Journal of Horticultural Science & Biotechnology (2008) 83 (3) 283304

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 Folwell Avenue, St. Paul, MN 55108, USA (e-mail: erwin001@umn.edu) (Accepted 22 January 2008)
SUMMARY Plant growth and development are controlled, in part, by endogenous growth substances which are affected by biotic and abiotic signals and events. A particular class of growth regulators, collectively called jasmonates are involved in plant responses to such events and elicit unique responses. The effects of jasmonates on plant growth are varied and include 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 how jasmonates may impact horticultural crop growth, physiology, protection from stresses, and/or handling.

asmonates are a class of endogenous plant growth regulators that have unique and potentially commercially useful properties that affect plant growth and development. As a class, these compounds generally aide in defending a plant and possibly surrounding plants from attack by pests and/or diseases. Here, we summarise jasmonate-related research on horticultural crops and possibilities for future research related to the application of this unique class of compounds in horticultural crop production. For the purposes of this review, jasmonates include jasmonic acid (JA), methyl jasmonate (MeJA), and closely-related analogues. Octadecanoid precursors to JA, or related products of fatty acid metabolism, are implicated in some JA-independent responses (Stinzi et al., 2001; Farmer et al., 2003), but they will not be discussed extensively here. Jasmonate is a broad term covering numerous compounds, but MeJA is particularly interesting because of the myriad of plant responses associated with its synthesis and presence. Post-harvest application of MeJA as a gas can activate defences and prevent postharvest disorders in a number of horticultural crops (see Pre- and post-harvest jasmonate application below). MeJA is emitted by wounded plants (Meyer et al., 2003) and, therefore, may represent a means of communication between damaged plants. Jasmonate-induced volatiles have been shown to attract beneficial arthropods (Table I), a potentially useful response in the production of horticultural crops. Numerous resources exist describing the analysis of jasmonate-mediated responses identified by altered gene expression, but here we will focus on the effects of exogenous jasmonates on plant responses downstream from molecular responses. Here, we outline: (i) what jasmonates are; (ii) jasmonateinduced morphological and physiological responses in plants; (iii) jasmonate research of relevance to
*Author for correspondence.

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

WHAT ARE JASMONATES? Definition and distribution in plants MeJA was discovered in 1962 as a sweet-smelling compound in Jasminium grandiflorum L. flower extracts (Demole et al., 1962). After its discovery in jasmine flowers, JA was isolated from a pathogenic fungus, Lasiodiplodia theobromae (Aldridge et al., 1971). The biological activity of MeJA, extracted from Artemisia absinthium L., was reported nearly 10 years later (Ueda and Kato, 1980). Since then, jasmonates have been found in many species and are considered ubiquitous (Meyer et al., 1984; Hamberg and Gardner, 1992). Jasmonates are defined as hormones because they elicit cellular responses at low concentrations distant from their site of synthesis. For instance, long-distance wound-signalling is at least partially mediated by the interplay of jasmonate and systemin throughout the vascular system, and likely involves H2O2 (Browse, 2006; Ryan and Moura, 2002; Schilmiller and Howe, 2005; Stratmann, 2003; Wasternack et al., 2006). The quantity of jasmonates in plants typically ranges from 0.01 3.0 ng g1 fresh weight (FW), but up to 95 g g1 MeJA was detected in Artemisia tridentata ssp. tridentata Nutt. (Preston et al., 2004). Jasmonate levels can be higher in some tissues than in others. As a percentage of the total JA and MeJA present in tomato flowers, MeJA content was 13% in pistils and 53% in petals (Miersch et al., 2004). Jasmonates are synthesised via the octadecanoid pathway, beginning at linolenic acid and ending at (+)-7-epiJA, and its conjugates and isomers [reviewed by Liechti and Farmer (2006); Schaller et al. (2005); Wasternack (2006)]. JA metabolite physiology has recently been discussed elsewhere (Delker et al., 2006; Wasternack, 2007).

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TABLE I Responses to exogenous jasmonates

Plant Species 52 55, 75 114 36 26, 109 90, 124126, 137, 153 50 52, 95, 129, 130 52 95 111 13 13, 32 13 101 4 2 52 92 44 16, 17 1, 52 151, 152 52 52 14 5 109 80 63 20

Formation of Tubers or Other Storage Organs Abscission or Degradation of Chlorophyll Enhanced Resistance to Pathogens

Reduced Transpiration or Closure of Stomata Accumulation of Non-Jasmonate Secondary Compounds Accumulation Decreased Performance of Anthocyanins of Arthropod or Herbivores Carotenoids (Weight, Proliferation, etc.)

Attraction of Predatory or Parasitic Arthropods

61, 64, 93 136

62, 64, 65

89 6 138

12 44, 45 106 6

41 134 43, 44 47 37, 55 86 52 25, 33, 52 52, 141 128 71 110 44 135 83, 144 49, 73 54 88 54 88, 94 69 7, 40, 56, 58, 91, 132 52 8 5 59, 77, 91, 132, 133 59 97 52 52 52 107

Horticultural applications of jasmonates

Agrostemma githago Allium sativum Apium graveolens Arabidopsis thaliana Arachis hypogaea Artemisia vulgaris Avena sativa Bellis perennis Brassica juncea Brassica napus Brassica oleracea Brassica rapa Bryophyllum calycinum Bupleurum falcatum Catharanthus roseus Chelidonium majus Commelina benghaensis Crotolaria cobalticola Cucumis melo Cucumis sativus Cupressus lusitanica Dioscorea opposita Dolichos lablab Dryopteris filix-mas Echinacea pallida Eschscholzia californica Forsythia intermedia Fragaria ananassa Fragaria vesca Gerbera jamesonii Ginkgo biloba Glycine max Glycyrrhiza glabra Gossypium hirsutum Gossypium spp. Helianthus annuus Hordeum vulgare Hyoscyamus muticus Kalanchoe blossfeldiana Lactuca sativa Larix decidua Lilium longiflorum Linum album Lithospermum erythrorhizon Macaranga tanarius Malus baccata mandschurica Malus spp. Mangifera indica Narcissus triandrus Nicotiana attenuata Nicotiana rustica Nicotiana sylvestris Nicotiana tabacum

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52, 145 70, 84, 131 74 108 115 18, 48 46, 52 34, 76, 148 81 34 38, 68, 148 143 100 3 44 79 44 44 140 140 52 57 51 29, 96 19 104, 105, 112 105 146 60 139, 142 82 147 52 10, 52 10 99 78 52 52 28 9 52 27, 149 85 127 9 15, 21, 23, 24, 53, 72, 113, 117123 116, 121 52 11, 52, 98 67, 150 52 52 52 35 31, 42 39 95

103 70

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C. L. ROHWER and J. E. ERWIN

Olea europaea Oryza sativa Panax ginseng Paphiopedilum Supersuk Pelargonium zonale Petunia hybrida Phaseolus lunatus Phaseolus vulgaris Picea abies Picea sitchensis Pisum sativum Prunus persica Pterostylils sanguinea Raphanus raphanistrum Rauvolfia canescens Rosa hybrida Rubia tinctorum Rubus idaeus Rubus occidentalis Ruta chalepensis Sambucus nigra Scopolia parviflora Sinapis arvensis Solanum lycopersicum Solanum tuberosum Spinacia oleracea Taraxacum officinale Taxus baccata Taxus canadensis Taxus chinensis Taxus cuspidata Taxus media Trifolium repens Triticum aestivum Tulipa gesneriana Ulmus minor Urtica dioica Vicia faba Vigna radiata Vitis vinifera Zea mays 22, 123 22

