Evidence for the variation in susceptibility
of bananas to wound anthracnose due to
Colletotrichum musae
and the in¯uence
of edaphic conditions
M. Chillet
a,*, L. de Lapeyre de Bellaire
a, M. Dorel
b,
J. Joas
c, C. Dubois
b, J. Marchal
b, X. Perrier
ba
Cirad ¯hor, Station de Neufchateau, Sainte Marie, 97130 Capesterre Belle Eau, Guadeloupe, FWI
b
Cirad ¯hor, BP 5035, 34032 Montpellier cedex 1, France
c
Cirad ¯hor, Station de Moutte, 97200 Fort de France, Martinique, FWI
Accepted 11 February 2000
Abstract
Wound anthracnose is a post-harvest disease which develops during storage and ripening of bananas. In the French West Indies, it mainly occurs on fruits coming from plantations situated on soils at low-altitude, during the second half of the year. It is caused by a pathogenic fungus,
Colletotrichum musae. A diagnostic survey was carried out on 106 plots representative of all the soil/climatic conditions and techniques in Guadeloupe in order to assess the variability of fruit susceptibility to wound anthracnose. Secondly, the effect of mineral nutrition on this susceptibility was analysed for the soil/climatic zone where the anthracnose problems are most serious. For this purpose, 54 plots on halloysitic and ferrallitic soils were chosen by including in the selection plots from all cultural situations. This study has brought to light a wide variation in the susceptibility of bananas toColletotrichum musae. Fruits from high-altitude plantations are the least susceptible. On low-altitude soils, where the most variability is observed, a relationship was found between the Mn content of fruit and susceptibility to anthracnose; the plants producing the most susceptible fruit had high foliar Mn concentrations and low Ca concentrations, and had grown on rather acid soils.
*
Corresponding author. Tel.:590-86-17-69; fax:590-86-80-77.
E-mail address: [email protected] (M. Chillet)
Hypotheses for the physiological mechanisms involved in the sensitisation of the fruit are discussed.
#2000 Elsevier Science B.V. All rights reserved.
Keywords: Banana;Musa; Wound anthracnose;Colletotrichum musae; Manganese; Calcium
1. Introductionz
Wound anthracnose is a disease that is caused by a fungus, Colletotrichum
musae, which infects the fruit in the ®eld in the ®rst month after ¯owering (de
Lapeyre de Bellaire and Mourichon, 1997). The conidia reach the surface of the fruit in rainwater trickling over the bunch (de Lapeyre de Bellaire, 1999). They germinate quickly and form a melanic appressorium which is a dormant structure of the pathogen. The melanic appressoria only germinate during fruit ripening, to form an infection hypha which will colonise the peel, and then the pulp of the fruit (Muirhead and Deverall, 1981; Swinburne and Brown, 1983). When the fruits are damaged, lesions develop though they are still green, and the lesions develop larger (Meredith, 1960). It is this form of the disease, called wound anthracnose, which is the cause of the damage during transport and storage of the bananas and which seriously detracts from the quality of the product from Guadeloupe (FWI).
This disease is usually controlled by means of treatments applied just before packing using a fungicide with an antimitotic action, thiabendazole. However, anthracnose problems appear every year at the same time (fruit exported between August and January) in the middle of the rainy season (the climate of Guadeloupe is of the tropical humid type), mainly on plantations situated in low-altitude zones. Strains ofC. musaeexist which are resistant to thiabendazole. Moreover, the timing of the appearance of the disease cannot be explained by resistance to the fungicide. It has, therefore, been suggested that this seasonal phenomenon is more likely to be the result of variation in the level of the quality potential of the fruit (Chillet and de Lapeyre de Bellaire, 1996). This quality potential is de®ned partly by a physiological component which conditions the susceptibility of fruit and partly by a parasitic component which appears as the level of contamination of the bananas. Accordingly to this hypothesis, the quality potential depends on the soil and climatic conditions of the production zone, and the cultural techniques used by the growers. These factors have an in¯uence on the physiological component of the potential via the mineral nutrition and water supply to the banana plants.
