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Rate-reducing resistance to Fusarium solani f. sp. phaseoli underlies field resistance to soybean sudden death syndrome.

SEVERE YIELD LOSSES Occur in soybean because of SDS caused by the fungus F. solani (Rupe, 1989; Roy et al., 1989; O'Donnell and Gray, 1995). Field resistance to SDS in adapted soybeans is incomplete and quantitative (Gibson et al., 1994; Hnetkovsky et al., 1996; Njiti et al., 1996). Although the pathogen is restricted to the roots, disease resistance is usually rated by leaf symptoms. Therefore, it is not clear whether field resistance represents a form of resistance or a form of tolerance (Parleviiet, 1979).

Race nonspecific resistance is never complete (hence the term partial) and is usually durable (Tooley and Grau, 1982; Wang et al., 1994; Chang et al., 1996). It retards the multiplication of the pathogen in the crop, so it has been termed rate-reducing resistance (Parlevliet, 1979; Tooley and Grau, 1982). Resistance may be expressed through a reduced infection frequency (IF), a longer latent period, reduced spore production or a combination of these. These components can be measured and used to predict cultivar resistance. Unfortunately, the procedures involved are laborious and time consuming. Therefore, breeders prefer to rely on established procedures for quantitative estimates of disease incidence (DI) and disease severity (DS) under field conditions. DI and DS combine the effects of IF, latent period, and spore production. However, DI and DS also measure tolerance in which infection is endured through a desensitization of the plant (Parlevliet, 1979; Tooley and Grail, 1982).

The use of DNA markers has made possible the dissection of field resistance to fungal pathogens into separate loci (Bubeck et al., 1993; Pe et al., 1993; Young et al., 1994; Wang et al., 1994; Li et al., 1995; Hnetkovsky et al., 1996). Each locus can potentially control one or several components of resistance or tolerance. Therefore, separation of field disease resistance into its components could be used to define the role of an individual locus.

Fusarium solani f. sp. phaseoli type A is characterized by slow growth on potato-dextrose agar, a slimy colony morphology with few micro conidia, and the production of macro conidia. The macro conidia often forms a blue to purple mass which stain the agar a deep maroon (Rupe, 1989). The identity of the sexual stage is not yet known. Therefore, the species designation is preliminary. However, a recent report that F. solani is a teleomorph of Nectria haematococca (Abney and Richards, 1994) is unlikely based on rRNA gene sequences (O'Donnell and Gray, 1995). The SDS pathogen is closely related to, but distinct from, F. solani f. sp. phaseoli, the causative organism of Fusarium root rot in Phaseolus vulgaris L. (Burke and Miller, 1983). Genetic fingerprinting using RAPD markers shows the existence of genetic variability and genotypic clusters among the F. solani SDS pathogenic strains and among infested field locations where SDS occurs (Achenbach et al., 1996). However, no convincing evidence exists for major differences among pathogenic strains in their pathotype so that races are not yet recognized. Other types of F. solani have been implicated in causing Essex disease (Farias and Griffin, 1990) and seedling disease complex (Killebrew et al., 1988) on soybeans. Therefore, the identification of distinct types of F. solani from soybean based on morphology can be difficult. However, molecular markers can be used for identification of f. sp and types of F. solani (O'Donell and Gray, 1995; Achenbach et al., 1996).

Disease etiology for SDS in soybean is typical of many fungal scorches of other plants. The fungus is soil-borne, infection probably occurs soon after seedling emergence, and throughout the life of the plant the pathogen is restricted to the taproot and lower stem, causing discoloration, and rotting (Rupe, 1989; Roy et al., 1989; O'Donnell & Gray, 1995). The rapid development of severe foliar chlorosis and necrosis, which prompted the disease name, occurs later during the reproductive stage of soybean growth (Gibson et al., 1994). Leaf symptoms may be caused by fungal toxin production (Lim et al., 1990). However, the plugging of xylem vessels by plant tyloses and/or xylem vessel plugging by aggregates derived from plant and fungal macromolecules may also cause or contribute to leaf symptoms (Bozzola et al., 1986). Severe reductions in soybean yields result from infection and symptom development. However, yield reductions are imperfectly correlated (r [is less than] 0.6) with leaf symptom development (Gibson et al., 1994). Root rotting caused by F. solani can be significant in the field but the degree of association with leaf symptom development or yield loss has not yet been adequately determined.