66, 87

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Horticultural applications of jasmonates range from 107 103 M. It is important to recognise that MeJA 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 responses to MeJA (Janoudi and Flore, 2003). Morphological responses Changes in plant development and structure are associated with the presence of jasmonates. Most notable is the promotion of storage organ formation by jasmonates (Table I). For instance, tuberisation in Chinese yam (Dioscorea opposita Thunb.) was promoted by jasmonates (Koda and Kikuta, 1991). Spraying field-grown Chinese yam with 5 10 mg l1 of a JA analogue increased tuber yield by 15 40% (Kim et al., 2005). JA was able to enhance tuber formation in Pterostylis sanguinea D. Jones and M. Clements in vitro, but this response also had an optimal concentration, and the response was dependent on the sucrose content of the medium (Debeljak et al., 2002). The need for jasmonates for tuberisation in soil-grown potato is not certain (Jackson, 1999), and a recent study showed no effect 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 than kinetin (11.6 M) in vitro (Pelacho and Mingo-Castel, 1991). Theobroxide, a metabolite from the fungus Lasiodiploidia 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 to jasmonates (Koda et al., 1991). Bulblet formation in garlic (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 (Ravnikar et al., 1993), and 10 M JA stimulated bulbing in onion plantlets (Koda, 1997). In vitro culture of Narcissus triandrus L. shoots on medium containing JA enhanced bulb number and quality (Santos and Salema, 2000). Gaseous MeJA reduced FW and bulblet number in Lilium longiflorum Thunb. and Asiatic hybrid Lilium Connecticut King explants, but the effects on Lilium speciosum Thunb. were minimal. Interestingly, MeJA reduced the cold requirement for bulblet sprouting (breaking of dormancy) in these lily species (Jsik and de Klerk, 2006). In some cases, flowering may be influenced by jasmonates. JA (106 M) inhibited flower bud formation in thin-layer explants of day-neutral N. tabacum L. (Barendse et al., 1985). Cultures of another day-neutral plant, Spirodela polyrrhiz (L.) Schleiden, showed enhanced flowering when JA was included in the culture medium (Krajni and Nemec, 1995). Theobroxide reduced flowering and stem elongation in spinach (Spinacia oleracea L.), a long-day plant, through a reduction in gibberellic acid content (Kong et al., 2006). MeJA also reduced or inhibited flowering in the longday plant Chenopodium rubrum L. (Albrechtov and Ullmann, 1994). Theobroxide induced flowering in the short-day plant Pharbitis nil Chois. under 18-h (non-inductive) photoperiods, but downstream signals, including jasmonates, may be the final signal of theobroxide effects (Yang et al., 2004; Yoshihara et al., 2000). Treating Pharbitis with MeJA before an inductive

Other jasmonates with biological activity include tuberonic acid (from the leaves of Solanum tuberosum L.; Yoshihara et al., 1989), dihydrojasmonic acid (from Vicia 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 some jasmonate 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 anthocyanin content of apples (Kondo et al., 2000). Coronatine is a phytotoxin from Pseudomonas syringae pv. tomato with structural similarities to octadecanoid precursors of JA. Within its structure is a 5-membered keto-ring compound with stereochemistry similar to (3R-7S)-JA, which is thought to be the most active isomer of JA. Coronatine induced tendril coiling in Bryonia dioica Jacq. and alkaloid accumulation in Eschscholzia californica Cham. (Weiler et al., 1994). Coronatine is active at lower concentrations than JA in inducing potato (S. tuberosum L.) tuber cell expansion (Koda, 1997).

HOW DO JASMONATES AFFECT PLANT MORPHOLOGY AND PHYSIOLOGY? Methods of application Jasmonates can be applied to plants in a variety of ways. For instance, MeJA may be applied to plants as a gas in an enclosed environment. In the gas phase, MeJA can induce plant defence responses. MeJA (at 8 nl l1, or approx. 8 g l1) saturated the promotion of protease inhibitor 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 responses were detected in cotton treated with 18 mol MeJA vapour in 31.8 l ventilated chambers (Rodriguez-Saona et al., 2001). The use of volatile MeJA as an application technique is worth more detailed study. Post-harvest treatments with other gases are not uncommon; ripening is often initiated and synchronised in bananas (Musa acuminata Colla) with ethylene (Reid, 1992), and 1-methylcyclopropene (1-MCP) may be used to prevent ethylene damage to fruit, cut flowers, or potted flowering plants (Blankenship and Dole, 2003), for example. In contrast to applying it as a gas, some researchers mix MeJA in a lanolin paste, and spread the paste on plant 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, some researchers applied MeJA in a liquid form to a hydroponic solution (Baldwin and Schmelz, 1996). If roots are the primary site of action for jasmonate responses (e.g., nicotine synthesis in Nicotiana roots), this method of application reduces the effects of jasmonate transport to the roots by exposing the site of action directly to the hormone. Jasmonate sprays typically contain a surfactant (such as polysorbate or Triton X-100), and a small amount of solvent, such as acetone or methanol, to dissolve the jasmonate. Typical concentrations of jasmonates sprays

C. L. ROHWER and J. E. ERWIN 8-h photoperiod inhibited flowering (Maciejewska and Kopcewicz, 2002), but theobroxide treatment during inductive photoperiods increased flower number (Yang et al., 2004; Yoshihara et al., 2000). It is difficult to compare these results directly due to the different chemical treatments and experimental conditions, but jasmonates appeared to have an effect on P. nil flowering. JA promoted flowering in a long-short-day plant, Wolffia arrhiza (L.) Horkel ex Wimm. when applied during the second photo-inductive period (Krajni and Cenci, 2000). JA also promoted flowering in the long-day plant Lemna minor L. (Krajni et al., 2006). It may be possible to use jasmonates for ornamental plant production, or for breeding purposes, to induce uniform flowering in some plants that flower unreliably or non-uniformly. Wasternack (2006) outlined other variable roles of jasmonates in flowering, including anther development and dehiscence, female organ development, chemical defence production, colour production (discussed later), and the attraction of pollinators. Many other morphological responses are not flowering- or storage organ-related. Shoot growth, fruit number, inflorescence number, and development rate of Phaseolus lunatus L. were enhanced by 1 mM JA (Heil, 2004b). More nodes and greater internode length were found on Vitis vinifera L. stems in tissue culture when 0.5 M JA was added to the culture medium (Ravnikar et al., 1990). Parenchyma cell diameter was smaller, and metaxylem vessel diameter and number were larger in Gloriosa rothschildiana OBrien grown in a culture medium with 25 mg l1 MeJA (Weryszko-Chmielewska and Kozak, 2002). MeJA generally inhibited root and shoot growth in P. nil, although a very low concentration (107 M) enhanced elongation (Maciejewska and Kopcewicz, 2002). Four or six applications of MeJA to 5-year-old peach (Prunus persica L. Batsch) trees reduced shoot growth, and 14 applications of MeJA reduced branch length, canopy density, leaf area, and leaf FW in Malus baccata mandschurica (Janoudi and Flore, 2003). Delayed development of S. lycopersicum plants was noted after treating plants with 5 10 mM MeJA, but this effect was temporary (Boughton et al., 2006). MeJA and JA promoted the germination of dormant Malus embryos (Ranjan et al., 1994). This may be a useful response to promote germination in difficult-togerminate plants. Some responses are morpho-physiological. Rapid changes in the shape or structure of a plant part often require rapid changes in cell physiology. For example, Mimosa pudica L. pulvinules closed in response to the presence of JA in darkness in the presence of indole-3acetic acid (IAA) and in the light without IAA (Tsurumi and Asahi, 1985). IAA caused tendril coiling in B. dioica, but higher concentrations of IAA were necessary for a similar response induced by MeJA (Falkenstein et al., 1991). Physiological responses Plants have a variety of defences against stress. Some of these are physical or morphological in nature, and some are chemical. Constitutive plant defences include glandular trichomes, cuticular waxes, and other structural and chemical defences (Wittstock and Gershenzon, 2002). Inducible chemical defences include a wide

