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CROP BREEDING, GENETICS & CYTOLOGY

Evaluation of a QTL for Waterlogging Tolerance in Southern Soybean Germplasm

^a Dep. Crop, Soil and Environmental Science, Univ. of Arkansas, Fayetteville, AR 72701
^b Dep. of Agronomy, Univ. of Missouri Delta Center, Portageville, MO 63873
^c Dep. Horticulture and Crop Science, The Ohio State Univ., Wooster, OH 44691

^* Corresponding author (sneller.5{at}osu.edu).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Water-saturated soils and flooding (submergence) can greatly reduce soybean [Glycine max (L.) Merr.] yield. Mapping analyses with the simple sequence repeat (SSR) marker Sat_064 have identified a quantiative trait locus (QTL) for tolerance to waterlogging in the cultivar Archer. Our objectives were to evaluate the effect of this QTL on waterlogging tolerance in southern environments and genetic backgrounds, and to assess variability for waterlogging tolerance in Archer derived populations. We used Sat_064 genotype data to create seven sets of NILs from the populations A5403 x Archer and 9641 x Archer. The NILs were grown under waterlogged (water level 70–120 mm above the soil surface for 2 wk starting at flowering) and irrigated control conditions at three environments in 1999 and 2000 and evaluated each for yield and visual waterlogging injury. Waterlogging injury was rated on a 0 (no symptoms) to 9 (>90% severely chlorotic or dead) scale. Checks and select RILs from the same crosses were also tested. Additional RILs from each population were tested for waterlogging injury in 2000. The Sat_064 marker did not account for a significant portion of the variability among the NILs for either waterlogging tolerance based on yield, yield in waterlogged conditions, or waterlogging injury. This may be due to the southern genetic backgrounds and environments in this study as the Sat_064 QTL was originally identified in northern genetic backgrounds and environments. Variation for waterlogging tolerance and waterlogging injury was noted in the RIL populations. The most tolerant RILs suffered a 32% yield reduction from waterlogging and had a waterlogging injury rating of 1.3 while the most susceptible RILs suffered a 77% yield loss and had a waterlogging injury score of 6.8. The populations segregated for waterlogging tolerance independently of the Sat_064 marker. Visual assessment of waterlogging injury was associated with yield-based assessment of waterlogging tolerance and could be used to select for lines with improved waterlogging tolerance.

Abbreviations: NIL, near isogenic lines • QTL, quantitative trait loci • RIL, recombinant inbred lines • SSR, simple sequence repeat

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
EXCESS SOIL MOISTURE causes waterlogging (root or a portion of the shoot is submerged in water) or complete submergence, and is estimated to affect 12% of the agricultural soils in the USA (Boyer, 1982). Waterlogging can be caused by inadequate drainage of soils after intense rainfall, excessive irrigation, or from a rising water table (Scott et al., 1990). Soybean is a major crop in the Midsouth. Yield losses in soybean because of waterlogging are common in the Midsouth because of the prevalence of heavy clay soils, poor surface drainage in areas with limited slope, poor soil structure, heavy rains, and cropping practices. For example, soybean in the Midsouth is often grown in rotation with rice (Oryza sativa L.) in fields that are ideal for flooded rice production, but suboptimal for soybean. Soybean is subjected to potential waterlogging damage in these fields because of the poor surface and internal soil drainage and the use of the same waterlogging irrigation system for the rice and soybean crops.

Waterlogging can greatly reduce soybean yield. In the Midsouth, yield can be reduced 17 to 43% if soybean is subjected to waterlogging at the vegetative growth stage, while yield can be reduced by 50 to 56% if waterlogging stress occurs at reproductive growth stages (Oosterhuis et al., 1990; Scott et al., 1990). Scott et al. (1989) estimated soybean yield in Arkansas is reduced by 89 and 129 kg ha^-1 per day of waterlogging stress at the vegetative and reproductive stages, respectively. In Ohio, Van Toai et al. (1994) reported that exposure to waterlogging for 4 wk beginning at flowering reduced the yield of 84 soybean cultivars by 25%. Several researchers report that soybean yield is more affected by waterlogging stress at the reproductive stages than at the vegetative stages (Linkemer et al., 1998; Oosterhuis et al., 1990; Scott et al., 1989, 1990). Yield losses from excess soil moisture likely arise from reduced root growth, nodulation, nitrogen fixation, photosynthesis, biomass accumulation, stomatal conductance, and plant death due to diseases and physiological stress (Oosterhuis et al., 1990; Sallam and Scott, 1987a, b; Schmitthenner, 1985; Scott et al., 1990).

