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Published in Agron J 100:795-800 (2008)
DOI: 10.2134/agronj2007.0142
© 2008 American Society of Agronomy
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MYCORRHIZAE

Arbuscular Mycorrhizal Colonization Response to Three Seed-Applied Fungicides

Adriana Murillo-Williamsa,* and Palle Pedersenb

a Centro para Investigaciones en Granos y Semillas (CIGRAS); Univ. de Costa Rica, San Pedro de Montes de Oca, San José, Costa Rica
b Dep. of Agronomy, Iowa State Univ., 2104 Agronomy Hall, Ames, IA 50011

* Corresponding author (adriana.murillowilliams{at}ucr.ac.cr).


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSION
 REFERENCES
 
In soybean [Glycine max (L.) Merr.], arbuscular mycorrhizae (AM) enhance nutrient and water status and may increase root resistance to soilborne pathogens. However, the fungicides that are routinely applied to the seed may reduce AM colonization, reducing these benefits. Thus, the objective of this research was to assess the effect of three commonly used seed-applied fungicides on AM colonization of soybean in Iowa. Soybean seeds were treated with the fungicides mefenoxam, fludioxonil, mefenoxam + fludioxonil, and a nontreated control. Soil fumigation with a mixture of 1,3-dichloropropene and chloropicrin was used as a tool to measure any direct effect of the fungicide on plant growth or yield parameters. There was a significant fumigation by seed treatment interaction in 2005. Seed-applied fungicides that contained fludioxonil favored AM colonization in nonfumigated soil, where fludioxonil-treated plants had double the root colonization of the control (6 vs. 2.8%, respectively) and five times more root colonization than plants treated with mefenoxam (6 vs. 1.1%, respectively). In the fumigated soil, plants treated with mefenoxam alone or in combination with fludioxonil had lower colonization than the control and fludioxonil-treated plants. Fumigation did not significantly reduce or increase mycorrhizal colonization across locations. No differences in grain yield, final stand, or grain composition were found among seed-applied fungicides or between nonfumigated and fumigated soil. With the exception of mefenoxam in fumigated soil in 2005, there was no evidence of a reduction in mycorrhizal colonization of soybean roots with seed-applied fungicides under field conditions.

Abbreviations: AM, arbuscular mycorrhizae


   NOTES
TOP
 NOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSION
 REFERENCES
 
All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher.

Received for publication April 17, 2007.
   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSION
 REFERENCES
 
EARLY PLANTING OF SOYBEAN has become more frequent in the upper Midwest since it has been shown to significantly increase yields (Oplinger and Philbrook, 1992; Pedersen and Lauer, 2003). Conversely though, early soybean planting exposes seed to cooler and more saturated soils, leading to slow germination and development (Hatfield and Egli, 1974), thus extending the time that seeds are exposed to pathogens that cause seed root and damping off (Hamman et al., 2002; Thomas et al., 1975).

In Iowa, the most common seedling diseases on soybean are caused by Pythium spp., Rhizoctonia solani, Phytophthora sojae, and Fusarium spp. (Rivzi and Yang, 1996). Alternating corn (Zea mays L.) with soybean is the most common rotation in the upper Midwest, but the rotation of these two crops does not effectively manage seed and seedling diseases. The severity of seedling diseases on soybean varies from year to year depending on both soil and environmental conditions (Dorrance and McClure, 2001; Dorrance et al., 2003). Although economic losses due to seedling diseases on soybean have been reported in the United States, yield losses in Iowa vary and are rarely a problem (Wrather and Koenning, 2006). This variability is most likely due to the fact that stand reduction will not always contribute to yield loss when the stand is uniform and above 240,000 plants per hectare at harvest (De Bruin, 2007), since the soybean crop compensates for low plant populations by allocating more assimilates for increased branching (Board, 2000).

Mycorrhizal fungi form a symbiotic relationship with plant roots. Arbuscular mycorrhizae are the most common type of mycorrhiza, where the fungi colonize the interior of the root and form specialized structures, known as arbuscules, for nutrient exchange with the host. Fungal hyphae extend from the root and explore the soil more efficiently than would fine plant roots. Arbuscular mycorrhizae can provide the plant with supplemental phosphorus (P), nitrogen (N), and micronutrients since the plant roots alone are not able to maximize the interception of nutrients (Allen et al., 2003). Specifically in soybean, AM have been shown to improve the overall water status of the plant (Porcel and Ruiz-Lozano, 2004; Vejsadova et al., 1993), due to a reduced resistance to water transport (Safir et al., 1971), associated with an enhanced nutrient (Safir et al., 1972).

