Stewart Postharvest Review An international journal for reviews in postharvest biology and technology

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Prospects for cut-flower postharvest disease management with host defence elicitors Son-Quang Dinh and Daryl C Joyce* Centre for Native Floriculture, School of Land, Crop and Food Sciences, The University of Queensland, Australia

Abstract Purpose of the review: There is increasing public awareness of socio-environmental risks in using synthetic fungicides. This imperative drives a move to seek more generally acceptable alternatives to protect cut-flowers and other fresh produce from pathogens. In the context of postharvest management of cut-flowers, this paper considers natural disease resistance (NDR) and its potential activation with environmentally sound chemical elicitors. Main findings: Plant NDR mechanisms are comprised of constitutive and induced defences. Induced defences involve the hyper-sensitive response, local and systemic acquired resistance, and induced systemic resistance. The various systemic resistance defence mechanisms differ in their natural elicitors, signalling pathways, and resultant defence compounds (eg, pathogenesis-related pro-teins). A range of exogenous biotic and abiotic agents can be used as elicitors to either prime (potentiate) or activate (elicit) NDR. Understanding the molecular, biochemical and physiological mechanisms involved in elicitation of NDR provides a basis for practi-cal utilisation of this approach in both pre- and postharvest disease management. However, for the most part, basic studies are car-ried out on model or immature plants (eg, Arabidopsis) grown in controlled environments. The cut-flowers of commerce are diverse in both botanical structure and physiological changes during postharvest handling. Nonetheless, most are generally highly perish-able, with many being vulnerable to pathogen attack. The polyphagus fungus Botrytis cinerea (Botrytis) is the single most impor-tant cut-flower pathogen. The diseases and symptoms it causes include petal specking, flower blight, and accelerated (ethylene-mediated) abscission. Exogenous treatments with host defence elicitors, such as methyl jasmonate and benzothiadiazole, potentially could suppress fungi infecting cut-flowers. However, their efficacy has proven limited in applied experimentation conducted to date. If elicitors of natural defence mechanisms are to find practical application in postharvest disease management for cut-flowers, then substantial research effort will be required to understand how production practices and conditions (eg, climate, nutrition, pest and disease pressures) and postharvest management practices (eg, temperature management) influence the ability of host plant tis-sues to respond. In the medium to long term, it is probable that elicitation of natural defence against pathogens, like Botrytis, will find a place within integrated pre- and postharvest disease management programs (IDM) for cut-flowers and other ornamentals. Direction for future research: Detailed molecular, biochemical and physiological studies on specific cut-flower pathosystems are needed, in the context of postharvest horticulture, to gain an understanding of the complex nature, magnitude and timing of host defence responses to elicitor treatments. Also, the possibility of priming, particularly preharvest, for enhancement of subse-quent elicitation of induced resistance merits attention. Finally, research is warranted into the prospects for integration of elicita-tion of natural defence into IDM packages for cut-flowers. Keywords: Botrytis; carnation; ethylene; freesia; Geraldton waxflower; rose; rhizobacteria

*Correspondence to: Daryl C Joyce, Centre for Native Floriculture, School of Land, Crop and Food Sciences, The University of Queensland, Gatton QLD 4343, Australia. Tel: +61 07 5460 1725; Fax: +61 07 5460 1112; email: d.joyce@uq.edu.au Stewart Postharvest Review 2007, 2:4 Published online 01 April 2007 doi: 10.2212/spr.2007.2.4

Abbreviations

BTH Benzothiadiazole [or Acibenzolar-S-methyl (ASM)] ET Ethylene HR Hypersensitive Response IDM Integrated Disease Management INA 2, 6-Dichloroisonicotinic Acid ISR Induced Systemic Resistance JA Jasmonic Acid

1-MCP 1-Methylcyclopropene

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Introduction Cut-flowers and ornamental plants constitute natural ‘living beauty’ that enriches the quality of human life. Moreover, the cut-flower and foliage sector represents an extremely impor-tant economic grouping within the ornamental horticulture industry [1, 2]. Not only is there high financial benefit at the farmgate level, but there is significant value-adding in opera-tions like the bunching of bouquets. Cut-flowers are gener-ally comprised of multiple organs, with stems typically bear-ing leaves and generally highly perishable floral structures. There is profound variation in inflorescence structure and individual blooms [3]. Flower development is often initiated by plant sensitivity to varying temperature or photoperiod, followed by bud growth until flower opening, pollination and, finally, senescence. Respiration and ethylene (ET) pro-duction during cut-flower senescence vary among genotypes from typically climacteric (eg, some carnation cultivars) to non-climacteric (eg, certain rose cultivars) [3]. The global cut-flower trade relies heavily on low temperature, high hu-midity handling to retard flower senescence. However, while such conditions effectively slow flower development and senescence, they may favour fungal pathogens like Botrytis cinerea. Botrytis infection usually occurs in the field, and the infection develops after harvest to adversely affect appear-ance and enhance senescence. Increasing worldwide demand for high quality floricultural produce requires due attention by industry to postharvest disease management. However, the use of synthetic fungicides is becoming increasingly prob-lematical. Their overuse has led to proliferation of fungicide resistance within pathogen populations. Also, they are be-coming more unacceptable in a socio-environmental context due to attendant human and environmental health risks. The pre- or postharvest use of safe chemical, biological or physi-cal treatments to elicit host defence against cut-flower patho-gens is a seemingly sound alternative approach for use in disease management programs by industry. This review con-siders chemical elicitation of natural disease resistance (NDR) in the context of disease management for cut-flowers.

Major diseases Only a few bacteria (eg, Xanthomonas and Erwinia) are ma-jor pathogens of ornamental crops [4–6]. However, ornamen-tals are afflicted, both pre- and postharvest, by many disease-causing fungi. Pot and field grown plants are attacked by both necrotrophic fungi (eg, Botrytis, Alternaria, Colleto-trichum) and biotrophic fungi that cause diseases such as downy (eg, Peronospora) and powdery (eg, Erysiphe) mil-dew. Fungal pathogens cause root rot (eg, Phytophthora, Pythium and Rhizoctonia [7*, 8]), wilt (eg, Fusarium [8]), and leaf and petal spot (specking) and flower blight (eg, Al-ternaria, Botrytis [4, 9**]). The most problematical posthar-vest pathogen to the cut-flower industry is B. cinerea [10*]. Alternaria alternata is another pathogen that infects har-vested cut-flowers [11*]. Grey mould (Botrytis blight) B. cinerea is a widespread necrotising fungus that infects more than 200 plant species. It causes leaf and fruit rot and flower blight on many horticultural products, both in the field and postharvest [12*, 13**, 14*, 15*]. B. cinerea is also a common saprotroph on all manner of damp plant materials. It colonises senescent or dead flower petal, anther or stigma tissues [12*]. Botrytis is particularly problematical during wet weather, when it readily infects a wide variety of orna-mentals (eg, chrysanthemum, freesia, gerbera, pelargonium, rose, ruscus and waxflower [12*, 15*, 16*, 17, 18]). In the field, conidial liberation can be by insect or splash dispersal [19, 20]. Air borne conidia are, however, considered most important for Botrytis dispersal [21*]. B. cinerea conidia germinate well on host surfaces under favourable tempera-tures of 22–25oC and at high relative humidities of 90–100%. Free water, including as condensate, is probably a pre-requisite for germination. Germ tubes then elongate and may branch. Botrytis can exist saprophytically, as hyphae, on the host surface before infection. B. cinerea hyphae were visible on the styles of harvested Geraldton waxflower flowers within 4 days of inoculation [22*]. The distal end of germ tubes can directly penetrate healthy tissues, including rose, gerbera and freesia petals [15*, 16*, 23*]. This polyphagous fungus is among species that may directly penetrate the ovary wall, as well as entering via the stigma-style pathway [10*]. Appressoria can form at hyphal germ tube tips [24]. Most Botrytis infection occurs preharvest during flower growth and development, especially if free water is present. The in-fection can become quiescent and remain inactive in the symptomless host [25*]. Limited infections may persist until postharvest changes in flower physiology and environmental conditions reactivate pathogenicity. This latent pattern of Botrytis disease development has been observed in rose [14*] and Geraldton waxflower [22*]. Limited lesions are fre-quently seen on petals of gerbera [15*] and freesia [16*]. B. cinerea can maintain active growth at temperatures lower than 5oC [26]. Also, prolific sporulation may occur during postharvest storage and contribute new inoculum to infect healthy flowers [12*]. In cut Geraldton waxflower flowers, favourable storage conditions result in visible infection and