Increasing the tolerance of soybean to waterlogging could increase yield in soils prone to waterlogging. Some tolerance to waterlogging has been reported. Van Toai et al. (1994) reported some tolerance among soybean cultivars adapted to the northern USA. Tolerance was defined as improved relative yield under stress conditions as compared with the control condition. The tolerance they reported was not associated with yield under nonstress conditions, maturity, height, or reaction to Phytophthora sojae Kaufmann & Gerdemann, a fungal pathogen of soybean that is prevalent in wet soils. These results suggest the existence of tolerance to soil waterlogging in soybean.

Tolerance to waterlogging has been noted in other crops and appears to be quantitatively inherited (Boru et al., 2001; Setter et al., 1997; Xu and Mackill, 1996). Breeding for stress tolerance controlled by multiple genes is difficult because of low heritability, variability among stress treatments, and the difficulty of screening large numbers of progeny in field or greenhouse assays of tolerance. Marker-assisted selection could be very useful. QTL for tolerance to waterlogging have been reported in rice (Xu and Mackill, 1996) and soybean (Van Toai et al., 2001). The allele for soybean tolerance to waterlogging was found in the cultivar Archer with the SSR marker Sat_064 from linkage group G (Cregan et al., 1999). Averaged over two RIL populations and two waterlogged trials in the northern USA, RIL families with the Archer allele at Sat_064 yielded 95% more, and were 16% taller than RIL families without the Archer allele (Van Toai et al., 2001).

Breeders realize that results from initial QTL mapping studies must be confirmed in additional genetic backgrounds and environments to assess fully the feasibility of marker-assisted selection (Reyna and Sneller, 2001). Our objectives were to evaluate the effect of this QTL on waterlogging tolerance in southern environments and genetic backgrounds, and to assess variability for waterlogging tolerance in Archer-derived populations.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Genetic Material
We created sets of NILs for the Sat_064 marker by selecting heterozygous F6 plants from populations inbred by single pod descent from the crosses ‘Asgrow A5403’ x Archer and ‘Pioneer 9641’ x Archer. The F6 populations were grown in 1996 and about 300 F6 plants from each cross were genotyped with Sat_064. Flanking markers within 10 centimorgans (cM) of Sat_064 (Cregan et al., 1999) were monomorphic for our populations and could not be used to create NILs. Seed from F6 plants that were heterozygous for Sat_064 alleles were harvested and the F6:7 families were grown in 1997. About 20 F7 plants from each segregating F6:7 were genotyped with the Sat_064 marker. F7 plants that were homozygous for the Archer allele or the southern (A5403 or 9641) allele were selected and harvested as F7:8 families. Multiple F7:8 families with the desired homozygous genotype were identified from some F6:7 families. These F7:8 families were maintained as separate lines. Thus a NIL set consisted of several F7 derived families homozygous for the Archer allele and several families homozygous for the southern allele (Table 1). NILs were not developed from F6:7 families that had poor agronomic value due to shattering, lodging, or deviant maturity in the 1997 plots. The selected F7:8 families were grown in Costa Rica during the winter of 1997-1998. The F7:9 families were grown in Stuttgart, AR, in 1998 as part of the waterlogging tolerance study. Poor stands rendered the 1998 data unsuitable for waterlogging tolerance analysis for most lines, though some waterlogging injury data was used to make some selections (see below). Seed was harvested from the 1998 plots though and the F7:10 seed was used to plant the 1999 study while F7:11 seed was used to plant the 2000 study. In the 1999 and 2000 trials, problems with stand (e.g., plots with stands <70% of desired population and with skips), shattering, lodging, and maturity still occurred such that reliable high quality data for waterlogging tolerance was only derived from seven sets of NIL (Table 1). Data from these seven NIL sets were analyzed in this study.

Data from the 1998 and 1999 studies indicated possible segregation for waterlogging tolerance and waterlogging injury in the two crosses. In 2000, we added a study of waterlogging injury involving 101 F6 derived RILs from A5403 x Archer and 63 F6 derived RILs from 9641 x Archer. We used F6:10 seed to plant the 2000 trial.

SSR Genotyping
The Sat_064 genotype was determined by first isolating DNA from leaves of field grown plants. Trifoliate leaves from individual plants were freeze dried and homogenized. The IsoQuick (ORCA Research Inc., Bothell, WA) kit was used to isolate DNA. The DNA was extracted by the extraction procedure described in the IsoQuick procedure with some modifications. Approximately 8 mg of freeze dried tissue was used. Step 1 of the procedure was modified by adding 100/50 µL lysis solution and sample buffer mix to each microcentrifuge tube. In step 2, only 500 µL of extraction matrix (reagent 2) was added to the sample lysate. After step 3, each sample was incubated in a 65°C water bath for 5 min and then vortexed for 10 s. No other modifications were done to the procedure. DNA quantification was performed with a fluorometer with the wavelength set between 365 and 460 nm. All samples were diluted with sterile water to a concentration of 500 ng of DNA/µL or 100 ng of DNA/µL depending on original concentration.