Arbuscular mycorrhizae interact in the rhizosphere with other beneficial organisms and pathogens, often competing for the same colonization sites (Harrier and Watson, 2004). Mycorrhizae have been shown to protect plants against pathogens in numerous crops (Azcon-Aguilar and Barea, 1997; Slezack et al., 2000; Zhu and Yao, 2004). In soybeans, AM-colonized plants have been reported to have significantly less damage due to Rhizoctonia solani, Macrophomina phaseolina, Fusarium solani, and root knot nematode (Meloidogyne incognita) (Schenck and Kinloch, 1974; Winkler et al., 1994; Zambolim and Schenck, 1983), although increases in AM colonization have also been associated with an increased severity of Phytophthora root rot in soybean seedlings (Ross and Harper, 1972). It has been demonstrated that the degree of soybean AM root colonization also depends on the predominant AM species (Schenck and Smith, 1982), temperature (Schenk and Smith, 1982), edaphic conditions (Khalil et al., 1992), soil disturbance (McGonigle et al., 1999), and growth stage (Bagyaraj et al., 1979), but these results have been primarily obtained using inoculated plants not under field conditions. Also, previously reported values of root colonization were influenced by the method used to determine colonization, as well as host growth stage and soil fertility. For example, Bagyaraj et al. (1979) reported values of 60% colonization 45 d after planting, and up to 75% 60 d after planting in a naturally infested soil. In Iowa, a survey conducted by Khalil et al. (1992) reported naturally occurring root colonization that ranged from 18 to 98% in different soil types.

With regard to soybean disease management, fungicide seed treatments are commonly used in addition to genetic resistance in order to effectively manage seedling diseases. Fungicide seed treatments alter the microbial population dynamics in the rhizosphere by reducing root pathogen infection, but may also affect nontarget organisms (Rodriguez-Kabana and Curl, 1980; Trappe et al., 1984). Soil applications of metalaxyl have been reported to favor AM colonization in corn and soybeans (Groth and Martinson, 1983). Seed-applied captan had no effect on AM colonization in studies conducted by Kucey and Bonetti (1988), and it reduced symptoms of Fusarium solani when applied along with AM inoculum in Phaseolus vulgaris plants (Gonçalves et al., 1991).

Reductions in plant growth, number of arbuscules, and length of infected roots when metalaxyl was applied as a soil drench in onions (Allium cepa) have been documented (Sukarno et al, 1993). Other fungicides such as benomyl, captan, pentachloronitrobenzene, and emisan, have been reported to also have negative effects on AM colonization when applied as soil drenches (Gnekow and Marschner, 1989; Kjoller and Rosendahl, 2000; Schreiner and Bethlenfalvay, 1997; Sugavanam et al., 1994).

Mefenoxam and fludioxonil are two of the most common fungicide seed treatments used in Iowa. Soil fumigation has been used for root health studies because it reduces pathogen inoculum (Hamm et al., 2003) and it can be used to evaluate the direct effect of chemicals in plant growth and yield. The hypothesis of this experiment was that the fungicide seed treatments mefenoxam and fludioxonil may reduce competition with seedling pathogens early in the growing season, enabling increased colonization of AM in plants grown from treated seed. A further hypothesis is that a fumigated soil environment would enable a measure of the direct effect of the fungicide on soybean growth and yield. Therefore, the objective of this study was to determine whether there was a difference in AM colonization when three fungicide seed treatments (mefenoxam, fludioxonil, and mefenoxam + fludioxonil) were applied in soybean across different environments with and without soil fumigation.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSION
 REFERENCES
 
Multi-year (2004 and 2005) and multi-location (De Witt, Nevada, and Whiting) field trials were conducted in Iowa to determine the effect of fungicide seed treatments on AM colonization of soybeans (Table 1 ). The predominant soil type was classified in De Witt as Tama silt loam (fine-silty, mixed mesic, Typic Arguidolls), in Nevada as Webster clay loam (fine-loamy, mixed mesic, Typic Hapludolls), and in Whiting as a Salix silty clay loam (fine-silty, mixed mesic, Typic Hapludolls). Fields were moldboard plowed or disked twice (Whiting) during the fall, and field cultivated once in the spring. In the two years of experiments, planting occurred during the last week of April or first week of May.


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  		Table 1. Soil characteristics of the three locations in Iowa (DeWitt, Nevada, and Whiting) and cumulative precipitation and average temperature from planting until root sampling at 42 d after emergence in 2004 and 2005 field trials.