Soybean resistance to F. solani in the field is expressed over the growing season. Resistance may be expressed through a reduced IF, a longer latent period, reduced spore production, and hence a lower IS. Tolerance might be expressed through reduced leaf symptom development but would not affect IF or IS. The objectives of this study were to evaluate resistance in resistant and susceptible cultivars, to compare Essex and Forrest cultivars, and to determine the relationships between actual root infection and leaf symptom rating systems.


The 12 soybean cultavars used in this study included six established cultivar -- Essex (SDS-susceptible) (Smith and Camper, 1973), Forrest (SDS-resistant) (Hartwig and Epps, 1973), Ripley (SDS-resistant) (Cooper et al., 1990), Spencer (SDS-susceptible) (Wilcox et al., 1989), Jack (SDS-resistant) (Nickell et al., 1990), and A5403 (SDS-susceptible) (Asgrow Co., Kalamazoo, MI). One highly SDS-resistant plant introduction (PI 520733) was included. Five [F.sub.5] recombinant inbred lines derived from Essex X Forrest (EXF) were included. EXF 44, 59, and 78 each possess alleles for resistance at the four major SDS QTL, while ExF 18 and 83 each carry the four loci with alleles for SDS sensitivity (Hnetkovsky et al., 1996; Chang et al., 1996). Essex contributes one of the major SDS resistance loci. Forrest contributes the other three major SDS resistance loci. The nature of the loci contributing SDS resistance to the other cultivars is not known. The initial SDS resistance classification of genotypes were made by field evaluation (Gibson et al., (1994).

The soybean cultivars [five SDS-susceptible (S) and seven SDS-resistant (R)] (Table 1) were planted in a randomized complete block design in four row plots, four replications, and two locations. The Ridgway, IL, soil type was Bonnie silt loam, fine-silty mix, acid, mesic Typic Fluvaquents and the Ullin, IL, soil type was Patton silty-clay loam, fine-silty mix, mesic, Typic Haplaquolls. Experiments were planted on 26 May 1995 at Ridgway and on 5 June 1995 at Ullin. Rows were 0.75 m wide and 3.0 m long, with about 17 plants/m. The outer two rows were used for destructive sampling and the middle two rows were used for plot evaluation of SDS disease incidence and severity.


Each cultivar was sampled six times during the growing season. The first sample was taken at the V0 growth stage (emergence), eight DAP and the last sample at R8 (harvest maturity) (Fehr et al., 1971). To more closely study the pattern of root invasion by F. solani, Essex (SDS-susceptible) and Forrest (SDS-resistant) were sampled more intensively (17 times at Ridgway and 16 times at Ullin). For each time point, five plants per plot were randomly harvested, recovering at least 15 cm of the taproot. During later stages where leaf symptoms were evident, DS was rated on the individual plants sampled for comparison with F. solani recovery from the roots. Roots from sampled plants were transported on ice to the laboratory where they were stored at 4 [degrees] C (1-7 d) until they were processed for F. solani isolation and quantification.

Based on the finding by Rupe (1989) that the epidermal tissue of the taproot had the highest frequency of F. solani recovery, the isolation in this study was limited to the taproot. A restrictive medium was used that limited fungal growth and restricted bacterial growth. The restrictive medium was composed of 960 mL of distilled water, 0.012 g/mL potato-dextrose agar (PDA, Difco Laboratories Detroit, MI), 0.012 g/mL agar (Sigma Chemical Co. St. Louis, MO), 10 mL/L of 10% (v/v) tergitol NP-10 (Sigma Chemical Co., St. Louis), 10 mL/L of 0.025 g/mL penta-chloro-nitro-benzene (PCNB, 75% (w/v), Uniroyal Chemical Co. Inc., Middlebury, CT), 10 mL/L of 0.012 g/mL of tetracycline (Fisher Scientific, St. Louis) plus neomycin sulfate (Sigma Chemicals Co. St. Louis), and 10 mL/L of 0.002 g/mL of Botran (Gowan Co. Yuma, AZ). The PDA, agar, and NP-10 were added to distilled water and autoclaved. The antibiotics (tetracycline and neomycin sulfate) and fungicides (PCNB and Botran) were added when the medium had cooled to about 60 [degrees] C. The medium was poured into sterile petri dishes and allowed to gel.

