignalling in plant defences against pathogens (Table I).Phytoalexin production in response to jasmonates hasbeen documented in many plants, including peanut[Arachis hypogaea (Chung et al., 2003)] and Mexicancypress [Cupressus lusitanica (Zhao et al., 2001; 2004)];but it was not detected in S. lycopersicum, S. tuberosum(Cohen et al.,1993),orA. thaliana (Thomma et al.,1999b).

Jasmonate-induced pathogen defences have potentialfor horticultural crop production (Pea-Corts et al.,2005). For example, jasmonate signalling is required forresistance to Pythium root diseases (Staswick et al., 1998;Vijayan et al., 1998) and to Plectosphaerella cucumerina(Thomma et al., 2000) in A. thaliana. Seedling diseaseswere reduced in Cucumis melo L. after gaseous or liquidMeJA seed treatment (Buzi et al.,2004a,b).MeJA-treatedPicea abies (L.) H. Karst plants had more resin flow (adefensive response) than untreated trees,when both weresubsequently inoculated with Ceratocystis polonica. Inaddition, lesion size was smaller in the MeJA-treatedtrees (Franceschi et al., 2002). The phenomenon of

induced systemic resistance (ISR), where non-pathogenicrhizobacteria primed plants for systemic pathogendefence, required jasmonate and ethylene signalling(Pieterse et al., 1998; Pozo et al., 2005).

The accumulated data from A. thaliana suggest thatjasmonate and ethylene signalling are involved in, or arerequired for, defence against necrotrophic pathogens,and that the SA signalling pathway is involved in defenceagainst biotrophic pathogens (Glazebrook, 2005;McDowell and Dangl, 2000; Thomma et al., 2001; vanPoecke, 2007; Zimmerli et al., 2004). Of course, there areexceptions to this (Pozo et al., 2005;Thaler et al.,2004).Inaddition, induction of SAR can be antagonistic tojasmonate-induced defences against herbivores (Feltonet al., 1999). Acetylsalicylic acid (ASA) inhibited JAsynthesis (Pea-Corts et al., 1993); and SA or ASAinhibited JA-induced accumulation, activity, or geneexpression of protease inhibitors (Doares et al., 1995;Stout et al., 1998). Since jasmonate- and SA-inducedresponses are often antagonistic, and some defencepathways are specific to jasmonate and ethylenesignalling, or to SA signalling, jasmonate-induceddefence against one pest or pathogen could make theplant more susceptible to another pest or pathogen(Kunkel and Brooks, 2002). For instance, MeJAenhanced resistance to Trichoplusia ni Hbner (cabbagelooper) in A. thaliana, but also enhanced the growth of

Pseudomonas syringae (Cui et al ., 2005). On the otherhand, a putative A. thaliana transporter of defensiveterpenoids required SA, jasmonate, and ethylene

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signalling (Campbell et al., 2003). Responses to specificchallenges obviously require the fine-tuning of hormonelevels and responsiveness within the plant.

Sequential or simultaneous activation of separatedefence pathways may help us to understand how thepathways function. Exposing S. lycopersicum to MeJAgas for 4 h slightly reduced the relative growth rate of

S. exigua on the plants relative to untreated plants, butthis was not true when the plants were treated with SAbefore MeJA. This response was correlated withincreased protease inhibitor activity (Stout et al., 1998).However, SA inhibition of jasmonate-induced defenceagainst S. exigua was not detected when plants weretreated with MeJA for 12 h instead of 4 h (Stout et al .,1998). The relative growth rate of S. exigua on tomatowas reduced by JA treatment, but reduced to a lesserextent by simultaneous application of BTH and JA(Thaler et al., 1999). Accordingly, JA-induced PPOactivity in tomato was reduced by simultaneousapplication of BTH (Thaler et al., 1999). BTH-treatedS. lycopersicum leaves allowed a greater relative growthrate of Helicoverpa zea (Boddie) than control leaves, butthe results were variable (Stout et al., 1999). In contrast,induction of SAR in A. thaliana by harpin can activatejasmonate- and SA-independent (but ethylene-dependent) defences against aphids (M. persicae; Donget al., 2004). SAR-inducing compounds had little effecton jasmonate-induced defences against nematodes inS. lycopersicum (Boughton et al., 2006). Simultaneousactivation of SAR and ISR, which requires jasmonatesignalling, protected A. thaliana from P. syringae in anadditive manner (van Wees et al., 2000), but no additiveeffect was seen in tomato (Thaler et al., 2002b). Therewas no interactive effect of simultaneous application of