 
For soil fertility analysis, subsamples of soil were collected randomly across the field at a depth of 15 cm. A composite sample from each location was analyzed for NO3-N, P, potassium (K), pH, and organic matter by the Iowa State University Soil Testing Laboratory. Nitrate-N was determined using colorimetric cadmium reduction (Gelderman and Beegle, 1998). Phosphorus and K were determined by the Mehlich-3 extraction method (Frank et al., 1998; Warncke and Brown, 1998). Soil pH was determined using a 1:1 soil water paste (Watson and Brown, 1998). Organic matter was determined by dry combustion with a LECO CHN-2000 analyzer (LECO Corp., St. Joseph, MI) (Nelson and Sommers, 1996).

At each location, 4 ha were fumigated (30 cm depth) with Telone-35 (Dow AgroSciences, Indianapolis, IN), which consisted of a mixture of 61.1% 1,3-dichloropropene and 34.7% chloropicrin at a rate of 113 kg a.i. ha–1. Fumigation was conducted during the fall at all locations, except Nevada 2005, where fumigation was done during the spring due to inclement weather conditions the previous fall. The soybean variety SOI2642 (Sands of Iowa, Marcus, IA) was inoculated with Bradyrhizobium japonicum (EMD Crop Bioscience, Brookfield, WI) and planted using an Almaco grain drill (Almaco, Nevada, IA) in plots of 3 m by 6.7 m, using 38-cm row spacing and a seeding rate of 420,000 seeds ha–1. For weed management, glyphosate [N-(phosphomethyl) glycine] was applied at a rate of 1.12 kg a.i. ha–1 twice in the growing season, when plants were at V2 and R1 stages of growth (Fehr and Caviness, 1977).

The experimental design was a two-way factorial in a split-plot arrangement. Whole-plot treatments were fumigated and nonfumigated soil. The subplot factor was arranged in a randomized complete block with four replications. Subplot treatments consisted of a control not treated with fungicide plus seed-applied fungicides: fludioxonil [4-(2,2-difluoro-1,3-benzodioxol-4-yl)-1H-pyrrole-3-carbonitrile]; mefenoxam {(R,S)-2-[(2,6-dimethylphenyl)-methoxyacetylamino]-propionic acid methyl ester}; and mefenoxam + fludioxonil. Fludioxonil (Maxim 4FS, Syngenta, Greensboro, NC) was applied at a rate of 0.07 g a.i. kg seed–1 and is a contact fungicide in the family of the phenyl-pyrroles with activity against soilborne and seedborne Rhizoctonia spp., Fusarium spp., Aspergillus spp., Penicillium spp., and Sclerotinia sclerotiorum (Lipps et al., 2000; Mueller et al., 1999). Mefenoxam (Apron XL LS, Syngenta, Greensboro, NC) was applied at a rate of 0.05 g a.i. kg seed–1 and is a systemic phenylamide fungicide that targets diseases caused by soilborne Pythium spp. and Phytophthora spp. (Davidse et al., 1983). The combination product is marketed as ApronMaxx RFC (Syngenta, Greensboro, NC) and was applied at a rate of 0.037 g a.i. kg seed–1 of fludioxonil and 0.025 g a.i. kg seed–1 of mefenoxam. All rates used were the current commercially applied rates in Iowa.

At 42 d after emergence, which corresponded to early reproductive stages (Khalil et al., 1992), five plants from the outside rows of each plot were clipped and their root systems excavated with a spade and placed in plastic bags for transport to the laboratory, where they were stored at 4°C. The whole root system was soaked in water and carefully washed to minimize fine root loss. From each plant, large segments of terminal fine roots were randomly sampled from different portions of the root system and placed in labeled plastic embedding cassettes (Unisette, Fisher Scientific, Pittsburgh, PA). Root staining for mycorrhizal observation followed using the method of Kormanik and McGraw (1982). The plastic cassettes were autoclaved for 10 min in a 10% potassium hydroxide solution and then rinsed under running tap water a minimum of three times, or until rinse water was clear. Cassettes were soaked in 1% hydrochloric acid for 5 min and then immersed in 0.01% acid-fuchsin-lactic acid staining solution and autoclaved for a further 10 min. From the stained samples, 30 1-cm root pieces per plant were cut and observed with a compound microscope at 20x. Root colonization was assessed according to the root slide method (Giovanetti and Mosse, 1980; Read et al., 1975). In this method, the percentage of root colonization per plant was calculated by dividing the total number of colonized sections (either with arbuscles, vesicles, or mycelium) by the total number of root pieces examined.

Agronomic variables were collected in the field prior to harvest, including stand counts, plant height, and lodging. Lodging was based on a 1 (no lodging) to 5 (completely lodged) scale. To determine plot yield, the middle four rows of each plot were harvested using a small plot combine (Almaco, Nevada, IA), and final yield was adjusted to 130 g kg–1 moisture.