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variety of compounds that are toxic, anti-nutritive, or injurious to attacking organisms, including alkaloids, phenolic compounds, chitinases, and protease inhibitors, among others. Plant enzyme systems or inhibitors can be defensive and 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 sticky polyphenolic compounds that may entangle arthropod herbivores as they move past glandular trichomes (Kennedy, 2003). PPO activity is inducible by volatile or liquid jasmonates in many plants (Alba-Meraz and Choe, 2002; Doan et al., 2004; Constabel and Ryan, 1998; Constabel et al., 2000). Peroxidases function in numerous biochemical processes, but they may be related to the production of reactive oxygen species or structural defences (e.g., lignin, cell wall crosslinks). Peroxidase and PPO were induced in tomato plants 36 h after a 12-h treatment with gas-phase MeJA (Thaler et al., 1996), 48 h after 0.5 10 mM JA treatment (Cipollini and Redman, 1999; Thaler, 2002; Thaler et al., 1996), or 72 h after spraying plants with 7.5 mM or 10 mM MeJA (Boughton et al., 2006). Treating Cucurbita melo L. seeds with gaseous MeJA induced defences against soil-borne seedling pathogens, but did not induce peroxidase (Buzi et al., 2004b). However, soaking seeds in 45 M MeJA induced both lipoxygenase and peroxidase synthesis (Buzi et al., 2004a). PPO and protease inhibitors were induced systemically in S. lycopersicum after treatment of one leaflet with 0.5 mM JA, and lipoxygenase was induced locally (Thaler et al., 1996). Protease inhibitors block the function of proteolytic enzymes in the gut of herbivores, but the mode of toxicity may also involve the stimulation or overproduction of digestive enzymes, leading to amino acid starvation (Broadway and Duffey, 1986). A S. lycopersicum protease inhibitor mRNA was systemically induced 3 h after an application of 1 mM JA (Fidantsef et al., 1999). JA, and intermediates in JA synthesis, induced the accumulation of protease inhibitors in S. lycopersicum. Less than 10 nmol per plant of 13(S)-hydroperoxylinoleic acid (a JA precursor) promoted the accumulation of protease inhibitor in 15-d-old plants (Farmer and Ryan, 1992). Gas-phase MeJA (80 nl l1) induced inhibitors in less than 1 h, and the response to constant MeJA application was saturated after 40 h (Farmer and Ryan, 1990). Less than 1 nl l1 MeJA induced inhibitors after 24 h of treatment (Farmer and Ryan, 1990). Artemisia tridentata (sagebrush) clippings, when put in an enclosed chamber with S. lycopersicum, induced protease inhibitor activity in S. lycopersicum. MeJA was isolated as the active component of the sagebrush (Farmer and Ryan, 1990). MeJA also induced protease inhibitor accumulation in Medicago sativa L. and N. tabacum cv. Xanthi NC (Farmer and Ryan, 1990). Jasmonate treatment increased protease 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; van Dam et al., 2001a, b), and Solanum (Bolter, 1993; Thaler et al., 1996, 2001; Stout et al., 1998).

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Horticultural applications of jasmonates Mutants unable to synthesise trienoic fatty acids (JA precursors), or an enzyme necessary for JA synthesis, were male-sterile because of unsuccessful pollen development (McConn and Browse, 1996; Stinzi and Browse, 2000). A tomato mutant (JL5) incapable of synthesising jasmonates has 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 pathway are abundant (Devoto and Turner, 2003, 2005; Glazebrook et al., 2003; Liechti et al., 2006; Gfeller et al., 2006). Genes specifically involved in jasmonate-induced defences in tomato and A. thaliana have also been reviewed (Walling, 2000). The jasmonate response pathway utilises a protein turnover mechanism, similar to other hormone response pathways (Browse, 2006). A skp-like/cullin/F-box (SCF) ubiquitin ligase, in conjunction with a proteasome, controls jasmonateregulated protein turnover (reviewed by Wasternack, 2006). In A. thaliana, COI1 is the F-box protein in the jasmonate response complex SCFCOI1 (Xu et al., 2002). In tomato, JAI1 is the COI1 homolog (Li et al., 2004). No discussion of jasmonate responses can occur independently 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 that jasmonate- and ethylene-responsive gene expression patterns cluster together in defence signalling (Glazebrook et al, 2003). In pathogen defence responses, PDF1.2 gene activation required simultaneous perception 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 at 5 nmol and 50 nmol JA plant1 (Schmelz et al., 2003b). MeJA-induced gum formation in Prunus persica Batsch was proposed to act through the induction of ethylene (Saniewski et al., 1998b). Ethylene perception was necessary for jasmonate-induced accumulation of protease inhibitor transcripts in S. lycopersicum (ODonnell et al., 1996), and simultaneous ethylene and MeJA treatment enhanced protease inhibitor transcript accumulation in N. sylvestris Speg., more than either MeJA 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 or ethylene-antagonised jasmonate responses have been discovered. Ethylene blocked MeJA-induced vegetative storage protein accumulation in A. thaliana (Matsushima et al., 2002). A. thaliana ethylene response mutants showed enhanced accumulation of jasmonate-responsive transcripts compared to wild-type plants (Rojo et al., 1999). An S. lycopersicum mutant impaired in jasmonate synthesis (def1) could be made resistant to Botrytis cinerea Pers. ex Fr. by treating plants with ethylene before inoculation. However, an S. lycopersicum line over-expressing pro-systemin, which activates jasmonate signalling, was more resistant to B. cinerea and did not require 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 from Botrytis by gas-phase MeJA (Thomma et al., 1999a).

The induction of anti-nutritive compound synthesis using jasmonates is a promising area of research for pest control (discussed below), and there is potential for specifically creating protease inhibitor-enforced plants to resist pests (Lawrence and Koundal, 2002). For instance, mortality in the first and second generation of potato aphid (Macrosiphium euphorbiae Thomas) was increased when they fed on S. lycopersicum treated with 1.5 mM JA, presumably due to anti-nutritive defence compounds induced in the plants, including protease inhibitors (Cooper and Goggin, 2005). Other research showed that jasmonate-induced deaminase enzymes in tomato plants caused the catabolism of essential amino acids in insects, further rendering the plant less nutritious (Chen et al., 2005). Some researchers have proposed undesirable effects on non-target organisms or predatory or parasitic arthropods following jasmonate-induced plant defences. One proposed mechanism for these effects is the accumulation of toxic compounds in the herbivore (Malone and Burgess, 2000). When S. lycopersicum was treated with JA, a reduction in the number of syrphid fly (a predator of aphids) eggs was noted. However, this was also correlated with a reduction in the number of aphids, suggesting that predator number differences could have been affected by aphid density (Thaler, 2002). The number of Aphelinid-parasitised aphids on S. lycopersicum was unaffected by JA treatment (Thaler, 2002). Survivorship of Spodoptera exigua Hbner caterpillars was reduced when they fed on JA-treated S. lycopersicum, but parasitism by Hyposoter exiguae wasps was less effective on caterpillars fed jasmonatetreated tissue (Thaler, 2002). This was explained by a lower body weight per caterpillar when reared on jasmonate-treated leaves. The negative effects of exogenous jasmonates on parasitoids or predators could result from the reduced performance of the host, or food source for these arthropods. Interestingly, it has been suggested that low doses of protease inhibitors may be more useful than high doses in biologically-oriented integrated pest management (IPM) programmes (Cloutier and Michaud, 2000). Low doses of toxic compounds would theoretically reduce pest performance without affecting predator or parasitoid survival or fecundity. If true, this means the that fine control of protease inhibitor induction with jasmonates is more useful than maximum induction. Structural defences also may be jasmonate-inducible, or require jasmonate signalling. For instance, trichome number and density increased after jasmonate application to Arabidopsis (Traw and Bergelson, 2003) or tomato (Boughton et al., 2005). An S. lycopersicum jasmonate signalling mutant had fewer trichomes, and glandular trichomes that had a lower terpenoid content (Li et al., 2004). MeJA induced phenolic- or resin duct-related structural defence responses in 16 species representing five gymnosperm families (Franceschi et al., 2002; Hudgins et al., 2003; 2004; Martin et al., 2002). Mutants and mechanisms of jasmonate action A number of A. thaliana mutants related to jasmonate synthesis and action have been identified [reviewed by Berger (2002); Rosahl and Feussner (2005); Beckers and Spoel (2006); Delker et al. (2006); Wasternack (2006)].

