Foliar Symptoms Of Sudden Death Syndrome Research Articles

Effect of Seed Treatment and Foliar Crop Protection Products on Sudden Death Syndrome and Yield of Soybean.

Sudden death syndrome (SDS), caused by Fusarium virguliforme, is an important soilborne disease of soybean. Risk of SDS increases when cool and wet conditions occur soon after planting. Recently, multiple seed treatment and foliar products have been registered and advertised for management of SDS but not all have been tested side by side in the same field experiment at multiple field locations. In 2015 and 2016, seed treatment fungicides fluopyram and thiabendazole; seed treatment biochemical pesticides citric acid and saponins extract of Chenopodium quinoa; foliar fungicides fluoxastrobin + flutriafol; and an herbicide, lactofen, were evaluated in Illinois, Indiana, Iowa, Michigan, South Dakota, Wisconsin, and Ontario for SDS management. Treatments were tested on SDS-resistant and -susceptible cultivars at each location. Overall, fluopyram provided the highest level of control of root rot and foliar symptoms of SDS among all the treatments. Foliar application of lactofen reduced foliar symptoms in some cases but produced the lowest yield. In 2015, fluopyram reduced the foliar disease index (FDX) by over 50% in both resistant and susceptible cultivars and provided 8.9% yield benefit in susceptible cultivars and 3.5% yield benefit in resistant cultivars compared with the base seed treatment (control). In 2016, fluopyram reduced FDX in both cultivars by over 40% compared with the base seed treatment. For yield in 2016, treatment effect was not significant in the susceptible cultivar while, in the resistant cultivar, fluopyram provided 3.5% greater yield than the base seed treatment. In this study, planting resistant cultivars and using fluopyram seed treatment were the most effective tools for SDS management. However, plant resistance provided an overall better yield-advantage than using fluopyram seed treatment alone. Effective seed treatments can be an economically viable consideration to complement resistant cultivars for managing SDS.

Soybean Sudden Death Syndrome Causal Agent Fusarium brasiliense Present in Michigan.

Sudden death syndrome (SDS), caused by members of Fusarium solani species complex (FSSC) clade 2, is a major and economically important disease in soybean worldwide. The primary causal agent of SDS isolated to date in North America has been F. virguliforme. In 2014 and 2016, SDS symptoms were found in two soybean fields located on the same farm in Michigan. Seventy Fusarium strains were isolated from roots of the SDS-symptomatic soybeans in two fields. Phylogenetic analysis of partial sequences of elongation factor-1α, the nuclear ribosomal DNA intergenic spacer region, and the RNA polymerase II beta subunit revealed that the primary FSSC species isolated was F. brasiliense (58 and 36% in each field) and the remaining Fusarium strains were identified as F. cuneirostrum, F. phaseoli, an undescribed Fusarium sp. from FSSC clade 2, and strains in FSSC clade 5 and FSSC clade 11. Molecular identification was supported with morphological analysis and a pathogenicity assay. The soybean seedling pathogenicity assay indicated that F. brasiliense was capable of causing typical foliar SDS symptoms. Both root rot and foliar disease severity were variable by strain, just as they are in F. virguliforme. Both FSSC 5 and FSSC 11 strains were also capable of causing root rot, but SDS foliar symptoms were not detected. To our knowledge, this is the first report of F. brasiliense causing SDS in soybean in the United States and the first report of F. cuneirostrum, F. phaseoli, an as-yet-unnamed Fusarium sp., and strains in FSSC clade 5 and FSSC clade 11 associated with or causing root rot of soybean in Michigan.

Quantitative trait loci underlying host responses of soybean to Fusarium virguliforme toxins that cause foliar sudden death syndrome.

