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Histopathology of Black Spot Symptoms in Sweet Oranges

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Histopathology of Black Spot Symptoms in Sweet Oranges Eur J Plant Pathol (2012) 133:439–448 DOI 10.1007/s10658-011-9917-9 Histopathology of black spot symptoms in sweet oranges João Paulo Rodrigues Marques & Marcel Bellato Spósito & Alexandre Furtado Silveira Mello & Lilian Amorim & Matheus Mondin & Beatriz Appezzato-da-Glória Accepted: 1 December 2011 /Published online: 23 December 2011 # KNPV 2011 Abstract In Brazil, citrus black spot (CBS) caused by alterations to the epicarp and mesocarp, but in our Guignardia citricarpa is a major disease that has samples only hard spot lesions contained pycnidia. different symptoms on fruit. In this study, fruit of Both of these symptoms were accompanied by protein Citrus sinensis infected by G. citricarpa and showing inclusions. Epidermal and sub-epidermal cells located the symptoms false melanosis, freckle spot and hard in the oil-gland region were obliterated, causing alter- spot were cross-sectioned and analysed anatomically ations in these structures. All symptoms had regions and histochemically by light microscopy. Immuno- that stained strongly for lipids and phenols. histological assays were performed. All symptoms were accompanied by a thickening of the cuticle. False Keywords Citrus sinensis . Guignardia citricarpa . melanosis lesions did not contain pycnidia and Phyllosticta citricarpa . Necrotic symptoms remained restricted to the epicarp or to the first layers of the mesocarp. The stomata in this type of lesion showed phenolic compounds in the guard cells and in the sub-stomatal chamber. In some samples, the guard Introduction cells and their surrounding cells lysed, and a wound meristem began to form underneath them. Freckle spot Citrus black spot (CBS), caused by Guignardia citri- and hard spot lesions had very similar histological carpa Kiely (Phyllosticta citricarpa Van der Aa), is an important disease in Brazil. All commercial varieties of oranges are susceptible to this disease (Spósito et al. J. P. R. Marques : M. B. Spósito : A. F. S. Mello : L. Amorim : M. Mondin : B. Appezzato-da-Glória (*) 2004), which is controlled by four to five fungicide Escola Superior de Agricultura “Luiz de Queiroz”, sprays in the field (Timmer 1999). As the disease is Universidade de São Paulo, not found in Europe, fruit with black spot symptoms Cx. Postal 9, may not be imported into the European Union (Smith CEP 13418-900 Piracicaba, SP, Brazil e-mail: [email protected] and Charles 1998; Aguilar-Vildoso et al. 2002). The state of São Paulo produces 80% of the oranges con- Present Address: sumedinBrazilandistheworld’s largest citrus- A. F. S. Mello producing region but less than 1% of this total is Monsanto do Brasil Ltda, Rod. BR 452, Km 149,Cx. Postal 3077, exported, primarily due to the presence of CBS in CEP 38407-049 Uberlândia, MG, Brazil the groves (Neves et al. 2007). 440 Eur J Plant Pathol (2012) 133:439–448 Fig. 1 Healthy fruits of Citrus sinensis Osbeck ‘Valência’. a-g, ferric trichloride reaction (c). e. Epicarp stained with Xylidine Transversal sections of the epicarp and mesocarp. a, Epicarp Ponceau. f-g, Details of the mesocarp. g. Oil cavity epithelial with oil cavity. b-d, Details of the stomata after staining with cells. e: fruit epidermis, ep: epicarp, mesocarp (me), oc: oil toluidine blue (b) and fast green pH 2.5 (d) and after negative cavity, st: stomata, vb: vascular bundles G. citricarpa is an ascomycete that produces asco- criterion of this disease is based on the presence of spores in pseudothecia on dead leaves on the citrus pycnidia, which appear in the centres of hard spot and grove floor as well as pycnidia and conidia on fruits, sometimes on freckle spot lesions (Kotzé 2000). The dead leaves and dead twigs (Timmer 1999). The asco- cause of the diversity in citrus black spot symptoms is spores are predominantly transported by the wind, not known. It could be due to the size of the fruit when whereas the conidia are dispersed over short distances infection occurs (Kotzé 2000; Aguilar-Vildoso et al. by rain splashes (Kotzé 1963). After the spores have 2002), the weather (Brodrick and Rabie 1970), the been deposited, the infection process starts, and symp- concentration or type of the inoculum (Almeida toms begin to appear in 4 months (Baldassari et al. 2009). As no reliable, practical and effective inocula- 2008). Usually symptoms appear on ripe fruit, some- tion method has been reported in the literature, the times even after harvest. Three symptoms are usually symptoms development is only observed under natural associated with this disease (Brodrick and Rabie 1970; Kotzé 2000): hard spot, false melanosis and freckle Fig. 2 Fruits of Citrus sinensis (L.) Osbeck ‘Valência’ withb spot. Hard spot is the most common symptom and is symptoms of “False melanosis”. a-b, ‘False melanosis’ lesions. characterised by black, circular and depressed lesions, The arrow in b indicated the rupture in fruit