- Email: [email protected]
Bean root rot management: Recommendations based on an integrated approach for plant disease control
Rhizosphere 4 (2017) 48–53
Contents lists available at ScienceDirect
Rhizosphere journal homepage: www.elsevier.com/locate/rhisph
Bean root rot management: Recommendations based on an integrated approach for plant disease control
MARK
⁎
Bita Naseria, , Roghaie Hemmatib a b
Plant Protection Research Department, Kermanshah Agricultural & Natural Resources Research & Education Center, AREEO, Kermanshah, Iran Department of Plant Protection, Faculty of Agriculture, University of Zanjan, Iran
A R T I C L E I N F O
A B S T R A C T
Keywords: Epidemiology Fungi Rhizosphere Root rot
A systematic understanding of agro-ecosystems suppressing soil-borne plant pathogens is one of the most desired objectives in plant disease management. Large-scale detection of agro-ecological descriptors of variations among crop-disease pathosystems will certainly save time to screen a wider range of conditions and identify more effective factors, to further examine at smaller scales, and to develop an integrated crop-disease management program. Therefore, a fairly comprehensive array of agronomic and environmental traits was examined across commercial fields cultivated with the common bean, Phaseolus vulgaris L. Then, ten factors chosen according to practical relevance to root rot epidemics and bean production were studied in laboratory, greenhouse or experimental field. The advantages and findings of this case study as a useful framework in plant pathology were discussed in this short review.
1. Introduction The common bean (Phaseolus vulgaris L.) is the most important food legume in human nutrition worldwide (Broughton et al., 2003). Dry beans were harvested from 30,612,842 ha globally, which produced 26,529,580 t of seeds (FAOSTAT, 2014). The production of bean crops has been mainly threatened by root rot pathogens in most bean growing areas around the world such as northeast Brazil, Mexico, Nicaragua, coastal Peru, and the United States (Abawi, 1989). However, there is no concise information on global yield losses due to root rots in bean crops. Due to difficulties in incorporating root rot resistance into bean cultivars (Miklas et al., 2006), non-economic and ineffective disease control using fungicides is commonly applied by bean growers. Thus, across bean cropping systems, root rot pathogens continue to prevent commercial bean production. It seems that a study framework is required to gain adequate information based on which more reliable and influential recommendations on root-rot-control can be made to bean farmers. In the present review, findings obtained at various scales from region to experimentalplot, to greenhouse and laboratory studies on bean production and root rots were integrated to develop a more effective and sustainable disease and crop management program. In the first step, associations of a large number of agro-ecological variables with the bean-root-rot pathosystem
were explored on a regional or macro-scale basis. Then, such systematic understanding of highly heterogeneous agro-ecosystems allowed the selection of more influential factors to be further examined at small scale. With this approach, uncertainties at regional scale can be addressed at either field-plots or controlled environment scales. This study framework as one of the main promising outcomes of our multi-scale findings has very important significance to advancing the epidemiology of bean root rots, ensuring the efficiency of crop and disease management strategies, saving time and reducing expenses by focusing research on effective management. In Iran, beans are widely cultivated over more than 109,000 ha of irrigated lands annually (Anonymous 2014). Zanjan province is the second major contributor to dry bean production in Iran, with an average production of 2519 kg/ha harvested from 13,280 ha in 2014 (Anonymous, 2014). A number of recent reports from this area demonstrate that soil-borne root rot diseases are threatening bean production. In Zanjan, Fusarium solani, Rhizoctonia solani, Macrophomina phaseolina and F. oxysporum, are the predominant root rot pathogens causing up to 65% yield losses in heavily infected bean crops (Naseri 2007, 2008a, 2008b; Naseri and Moradi, 2007). The distribution of root rot pathogens across the region and the significant yield loss encouraged a systematic epidemiological understanding of bean root rots prevalent in agro-ecosystems to provide recommendations from an
Abbreviations: CRR, Charcoal root rot caused by Macrophomina phaseolina; FRR, Fusarium root rot by Fusarium solani; FW, Fusarium wilt by F. oxysporum; RRR, Rhizoctonia root rot by Rhizoctonia solani ⁎ Corresponding author. E-mail address: [email protected] (B. Naseri). http://dx.doi.org/10.1016/j.rhisph.2017.07.001 Received 10 June 2017; Received in revised form 5 July 2017; Accepted 5 July 2017 Available online 06 July 2017 2452-2198/ © 2017 Elsevier B.V. All rights reserved.
Rhizosphere 4 (2017) 48–53
B. Naseri, R. Hemmati
integrated disease-management program. Therefore, Zanjan's main bean growing areas were chosen for this case study.
Table 1 Soil and agronomic parameters that intensified root rot epidemics in commercial bean fields.
2. Description of study sites and region A representative subset of 122 common bean fields (35 in 2008 and 87 in 2009) ranging from 0.5 to 14 ha in size were randomly selected across the main bean growing area of Zanjan province in order to include all common agronomic and environmental conditions. The study region was located between longitudes 48 °20′–49°30′W to E and latitudes 36°–36°40'S to N. The normal bean growing season in Zanjan involves planting in mid to late spring (May–June) and harvesting in late summer (September). Bean growers were queried about their applications of fungicides and herbicides, planting date and rotation program. Then, commercial bean fields were examined for bean market class, planting depth, rhizobial nodulation and root rot diseases at vegetative, flowering, and pod maturity stages. The complete details on confirmation of major root-rot-pathogen infections and pathogenicity tests, disease assessments, status of rhizobial symbiosis were provided in previous reports (Naseri, 2008b, 2014a; Naseri and Marefat, 2011). At vegetative and pod maturity stages, field soils were sampled and analyzed according to standard methods as Naseri (2013a) described earlier. The soil organic matter, pH, clay, sand and silt in the fields were within the 0.4–1.8%, 7.0–7.9, 14–53%, 4–65% and 15–48% ranges, respectively. The field-plot and greenhouse experiments were conducted in the Agricultural and Natural Resource Research Center located at Kheirabad region (36°30’N, 48°47’E, 1770m a.s.l.) during 2009 and 2010. Mean annual rainfall and temperature in Zanjan, with a cold semi-arid climate and a hot and dry season from June to September, is 315.4 mm and 11.7 °C, respectively (Zanjan Meteorological Office 2009).
Variable
Fusarium root rot
Rhizoctonia root rot
Charcoal root rot
Fusarium wilt
Bean class Early-season drought Irrigation interval Irrigation system Field size Herbicide Planting density Weeds
Pinto, white NSa
White Applied
Pinto, white NS
Pinto, white NS
2–3 days
2–3 days
NS
NS
Furrow
Furrow
NS
NS
NS Not applied 8–17 plant/ quadratb > 16 weed/ quadrat May 2nd wk > 5 cm NS 30–48% NS Mechanical
NS Not applied 8–17 plant/ quadrat > 16 weed/ quadrat May 2nd wk > 5 cm NS 15–30% 45–65% Mechanical
large Not applied NS
NS Applied NS
NS
NS
May 2nd wk > 5 cm NS NS 45–65% Mechanical
May 2nd wk > 5 cm 35–53% 30–48% NS Mechanical
50–500 kg/ha
50–500 kg/ha
50–500 kg/ha
Absent
Absent
50–500 kg/ ha Absent
Treated Non-treated
Treated Non-treated
NS NS
NS NS
Raised Barley, bean, tomato, wheat 0.4–0.8%
Raised Legumes
NS Legumes
0.4–0.8%
NS Legumes, cereals NS
NS
Not applied 7.0–7.5
Not applied 7.5–7.9
NS 7.5–7.9
NS 7.5–7.9
Planting date Planting depth Soil clay Soil silt Soil sand Sowing technique Urea Rhizobial nodule Soil-fungicide Seedfungicide Seedbed Previous crop Organic matter Manure Soil pH
3. Synthesis of regional findings Epidemic levels and consequent yield reductions differ between bean fields of the same area, as well as in the same field from season to season. A considerable part of such differences corresponded with variations in agronomic and environmental conditions, which are known as influential factors on the root-rot–bean pathosystem from planting to harvesting time (Table 1). More severe Fusarium root rot (FRR) epidemics occurred in pinto and white beans, frequent irrigations at 2–3 days intervals at flowering growth stage, denser plant population, earlier and deeper sowings, rotations with barley, bean, tomato or wheat, overuse of urea (50–500 kg/ha), soils with greater silt content (30–48%), soil treatment with fungicides, low soil organic matter, nonnodulated roots, pH levels of 7.0–7.5, lacking herbicide and manure use, sowing non-fungicide-treated seeds, mechanical sowing, furrow irrigation, and planting on raised seedbeds (Naseri, 2010; Naseri and Marefat, 2011; Naseri, 2014a; Naseri et al., 2016). Rhizoctonia root rot (RRR) epidemics were restricted in red beans, drought-free fields, irrigations at 6–9 days intervals, shallow planting, lower plant and weed densities, rotations with potato and tomato, non-fungicide-treated soils, at a level of 4–25% sand content, high soil organic matter, highly nodulated roots, lower soil silt, lower soil sand and pH, lacking urea application, later plantings, manure application, sprinkler irrigation, manual cultivation, weed control using paraquat or bentazon (Naseri, 2013a, 2013c, 2016; Naseri and Moradi, 2015). Large field size, high soil pH and sand, early and deep planting, lacking herbicide use, rotations with legumes or cereals, growing pinto and white beans, nonnodulated roots, mechanical cultivation and urea overuse intensified charcoal root rot (CRR) epidemics (Naseri, 2014b). Lower Fusarium wilt (FW) levels were associated with postponing sowing, growing red beans, lacking urea application, rotations with potato and tomato, shallow planting, neutral soil pH, manual sowing, lower soil clay and silt (Naseri, 2014c; Naseri and Tabannde, 2017). Higher yield levels were detected in red beans, lower root rots, proper planting date and
a b
Absent
NS means non-significant association. Quadrat size was 0.25 m2.
