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Published online 23 September 2005
Published in Crop Sci 45:2312-2317 (2005)
© 2005 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
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CROP BREEDING, GENETICS & CYTOLOGY

Relationship between Yield Potential and Percentage Yield Suppression Caused by the Southern Root-Knot Nematode in Cotton

R. F. Davisa,* and O. L. Mayb

a USDA-ARS, Crop Protection and Management Research Unit, P.O. Box 748, Tifton, GA 31793
b University of Georgia, Dep. of Crop and Soil Sciences, P.O. Box 748, Tifton, GA 31793

* Corresponding author (rfdavis{at}tifton.usda.gov)


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Currently available cotton (Gossypium hirsutum L.) cultivars support significant reproduction of the southern root-knot nematode [Meloidogyne incognita (Kofoid & White) Chitwood], but they have not been evaluated for differing levels of yield suppression (tolerance) to this nematode. If nematode tolerant (low yield suppression) but susceptible (high nematode reproduction) cotton cultivars can be identified, they could be grown rather than intolerant cultivars to reduce yield loss. The objective of this study was to evaluate a collection of M. incognita–susceptible cotton cultivars for tolerance to parasitism by this nematode. The yield potential and percentage yield loss to M. incognita were measured in 12 genotypes in 2002 and 2003 by comparing yields in 1,3-dichloropropene–fumigated and nonfumigated plots. The percentage yield suppression caused by M. incognita differed among cotton genotypes in both 2002 and 2003. Yield suppression ranged from 18.0 to 47.3% in 2002 and from 8.5 to 35.7% in 2003. Though significant levels of tolerance were measured in our study, 2 yr of data on percentage yield suppression show that tolerance is not consistently related to specific cultivars in the absence of nematode resistance: susceptible cultivars did not consistently express tolerance, but resistant germplasm did. Thus, it appears unlikely that cotton cultivar selection for tolerance to M. incognita can be utilized to minimize yield suppression. Regression analysis based on the 2 yr of field data revealed a relationship in which percentage yield suppression caused by M. incognita increased linearly as yield potential increased. Because the absolute and percentage losses to nematodes increase as yield potential increases, nematode management becomes increasingly important and beneficial in cotton.


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
HOST-PLANT RESISTANCE to plant-parasitic nematodes is defined as the suppressive effect of the plant on the nematode's ability to reproduce (Cook and Evans, 1987). In contrast, tolerance describes the degree of damage, usually measured in terms of yield suppression, inflicted by the nematode on the plant (Cook and Evans, 1987). Plants that are tolerant but have no resistance will suffer less damage even though nematode levels are not reduced. Both host-plant resistance and tolerance could be useful for managing nematodes in crops (McSorley, 1998; Potter and Dale, 1994; Reese et al., 1988; Seinhorst, 1970; Young, 1998). Resistance in cotton to Meloidogyne incognita, the southern root-knot nematode, has been studied extensively (Cook et al., 1997; Ogallo et al., 1997; Robinson et al., 1999; Shepherd, 1974, 1983) because M. incognita causes more damage to cotton in the USA than any other pathogen (National Cotton Council of America disease loss estimates, www.cotton.org/tech/pest/index.cfm [verified 14 June 2005]). In contrast, tolerance to M. incognita in cotton is poorly documented and has received relatively little study (Davis and May, 2003).

Resistance and tolerance to nematodes can be expressed independently in potato (Solanum tuberosum L.) (Arntzen et al., 1994; Evans and Haydock, 1990; Trudgill and Coates, 1983) and soybean [Glycine max (L.) Merr.] (Boerma and Hussey, 1984, 1992). It is not known if M. incognita tolerance in cotton can be expressed independently of resistance. Resistance to M. incognita in cotton also imparts tolerance to the nematode (Davis and May, 2003; Zhou and Starr, 2003), although factors other than resistance also are believed to affect the expression of tolerance. Consequently, nematode tolerant but susceptible cultivars could exist.