The portion of the taproot from the soil line to 30 cm below was cut and lateral roots were removed. The taproots were washed with water containing 1% (v/v) detergent, rinsed in distilled water, and blotted dry. The taproots were surface sterilized in 100 mL/L NaClO for 3 min. Under sterile conditions the roots were blotted dry, dipped in dilute (40 [micro]g/mL) tetracycline solution, blotted dry, and placed on paper. With a sterile knife, each taproot was chopped into several 1-cm segments, six of which were randomly selected and placed on the restrictive medium. Each plant was treated separately. The plates were incubated at room temperature for 14 d. Pure colonies of all slow growing fungi from each segment were transferred onto fresh medium, consisting of 24 g/L of PDA and agar, 10 mL/L of 10% NP-10 and 0.064 g/L of tetracycline. The plates were allowed to incubate at room temperature for 14 d.

The percentage of plants yielding blue F solani from at least one segment was determined as IF. The percentage of segments yielding blue F. solani from all sampled plants of each plot were determined as IS. The results were then grouped under resistant and susceptible cultivars. Essex and Forrest were the only cultivars analyzed separately.

The data were subjected to ANOVA (SAS Institute Inc., Cary, NC), with mean separation by LSD. Graphs were constructed by Quattro Pro version 5.0 (Novell Inc., Orem, Utah). Correlations across genotype and covariance analysis were done with MSTAT-C (Michigan State University, 1984).

To verify the visual identification of F. solani, 10 isolates initially identified as F. solani f. sp. phaseoli type A and six isolates thought not to be F. solani f. sp. phaseoli type A were selected for molecular fingerprinting. Liquid PDA cultures were inoculated from the edge of a growing colony isolated from soybean after one subculture (not single spore derived). The F. solani DNA was extracted and purified (Achenbach et al., 1996). The internal spacer region of the ribosomal RNA gene cluster was amplified between primers ITS4 and ITS5 and subjected to EcoRl digestion (O'Donnell and Gray, 1995). RAPD profiles were generated for each isolate with primers OA04 and OG06 using standard conditions (Williams et al., 1990), except that 100 ng of DNA was used per amplification. DNA fragments were separated by electrophoresis in a 14 g/L agarose gel.


Comparisons between SDS-R and SDS-S Cultivars

All seven lines that were initially designated as SDS resistant (R) had low average DX (0.04-1.64, Table 1). Those that were initially designated as SDS susceptible (S) had high average DX (9.82-42.64). The data confirmed our designations of lines as SDS-R and SDS-S, based on previous field data and molecular marker assisted selections (Gibson et al., 1994; Hnetkovsky et al., 1996; Chang et al., 1996).

It was observed that both susceptible and resistant cultivars were initially infected by F. solani by 15 to 24 DAP and infection increased over the growing season (Fig. 1). At 8 DAP at Ullin and at 8 and 15 DAP at Ridgway, F. solani could not be recovered from surface sterilized taproots suggesting infection had not yet taken place. Over the growing season, the mean IF was higher (35.2-54.7) for susceptible cultivars than for resistant cultivars (25.4-42.3). IF was higher (P [is less than] 0.05) for susceptible cultivars (Fig. la, Fig. 1b). Separation between the two groups was significant at several time points (P [is less than] 0. 05) following the beginning of the reproductive stage (Fig. la, Fig. 1b) at individual sample time points later than 60 DAP at Ullin and later than 81 DAP at Ridgway.

IS development paralleled the pattern observed for IF increase. The SDS-R cultivars' IS seasonal mean ranged from 5.6 to 14.6, while the SDS-S cultivars' IS seasonal mean ranged from 10.0 to 20.0 (Table 1). Again, Ullin showed earlier separation between SDS-R and SDS-S cultivars (Fig. 1c) than Ridgway (Fig. 1d). Separation in IS was significant between the two soybean cultivar classes (P [is less than] 0.05) immediately following the onset of the reproductive period with several points after that showing significant separation.

Mean IF and IS consistently showed that the SDS-R class had significantly less FSA invasion of the roots than the SDS-S class in each location. However, for the two location average only IF was significantly different (Table 2).