density, lower weed density, soils with lower sand (25–45%) and silt (15–30%) contents, greater soil organic matter (1.2–1.8%), higher rhizobial nodulation, fungicidal treatment of seed, lacking urea fertilization, herbicide and manure applications, manual sowing, sprinkler irrigation, rotations with potato and tomato (Naseri and Marefat, 2011; Naseri, 2014a; Naseri and Tabannde, 2017). Understanding how strongly farmers’ operations interact with the plant-disease pathosystem is important if farmers are to achieve recommendations on efficient cultural strategies to control diseases and improve yield. Indeed, this information should help identify agronomic practices that might restrict root rots establishment on bean crops and thus lead to the selection of most relevant root-rot-control strategies for further field experimentations with the purpose of saving study time. However, information on interrelationships among bean production, root rots epidemics, and prevalence of pathogens in roots, seeds and soils was also necessary to optimize control methods. Therefore, attempts were made to meet these research requirements. The soil population and frequency of pathogens isolated from roots and seeds differed between pathogens and bean fields. F. solani was the most prevalent pathogen isolated from rotted roots and seeds and bean-field soils in comparison with R. solani, M. phaseolina and F. oxysporum (Naseri, 2008b; Naseri and Mousavi, 2015). Macro-scale findings revealed that the root rot index corresponded more strongly with root and seed infections compared to soil populations. This indicates that the infestation of bean seeds due to late-season epidemics occurs more commonly than the soil-borne infection of bean roots in the pathosystems studied. Therefore, the fungicidal treatment of bean seeds to reduce seedborne infections in bean crops should be considered prior to 49
Rhizosphere 4 (2017) 48–53
B. Naseri, R. Hemmati
4.1. Bean market class
the control of soil-borne pathogens in the development of disease management programs for the region. Indeed, CRR, FRR and RRR epidemics were recognized as more important determinants of seed losses in the bean-root-rot pathosystem (Naseri and Mousavi, 2015). There were also associations among the four pathogens infecting either roots or seeds. Knowledge of the prevalence of root rot pathogens in the root, seed and soil is useful to determine the most prominent indicators of the presence of different pathogens in the field, leading to improve the efficiency of root rot control programs. Although Naseri and Mousavi (2015) reported stronger relevance of seed infections to root rot epidemics compared to soil populations, rootrot-control methods still benefit from lowering pathogens densities in field soils. As the next step in bean-root-rot epidemiology, understanding the interactions of various agronomic and soil properties with the prevalence of root rot pathogens in the soil on a regional basis was also required to develop more efficient disease-management programs. Based on multiple assessments mode during the growing season, the populations of these soil-borne pathogens in field soil varied among pathogen species and experimental sites (Naseri and Mousavi, 2015). Thus, attempts were made to elucidate how much of this variation can be explained by differences in the application of fertilizers and herbicides, market classes of beans, previous crop, soil texture, soil electrical conductivity and pH. Lower populations of F. oxysporum and M. phaseolina in farm soils were detected in red beans, herbicide and P-fertilizer applications, clay-loamy soils, greater soil-sand content, higher soil pH (7.5–7.9), larger farms, lack of urea use, and the Kheirabad region. The density of F. solani in soil was associated with bean class, herbicide and P-fertilizer. Region, soil pH and sand affected soil populations of R. solani. A lower total population of four pathogens was observed in red beans, larger fields, the Kheirabad and Khodabandeh regions, P-fertilization, lack of trifluralin and urea application, and at higher levels of electrical conductivity, soil pH and sand (Naseri and Hamadani, 2017). These preliminary assumptions on soil-borne pathogens in interaction with various agro-ecological characteristics should assist with choosing more effective factors for plot-scale and controlled-environment studies to manage disease and improve yield. In other words, this knowledge proceed identifying important factors that affect inocula dynamics in farm soils needed for experimental designs and inducing disease-suppressiveness of farming soils.
Our macro- and plot-scale findings were in agreement regarding the lowest FRR and RRR at pod maturity stage and the highest level of seed production in red beans than pinto and white beans (Naseri, 2013b, 2013c; Naseri and Marefat, 2011; Naseri and Mousavi, 2013). 4.2. Fungicidal treatments of seeds Treatment of bean seeds with fungicides corresponded with remarkable improvements in productivity and reductions in the progression of CRR, FRR and RRR epidemics in commercial bean crops (Naseri et al., 2016; Naseri and Moradi, 2014, 2015). In the greenhouse study, pre-treatment of bean seeds with fungicide improved bean productivity and reduced single or multiple FW, FRR and RRR infections (Faraji, 2013). Our macro-scale findings on the benefits of the fungicide-treated seeds to bean cultivation, which was confirmed by Faraji's (2013) studies, support previous small-scale experiments (Gupta et al., 1999, Dorrance et al., 2003; Papavizas and Lewis, 1975; Valenciano et al., 2006). Thus, we recommend that bean seeds should be treated with a proper fungicide prior to planting. 4.3. Fungicidal treatments of soil Due to the noticeable association of fungicidal treatment of field soils with more severe FRR and RRR epidemics (Naseri, 2013a, 2014a), the fungicide application looked a faulty strategy to improve the sustainability of bean farming systems. In Zanjan, benomyl was the most commonly used fungicide by bean growers followed by mancozeb (Naseri, 2013a). In addition to suppressing beneficial antagonists such as Trichoderma spp. following extensive soil-application of fungicides in particular Benomyl (Papavizas et al., 1982; McAllister et al., 1994; McLean et al., 2001), the over-use of this fungicide induces fungicidal resistance in plant pathogenic fungi (Carling et al., 1990; Weiland and Halloin, 2001). Therefore, a number of controlled-environment studies were performed to advance our understanding of the fungicide-root-rot interaction. Faraji (2013) found that complete inhibition of hyphal growth for F. oxysporum, F. solani and R. solani on agar culture media amended with 6, 8 and 10 × 10−3 g l−1 concentrations of benomyl. However, the 2 g l−1 concentration of fungicide failed to control separate infections by F. solani or R. solani and the combination of FW, FRR and RRR, when added to the irrigation water of bean seedlings in the greenhouse (Faraji, 2013). In conclusion, despite an earlier report of successful control of mung-bean-RRR by benomyl (Kataria and Grover, 1976), chemical control of bean root rots on the expanding roots is uneconomical and therefore impractical under commercial production conditions. Thus, we recommend bean growers to avoid fungicidal treatment of field soils for root-rot-control purposes.
4. Verification of large-scale findings It is believed that the epidemiological knowledge obtained from a highly diverse range of commercial agro-ecosystems extends the understanding gained through small scale studies on a pathosystem (Naseri, 2013a). Despite disadvantages of complicated impacts of diverse agro-ecological properties, surveying commercial fields provide comprehensive information on a large number of crops grown under highly different compositions of agricultural practices and environmental conditions (Fernandez et al., 2007). The conclusions drawn from such regional studies must improve the efficiency of crop management programs (Williams et al., 2009) and applicability of findings in different areas. Although advanced information on soil properties such as soil texture and pH on pathosystems is beneficial to the development of disease control strategies, the plot-scale studies were concentrated on those important agro-ecological factors which could be easily manipulated by farmers without extra inputs. Thus, bean class, herbicide, planting date and depth, which also indicated strong linkages with the development of root rot epidemics at large scale, were selected for plot-scale studies. Fungicidal treatments of seeds and soil, genetic diversity of the pathogen, rotational crops, rhizobial nodulation on bean roots, and temperature were investigated in either greenhouse or laboratory.
4.4. Genetic diversity of the pathogen In the study of population diversity of F. solani f.sp. phaseoli in Zanjan province, Iran, there was phenotypic and genotypic diversity among the 30 pathogen isolates collected from commercial bean fields. DNA fingerprinting patterns from both RAPD and ERIC primers demonstrated high genetic diversity of isolates, which had no significant difference in pathogenicity to bean seedlings in the greenhouse (Khodagholi et al., 2013). The vegetative compatibility of 42 F. solani f.sp. phaseoli isolates collected from Zanjan's bean growing area demonstrated that majority of the pathogen isolates were compatible (Safarloo, 2011). The ability of fungal isolates to form heterokaryons with each other was tested based on hyphal pairings of complementary nitrate-nonutilizing (nit) mutants. Therefore, the high genetic diversity of F. solani f.sp. phaseoli populations (Khodagholi et al., 2013) with the notable ability to form heterokaryon and exchange genetic information (Safarloo, 2011) might explain why no resistant cultivar was found in 50
Rhizosphere 4 (2017) 48–53
B. Naseri, R. Hemmati
FRR, FW and RRR epidemics, and improved yield across a highly diverse agricultural and soil conditions (Naseri, 2013a, 2014b; Naseri and Marefat, 2011; Naseri and Tabande, 2017). Moreover, sowing depth accounted for 28–49% of variations in FRR epidemics across 122 commercial bean fields (Naseri and Marefat, 2011). These profound interactions of planting depth with FRR and RRR were confirmed at the experimental-plot scale (Naseri, 2014b; Naseri and Mousavi, 2013). An Australian study also reported shallow seeding at 2.5 cm depth as the most effective cultural method to control bean root rot, in comparison with hilling depth and fungicidal soil-treatment (Brien et al., 1991). Therefore, we recommend that shallow sowing at 5 cm is recognized as crucial in an integrated root rot control program for bean production.
the study region. As a result, resistance to diseases was considered of minor importance in the development of an integrated program to manage bean root rots. 4.5. Herbicide Herbicide stress is known to influence infections by soil-borne pathogens. Applications of trifluralin and bentazon intensified bean FRR when there was no weed in pot experiments (Mussa and Russell, 1977). Trifluralin increased herbicide-induced susceptibility of potted beans to RRR (Katan and Eshel, 1973; Cull, 1975; Wrona et al., 1981) and soybeans to FW (Carson et al., 1991). Paraquat decreased Rhizoctonia foliar blight in potted soybeans (Black et al., 1996). At plot scale, soybean CRR reduced by applying trifluralin (Canaday et al., 1986) which can enhance soil microbial populations such as actinomycetes (Tang et al., 1970) and then possibly reduce pathogen competition ability in the rhizosphere. In this study, both regional and plot-scale attempts were made to determine whether herbicide applications intensify root rots by exposing bean roots to herbicide stress or restrict the disease epidemic by removing weeds as possible competitors and pathogen reservoirs. The application of farmers’ choice herbicides (trifluralin, paraquat and bentazon) decreased over-season occurrence of CRR, FRR and RRR epidemics and improved productivity in commercial bean fields (Naseri, 2014b; Naseri and Moradi, 2015; Naseri et al., 2016). It could be that without herbicide application, denser weed populations intensified root rot epidemics (Naseri and Marefat, 2011; Naseri, 2013b). Furthermore, the removal of weeds with herbicides may have lowered the pathogen population and distribution in the soil reducing epidemics. Our regional findings were confirmed by the plot-scale research which indicated lower root rots and higher seed production following trifluralin applications (Naseri, unpublished data). Despite different cropping properties, environmental conditions, pathogens populations, bean and pathogen genotypes used, the large-scale results are also in agreement with previous small-scale findings (Canaday et al., 1986; Black et al., 1996). Therefore, we recommend that efficient weed management should be a major part of the bean cropping program.