To identify the factors which might explain variation in fruit susceptibility to wound anthracnose, a diagnostic survey was conducted in all of the soil and climatic conditions of Guadeloupe. Firstly the variation in fruit susceptibility to
C. musaeover the whole of the zone studied was observed, and the relationships
2. Materials and methods
2.1. Soil characteristics of the study zone
2.1.1. Andosols of the windward coast
These soils, developed on a volcanic material, are characterised by the presence of gibbsite and allophanes. They are situated in high-altitude, high-rainfall areas, and presented physical properties which are generally favourable to the crop (large water reserve, good internal drainage and structural stability).
2.1.2. Andosols of the leeward coast
Developed on more recent volcanic material than the corresponding soils on the windward coast, these soils are less weathered and more fertile. They are also distinguished by the absence of gibbsite.
2.1.3. Vertisols
These soils, developed on coral limestone, contain large amounts of expanding clays, smectites, which confer on them particular hydrodynamic properties. Water in®ltration is notably controlled by swelling and shrinking phenomena, which causes the appearance and disappearance of large cracks.
2.1.4. Halloysitic and ferrallitic soils
These two soil types contain a large percentage of clay (80%). The dominant clay mineral is halloysite in both soil types (Van Oort, 1988).
Their structural stability and hydraulic conductivity are high. However, in certain topographic conditions one can ®nd signs of hydromorphy in agricultural soils which have been subjected to intense mechanical cultivation.
2.2. Plot sampling
The survey of wound anthracnose incidence took place during the period of poor banana quality in 1996. One hundred and six plots of banana plants (six on a vertisol, 54 on halloysitic and ferrallitic soil, 35 on windward coast andosols and 11 on leeward coast andosols) of theMusa acuminatatriploid (Grande Naine and Poyo cultivars) were chosen in the four types of soil described above. For the second part of the study, the 54 plots on the halloysite and ferrallitic zone soils were chosen according to the technical level of the farm. The plots were selected by the level of intensi®cation, notably irrigation, fertilisation, and preceding crop.
2.3. Methodology
as possible as regards to stage of development and bunch shape and were representative of the plot.
2.3.1. Diagnosis of mineral nutrition
A sampling of the third leaf was collected for mineral analysis (Martin-PreÂvel, 1974). The elements analysed were N, P, K, Ca, Mg, Na, Mn, Fe, Cl, Zn, B, Cu and S. A soil sample was taken for chemical analysis. This was analysed for total C and N content, Olsen±Dabin-available P, exchangeable K, Ca, Mg, Na and Mn, analysed after extraction with cobaltihexamine, pH and CEC (cation exchange capacity).
A median internal fruit of the third hand was sampled at the harvest stage for mineral analysis of the pulp and peel. The harvest stage of the bunches is reached when the median external ®nger of the fourth hand reaches the 34 mm grade.
2.3.2. Assessment of the susceptibility of fruit to anthracnose
At ¯owering, two median internal ®ngers of the third hand were inoculated by placing 25ml of a suspension ofC. musae containing 106conidia/ml. The strain ofC. musae used for these inoculations is sensitive to thiabendazole.
At the harvest stage, the two inoculated fruits were sampled and wounded by applying pressure to the inoculation zone. To create a uniform bruise and to take account of possible grade variations, each fruit was compressed to 15% of its grade by means of a piston with a rounded end, guided by a texture analyser. One of the two fruits was treated with thiabendazole by soaking it in a 500 ppm solution for 2 min. The fruits were stored at 13.58C for 10 days to simulate transport conditions. They were then placed for 10 days in a room at 218C, where they ripened naturally.
After these 20 days of storage, the length and breadth of the lesions were measured. The area of the lesion was estimated using the formula for the area of an ellipse. For each plot, the mean area of the lesions on untreated (SDN0) and treated (SDNZ) fruits was calculated.
2.4. Statistical analysis
The data were subjected to principal component analysis (PCA) and analysis of variance using the WINSTATic(1998) and SAS (1996) software.
Two PCAs were done; the ®rst with the soil mineral analysis data (PCA soil) and the second from the leaf analysis data (PAC leaf).
3. Results
3.1. Evidence for variation in fruit susceptibility
from the andosols of the leeward coast had smaller lesion areas; they seem to be less susceptible to wound anthracnose. A more erratic distribution occurs in the low-altitude soil (halloysitic and ferrallitic), with generally higher lesion areas. This variability is less for the fruit produced on the andosols of the windward coast and on the vertisols.