C. L. ROHWER and J. E. ERWIN Ethylene blocked jasmonate-inducible nicotine accumulation, or biosynthesis, in N. attenuata (Kahl et al., 2000; Winz and Baldwin, 2001) and in N. sylvestris (Shoji et al., 2000). Jasmonate signalling is required for the containment of cell death in ozone-treated A. thaliana; but ethylene 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 plants compared to plants treated with AgNO3, without MeJA (Curtis, 1984), suggesting ethylene-independent abscission. It is clear that ethylene and jasmonates are involved in induced defence responses, and that the signalling pathways needed for resistance responses are specific to particular species and stress systems.

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The utility of commercial inducers of plant defences has been established by these examples. The impact of SAR on jasmonate-regulated responses is varied and will be discussed in the next section. Use of jasmonates in induced defences against pests and pathogens Jasmonates are an integral part of plant biotic defence signalling. Resistance to plant pests can be enhanced by jasmonate treatment (Table I), and jasmonate synthesis or response mutants have helped to explain possible mechanisms (Halitschke and Baldwin, 2006; van Poecke, 2007). Stout and others (2002) noted that the utility of eliciting multiple defences within a single plant, including direct and indirect defences, is inherently resilient to the development of pest resistance. Much of the work in this area has focussed on the inhibition of feeding by lepidopteran larvae; but Thaler et al. (2001) showed that Frankliniella occidentalis Pergande (thrips, a cell content-feeding insect) and aphid (a phloem-feeding insect) populations were reduced in field plots of tomatoes treated with JA. JA (1 mM) sprayed on fieldgrown S. lycopersicum reduced the survivorship of S. exigua placed on the plants, and reduced the number of naturally-occurring F. occidentalis found 3 weeks after treatment (Thaler et al., 1999). In a separate study, thrips survivorship on tomatoes was not affected by JA treatment, but thrips damage was reduced by JA treatment (Thaler et al., 2002c). M. persicae populations were reduced in tomato plants treated with 5 10 mM MeJA (Boughton et al., 2006). Jasmonate signalling was required for defence against T. urticae in S. lycopersicum (Li et al., 2002; 2004), and exogenous JA reduced Tetranychus pacificus McGregor (Pacific spider mite) performance on grapevines (Omer et al., 2000) and T. urticae performance on tomato (Thaler et al., 2002c). MeJA reduced T. urticae preference for, and performance on Viola wittrockiana Gams and Impatiens walleriana Hook.f. (Rohwer and Erwin, unpublished). Other studies suggest varied, yet specific, responses to particular pests. Defence responses therefore seem to be specific and tightly controlled. A jasmonate-inducible metallopeptidase-like gene in Cucurbita pepo (SLW1) was induced by Bemisia argentifolii Bellows and Perring (silverleaf whitefly) nymphs, but not by B. argentifolii adults or B. tabaci Gennadius (sweetpotato whitefly; van de Ven et al., 2000). Even within a feeding guild, jasmonate responses may vary. As the feeding mechanisms of these insects are very similar, this response is probably a result of unique components in the saliva, or different concentrations of salivary constituents (Thompson and Goggin, 2006). There is also evidence for the involvement of jasmonates in resistance to root pests. Jasmonatedeficient A. thaliana were sensitive to fungus gnat (Bradysia impatiens) infestation (McConn et al., 1997), and fungus gnat survivorship was lower on MeJAtreated spinach compared to control-treated plants (Schmelz et al., 2002). The performance of Daktulosphaira vitifoliae Fitch (grape phylloxera) on grapevines was reduced by treating the plants with JA (Omer et al., 2000). Partial resistance to the avirulent nematode Meloidogyne javanica isolate VW4 was imparted to S. lycopersicum by treating the foliage with

PRACTICAL APPLICATIONS AND HORTICULTURAL RELEVANCE Use of other compounds for defence induction Commercial applications of materials that induce plant defences are just beginning to be appreciated as a means to reduce pest and disease infestation. Such compounds are often called plant activators. To our knowledge, all available products are activators of systemic acquired resistance (SAR) and are applied preventatively to control disease. SAR is a plant defence response that requires salicylic acid (SA) for withinplant defence activation against viruses and pathogens (Mtraux et al., 2002). The use of plant activators is not widespread in commercial horticulture. For instance, harpin protein, an activator of SAR (Dong et al., 1999), was applied commercially to 3% of the U.S. strawberry crop 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). Harpin alone, or in rotation with chemical fungicides, reduced the incidence and severity of disease in tomatoes in Florida, but acibenzolar-S-methyl benzothiadiazole; (BTH) provided better prevention (Pernezny et al., 2002). BTH is an analog of SA, and is another commercially available (Actigard or Blockade) inducer of SAR, labelled in the United States for preventative disease resistance in cole crops, tomatoes, leafy vegetables, and tobacco (Syngenta Crop Protection, Greensboro, NC, USA). BTH can also protect plants against some piercing-sucking insects, as seen 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 lesser extent in Bemisia argentifolii-tomato (Inbar et al., 1998) interactions. No effect, or variable effects of BTH were detected against Helicoverpa armigera on cotton plants (Inbar et al., 2001), but Liriomyza spp. (leafminer) preferred control tomato leaves over leaves treated with BTH (Inbar et al., 1998). Harpin is also being studied for induced insect defences. For instance, reduced feeding of the striped cucumber beetle [Acalymma vittatum (F.)] on Cucumis sativus L. was noted when insects were applied 7 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 harpin had a reduced rate of reproduction (Dong et al., 2004).