Soybean deploys multiple genetic mechanisms to confer tolerance to Fusarium virguliforme toxins. This study revealed that F. virguliforme culture filtrates could be used in mapping QTL underlying foliar SDS resistance. Sudden death syndrome (SDS) is a major soybean disease throughout most of the soybean growing regions in the world including the United States. The disease is caused by the fungal pathogen, Fusarium virguliforme (Fv). The fungus produces several toxins that are responsible for development of interveinal leaf chlorosis and necrosis, which are typical foliar SDS symptoms. Growing of resistant cultivars has been the most effective method in controlling the disease. The objective of the present study was to identify quantitative trait loci (QTL) underlying host responses of soybean to Fv toxins present in culture filtrates. To accomplish this objective, two recombinant inbred line (RIL) populations, AX19286 (A95-684043 × LS94-3207) and AX19287 (A95-684043 × LS98-0582), segregating for SDS resistance were evaluated for foliar symptom development by applying two screening protocols, the stem cutting and the root feeding assays. The AX19286 population revealed two major and seven minor QTL for SDS resistance. In the AX19287 population, we identified five major QTL and three minor QTL. The two QTL mapped to Chromosome 7 [molecular linkage group (MLG) M] and Chromosome 20 (MLG I) are most likely novel, and were detected through screening of the AX19287 population with stem cutting and root feeding assays, respectively. This study established that Fv culture filtrates could be employed in mapping QTL underlying foliar SDS resistance. The outcomes of the research also suggest that multiple genetic mechanisms might be used by soybean to overcome the toxic effects of the toxins secreted by the pathogen into culture filtrates.

Contributions of Fusarium virguliforme and Heterodera glycines to the disease complex of sudden death syndrome of soybean.

BackgroundSudden death syndrome (SDS) of soybean caused by Fusarium virguliforme spreads and reduces soybean yields through the North Central region of the U.S. The fungal pathogen and Heterodera glycines are difficult to manage.Methodology/Principal FindingsThe objective was to determine the contributions of H. glycines and F. virguliforme to SDS severity and effects on soybean yield. To quantify DNA of F. virguliforme in soybean roots and soil, a specific real time qPCR assay was developed. The assay was used on materials from soybean field microplots that contained in a four-factor factorial-design: (i) untreated or methyl bromide-fumigated; (ii) non-infested or infested with F. virguliforme; (iii) non-infested or infested with H. glycines; (iv) natural precipitation or additional weekly watering. In years 2 and 3 of the trial, soil and watering treatments were maintained. Roots of soybean ‘Williams 82’ were collected for necrosis ratings at the full seed growth stage R6. Foliar symptoms of SDS (area under the disease progress curve, AUDPC), root necrosis, and seed yield parameters were related to population densities of H. glycines and the relative DNA concentrations of F. virguliforme in the roots and soil. The specific and sensitive real time qPCR was used. Data from microplots were introduced into models of AUDPC, root necrosis, and seed yield parameters with the frequency of H. glycines and F. virguliforme, and among each other. The models confirmed the close interrelationship of H. glycines with the development of SDS, and allowed for predictions of disease risk based on populations of these two pathogens in soil.Conclusions/SignificanceThe results modeled the synergistic interaction between H. glycines and F. virguliforme quantitatively in previously infested field plots and explained previous findings of their interaction. Under these conditions, F. virguliforme was mildly aggressive and depended on infection of H. glycines to cause highly severe SDS.

Synergism in the interaction of Fusarium virguliforme with Heterodera glycines in sudden death syndrome of soybean

Sudden death syndrome (SDS) of soybean caused by Fusarium virguliforme has increased in geographical distribution in the North Central region of the U.S. The disease often co-occurs with the widely distributed Heterodera glycines. The extensiveness of the interaction of SDS and H. glycines at different soil moisture levels is not fully defined. Further, it is not clear if Meloidogyne spp., that recently is more frequently observed in soybean areas, forms a disease complex with F. virguliforme. In a multi-factor factorial-designed mi-croplot experiment, SDS symptoms and yield parameters were determined following infestation with F. virguliforme and either H. glycines or M. incognita at different soil moisture regimes in different microbial backgrounds rendered by soil fumigation. On soybean ‘Williams 82’, susceptible to the three pathogens, H. glycines increased severity of foliar symptoms of SDS irrespective of being naturally present or added to previously fumigated soil, while yield parameters declined in the plots co-infested with F. virguliforme. This increase was synergistic in some contexts as determined by Gowing’s formula. In pre-season-fumigated soil, only plants in plots concomitantly inoculated with H. glycines and F. virguliforme had more severe SDS than plots with no nematode or M. incognita amendment when the plots were heavily watered (P < 0.01). No synergism between F. virguliforme and M. incognita was detected. The results provided the conceptual framework of the synergistic interaction of H. glycines and F. virguliforme in a disease complex under different soil moisture conditions.