Fig. 2 shows the distribution of susceptibility of fruit treated with thiabendazole by soil type. These graphs illustrate the wide dispersion of the variable SDNZ; the lesion areas of treated fruit ranged from 48 to 370 mm2. As in the absence of fungicide treatment, the fruit produced on the andosols of the leeward coast seems to have less developed lesions. Similarly, most of the variability is found on the halloysitic and ferrallitic soils. For the fruit produced on the andosols of the windward coast and on the vertisols, this variability is less.
3.2. Halloysitic and ferrallitic soils
Fig. 3 presents the lesion sizes on treated fruit (SDNZ) in relation to the lesion areas on untreated fruit (SDN0) for the halloysitic and ferrallitic soil types. This graph shows that there is no correlation between the two variables. When the lesions on untreated fruits are larger than 600 mm2, the lesions on treated fruit can be very large (more than 300 mm2) or very small (less than 100 mm2).
3.2.1. Effect of mineral nutrition on fruit susceptibility
Fig. 4 shows the correlation pattern for the primary factorial plane of the PCA of soil variables, which accounts for 60% of the total inertia.
Axis 1 opposes pH, Ca content and CEC to the Mn content. Axis 2 opposes the C and N contents to those of potassium and phosphorus. The lesion areas, SDN0 and SDNZ, which enter as supplementary variables, tend to follow the alignment
of the variable Mn and to be inversely related to the variables pH and Ca. This graph seems to indicate a relation between the soil chemical characteristics and fruit susceptibility; the most susceptible fruits were produced on low-pH soils, with little Ca and a lot of available Mn.
Fig. 5 shows the correlation pattern for the primary factorial plane of the leaf PCA, which accounts for 48% of the total inertia.
All the variables are located on the same side of axis 1: most of the correlations are positive or absent. On axis 2, the Mn and Ca contents are opposed. As in the case of the soil, the supplementary variables relating to fruit susceptibility, SDN0 and SDNZ, tend to follow the line of the variable Mn and to be inversely related to Ca. Banana plants low in Ca and with high Mn contents thus produce the most susceptible fruit and vice versa.
3.2.2. Relationship between Mn content and fruit susceptibility
The PCA suggests the existence of a relationship between the plant Mn and Ca content and fruit susceptibility.
The leaf Mn contents (L_Mn) were grouped into three classes with equal numbers of samples. The mean Mn contents of the soil, the peel and the pulp and the mean lesion areas were calculated for each of these three classes (Tables 1 and 2).
The data in Table 1 show that there is a close relationship between leaf and green fruit Mn content, both for peel and pulp. There is no evidence for signi®cant differences between soil Mn contents, but nevertheless there appears to be a steady trend.
The analysis of the values for lesion area in relation to leaf Mn content shown in Table 2 con®rms the trends apparent from the PCA. For fruit not treated with thiabendazole (SDN0), analysis of variance indicates a signi®cant difference between the third class of L_Mn and the two other classes. The banana plants with the highest Mn levels have high SDN0 values. For fruit treated with thiabendazole (SDNZ), the differences are not signi®cant. However, the trend is still consistent: the highest SDNZ values correspond to the third class of L_Mn. The banana plants with the highest Mn contents thus produce the most susceptible fruit.
3.2.3. Relationship between Ca contents and fruit susceptibility
The PCA also suggests the existence of a relation between leaf Ca contents and lesion area (both for SDN0 and SDNZ).
The leaf Ca contents (L_Ca) were grouped into three classes of equal sample numbers. The mean Ca content of the soil, the peel and the pulp and the mean lesion area were calculated for each of the three classes (Tables 3 and 4).
Fig. 5. Primary factorial plane of the correlation pattern of the principal component analysis (PCA) of leaf variables. The soil variables marked L_xxx are active; the variables SDN0 and SDNZ are supplementary.
Table 1
Relation between leaf Mn content and Mn content of soil (S_Mn), pulp (CV_Mn) and peel (PV_Mn) of green fruit (means within a column followed by the same letter in brackets are not signi®cantly different according to Newman±Keuls' test of multiple comparison of means at the 5% probability level)
Class limits for L_Mn (ppm)
Class mean
S Mna (meq/100 g)
CV Mnb (in ppm)
PV Mnc (in ppm)
Mn(1): [194; 795] 576 0.213 (a) 24.1 (a) 126 (a) Mn(2): ]795; 1340] 1010 0.252 (a) 55.4 (b) 223 (b) Mn(3): ]1340; 2508] 1623 0.293 (a) 83.2 (c) 323 (c)
Prob>F 0.541 <0.001 <0.001
aThe Mn content of the soil. b
The Mn content of the pulp of the green fruit.