LAR Local Acquired Resistance MeJA Methyl Jasmonate NDR Natural Disease Resistance PAL Phenylalanine Ammonia-lyase

PR Pathogenesis-related SA Salicylic Acid SAR Systemic Acquired Resistance

UV-C Ultraviolet-C

STS Silver Thiosulphate

PGPR Plant Growth Promoting Rhizobacteria

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sporulation within 2–4 days after inoculation [22*]. Early signs of waxflower colonisation are tan necrotic lesions at the base of petals. Thereafter, the pathogen produces superficial grey fungal mycelium [12*]. For waxflower flowers incu-bated at 20oC and >95% relative humidity, Botrytis-related flower fall from harvested stems started at around 4 days after inoculation [22*, 27**]. Induced defence in natural disease resistance Recognition of pathogen infection and signal transduction Induction of defence reactions in a plant depends on recogni-tion of the pathogen by the host. Recognition occurs via a system of pathogen-derived elicitors, host plant receptors, and signal transduction pathways that lead to production of defence compounds [28]. Defence mobilisation is, therefore, based on binding of elicitors to receptors during an incom-patible host-pathogen interaction [29]. Messengers can be transmitted intra- or intercellularly to activate genes to pro-duce the defence compound(s) that include antifungal chemi-cals (eg, phenolics) and enzymes (eg, some pathogenesis-related [PR] proteins) [28]. Endogenous transducers include protein kinases, calcium ions, phospholipases, and hydrogen peroxide. Specific systemic resistance signalling molecules include salicylic acid (SA), jasmonic acid (JA), and ET. In addition to natural defence processes per se, exogenous treat-ments with both natural and synthetic substances [eg, 2,6-dichloroisonicotinic acid (INA)] can activate defence signal-ling pathways [30]. Hypersensitive response The hypersensitive response (HR) is a rapid plant response that results in localised cell death [31, 32]. The incompatible interaction of a specific host-pathogen combination leads to failure of the pathogen to infect or colonise the host. The HR is not always visible due to involvement of only a single or a few cells. It effectively isolates the pathogen in the dead area. Recognition of elicitors activates a cascade of cellular HR reactions at the attack site. These reactions result in accumu-lation of reactive oxygen species (ROS; eg, superoxide, hy-drogen peroxide, hydroxyl radicals) around the infection site. This rapid oxidative burst can effectively arrest pathogen growth [33]. Local acquired resistance HR reactions lead to activation of host defence responses in neighbouring cells, or local acquired resistance (LAR) [32]. LAR is characterised by elevated levels of antifungal com-pounds and defence enzymes. Like the HR, LAR is effective against a broad range of pathogens. Secondary metabolites, such as phenolics, phytoalexins and lignin-based polymers [34], can rapidly accumulate in a host’s response to infection by a pathogen. Increased chloro-genic acid, a simple phenolic compound, was found in potato tubers treated with arachidonic acid, an elicitor of HR [35].

Phenolic compounds play a role in disease resistance of kiwi-fruit leaves against B. cinerea [36]. Phytoalexins are produced de novo and accumulate to toxic levels that provide host resis-tance in healthy cells adjacent to fungal infected cells [37]. Phytoalexins inhibit germ tube elongation and host tissue colo-nisation by disrupting fungal cell membranes, thereby destroy-ing cellular integrity [38]. Grayer and Harborne [39] reviewed antifungal compounds in higher plants and listed phytoalexins characterised in 31 families of flowering plants. PR proteins are structurally diverse plant proteins induced either under pathogen stress or other biotic or abiotic stress situations. Transcription of genes that code for PR proteins depends on signal compounds, such as SA, xylanase (enzyme), ET, systemin (a polypeptide), and JA [40]. PR proteins may either have direct antifungal activity or be in-volved in indirect host defence mechanisms, such as strength-ening host cell walls or the pathogen recognition process. They were first observed in Tomato Mosaic Virus-infected tobacco [41]. At least 14 different families of PR proteins have been recognised [42]. PR-1 (antioomycete and antifun-gal) is an abundant PR protein. Trace amounts of PR proteins appear in healthy plants. However, accumulation takes place following elicitor treatment, pathogen attack or under other stress conditions [30]. Alexander et al. [43] reported a 10,000-fold increase in PR-1 levels in tobacco tissue upon infection by oomycete pathogens. This level of accumulation equated to 1-2% of the total leaf protein. Other well known PR protein families include PR-2 (β-1,3-glucanases), PR-3 (chitinases), PR-4 (antifungal), PR-5 (thaumatin-like), PR-6 (proteinase inhibitors) and PR-9 (peroxidases). SA (2-hydroxybenzoic acid) is a plant phenolic compound that accumulates at pathogen-induced necrosis sites on in-fected leaves and also in phloem fluid and distal healthy leaves [30, 44]. SA accumulation leads to elevated levels of endogenous hydrogen peroxide, that, in turn, acts as a second messenger to switch on defence gene expression [45]. Plants (eg, tobacco, Arabidopsis) transformed with the nahG gene, which encodes the SA-degrading enzyme salicylate hydroxy-lase, weakly accumulated SA. The reduction in accumulation resulted in blocking of both localised and systemic acquired resistance. Thus, SA is required for LAR expression [32]. JA occurs naturally in plants and has been implicated in the octadecanoid signalling pathway of plant responses. JA, and its derivative methyl jasmonate (MeJA), trigger responses that allow cells to cope with pathogens and some other exter-nal stimuli [46]. Developing tissues, such as flowers or the pericarps of reproductive structures, normally contain high levels of JA. Lower levels of JA are found in roots and ma-ture leaves. Endogenous JA levels were elevated in Arabi-dopsis in response to a challenge inoculation with A. brassi-cicola [47]. JA modulates the expression of genes encoding defence-related antifungal proteins [48], cell wall proteins [49], phytoalexins [49, 50] and phenolics [51].

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Systemic acquired resistance Induced resistance in plants is generally systemic. Thus, de-fence responses to pathogenic infection occur not only at the initial infection site, but also in spatially separated tissues. Systemic acquired resistance (SAR) helps plants tolerate sub-sequent infections. For example, Cameron et al. [52] found that 2 days after inoculating avirulent Pseudomonas syringae pv. tomato onto a single leaf of Arabidopsis thaliana, resis-tance developed in other leaves upon challenge with avirulent P. syringae pv. maculicola. SAR confers potentially long-lasting and effective resistance against a broad range of pathogens and parasites, and is found across a wide range of plant species [53]. SAR is similar to LAR in conferring broad-spectrum resistance. However, the enhanced defence capacity in SAR is mediated by a systemic signal which is not necessary in LAR [53]. SA is a key signal compound in the SAR response to patho-gen infection. Lipid-based molecules are also suggested to be mobile signals in SAR [54]. A study on tobacco suggested that SA can bind with enzymes (eg, catalase). In turn, SA-binding proteins may mediate lipid peroxidation [44]. Peroxi-dation products are involved in activating SAR genes [55]. An important component of SA signal transduction identified in Arabidopsis is the NPR1 protein [56]. This protein posi-tively regulates defence gene expression to activate SAR by moving to the nucleus and interacting with basic leucine zip-per transcription factors [57]. Induced systemic resistance Induced systemic resistance (ISR) is induced by certain non-

pathogenic, root-colonising, plant growth promoting rhizo-bacteria (PGPR) [58]. Most ISR studies have been conducted with fluorescent Pseudomonas species. After colonisation of carnation by the PGPR P. fluorescens WCS417 strain, plants developed induced defence against Fusarium oxysporum f.sp. dianthi [59]. PGPR-induced ISR is similar to necrotising pathogen-induced SAR in that resistance towards a broad range of diseases is enhanced systemically in distant, unin-fected plant parts. However, the specific pathogens effec-tively suppressed by ISR differ from those suppressed by SAR. Ton et al. [60] used an Arabidopsis-pathosystem to demonstrate that SAR was more effective than ISR against the biotroph Peronospora parasitica. On the other hand, ISR protected the plant from the necrotroph A. brassicicola, but SAR did not. Interaction between defence signalling pathways Various studies have documented crosstalk among plant de-fence signal networks involving SA, JA and ET signalling molecules [61–63]. These signal molecules are pivotally im-portant in systemic resistance in plant-pathosystems and may interact either synergistically or antagonistically. SA is essen-tial in pathogen defence signalling pathway-induced expres-sion of acidic PR protein genes [64]. In contrast, JA is re-sponsible for inducing expression of basic PR proteins [64]. Combined MeJA and SA treatments of tobacco resulted in greater induction of PR1b expression than did treatment with SA alone [48]. SA-dependent PR1 expression is elevated by ET [65]. MeJA-induced defence responses are also mediated by ET [66]. Antagonism between SA and JA/ET has been reported by Heil and Bostock [67], Kunkel and Brooks [68]

Host Elicitors Target pathogen Treatment timing Reference

Rose (Rosa hybrida) Gibberellic acid B. cinerea Postharvest [109**]

Methyl jasmonate B. cinerea Postharvest [99**,100**]

Benzothiadiazole Diplocarpon rosae Preharvest [95*]

Geraldton waxflower (Chamelaucium uncinatum)

Salicylic acid Alternaria sp.; Epicoccum sp.