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Horticultural applications of jasmonates 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 the nicotine production rate increased in N. sylvestris after MeJA application, the production rate returned to the same as in untreated plants 6 d after elicitation. There was no ultimate difference in nicotine content between plants that were treated several times with MeJA, and plants that were treated once. However, prior elicitation of plants caused a more rapid accumulation of nicotine than in plants with no history of elicitation (Baldwin and Schmelz, 1996). This supports the theory that more rapid induction of defenses is a mechanism for enhanced resistance in MeJA-treated plants when jasmonatemediated defenses are subsequently elicited by a biotic or abiotic challenge. Priming plants, rather than inducing defenses directly, may incur fewer energy costs and result in similar benefits, as seen in the defense against pathogens in Arabidopsis (van Hulten et al., 2006). Some physiological responses to jasmonates are not directly defensive, but can also serve to defend plants indirectly. Jasmonate-treated plants have attracted predators or parasitoids in at least eight plant species (Table I). Jasmonate signalling within the plant is required to attract the parasitoid Cotesia rubecula Marshall to A. thaliana under attack by the herbivore Pieris rapae L. (van Poecke and Dicke, 2002). Similarly, S. lycopersicum infested with T. urticae, and defective in JA synthesis, failed to attract predatory mites (Phytoseiulus persimilis Athias-Henriot) or to emit predator-attractive volatiles to the same extent as wildtype plants (Ament et al., 2004). Parasitoids preferred A. thaliana plants treated with exogenous JA over untreated plants, 24 h after a JA treatment (van Poecke and Dicke, 2002). Hyposoter exiguae parasitoids were preferentially attracted to Spodoptera exigua Viereck caterpillars placed in a field of S. lycopersicum treated with JA, compared to caterpillars in plots of untreated plants (Thaler, 1999a). P. lunatus treated with 1.0 mM JA, but not 0.1 mM, attracted P. persimilis better than plants treated with water, but not as well as plants infested with prey (T. urticae; Dicke et al., 1999). Water-treated P. lunatus plants with T. urticae damage were less attractive to P. persimilis than 0.1 mM JA-treated plants damaged by T. urticae (Gols et al., 2003). Interestingly, JA-elicited volatiles from P. lunatus were similar to S. exigua-elicited volatiles, but applications of JA followed by methyl salicylate (MeSA) to plants were needed for terpenoid emissions similar to emissions from T. urticae-treated plants (Ozawa et al., 2000). An understanding of the role of jasmonates in tritrophic interactions may permit more effective use of natural enemies in horticultural crop production. Other unique means of jasmonate-induced tritrophic defence responses have been noted. Natural herbivory on Macaranga tanarius Mll. Arg. was reduced by the application of JA. Extrafloral nectaries, induced by JA, attracted beneficial insects to plants, with an associated reduction in herbivore numbers and damage (Arimura et 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 after jasmonate application were the primary attractants in predator or parasite-attracting olfactometer experiments.

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 of MeJA to the roots (Soriano et al., 2004a, b). Specialist and generalist herbivores typically behave differently on jasmonate-treated plants. This supports the theory that generalist herbivores are more strongly affected by host plant defences than specialist herbivores (Strauss and Zangerl, 2002). Two generalist lepidopteran herbivores (S. exigua and Trichoplusia ni Hbner) performed less well on JA-treated tomato than on untreated plants, but the results were somewhat variable and may depend on host genotype (Thaler et al., 1996; 1999; 2001; 2002b; c). Feeding of a specialist herbivore of solanaceous plants (Epilachna vigintioctopunctata) on tomato was unaffected by jasmonate treatment, but feeding was reduced on non-host brassicas such as Brassica rapa L. ssp. pekinensis and A. thaliana (Shinogi et al., 2005). The relative growth rate of another specialist lepidopteran (Manduca sexta L.) on tomato was unaffected by treating the plants with 1.5 mM JA (Thaler et al., 2002c). Conflicting results have been reported for this response (Iverson et al., 2001); but, in this case, 0.45 mM MeJA was used for elicitation of defenses and a different tomato cultivar was used. An undesirable effect of using jasmonate treatment to reduce generalist herbivore damage under field conditions might be the greater potential for proliferation, or at least minimal control of specialist herbivores (Cipollini et al., 2003). Exogenous jasmonates increased resistance to pests in Nicotiana species, including tobacco hornworm (Manduca sexta L.). The nicotine defence system of the host was effective and induction was measurable. Feeding by 2nd-instar tobacco hornworm larvae on N. tabacum leaf discs was reduced when whole plants were treated for 5 d with 0.5 l MeJA. Similar results were noticed when plants were grown free of MeJA for 6 d after treatment (Avdiushko et al., 1997). The growth and feeding of larvae fed on MeJA-treated leaves were also reduced. Hornworm egg hatching was not affected, but feeding of newly-hatched larvae was reduced (Avdiushko et al., 1997). Herbivore (Manduca quinquemaculata) oviposition on N. attenuata Torr ex. S. Watts was reduced when the plants were treated with MeJA, or when plants were under attack by caterpillars (Kessler and Baldwin, 2001). Both herbivory and florivory were reduced in N. attenuata treated with MeJA (McCall and Karban, 2006). Manduca sexta larvae grew more rapidly on lipoxygenase-impaired (and therefore jasmonate-deficient) N. attenuata compared to wild-type plants, and MeJA restored native defences (Kessler et al., 2004). Native herbivores also attacked jasmonatedeficient plants more than wild-type plants (Kessler et al., 2004). A correlative relationship between MeJA released from damaged sagebrush (A. tridentata Nutt.) and reduced feeding by grasshoppers on natural stands of neighbouring N. attenuata has been established (Karban et al., 2000), and may be a result of the emission of MeJA from the sagebrush (Farmer and Ryan, 1990). Recent results suggest that the enhanced resistance in the tobacco was not directly due to the immediate induction of defensive compounds, but rather to enhanced induction of defensive compounds once the Nicotiana was attacked (Kessler et al., 2006). In addition,

C. L. ROHWER and J. E. ERWIN Jasmonates can induce the emission of a myriad volatiles from plants, often similar to responses induced during herbivore feeding. The release of stored compounds and de novo synthesis of volatiles are probably both responsible 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 plants after exposure to 18 mol MeJA vapour for 18 h (Rodriguez-Saona et al., 2001). Volatile MeJA induced local, but not systemic, emission of monoterpenes and sesquiterpenes in Z. mays (Farag and Par, 2002). Interestingly, MeJA emission, following JA treatment, was noted in seven species representing the Dryopteridaceae (wood ferns), Ginkgoaceae, Solanaceae, Fabaceae, and Poaceae; but JA did not induce MeJA emission in four other species representing the Brassicaceae, Myrtaceae, Asteraceae, and Salicaceae (Boland et al., 1995). The basis for differences in the inducibility of MeJA emission was not addressed, but the ecological purpose of this response poses a fascinating question. In addition to their indirect effects, jasmonates may have direct effects on insect predators. MeJA and cis-jasmone attracted members of two families of insect parasitoids (Braconidae and Sarcophagidae) in hop (Humulus lupulus L.) cultivation (James, 2005). MeJA-baited traps attracted more Anagrus and Metaphycus parasitic wasps than untreated traps among grapevines (Vitis labrusca L.), but this study contradicted previous research and could have resulted from MeJA-elicited volatiles from the grapes (James et al., 2005). Interestingly, minimal induction of volatile emission 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 already lightly infested with T. urticae, but the mites were repelled from heavily infested plants. Predatory mites (P. persimilis) were only attracted to plants moderately or heavily infested with their prey (Horiuchi et al., 2003). Therefore, in horticultural situations, it may be important to fully induce volatile emissions to attract predators or parasitoids and to repel herbivores. The importance of jasmonate signalling in repelling herbivores through volatile emissions was recently demonstrated in tomato, using a jasmonate synthesis mutant. JA-deficient tomato plants showed reduced volatile emissions and corresponding enhanced preference by B. tabaci and M. sexta for oviposition (Snchez-Hernndez et al., 2006). Jasmonate-treated B. rapa were less attractive to the herbivorous insect Plutella xylostella L.; but jasmonate-treated B. oleracea L. var. capitata was more attractive to the herbivore (Lu et al., 2004). It is obviously undesirable to attract pests to crop plants, so further investigation seems necessary for specific host-herbivore interactions. Jasmonates have shown no direct activity against arthropods (Avdiushko et al., 1997). However, MeJA can inhibit spore germination and germ tube elongation in B. cinerea (Meir et al., 1998), but promote spore germination in Botrytis (Darras et al., 2005) or Pythium ultimum (Kozlowski et al., 1999). Jasmonates had no negative effect on spore germination or growth in Penicillium digitatum Wehmer (green mould; Droby