4.8. Rhizobial nodulation on bean roots The nodulation of bean roots by rhizobial bacteria restricted FRR, RRR, CRR and FW epidemics and improved productivity under highly diverse microbial and agro-ecological traits on a regional basis (Naseri, 2013a, 2014a; Naseri and Mousavi, 2014; Naseri and Moradi, 2014; Naseri and Tabande, 2017). These regional-scale findings were supported by small-scale findings in experimental pots or plots on the reduction of FRR and improvement of bean biomass (Hassan Dar et al., 1997), or yield (Estevez de Jensen et al., 2004), suppression of bean RRR (Blum et al., 1989; Ehteshamul-Haque and Ghaffar, 1993; ÖzkoC and Delıvelı, 2001) and soybean CRR (Ansari, 2010). Our regional findings were confirmed by additional greenhouse studies which demonstrated that seed inoculations with Rhizobium sp. as the most prevalent bacterial symbiont, both improved bean production and reduced FRR (Kalantari, 2011). Although the significant linkage of rhizobial symbiosis on bean yield was detected at both small and large scales (Kalantari, 2011; Naseri, 2014a), insufficient nodulation in 88% of the commercial bean fields might be partially due to the iron deficiency in calcareous soils of the study region (Naseri, 2013a) that reduces legume-rhizobia symbiosis and consequently plant growth (Slatni et al., 2008). Another explanation for low nodulation in Zanjan bean crops may be attributed to 66.4% of fields fertilized with excess urea (50–500 kg/ha, Naseri and Marefat, 2011) which has been linked to reduced rhizobial nodulation in Legumes (Zhang and Smith, 2002). Improvement of effective rhizobial nodulation should be a major objective in bean crop agronomy. We recommend that farmers use either bean seeds pre-coated with rhizobia or amend the soil with biofertilizers including these beneficial microorganisms. This also merits further investigation.
4.6. Planting date Likewise, our plot-scale experimental results which confirmed earlier regional scale reports of more severe early-season FRR and RRR epidemics and lower seed production occurred in early-planting in May than later-planting in June (Naseri, 2013b,c; Naseri and Marefat, 2011; Naseri and Mousavi, 2013). This conclusion is in agreement with other small-scale results of more severe root rots at lower temperatures and higher moisture levels (Abawi, 1989; Bolkan et al., 1974; Sippell and Hall, 1982; Burke and Miller, 1983). According to our macro-scale findings, more severe early- and late-season CRR epidemics occurred in early-sown bean fields following a cooler and moister climate in May than in June (Naseri, 2014b). This regional finding is in agreement with the small-scale observation of severe CRR under cooler and moister conditions in another study (Dhingra and Chagas, 1981). Although moving the planting date from early spring to early winter in Spain intensified FW epidemics in chickpea plots (Navas-Cortés et al., 1998), postponing sowing date from early May (mid-spring in the study area) to late June (early summer) at shallow depths decreased bean-FW epidemics in Zanjan, Iran (Naseri, 2014c). This disagreement might be due to the differences in environmental conditions in particular moisture and temperature at planting, host and pathogen genotypes. Therefore, we recommend that seeding occur after cool and wet periods are passed. Further investigation on appropriate environmental conditions for both plant-growth and pathogen-attack is required.
4.9. Rotational crops Another easily achievable agronomic control of root rot diseases is rotation of beans with appropriately chosen crops. Therefore, we analyzed our regional data for correlations and significant associations of the preceding crop with intensity of bean root rot epidemics. Subsequently, the disease establishment was measured in the greenhouse on a manageable number of commonly cultivated crops in the region, which could be used as potential alternate crops in a rotation program. To meet this requirement, three two-week-old seedlings in each of three replicate pots per test plant were inoculated with a conidial suspension (25 × 106 conidium ml−1 concentration) and disease symptoms were recorded after five weeks. Based on the greenhouse studies, F. solani f.sp. phaseolin can incite FRR symptoms on alfalfa, bean (red, pinto, and white cultivars), chickpea, lentil, faba bean, and sainfoin, but not in wheat (Khodagholi et al., 2013). Furthermore, the highest FRR was detected on chickpea, lentil, faba bean, while alfalfa and red bean had the lowest disease severity levels (Khodagholi et al., 2013). Growing beans following maize and potato decreased the development of FRR and RRR epidemics in commercial fields, respectively (Naseri and Marefat, 2011). More severe CRR epidemics occurred in beans rotated with legumes or cereals, than in potato or tomato (Naseri,
4.7. Planting depth Our regional studies showed that shallower planting reduced CRR, 51
Rhizosphere 4 (2017) 48–53
B. Naseri, R. Hemmati
References
2014b). However, the similarity of CR, FRR, RRR disease severity and bean yield levels when grown following alfalfa, barley, and wheat, to bean mono-croppings (Naseri and Marefat, 2011) disagrees with several field-plot-scale studies by others carried out elsewhere. Rotations of beans with maize, wheat or barley (Abawi and Pastor Corrales, 1990; Maloy and Burkholder, 1959), or alfalfa (Román-Avilés et al., 2003) lowered root rots and enhanced yield in parts of Africa and America. Moreover, maize debris lowered RRR even nearly a year after soil incorporation in both the greenhouse and field (Manning and Crossan, 1969). The over-use of urea in most of the commercial fields (Naseri and Marefat, 2011) might have caused similar disease and yield levels in beans grown after barley and wheat compared to bean-monocultures. It was previously shown that N-fertilizers can reduce the benefits of cereal residue in the soil (Huber, 1963). Thus, our regional and smallscale findings support the recommendation from Bruehl (1989) that crop rotation with both weed and insect control should be used as a major method to manage bean root rots. We therefore recommend that bean rotations should be implemented to avoid and manage root rot occurrence and intensity. Additional studies will be required to describe more precisely a standard recommended rotation schedule, as there remains confounding field and environmental factors to control for, at least for this region.
Abawi, G.S., 1989. Root rot. In: Schwartz, H.F., Pastor Corrales M. (eds.) Bean Production Problems: Disease, Insect, Soil and Climatic Constraints of Phaseolus Vulgaris. Centro Internacional de Agricultura Tropical, Cali. Abawi, G.S., Pastor Corrales, M.A., 1990. Root Rots of Beans in Latin America and Africa: diagnosis, Research Methodologies, and Management Strategies. Centro Internacional de Agricultura Tropical, Cali. Anonymous, 2014. Agricultural Production Report in 2007 and 2014. The Iranian Ministry of Agriculture, Tehran, Iran. Ansari, M.M., 2010. Integrated management of charcoal rot of soybean caused by Macrophomina phaseolina (Tassi) Goid. Soybean Res. 8, 39–47. Black, B.D., Russin, J.S., Griffin, J.L., Snow, J.P., 1996. Herbicide Effects on Rhizoctonia solani in vitro and Rhizoctonia foliar blight of soybean (Glycine max). Weed Sci. 44, 711–716. Blum, L.K., Frey, S.D., Soto, G., 1989. Effect of fluorescent-pigment producing Rhizobium on the severity of Rhizoctonia solani seed and root rot of Phaseolus vulgaris. A paper presented at a symposium held at the Beltsville Agricultural Research Center (BARC), held on 8–11 May. Bolkan, H.A., Wenhara, H.T., Milne, K.S., 1974. Effect of soil temperature on severity of Rhizoctonia solani infection on potato shoots. Plant Dis. Rep. 58, 646–649. Brien, R.G.O., Hare, P.J.O., Glass, R.J., 1991. Cultural practices in the control of bean root rot. Aust. J. Exp. Agric. 31, 551–555. Bruehl, G.W., 1989. Integrated control of soilborne plant pathogens: an overview. Can. J. Plant Pathol. 11, 153–157. Broughton, W.J., Hernandez, G., Blair, M., Beebe, S., Gepts, P., Vanderleyden, J., 2003. Bean (Phaseolus spp.)-model food legumes. Plant Soil 252, 55–128. Burke, D.W., Miller, D.E., 1983. Control of Fusarium root rot with resistant beans and cultural management. Plant Dis. 67, 1312–1317. Canaday, C.H., Helsel, D.G., Wyllie, T.D., 1986. Effects of herbicide-induced stress on root colonization of soybeans by Macrophomina phaseolina. Plant Dis. 70, 863–866. Carling, D.E., Helm, D.J., Leiner, R.H., 1990. In vitro sensitivity of Rhizoctonia solani and other multinucleate and binucleate Rhizoctonia to selected fungicides. Plant Dis. 74, 860–863. Carson, M.L., Arnold, W.E., Todt, P.E., 1991. Predisposition of soybean seedlings to Fusarium root rot with trifluralin. Plant Dis. 75, 342–347. Cull, S.W., 1975. Physiological Studies on Trifluralin-induced Susceptibility of Phaseolus vulgaris to Post-emergence Damping-off Caused by Rhizoctonia solani Kuhn (M.S. Thesis). University of California, Davis, California. Dhingra, O.D., Chagas, D., 1981. Effect of soil temperature, moisture, and nitrogen on competitive saprophytic ability of Macrophomina phaseolina. Trans. Br. Mycol. Soc. 77, 15–20. Dorrance, A.E., Kleinhenz, M.D., McClure, S.A., Tuttle, N.T., 2003. Temperature, moisture, and seed treatment effects on Rhizoctonia solani root rot of soybean. Plant Dis. 87, 533–538. Ehteshamul-Haque, S., Ghaffar, A., 1993. Use of rhizobia in the control of root rot diseases of sunflower, okra, soybean and mungbean. J. Phytopathol. 138, 157–163. Estevez de Jensen, C., Kurle, J.E., Percich, J.A., 2004. Integrated management of edaphic and biotic factors limiting yield of irrigated soybean and dry bean in Minnesota. Field Crops Res. 86, 211–224. FAOSTAT, 2014. Food and Agricultural Organization of the United Nations. 〈http:// www.fao.org/faostat/en〉 (Accessed 30 June 2017). Faraji, A., 2013. Interaction of Major Fungi Causing Root and Crown Rot of Bean and Some Indigenous Antagonistic Rhizobacteria in Zanjan Province (M.S. Thesis). University of Zanjan, Iran. Fernandez, M.R., Zentner, R.P., DePauw, R.M., Gehl, D., Stevenson, F.C., 2007. Impacts of crop production factors on Fusarium head blight in barley in eastern Saskatchewan. Crop Sci. 47, 1574–1584. Gupta, S.K., Mathew, K.A., Shyam, K.R., Sharma, A., 1999. Fungicidal management of root rot (Rhizoctonia solani) of French bean. Plant Dis. Res. 14, 20–24. Hassan Dar, G., Zargar, M.Y., Beigh, G.M., 1997. Biocontrol of fusarium root rot in the common bean (Phaseolus vulgaris L.) by using symbiotic Glomus mosseae and Rhizobium leguminosarum. Microbiol. Ecol. 34, 74–80. Huber, D.M., 1963. Investigations on root rot of beans caused by Fusarium solani f. sp. phaseoli (Ph.D. Thesis). Michigan State University, USA. Kalantari, S., 2011. Biological control of Fusarium root rot on bean by microbial agent in Zanjan province (M.S. Thesis). University of Zanjan, Iran. Katan, J., Eshel, Y., 1973. Interactions between herbicides and plant pathogens. Residue Rev. 45, 145–177. Khodagholi, M., Hemmati, R., Naseri, B., Marefat, A., 2013. Genotypic, phenotypic and pathogenicity variation of Fusarium solani isolates, the causal agent of bean root rots in Zanjan province. Iran. J. Pulses Res. 4, 111–125. Maloy, O.C., Burkholder, W.H., 1959. Some effects of crop rotation on Fusarium root rot of bean. Phytopathology 49, 583–587. Manning, W.J., Crossan, D.F., 1969. Field and greenhouse studies on the effects of plant amendments on Rhizoctonia hypocotyl rot of snapbean. Plant Dis. Rep. 53, 227–231. McAllister, C.B., Garcia-Romera, I., Godeas, A., Ocampo, J.A., 1994. In vitro interactions between Trichoderma koningii, Fusarium solani and Glomus mosseae. Soil Biol. Biochem. 26, 1369–1374. McLean, K.L., Hunt, J., Stewart, A., 2001. Compatibility of the biocontrol agent Trichoderma harzianum C52 with selected fungicides. N.Z. Plant Protect. 54, 84–88. Miklas, P.N., Kelly, J.D., Beebe, S.E., Blair, M.W., 2006. Common bean breeding for resistance against biotic and abiotic stresses: from classical to MAS breeding. Euphytica 147, 105–131. Mussa, A.E.A., Russell, P.E., 1977. The influence of pesticides and herbicides on the