Preharvest [82*]

Methyl jasmonate B. cinerea Postharvest [101**]

Freesia (Freesia hybrida) Methyl jasmonate B. cinerea Postharvest [13**]

Methyl jasmonate B. cinerea Preharvest [9**]

Benzothiadiazole B. cinerea Preharvest [9**]

Sunflower (Helianthus annuus) Benzothiadiazole, methyl jas-monate, salicylic acid, 2,6-dichloroisonicotinic acid

B. cinerea Preharvest [145*]

Petunia (Petunia x hybrida) Benzothiadiazole Phytophthora infestans Preharvest [7*]

Cyclamen (Cyclamen persicum) Benzothiadiazole Fusarium oxysporum f. sp. cyclaminis

Preharvest [146*]

Table 1. Examples of (probable) chemical elicitation of NDR against pre- and postharvest pathogens of floricultural species.

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and Glazebrook et al. [69]. In tobacco, exogenously supplied JA inhibited expression of SA-mediated acidic PR genes, and SA treatment inhibited expression of JA-mediated basic PR genes [64]. Combined treatment of Arabidopsis with SA and JA blocked expression of JA-responsive genes [70]. A dual role has been suggested for SA. The first role is to enhance expression of synergistically induced JA/ET-dependent genes. The second is to repress solely JA-induced genes [67, 71, 72]. The complex crosstalk between defence pathways involving SA, JA, ET and other signalling molecules (eg, nitric oxide; [73]) in signalling pathways requires further elucidation. Elicitor-induced resistance With increasing demand for alternatives to the use of conven-tional fungicides in postharvest horticulture, induced resis-tance is seen as a promising practical approach for disease management [74*]. Three categories of elicitors have demon-strated potential for postharvest disease management on fruits and vegetables. These categories are chemical (eg, SA), physical (eg, ultraviolet-C [UV-C] at 190–280 nm) and bio-logical (eg, the yeast Candida saitoana). The present review is focussed on natural and synthetic chemical elicitors (viz., SA, benzothiadiazole [BTH or acibenzolar-S-methyl – ASM], JA and MeJA) that have been trialled for cut-flowers and ornamentals (Table 1). Salicylic acid SA is a key compound in LAR and SAR expression. SA was first found to effectively induce resistance against TMV in tobacco. When a 0.2% solution of SA was injected into to-bacco leaves whose upper surface was inoculated with TMV 4 days later, the number of lesions decreased by over 90% as compared with the control [75]. Many subsequent studies have confirmed that SA has an important function in mediat-ing induced resistance [76–78]. Exogenous application of SA has reduced fungal disease severity in fruits; eg, B. cinerea on kiwifruit and C. gloeosporioides on mango [79, 80]. SA treatment of sweet cherry fruit enhanced levels of the de-fence-related enzymes β-1,3-glucanase, phenylalanine am-monia-lyase (PAL) and peroxidase [81]. A preharvest SA spray (2,000 µg/mL) onto Geraldton waxflower cv. CWA Pink plants reportedly reduced flower disease incidence caused by Alternaria sp. and Epicoccum sp. [82*]. However, SA treatment did not suppress postharvest B. cinerea infec-tion on flowers of this cultivar. While SA can induce resis-tance [32], it can also be directly toxic to pathogens. Direct toxicity has been shown against Cladosporium cladosporioides and B. cinerea [79, 82*, 83*]. Moreover, phytotoxicity may occur to treated host plants, as has been reported for both kiwifruit and Geraldton waxflower leaves [82*, 84]. Benzothiadiazole BTH (or ASM) is a functional analogue of SA. BTH was first released for commercial use in Germany in 1996 under the trade name ‘Bion’ [85]. BTH was not fungitoxic in vitro and activated SAR in many plant species against a broad range of

pathogens [86]. BTH can be applied as either a foliar spray or a soil drench [87], as well as a seed treatment [88]. These methods of application can all provide high level host plant protection against pathogens. Field treatment of grapevines with BTH (0.3 mM) reduced postharvest Botrytis disease on bunches via induction of SAR [89]. In peach fruit, a 5 min. postharvest dip in 200 mg/L BTH solution enhanced activi-ties of ß-1,3-glucanase and chitinase, the levels of phenolic compounds and also lignin content [90]. These effects re-sulted in resistance of the fruit to infection by Penicillium expansum. Similarly, infiltration of pear fruit with BTH sig-nificantly enhanced activities of the defence enzymes peroxi-dase, PAL and chitinase [91]. However, BTH is not effective in all host-pathosystems. Cucumber leaves infiltrated with BTH did not show defence against Sphaerotheca fuliginea [92]. Similarly, BTH was ineffective against Ralstonia so-lanacearum on the susceptible tomato cultivars Equinox and FL47 [93]. However, resistance was greatly increased in the moderately resistant cultivars Neptune and BHN466. BTH treatments (2.86 mM or 1.43 mM, respectively) of freesia cvs. Cote d’Azur and Dukaat before harvest suppressed B. cinerea infection of the cut-flowers during postharvest incu-bation at temperatures of 5, 12, and 20°C under 100% RH [9**]. However, a BTH spray (500 mg/L) before harvest did not suppress Ciborinia camelliae infecting camellia flowers [94]. In rose, pronounced accumulation of PR proteins oc-curred in BTH (50 µM) pre-treated leaves upon challenge inoculation with Diplocarpon rosae [95*]. This treatment resulted in increased resistance to the fungi, with signifi-cantly reduced blackspot severity. Jasmonates Jasmonate treatments result in induced resistance by activat-ing sets of genes encoding PR proteins in plants [49]. When Picea abies seedlings were treated with MeJA vapour (25 µL/100 L air) for 3 days, chitinase activity was increased in their cotyledons and disease incidence upon exposure to Pythium ultimum was 75% less than in the control [96]. Soaking melon seed in 45 µM MeJA solution induced rapid increase in chitinase, peroxidase and lipoxygenase in seed-lings upon challenge with the soil borne pathogens Didymella bryoniae and Sclerotinia sclerotium [97]. Vapour treatment with MeJA (100 µM solution in a sealed container) decreased microbial growth on fresh-cut pineapple without adverse effects on produce quality [98]. Postharvest pulsing treatment of six rose cultivars with MeJA provided local and systemic resistance to B. cinerea [99**]. A combination of pulsing with 350 µM MeJA and spraying with 500 µM MeJA was the best treatment to protect cut roses against postharvest grey mould (Botrytis) development arising from both natural and artificial infection [100**]. Interestingly, postharvest MeJA treatment was reported to improve cut rose appearance by inhibiting petal colour fading during vase life. Although variable responses were recorded across the range of concen-trations tested, postharvest MeJA vapour treatments of cut Geraldton waxflower cvs. Purple Pride (43.6 and 436 µM) and Mullering Brook (4.36 µM) flowers reduced Botrytis disease severity [101**]. Similarly, certain postharvest MeJA