BTH and JA to P. syringae pv. tomato on cultivatedtomato (S. lycopersicum) or wild tomato [S. lycopersicumvar cerasiforme (Dunal) Spooner, J. Anderson & R.K.Jansen]. Interestingly, neither JA, nor BTH enhancedresistance to P. syringae in the wild tomato (in fact, BTHenhanced susceptibility!), but resistance was enhanced inthe cultivated variety (Thaler et al., 2002c). Thisillustrates, again, that extrapolating jasmonate responsesfrom one plant to the entire plant kingdom is over-reaching. The result of simultaneous perception of thesetwo hormones may depend on their concentrations (Muret al., 2006). Antagonism between JA and SA signallingin defence, as well as a requirement for both compoundsin some responses, was recently reviewed (Beckers andSpoel, 2006; Pozo et al., 2005). In addition, reviews on thetripartite interactions of pathogens, herbivores, andplants, including molecular plant responses, wererecently published (Rosts et al., 2003; Stout et al., 2006;Taylor et al., 2004). Much work, including field trials, oninteractions between jasmonate- and SA-induceddefences in horticulturally important crops is needed.

For horticultural applications, it is often not necessaryto consider plant fitness in an ecological sense, includingfecundity or survivorship. However, the induction ofdefence responses may enhance resistances at a cost toyield.For instance, tomato fruit number, fruit weight,andseed number per plant were reduced after the

application of 10 mM JA, but not 1 mM JA (Redmanet al ., 2001; Thaler et al., 1999). However, there was noeffect of jasmonate sprays on fruit yield (number and

size) over 3 years in a tomato field (Thaler, 1999b). JA(0.5 1 mM) applied to flowering strawberry plantsaccelerated ripening and increased the total yield perplant by 26 37% (Yilmaz et al., 2003). Under moderateherbivory, in a natural ecosystem, MeJA-inductionincreased lifetime seed set and capsule number inN. attenuata. However, under low levels of herbivory,

non-induced plants performed better than inducedplants and, under high herbivory, there was no differencebetween MeJA-induced plants and non-induced plants(Baldwin, 1998).Soybean yield increased when the seedswere inoculated with Bradyrhizobium cultured with 50M MeJA compared to inoculation with untreatedBradyrhizobium (Mabood et al., 2006). The number ofpollen grains per flower in wild radish (Raphanusraphanistrum L.) was reduced by approx. 6% by JAapplication, and plants flowered approx. 2 d later thanuntreated plants (Agrawal et al., 1999). Pollen grainnumber per flower is unimportant in the production of acut-flower crop, but pollen grain number per flower maybe an important consideration in seed production and/orfor fruit size. Fruit number per plant is unimportant in apotted geranium, but is critical in cucumber production.Research on specific crops will need to be conducted todetermine the effects of JA on economically importantattributes in food and ornamental plants.

Generalising jasmonate-related responses important inplant-pest interactions can be misleading. The modelsystems most studied in this area are tomato,A. thaliana,and tobacco. Interactions of these plants with specificpests are distinct and should not be applied directly to theother species (Gatehouse, 2002). Each plant species hasits own unique set of defences, and induction of defencesshould not be attributed unequivocally to jasmonates, nor

should defence induction lead to the conclusion that theplants will be better defended against pests. Also,JA-induced defences, such as protease inhibitors (PI),may simply lead to the production of PI-resistantdigestive enzymes in herbivores without affectingherbivore performance (Broadway, 1995; 2000).