Investigation of the Fusarium virguliforme fvtox1 mutants revealed that the FvTox1 toxin is involved in foliar sudden death syndrome development in soybean

The soil borne fungus, Fusarium virguliforme, causes sudden death syndrome (SDS) in soybean, which is a serious foliar and root rot disease. The pathogen has never been isolated from the diseased foliar tissues; phytotoxins produced by the pathogen are believed to cause foliar SDS symptoms. One of these toxins, a 13.5-kDa acidic protein named FvTox1, has been hypothesized to interfere with photosynthesis in infected soybean plants and cause foliar SDS. The objective of this study is to determine if FvTox1 is involved in foliar SDS development. We created and studied five independent knockout fvtox1 mutants to study the function of FvTox1. We conducted Agrobacterium tumefaciens-mediated transformation to accomplish homologous recombination of FvTox1 with a hygromycin B resistance gene, hph, to generate the fvtox1 mutants. Approximately 40 hygromycin-resistant transformants were obtained from 10(6) conidial spores of the F. virguliforme Mont-1 isolate when the spores were co-cultivated with the A. tumefaciens EHA105 but not with LBA4044 strain carrying a recombinant binary plasmid, in which the hph gene encoding hygromycin resistance was flanked by 5'- and 3'-end FvTox1 sequences. We observed homologous recombination-mediated integration of hph into the FvTox1 locus among five independent fvtox1 mutants. In stem-cutting assays using cut soybean seedlings fed with cell-free F. virguliforme culture filtrates, the knockout fvtox1 mutants caused chlorophyll losses and foliar SDS symptoms, which were over twofold less than those caused by the virulent F. virguliforme Mont-1 isolate. Similarly, in root inoculation assays, more than a twofold reduction in foliar SDS development and chlorophyll losses was observed among the seedlings infected with the fvtox1 mutants as compared to the seedlings infected with the wild-type Mont-1 isolate. These results suggest that FvTox1 is a major virulence factor involved in foliar SDS development in soybean. It is expected that interference of the function of this toxin in transgenic soybean plants will lead to generation of SDS-resistant soybean cultivars.

The Fusarium virguliforme Toxin FvTox1 Causes Foliar Sudden Death Syndrome-Like Symptoms in Soybean

Fusarium virguliforme causes sudden death syndrome (SDS) in soybean. The pathogen has never been isolated from diseased foliar tissues; therefore, one or more toxins have been considered to cause foliar SDS development. Cell-free F. virguliforme culture filtrates containing a toxin causes foliar SDS in soybean. A low-molecular-weight protein of approximately 13.5 kDa (FvTox1), purified from F. virguliforme culture filtrates, produces foliar SDS-like symptoms in cut soybean seedlings. Anti-FvTox1 monoclonal antibodies raised against the purified FvTox1 were used in isolating the FvTox1 gene. In the presence of light, recombinant FvTox1 protein expressed in an insect cell line resulted in chlorosis and necrosis in soybean leaf disks that are typical foliar SDS symptoms. SDS-susceptible but not the SDS-resistant soybean lines were sensitive to the baculovirus-expressed toxin. The requirement of light for foliar SDS-like symptom development indicates that FvTox1 induces foliar SDS in soybean, most likely through production of free radicals by interrupting photosynthesis.

