Bean common bacterial blight: pathogen epiphytic life and effect of irrigation practices
© Akhavan et al; licensee Springer. 2013
Received: 10 September 2012
Accepted: 4 February 2013
Published: 8 February 2013
In recent years, bean common bacterial blight (CBB) caused by Xanthomonas axonopodis pv. phaseoli (Xap) has caused serious yield losses in several countries. CBB is considered mainly a foliar disease in which symptoms initially appear as small water-soaked spots that then enlarge and become necrotic and usually bordered by a chlorotic zone. Xap epiphytic population community has a critical role in the development of the disease and subsequent epidemics. The epiphytic population of Xap in the field has two major parts; solitary cells (potentially planktonic) and biofilms which are sources for providing and refreshing the solitary cell components. Irrigation type has a significant effect on epiphytic population of Xap. The mean epiphytic population size in the field with an overhead sprinkler irrigation system is significantly higher than populations under furrow irrigation. A significant positive correlation between the epiphytic population size of Xap and disease severity has been reported in both the overhead irrigated (r=0.64) and the furrow irrigated (r= 0.44) fields.
KeywordsBean common Bacterial blight Epiphytic life Irrigation Disease severity Xanthomonas axonopodis pv. phaseoli
Pulse legumes are a very critical protein source in many developing countries. Among them, common bean (Phaseolus vulgaris L.) is consumed worldwide as a main source of protein, particularly in most Latin-American and African countries (Reynoso-Camacho et al. 2006).
Common bacterial blight symptoms
The causal agent of common bacterial blight
Cells of Xap can enter bean plants through openings such as stomata in leaves and other plant organs and through hydathodes at leaf margins, wounding of plants, such as that created by wind-blown soil particles can create pores for bacteria entry (Rudolph 1993). Bacterial cells are also readily transmitted mechanically, especially when plants are wet, while arthropods may transmit the bacterium from plant to plant (Kaiser and Vakili 1978; Lindemann and Upper 1985). The bean stem can also be penetrated in three ways: i.e., via the stomata, vascular system of the leaf and from infected cotyledons (Kaiser and Vakili 1978). Bacterial cells can also enter seeds via the vascular system or through the pedicel, while infection of the young plant occurs when internally infected seed germinates and the bacterium is transmitted from the seed to seedling (Gilbertson and Maxwell 1992; Saettler 1989a).
Favourable environmental conditions
In general, Xap causes very severe disease under high rainfall and humidity and warm temperature conditions (25-35°C) with maximum development occurring around 28°C (Gilbertson and Maxwell 1992; Saettler 1989a). Dissemination in the field is facilitated by wind-driven rain, while insects, people and contaminated equipment can be considered vectors (Gilbertson and Maxwell 1992; Saettler 1989a). Overhead sprinkler irrigation like high rainfall may provide a mean for bacterial dispersal, unlike furrow irrigation (EPPO/CABI 1996; Harveson 2009). Splashing water spreads the bacterial pathogen from diseased plants to healthy plants (Lindemann and Upper 1985). However, increases in relative humidity may not facilitate CBB epidemics. For example, it has been shown that a 20 percent difference in relative humidity (53% vs. 73%) did not significantly affect the Xap epiphytic population size and number of bacterial spots per plant in the greenhouse under controlled conditions (Akhavan et al. 2009a).
Survival of the pathogen in soil or plant debris is influenced by geographical area, climate, cultural practices, host genotypes, and bacterial strains (Karavina et al. 2008). Xap may survive in crop debris in the soil from season to season (Arnaud-Santana and Pena-Matos 1991; Gilbertson et al. 1990). However, such survival might not be realistic in most major bean growing areas of the world where the non-cropping period occurs under conditions where decomposition of crop debris is rapid and almost complete. Significant populations of Xap would not be expected to survive beyond six weeks under such conditions (Pernezny and Jones 2002) while in Zimbabwe, it was shown that Xap can over-winter between crops in crop residues; therefore, residues can be considered as sources of inocula for CBB in that country (Karavina et al. 2008). Xap can also survive and multiply as an epiphyte or resident on the shoot surfaces of weed hosts, primarily members of the legume family without showing symptoms (Pernezny and Jones 2002). In the Dominican Republic, Xap has been detected on Euphorbia heterophylla (L.), Acanthospermum hispidum (D.C.) and Portulaca oleracea (L.) (Angeles-Ramos et al. 1991). In Tanzania and Uganda, Saettler reported the pathogen on Chenopodium album (L.), Solanum nigrum (L.), Echinochloa crus-galli (L.), Beta vulgaris (L.) and Amaranthus retroflexus (L.) (Saettler 1989b).