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vapour treatments of cut freesia suppressed petal speckling (ie, disease severity, lesion number and lesion diameter) caused by B. cinerea [13**]. Preharvest treatment of this freesia cv. with MeJA (0.2 mM) by means of spraying also suppressed disease on blooms inoculated after harvest with B. cinerea [9**]. JA and MeJA treatment can have adverse ef-fects on horticultural produce. Accelerated senescence and organ abscission can be induced. Exogenous MeJA treatment (1,000 µL/L) enhanced cherry tomato fruit abscission from harvested trusses [102]. Aqueous MeJA (50 nM) applied to the stigma of cut Dendrobium orchid flowers enhanced se-nescence via increased ET production [103*]. Spraying MeJA (500–1,000 µL/L) 3–5 days before harvest did not affect postharvest flower abscission in cut Geraldton wax-flower cv. Mullering Brook [27**]. However, increased flo-ral organ fall was recorded 4–8 days after exposure of cut stems of the same cultivar to MeJA vapour (10 µL/L) [101**]. MeJA (1,000 µL/L) applied twice as a field spray reduced the vase life of Geraldton waxflower cvs. Mullering Brook and My Sweet Sixteen [27**]. Rhizobacteria Certain fluorescent Pseudomonas spp. that colonise plant roots lead to enhanced defence capacity in the host against a broad spectrum of pathogens that infect upper plant parts. Only a limited number of ISR systems elicited by PGPRs have been identified [104]. The NPR1 gene and JA and ET responsive genes are involved in ISR elicited by effective strains of rhizobacteria [105]. Rhizobacteria have been shown to elicit defence responses in tomato [106] and Arabi-dopsis [105]. Moreover, root inoculation of carnation plants with the ISR-inducing P. fluorescens WCS417r bacteria 1 week prior to stem inoculation with F. oxysporum f. sp. dianthi reduced disease [59]. Other elicitors, including non-chemical Chitosan, beside having direct fungicidal activity, is an elici-tor of host defence responses and can help control many post-harvest diseases on fruits and vegetables [107*]. For exam-ple, chitosan spray treatment (0.1%) of cucumber plants ei-ther 4 or 24 h before inoculation with B. cinerea reduced grey mould development by 82% and 87%, respectively [108*]. GA3 pulsing treatment (20 mg/L for 24 h) suppressed B. cine-rea in detached rose petals cvs. Mercedes and Sonata [109**]. Since the studied concentrations of GA3 were non-toxic to the fungal development in vitro, the authors sug-gested that GA3 may activate natural disease mechanisms. Heat treatments and UV-C irradiation are common physical elicitor methods used against diseases of agricultural prod-ucts. In addition to direct effects of heat treatments against postharvest pathogens, heat can induce host resistance [110–113]. Heat (50°C for 60 s) applied to barley leaves resulted in production of superoxide anions and hydrogen peroxide, and induced resistance against B. graminis f.sp. hordei [114].

Grapefruit fruit pretreated at 62oC by hot water brushing for 20 s showed induced resistance against P. digitatum within 1–3 days [115]. Chitinase and β-1,3-glucanase accumulated in the hot water brushed fruit. Exposure to short wave ultraviolet radiation (UV-C at 190–280 nm) can also provide disease control for many fruits and vegetables [83*]. Tobacco plants irradiated with UV-C (254 nm; 70 gW/cm2) accumulated SA levels about 9-fold higher than in the control [116]. The treatment led to accumulation of PR proteins and increased resistance to TMV. Citrus fruit treated with UV-C had higher concentrations of the phy-toalexin scoparone in their flavedo [117, 118]. UV-C treated tomatoes were resistant to R. stolonifer, which correlated with elevated concentrations of tomatin [119]. Chitinase, glucanase and PAL activities were enhanced after UV-C treatment of harvested peach fruits [120]. Biological elicitors, in addition to PGPRs (see above), have the potential to control postharvest diseases in cut-flowers. Antifungal activity in strawberry fruit skin tissue was en-hanced after dip treatment with an Aureobasidium pullulans cell suspension [121]. The treated fruit were more resistant to B. cinerea infection than the control. Application of C. sai-toana (108 CFU/mL) induced increases in chitinase and ß-1,3-glucanase activity in fresh apples and conferred systemic resistance to B. cinerea infection [122]. Harpin, a protein elicitor of LAR and SAR isolated from the apple fire blight bacterium E. amylovora, is marketed as ‘Messenger’. This product prevented decay caused by Trichothecium roseum on stored Hami melon [123]. Harpin may elicit different signal-ling pathways in various plant-pathogen systems, which can lead to either compatible or incompatible interactions [124]. Ethylene and Botrytis-host interactions B. cinerea is the most common cause of petal necrosis or flower blight [12, 15*, 16*, 23*, 125*]. B. cinerea infection of plant tissues is often associated with enhanced ET produc-tion by the pathogen itself or the host [126*]. This ET can promote abscission or senescence [22*, 127*]. B. cinerea can utilise methionine in vitro to produce α-keto γ-methylthiobutyric acid which in turn, can be oxidised, when exposed to light or peroxidase, to release ET [128, 129]. Di-rect inhibition, by 30% as compared with the control, of B. cinerea hyphal growth has been recorded after 72 h exposure to 200 µL/L ET [126*]. In A. thaliana, healthy leaves treated with intercellular fluid extracted from B. cinerea-infected leaves showed rapid induction of ET production [130]. B. cinerea infection elicits endogenous ET production in cut Geraldton waxflower flowers that, in turn, causes flower fall during storage and transport [12*, 22*, 127*]. Plants that are ET insensitive or fail to produce ET can show increased sus-ceptibility to B. cinerea [126*, 131]. Tomato plants pre-treated with ET were less susceptible to subsequent B. cine-rea infection [132]. Moreover, there is evidence of ET-mediated systemic resistance to B. cinerea [133]. ET is sug-gested to have specific involvement in rhizobacteria-

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mediated resistance [134]. Activation of JA- or ET-dependent defence pathways has been associated with in-creased ET production via enhanced activities of ACC syn-thase and ACC oxidase, two key ET biosynthetic enzymes [103*, 135]. In cut Geraldton waxflower and fressia flowers, MeJA was suggested to induce resistance against B. cinerea [13**, 101**]. However, MeJA treatment increased ET-mediated floral abscission from cut Geraldton waxflower stems [101**, 127*]. Inhibiting ET production (eg, ami-nooxyacetic acid) and perception (eg, silver thiosulphate [STS] and 1-methylcyclopropene [1-MCP]) is potentially beneficial to cut-flower storage and display life, but could potentially result in increased susceptibility of the host to B. cinerea infection. For example, increased grey mould sever-ity on tomato was found when 1-MCP was used to inhibit ET perception [132]. In contrast to waxflower [27**, 101**], MeJA treatments suppressed B. cinerea in cut roses without causing petal abscission [99**]. ET production did not change in MeJA-treated rose cv. Frisco [100**]. Conclusion and future directions The study of pre- or postharvest enhancement of NDR with chemical elicitors with a view to managing postharvest dis-

eases of cut-flowers is in its infancy. Nevertheless, a limited number of investigations to date (Table 1) suggest that elici-tation of host defence in harvested cut-flowers and ornamen-tals holds promise as an alternative to the conventional prac-tice of control with synthetic fungicides. Although funds for basic research on the cut-flowers of commerce are severely limited, it is clear that, if this disease management strategy is to find practical application in the industry, then NDR re-sponses to elicitors in floriculture crops will require investi-gation at the molecular, biochemical and physiological levels. The limited literature reviewed herein reveals that chemical elicitor treatments against postharvest pathogens of cut-flowers can have no (eg, camellia [94]), little (eg, waxflower [27**, 82*, 101**]), variable (eg freesia [9**, 13**]) or sub-stantial (eg, rose [99**, 100**]) efficacy. Also, treatments against postharvest diseases with chemical elicitors may have adverse side-effects in terms of accelerating senescence [103*] or inducing abscission [101**], and they may even be phytotoxic [82*]. General variability in efficacy and side-effects may be mediated by the genotype by environment interaction (G x E) [136]. That is, the nature, degree and tim-ing of NDR responses to elicitor treatments is likely to be genotype specific [57, 136] and to vary with plant history, in terms of climate, management practices or exposure to abiotic or biotic stresses [104] (Figure 1). Moreover, the level of inherent NDR, and the capacity to maintain or enhance it, will probably decline up to and after harvest in association with continuing host development and senescence processes [74*, 137*]. There is a potential to further explore the use of combinations of chemical elicitor treatments for cut flowers. Additionally, there are largely unexplored prospects for utilisation of physical (eg, UV-C) and biological (eg, Aureobasidium spp.) elicitors alone and together across categories. There is also opportunity to explore ancillary treatments that ameliorate adverse effects of elicitors. However, when postharvest treat-ment of Geraldton waxflower flowers with the chemical elicitor MeJA was combined with STS pulsing with a view to prevent ET-mediated flower abscission, the result was an increase in Botrytis disease severity (author’s unpublished data). Priming of NDR is another interesting area for study. Prim-ing of plant resistance is a state of enhanced capacity by the host plant to mount defensive responses [138]. Sometimes, limited defence can be obtained upon the initial treatment with an inducer, such as a pathogen or with biotic or chemi-cal elicitors [139]. However, a more intensive resistance re-sponse may occur upon secondary pathogen challenge or application of an elicitor [67, 140]. That is, plant cells can be primed by pretreatment with elicitors (eg, SA, BTH and INA) to respond more quickly and strongly to subsequent elicita-tion by biotic or abiotic stressors [139]. This phenomenon may help explain why pulsing followed by spraying MeJA enhanced the suppression of B. cinerea on cut roses [100**]. Somewhat similarly, a combination of pre- and postharvest

Figure 1. Schematic representation of the various interacting factors involved in induced natural defence processes (1, 2, 3, 4), and it’s elici-tation (5), and it’s modulation (6, 7); and, also its future utilisation (8).