Interaction of Fusarium solani f. sp. glycines and Heterodera glycines in Sudden Death Syndrome of Soybean

ABSTRACT Sudden death syndrome (SDS) of soybean is caused by the soilborne Fusarium solani f. sp. glycines (synonym F. virguliforme). In a sequential approach, two multifactor factorial-design microplot experiments were conducted to investigate the effects of fungal infestation levels and soil moisture on both root necrosis and foliar SDS severity, and the interaction between F. solani f. sp. glycines and Heterodera glycines in fumigated versus nonfumigated soil. In 2003, soybean cv. Spencer was grown in nonfumigated or methyl bromide-fumigated soil and infested with increasing levels of F. solani f. sp. glycines, either under rainfall or irrigated after growth stage V6/R1. In 2004, interactions between F. solani f. sp. glycines and H. glycines were explored in a factorial inoculation design in fumigated or nonfumigated soil, planted to Williams 82 or Cyst-X20-18. In both years, higher levels of foliar SDS severity and root necrosis were found in F. solani f. sp. glycines-infested soils with H. glycines than in soils without the nematode on the soybean cultivars susceptible to both pathogens. Both natural infestations of H. glycines in 2003 and artificially amended populations of H. glycines in 2004 contributed to higher foliar SDS severity. More severe foliar SDS symptoms always were associated with more root necrosis, but elevated levels of root necrosis did not predict severe leaf symptoms. In contrast to the critical role of H. glycines, increasing fungal infestation levels had no significant effects on increasing either foliar SDS symptoms or root necrosis. Effects of moisture regime and fungal infestation levels also were examined in factorial greenhouse and growth chamber experiments. High soil moisture resulted in higher levels of SDS root necrosis. In the greenhouse, root necrosis increased at a higher rate in low soil moisture than the rate in high soil moisture. The two pathogens acted as a complex and the disease development was strongly dependent on high soil moisture.

Recent Outbreak of Soybean Sudden Death Syndrome Caused by Fusarium virguliforme and F. tucumaniae in Argentina.

Sudden death syndrome (SDS) of soybean was detected initially in Argentina during 1991-1992 in the Pampas Region and 1992-1993 in the Northwest Region. The first report of the fulfillment of Koch's postulates of SDS caused by Fusarium solani f. sp. glycines in Argentina was published in 2003 (3). Subsequently, analyses have shown that F. solani f. sp. glycines represents several morphologically and phylogenetically distinct species, including F. tucumaniae in Argentina and F. virguliforme in the United States (1). Isolations were made from plants that exhibited typical SDS symptoms (interveinal foliar chlorosis and necrosis leading to defoliation of the leaflets but not the petioles) from fields in Santa Fe and Buenos Aires provinces in 2001, 2002, and 2003. To determine which species are responsible for SDS in Argentina, cultures of eight slow growing isolates that developed bluish pigmentation and produced abundant macroconidia in sporodochia on potato dextrose agar were subjected to morphological and molecular phylogenetic analyses and pathogenicity tests. Morphological analyses demonstrated that three of the isolates were F. virguliforme and five were F. tucumaniae. Isolates of F. tucumaniae produced long and narrow sporodochial conidia while F. virguliforme produced diagnostic comma-shaped conidia. Molecular phylogenetic analyses of DNA sequences from multiple loci confirmed morphology-based identifications and showed that the soybean SDS pathogen in the United States, F. virguliforme, was also present in Argentina. To our knowledge, this is the first report of F. virguliforme in Argentina and of this pathogen outside the United States. Five isolates of F. tucumaniae and three isolates of F. virguliforme were used for pathogenicity tests. F. virguliforme isolate 171 provided by J. Rupe (University of Arkansas, Fayetteville) was used as a positive control. Soybean cultivars Ripley, RA 702, Pioneer 9492RR, Spencer, and A-6445RG were inoculated with each of the isolates tested in a greenhouse assay using soil infestation and toothpick methods (2). All eight isolates produced typical foliar SDS symptoms 15 to 25 days after inoculation. Severity of foliar symptoms averaged 3.3 for F. virguliforme, 2.6 for F. tucumaniae, and 3.3 for the positive control using a disease severity scale in which 1 = no symptoms and 5 = severely infected or dead plants. Under these conditions, F. virguliforme appeared to be more virulent than F tucumaniae. Noninoculated plants remained symptomless. Koch's postulates were confirmed with soybean cultivars RA 702 and A6445RG. Isolates recovered from symptomatic plants inoculated by the soil infestation and toothpick methods were identical to those used to inoculate the plant. Strains were recovered at frequencies of 100 and 60% from plants inoculated by the toothpick and soil infestation methods, respectively. To our knowledge, this is the first report of the fulfillment of Koch's postulates for F. tucumaniae and F. virguliforme in Argentina.