4.10. Temperature Because earlier reports attributed the impact of planting date on bean root rots to air temperature (see Section 4.6) in previous experimental field plot- and regional-scale studies (Naseri, 2013b, 2013c, 2014b, 2014c; Naseri and Mousavi, 2013), attempts were made to determine the effect of temperature on a root rot pathogen. Khodagholi et al. (2013) indicated that F. solani f.sp. phaseoli had no growth at 5 °C in a controlled environment, but it grew at 15, 25, 35 °C, with the optimum growth temperature being at about 25 °C. This optimum temperature is in agreement with the earlier finding from Schuerger and Mitchell (1992). However, the most severe FRR and RRR levels in bean crops were detected at 20 °C (Sippell and Hall, 1982; Abawi, 1989; Schuerger and Mitchell, 1992). Considering the optimum soil temperature is 28 °C for bean growth, it is clear why June-sown beans grew more rapidly at relatively higher temperatures and escaped from more aggressive attacks to slower growing beans planted earlier in May, perhaps with a prolonged pre-emergence period and longer exposure to soil-borne pathogens. Thus, cooler soil temperatures at seeding allow faster root-rot fungi to grow at the expense of the slower bean-root growth. At higher planting temperature (or later seeding) roots obtain a growth rate advantage over the pathogens. A better understanding of the interaction of soil temperature and moisture with root rot intensity and bean production can contribute to restrict disease epidemics at more scientifically chosen sowing dates. These results confirm our previous recommendation (see Section 4.6). 5. Concluding remarks
• This case study integrates various findings on bean root rot epi• •
demics at regional, experimental field-plot, greenhouse and controlled environment scales in order to develop an effective diseasecontrol program. Based on these results we recommend avoiding soil-treatment with fungicides, improving rhizobial nodulation, managing weeds, preplanting treatment of seeds with an appropriate fungicide, rotating beans with appropriate crops, and shallower and later seeding. The optimization of an appropriate planting date, provision of rhizobium-based biofertilizers, selecting appropriate crop rotations, and weed management methods need further research.
52
Rhizosphere 4 (2017) 48–53
B. Naseri, R. Hemmati
100–104. Navas-Cortés, J.A., Hau, B., Jiménez-Díaz, R.M., 1998. Effect of sowing date, host cultivar, and race of Fusarium oxysporum f. sp. ciceris on development of Fusarium wilt of chickpea. Phytopathology 88, 1338–1346. ÖzkoC, I., Delıvelı, M.H., 2001. In vitro inhibition of the mycelia growth of some root rot fungi by Rhizobium leguminosarum biovar phaseoli isolates. Turkish J. Biol. 25, 435–445. Papavizas, G.C., Lewis, J.A., 1975. Effect of seed treatment with fungicides on bean root rots. Plant Dis. Rep. 59, 24–28. Papavizas, G.C., Lewis, J.A., Abd-El Moity, T.H., 1982. Evaluation of new biotypes of Trichoderma harzianum for tolerance to benomyl and enhanced biocontrol capabilities. Phytopathology 72, 126–132. Román-Avilés, B., Snapp, S.S., Kelly, J.D., Kirk, W.W., 2003. Fusarium root rot of common beans (Extension bulletin E2876). Michigan State University, USA. Safarloo, Z., 2011. Vegetative compatibility groups among isolates of Fusarium solani, the causal agent of bean root rot in Zanjan province (M.Sc. Thesis). University of Zanjan, Iran. Schuerger, A.C., Mitchell, D.J., 1992. Effects of temperature, hydrogen ion concentration, humidity, and light quality on disease caused by Fusarium solani f.sp. phaseoli in mung bean. Can. J. Bot. 70, 1798–1808. Sippell, D.W., Hall, R., 1982. Effects of pathogen species, inoculum concentration, temperature, and soil moisture on bean root rot and plant growth. Can. J. Plant Pathol. 4, 1–7. Slatni, T., Krouma, A., Aydi, S., Chaiffi, C., Gouia, H., Abdelly, C., 2008. Growth, nitrogen fixation and ammonium assimilation in common bean (Phaseolus vulgaris L) subjected to iron deficiency. Plant Soil 312, 49–57. Tang, A., Curl, E.A., Rodriguez-Kabana, R., 1970. Effect of trifluraline on inoculum density and spore germination of Fusarium oxysporum f. sp. vasinfectum in soil. Phytopathology 60, 1082–1086. Valenciano, J.B., Casquero, P.A., Boto, J.A., Marcelo, V., 2006. Evaluation of the occurrence of root rots on bean plants (Phaseolus vulgaris) using different sowing methods and with different techniques of pesticide application. N.Z. J. Crop Hortic. Sci. 34, 291–298. Weiland, J.J., Halloin, J.M., 2001. Benzimidazole resistance in Cercospora beticola sampled from sugarbeet fields in Michigan, U.S.A. Can. J. Plant Pathol. 23, 78–82. Williams, M.M., Davis, A.S., Rabaey, T.L., Boerboom, C.M., 2009. Linkages among agronomic, environmental and weed management characteristics in North American sweet corn. Field Crops Res. 113, 161–169. Wrona, A.F., Vandermolen, G.E., Devay, E., 1981. Trifluralininduced changes in hypocotyls of Phaseolus vulgaris in relation to lesion development caused by Rhizoctonia solani Kuhn. Physiol. Plant Pathol. 18, 99–106. Zanjan Meteorological Office, 2009. 〈http://www.zanjanmet.ir/〉 (Accessed 09 September 2015). Zhang, F., Smith, D.L., 2002. Interorganismal signaling in suboptimum environments: the legume-rhizobia symbiosis. Adv. Agron. 76, 125–161.
growth and virulence of Fusarium solani f. sp. phaseoli. J. Agric. Sci. 88, 705–709. Naseri, B., 2007. First report of Macrophomina phaseolina causing charcoal root rot on common bean in Zanjan, Iran. Iran. J. Plant Pathol. 43, 84. Naseri, B., 2008a. Major fungi causing root rot of common bean in Zanjan, Iran. Iran. J. Plant Pathol. 43, 159. Naseri, B., 2008b. Root rot of common bean in Zanjan, Iran: major pathogens and yield loss estimates. Australas. Plant Pathol. 37, 546–551. Naseri, B., 2010. Effects of weed density and soil moisture on the development of bean Fusarium root rot. In: Proceedings of the 3th Iranian Pulse Crops Symposium, Kermanshah, Iran. Naseri, B., 2013a. Epidemics of Rhizoctonia root rot in association with biological and physicochemical properties of field soil in bean crops. J. Phytopathol 161, 397–404. Naseri, B., 2013b. Interpretation of variety × sowing date × sowing depth interaction for bean–Fusarium–Rhizoctonia pathosystem. Arch. Phytopathol. Plant Protect. 46, 2244–2252. Naseri, B., 2013c. Linkages of farmers' operations with Rhizoctonia root rot spread in bean crops on a regional basis. J. Phytopathol. 161, 814–822. Naseri, B., 2014a. Bean production and Fusarium root rot in diverse soil environments in Iran. J. Soil Sci. Plant Nutr. 14, 177–188. Naseri, B., 2014b. Charcoal rot of bean in diverse cropping systems and soil environments. J. Plant Dis. Protect. 121, 20–25. Naseri, B., 2014c. Sowing, field size, and soil characteristics affect bean-Fusarium-wilt pathosystems. J. Plant Dis. Protect. 121, 171–176. Naseri, B., 2016. Epidemiology and integrated management of bean Rhizoctonia root rot. Sci. Plant Pathol. 5, 42–52. Naseri, B., Hamadani, S.A., 2017. Characteristic agro-ecological features of soil populations of bean root rot pathogens. Rhizosphere 3, 203–208. Naseri, B., Marefat, A., 2011. Large-scale assessment of agricultural practices affecting Fusarium root rot and common bean yield. Eur. J. Plant Pathol. 131, 179–195. Naseri, B., Moradi, P., 2007. Prevalence of root rot pathogens and yield losses to the disease on common bean in Zanjan, Iran. Iran J. Plant Pathol. 43, 126. Naseri, B., Moradi, P., 2014. Epidemiology of charcoal root rot in bean growers' fields. In: Proceedings of the 3rd National Congress on Organic and Conventional Agriculture, Ardebil, Iran. Naseri, B., Moradi, P., 2015. Farm management strategies and the prevalence of Rhizoctonia root rot in bean. J. Plant Dis. Protect. 5, 238–243. Naseri, B., Mousavi, S.S., 2013. The development of Fusarium root rot and productivity according to planting date and depth, and bean variety. Australas. Plant Pathol. 42, 133–139. Naseri, B., Mousavi, S.S., 2015. Root rot pathogens in field soil, root and seed in relation to common bean (Phaseolus vulgaris) disease and seed production. Int. J. Pest. Manag. 61, 60–67. Naseri, B., Shobeiri, S.S., Tabande, L., 2016. The intensity of a bean Fusarium root rot epidemic is dependent on planting strategies. J. Phytopathol. 164, 147–154. Naseri, B., Tabande, L., 2017. Patterns of Fusarium wilt epidemics and bean production determined according to a large-scale dataset from agro-ecosystems. Rhizosphere 3,
53
Contents lists available at ScienceDirect
Rhizosphere journal homepage: www.elsevier.com/locate/rhisph
Bean root rot management: Recommendations based on an integrated approach for plant disease control
MARK
⁎
Bita Naseria, , Roghaie Hemmatib a b
Plant Protection Research Department, Kermanshah Agricultural & Natural Resources Research & Education Center, AREEO, Kermanshah, Iran Department of Plant Protection, Faculty of Agriculture, University of Zanjan, Iran
A R T I C L E I N F O
A B S T R A C T
Keywords: Epidemiology Fungi Rhizosphere Root rot
A systematic understanding of agro-ecosystems suppressing soil-borne plant pathogens is one of the most desired objectives in plant disease management. Large-scale detection of agro-ecological descriptors of variations among crop-disease pathosystems will certainly save time to screen a wider range of conditions and identify more effective factors, to further examine at smaller scales, and to develop an integrated crop-disease management program. Therefore, a fairly comprehensive array of agronomic and environmental traits was examined across commercial fields cultivated with the common bean, Phaseolus vulgaris L. Then, ten factors chosen according to practical relevance to root rot epidemics and bean production were studied in laboratory, greenhouse or experimental field. The advantages and findings of this case study as a useful framework in plant pathology were discussed in this short review.