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MeJA treatments of Geraldton waxflower resulted in de-creased B. cinerea severity (author’s unpublished data). Us-ing ISR-inducing PGPRs to potentiate plant defence against pathogens before harvest is a potentially promising approach for cut-flowers [59]. It is possible that combining partially or inconsistently effec-tive elicitor treatments with other socio-environmentally sound disease management technologies may form the basis of an effective integrated disease management (IDM) strat-egy [83*, 136] for cut-flower crops. For instance, using an-tagonistic microbes to help manage pathogen loads may be synergistic with elicitor treatments. Pseudomonas sp. 677, an antagonistic bacteria isolated from Geraldton waxflower, reduced B. cinerea conidial germination, retarded germ tube elongation and inhibited mycelial growth in vitro. It was also shown to reduce Botrytis-related floral abscission for flower-ing waxflower sprigs [141*]. Since pathogen inoculum levels may overload the host tissue’s defence capacity and limit the potential efficacy of an elicitor [27**, 101**], introduction of antagonistic organisms prior to postharvest elicitor treatment may enhance potential for Botrytis management on cut flow-ers. Finally, unlike fruit and vegetable crops, and as demonstrated by commercial production and sales of novel violet-coloured ‘Moonshadow’ carnations [142], consumers are accepting of genetically modified cut-flowers. Thus, there is a real pros-pect for creation of cut-flowers with either an enhanced ca-pacity to respond to elicitor treatments or inherently higher levels of one or more natural defence compounds. For exam-ple, the introduction into strawberry plants of genes encoding defence proteins (eg, chitinase, thaumatin II) increased their resistance to B. cinerea [143, 144]. In conclusion, it is suggested that the limited published litera-ture on potential elicitation of host defences against cut-flower pathogens shows that this socio-environmentally sound approach holds promise. However, while there is ex-tensive ongoing fundamental research into induced disease resistance, there is a need for a parallel effort of more de-tailed research into manipulation of NDR in ‘real world’ pro-duction systems for cut-flowers and other crops. Nonetheless, if not as a stand-alone technology, then as part of an overall IDM strategy, elicitor-based disease management is likely to be adopted in the medium to long term by the cut-flower in-dustry.

References Papers of interest have been highlighted as: * Importance reading ** Essential reading 1 Behe BK. Floral marketing and consumer research. HortScience 1993:

28:11–14. 2 Laws N. World commerce in cut-flower and roses. FloraCulture Interna-

tional 2002: 12:23–25.

3 Wills R, McGlasson B, Graham D and Joyce DC. Postharvest - An introduc-tion to the physiology and handling of fruit, vegetables and ornamentals. 4th Edition. Wallingford, UK: CAB International; 1998 pp. 262.

4 Gombert L, Windham M and Hamilton S. Evaluation of disease resistance among 57 cultivars of zinnia. HortTechnology 2001: 11:71–74.

5 Kuehnle AR, Fujii T, Chen FC, Alvarez A, Sugii N, Fukui R and Aragon SL. Peptide biocides for engineering bacterial blight tolerance and susceptibility in cut-flower Anthurium. HortScience 2004: 39:1327–1331.

6 Gracia-Garza JA, Blom TJ, Brown W, Roberts DP, Schneider K, Freisen M and Gombert D. Increased incidence of Erwinia soft-rot on calla lilies in the presence of phosphorous. European Journal of Plant Pathology 2004: 110:293–298.

7 *Becktell MC, Daughtrey ML and Fry WE. Epidemiology and management of petunia and tomato late blight in the greenhouse. Plant Disease 2005: 89:1000–1008.

8 Gerik JS. Evaluation of soil fumigants applied by drip irrigation for Liatris production. Plant Disease 2005: 89:883–887.

9 **Darras AI, Joyce DC and Terry LA. Acibenzolar-S-methyl and methyl jasmonate treatments of glasshouse-grown freesias suppress post-harvest petal specking caused by Botrytis cinerea. Journal of Horticultural Science & Biotechnology 2006: 81:1043–1051.

10 *Ngugi HK and Scherm H. Biology of flower-infecting fungi. Annual Re-view of Phytopathology 2006: 44:261–282.

11 *Taylor MN, Wearing AH, Joyce DC and Simons DH. Alternaria alternata causes petal blight and flower drop in harvested Geraldton waxflower. Aus-tralasian Plant Pathology 1998: 27:207–210.

12 *Tomas A, Wearing AH and Joyce DC. Botrytis cinerea - a causal agent of premature flower drop in packaged Geraldton waxflower. Australasian Plant Pathology 1995: 24:26–28.

13 **Darras AI, Terry LA and Joyce DC. Methyl jasmonate vapour treatment suppresses specking caused by Botrytis cinerea on cut Freesia hybrida L. flowers. Postharvest Biology and Technology 2005: 38:175–182.

14 *Elad Y. Latent infection of Botrytis cinerea in rose flowers and combined chemical and physiological control of the disease. Crop Protection 1988: 7:361–366.

15 *Salinas J and Verhoeff K. Microscopic studies of the infection of gerbera flowers by Botrytis cinerea. European Journal of Plant Pathology 1995: 101:377–386.

16 *Darras AI, Terry LA, Joyce DC and Vloutoglou I. Postharvest infection of Freesia hybrida flowers by Botrytis cinerea. Australasian Plant Pathology 2006: 35:1–9.

17 Dirkse FB. Preharvest treatment of chrysanthemum against Botrytis cinerea. Acta Horticulturae 1982: 125:221–226.

18 Elad Y and Volpin H. The involvement of ethylene and calcium in gray mold of Pelargonium, Ruscus, and rose plants. Phytoparasitica 1988: 16:119–131.

19 Jarvis WR. The infection of strawberry and raspberry fruits by Botrtytis cinerea Pers. Annals of Applied Biology 1962: 50:569–575.

20 Cook DWM. A laboratory simulation for vectoring of Trichosporon pullu-lans by conidia of Botrytis cinerea. Phytopathology 2002: 92:1293–1299.

21 *Kerssies A. Influence of environmental conditions on dispersal of Botrytis cinerea conidia and on postharvest infection of gerbera flowers grown under glass. Plant Pathology 1993: 42:754–762.

22 *Beasley DR and Joyce DC. A review of the flower characteristics of Ger-aldton waxflower and factors influencing their abscission from harvested stems. Australian Journal of Experimental Agriculture 2002: 42:519–525.

23 *Pie K and Leeuw GTND. Histopathology of the initial stages of the interac-tion between rose flowers and Botrytis cinerea. Netherlands Journal of Plant Pathology 1991: 97:335–344.

24 Fourie JF and Holz G. Initial infection processes by Botrytis cinerea on nectarine and plum fruit and the development of decay. Phytopathology 1995: 85:82–87.

25 * Prusky D. Pathogen quiescence in postharvest diseases. Annual Review of Phytopathology 1996: 34:413–434.

26 Couey H and Follstad M. Heat pasterization for control of postharvest decay

Dinh and Joyce / Stewart Postharvest Review 2007, 2:4

9

in fresh strawberries. Phytopathology 1966: 56:1345–1347. 27 **Dinh SQ, Joyce DC, Irving DE and Wearing AH. Field applications of

three different classes of known host plant defence elicitors did not suppress Botrytis cinerea infecting Geraldton waxflower. Australasian Plant Pathol-ogy 2007: 36:142–148.