Data Analysis
For AM colonization data, years were analyzed individually based on residual plot analysis, and a significant year by treatment interaction detected in the two-year combined analysis of variance. Locations were considered random for the single-year ANOVA.

Analysis of variance for agronomic variables was conducted across years based on homogeneity of variances. Locations and replications were considered random effects. For AM colonization and agronomic data, least significant difference tests at the 0.05 level were calculated to compare main plots and subplots. Data were analyzed with PROC MIXED of SAS (SAS Institute, Cary, NC).


   RESULTS AND DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSION
 REFERENCES
 
Incidence of seedling pathogens varied across years and locations as the spring weather conditions were very different. In spring 2004, the weather was wetter and cooler compared with 2005. A higher incidence of Pythium spp. in soybean seedlings was observed in 2004. The spring of 2005 was considerably drier and was characterized by a higher incidence of Rhizoctonia solani in seedlings, which was observed in both the fumigated and nonfumigated soils (Murillo-Williams, 2007). Furthermore, soil fertility levels were not influenced by the fumigation treatment at any location in the two years of experiments (Table 1).

Fumigation
A fumigation by seed treatment interaction was found in 2005 (Table 2 ). Differences in AM colonization among seed treatments varied according to the level of fumigation. In the nonfumigated soil, treatments that contained fludioxonil had three times more AM colonization compared with the nontreated control and mefenoxam treatment (Table 3 ). However, in the fumigated soil, soybean plants treated with fludioxonil had the highest AM colonization among treatments, although fludioxonil and mefenoxam + fludioxonil did not differ from the nontreated control in terms of AM colonization. Mefenoxam resulted in significantly lower root colonization than the control, although not statistically different from mefenoxam + fludioxonil (Table 3).


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  		Table 2. Effect of fumigation and seed-applied fungicides on percentage of root mycorrhizal colonization of soybean grown in 2004 and 2005 at three locations in Iowa.

 

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  		Table 3. Soybean mycorrhizal root colonization in 2005 at three locations in Iowa.

 
Pathogens that infect seedlings may reduce root colonization by mycorrhizal fungi (Cordier et al., 1998; Yao et al., 2002; Zambolim and Schenck, 1983). The seed treatments used in this experiment targeted different pathogens. Specifically, mefenoxam systemically protects roots against water molds like Pythium spp. and Phytophthora sojae, while fludioxonil targets pathogens like Fusarium spp., Rhizoctonia solani, and seedborne Aspergillus spp. and Penicillium spp. Precipitation was less than average in 2005, which favored seedling infection by Rhizoctonia over Pythium spp. (Murillo-Williams, 2007). In nonfumigated soil, greater AM colonization in the fludioxonil-treated soybean plots may be explained by a reduction in competition of AM with aggressive pathogens like Rhizoctonia solani. This principle of competition has been documented under controlled conditions (Zambolim and Schenck, 1983).

In 2004, Pythium incidence was 95% in the nonfumigated soil (Murillo-Williams, 2007). Although there was no significant difference in AM root colonization among seed treatments in 2004 (Table 3), colonization tended to be higher for treatments that had mefenoxam, a fungicide that targets oomycetes such as Pythium and Phytophthora. Our results from 2004 were consistent with the results of Groth and Martinson (1983) who suggested that soil applications of metalaxyl increased mycorrhizal colonization of corn and soybeans due to a reduction in competition with pathogenic oomycetes, and not by having a stimulatory effect on AM fungi.

Fumigation did not influence AM colonization in 2004 (Table 2). Previous research has shown that the dynamics of recolonization by soil microflora will vary according to the type of fumigant used, as well as the specific soil conditions (An et al., 1990; Ladd et al., 1976; Warcup, 1976). Fumigation may thus result in an initial depletion in populations of beneficial organisms (Ladd et al., 1976; Ridge, 1976), although there are reports of fumigation having stimulated AM populations after some time in the presence of the host (An et al., 1990). In the current study, lack of significant differences in AM colonization between the nonfumigated and the fumigated soil could be related to a limited movement of the fumigant deep enough in the soil to reduce AM inoculum, or by rapid recovery of AM populations (An et al., 1990).