Reaction mixes for polymerase chain reaction (PCR) included: 10 ng of soybean genomic DNA, 2.5 mM Mg⁺², 0.5 µM of each Sat_064 primer, 100 µM of each nucleotide, 1x PCR buffer, 1x dye, and 0.07 µL of Taq DNA polymerase in a total volume of 11 µL. The thermocycler program for PCR was 32 cycles consisting of a 2-min denaturation at 94°C, 25-s denaturation at 94°C, 25-s annealing at 47°C, and 25-s elongation at 72°C with a 2-min final extension at 72°C. Electrophoresis was performed on a 6% (w/v) polyacrylamide gel (19:1 crosslinking ratio) with 0.5x TAE (Tris-acetate EDTA) running buffer. Ten microliters of the PCR product was loaded per lane and electrophoresis was performed for 100 min at 300 V. The gel was then stained with SYBER Green I nucleic acid gel stain (FMC Bio-Products, Rockland ME) for 10 min under dark conditions. The stained gel was visualized under UV light and photographed. Progeny were scored by comparing their banding pattern with the patterns of both parents.

Field Evaluation
Field evaluations for waterlogging tolerance based on yield and waterlogging injury were conducted at the University of Arkansas Rice Research and Extension Center (AR) at Stuttgart (Calloway silt loam, Fine smectitic, hyperthermic, Typic Aldaqualf), AR, in 1999 and 2000, and at the University of Missouri Research Center (MO) in Portageville (Tiptonville silt loam, fine-silty, mixed, thermic, Typic Argiudoll), Missouri in 2000. We used a split plot design with water treatment (waterlogged or irrigated control) as the whole plot and NIL set as the sub plot. All checks and RILs were blocked together in a subplot. NIL sets were randomly assigned to a split plot and members of a NIL set were randomly assigned to plots within a subplot. Plots consisted of four 4.2 m long rows 790 mm apart. Plots were planted on a flat soil surface, but beds 200 mm high were later formed by cultivation to facilitate furrow irrigation. Irrigated control treatments had two replications and waterlogged treatments had three replications. All plots were furrow irrigated as needed until the genotypes reached the R2 growth stage (Fehr and Caviness, 1977). At that time, levees were constructed around the whole plots that would receive the waterlogging treatment and water was applied to these whole plots until it reached 70 to 120 mm above the soil surface. The depth of the water in the waterlogged treatment varied during the treatment period because of daily evaporation, but the soil remained saturated for the entire period. The waterlogging was maintained until moderate chlorosis was noted. The waterlogging treatment lasted from 10 to 14 d. After appearance of waterlogging injury, water was drained from the waterlogged whole plots and all plots were then irrigated as needed for the remainder of the study. The control whole plots received furrow irrigation as needed while the waterlogged whole plots were inundated.

All waterlogged treated plots were visually rated for visual waterlogging injury 7 d after the waterlogging was removed. Rating was based on the extent of chlorosis and death. Plots were rated from 0 (no chlorotic or dead plants) to 9 (90% of the plants very chlorotic or dead). Plots were rated again after 14 and 21 d. Generally, symptomatic plants did not recover from the waterlogging stress and plants that showed chlorosis at 7 d were generally dead at 21 d. Data from 7 d were analyzed in this study. Plants at or near the unbordered edge of plots generally showed the most severe waterlogging injury symptoms, perhaps becaue of high water temperature of the adjacent unshaded flood water. This phenomenon had great effect on plots with poor stands, and thus more unshaded water, requiring that we delete all data from plots with weak stands (generally <75% of normal stand, or plots with skips exceeding 0.6 m) from our analyses. We rated waterlogging injury only on plants from the middle two rows of the four row plots with acceptable stands. This allowed for greater differences to be noted than rating the entire plot as plants of even the most tolerant lines would at times show extensive injury when they were located next to open water. The center two rows of each plot were harvested for yield and seed yield was adjusted to 130 g kg^-1 moisture. Plant height (distance from soil surface to end of main stem) and date of maturity were noted on each plot but was not used in the analysis.