Table 2. Mean infection frequency (IF) and infection severity (IS) by F. solani on soybean taproots of seven SDS resistant cultivars (SDS-R), five susceptible (SDS-S) cultivars, and Essex and Forrest, within locations and their mean.
                     Ullin            Ridgway            Mean
Genotype       IF            IS       IF     IS       IF     IS

SDS-R     38.2a([dagger])   14.0a   23.9a    6.9a   31.1a   10.7a
SDS-S     55.5b             22.8b   34.7b   11.7b   45.1b   17.4a
Forrest   44.5a             15.4a   21.6a    5.2a   33.1a   10.3a
Essex     65.3b             28.8b   41.3b   15.0b   53.3b   21.9b

([dagger]) Pairs of means within the same column and paired comparisons followed by the same letter are not significantly different (P < 0.05).

Forrest vs. Essex

Forrest (DX = 0. 13) ranked second to P1520733 (DX 0.04) in SDS resistance (Table 1). Essex (DX = 13.1) was only more resistant to SDS than Spencer, E X F 83, and E X F 18 (DX = 33.3, 37.9, and 42.6 respectively, Table 1). Therefore, the initial designation of Forrest as stably and durably SDS-R and Essex as consistently SDS-S (Gibson et al., 1994; Hnetkovsky et al., 1996; Chang et al., 1996) was confirmed.

The mean IF and mean IS (Table 2) consistently showed that Forrest was significantly less infected by F. solani than Essex both within and across locations. However, data for the individual cultivars was much more variable than for the SDS cultivar class data. This reflected greater variability caused by fewer samples contributing to the mean (five taproots and 30 sections compared with 25 to 35 taproots and 150-195 sections).

At Ridgway in 1995, the first isolation of F. solani from the taproot occured at 24 DAP (16 June, Fig. 2b). At 35 DAP, a significantly (P [is less than] 0.05) higher IF for Forrest than Essex occurred. However later than 35 DAP, the IF was consistently higher in Essex than Forrest (Fig. 2a). At Ridgway, the two cultivars were significantly (P [is less than] 0.05) separated at several sampling time points immediately following the beginning of the reproductive stage and the onset of disease (Fig. 2b). At Ullin in 1995, the first isolation of blue F. solani was at 15 DAP (20 June) (Fig. 2a). Forrest and Essex had about the same IF until about 53 DAP when the two cultivars were clearly separated with Essex having a higher IF than Forrest. The cultivars were significantly (P [is less than] 0.05) separated by IF at several time points after the beginning of reproduction and the onset of leaf symptoms (Fig. 2a).

At Ridgway 1995, IS (Fig. 2d) showed a similar pattern to IF. Again at 35 DAP Forrest had a significantly (P [is less than] 0.05) higher IS than Essex. However, after the beginning of reproduction, Essex had a significantly (P [is less than] 0.05) higher IS than Forrest at several sampling time points. At Ullin 1995, the general pattern of IS development was similar to that of IF, but only two time points showed significant separation (Fig. 2c) of genotypic classes.

Genotype X Environment Interaction

Combined location analysis of variance on all cultivars showed that significant (P [is less than] 0.05) genotype X location interaction occurred in all disease measures (Table 3). However, when the analysis was restricted to Essex and Forrest, the genotype X location interaction was not significant (Table 3). A significant genotype X location interaction is an indication that there was either a fungal strain (or race) specific response by some cultivars, or that there were specific environmental factors that control the different SDS responses.
Table 3. Combined location analysis of variance for all genotypes
and Essex and Forrest.

                               Disease         Infection
                                index          frequency
Source of variation    df    MS        F      MS        F

SDS Resistance Class

Genotype               11   2156   10.3(*)    753     4.1(*)
Location                1   1334    6.3(*)   7596    41.1(*)
Location X Genotype    11    210    4.3(*)    185     3.3(*)
Pooled Error           33     49               56

Essex and Forrest

Genotype                1    416    1.0      2204   169(*)
Location                1    673    1.6      1644   126(*)
Location X Genotype     1    412    4.3         1     0.1
Pooled Error            6     96               13

Source of variation               MS      F

SDS Resistance Class

Genotype                          176    1.7ns
Location                         2460   24.1(*)
Location X Genotype               102   10.2(*)
Pooled Error                       10

Essex and Forrest

Genotype                          626   19.0(*)
Location                          432   13.1(*)
Location X Genotype                33    3.7
Pooled Error                        9

(*) = F-value significant at P [is less than or equal to] 0.05. The F-test denominator was the one appropriate for genotype and locations both considered random effects.