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et al., 1999), but MeJA (100 600 M) inhibited mycelial growth 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.) de Bary was either inhibited or promoted, depending on the growth medium, the concentration of MeJA and JA, and the isolate (Cohen et al., 1993). MeJA and JA inhibited zoospore discharge and germination in P. infestans, but enhanced germ tube formation directly from sporangia (Cohen et al., 1993). MeJA had no effect on mycelial growth in vitro in Pythium mastophorum Drechsler (Vijayan et al., 1998). Regardless of whether jasmonates act directly on pathogens or not, it is clear that there is jasmonate signalling in plant defences against pathogens (Table I). Phytoalexin production in response to jasmonates has been documented in many plants, including peanut [Arachis hypogaea (Chung et al., 2003)] and Mexican cypress [Cupressus lusitanica (Zhao et al., 2001; 2004)]; but it was not detected in S. lycopersicum, S. tuberosum (Cohen et al., 1993), or A. thaliana (Thomma et al., 1999b). Jasmonate-induced pathogen defences have potential for horticultural crop production (Pea-Corts et al., 2005). For example, jasmonate signalling is required for resistance to Pythium root diseases (Staswick et al., 1998; Vijayan et al., 1998) and to Plectosphaerella cucumerina (Thomma et al., 2000) in A. thaliana. Seedling diseases were reduced in Cucumis melo L. after gaseous or liquid MeJA seed treatment (Buzi et al., 2004a,b). MeJA-treated Picea abies (L.) H. Karst plants had more resin flow (a defensive response) than untreated trees, when both were subsequently inoculated with Ceratocystis polonica. In addition, lesion size was smaller in the MeJA-treated trees (Franceschi et al., 2002). The phenomenon of induced systemic resistance (ISR), where non-pathogenic rhizobacteria primed plants for systemic pathogen defence, required jasmonate and ethylene signalling (Pieterse et al., 1998; Pozo et al., 2005). The accumulated data from A. thaliana suggest that jasmonate and ethylene signalling are involved in, or are required for, defence against necrotrophic pathogens, and that the SA signalling pathway is involved in defence against biotrophic pathogens (Glazebrook, 2005; McDowell and Dangl, 2000; Thomma et al., 2001; van Poecke, 2007; Zimmerli et al., 2004). Of course, there are exceptions to this (Pozo et al., 2005; Thaler et al., 2004). In addition, induction of SAR can be antagonistic to jasmonate-induced defences against herbivores (Felton et al., 1999). Acetylsalicylic acid (ASA) inhibited JA synthesis (Pea-Corts et al., 1993); and SA or ASA inhibited JA-induced accumulation, activity, or gene expression of protease inhibitors (Doares et al., 1995; Stout et al., 1998). Since jasmonate- and SA-induced responses are often antagonistic, and some defence pathways are specific to jasmonate and ethylene signalling, or to SA signalling, jasmonate-induced defence against one pest or pathogen could make the plant more susceptible to another pest or pathogen (Kunkel and Brooks, 2002). For instance, MeJA enhanced resistance to Trichoplusia ni Hbner (cabbage looper) in A. thaliana, but also enhanced the growth of Pseudomonas syringae (Cui et al., 2005). On the other hand, a putative A. thaliana transporter of defensive terpenoids required SA, jasmonate, and ethylene

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Horticultural applications of jasmonates size) over 3 years in a tomato field (Thaler, 1999b). JA (0.5 1 mM) applied to flowering strawberry plants accelerated ripening and increased the total yield per plant by 26 37% (Yilmaz et al., 2003). Under moderate herbivory, in a natural ecosystem, MeJA-induction increased lifetime seed set and capsule number in N. attenuata. However, under low levels of herbivory, non-induced plants performed better than induced plants and, under high herbivory, there was no difference between MeJA-induced plants and non-induced plants (Baldwin, 1998). Soybean yield increased when the seeds were inoculated with Bradyrhizobium cultured with 50 M MeJA compared to inoculation with untreated Bradyrhizobium (Mabood et al., 2006). The number of pollen grains per flower in wild radish (Raphanus raphanistrum L.) was reduced by approx. 6% by JA application, and plants flowered approx. 2 d later than untreated plants (Agrawal et al., 1999). Pollen grain number per flower is unimportant in the production of a cut-flower crop, but pollen grain number per flower may be an important consideration in seed production and/or for fruit size. Fruit number per plant is unimportant in a potted geranium, but is critical in cucumber production. Research on specific crops will need to be conducted to determine the effects of JA on economically important attributes in food and ornamental plants. Generalising jasmonate-related responses important in plant-pest interactions can be misleading. The model systems most studied in this area are tomato, A. thaliana, and tobacco. Interactions of these plants with specific pests are distinct and should not be applied directly to the other species (Gatehouse, 2002). Each plant species has its own unique set of defences, and induction of defences should not be attributed unequivocally to jasmonates, nor should defence induction lead to the conclusion that the plants will be better defended against pests. Also, JA-induced defences, such as protease inhibitors (PI), may simply lead to the production of PI-resistant digestive enzymes in herbivores without affecting herbivore performance (Broadway, 1995; 2000). Pre- and post-harvest jasmonate applications Some research on horticultural uses of MeJA has focussed on pre-harvest and post-harvest treatments to protect against microbial development on harvested tissue. Pathogen growth on celery (Apium graveolens L.) and pepper (Capsicum annuum L.) was reduced by treatment with MeJA (Buta and Moline, 1998). MeJA vapour at 1 M was more effective than 10 M at reducing post-harvest decay in two strawberry (Fragaria ananassa Duch.) cultivars stored at 20C (Moline et al., 1997). Strawberries stored for 12 d at 7.5C had higher quality and were protected from decay by 100 mM MeJA vapour (Ayala-Zavala et al., 2005). MeJA vapour (100 M) also eliminated decay in raspberry (Rubus idaeus L.) fruit stored at 10C for 10 d (Wang, 2003). Dipping grapefruit (Citrus paradisi Macfad.) in 1 50 M MeJA reduced green mould (Penicillium) during storage (Droby et al., 1999). MeJA applied to cut pineapple (Ananas comosus Merr.) as a vapour or a dip reduced softening and microbiological load after 6 and 12 d storage (Martnez-Ferrer and Harper, 2005), respectively. Peach fruit treated with volatile MeJA showed slower decay and higher quality than untreated

signalling (Campbell et al., 2003). Responses to specific challenges obviously require the fine-tuning of hormone levels and responsiveness within the plant. Sequential or simultaneous activation of separate defence pathways may help us to understand how the pathways function. Exposing S. lycopersicum to MeJA gas for 4 h slightly reduced the relative growth rate of S. exigua on the plants relative to untreated plants, but this was not true when the plants were treated with SA before MeJA. This response was correlated with increased protease inhibitor activity (Stout et al., 1998). However, SA inhibition of jasmonate-induced defence against S. exigua was not detected when plants were treated with MeJA for 12 h instead of 4 h (Stout et al., 1998). The relative growth rate of S. exigua on tomato was reduced by JA treatment, but reduced to a lesser extent by simultaneous application of BTH and JA (Thaler et al., 1999). Accordingly, JA-induced PPO activity in tomato was reduced by simultaneous application of BTH (Thaler et al., 1999). BTH-treated S. lycopersicum leaves allowed a greater relative growth rate of Helicoverpa zea (Boddie) than control leaves, but the results were variable (Stout et al., 1999). In contrast, induction of SAR in A. thaliana by harpin can activate jasmonate- and SA-independent (but ethylenedependent) defences against aphids (M. persicae; Dong et al., 2004). SAR-inducing compounds had little effect on jasmonate-induced defences against nematodes in S. lycopersicum (Boughton et al., 2006). Simultaneous activation of SAR and ISR, which requires jasmonate signalling, protected A. thaliana from P. syringae in an additive manner (van Wees et al., 2000), but no additive effect was seen in tomato (Thaler et al., 2002b). There was no interactive effect of simultaneous application of BTH and JA to P. syringae pv. tomato on cultivated tomato (S. lycopersicum) or wild tomato [S. lycopersicum var cerasiforme (Dunal) Spooner, J. Anderson & R.K. Jansen]. Interestingly, neither JA, nor BTH enhanced resistance to P. syringae in the wild tomato (in fact, BTH enhanced susceptibility!), but resistance was enhanced in the cultivated variety (Thaler et al., 2002c). This illustrates, again, that extrapolating jasmonate responses from one plant to the entire plant kingdom is overreaching. The result of simultaneous perception of these two hormones may depend on their concentrations (Mur et al., 2006). Antagonism between JA and SA signalling in defence, as well as a requirement for both compounds in some responses, was recently reviewed (Beckers and Spoel, 2006; Pozo et al., 2005). In addition, reviews on the tripartite interactions of pathogens, herbivores, and plants, including molecular plant responses, were recently published (Rosts et al., 2003; Stout et al., 2006; Taylor et al., 2004). Much work, including field trials, on interactions between jasmonate- and SA-induced defences in horticulturally important crops is needed. For horticultural applications, it is often not necessary to consider plant fitness in an ecological sense, including fecundity or survivorship. However, the induction of defence responses may enhance resistances at a cost to yield. For instance, tomato fruit number, fruit weight, and seed number per plant were reduced after the application of 10 mM JA, but not 1 mM JA (Redman et al., 2001; Thaler et al., 1999). However, there was no effect of jasmonate sprays on fruit yield (number and