Pre- and post-harvest jasmonate applicationsSome research on horticultural uses of MeJA has

focussed on pre-harvest and post-harvest treatments toprotect against microbial development on harvestedtissue. Pathogen growth on celery (Apium graveolens L.)and pepper (Capsicum annuum L.) was reduced bytreatment with MeJA (Buta and Moline, 1998). MeJAvapour at 1 M was more effective than 10 M atreducing post-harvest decay in two strawberry(Fragaria ananassa Duch.) cultivars stored at 20C(Moline et al., 1997).Strawberries stored for 12 d at 7.5Chad higher quality and were protected from decay by 100mM MeJA vapour (Ayala-Zavala et al., 2005). MeJAvapour (100 M) also eliminated decay in raspberry(Rubus idaeus L.) fruit stored at 10C for 10 d (Wang,2003). Dipping grapefruit (Citrus paradisi Macfad.) in1 50 M MeJA reduced green mould (Penicillium)during storage (Droby et al., 1999). MeJA applied to cutpineapple (Ananas comosus Merr.) as a vapour or a dipreduced softening and microbiological load after 6 and

12 d storage (Martnez-Ferrer and Harper, 2005),respectively. Peach fruit treated with volatile MeJAshowed slower decay and higher quality than untreated

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fruit 8 d after treatment (Jin et al., 2006).Applying 200 600 M MeJA to cut roses (Rosa hybrida L.), through thepulsing solution, or as a spray, reduced the incidence andseverity of Botrytis (Meir et al., 1998; 2005), andenhanced flower colour persistence (Meir et al., 2005).Volatile MeJA (0.025 0.1 l l1) reduced the severity,lesion number, and lesion diameter of Botrytis in Freesia

hybrida Hort. (Darras et al., 2005). Many otherornamental crops may also benefit from MeJAapplication pre- or post-harvest to block post-harvestBotrytis development. Care must be taken, however, asjasmonate-induced ethylene may reduce flowerlongevity in ethylene-sensitive species, as was shown fora Dendrobium hybrid and Petunia hybrida Hort. ex.Vilm. (Porat et al., 1993). In addition, another potentialdrawback is reduced volatile formation, which was notedin apples treated with MeJA after controlled atmospherestorage (Olas et al., 1992). However, MeJA-enhancedproduction of beneficial volatiles from plant tissue hasbeen detected numerous times, including in strawberry(Ayala-Zavala et al., 2005), mango [Mangifera indica L.(Lalel et al., 2003)] and apple (Fan et al., 1997) fruit.Recent reviews of chemical, biological, and physicalinduction of post-harvest disease resistance reveal thatjasmonates have not garnered as much attention as othermeans of induced post-harvest defence (Gozzo, 2003;Terry and Joyce, 2004).

Potential uses of MeJA in preventing chilling injury orpost-harvest disorders have also been studied. MeJAapplied as a dip ( 25 M) or gas ( 100 M) to avocado(Persea americana Mill.), grapefruit, or pepper fruit priorto chilling reduced chilling injury (Meir et al., 1996; Funget al., 2004). Banana fruit stored for 1 week at 5C wereprotected from chilling injury by 1 mM n-propyl

dihydrojasmonate (PDJ; Chaiprasart et al., 2002). MeJAreduced decay in three strawberry cultivars stored at 5Cor 10C (Moline et al., 1997) and delayed chilling injuryin zucchini squash (C. pepo) and cucumber fruit (Wangand Buta, 1994; 1999). MeJA reduced chilling injury anddecay in papaya (Carica papaya L.) fruit and, inconjunction with modified atmosphere packaging(MAP), resulted in the least decay (Gonzlez-Aguilar etal., 2003). Chilling injury was reduced in two cultivars ofguava (Psidium guajava L.) treated with MeJA, butquality maintenance was cultivar-specific (Gonzlez-Aguilar et al., 2004). Peaches dipped in 1 mM MeJA hadelevated polygalacturonase activity (Budde et al., 2005),which may reduce woolliness in cold-stored fruit (Buddeet al., 2005; Ben-Arie and Sonego, 1980). MeJA appliedas a dip or a gas at 100 M inhibited root and shootgrowth of harvested, topped radish (Raphanus sativus L.;Wang, 1998). MeJA applied as a gas (0.01 mM) reducedchilling injury and decay in tomato fruit stored at 5C for2 4 weeks, enhanced the uniformity of ripening, anddelayed ripening (Ding et al., 2001; 2002). A dip in PDJslowed development of chilling injury in mango at 6C(Kondo et al., 2005),and MeJA as a gas was also effective(Gonzlez-Aguilar et al., 2000). Treatment with volatileMeJA enhanced the soluble sugar content and slowedthe loss of organic acids in raspberries after storage(Wang, 2003). Therefore, MeJA can positively modify

post-harvest physiology for horticultural gain in anumber of crops.Jasmonates may enhance the harvestability of fruits.