Response of Soybean Sudden Death Syndrome to Subsoil Tillage.

The soilborne pathogen Fusarium solani f. sp. glycines causes sudden death syndrome (SDS) of soybean. Previous research indicated that soil compaction related directly to disease foliar symptoms. Therefore, we hypothesized that decreasing soil compaction would increase soil porosity and provide a more aerated root zone that would hinder root infection by the fungus and decrease SDS foliar symptom severity. Two experimental areas (110 by 120 m) were established to evaluate the relationship between soil variables and SDS. Across the experimental area, strips (9.14 m wide) were subsoiled perpendicular to soybean rows to a depth of 40 to 45 cm, which alternated with strips that were not tilled. In both 1999 and 2000, subsoiling dramatically reduced foliar symptoms of SDS. Compared with no-till plots, subsoiled plots had lower soil bulk density, greater soil porosity, and less soil moisture. In areas where SDS occurs and soil compaction exists, the use of subsoiling can be used to reduce severity of foliar symptoms of SDS.

First Report of Sudden Death Syndrome Caused by Fusarium solani f. sp. glycines on Soybean in Pennsylvania.

A small, circular patch of soybean (Glycine max) showing symptoms consistent with sudden death syndrome (SDS) (2) was noted on July 25, 1998, in a producer's field in Jersey Shore, PA. Foliar symptoms included interveinal chlorosis and necrosis, leaf cupping, and leaf abscission. The vascular cylinder of roots and stems had areas of reddish-brown discoloration. A slow-growing Fusarium sp., which produced a bluish-purple color on potato dextrose agar, was isolated from the roots of several symptomatic plants. The fungus was identified as Fusarium solani by The Fusarium Research Center, The Pennsylvania State University. Koch's postulates were tested on soybean cultivars A2506, Stine 3171, Pioneer 9305 and 9306, and Jack. Five plants per cultivar were inoculated at growth stage V1 by pouring 35 ml of a 4 × 107 spores per ml suspension on the growth mix in each pot. Five plants per cultivar were treated similarly with sterile water. Foliar symptoms of SDS began to appear 3 weeks after inoculation. Seven weeks after inoculation, symptoms of interveinal chlorosis and/or necrosis, leaf cupping, and occasional leaf abscission were apparent on the inoculated plants and on several noninoculated plants. The percentage of the plant showing symptoms was recorded and converted to the 0 to 5 scale (in which 0 = 0%, 1 = 1-10%, 2 = 11-30%, 3 = 31-40%, 4 = 41-90%, and 5= 91-100% of the leaf area affected) used by Rupe (3). Regardless of the rating method, there was a significant difference (P = 0.0001) between inoculated and noninoculated plants. There were no significant differences among cultivars. Roots of the inoculated plants were frequently discolored, in contrast to those of the noninoculated plants. F. solani was isolated from the roots of 97% of the inoculated plants and 23% of the noninoculated plants. Fungus gnats were suspected of spreading the pathogen to the noninoculated plants (1). F. solani f. sp. glycines causes SDS in soybean and its identity is confirmed by the symptoms produced on soybean (2). The symptoms produced when soybean plants were inoculated in the greenhouse were consistent with those of SDS (2) and indicate that the F. solani isolate recovered from symptomatic plants in the field was F. solani f. sp. glycines. This is the first documented occurrence of SDS on soybean in Pennsylvania.

First Report of Fusarium solani f. sp. glycines Causing Sudden Death Syndrome of Soybean in Canada.