C. L. ROHWER and J. E. ERWIN fruit 8 d after treatment (Jin et al., 2006). Applying 200 600 M MeJA to cut roses (Rosa hybrida L.), through the pulsing solution, or as a spray, reduced the incidence and severity of Botrytis (Meir et al., 1998; 2005), and enhanced 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 other ornamental crops may also benefit from MeJA application pre- or post-harvest to block post-harvest Botrytis development. Care must be taken, however, as jasmonate-induced ethylene may reduce flower longevity in ethylene-sensitive species, as was shown for a Dendrobium hybrid and Petunia hybrida Hort. ex. Vilm. (Porat et al., 1993). In addition, another potential drawback is reduced volatile formation, which was noted in apples treated with MeJA after controlled atmosphere storage (Olas et al., 1992). However, MeJA-enhanced production of beneficial volatiles from plant tissue has been 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 physical induction of post-harvest disease resistance reveal that jasmonates have not garnered as much attention as other means of induced post-harvest defence (Gozzo, 2003; Terry and Joyce, 2004). Potential uses of MeJA in preventing chilling injury or post-harvest disorders have also been studied. MeJA applied as a dip ( 25 M) or gas ( 100 M) to avocado (Persea americana Mill.), grapefruit, or pepper fruit prior to chilling reduced chilling injury (Meir et al., 1996; Fung et al., 2004). Banana fruit stored for 1 week at 5C were protected from chilling injury by 1 mM n-propyl dihydrojasmonate (PDJ; Chaiprasart et al., 2002). MeJA reduced decay in three strawberry cultivars stored at 5C or 10C (Moline et al., 1997) and delayed chilling injury in zucchini squash (C. pepo) and cucumber fruit (Wang and Buta, 1994; 1999). MeJA reduced chilling injury and decay in papaya (Carica papaya L.) fruit and, in conjunction with modified atmosphere packaging (MAP), resulted in the least decay (Gonzlez-Aguilar et al., 2003). Chilling injury was reduced in two cultivars of guava (Psidium guajava L.) treated with MeJA, but quality maintenance was cultivar-specific (GonzlezAguilar et al., 2004). Peaches dipped in 1 mM MeJA had elevated polygalacturonase activity (Budde et al., 2005), which may reduce woolliness in cold-stored fruit (Budde et al., 2005; Ben-Arie and Sonego, 1980). MeJA applied as a dip or a gas at 100 M inhibited root and shoot growth of harvested, topped radish (Raphanus sativus L.; Wang, 1998). MeJA applied as a gas (0.01 mM) reduced chilling injury and decay in tomato fruit stored at 5C for 2 4 weeks, enhanced the uniformity of ripening, and delayed ripening (Ding et al., 2001; 2002). A dip in PDJ slowed 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 volatile MeJA enhanced the soluble sugar content and slowed the loss of organic acids in raspberries after storage (Wang, 2003). Therefore, MeJA can positively modify post-harvest physiology for horticultural gain in a number of crops. Jasmonates may enhance the harvestability of fruits.

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Reducing the force required to detach Hamlin orange [Citrus sinensis (L.) Osb.] fruit from trees was accomplished with < 10 mM MeJA as a spray, but MeJA caused undesirable leaf abscission (Hartmond et al., 2000). MeJA applied to Valencia orange at 15 mM caused less leaf abscission than a mix of ethephon (2-chloro-2-ethyl-phosphonic acid) and 1-MCP (an anti-ethylene agent), while reducing the fruit detachment force to levels equal to ethephon-treated plants (Pozo et al., 2004). MeJA (1 mM) also increased abscission in harvested cherry tomatoes (Beno-Moualem et al., 2004), which is undesirable in such fruits, marketed attached to the peduncle. These results were, at least in part, a result of MeJA-enhanced ethylene production, but ethylene-independent abscission can not be ruled-out (Beno-Moualem et al., 2004; Hartmond et al., 2000; Miyamoto et al., 1997). Enhancing crop quality for human utility There are other unique, potential uses for MeJA in horticultural applications to enhance food quality. MeJA enhanced resveratrol accumulation in Vitis vinifera L. leaves (Belhadj et al., 2006), and resveratrol has benefits for human health (Opie and Lecour, 2007). Jasmonates also increased the glucosinolate content of cruciferous vegetables such as Brassica napus, B. rapa, B. juncea, and Raphanus raphanistrum (Agrawal et al., 1999; Bodnaryk, 1994; Doughty et al., 1995). Glucosinolates are precursors of isothiocyanates, which act as chemopreventative agents (Hecht, 1999). Similarly, it may be possible to enhance the anthocyanin contents of fruits and vegetables (Table I). V. vinifera cell cultures showed enhanced anthocyanin accumulation when treated with jasmonates (Curtin et al., 2003; Zhang et al., 2002), and MeJA increased the anthocyanin (Rudell et al., 2002) and carotenoid (Prez et al., 1993) contents of apple fruit and the anthocyanin content of A. thaliana (Jung, 2004). Raspberry (Rubus idaeus) fruit treated with 100 M MeJA vapour and stored at 10C were darker and more red in colour than untreated fruit, presumably due to elevated anthocyanin contents (Wang, 2003). Pre-harvest treatment of young R. idaeus and R. occidentalis L. fruits with 0.01 mM or 0.1 mM MeJA enhanced anthocyanin, phenolic, anti-oxidant, and flavonoid contents (Wang and Zheng, 2005). This was also shown by the fact that MeJA-treated raspberries had a greater oxygen radical absorbance capacity (ORAC) than untreated raspberries after 10 d in storage (Wang, 2003). MeJA-treated strawberry fruit also had greater anthocyanin and phenolic contents, and greater ORAC after 12 d storage (Ayala-Zavala et al., 2005). However, a conflicting report showed that MeJA inhibited anthocyanin accumulation in apple (Saniewski et al., 1988). Some glucosinolates and anthocyanins have chemopreventative or other healthrelated properties (Wattenberg, 1985), so jasmonates may increase the healthfulness of treated products. Other health-giving properties of plants may be affected by jasmonates. Leaves of drought-stressed strawberry have lower than normal levels of ascorbic acid [vitamin C, a powerful anti-oxidant in the human diet (Byers and Perry, 1992; Wang, 1999)]. However, treating strawberry plants with 0.1 mM MeJA, prior to drought stress, maintained their ascorbic acid levels (Wang, 1999). Drought-resistant corn seedlings had