Reducing the force required to detach Hamlin orange[Citrus sinensis (L.) Osb.] fruit from trees wasaccomplished with < 10 mM MeJA as a spray, but MeJAcaused undesirable leaf abscission (Hartmond et al.,2000). MeJA applied to Valencia orange at 15 mMcaused less leaf abscission than a mix of ethephon(2-chloro-2-ethyl-phosphonic acid) and 1-MCP (an

anti-ethylene agent), while reducing the fruitdetachment force to levels equal to ethephon-treatedplants (Pozo et al., 2004). MeJA (1 mM) also increasedabscission in harvested cherry tomatoes (Beno-Moualemet al., 2004),which is undesirable in such fruits, marketedattached to the peduncle. These results were, at least inpart, a result of MeJA-enhanced ethylene production,but ethylene-independent abscission can not beruled-out (Beno-Moualem et al., 2004; Hartmond et al.,2000; Miyamoto et al., 1997).

Enhancing crop quality for human utilityThere are other unique, potential uses for MeJA in

horticultural applications to enhance food quality. MeJAenhanced resveratrol accumulation in Vitis vinifera L.leaves (Belhadj et al., 2006), and resveratrol has benefitsfor human health (Opie and Lecour, 2007). Jasmonatesalso increased the glucosinolate content of cruciferousvegetables such as Brassica napus, B. rapa, B. juncea,andRaphanus raphanistrum (Agrawal et al., 1999; Bodnaryk,1994;Doughty et al., 1995).Glucosinolates are precursorsof isothiocyanates, which act as chemopreventativeagents (Hecht, 1999). Similarly, it may be possible toenhance the anthocyanin contents of fruits andvegetables (Table I). V. vinifera cell cultures showedenhanced anthocyanin accumulation when treated withjasmonates (Curtin et al., 2003; Zhang et al., 2002), and

MeJA increased the anthocyanin (Rudell et al.,2002) andcarotenoid (Prez et al., 1993) contents of apple fruit andthe anthocyanin content of A. thaliana (Jung, 2004).Raspberry (Rubus idaeus) fruit treated with 100 MMeJA vapour and stored at 10C were darker and morered in colour than untreated fruit, presumably due toelevated anthocyanin contents (Wang, 2003). Pre-harvesttreatment of young R. idaeus and R. occidentalis L. fruitswith 0.01 mM or 0.1 mM MeJA enhanced anthocyanin,phenolic, anti-oxidant, and flavonoid contents (Wangand Zheng, 2005). This was also shown by the fact thatMeJA-treated raspberries had a greater oxygen radicalabsorbance capacity (ORAC) than untreated raspberriesafter 10 d in storage (Wang, 2003). MeJA-treatedstrawberry fruit also had greater anthocyanin andphenolic contents, and greater ORAC after 12 d storage(Ayala-Zavala et al., 2005).However, a conflicting reportshowed that MeJA inhibited anthocyanin accumulationin apple (Saniewski et al., 1988).Some glucosinolates andanthocyanins have chemopreventative or other health-related properties (Wattenberg, 1985), so jasmonatesmay increase the healthfulness of treated products.

Other health-giving properties of plants may beaffected by jasmonates. Leaves of drought-stressedstrawberry have lower than normal levels of ascorbicacid [vitamin C, a powerful anti-oxidant in the humandiet (Byers and Perry, 1992; Wang, 1999)]. However,

treating strawberry plants with 0.1 mM MeJA, prior todrought stress, maintained their ascorbic acid levels(Wang, 1999). Drought-resistant corn seedlings had

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higher ascorbic acid levels after a 2 d drought stress if theseeds were treated with 112 M MeJA (Li et al., 1998).