The significant genotype X environment interaction showed that cultivars responded differently in different environments. The genotype X environment interaction has been common with SDS response (Rupe and Gbur, 1995; Gibson et al., 1994; Njiti et al., 1996). The G X E interaction might reflect the occurrence of pathotypes of F solani (Lim and Jin, 1991) or environmental factors that alter the plant's response to the pathogen (Gibson et al., 1994; Rupe and Gbur, 1995; Njiti et al., 1996). In either case, breeders should develop cultivars with broad-based resistance rather than cultivars with environment or pathotype specific resistance to SDS.

Correlation between Taproot Infection and SDS Leaf Symptoms

Across all genotypes the disease index was significantly associated with IF and IS at both Ridgway (r = 0.61 and 0.37 respectively) and Ullin (r = 0.38 and 0.29, respectively). Therefore, leaf symptoms may be used to roughly predict the effect of plant resistance on infection by F. solani. In addition, a significant correlation occurred between IF and DS on an individual plant basis at Ridgway (r = 0.62). Therefore, DI, DS, and DX are imperfect indicators of IF and IS.

Implications for Field Management

The first infection of soybeans by F. solani occured at Ullin within 15 DAP and at Ridgway within 24 DAP (Fig. 1 and Fig. 2). The variation may be caused by environmental conditions at planting. While the soil types were different, both environments have poorly drained soils. However, soil moisture content at planting was higher at Ullin than at Ridgway and might have increased the rapidity of infection at Ullin. Gibson et al. (1994) have noted that high soil moisture at planting accelerated stem browning and SDS leaf symptoms. Our data suggests that by delaying planting in wet fields to allow drying, the time to first infection may be increased and the infection severity might be decreased.

The pattern of infection later in the growing season was consistent between locations. IF and IS increased gradually, reaching their peaks after the onset of reproduction (Fig. I and 2). Higher IF during the reproductive period may be due to cumulative secondary infections or the spread of a primary infection (Parlevliet, 1979; Tooley and Grau, 1984). The gradual spread of a primary chronic infection to exceed some threshold level of IS could explain the sudden and unpredictable onset of leaf symptoms of SDS (Gibson et al., 1994). It has been observed that SDS is more severe in highly productive fields and among productive cultivars (Rupe et al., 1993). Therefore, fertile fields with a history of SDS should be planted with the most highly resistant cultivars available.

Implications for Breeding Resistance to SDS

SDS susceptible cultivars were infected and colonized by F solani more than the SDS resistant cultivars (Fig. I and 2). However, since all the SDS resistant cultivars were infected and colonized, the resistance possessed by these genotypes is partial. Partial resistance was consistent with reports of field resistance to SDS based on the appearance of leaf symptoms (Gibson et al., 1994; Hnetkovsky et al., 1996; Chang et al., 1996; Njiti et al., 1996). Partial resistance in the field is not consistent with the complete resistance to SDS leaf symptoms conditioned by rfs in the greenhouse (Stephens et al., 1993).

It is often observed that SDS is more severe in highly productive fields (Gibson et al., 1994) and cultivars (Rupe and Gbur, 1995). Possibly this is caused by competition between the plant's reproductive mechanisms and defense mechanisms that causes SDS severity to increase. Our data suggests that in the early reproductive phase both IF and IS increase substantially but in later stages infection and colonization is limited in resistant genotypes. Therefore, new cultivars. intended for use in highly productive, but F. solani infested, areas may need to be selected for increased resistance to SDS during the early reproductive stage.

Although a positive relationship between IF and SDS leaf symptoms occurred, several plants with no leaf symptoms but high IF were noted. Molecular markers were used to verify that fungal identification by morphological traits was accurate. More than 80% of isolates tested by ITS amplification and RAPD profiles were clearly F. solani. The remainder may have been mixed cultures (data not shown). The occurrence of high levels of infection without leaf symptom development suggests a tolerance with environmental sensitivity exists and may be confused with resistance in SDS evaluations by DI and DS. Therefore, effective breeding should use a combination of root invasion rating, leaf symptom rating, and molecular marker data as selection criteria rather than leaf symptoms alone. Plant sampling for IF and IS after reproduction begins should be an effective strategy for resistance evaluation as it is for DI and DS rating (Gibson et al., 1994).