1. Introduction The common bean (Phaseolus vulgaris L.) is the most important food legume in human nutrition worldwide (Broughton et al., 2003). Dry beans were harvested from 30,612,842 ha globally, which produced 26,529,580 t of seeds (FAOSTAT, 2014). The production of bean crops has been mainly threatened by root rot pathogens in most bean growing areas around the world such as northeast Brazil, Mexico, Nicaragua, coastal Peru, and the United States (Abawi, 1989). However, there is no concise information on global yield losses due to root rots in bean crops. Due to difficulties in incorporating root rot resistance into bean cultivars (Miklas et al., 2006), non-economic and ineffective disease control using fungicides is commonly applied by bean growers. Thus, across bean cropping systems, root rot pathogens continue to prevent commercial bean production. It seems that a study framework is required to gain adequate information based on which more reliable and influential recommendations on root-rot-control can be made to bean farmers. In the present review, findings obtained at various scales from region to experimentalplot, to greenhouse and laboratory studies on bean production and root rots were integrated to develop a more effective and sustainable disease and crop management program. In the first step, associations of a large number of agro-ecological variables with the bean-root-rot pathosystem
were explored on a regional or macro-scale basis. Then, such systematic understanding of highly heterogeneous agro-ecosystems allowed the selection of more influential factors to be further examined at small scale. With this approach, uncertainties at regional scale can be addressed at either field-plots or controlled environment scales. This study framework as one of the main promising outcomes of our multi-scale findings has very important significance to advancing the epidemiology of bean root rots, ensuring the efficiency of crop and disease management strategies, saving time and reducing expenses by focusing research on effective management. In Iran, beans are widely cultivated over more than 109,000 ha of irrigated lands annually (Anonymous 2014). Zanjan province is the second major contributor to dry bean production in Iran, with an average production of 2519 kg/ha harvested from 13,280 ha in 2014 (Anonymous, 2014). A number of recent reports from this area demonstrate that soil-borne root rot diseases are threatening bean production. In Zanjan, Fusarium solani, Rhizoctonia solani, Macrophomina phaseolina and F. oxysporum, are the predominant root rot pathogens causing up to 65% yield losses in heavily infected bean crops (Naseri 2007, 2008a, 2008b; Naseri and Moradi, 2007). The distribution of root rot pathogens across the region and the significant yield loss encouraged a systematic epidemiological understanding of bean root rots prevalent in agro-ecosystems to provide recommendations from an
Abbreviations: CRR, Charcoal root rot caused by Macrophomina phaseolina; FRR, Fusarium root rot by Fusarium solani; FW, Fusarium wilt by F. oxysporum; RRR, Rhizoctonia root rot by Rhizoctonia solani ⁎ Corresponding author. E-mail address: [email protected] (B. Naseri). http://dx.doi.org/10.1016/j.rhisph.2017.07.001 Received 10 June 2017; Received in revised form 5 July 2017; Accepted 5 July 2017 Available online 06 July 2017 2452-2198/ © 2017 Elsevier B.V. All rights reserved.
Rhizosphere 4 (2017) 48–53
B. Naseri, R. Hemmati
integrated disease-management program. Therefore, Zanjan's main bean growing areas were chosen for this case study.
Table 1 Soil and agronomic parameters that intensified root rot epidemics in commercial bean fields.
2. Description of study sites and region A representative subset of 122 common bean fields (35 in 2008 and 87 in 2009) ranging from 0.5 to 14 ha in size were randomly selected across the main bean growing area of Zanjan province in order to include all common agronomic and environmental conditions. The study region was located between longitudes 48 °20′–49°30′W to E and latitudes 36°–36°40'S to N. The normal bean growing season in Zanjan involves planting in mid to late spring (May–June) and harvesting in late summer (September). Bean growers were queried about their applications of fungicides and herbicides, planting date and rotation program. Then, commercial bean fields were examined for bean market class, planting depth, rhizobial nodulation and root rot diseases at vegetative, flowering, and pod maturity stages. The complete details on confirmation of major root-rot-pathogen infections and pathogenicity tests, disease assessments, status of rhizobial symbiosis were provided in previous reports (Naseri, 2008b, 2014a; Naseri and Marefat, 2011). At vegetative and pod maturity stages, field soils were sampled and analyzed according to standard methods as Naseri (2013a) described earlier. The soil organic matter, pH, clay, sand and silt in the fields were within the 0.4–1.8%, 7.0–7.9, 14–53%, 4–65% and 15–48% ranges, respectively. The field-plot and greenhouse experiments were conducted in the Agricultural and Natural Resource Research Center located at Kheirabad region (36°30’N, 48°47’E, 1770m a.s.l.) during 2009 and 2010. Mean annual rainfall and temperature in Zanjan, with a cold semi-arid climate and a hot and dry season from June to September, is 315.4 mm and 11.7 °C, respectively (Zanjan Meteorological Office 2009).
Variable
Fusarium root rot
Rhizoctonia root rot
Charcoal root rot
Fusarium wilt
Bean class Early-season drought Irrigation interval Irrigation system Field size Herbicide Planting density Weeds
Pinto, white NSa
White Applied
Pinto, white NS
Pinto, white NS
2–3 days
2–3 days
NS
NS
Furrow
Furrow
NS
NS
NS Not applied 8–17 plant/ quadratb > 16 weed/ quadrat May 2nd wk > 5 cm NS 30–48% NS Mechanical
NS Not applied 8–17 plant/ quadrat > 16 weed/ quadrat May 2nd wk > 5 cm NS 15–30% 45–65% Mechanical
large Not applied NS
NS Applied NS
NS
NS
May 2nd wk > 5 cm NS NS 45–65% Mechanical
May 2nd wk > 5 cm 35–53% 30–48% NS Mechanical
50–500 kg/ha
50–500 kg/ha
50–500 kg/ha
Absent
Absent
50–500 kg/ ha Absent
Treated Non-treated
Treated Non-treated
NS NS
NS NS
Raised Barley, bean, tomato, wheat 0.4–0.8%
Raised Legumes
NS Legumes
0.4–0.8%
NS Legumes, cereals NS
NS
Not applied 7.0–7.5
Not applied 7.5–7.9
NS 7.5–7.9
NS 7.5–7.9
Planting date Planting depth Soil clay Soil silt Soil sand Sowing technique Urea Rhizobial nodule Soil-fungicide Seedfungicide Seedbed Previous crop Organic matter Manure Soil pH
3. Synthesis of regional findings Epidemic levels and consequent yield reductions differ between bean fields of the same area, as well as in the same field from season to season. A considerable part of such differences corresponded with variations in agronomic and environmental conditions, which are known as influential factors on the root-rot–bean pathosystem from planting to harvesting time (Table 1). More severe Fusarium root rot (FRR) epidemics occurred in pinto and white beans, frequent irrigations at 2–3 days intervals at flowering growth stage, denser plant population, earlier and deeper sowings, rotations with barley, bean, tomato or wheat, overuse of urea (50–500 kg/ha), soils with greater silt content (30–48%), soil treatment with fungicides, low soil organic matter, nonnodulated roots, pH levels of 7.0–7.5, lacking herbicide and manure use, sowing non-fungicide-treated seeds, mechanical sowing, furrow irrigation, and planting on raised seedbeds (Naseri, 2010; Naseri and Marefat, 2011; Naseri, 2014a; Naseri et al., 2016). Rhizoctonia root rot (RRR) epidemics were restricted in red beans, drought-free fields, irrigations at 6–9 days intervals, shallow planting, lower plant and weed densities, rotations with potato and tomato, non-fungicide-treated soils, at a level of 4–25% sand content, high soil organic matter, highly nodulated roots, lower soil silt, lower soil sand and pH, lacking urea application, later plantings, manure application, sprinkler irrigation, manual cultivation, weed control using paraquat or bentazon (Naseri, 2013a, 2013c, 2016; Naseri and Moradi, 2015). Large field size, high soil pH and sand, early and deep planting, lacking herbicide use, rotations with legumes or cereals, growing pinto and white beans, nonnodulated roots, mechanical cultivation and urea overuse intensified charcoal root rot (CRR) epidemics (Naseri, 2014b). Lower Fusarium wilt (FW) levels were associated with postponing sowing, growing red beans, lacking urea application, rotations with potato and tomato, shallow planting, neutral soil pH, manual sowing, lower soil clay and silt (Naseri, 2014c; Naseri and Tabannde, 2017). Higher yield levels were detected in red beans, lower root rots, proper planting date and
a b
Absent
NS means non-significant association. Quadrat size was 0.25 m2.