28 Agrios GN. Plant Pathology. 5th Edition. Burlington, MA: Elsevier Aca-demic Press; 2005 pp. 922.

29 Kombrink E and Somssich I. Defense responses of plants to pathogens. Advances in Botanical Research 1995: 21:2–34.

30 Sticher L, Mauch-Mani B and Métraux J. Systemic acquired resistance. Annual Review of Phytopathology 1997: 35:235–270.

31 Stakman E. Relation between Puccinia graminis and plants highly resistant to its attack. Journal of Agricultural Research 1915: 4:193–199.

32 Kombrink E and Schmelzer E. The hypersensitive response and its role in local and systemic disease resistance. European Journal of Plant Pathology 2001: 107:69–78.

33 Heath MC. Hypersensitive response-related death. Plant Molecular Biology 2000: 44:321–334.

34 Hahlbrock K and Scheel D. Physiology and molecular biology of phenylpro-panoid metabolism. Annual Review of Plant Physiology and Plant Molecular Biology 1989: 40:347–369.

35 Yao KN, Deluca V and Brisson N. Creation of a metabolic sink for trypto-phan alters the phenylpropanoid pathway and the susceptibility of potato to Phytophthora infestans. The Plant Cell 1995: 7:1787–1799.

36 Wurms KV, George MP and Lauren DR. Involvement of phenolic com-pounds in host resistance against Botrytis cinerea in leaves of the two com-mercially important kiwifruit (Actinidia chinensis and A. deliciosa) cultivars. New Zealand Journal of Crop and Horticultural Science 2003: 31:221–233.

37 Kuć J. Phytoalexins, stress metabolism, and disease resistance in plants. Annual Review of Phytopathology 1995: 33:275–297.

38 Elad Y. Responses of plants to infection by Botrytis cinerea and novel means involved in reducing their susceptibility to infection. Biological Reviews of the Cambridge Philosophical Society 1997: 72:381–422.

39 Grayer RJ and Harborne JB. A survey of antifungal compounds from higher plants, 1982–1993. Phytochemistry 1994: 37:19–42.

40 Van Loon LC. Occurrence and properties of plant pathogenesis-related proteins. In: Pathogenesis-related proteins in plants. Edited by Datta SK, Muthukrishnan S. Boca Raton, Florida: CRC Press LLC.; 1999 pp. 1–20.

41 Van Loon LC and Van Kammen A. Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. ‘Samsun’ and ‘Samsun NN’: II. Changes in protein constitution after infection with tobacco mosaic virus. Virology 1970: 40:199–211.

42 Van Loon LC and Van Strien EA. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiological and Molecular Plant Pathology 1999: 55:85–97.

43 Alexander D, Goodman RM, Gutrella M, Glascock C, Weymann K, Frie-drich L, Maddox D, Ahlgoy P, Luntz T, Ward E and Ryals J. Increased tolerance to two oomycete pathogens in transgenic tobacco expressing patho-genesis-related protein 1a. Proceedings of the National Academy of Sciences of the United States of America 1993: 90:7327–7331.

44 Métraux J-P, Nawrath C and Genoud T. Systemic acquired resistance. Euphytica 2002: 124:237–243.

45 Durner J and Klessig DF. Salicylic acid is a modulator of tobacco and mam-malian catalases. The Journal of Biological Chemistry 1996: 271:28492–28501.

46 Staswick PE, Yuen GY and Lehman CC. Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare. The Plant Journal 1998: 15:747–754.

47 Penninckx IA, Thomma BP, Buchala A, Métraux JP and Broekaert WF. Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. The Plant Cell 1998: 10:2103–2113.

48 Xu Y, Chang P, Liu D, Narasimhan ML, Raghothama KG, Hasegawa PM and Bressan RA. Plant defense genes are synergistically induced by ethylene and methyl jasmonate. The Plant Cell 1994: 6:1077–1085.

49 Creelman RA, Tierney ML and Mullet JE. Jasmonic acid/methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expression. Proceedings of the National Academy of Sciences of the United States of America 1992: 89:4938–4941.

50 Choi D, Bostock RM, Avdiushko S and Hildebrand DF. Lipid-derived sig-nals that discriminate wound- and pathogen-responsive isoprenoid pathways in plants: methyl jasmonate and the fungal elicitor arachidonic acid induce different 3-hydroxy-3-methylglutaryl-coenzyme A reductase genes and antimicrobial isoprenoids in Solanum tuberosum L. Proceedings of the Na-tional Academy of Sciences of the United States of America 1994: 91:2329–2333.

51 Doares SH, Narvaez-Vasquez J, Conconi A and Ryan CA. Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by sys-temin and jasmonic acid. Plant Physiology 1995: 108:1741–1746.

52 Cameron RK, Dixon RA and Lamb CJ. Biologically induced systemic ac-quired resistance in Arabidopsis thaliana. The Plant Journal 1994: 5:715–725.

53 Van Loon LC, Bakker PA and Pieterse CM. Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology 1998: 36:453–483.

54 Maldonado AM, Doerner P, Dixon RA, Lamb CJ and Cameron RK. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 2002: 419:399–403.

55 Farmer EE, Weber H and Vollenweider S. Fatty acid signaling in Arabidop-sis. Planta 1998: 206:167–174.

56 Dong X. NPR1, all things considered. Current Opinion in Plant Biology 2004: 7:547–552.

57 Durrant WE and Dong X. Systemic acquired resistance. Annual Review of Phytopathology 2004: 42:185–209.

58 Pieterse CMJ, Van Pelt JA, Van Wees SCM, Ton J, Léon-Kloosterziel KM, Keurentjes JJB, Verhagen BWM, Knoester M, Van der Sluis I, Bakker PAHM and Van Loon LC. Rhizobacteria-mediated induced systemic resis-tance: triggering, signalling and expression. European Journal of Plant Pa-thology 2001: 107:51–61.

59 Van Peer R, Niemann G and Schippers B. Induced resistance and phy-toalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology 1991: 81:728–734.

60 Ton J, Van Pelt JA, Van Loon LC and Pieterse CMJ. Differential effective-ness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. Molecular Plant-Microbe Interactions 2002: 15:27–34.

61 Chamberlain K, Pickett JA and Woodcock CM. Plant signalling and induced defence in insect attack. Molecular Plant Pathology 2000: 1:67–72.

62 Devoto A and Turner JG. Jasmonate-regulated Arabidopsis stress signalling network. Physiologia Plantarum 2005: 123:161–172.

63 Lorenzo O and Solano R. Molecular players regulating the jasmonate signal-ling network. Current Opinion in Plant Biology 2005: 8:532–540.

64 Niki T, Mitsuhara I, Seo S, Ohtsubo N and Ohashi Y. Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant and Cell Physi-ology 1998: 39:500–507.

65 Lawton K, Weymann K, Friedrich L, Vernooij B, Uknes S and Ryals J. Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Molecular Plant-Microbe Interactions 1995: 8:863–870.

66 Hudgins JW and Franceschi VR. Methyl jasmonate induced ethylene pro-duction is responsible for conifer phloem defense responses and reprogram-ming of stem cambial zone for traumatic resin duct formation. Plant Physiol-ogy 2004: 135:2134–2149.

67 Heil M and Bostock RM. Induced systemic resistance (ISR) against patho-gens in the context of induced plant defences. Annals of Botany 2002: 89:503–512.

68 Kunkel BN and Brooks DM. Cross talk between signaling pathways in pathogen defense. Current Opinion in Plant Biology 2002: 5:325–331.

69 Glazebrook J, Chen W, Estes B, Chang H-S, Nawrath C, Métraux J-P, Zhu T and Katagiri F. Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. The Plant Journal 2003: 34:217–228.

Dinh and Joyce / Stewart Postharvest Review 2007, 2:4

10

70 Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Pelt JAV, Mueller MJ, Buchala AJ, Métraux J-P, Brown R, Kazan K, Loon LCV, Dong X and Pieterse CMJ. NPR1 modulates cross-talk between salicylate- and jas-monate-dependent defense pathways through a novel function in the cytosol. The Plant Cell 2003: 15:760–770.

71 Norman-Setterblad C, Vidal S and Palva ET. Interacting signal pathways control defense gene expression in Arabidopsis in response to cell wall-degrading enzymes from Erwinia carotovora. Molecular Plant-Microbe Interactions 2000: 13:430–438.

72 Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Métraux J-P, Brown R, Kazan K, Van Loon LC, Dong X, and Pieterse CMJ. NPR1 modulates cross-talk between salicylate- and jas-monate-dependent defense pathways through a novel function in the cytosol. The Plant Cell 2003: 15:760–770.