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Horticultural applications of jasmonates firmness. Enhanced and uniform colour in ornamental and food crops may add to their economic value, and jasmonates may be useful to this end. Jasmonates in abiotic stress responses Physiological stress responses in growing plants may be modified by jasmonates. JA and JA-induced protein levels in barley leaf segments were enhanced by osmotic stress via sorbitol treatment (Kramell et al., 1995; Lehmann et al., 1995). Jasmonates play a role in water stress through their effects on stomatal apertures. Stomatal closure is regulated or enhanced by jasmonates (Pospilov, 2003; Table I). Sensitivity to both jasmonates and ABA was required for the full stomatal closure response in Arabidopsis (Suhita et al., 2004). Levels of the osmoprotectant, glycine betaine, increased as the JA content in grafted Pyrus bretschneideri Redh. increased in response to exogenous JA application (Gao et al., 2004). There is strong evidence for the interaction of jasmonates and ABA in water-stress signalling, but the utility of jasmonates in preventing stress is unclear. Would treating transplants in plug trays, or bareroot transplants, with JA reduce dessiccation stress during shipping or storage? Would JA treatment increase salt tolerance? Treating barley with 25 M JA prevented the stress caused to photosynthetic systems after transfer to 100 mM NaCl (Tsonev et al., 1998). MeJA (10 M) reduced photosynthesis in Pisum sativum, but moderated NaCl-induced declines in photosynthesis and RuBisCO enzyme activity and NaCl-induced increases in photorespiration, CO2 compensation point, and respiration (Fedina and Tsonev, 1997; Velitchkova and Fedina, 1998). The effects of water stress in strawberry (Fragaria vesca), including elevated levels of oxidative stress, were reduced when plants were treated with MeJA (Wang, 1999). Hordeum vulgare roots treated with 5 M JA for 24 h, then osmotically stressed, had less membrane damage than stressed roots not treated with JA (Bandurska and Stroiski, 2001). These data suggest that pre-treating plants, before transplanting into saline soil or media, or before prolonged drought, may allow them to be productive in soils with high salts or when under drought stress. Jasmonates also play a role in reducing ozone stress responses. Exogenously applied jasmonates protected A. thaliana (Overmyer et al., 2000; Rao et al., 2000) and N. tabacum (rvar et al., 1997) from ozone-induced hypersensitive cell death, which was probably the result of attenuated SA-mediated hypersensitivity. A hybrid poplar (Populus maximowiczii Henry P. trichocarpa Torr & A.Gray), tolerant of ozone damage, was less damaged by ozone when treated with jasmonates 3 24 h before ozone treatment (Koch et al., 2000). Similar to salt stress, jasmonates may be useful in protecting plants prior to transplantation into high-ozone areas.

higher ascorbic acid levels after a 2 d drought stress if the seeds were treated with 112 M MeJA (Li et al., 1998). A. thaliana cell cultures treated for 21 h with 50 M MeJA had 64% more ascorbic acid than untreated cells, but cell growth (and ascorbic acid levels) depended on the presence of auxin and cytokinin (Wolucka et al., 2005). However, the total carotenoid contents of S. lycopersicum and S. tuberosum decreased after treatment with a high concentration (> 4 mM) of MeJA as a spray (Cohen et al., 1993), and 10 mM MeJA reduced the 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 tomato fruit, but raised -carotene levels (Saniewski and Czapski, 1983; Czapski and Saniewski, 1985). This was supported by research suggesting that reduced endogenous levels of jasmonates in tomato fruit at the later stages of ripening are needed to permit lycopene synthesis (Fan et al., 1998a). Further research in this area is necessary to study the specific effects of MeJA on healthful compounds in foods. The pharmaceutical content of plants may be enhanced by jasmonates (Zhao et al ., 2005). Potentially medically-useful saponins were induced by jasmonates in Glycyrrhiza glabra L. (Hayashi et al., 2003), Panax ginseng C.A.Mey. (Lu et al., 2001), and Bupleurum falcatum Dalzell and Gibs. (Aoyagi et al., 2001) cell cultures. Taxol (paclitaxel) from Taxus chinensis cell cultures is a useful metabolite that is induced by MeJA (Wang and Wu, 2005; Wu and Lin, 2003). Alkaloids were induced by MeJA in Catharanthus 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 by jasmonates (Zhao et al ., 2001; 2004). A podophyllotoxin derivative is used in cancer treatment, and podophyllotoxin is inducible in in vitro cultures of Linum album (van Frden et al., 2005). It may be profitable to enhance pharmaceutical production by plants through the elicitation of secondary metabolite production using jasmonates. Anthocyanins are not just healthful, they add colour to ornamental plants and food. Enhancing anthocyanin accumulation for aesthetic purposes may be useful in greenhouse-grown ornamental crops, where the absence of natural ultraviolet light and high temperature may limit anthocyanin production. Examples of crops in which anthocyanins are an important part of plant appearance 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 detached petunia (Petunia hybrida) corollas (Tamari et al., 1995). Colour is also an important quality attribute in produce. MeJA vapour (8.3 mg fruit1) or spray (10 mM) or JA spray (1 10 mM) promoted degreening and intensified the colour of Golden Delicious or Fuji apples (Fan et al., 1998b). Mango degreening was also enhanced by 104 M MeJA vapour (Lalel et al., 2003). Peach fruit were more red than control fruit when the trees were sprayed six times with 10 mM MeJA (Janoudi and Flore, 2003), although MeJA also reduced fruit

SUMMARY AND FUTURE DIRECTIONS As biological control becomes more prevalent, useful, and important in horticultural crop production, targeted use of jasmonate-induced defences may provide valuable augmentation of integrated pest management strategies. For example, jasmonates may be used to treat localised infestations where a pest threshold is exceeded, with the

C. L. ROHWER and J. E. ERWIN goal of attracting pre-released predators or parasitoids to that area. In a greenhouse, it may be possible to use a combination of treating ornamentals with jasmonates, and growing trap crops (plants naturally attractive to pests) nearby, to reduce the pest pressure on the ornamentals through: (i) attraction of beneficials to the ornamentals, (ii) induction of chemical defences in the ornamentals, and (iii) accumulation of pests on the trap crops. Further research in this area is necessary before any of these unique strategies become feasible as control strategies. It is also crucial to recognise that the horticultural utility of JA-induced defence is highest when economic thresholds are high and when pest proliferation may be predicted (Stout et al., 2002). In addition to the role of jasmonates in protecting growing plants from herbivorous arthropods, jasmonates have a clear record of protecting ornamental and food crops from post-harvest disorders and diseases. Jasmonates also may enhance aspects of plant quality, or be useful in propagation. However regulatory approval of jasmonates or their analogues is necessary before many of these applications can be used commercially. Research comparing the efficacy of various application methods of jasmonates and their analogues (e.g., MeJA as a gas or spray? Coronatine sprays? Dihydrojasmonic acid sprays?) needs to continue. It is clear that controlled application of MeJA as a gas can

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elicit jasmonate responses in plants. It may be possible that treating plants with volatile MeJA in a cooler, shipping truck, box, or greenhouse may elicit beneficial jasmonate responses. Results from early work on jasmonate-induced defence responses suggest that some plants 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. They are involved in complex, yet specific, interactions between plants and pests, and between plants and pathogens. Jasmonates are involved in tritrophic interactions between plants, pests, and predators of those pests. The web of interactions linking jasmonate responses with other hormone signalling pathways is becoming clearer. Jasmonates can alter physiological processes in plants, to make plants more valuable to humans, or more easily propagated. Much jasmonate research, compared to work on other plant hormones, is in its infancy, but continued research into many varied aspects of horticultural science is important. Such work will undoubtedly result in useful applications of jasmonates for horticultural crop production. References to commercial products are not intended to be endorsements of the product to the exclusion of other products.

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