density, lower weed density, soils with lower sand (25–45%) and silt (15–30%) contents, greater soil organic matter (1.2–1.8%), higher rhizobial nodulation, fungicidal treatment of seed, lacking urea fertilization, herbicide and manure applications, manual sowing, sprinkler irrigation, rotations with potato and tomato (Naseri and Marefat, 2011; Naseri, 2014a; Naseri and Tabannde, 2017). Understanding how strongly farmers’ operations interact with the plant-disease pathosystem is important if farmers are to achieve recommendations on efficient cultural strategies to control diseases and improve yield. Indeed, this information should help identify agronomic practices that might restrict root rots establishment on bean crops and thus lead to the selection of most relevant root-rot-control strategies for further field experimentations with the purpose of saving study time. However, information on interrelationships among bean production, root rots epidemics, and prevalence of pathogens in roots, seeds and soils was also necessary to optimize control methods. Therefore, attempts were made to meet these research requirements. The soil population and frequency of pathogens isolated from roots and seeds differed between pathogens and bean fields. F. solani was the most prevalent pathogen isolated from rotted roots and seeds and bean-field soils in comparison with R. solani, M. phaseolina and F. oxysporum (Naseri, 2008b; Naseri and Mousavi, 2015). Macro-scale findings revealed that the root rot index corresponded more strongly with root and seed infections compared to soil populations. This indicates that the infestation of bean seeds due to late-season epidemics occurs more commonly than the soil-borne infection of bean roots in the pathosystems studied. Therefore, the fungicidal treatment of bean seeds to reduce seedborne infections in bean crops should be considered prior to 49
Rhizosphere 4 (2017) 48–53
B. Naseri, R. Hemmati
4.1. Bean market class
the control of soil-borne pathogens in the development of disease management programs for the region. Indeed, CRR, FRR and RRR epidemics were recognized as more important determinants of seed losses in the bean-root-rot pathosystem (Naseri and Mousavi, 2015). There were also associations among the four pathogens infecting either roots or seeds. Knowledge of the prevalence of root rot pathogens in the root, seed and soil is useful to determine the most prominent indicators of the presence of different pathogens in the field, leading to improve the efficiency of root rot control programs. Although Naseri and Mousavi (2015) reported stronger relevance of seed infections to root rot epidemics compared to soil populations, rootrot-control methods still benefit from lowering pathogens densities in field soils. As the next step in bean-root-rot epidemiology, understanding the interactions of various agronomic and soil properties with the prevalence of root rot pathogens in the soil on a regional basis was also required to develop more efficient disease-management programs. Based on multiple assessments mode during the growing season, the populations of these soil-borne pathogens in field soil varied among pathogen species and experimental sites (Naseri and Mousavi, 2015). Thus, attempts were made to elucidate how much of this variation can be explained by differences in the application of fertilizers and herbicides, market classes of beans, previous crop, soil texture, soil electrical conductivity and pH. Lower populations of F. oxysporum and M. phaseolina in farm soils were detected in red beans, herbicide and P-fertilizer applications, clay-loamy soils, greater soil-sand content, higher soil pH (7.5–7.9), larger farms, lack of urea use, and the Kheirabad region. The density of F. solani in soil was associated with bean class, herbicide and P-fertilizer. Region, soil pH and sand affected soil populations of R. solani. A lower total population of four pathogens was observed in red beans, larger fields, the Kheirabad and Khodabandeh regions, P-fertilization, lack of trifluralin and urea application, and at higher levels of electrical conductivity, soil pH and sand (Naseri and Hamadani, 2017). These preliminary assumptions on soil-borne pathogens in interaction with various agro-ecological characteristics should assist with choosing more effective factors for plot-scale and controlled-environment studies to manage disease and improve yield. In other words, this knowledge proceed identifying important factors that affect inocula dynamics in farm soils needed for experimental designs and inducing disease-suppressiveness of farming soils.
Our macro- and plot-scale findings were in agreement regarding the lowest FRR and RRR at pod maturity stage and the highest level of seed production in red beans than pinto and white beans (Naseri, 2013b, 2013c; Naseri and Marefat, 2011; Naseri and Mousavi, 2013). 4.2. Fungicidal treatments of seeds Treatment of bean seeds with fungicides corresponded with remarkable improvements in productivity and reductions in the progression of CRR, FRR and RRR epidemics in commercial bean crops (Naseri et al., 2016; Naseri and Moradi, 2014, 2015). In the greenhouse study, pre-treatment of bean seeds with fungicide improved bean productivity and reduced single or multiple FW, FRR and RRR infections (Faraji, 2013). Our macro-scale findings on the benefits of the fungicide-treated seeds to bean cultivation, which was confirmed by Faraji's (2013) studies, support previous small-scale experiments (Gupta et al., 1999, Dorrance et al., 2003; Papavizas and Lewis, 1975; Valenciano et al., 2006). Thus, we recommend that bean seeds should be treated with a proper fungicide prior to planting. 4.3. Fungicidal treatments of soil Due to the noticeable association of fungicidal treatment of field soils with more severe FRR and RRR epidemics (Naseri, 2013a, 2014a), the fungicide application looked a faulty strategy to improve the sustainability of bean farming systems. In Zanjan, benomyl was the most commonly used fungicide by bean growers followed by mancozeb (Naseri, 2013a). In addition to suppressing beneficial antagonists such as Trichoderma spp. following extensive soil-application of fungicides in particular Benomyl (Papavizas et al., 1982; McAllister et al., 1994; McLean et al., 2001), the over-use of this fungicide induces fungicidal resistance in plant pathogenic fungi (Carling et al., 1990; Weiland and Halloin, 2001). Therefore, a number of controlled-environment studies were performed to advance our understanding of the fungicide-root-rot interaction. Faraji (2013) found that complete inhibition of hyphal growth for F. oxysporum, F. solani and R. solani on agar culture media amended with 6, 8 and 10 × 10−3 g l−1 concentrations of benomyl. However, the 2 g l−1 concentration of fungicide failed to control separate infections by F. solani or R. solani and the combination of FW, FRR and RRR, when added to the irrigation water of bean seedlings in the greenhouse (Faraji, 2013). In conclusion, despite an earlier report of successful control of mung-bean-RRR by benomyl (Kataria and Grover, 1976), chemical control of bean root rots on the expanding roots is uneconomical and therefore impractical under commercial production conditions. Thus, we recommend bean growers to avoid fungicidal treatment of field soils for root-rot-control purposes.
4. Verification of large-scale findings It is believed that the epidemiological knowledge obtained from a highly diverse range of commercial agro-ecosystems extends the understanding gained through small scale studies on a pathosystem (Naseri, 2013a). Despite disadvantages of complicated impacts of diverse agro-ecological properties, surveying commercial fields provide comprehensive information on a large number of crops grown under highly different compositions of agricultural practices and environmental conditions (Fernandez et al., 2007). The conclusions drawn from such regional studies must improve the efficiency of crop management programs (Williams et al., 2009) and applicability of findings in different areas. Although advanced information on soil properties such as soil texture and pH on pathosystems is beneficial to the development of disease control strategies, the plot-scale studies were concentrated on those important agro-ecological factors which could be easily manipulated by farmers without extra inputs. Thus, bean class, herbicide, planting date and depth, which also indicated strong linkages with the development of root rot epidemics at large scale, were selected for plot-scale studies. Fungicidal treatments of seeds and soil, genetic diversity of the pathogen, rotational crops, rhizobial nodulation on bean roots, and temperature were investigated in either greenhouse or laboratory.
4.4. Genetic diversity of the pathogen In the study of population diversity of F. solani f.sp. phaseoli in Zanjan province, Iran, there was phenotypic and genotypic diversity among the 30 pathogen isolates collected from commercial bean fields. DNA fingerprinting patterns from both RAPD and ERIC primers demonstrated high genetic diversity of isolates, which had no significant difference in pathogenicity to bean seedlings in the greenhouse (Khodagholi et al., 2013). The vegetative compatibility of 42 F. solani f.sp. phaseoli isolates collected from Zanjan's bean growing area demonstrated that majority of the pathogen isolates were compatible (Safarloo, 2011). The ability of fungal isolates to form heterokaryons with each other was tested based on hyphal pairings of complementary nitrate-nonutilizing (nit) mutants. Therefore, the high genetic diversity of F. solani f.sp. phaseoli populations (Khodagholi et al., 2013) with the notable ability to form heterokaryon and exchange genetic information (Safarloo, 2011) might explain why no resistant cultivar was found in 50
Rhizosphere 4 (2017) 48–53
B. Naseri, R. Hemmati
FRR, FW and RRR epidemics, and improved yield across a highly diverse agricultural and soil conditions (Naseri, 2013a, 2014b; Naseri and Marefat, 2011; Naseri and Tabande, 2017). Moreover, sowing depth accounted for 28–49% of variations in FRR epidemics across 122 commercial bean fields (Naseri and Marefat, 2011). These profound interactions of planting depth with FRR and RRR were confirmed at the experimental-plot scale (Naseri, 2014b; Naseri and Mousavi, 2013). An Australian study also reported shallow seeding at 2.5 cm depth as the most effective cultural method to control bean root rot, in comparison with hilling depth and fungicidal soil-treatment (Brien et al., 1991). Therefore, we recommend that shallow sowing at 5 cm is recognized as crucial in an integrated root rot control program for bean production.
the study region. As a result, resistance to diseases was considered of minor importance in the development of an integrated program to manage bean root rots. 4.5. Herbicide Herbicide stress is known to influence infections by soil-borne pathogens. Applications of trifluralin and bentazon intensified bean FRR when there was no weed in pot experiments (Mussa and Russell, 1977). Trifluralin increased herbicide-induced susceptibility of potted beans to RRR (Katan and Eshel, 1973; Cull, 1975; Wrona et al., 1981) and soybeans to FW (Carson et al., 1991). Paraquat decreased Rhizoctonia foliar blight in potted soybeans (Black et al., 1996). At plot scale, soybean CRR reduced by applying trifluralin (Canaday et al., 1986) which can enhance soil microbial populations such as actinomycetes (Tang et al., 1970) and then possibly reduce pathogen competition ability in the rhizosphere. In this study, both regional and plot-scale attempts were made to determine whether herbicide applications intensify root rots by exposing bean roots to herbicide stress or restrict the disease epidemic by removing weeds as possible competitors and pathogen reservoirs. The application of farmers’ choice herbicides (trifluralin, paraquat and bentazon) decreased over-season occurrence of CRR, FRR and RRR epidemics and improved productivity in commercial bean fields (Naseri, 2014b; Naseri and Moradi, 2015; Naseri et al., 2016). It could be that without herbicide application, denser weed populations intensified root rot epidemics (Naseri and Marefat, 2011; Naseri, 2013b). Furthermore, the removal of weeds with herbicides may have lowered the pathogen population and distribution in the soil reducing epidemics. Our regional findings were confirmed by the plot-scale research which indicated lower root rots and higher seed production following trifluralin applications (Naseri, unpublished data). Despite different cropping properties, environmental conditions, pathogens populations, bean and pathogen genotypes used, the large-scale results are also in agreement with previous small-scale findings (Canaday et al., 1986; Black et al., 1996). Therefore, we recommend that efficient weed management should be a major part of the bean cropping program.