Field resistance to SDS can be classified as incomplete, horizontal rate-reducing resistance (Parlevliet, 1979). This type of resistance is often inherited multigenically, as in crosses with Forrest and Pyramid (Hnetkovsky et al, 1996; Chang et al., 1996; Njiti et al., 1996). Rate-reducing resistance is very difficult to improve by conventional selection because of its multigenic nature and interactions with the environment (Hnetkovsky et al., 1996; Njiti et al., 1996). However, resistance to SDS by Forrest, and progeny lines of Essex X Forrest, has been stable across environments and durable over many years and QTL underlying resistance have been identified (Gibson et al., 1994; Hnetkovsky et al., 1996; Chang et al., 1996). Therefore, with marker assisted selection for SDS resistance QTL we can minimize the use of multiple environments as the selection unit (Njiti et al., 1996) and the concomitant delays in cultivar development. Marker assisted selection will play a major role in developing stronger rate-reducing resistance to SDS (Hnetkovsky et al., 1996; Chang et al., 1996).

The resistance mechanism was shown to be similar in four cultivars used as sources of SDS resistance (Forrest, Ripley, Jack, and P1520733). Unfortunately, the allelic nature of inheritance of field resistance to SDS in Ripley, Jack, and P1520733 compared with Forrest has not been determined. Gene pyramiding might not be effective if the SDS resistance loci were allelic in all resistant cultivars. However, germplasm screening by IF and IS in the field may identify novel mechanisms of tolerance and resistance. In addition, IF and IS will be useful to measure the relative degree of resistance to SDS within groups of highly resistant cultivars or RILs selected by markers where leaf symptom scoring is ineffective (Hnetkovsky et al., 1996).

Cultivars Essex and A5403 showed intermediate DX but high IF and IS, implying some tolerance to SDS that was different from resistance in the resistant cultivars. In fact, Essex contributes at least one major QTL for SDS resistance detected in an Essex X Forrest RIL population. The unfavorable allele is carried by Forrest, EXF83, and EXF18 (Hnetkovsky et al., 1996). This QTL is not associated with yield protection in F. solani infested environments, unlike the other three major SDS resistance QTL with beneficial alleles from Forrest (Hnetkovsky et al., 1996). The possibility that this QTL is involved in SDS tolerance will be explored by estimation of IF, IS, and DX in near isogeneic lines in 1996.


Particular thanks to J. Klein and Dr. M. Schmidt for excellent management of the field program in southern Illinois. Thanks to all the workers on the SDS field team at Southern Illinois University at Carbondale during 1995. We thank G. Torto R. Gelin, R. Prabhu, J. Abu-Thredeih, and R. Massinga for assistance with the molecular fingerprinting. We thank Dr. O. Myers Jr. for critical reading of the manuscript. This work was supported in part by grants from the Illinois Soybean Program Operating Board Nos. 93-19-132-3 and 94-20-143-3, and North Central Soybean Program Operating Board Nos. 95-20-431 and 95-20-432.


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Abbreviations: DAP, days after planting; DI, disease incidence; DS, disease severity; DX, disease index; IF, infection frequency; IS, infection severity; QTL, quantitative trait loci; R, resistant; RAPD, random amplified polymorphic DNA; RIL, recombinant inbred line; S, susceptible; SDS, sudden death syndrome.

V.N. Njiti, R.J. Suttner, L.E. Gray, P.T. Gibson, and D.A. Lightfoot(*)

V.N. Njiti, R.J. Suttner, P.T. Gibson and D.A. Lightfoot, Dep. of Plant and Soil Science, Molecular Science Program, Southern Illinois Univ., Carbondale, IL 62091; and L.E. Gray, USDA, ARS, Dep. of Crop Science, Univ. of Illinois, Urbana, IL 61801. Authors names are necessary to report factually on the available data; however, the USDA neither guarantees nor warrants the standard of the product, and the use of the name by USDA implies no approval of the product to the exclusion of others that may also be suitable. Received 12 Feb. 1996. (*) Corresponding author (GA4082@SIU.EDU).

Published in Crop Sci. 37:132-138 (1997).
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Author:Njiti, V.N.; Suttner, R.J.; Gray, L.E.; Gibson, P.T.; Lightfoot, D.A.
Publication:Crop Science
Date:Jan 1, 1997
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