The secret life of Xanthomonas axonopodis pv. phaseoli as a foliar bacterial pathogen on leaves (symptomless colonization of leaves and biofilm formation)
A large number of foliar bacterial pathogens are able to survive and multiply on aerial parts of plants without any visible symptoms (Andrews and Harris 2000). It was demonstrated previously that Xap could survive both epiphytically and endophytically (Weller and Saettler 1980). The epiphytic population community has a very critical major role in the development of the disease and subsequent epidemics (Beattie and Lindow 1999). This symptomless period can lead to such a huge bacterial population that disease can develop later when more favorable environmental conditions occur (Wilson et al. 1999).
Xap is a seed-borne pathogen with an epiphytic symptomless population and is able to go through a long epiphytic phase on bean plants (Beattie and Lindow 1995). In general, the epiphytic population of Xap in the field has two major parts; solitary cells (potentially planktonic) and biofilms. Using ERIC fingerprinting, it has been shown for Xap that strains in the two fractions of the population are genetically identical (Jacques et al. 2005). A similar result has been demonstrated for strains of plant-associated Pseudomonas fluorescens (Boureau et al. 2004). Biofilms which are present on the surfaces of leaves are similar to those in aquatic ecosystems and hospital environments and they include a large aggregation of bacterial cells embedded in polymeric materials like extracellular polysaccharides. Comprehensive reviews on biofilm formation by plant-associated bacteria were published by Danhorn and Fuqua (2007) and Morris and Monier (2003). Among the bacteria which can form biofilms, one which is closest to Xap, is X. campestris pv. campestris in which there is a cell to cell signalling procedure. This system is coded by rpf genes cluster, which were previously known as an important cluster in the pathogenicity of bacterium (Crossman and Dow 2004). These genes have a role in production of diffusible factors like butyrolactones. The most well-known chemical in biofilm formation in many bacteria is called Acyl Homoserine Lactones (AHL), but it has not been found in the genus Xanthomonas; even though this molecule has an important role in biofilm formation of another bean bacterial pathogen; Pseudomonas syringae pv. syringae which has the same ecological cycle as the causal agent of CBB (Cha et al. 1998; Crossman and Dow 2004; Dow et al. 2003). Instead of AHL, butyrolactones may act as signal molecules in quorum-sensing-like systems in Xanthomonas (von Bodman et al. 2003; Jacques et al. 2005). Regarding Xap, AHL has not been found in the bacterium population; however, butyrolactones have been confirmed to have a role in biofilm formation (Jacques et al. 2005).
Cell viability within biofilms and its role in providing inoculum
The microbial epiphytic community of Xap needs to reach a threshold to be able to enter the leaves through natural openings like stomata or wounds and establish an endophytic population which leads to development of the disease (Beattie and Lindow 1999). In Michigan, this threshold has been indicated to be 2.5*105 cfu per centimetre of bean leaves for Xap (Weller and Saettler 1980). It has been shown that the biofilm component looks stable following an initial period of growth of the Xap microbial community with population estimates of around 105 cfu per gram of bean leaves, which is likely under the population threshold needed for disease development (Jacques et al. 2005). In contrast, it seems that solitary cell components of the population are responsible for plant infection and these biofilms are a reliable source to support the development of solitary cells. Biofilms are not easily influenced by any antimicrobial factors while solitary cells can be harmed by any antimicrobial environmental factors. It is now clear that populations of solitary cells under unfavorable conditions are easily influenced by a number of abiotic and biotic factors (Monier and Lindow 2003). In general, solitary cells are sensitive to a series of environmental factors such as temperature and UV radiation and also antimicrobial chemicals. Bacteria harbored in biofilms can easily resist any copper based chemicals since the extracellular polysaccharides of the biofilm can bind the chemicals while most solitary cells are sensitive to these compounds (Costerton et al. 1995). In the same way, antibiotics may not be effective tools against biofilms. Regarding UV radiation of different wavelengths, bacteria in biofilms can be physically protected since the polysaccharides intercept the radiation and thus the embedded cells are not exposed to UV radiation (Davey and O’ Toole 2000). In the case of Xap, it has been demonstrated that desiccation stress had no significant effect on biofilm population size, while solitary cell populations are drastically decreased by desiccation, overall, aggregation of bacterial cells in biofilms can protect them against unfavourable environmental conditions (Jacques et al. 2005; Amano 2010) while the same conditions can be lethal for solitary cells. A similar trend has been demonstrated for another destructive bean bacterium; P. syringae pv. syringae (Monier and Lindow 2003). Cells of Xap aggregated in biofilms constitute a more stable population than do solitary cell populations. In Xap, biofilm population sizes are always lower than solitary population sizes; in contrast, it was shown that solitary cell populations which provide the bacteria that enter the plant through potential pores can multiply sharply when favorable conditions occur and even right after unfavorable circumstances (Jacques et al. 2005). This scenario raises the hypothesis that biofilms are sources for providing and refreshing the solitary cell components of epiphytic communities of plant pathogenic bacteria (Boureau et al. 2004; Jacques et al. 2005). For instance, it has been demonstrated that a reduction in hydric stress, i.e. excessive moisture, allowed solitary bacterial populations to increase again and it was suggested that biofilms were reservoirs for establishing solitary cell populations (Jacques et al. 2005).