4.8. Rhizobial nodulation on bean roots The nodulation of bean roots by rhizobial bacteria restricted FRR, RRR, CRR and FW epidemics and improved productivity under highly diverse microbial and agro-ecological traits on a regional basis (Naseri, 2013a, 2014a; Naseri and Mousavi, 2014; Naseri and Moradi, 2014; Naseri and Tabande, 2017). These regional-scale findings were supported by small-scale findings in experimental pots or plots on the reduction of FRR and improvement of bean biomass (Hassan Dar et al., 1997), or yield (Estevez de Jensen et al., 2004), suppression of bean RRR (Blum et al., 1989; Ehteshamul-Haque and Ghaffar, 1993; ÖzkoC and Delıvelı, 2001) and soybean CRR (Ansari, 2010). Our regional findings were confirmed by additional greenhouse studies which demonstrated that seed inoculations with Rhizobium sp. as the most prevalent bacterial symbiont, both improved bean production and reduced FRR (Kalantari, 2011). Although the significant linkage of rhizobial symbiosis on bean yield was detected at both small and large scales (Kalantari, 2011; Naseri, 2014a), insufficient nodulation in 88% of the commercial bean fields might be partially due to the iron deficiency in calcareous soils of the study region (Naseri, 2013a) that reduces legume-rhizobia symbiosis and consequently plant growth (Slatni et al., 2008). Another explanation for low nodulation in Zanjan bean crops may be attributed to 66.4% of fields fertilized with excess urea (50–500 kg/ha, Naseri and Marefat, 2011) which has been linked to reduced rhizobial nodulation in Legumes (Zhang and Smith, 2002). Improvement of effective rhizobial nodulation should be a major objective in bean crop agronomy. We recommend that farmers use either bean seeds pre-coated with rhizobia or amend the soil with biofertilizers including these beneficial microorganisms. This also merits further investigation.
4.6. Planting date Likewise, our plot-scale experimental results which confirmed earlier regional scale reports of more severe early-season FRR and RRR epidemics and lower seed production occurred in early-planting in May than later-planting in June (Naseri, 2013b,c; Naseri and Marefat, 2011; Naseri and Mousavi, 2013). This conclusion is in agreement with other small-scale results of more severe root rots at lower temperatures and higher moisture levels (Abawi, 1989; Bolkan et al., 1974; Sippell and Hall, 1982; Burke and Miller, 1983). According to our macro-scale findings, more severe early- and late-season CRR epidemics occurred in early-sown bean fields following a cooler and moister climate in May than in June (Naseri, 2014b). This regional finding is in agreement with the small-scale observation of severe CRR under cooler and moister conditions in another study (Dhingra and Chagas, 1981). Although moving the planting date from early spring to early winter in Spain intensified FW epidemics in chickpea plots (Navas-Cortés et al., 1998), postponing sowing date from early May (mid-spring in the study area) to late June (early summer) at shallow depths decreased bean-FW epidemics in Zanjan, Iran (Naseri, 2014c). This disagreement might be due to the differences in environmental conditions in particular moisture and temperature at planting, host and pathogen genotypes. Therefore, we recommend that seeding occur after cool and wet periods are passed. Further investigation on appropriate environmental conditions for both plant-growth and pathogen-attack is required.
4.9. Rotational crops Another easily achievable agronomic control of root rot diseases is rotation of beans with appropriately chosen crops. Therefore, we analyzed our regional data for correlations and significant associations of the preceding crop with intensity of bean root rot epidemics. Subsequently, the disease establishment was measured in the greenhouse on a manageable number of commonly cultivated crops in the region, which could be used as potential alternate crops in a rotation program. To meet this requirement, three two-week-old seedlings in each of three replicate pots per test plant were inoculated with a conidial suspension (25 × 106 conidium ml−1 concentration) and disease symptoms were recorded after five weeks. Based on the greenhouse studies, F. solani f.sp. phaseolin can incite FRR symptoms on alfalfa, bean (red, pinto, and white cultivars), chickpea, lentil, faba bean, and sainfoin, but not in wheat (Khodagholi et al., 2013). Furthermore, the highest FRR was detected on chickpea, lentil, faba bean, while alfalfa and red bean had the lowest disease severity levels (Khodagholi et al., 2013). Growing beans following maize and potato decreased the development of FRR and RRR epidemics in commercial fields, respectively (Naseri and Marefat, 2011). More severe CRR epidemics occurred in beans rotated with legumes or cereals, than in potato or tomato (Naseri,
4.7. Planting depth Our regional studies showed that shallower planting reduced CRR, 51
Rhizosphere 4 (2017) 48–53
B. Naseri, R. Hemmati
References
2014b). However, the similarity of CR, FRR, RRR disease severity and bean yield levels when grown following alfalfa, barley, and wheat, to bean mono-croppings (Naseri and Marefat, 2011) disagrees with several field-plot-scale studies by others carried out elsewhere. Rotations of beans with maize, wheat or barley (Abawi and Pastor Corrales, 1990; Maloy and Burkholder, 1959), or alfalfa (Román-Avilés et al., 2003) lowered root rots and enhanced yield in parts of Africa and America. Moreover, maize debris lowered RRR even nearly a year after soil incorporation in both the greenhouse and field (Manning and Crossan, 1969). The over-use of urea in most of the commercial fields (Naseri and Marefat, 2011) might have caused similar disease and yield levels in beans grown after barley and wheat compared to bean-monocultures. It was previously shown that N-fertilizers can reduce the benefits of cereal residue in the soil (Huber, 1963). Thus, our regional and smallscale findings support the recommendation from Bruehl (1989) that crop rotation with both weed and insect control should be used as a major method to manage bean root rots. We therefore recommend that bean rotations should be implemented to avoid and manage root rot occurrence and intensity. Additional studies will be required to describe more precisely a standard recommended rotation schedule, as there remains confounding field and environmental factors to control for, at least for this region.
Abawi, G.S., 1989. Root rot. In: Schwartz, H.F., Pastor Corrales M. (eds.) Bean Production Problems: Disease, Insect, Soil and Climatic Constraints of Phaseolus Vulgaris. Centro Internacional de Agricultura Tropical, Cali. Abawi, G.S., Pastor Corrales, M.A., 1990. Root Rots of Beans in Latin America and Africa: diagnosis, Research Methodologies, and Management Strategies. Centro Internacional de Agricultura Tropical, Cali. Anonymous, 2014. Agricultural Production Report in 2007 and 2014. The Iranian Ministry of Agriculture, Tehran, Iran. Ansari, M.M., 2010. Integrated management of charcoal rot of soybean caused by Macrophomina phaseolina (Tassi) Goid. Soybean Res. 8, 39–47. Black, B.D., Russin, J.S., Griffin, J.L., Snow, J.P., 1996. Herbicide Effects on Rhizoctonia solani in vitro and Rhizoctonia foliar blight of soybean (Glycine max). Weed Sci. 44, 711–716. Blum, L.K., Frey, S.D., Soto, G., 1989. Effect of fluorescent-pigment producing Rhizobium on the severity of Rhizoctonia solani seed and root rot of Phaseolus vulgaris. A paper presented at a symposium held at the Beltsville Agricultural Research Center (BARC), held on 8–11 May. Bolkan, H.A., Wenhara, H.T., Milne, K.S., 1974. Effect of soil temperature on severity of Rhizoctonia solani infection on potato shoots. Plant Dis. Rep. 58, 646–649. Brien, R.G.O., Hare, P.J.O., Glass, R.J., 1991. Cultural practices in the control of bean root rot. Aust. J. Exp. Agric. 31, 551–555. Bruehl, G.W., 1989. Integrated control of soilborne plant pathogens: an overview. Can. J. Plant Pathol. 11, 153–157. Broughton, W.J., Hernandez, G., Blair, M., Beebe, S., Gepts, P., Vanderleyden, J., 2003. Bean (Phaseolus spp.)-model food legumes. Plant Soil 252, 55–128. Burke, D.W., Miller, D.E., 1983. Control of Fusarium root rot with resistant beans and cultural management. Plant Dis. 67, 1312–1317. Canaday, C.H., Helsel, D.G., Wyllie, T.D., 1986. Effects of herbicide-induced stress on root colonization of soybeans by Macrophomina phaseolina. Plant Dis. 70, 863–866. Carling, D.E., Helm, D.J., Leiner, R.H., 1990. In vitro sensitivity of Rhizoctonia solani and other multinucleate and binucleate Rhizoctonia to selected fungicides. Plant Dis. 74, 860–863. Carson, M.L., Arnold, W.E., Todt, P.E., 1991. Predisposition of soybean seedlings to Fusarium root rot with trifluralin. Plant Dis. 75, 342–347. Cull, S.W., 1975. Physiological Studies on Trifluralin-induced Susceptibility of Phaseolus vulgaris to Post-emergence Damping-off Caused by Rhizoctonia solani Kuhn (M.S. Thesis). University of California, Davis, California. Dhingra, O.D., Chagas, D., 1981. Effect of soil temperature, moisture, and nitrogen on competitive saprophytic ability of Macrophomina phaseolina. Trans. Br. Mycol. Soc. 77, 15–20. Dorrance, A.E., Kleinhenz, M.D., McClure, S.A., Tuttle, N.T., 2003. Temperature, moisture, and seed treatment effects on Rhizoctonia solani root rot of soybean. Plant Dis. 87, 533–538. Ehteshamul-Haque, S., Ghaffar, A., 1993. Use of rhizobia in the control of root rot diseases of sunflower, okra, soybean and mungbean. J. Phytopathol. 138, 157–163. Estevez de Jensen, C., Kurle, J.E., Percich, J.A., 2004. Integrated management of edaphic and biotic factors limiting yield of irrigated soybean and dry bean in Minnesota. Field Crops Res. 86, 211–224. FAOSTAT, 2014. Food and Agricultural Organization of the United Nations. 