73 Wendehenne D, Durner J and Klessig DF. Nitric oxide: a new player in plant signalling and defence responses. Current Opinion in Plant Biology 2004: 7:449–455.

74 * Wilson CL, El Ghaouth A, Chalutz E, Droby S, Stevens C, Lu JY, Khan V and Arul J. Potential of induced resistance to control postharvest diseases of fruits and vegetables. Plant Disease 1994: 78:837–844.

75 White RF. Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology 1979: 99:410–412.

76 Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chan-dler D, Slusarenko A, Ward E and Ryals J. Acquired resistance in Arabidop-sis. The Plant Cell 1992: 4:645–656.

77 Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Métraux JP and Ryals JA. Coordinate gene activity in re-sponse to agents that induce systemic acquired resistance. The Plant Cell 1991: 3:1085–1094.

78 Fodor J, Gullner G, Adam AL, Barna B, Komives T and Kiraly Z. Local and systemic responses of antioxidants to tobacco mosaic virus infection and to salicylic acid in tobacco (role in systemic acquired resistance). Plant Physiol-ogy 1997: 114:1443–1451.

79 Zainuri, Joyce DC, Wearing H, Coates L and Terry L. Effects of phospho-nate and salicylic acid treatments on anthracnose disease development and ripening of 'Kensington Pride' mango fruit. Australian Journal of Experimen-tal Agriculture 2001: 41:805 – 813.

80 Poole PR and McLeod LC. Development of resistance to picking wound entry Botrytis cinerea storage rots in kiwifruit. New Zealand Journal of Crop and Horticultural Science 1994: 22:387–392.

81 Yao H and Tian S. Effects of pre- and post-harvest application of salicylic acid or methyl jasmonate on inducing disease resistance of sweet cherry fruit in storage. Postharvest Biology and Technology 2005: 35:253–262.

82 * Beasley DR. Strategies for control of Botrytis cinerea on Geraldton wax-flower flowers. PhD thesis. The University of Queensland; 2001.

83 * Terry LA and Joyce DC. Elicitors of induced disease resistance in posthar-vest horticultural crops: a brief review. Postharvest Biology and Technology 2004: 32:1–13.

84 Reglinski T, Poole PR, Whitaker G and Hoyte SM. Induced resistance against Sclerotinia sclerotiorum in kiwifruit leaves. Plant Pathology 1997: 46:716–721.

85 Huang Y and Deverall BJ. Pratical approaches for controlling plant diseases through systemic induced resistance. In: Disease Resistance in Fruit. Edited by Johnson GI, Highley E, Joyce DC (editors). Canberra: ACIAR Proceed-ings No. 80; 1998. pp. 136–138.

86 Friedrich L, Lawton K, Ruess W, Masner P, Specker N, Rella MG, Meier B, Dincher S, Staub T, Uknes S, Métraux J-P, Kessmann H and Ryals J. A benzothiadiazole derivative induces systemic acquired resistance in tobacco. The Plant Journal 1996: 10:61–70.

87 Dann E, Diers B, Byrum J and Hammerschmidt R. Effect of treating soybean with 2,6-dichloroisonicotinic acid (INA) and benzothiadiazole (BTH) on seed yields and the level of disease caused by Sclerotinia sclerotiorum in field and greenhouse studies. European Journal of Plant Pathology 1998: 104:271–278.

88 Mondal AH, Nehl DB and Allen SJ. Acibenzolar-S-methyl induces systemic resistance in cotton against black root rot caused by Thielaviopsis basicola.

Australasian Plant Pathology 2005: 34:499–507. 89 Iriti M, Rossoni M, Borgo M and Faoro F. Benzothiadiazole enhances res-

veratrol and anthocyanin biosynthesis in grapevine, meanwhile improving resistance to Botrytis cinerea. Journal of Agricultural and Food Chemistry 2004: 52:4406–4413.

90 Liu H, Jiang W, Bi Y and Luo Y. Postharvest BTH treatment induces resis-tance of peach (Prunus persica L. cv. Jiubao) fruit to infection by Penicillium expansum and enhances activity of fruit defense mechanisms. Postharvest Biology and Technology 2005: 35:263–269.

91 Cao J, Jiang W and He H. Induced resistance in Yali pear (Pyrus bretschnei-deri Rehd.) fruit against infection by Penicillium expansum by postharvest infiltration of acibenzolar-S-methyl. Journal of Phytopathology 2005: 153:640–646.

92 Wurms K, Labbé C, Benhamou N and Bélanger RR. Effects of milsana and benzothiadiazole on the ultrastructure of powdery mildew haustoria on cu-cumber. Phytopathology 1999: 89:728-736.

93 Pradhanang PM, Ji P, Momol MT, Olson SM, Mayfield JL and Jones JB. Application of acibenzolar-S-methyl enhances host resistance in tomato against Ralstonia solanacearum. Plant Disease 2005: 89:989–993.

94 van Toor RF, Jaspers MV and Stewart A. Evaluation of acibenzolar-S-methyl for induction of resistance in camellia flowers to Ciborinia camelliae. New Zealand Plant Protection 2001: 54:209–212.

95 *Suo Y and Leung DWM. BTH-induced accumulation of extracellular proteins and blackspot disease in rose. Biologia Plantarum 2002: 45:273–279.

96 Kozlowski G, Buchala A and Métraux J-P. Methyl jasmonate protects Nor-way spruce [Picea abies (L.) Karst.] seedlings against Pythium ultimum Trow. Physiological and Molecular Plant Pathology 1999: 55:53–58.

97 Buzi A, Chilosi G, De Sillo D and Magro P. Induction of resistance in melon to Didymella bryoniae and Sclerotinia sclerotiorum by seed treatments with acibenzolar-S-methyl and methyl jasmonate but not with salicylic acid. Journal of Phytopathology 2004: 152:34–42.

98 Martinez-Ferrer M and Harper C. Reduction in microbial growth and im-provement of storage quality in fresh-cut pineapple after methyl jasmonate treatment. Journal of Food Quality 2005: 28:3–12.

99 ** Meir S, Droby S, Davidson H, Alsevia S, Chohen L, Horev B and Phi-losoph-Hadas S. Suppression of Botrytis rot in cut rose flowers by posthar-vest application of methyl jasmonate. Postharvest Biology and Technology 1998: 13:235–243.

100 **Meir S, Droby S, Kochanek B, Salim S and Philosoph-Hadas S. Use of methyl jasmonate for suppression of Botrytis rot in various cultivars of cut rose flowers. Acta Horticulturae 2005: 669:91–98.

101 **Eyre JX, Joyce DC, Faragher J and Franz PR. Effects of postharvest methyl jasmonate treatments against Botrytis cinerea on Geraldton wax-flower (Chamelaucium uncinatum). Australian Journal of Experimental Agriculture 2006: 46:717–723.

102 Beno-Moualem D, Gusev L, Dvir O, Pesis E, Meir S and Lichter A. The effects of ethylene, methyljasmonate and 1-MCP on abscission of cherry tomatoes from the bunch and expression of endo-1,4-beta-glucanases. Plant Science 2004: 167:499–507.

103 * Porat R, Borochov A and Halevy AH. Is jasmonic acid involved in the endogenous regulation of Dendrobium orchid flower senescence? Acta Horticulturae 1995: 405:314–319.

104 Vallad GE and Goodman RM. Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Science 2004: 44:1920–1934.

105 Verhagen BWM, Glazebrook J, Zhu T, Chang HS, van Loon LC and Piet-erse CMJ. The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Molecular Plant-Microbe Interactions 2004: 17:895–908.

106 Yan ZN, Reddy MS, Ryu CM, McInroy JA, Wilson M and Kloepper JW. Induced systemic protection against tomato late blight elicited by plant growth-promoting rhizobacteria. Phytopathology 2002: 92:1329–1333.

107 *Bautista-Banos S, Hernandez-Lauzardo AN, Velazquez-del Valle MG, Hernandez-Lopez M, Barka EA, Bosquez-Molina E and Wilson CL. Chito-san as a potential natural compound to control pre and postharvest diseases of horticultural commodities. Crop Protection 2006: 25:108–118.

Dinh and Joyce / Stewart Postharvest Review 2007, 2:4

11

108 *Ben-Shalom N, Ardi R, Pinto R, Aki C and Fallik E. Controlling gray mould caused by Botrytis cinerea in cucumber plants by means of chitosan. Crop Protection 2003: 22:285–290.