The effect of irrigation system on epiphytic population size and disease severity
In the field, rainstorms can usually be related to rises in bacterial population sizes to the threshold level with subsequent rapid disease development. The effect of rainstorms on Xap epidemics could be result of a sudden decrease of temperature or a rapid inflow of water or raindrop occurrence (Hirano et al. 1996; Jacques et al. 2005). It has been shown that epiphytic population of Xanthomonas campestris pv. vesicatoria, the cause of pepper bacterial leaf spot increased drastically following a 2-day wind-driven rain (Bernal and Berger 1996). Overhead sprinkler irrigation seems to have similar effects on bacterial population sizes as rainstorms. It has been demonstrated that the type of irrigation had a significant effect on epiphytic populations of Xap. Although the bacterial populations were the same size at the beginning, the mean epiphytic population size in the field with an overhead sprinkler irrigation system was 1.04*106 colony forming unit per each squared centimeter of bean leaves (cfu/cm2) while for a furrow irrigation system, population size was 4.89*104 cfu/cm2 (Akhavan et al. 2009a).
It has been revealed that irrigation type significantly influenced disease severity. Disease severity means were 5.8 and 2.8 in fields with overhead sprinkler irrigation and furrow irrigation, respectively using the standard system for the evaluation of bean germplasm with 1 as “no visible disease symptoms” and 9 as “very severe disease symptoms”(Schoonhoven and Pastor-Corrales 1994; Akhavan et al. 2009a). In addition to dispersing bacterial cells and helping them to reach healthy plants as the key factor, and promoting release of leaf nutrients to the microbial community, overhead sprinkler irrigation can generate a film of water over the leaf surface including stomata, providing the symptomless epiphytic populations with a bridge to enter the plant resulting in disease symptoms development (Carvalho et al. 2011). Previously, it has also been shown that Asiatic citrus canker was more severe when applying overhead irrigation system which also increased the incidence of this disease caused by Xanthomonas axonopodis pv. citri (Pruvost et al. 1999). In contrast, Wheeler et al. (2007) showed that overhead irrigation increased disease incidence of cotton bacterial blight by Xanthomonas axonopodis pv. malvacearum in a partially resistant cultivar; PM 2200 RR compared with drop hoses, while irrigation method did not influence disease incidence for the susceptible cultivar; PM 2326RR.
Epiphytic population size, disease severity and yield correlations: a brief conclusion
A significant (P<0.05) positive correlation between the epiphytic population size of Xap and disease severity in both the overhead irrigated field (r=0.64) and the furrow irrigated field (r= 0.44) has been reported (Akhavan et al. 2009a). The reason for the higher correlation coefficient with the overhead sprinkler irrigation system can be due to the effect of this type of irrigation on bacterial penetration to interior leaf spaces and subsequent development of disease. Similar results have been reported by other studies on the effect of windblown rain fall (Gilbertson and Maxwell 1992). Significant positive correlations between bacterial populations and disease severity have also been shown in other studies. For example, the epiphytic population of X. campestris pv. vesicatoria, the causal agent of tomato bacterial spot, was positively correlated with plant defoliation as a result of disease development (McGuire et al. 1991). Previously, Lindemann et al. (1984) also showed that the severity of brown spot of bean was correlated more consistently with epiphytic Pseudomonas syringae pv. syringae population sizes than with disease incidence. A significant (P<0.05) negative correlation between disease severity and seed yield per plant for both the furrow irrigated field (r=- 0.59) and the overhead sprinkler irrigated field (r=- 0.68) has also been reported (Akhavan et al. 2009a). Furthermore, in both systems, there was a significant (P<0.05) negative correlation between disease severity and total seed yield, but the coefficient correlation was higher under overhead sprinkler irrigation (r=- 0.83) compared to furrow irrigation (r=-0.66). This difference is likely due to more severe disease in the field under overhead sprinkler irrigation system. Since the only difference between the two fields was the type of irrigation method, it can be interpreted that the overhead sprinkler system provided several factors that encouraged epiphytic populations to increase and to establish an endophytic population of Xap. Overhead irrigation can provide an ideal multiplication site, i.e. a thin layer or film of water on the bean leaf surface, while also disseminating the pathogen from diseased to healthy plants. Overhead sprinkler irrigation may also help the epiphytic population of Xap to establish an aggressive endophytic population by facilitating the entry of bacterial cells through leaf openings followed by symptom development.
Common bacterial blight
- Xap :
Xanthomonas axonopodis pv. phaseoli
We wish to express our appreciation to Mr. Mojtaba Emam-Jomeh, Mr. Valiollah Rahmati and Mr. Esmaeel Azizi for excellent field and technical assistance. This work was funded by a grant from the graduate school of Isfahan University of Technology in Iran.
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