A. thaliana cell cultures treated for 21 h with 50 MMeJA had 64% more ascorbic acid than untreated cells,but cell growth (and ascorbic acid levels) depended onthe presence of auxin and cytokinin (Wolucka et al.,2005). However, the total carotenoid contents of

S. lycopersicum and S. tuberosum decreased aftertreatment with a high concentration (> 4 mM) of MeJAas a spray (Cohen et al., 1993),and 10 mM MeJA reducedthe carotenoid content of Pisum sativum seedlings(Fedina and Tsonev, 1997). MeJA [as a gas or 5% (w/w)in lanolin paste] reduced the lycopene content of tomatofruit, but raised -carotene levels (Saniewski andCzapski, 1983; Czapski and Saniewski, 1985). This wassupported by research suggesting that reducedendogenous levels of jasmonates in tomato fruit at thelater stages of ripening are needed to permit lycopenesynthesis (Fan et al., 1998a). Further research in this areais necessary to study the specific effects of MeJA onhealthful compounds in foods.

The pharmaceutical content of plants may beenhanced by jasmonates (Zhao et al., 2005).Potentially medically-useful saponins were induced byjasmonates in Glycyrrhiza glabra L. (Hayashi et al.,2003), Panax ginseng C.A.Mey. (Lu et al. , 2001), andBupleurum falcatum Dalzell and Gibs. (Aoyagi et al.,2001) cell cultures. Taxol (paclitaxel) from Taxuschinensis cell cultures is a useful metabolite that isinduced by MeJA (Wang and Wu, 2005; Wu and Lin,2003). Alkaloids were induced by MeJA inCatharanthus roseus L.G. Don seedlings (Aerts et al.,1994), and such alkaloids are used in human medicine(van der Heijden et al., 2004). An anti-microbial

compound from Cupressus lusitanica cell cultures,with potential uses in medicine, was induced byjasmonates (Zhao et al., 2001; 2004). Apodophyllotoxin derivative is used in cancertreatment, and podophyllotoxin is inducible in in vitrocultures of Linum album (van Frden et al. , 2005). Itmay be profitable to enhance pharmaceuticalproduction by plants through the elicitation ofsecondary metabolite production using jasmonates.

Anthocyanins are not just healthful, they add colour toornamental plants and food. Enhancing anthocyaninaccumulation for aesthetic purposes may be useful ingreenhouse-grown ornamental crops, where the absenceof natural ultraviolet light and high temperature maylimit anthocyanin production. Examples of crops inwhich anthocyanins are an important part of plantappearance include ornamental kale (B. oleracea),purple fountain grass (Pennisetum setaceum Rubrum),and numerous potted and cut-flowering crops. MeJA(5 M) enhanced the anthocyanin content of detachedpetunia (Petunia hybrida) corollas (Tamari et al.,1995). Colour is also an important quality attribute inproduce. MeJA vapour (8.3 mg fruit1) or spray (10 mM)or JA spray (1 10 mM) promoted degreening andintensified the colour of Golden Delicious or Fujiapples (Fan et al ., 1998b). Mango degreening was alsoenhanced by 104 M MeJA vapour (Lalel et al., 2003).

Peach fruit were more red than control fruit when thetrees were sprayed six times with 10 mM MeJA (Janoudiand Flore, 2003), although MeJA also reduced fruit

firmness. Enhanced and uniform colour in ornamentaland food crops may add to their economic value, andjasmonates may be useful to this end.

Jasmonates in abiotic stress responsesPhysiological stress responses in growing plants may

be modified by jasmonates. JA and JA-induced protein

levels in barley leaf segments were enhanced by osmoticstress via sorbitol treatment (Kramell et al., 1995;Lehmann et al., 1995). Jasmonates play a role in waterstress through their effects on stomatal apertures.Stomatal closure is regulated or enhanced by jasmonates(Pospilov, 2003; Table I). Sensitivity to bothjasmonates and ABA was required for the full stomatalclosure response in Arabidopsis (Suhita et al., 2004).Levels of the osmoprotectant, glycine betaine, increasedas the JA content in grafted Pyrus bretschneideri Redh.increased in response to exogenous JA application (Gaoet al., 2004). There is strong evidence for the interactionof jasmonates and ABA in water-stress signalling, but theutility of jasmonates in preventing stress is unclear.Would treating transplants in plug trays, or bareroottransplants, with JA reduce dessiccation stress duringshipping or storage? Would JA treatment increase salttolerance? Treating barley with 25 M JA prevented thestress caused to photosynthetic systems after transfer to100 mM NaCl (Tsonev et al., 1998). MeJA (10 M)reduced photosynthesis in Pisum sativum, butmoderated NaCl-induced declines in photosynthesis andRuBisCO enzyme activity and NaCl-induced increasesin photorespiration, CO2 compensation point, andrespiration (Fedina and Tsonev, 1997; Velitchkova andFedina, 1998). The effects of water stress in strawberry(Fragaria vesca), including elevated levels of oxidative