Table 2
Relation between leaf Mn content and fruit susceptibility to wound anthracnose in the absence (SDN0) and presence (SDNZ) of thiabendazole treatment (means within a column followed by the same letter in brackets are not signi®cantly different according to Newman±Keuls' test of multiple comparison of means at the 5% probability level)
Class limits for
aThe mean area of a lesion on untreated fruit after 20 days of storage. b
The mean area of a lesion on thiabendazole-treated fruit after 20 days of storage.
Table 3
Relation between leaf Ca content and Ca content of the soil (S_Ca), the pulp (CV_Ca) and the peel (PV_Ca) of the green fruit (means within a column followed by the same letter in brackets are not signi®cantly different according to Newman±Keuls' test of multiple comparison of means at the 5% probability level)
The Ca content of the soil.
b
The Ca content of the pulp of the green fruit.
c
The Ca content of the peel of the green fruit.
Table 4
Relation between leaf Ca content and susceptibility of the fruit to wound anthracnose in the absence (SDN0) and presence (SDNZ) of thiabendazole treatment (means within a column followed by the same letter in brackets are not signi®cantly different according to Newman±Keuls' test of multiple comparison of means at the 5% probability level)
Class limits
The mean area of a lesion on untreated fruit after 20 days of storage.
Table 3 provides evidence of a relationship between soil Ca levels and the levels of Ca in the reference leaf and the different organs analysed.
Table 4 shows the correlation between lesion area of treated and non-treated fruit and foliar Ca content. Fruit from plants whose leaves are poorest in Ca show the greatest susceptibility to C. musae.
4. Discussion
4.1. Evidence for variation in fruit susceptibility to C. musae
This diagnostic survey has provided evidence, not reported before, for wide variation in the susceptibility of bananas to wound anthracnose. This variation is found both on fruit treated with thiabendazole (with lesion areas varying over a 6-fold range) and on untreated fruit (with lesion areas varying 8-fold).
This variability has been demonstrated for the whole of Guadeloupe, where very different soil and climatic conditions are found, but also within the zone of halloysitic and ferrallitic soils. In general it seems that fruit from high-altitude plantations on andosols on the leeward coast are the least susceptible to wound anthracnose. The soil and climatic conditions therefore seem to have an in¯uence on fruit susceptibility, and presumably on the physiological component of quality potential. Similar results showing the effect of different growing districts on physiological characteristics of fruit quality were obtained for mango (Hofman et al., 1997).
For fruit from the low-altitude zone, the complete range of variability is observed. This, therefore, shows that it is not only the soil/climatic conditions which determine the susceptibility of the fruit. Within a relatively uniform growing region, the mineral status of the plant and the fruit, resulting from the cultural techniques applied in the ®eld, may have a considerable effect on the susceptibility of fruit to wound anthracnose.
The results obtained with treated fruit draw attention to the fact that the fungicide is not completely effective in preventing the development of the pathogen after damaging the fruit by compression, although the strain used for inoculation is sensitive to thiabendazole. This suggests that the fungicide is ineffective while the fungus is in the appressorium form or when it develops on damaged fruit.
4.2. Characterisation of the fruit which is most susceptible to C. musae
No correlation could be found between fruit susceptibility to C. musae and other fruit characteristics such as grade, texture (®rmness, hardness) and green life (results not shown).
The very marked features of the plots producing the most susceptible fruit (high leaf and fruit Mn content, Mn/Ca antagonism in leaves and fruit, acid soil) lead us to suggest certain hypotheses about the physiological mechanisms involved in the sensitisation to anthracnose.