surface. c-j, Trans- versal sections of the lesioned pericarp. c-e, Phenolic com- usually with pycnidia in the centre, but not always. It pounds in guard cells (arrows in c and d) and in the sub- appears usually after fruit colour changes from green stomatic chamber (arrows in e) after positive ferric trichloride to orange (Kotzé 2000). False melanosis is character- reaction. f, Presence of the fungus between guard cells (arrow). ised by small black lesions with no depression, similar g, Installation of wound meristem (arrows) in the sub-stomatic chamber. h, Rupture of the epidermal and sub-epidermal layers to those seen in the melanosis symptom caused by (arrow) above the wound meristem. i, Detail of the wound tissue Diaporthe citri. It typically develops on green fruit composed of a layer of cells with phenolic compounds (arrow), and do not contain pycnidia (Kotzé 2000). Freckle one layer of cells with lipidic compounds (arrowhead) and some spot is characterised by red-to-brown depressed layers of meristematic cells. There are fungi hyphae on the surface. j, General view of the lesion indicated in b. The arrow lesions that develop pre-harvest. indicated the rupture in the fruit surface. e: fruit epidermis, ep: Since the symptoms are extremely variable and can epicarp, hy: hyphae, me: mesocarp, oc: oil cavities, st: stomata, be difficult to identify, the most reliable diagnostic wm: wound meristem Eur J Plant Pathol (2012) 133:439–448 441 infection. In the first report of a successful artificial lesions took 6 months to be produced on lemons (Lemir inoculation with ascospores obtained in vitro, black spot et al. 2000), the most susceptible citrus species to G. 442 Eur J Plant Pathol (2012) 133:439–448 citricarpa (Kotzé 2000). It was not clear in that report under a stereomicroscope (Nikon, model SMZ-2T). Af- how the authors guarantee that the symptoms originated terwards, samples were fixed in Karnovsky solution from the artificial inoculation, because no control was (Karnovsky 1965), dehydrated in ethanol and embedded described. Even the latest reported method of artificial in plastic resin (Leica Historesin). Serial sections (5– inoculation of oranges does not allow a precise study for 7 μm thick) were cut on a rotary microtome and stained symptom development, because only false melanosis with toluidine blue O (Sakai 1973). The main classes of was consistently reproduced 150 days after inoculation metabolites in the lesions were investigated in sections on Pera sweet orange cultivar (Baldassari et al. 2009). from plastic resin-embedded samples using the follow- No hard spot symptoms developed on inoculated fruit of ing histochemical tests: Sudan black B (Jensen 1962)for Pera cv. Detached fruit cannot be inoculated because of total lipids, Ruthenium red (Johansen 1940) for pectins, the long incubation period of the disease. ferric trichloride (Johansen 1940) for phenolic com- Although the reproductive structures of the fungus pounds, Xylidine Ponceau for protein compounds and responsible for its spread are only present in fruit with fast green pH 2.5 for acid proteins (Cortelazzo 2007). hard spot or freckle spot symptoms, the European Union Images were captured digitally with a Leica DM LB does not allow the entry of fruit with any symptom. microscope with a video camera attached to a PC, using All symptoms are restricted to the orange peel, the IM50 image analysis software. reducing the price of diseased fruit on the fresh mar- For the immunohistochemical tests, the samples ket. Under high disease intensity, the fruit often drop were immersed in Bouin’s fixative solution (Sass prematurely, decreasing yield (Kotzé 2000). One of 1951), dehydrated in a graded ethanol series and em- the by-products of the orange juice industry that is bedded in Paraplast®. The paraffin blocks were sec- becoming increasingly valuable is the oil extracted tioned with a rotary microtome (5 μm thickness) and from the peels of citrus fruits. Fruits that show signs deposited on slides. Later, the paraffin was removed of hard spot surprisingly have higher oil content than using xylene, and the samples were rehydrated with a those that show false melanosis (Spósito et al. 2009). decreasing ethanol series. Toluidine blue (0.01%) in This difference could be explained by different phosphate-buffered saline solution (PBS) was used to changes in the pericarp associated with each symptom. inhibit the natural auto-fluorescence of the cuticle The aim of this study was to characterise anatomical- (Ruzin 1999). Subsequently, the samples were ly and histochemically the false melanosis, freckle spot blocked in a 1:1 mixture of PBS and Bovine serum and hard spot symptoms caused by Guignardia citri- albumin (BSA) for 5 min. The primary polyclonal carpa to better understand the colonisation process of antibody was obtained from fungal mycelia emulsified this pathogen and assess the damage caused by the fun- with incomplete Freund’s adjuvant (1:1) injected in- gus in naturally occurring symptoms on sweet oranges.
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