109 **Shaul O, Elad Y and Zieslin N. Suppression of Botrytis blight in cut rose flowers with gibberellic acid: effect of concentration and mode of applica-tion. Postharvest Biology and Technology 1995: 6:321–330.

110 Lurie S, Fallik E, Handros A and Shapira R. The possible involvement of peroxidase in resistance to Botrytis cinerea in heat treated tomato fruit. Physiological and Molecular Plant Pathology 1997: 50:141–149.

111 Fallik E, Grinberg S, Gambourg M, Klein JD and Lurie S. Prestorage heat treatment reduces pathogenicity of Penicillium expansum in apple fruit. Plant Pathology 1996: 45:92–97.

112 Lurie S. Postharvest heat treatments. Postharvest Biology and Technology 1998: 14:257–269.

113 Elad Y and Volpin H. Heat treatment for the control of rose and carnation gray mold (Botrytis cinerea). Plant Pathology 1991: 40:278–286.

114 Vallelian-Bindschedler L, Schweizer P, Mosinger E and Métraux J-P. Heat-induced resistance in barley to powdery mildew (Blumeria graminis f.sp. hordei) is associated with a burst of active oxygen species. Physiological and Molecular Plant Pathology 1998: 52:185–199.

115 Pavoncello D, Lurie S, Droby S and Porat R. A hot water treatment induces resistance to Penicillium digitatum and promotes the accumulation of heat shock and pathogenesis-related proteins in grapefruit flavedo. Physiologia Plantarum 2001: 111:17–22.

116 Yalpani N, Enyedi AJ, Leon J and Raskin I. Ultraviolet light and ozone stimulate accumulation of salicylic acid, pathogenesis-related proteins and virus-resistance in tobacco. Planta 1994: 193:372–376.

117 Ben-Yehoshua S, Rodov S, Kim JJ and Carnelli S. Preformed and induced antifungal materials of citrus fruit in relation to enhancement of decay resis-tance by heat and UV treatment. Journal of Agricultural and Food Chemistry 1992: 40:1217–1221.

118 D'Hallewin G, Schirra M, Manueddu E, Piga A and Ben-Yehoshua S. Sco-parone and scopoletin accumulation and ultraviolet-C induced resistance to postharvest decay in oranges as influenced by harvest date. Journal of the American Society for Horticultural Science 1999: 124:702–707.

119 Stevens C, Liu J, Khan VA, Lu JY, Wilson CL, Igwegbe ECK, Kabwe MK, Chalutz E and Droby S. Application of hermetic UV-C for delayed ripening and reduction of Rhizopus soft rot in tomatoes: the effect of tomatine on storage rot development. Journal of Phytopathology 1998: 146:211–221.

120 El Ghaouth A, Wilson CL and Callahan AM. Induction of chitinase, beta-1,3-glucanase, and phenylalanine ammonia lyase in peach fruit by UV-C treatment. Phytopathology 2003: 93:349–355.

121 Adikaram NKB, Joyce DC and Terry LA. Biocontrol activity and induced resistance as a possible mode of action for Aureobasidium pullulans against grey mould of strawberry fruit. Australasian Plant Pathology 2002: 31:223–229.

122 El Ghaouth A, Wilson CL and Wisniewski M. Control of postharvest decay of apple fruit with Candida saitoana and induction of defense responses. Phytopathology 2003: 93:344–348.

123 Yang B, Shiping T, Jie Z and Yonghong G. Harpin induces local and sys-temic resistance against Trichothecium roseum in harvested Hami melons. Postharvest Biology and Technology 2005: 38:183–187.

124 Reboutier D, Frankart C, Briand J, Biligui B, Laroche S, Rona J-P, Barny M-A and Bouteau F. The HrpNea harpin from Erwinia amylovora triggers dif-ferential responses on the nonhost Arabidopsis thaliana cells and on the host apple cells. Molecular Plant-Microbe Interactions 2007: 20:94–100.

125 * Edney KL. The development of Botrytis cinerea on cut flowers of carna-tion. Annals of Applied Biology 1967: 60:367–374.

126 * Chagué V, Danit LV, Siewers V, Gronover CS, Tudzynski P, Tudzynski B and Sharon A. Ethylene sensing and gene activation in Botrytis cinerea: A

missing link in ethylene regulation of fungus-plant interactions? Molecular Plant-Microbe Interactions 2006: 19:33–42.

127 *Joyce DC. Postharvest floral organ fall in Geraldton waxflower (Chamelaucium uncinatum Schauer). Australian Journal of Experimental Agriculture 1993: 33:481–487.

128 Chagué V, Elad Y, Barakat R, Tudzynski P and Sharon A. Ethylene biosyn-thesis in Botrytis cinerea. FEMS Microbiology Ecology 2002: 40:143–149.

129 Cristescu SM, De Martinis D, Hekkert ST, Parker DH and Harren FJM. Ethylene production by Botrytis cinerea in vitro and in tomatoes. Applied and Environmental Microbiology 2002: 68:5342–5350.

130 Govrin EM, Rachmilevitch S, Tiwari BS, Solomon M and Levine A. An elicitor from Botrytis cinerea induces the hypersensitive response in Arabi-dopsis thaliana and other plants and promotes the gray mold disease. Phyto-pathology 2006: 96:299–307.

131 Thomma BPHJ, Eggermont K, Tierens KFM-J and Broekaert WF. Require-ment of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiology 1999: 121:1093–1101.

132 Díaz J, ten Have A and van Kan JAL. The role of ethylene and wound sig-naling in resistance of tomato to Botrytis cinerea. Plant Physiology 2002: 129:1341–1351.

133 Berrocal-Lobo M, Molina A and Solano R. Constitutive expression of ethyl-ene-response-factor1 in Arabidopsis confers resistance to several necrotro-phic fungi. The Plant Journal 2002: 29:23–32.

134 Broekaert WF, Delaure SL, De Bolle MFC and Cammue BPA. The role of ethylene in host-pathogen interactions. Annual Review of Phytopathology 2006: 44:393–416.

135 Walling LL. The myriad plant responses to herbivores. Journal of Plant Growth Regulation 2000: 19:195–216.

136 Walters D, Walsh D, Newton A and Lyon G. Induced resistance for plant disease control: Maximizing the efficacy of resistance elicitors. Phytopathol-ogy 2005: 95:1368–1373.

137 *Prusky D. Mechanisms of resistance of fruits and vegetables to postharvest diseases. In: Disease Resistance in Fruit. Edited by Johnson GI, Highley E, Joyce DC (editors). Canberra: ACIAR Proceedings No. 80;1998. pp. 19–33.

138 Katz VA, Thulke OU and Conrath U. A benzothiadiazole primes parsley cells for augmented elicitation of defense responses. Plant Physiology 1998: 117:1333–1339.

139 Conrath U, Pieterse CMJ and Mauch-Mani B. Priming in plant-pathogen interactions. Trends in Plant Science 2002: 7:210–216.

140 Conrath U, Beckers GJM, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman MA, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L and Mauch-Mani B. Priming: Getting ready for battle. Molecular Plant-Microbe Interactions 2006: 19:1062–1071.

141 * Beasley DR, Joyce DC, Coates LM and Wearing AH. Saprophytic micro-organisms with potential for biological control of Botrytis cinerea on Gerald-ton waxflower flowers. Australian Journal of Experimental Agriculture 2001: 41:697–703.

142 Agrifood Awareness Australia. Accessed on February 2nd, 2007. [ h t t p : / /www.afaa.com.au/resource_guides/Resource_Carnations.pdf]

143 Schestibratov KA and Dolgov SV. Transgenic strawberry plants expressing a thaumatin II gene demonstrate enhanced resistance to Botrytis cinerea. Sci-entia Horticulturae 2005: 106:177–189.

144 Vellicce GR, Ricci JCD, Hernandez L and Castagnaro AP. Enhanced resis-tance to Botrytis cinerea mediated by the transgenic expression of the chiti-nase gene ch5B in strawberry. Transgenic Research 2006: 15:57–68.

145 *Dmitriev A, Tena M and Jorrin J. Systemic acquired resistance in sunflower (Helianthus annuus L.). TSitologiia i Genetika 2003: 37:9–15.

146 *Elmer WH. Effects of acibenzolar-S-methyl on the suppression of Fusarium wilt of cyclamen. Crop Protection 2006: 25:671–676.

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