〈http:// www.fao.org/faostat/en〉 (Accessed 30 June 2017). Faraji, A., 2013. Interaction of Major Fungi Causing Root and Crown Rot of Bean and Some Indigenous Antagonistic Rhizobacteria in Zanjan Province (M.S. Thesis). University of Zanjan, Iran. Fernandez, M.R., Zentner, R.P., DePauw, R.M., Gehl, D., Stevenson, F.C., 2007. Impacts of crop production factors on Fusarium head blight in barley in eastern Saskatchewan. Crop Sci. 47, 1574–1584. Gupta, S.K., Mathew, K.A., Shyam, K.R., Sharma, A., 1999. Fungicidal management of root rot (Rhizoctonia solani) of French bean. Plant Dis. Res. 14, 20–24. Hassan Dar, G., Zargar, M.Y., Beigh, G.M., 1997. Biocontrol of fusarium root rot in the common bean (Phaseolus vulgaris L.) by using symbiotic Glomus mosseae and Rhizobium leguminosarum. Microbiol. Ecol. 34, 74–80. Huber, D.M., 1963. Investigations on root rot of beans caused by Fusarium solani f. sp. phaseoli (Ph.D. Thesis). Michigan State University, USA. Kalantari, S., 2011. Biological control of Fusarium root rot on bean by microbial agent in Zanjan province (M.S. Thesis). University of Zanjan, Iran. Katan, J., Eshel, Y., 1973. Interactions between herbicides and plant pathogens. Residue Rev. 45, 145–177. Khodagholi, M., Hemmati, R., Naseri, B., Marefat, A., 2013. Genotypic, phenotypic and pathogenicity variation of Fusarium solani isolates, the causal agent of bean root rots in Zanjan province. Iran. J. Pulses Res. 4, 111–125. Maloy, O.C., Burkholder, W.H., 1959. Some effects of crop rotation on Fusarium root rot of bean. Phytopathology 49, 583–587. Manning, W.J., Crossan, D.F., 1969. Field and greenhouse studies on the effects of plant amendments on Rhizoctonia hypocotyl rot of snapbean. Plant Dis. Rep. 53, 227–231. McAllister, C.B., Garcia-Romera, I., Godeas, A., Ocampo, J.A., 1994. In vitro interactions between Trichoderma koningii, Fusarium solani and Glomus mosseae. Soil Biol. Biochem. 26, 1369–1374. McLean, K.L., Hunt, J., Stewart, A., 2001. Compatibility of the biocontrol agent Trichoderma harzianum C52 with selected fungicides. N.Z. Plant Protect. 54, 84–88. Miklas, P.N., Kelly, J.D., Beebe, S.E., Blair, M.W., 2006. Common bean breeding for resistance against biotic and abiotic stresses: from classical to MAS breeding. Euphytica 147, 105–131. Mussa, A.E.A., Russell, P.E., 1977. The influence of pesticides and herbicides on the
4.10. Temperature Because earlier reports attributed the impact of planting date on bean root rots to air temperature (see Section 4.6) in previous experimental field plot- and regional-scale studies (Naseri, 2013b, 2013c, 2014b, 2014c; Naseri and Mousavi, 2013), attempts were made to determine the effect of temperature on a root rot pathogen. Khodagholi et al. (2013) indicated that F. solani f.sp. phaseoli had no growth at 5 °C in a controlled environment, but it grew at 15, 25, 35 °C, with the optimum growth temperature being at about 25 °C. This optimum temperature is in agreement with the earlier finding from Schuerger and Mitchell (1992). However, the most severe FRR and RRR levels in bean crops were detected at 20 °C (Sippell and Hall, 1982; Abawi, 1989; Schuerger and Mitchell, 1992). Considering the optimum soil temperature is 28 °C for bean growth, it is clear why June-sown beans grew more rapidly at relatively higher temperatures and escaped from more aggressive attacks to slower growing beans planted earlier in May, perhaps with a prolonged pre-emergence period and longer exposure to soil-borne pathogens. Thus, cooler soil temperatures at seeding allow faster root-rot fungi to grow at the expense of the slower bean-root growth. At higher planting temperature (or later seeding) roots obtain a growth rate advantage over the pathogens. A better understanding of the interaction of soil temperature and moisture with root rot intensity and bean production can contribute to restrict disease epidemics at more scientifically chosen sowing dates. These results confirm our previous recommendation (see Section 4.6). 5. Concluding remarks
• This case study integrates various findings on bean root rot epi• •
demics at regional, experimental field-plot, greenhouse and controlled environment scales in order to develop an effective diseasecontrol program. Based on these results we recommend avoiding soil-treatment with fungicides, improving rhizobial nodulation, managing weeds, preplanting treatment of seeds with an appropriate fungicide, rotating beans with appropriate crops, and shallower and later seeding. The optimization of an appropriate planting date, provision of rhizobium-based biofertilizers, selecting appropriate crop rotations, and weed management methods need further research.
52
Rhizosphere 4 (2017) 48–53
B. Naseri, R. Hemmati
100–104. Navas-Cortés, J.A., Hau, B., Jiménez-Díaz, R.M., 1998. Effect of sowing date, host cultivar, and race of Fusarium oxysporum f. sp. ciceris on development of Fusarium wilt of chickpea. Phytopathology 88, 1338–1346. ÖzkoC, I., Delıvelı, M.H., 2001. In vitro inhibition of the mycelia growth of some root rot fungi by Rhizobium leguminosarum biovar phaseoli isolates. Turkish J. Biol. 25, 435–445. Papavizas, G.C., Lewis, J.A., 1975. Effect of seed treatment with fungicides on bean root rots. Plant Dis. Rep. 59, 24–28. Papavizas, G.C., Lewis, J.A., Abd-El Moity, T.H., 1982. Evaluation of new biotypes of Trichoderma harzianum for tolerance to benomyl and enhanced biocontrol capabilities. Phytopathology 72, 126–132. Román-Avilés, B., Snapp, S.S., Kelly, J.D., Kirk, W.W., 2003. Fusarium root rot of common beans (Extension bulletin E2876). Michigan State University, USA. Safarloo, Z., 2011. Vegetative compatibility groups among isolates of Fusarium solani, the causal agent of bean root rot in Zanjan province (M.Sc. Thesis). University of Zanjan, Iran. Schuerger, A.C., Mitchell, D.J., 1992. Effects of temperature, hydrogen ion concentration, humidity, and light quality on disease caused by Fusarium solani f.sp. phaseoli in mung bean. Can. J. Bot. 70, 1798–1808. Sippell, D.W., Hall, R., 1982. Effects of pathogen species, inoculum concentration, temperature, and soil moisture on bean root rot and plant growth. Can. J. Plant Pathol. 4, 1–7. Slatni, T., Krouma, A., Aydi, S., Chaiffi, C., Gouia, H., Abdelly, C., 2008. Growth, nitrogen fixation and ammonium assimilation in common bean (Phaseolus vulgaris L) subjected to iron deficiency. Plant Soil 312, 49–57. Tang, A., Curl, E.A., Rodriguez-Kabana, R., 1970. Effect of trifluraline on inoculum density and spore germination of Fusarium oxysporum f. sp. vasinfectum in soil. Phytopathology 60, 1082–1086. Valenciano, J.B., Casquero, P.A., Boto, J.A., Marcelo, V., 2006. Evaluation of the occurrence of root rots on bean plants (Phaseolus vulgaris) using different sowing methods and with different techniques of pesticide application. N.Z. J. Crop Hortic. Sci. 34, 291–298. Weiland, J.J., Halloin, J.M., 2001. Benzimidazole resistance in Cercospora beticola sampled from sugarbeet fields in Michigan, U.S.A. Can. J. Plant Pathol. 23, 78–82. Williams, M.M., Davis, A.S., Rabaey, T.L., Boerboom, C.M., 2009. Linkages among agronomic, environmental and weed management characteristics in North American sweet corn. Field Crops Res. 113, 161–169. Wrona, A.F., Vandermolen, G.E., Devay, E., 1981. Trifluralininduced changes in hypocotyls of Phaseolus vulgaris in relation to lesion development caused by Rhizoctonia solani Kuhn. Physiol. Plant Pathol. 18, 99–106. Zanjan Meteorological Office, 2009. 〈http://www.zanjanmet.ir/〉 (Accessed 09 September 2015). Zhang, F., Smith, D.L., 2002. Interorganismal signaling in suboptimum environments: the legume-rhizobia symbiosis. Adv. Agron. 76, 125–161.
growth and virulence of Fusarium solani f. sp. phaseoli. J. Agric. Sci. 88, 705–709. Naseri, B., 2007. First report of Macrophomina phaseolina causing charcoal root rot on common bean in Zanjan, Iran. Iran. J. Plant Pathol. 43, 84. Naseri, B., 2008a. Major fungi causing root rot of common bean in Zanjan, Iran. Iran. J. Plant Pathol. 43, 159. Naseri, B., 2008b. Root rot of common bean in Zanjan, Iran: major pathogens and yield loss estimates. Australas. Plant Pathol. 37, 546–551. Naseri, B., 2010. Effects of weed density and soil moisture on the development of bean Fusarium root rot. In: Proceedings of the 3th Iranian Pulse Crops Symposium, Kermanshah, Iran. Naseri, B., 2013a. Epidemics of Rhizoctonia root rot in association with biological and physicochemical properties of field soil in bean crops. J. Phytopathol 161, 397–404. Naseri, B., 2013b. Interpretation of variety × sowing date × sowing depth interaction for bean–Fusarium–Rhizoctonia pathosystem. Arch. Phytopathol. Plant Protect. 46, 2244–2252. Naseri, B., 2013c. Linkages of farmers' operations with Rhizoctonia root rot spread in bean crops on a regional basis. J. Phytopathol. 161, 814–822. Naseri, B., 2014a. Bean production and Fusarium root rot in diverse soil environments in Iran. J. Soil Sci. Plant Nutr. 14, 177–188. Naseri, B., 2014b. Charcoal rot of bean in diverse cropping systems and soil environments. J. Plant Dis. Protect. 121, 20–25. Naseri, B., 2014c. Sowing, field size, and soil characteristics affect bean-Fusarium-wilt pathosystems. J. Plant Dis. Protect. 121, 171–176. Naseri, B., 2016. Epidemiology and integrated management of bean Rhizoctonia root rot. Sci. Plant Pathol. 5, 42–52. Naseri, B., Hamadani, S.A., 2017. Characteristic agro-ecological features of soil populations of bean root rot pathogens. Rhizosphere 3, 203–208. Naseri, B., Marefat, A., 2011. Large-scale assessment of agricultural practices affecting Fusarium root rot and common bean yield. Eur. J. Plant Pathol. 131, 179–195. Naseri, B., Moradi, P., 2007. Prevalence of root rot pathogens and yield losses to the disease on common bean in Zanjan, Iran. Iran J. Plant Pathol. 43, 126. Naseri, B., Moradi, P., 2014. Epidemiology of charcoal root rot in bean growers' fields. In: Proceedings of the 3rd National Congress on Organic and Conventional Agriculture, Ardebil, Iran. Naseri, B., Moradi, P., 2015. Farm management strategies and the prevalence of Rhizoctonia root rot in bean. J. Plant Dis. Protect. 5, 238–243. Naseri, B., Mousavi, S.S., 2013. The development of Fusarium root rot and productivity according to planting date and depth, and bean variety. Australas. Plant Pathol. 42, 133–139. Naseri, B., Mousavi, S.S., 2015. Root rot pathogens in field soil, root and seed in relation to common bean (Phaseolus vulgaris) disease and seed production. Int. J. Pest. Manag. 61, 60–67. Naseri, B., Shobeiri, S.S., Tabande, L., 2016. The intensity of a bean Fusarium root rot epidemic is dependent on planting strategies. J. Phytopathol. 164, 147–154. Naseri, B., Tabande, L., 2017. Patterns of Fusarium wilt epidemics and bean production determined according to a large-scale dataset from agro-ecosystems. Rhizosphere 3,
53