4.3. Hypotheses about the mechanisms involved
4.3.1. Effect of calcium on fruit susceptibility
Calcium is implicated in certain fruit/pathogen interactions. In the case of the apple, calcium de®ciency causes weakening and sensitisation of the fruit to certain pathogenic agents (Conway et al., 1988; Conway, 1989). In fact it is often used in post-harvest treatments to control development of rots (Mason and Jeffries, 1993). For the banana/C. musaeinteraction, the analysis shows a relation between leaf Ca content and fruit susceptibility on both soil types studied. Although the high Ca contents limited the development of the lesions, calcium is not the only component involved in fruit susceptibility. In fact, fruit from plots on vertisols have very high Ca levels but are not particularly resistant. However, one cannot at present rule out the possibility that calcium has an effect on the growth of the lesions. Further experiments are needed to check this hypothesis.
On halloysitic and ferrallitic soil, low Ca contents result from the growing conditions on acid or compacted soil. These situations also result in high levels of plant Mn. Calcium may not have a direct effect, but is perhaps an indicator of growing conditions on soils which are too acidic or too compact.
4.3.2. Direct effect of Mn on fruit susceptibility
In the light of these results, one might suggest a direct effect of fruit peel Mn content on susceptibility to anthracnose. Manganese is often implicated in host± pathogen relationships (Graham et al., 1988), but it often confers upon plants resistance characteristics.
For theC. musae/banana interaction, it is necessary to verify whether or not Mn is an activator of parasitic expression.
4.3.3. Relationship between Mn content and ethylene
Ethylene can play a very important role at different levels in the host±pathogen interaction. It has been shown that this hormone activates germination and formation of appressoria in the case ofC. musae±banana andC. gloeosporioides± avocado interactions (Flaishman and Kolattukudy, 1994). Ethylene treatment can also induce development of lesions caused by C. gloeosporioides on tangerine, whereas they do not develop in the absence of this treatment (Brown, 1975).
It has been shown that the Mn2
ion stimulates ethylene synthesis (Konze and Kwiatkowski, 1981) and that it is essential for the oxidation of 1-aminocyclo-propane-1-carboxylic acid (ACC), which is the direct precursor of ethylene, into ethylene (Penel et al., 1990). Thus it is possible to surmise that after compression damage sustained after harvest, the fruit with the highest Mn contents might be able to produce larger amounts of ethylene, which would lead to more rapid development of lesions. This hypothesis will be tested experimentally.
Another hypothesis may be suggested: the high Mn contents observed in the plant might have arisen from stress situations which could reinforce the ability of the fruit to synthesise ethylene. In fact, in the case of soils containing manganese in the oxidised form, when rainfall is high and drainage inadequate, waterlogging conditions set in. These anoxic conditions lead to reduction of different forms of manganese into Mn2
(Patrick and Turner, 1968; Jones, 1972). Furthermore, the more acid the soils, the more the manganese is reduced (Gotoh and Patrick, 1972). It is in this form that it is absorbed by the plant. This waterlogging effect causing rapid Mn2
uptake by the plant has been demonstrated for rice (Clark et al., 1957), beans (Fergus, 1954), alfalfa (Graven et al., 1965) and oats (Godden and Grimmett, 1928). The effect has also been noted with banana plant (Marchal and FoureÂ, 1983; Dorel, 1993). Also, Dorel (1993) showed that compaction of a Guadeloupe andosol, causing restricted drainage and the appearance of reducing conditions, lead to massive absorption of Mn2
by the banana plant, accompanied by a lowering of the leaf Ca2
content.
The survey results are fully in accord with this hypothesis. In fact, during fruit growth rainfall was very high in the whole of the area under study (between 600 and 1100 mm during the period from ¯owering to cutting). It is thus quite conceivable that the Mn levels measured in the leaves are the re¯ection of growing conditions characterised by temporary anoxia.
For many plants, it has been shown that root anoxia causes ethylene synthesis by the plant shoots. In tomato, root anoxia, resulting from poor drainage, leads to an increase in root ACC synthesis, which is transported into the shoot where it can be oxidised (Jackson, 1985).
the anoxic stress and the capacity of the fruit to synthesise ethylene will be set up to test the validity of this hypothesis.
5. Conclusions
This diagnostic survey has, on the one hand, provided evidence for variability in the parasitic expression on fruits coming from a region which is uniform in terms of soil and climate, and on the other, demonstrated a relationship between the mineral status of the plant and the susceptibility of the fruit to anthracnose. The hypotheses about the physiological mechanisms underlying the susceptibility of fruit, notably manganese nutrition and the hydromorphic growing conditions, must be tested by experiments in controlled environments.
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