The large set of RILs from each population were planted irrigated, and waterlogged the same as the 2000 AR yield and waterlogging injury evaluation of the NILs described above. Plots consisted of a single 3-m row seeded with approximately 30 seeds and there were two replications per line. This study only had a waterlogged treatment and visual waterlogging injury was rated on the individual rows as described above. Data were discarded from plots with poor stands (stands <75%), or from plots whose adjacent plot(s) had a poor stand.

Data Analysis
Analyses of variance for yield and waterlogging injury were performed by SAS (SAS Institute Inc., Cary, NC, USA). Data from the NILs were analyzed separately from data from the RILs and checks. An analysis of yield data was performed over all three trial environments considering water treatment (control vs. waterlogged) and marker genotype (Archer allele at Sat_064 or allele from southern parent at Sat_064) as fixed factors while environment (the three trials), NIL sets, and replication were considered random effects. Tests of significance were performed by either the random statement of PROC GLM or by specific F tests. A similar analysis was performed for waterlogging injury but without water treatment (data collected from waterlogged treatment only). The above analyses were performed over all three trials and for just the AR trials. In addition, we performed a separate analysis for each individual NIL set, for each environment, for each NIL in each environment, and for each combination of NIL set, environment, and water treatment. The significance of waterlogging injury on the large sets of RILs was tested with an ANOVA considering family and replication as random factors. We also tested the effect of the Sat_064 marker genotype on waterlogging injury in each RIL population using a single factor ANOVA and family means. Pearson correlation coefficients among genotype means were obtained by means of the CORR procedure of SAS.

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
The effect of waterlogging on yield was significant in all three environments. Stress was very severe in the 2000 MO test, as the waterlogged treatment reduced NIL yield from 2446 to 201 kg ha^-1 and the average waterlogging injury score was 8.2 for the NILs (Table 2). This high level of stress was due to heavy rains that occurred just as the waterlogging treatment was removed. The rainfall caused flooding and effectively prolonged the duration of the waterlogging stress by at least 1 wk resulting in excessive injury. Stress was more moderate in the 1999 and 2000 AR trials.

We also analyzed yield for each NIL set separately to evaluate further the marker effect in different genetic backgrounds. Marker genotype x water treatment interaction was only significant (P < 0.05) for NIL set 2, suggesting some effect of the Sat_064 on waterlogging tolerance in this NIL set. This interaction for NIL set 2 though appears to be from the members of the NIL set with the Archer allele having a greater yield advantage over the members with the southern allele in the control treatment than in the waterlogged treatment (Table 3). The data (Table 3) suggest that there may be a yield advantage in waterlogged conditions for the southern (A5403) Sat_064 allele in NIL set 1. The marker genotype x treatment x environment interaction was significant only for this NIL set. The yield advantage of the southern allele was quite large in the AR environments for NIL set 1 (Table 3), but essentially nonexistent in the MO waterlogged environment (232 vs. 336 kg ha^-1 for the Archer and southern NIL members, respectively). It is possible that the stress level at the MO environment was too great for expression of tolerance.

It is possible that the AR tests did not provide enough stress for proper expression of the Archer waterlogging tolerance QTL allele (Table 2). The original mapping of the Archer QTL allele for waterlogging tolerance indicated that lines with the Archer allele at Sat_064 suffered a 73% yield reduction from waterlogging while those without the Archer allele suffered a 79% reduction (Van Toai et al., 2001). This level of stress is closer to that of the MO 2000 environment of this study (Table 2) than the AR environments. The Sat_064 marker genotype x water treatment interaction was not significant for yield at the Missouri test and marker genotype had no significant effect on waterlogged yield or waterlogging injury. In the Missouri trial, the average yield of the NILs without the Archer allele (201 kg ha^-1) was 26.4% lower than the NIL with the Archer allele (254 kg ha^-1), a difference very similar to that reported by Van Toai et al. (2001). Still the advantage of 54 kg ha^-1 imparted by the Archer marker in the MO 2000 trial was not statistically or agronomically significant.

Marker Effect on Flood Injury
Visual rating of waterlogging injury was also used to assess waterlogging tolerance. Waterlogging injury was significantly correlated with yield under waterlogged conditions on the basis of the NIL data from all environments (r = -0.97) or just Arkansas (r = -0.92), but was not correlated to yield from control plots. No model effect involving marker genotype was significant for waterlogging injury in an analysis of data from all environments and NIL sets. The average waterlogging injury of NIL members with and without the Archer allele at Sat_064 were nearly identical (Table 3). No significant difference was observed between lines with and without the Archer allele when the waterlogging injury was analyzed separately for each NIL set using all the data or just the Arkansas data. The average waterlogging injury data for each NIL set (Table 3) indicates that any difference between NIL members with the southern or Archer allele at Sat_064 is small and the effect was inconsistent across genetic backgrounds.