Sudden death syndrome (SDS), caused by Fusarium solani (Mart.) Sacc. f. sp. glycines, is a disease of soybean (Glycine max (L.) Merr.) in several central and southern states of the United States. In Ontario, Canada, individual soybean plants with typical foliar symptoms of SDS (1) have been observed annually in Kent County since 1993 but the causal organism was not isolated or identified. In 1996, plants with symptoms of SDS were observed in six fields located in Essex, Kent, and Lambton counties. Interveinal chlorosis and necrosis occurred on top leaves of affected plants and a pale brown discoloration occurred in the vascular system in lower stems and upper tap roots. Slow-growing isolates of F. solani f. sp. glycines with typical blue sporodochia were isolated from symptomatic plants on acidified potato dextrose agar (1). Root inoculation of 15 2-week-old seedlings with colonized oat kernals with each of five single-spore isolates caused typical SDS symptoms on 5-week-old soybean plants of cvs. Conrad, A2540, S19-90, and Ripley in the greenhouse. The severity and incidence of symptoms varied with cultivar and isolate. Of 125 plants inoculated, 6% of Conrad, 10% of A2540, 14% of S19-90, and 17% of Ripley plants developed foliar symptoms. Symptoms did not develop on noninoculated controls. F. solani f. sp. glycines was reisolated from roots of symptomatic plants. Although Ripley is known to have resistance to SDS (2), foliar and root symptoms developed following inoculation with each Ontario isolate of F. solani f. sp. glycines. Yield losses in 1996 were difficult to assess because of the scattered distribution of diseased plants in most fields. Diseased plants had few and poorly filled pods. In two fields, soybean growth was severely restricted in large areas covering 2 ha each; however, soybean cyst nematode (SCN) was present in both fields. SCN was present at all locations. Although total yield losses are currently low, it is evident that F. solani f. sp. glycines causing SDS has become widely distributed in southwest Ontario and disease severity is increasing.

Effect of Plant Age, Maturity Group, and the Environment on Disease Progress of Sudden Death Syndrome of Soybean

Disease progress of sudden death syndrome (SDS) of soybean, caused by Fusarium solani, was determined in a standard susceptible cultivar, Lee 74, planted uniformly throughout the test site and in 42 soybean cultivars representing maturity groups (MG) IV-VIII, 1986-1989. Disease severity was assessed weekly from the middle of July through the first of October using a visual rating scale of percent leaf area exhibiting foliar symptoms of SDS. The disease ratings were used to calculate the absolute infection rate (dy/dt) for each cultivar at each rating time and the area under the disease progress curve (AUDPC). In Lee 74, SDS progressed in two phases: an initial rapid increase in disease to about 35% leaf area affected and a slower increase after that point. This two-phase disease progress curve was fit by a segmented model using two exponential equations. The fits of these equations were highly significant (P 1%/day or, if lower than 1%/day, the highest dy/dt attained). DAP and dy/dt were significantly (P < 0.0001) related to AUDPC (R = −0.58 and R = 0.38, respectively). Cultivars susceptible to race 6 of the soybean cyst nematode (SCN), Heterodera glycines, the predominate race in the field, developed SDS 10 days earlier and had significantly higher levels of disease than cultivars resistant to race 6 of SCN. The earliest increases in SDS occurred between 71 and 77 DAP in 1986, 69 and 74 DAP in 1987, and 75 and 83 DAP in 1988 for most MGs. Accumulated heat for these periods was 910-942, 852-916, and 857-963 degree-days in 1986, 1987, and 1988, respectively. In 1987, three cultivars in MG VII and VIII had large increases 52 DAP after 608 degree-days. In general, however, disease increased at the same time across MGs, but at no specific reproductive stage

Cultivar Responses to Sudden Death Syndrome of Soybean

Forty-two soybean (Glycine max) cultivars representing maturity groups IV-VIII were evaluated for their response to sudden death syndrome (SDS), caused by Fusarium solani, over 3 yr in a field with a history of the disease. Disease severity was assessed weekly from the middle of July through September using a rating scale of 0-5 where 0=0%, 1=1-10%, 2=11-30%, 3=31-70%, 4=71-90%, and 5=>90% of the leaf area exhibiting foliar symptoms of SDS. Area under the disease progress curve was calculated for each cultivar(.)