Relatively low levels of AM colonization were found during this experiment. Low AM colonization has been associated with high P content in the soil, P fertilization, and tillage (Allen et al., 2003; Fairchild and Miller, 1990; Khalil et al., 1992; Goss and de Varennes, 2002). In Iowa, Khalil et al. (1992) documented AM colonization (expressed as vesicles) in Tama soils that ranged from 44 to 60% and from 24 to 58% in Webster soils. Khalil et al. (1992) observed a negative correlation between available P in the soil and percentage of roots with hyphae and arbuscules. The P level at most of our locations (except for Nevada) was above 30.5 mg kg–1, which is considered high for Iowa soils (Sawyer et al., 2002). High levels of soil P and tillage practices may also affect AM colonization. The fields in this study were either moldboard plowed or disked in the fall, followed by a preplant spring cultivation. Previous research has indicated that tillage may: (i) reduce the colonization rate of AM, (ii) negatively affect winter survival of mycorrhizal hyphae, and (iii) enable one AM species to be predominant over other species (Douds et al., 1995; Fairchild and Miller, 1990; Goss and de Varennes, 2002; Kabir et al., 1997; Kurle and Pfleger, 1996). The detrimental effect of soil disturbance on AM colonization has been suggested as a consequence of the rupture of the hyphal network, thereby reducing colonization (Jasper et al., 1989). In soybeans, Goss and de Varennes (2002) reported significant reductions in the percentage of colonization (expressed as vesicles) caused by soil disturbance from 5 to 0.3% 23 d after emergence, and from 21 to 11% 49 d after emergence. Other possible explanations for the low AM colonization in this study include an intrinsically low mycorrhizal dependency of the chosen variety (Khalil et al., 1999), which could be reflected in low root colonization. From an experimental standpoint, the use of locations as replications for fumigation when years were analyzed separately could also have led to the low AM colonization values found in this experiment.

Agronomic Variables
There was no significant effect of fumigation or fungicide seed treatments on grain yield, grain moisture, final plant population, lodging, height, seed mass, protein content, or oil content (Table 4 ). These results were not surprising since fungicide seed treatments may increase or reduce emergence and final stand (Guy and Oplinger, 1989; Lueschen et al., 1991) without an effect on yield (Athow and Caldwell, 1975; Guy and Oplinger, 1989). Previous research by Lueschen et al. (1991) in Wisconsin showed that the response to seed treatment depended more on cultivar susceptibility to seedling pathogens and seed quality, compared with the effect of agronomic practices such as tillage. In field experiments conducted in Iowa by Wall et al. (1983), seed lots with 50% Phomopsis infection produced higher yields when treated with a fungicidal seed treatment, but the authors concluded that fungicidal seed treatment did not improve emergence or increase yield when the seedlots were mechanically damaged, small sized, or aged.


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  		Table 4. Effect of fumigation and three seed-applied fungicides on soybean plant density, height, lodging, seed weight, grain yield, and composition across three locations during 2004 and 2005 in Iowa.

 
It has been documented that yield is often related to the maintenance of critical plant population (Athow and Caldwell, 1975). Recently, it has been documented that 240,000 plants ha–1 in Iowa (De Bruin, 2007) is an adequate population to maximize yield since soybean will compensate for space by allocating more dry matter to branches (Board, 2000). Results from this experiment showed that final plant populations for all seed treatments and the control were above the critical final plant population. The results of our study are similar to the observations of Bierman et al. (2006), who found that while there was a significantly lower plant population when soybean seeds were treated with fludioxonil, the final plant population was still above the acceptable level thought to maximize yield.


   CONCLUSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSION
REFERENCES
 
The benefit of mycorrhizal associations for soybeans is well known. Little information exists about the effect that seed-applied fungicides may have on soybean AM colonization. Mefenoxam, fludioxonil, and mefenoxam + fludioxonil were evaluated as seed treatments on soybean to determine their effect on AM colonization. Results varied for the different years of the study. In 2005, differences in AM colonization were detected among fungicides according to the level of fumigation. Under natural pathogen inoculum (nonfumigated soil), seed-applied fungicides with fludioxonil seemed to favor AM colonization due to a reduced competition with aggressive pathogens like Rhizoctonia spp., an organism that is targeted by this fungicide. Further conclusions cannot be drawn regarding this result because pathogen inoculum was not added to the soil as a third treatment. Also, mefenoxam, fludioxonil, and mefenoxam + fludioxonil did not affect any of the agronomic variables. In summary, no conclusive evidence was found that indicated fungicide seed treatments have detrimental effects on mycorrhizal root colonization of soybeans when applied at recommended commercial rates in Iowa.


   ACKNOWLEDGMENTS
 
The authors thank Jason De Bruin and Jodee Stuart for their assistance. This research was partially funded by the Iowa Soybean Assoc., Syngenta Crop Protection, Iowa State Univ. College of Agric. and Life Sci., and Dep. of Agronomy at Iowa State Univ.

All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher.


   REFERENCES
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSION
 REFERENCES
 





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