stress, were reduced when plants were treated withMeJA (Wang, 1999). Hordeum vulgare roots treated with5 M JA for 24 h, then osmotically stressed, had lessmembrane damage than stressed roots not treated withJA (Bandurska and Stroiski, 2001). These data suggestthat pre-treating plants, before transplanting into salinesoil or media, or before prolonged drought, may allowthem to be productive in soils with high salts or whenunder drought stress.

Jasmonates also play a role in reducing ozone stressresponses. Exogenously applied jasmonates protected

A. thaliana (Overmyer et al., 2000; Rao et al., 2000) andN. tabacum (rvar et al., 1997) from ozone-inducedhypersensitive cell death, which was probably the resultof attenuated SA-mediated hypersensitivity. A hybridpoplar (Populus maximowiczii Henry P. trichocarpaTorr & A.Gray), tolerant of ozone damage, was lessdamaged by ozone when treated with jasmonates 3 24 hbefore ozone treatment (Koch et al., 2000).Similar to saltstress, jasmonates may be useful in protecting plantsprior to transplantation into high-ozone areas.

SUMMARY AND FUTURE DIRECTIONSAs biological control becomes more prevalent, useful,

and important in horticultural crop production, targeteduse of jasmonate-induced defences may provide valuable

augmentation of integrated pest management strategies.For example, jasmonates may be used to treat localisedinfestations where a pest threshold is exceeded, with the

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goal of attracting pre-released predators or parasitoidsto that area. In a greenhouse, it may be possible to use acombination of treating ornamentals with jasmonates,and growing trap crops (plants naturally attractive topests) nearby, to reduce the pest pressure on theornamentals through: (i) attraction of beneficials to theornamentals, (ii) induction of chemical defences in the

ornamentals, and (iii) accumulation of pests on the trapcrops. Further research in this area is necessary beforeany of these unique strategies become feasible as controlstrategies. It is also crucial to recognise that thehorticultural utility of JA-induced defence is highestwhen economic thresholds are high and when pestproliferation may be predicted (Stout et al., 2002). Inaddition to the role of jasmonates in protecting growingplants from herbivorous arthropods, jasmonates have aclear record of protecting ornamental and food cropsfrom post-harvest disorders and diseases. Jasmonatesalso may enhance aspects of plant quality, or be useful inpropagation. However regulatory approval ofjasmonates or their analogues is necessary before manyof these applications can be used commercially.

Research comparing the efficacy of variousapplication methods of jasmonates and their analogues(e.g., MeJA as a gas or spray? Coronatine sprays?Dihydrojasmonic acid sprays?) needs to continue. It isclear that controlled application of MeJA as a gas can

elicit jasmonate responses in plants. It may be possiblethat treating plants with volatile MeJA in a cooler,shipping truck, box, or greenhouse may elicit beneficialjasmonate responses. Results from early work onjasmonate-induced defence responses suggest that someplants themselves may serve as a source of volatile MeJA(Farmer and Ryan, 1990), but the practicality of using

this in a commercial production situation is uncertain.Jasmonates are a curious class of plant hormones.Theyare involved in complex, yet specific, interactionsbetween plants and pests, and between plants andpathogens. Jasmonates are involved in tritrophicinteractions between plants,pests, and predators of thosepests. The web of interactions linking jasmonateresponses with other hormone signalling pathways isbecoming clearer. Jasmonates can alter physiologicalprocesses in plants, to make plants more valuable tohumans, or more easily propagated. Much jasmonateresearch, compared to work on other plant hormones, isin its infancy, but continued research into many variedaspects of horticultural science is important. Such workwill undoubtedly result in useful applications ofjasmonates for horticultural crop production.

References to commercial products are not intendedto be endorsements of the product to the exclusion ofother products.

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