There are several possible reasons why the Archer allele at Sat_064 did not affect waterlogging tolerance in this study. Recombination between the marker and the QTL, as well as epistasis, may have nullified the effect of the Archer Sat_064 marker allele on waterlogging tolerance. Polymorphic flanking markers to monitor recombination in this region were not available when this research was conducted so only one marker was used to select the NILs. If recombination or epistasis occurred then we would expect to see the effect of the marker in some NIL sets as each represents a unique genetic background from sampling of recombinant gametes. There is little evidence that stress tolerance associated with either marker alleles in any NIL as shown by the nonsignificant marker genotype x water treatment interaction for most NILs. There did seem to be some yield advantage in waterlogged environments associated with certain Sat_064 alleles in certain NIL sets, though this advantage was not expressed consistently over environments (see the southern allele and NIL set 1) or appeared to be associated with a yield advantage in the control treatments as well (see the Archer allele in NIL sets 2 and 4). Thus, while epistasis and recombination cannot be ruled out as explanations for a lack of association of waterlogging and the Sat_064 marker, they seem unlikely. It seems more likely that the Archer waterlogging tolerance allele near Sat_064 simply did not improve waterlogging tolerance in the southern environments and relative to the southern alleles at Sat_064. The study cannot identify which of these two causes are more likely, but does indicate that selection for this marker may not universally improve waterlogging tolerance for southern breeders.

Evidence for Waterlogging Tolerance in RILs and Checks
It is important to note that NIL set x water treatment interaction was significant for yield, and that some NIL sets had less waterlogging injury than others. NIL set 2 appeared quite susceptible to waterlogging with an average waterlogging injury of 7.8 and an 82% reduction in yield due to waterlogging (Table 3). In contrast, NIL set 3 had an average waterlogging injury of 4.0 and suffered only a 39% yield reduction from waterlogging. These results indicate that there was genetic variation for waterlogging tolerance in the A5403 x Archer and 9641 x Archer populations, but the Sat_064 did not model any of this variation.

Data from the checks and RILs in the yield study were analyzed separately from the NIL data. Data was again analyzed with and without the 2000 MO data. For yield, the effects of environment, water treatment, genotype, and the interaction among these factors were significant in both analyses.

For yield, the genotype x water treatment interaction was significant, indicating difference in tolerance to waterlogging among these genotypes. Genotype differences were also significant for waterlogging injury. Yield under waterlogged conditions and waterlogging injury were not significantly (P > 0.05) correlated (r = -0.22) when averaged over all three tests, but were highly correlated in the data from only Arkansas (r = -0.92). Tolerant and susceptible RILs from each population were observed. Tolerant RILs were 91209-284 and 91210-350, while 91209-293 and 91210-365 appeared quite susceptible on the basis of yield and injury in the Arkansas only data (Table 3).

A large set of RILs from the crosses A5403 x Archer and 9641 x Archer was evaluated for waterlogging injury only in 2000 Arkansas. The effect of genotype was significant for each population, indicating that each was segregating for genes controlling the extent of waterlogging injury. Lines with low (<2) injury levels were noted in the A5403 x Archer population (Fig. 1) while no lines in the 9641 x Archer population had average injury scores less than 3. Both populations had RILs with high injury scores. Both of these populations also produced tolerant and susceptible RILs based on yield analysis of tolerance (Table 3). Variation for waterlogging injury was not significantly associated with Sat_064 genotype of the RILs in either population.

View larger version (16K): [in this window] [in a new window]   Fig. 1. Distribution of soybean recombinant inbred family (RIL) family means for waterlogging injury from two populations tested for waterlogging tolerance in Arkansas in 2000. Flood injury was rated on a 0 to 9 scale where 0 = no injury and 9 = severe injury.

	ACKNOWLEDGMENTS

 
Salaries and research support provided by state and federal funds appropriated to the Arkansas Agricultural Experiment Station, Ohio Agricultural Research and Development Center, The Ohio State University as well as funding from the United Soybean Board.

Received for publication May 24, 2002.

	REFERENCES

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This Article Abstract Figures Only Full Text (PDF) Free Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in ISI Web of Science Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (5) Citing Articles via Google Scholar Google Scholar Articles by Reyna, N. Articles by Sneller, C. H. Search for Related Content PubMed Articles by Reyna, N. Articles by Sneller, C. H. Agricola Articles by Reyna, N. Articles by Sneller, C. H. Related Collections Soybean Cell Biology & Molecular Genetics Plant and Environment Interactions