No cotton cultivars are available in the southeastern USA with a high level of resistance to M. incognita, and Stoneville ST5599BR is the only currently available cultivar with a moderate level of resistance. All other available cultivars are believed to be susceptible to M. incognita, but their levels of tolerance have not been quantified. If nematode tolerant but susceptible cotton cultivars can be identified, then they could be grown to help minimize yield losses. The objective of this study was to evaluate a collection of cotton cultivars that are susceptible to M. incognita to determine if some are more tolerant than others of parasitism by this nematode.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Yield Potential and Percentage Yield Suppression
Percentage yield suppression due to M. incognita was measured in 12 cotton genotypes (1 germplasm and 11 cultivars) in 2002 and 2003 in field experiments with six replications in a strip-plot design at the University of Georgia Gibbs Farm in Tifton, GA. The soil type was a Tifton loamy sand (fine, loamy, siliceous, thermic Plinthic Kandiudult; 85% sand, 11% silt, 4% clay, <1% organic matter). The field was naturally infested with M. incognita and had been planted to cotton for several years before initiation of this study. The horizontal factor was genotype and the vertical factor was fumigation treatment (nonfumigated or 1,3-dichloropropene [Telone II, Dow AgroSciences, Indianapolis, Indiana] at 56 L ha–1). Twelve cotton genotypes were evaluated, including 11 cultivars which accounted for 28% of cotton hectarage in the southeastern USA in 2002 and 37% in 2003 (USDA Agricultural Marketing Service). The germplasm line GA96-211 was included because it is moderately resistant and tolerant to M. incognita (May et al., 2004; Davis and May, 2003). All plots were tilled with a single subsoil chisel per row with disks creating a raised bed above the chisel trace. In fumigated plots, 1,3-dichloropropene was applied behind the subsoil chisel approximately 35 cm deep on 8 May 2002 and 2 May 2003. Subplots consisted of two 12.2-m-long rows spaced 91 cm apart. Genotypes were planted at four seeds per 30 cm of row. Plots were oversprayed as necessary with acephate (Orthene 75, Valent USA Corp., Walnut Creek, CA) at 0.20 kg a.i. ha–1 for thrips control. All plots received fertilizer, insecticide, and herbicide as recommended by the University of Georgia Cooperative Extension Service (Brown et al., 2001; Jost et al., 2002). All plots were managed identically and irrigation was applied as needed. Yield data were collected at harvest on 8 Nov. 2002 and 23 Oct. 2003. Seed cotton from each plot was harvested and weighed, and lint yield was determined by ginning a subsample from each plot and using the percentage lint in the subsample to calculate a lint yield for the plot. Percentage yield suppression was calculated for each replication of each genotype as the difference in yield between the fumigated and nonfumigated plot divided by the yield of the fumigated plot. Data on percentage yield suppression were analyzed as a randomized complete block design.

Soil samples for nematode analysis were collected from the field trials in midseason (17 July 2002 and 9 July 2003) and near harvest (4 Dec. 2002 and 5 Nov. 2003). Soil samples consisted of a composite of 8 to 10 cores per plot (2.5-cm diam. and approximately 20 cm deep) collected from the root zone. Nematodes were extracted from 150 cm3 soil by centrifugal flotation (Jenkins, 1964). Root galling was evaluated on a 0 to 10 scale within a few days of harvest in 2002 and 2003 by digging and rating 10 root systems per plot. The scale used was as follows: 0 = no galling; 1 = 1 to 10% of the root system galled; 2 = 11 to 20% of the roots system galled, etc.; with 10 = 91 to 100% of the root system galled.

The relationship between yield potential and percentage yield suppression caused by M. incognita was evaluated by regression analysis. Yield potential for each genotype was estimated from fumigated plots. Mean yield potential (achievable yield) and mean percentage yield suppression were calculated for each genotype in each year on the basis of data from the two field trials (six observations per genotype per year). A single pair of yield potential and yield suppression means for each genotype in each year was calculated for the analysis. Regressions of midseason nematode population densities and end-of-season root galling against percentage yield suppression caused by M. incognita also were calculated. Multiple regression analysis was used to evaluate the combined effects of midseason nematode population densities and yield potential on percentage yield suppression.

Nematode Reproduction Experiments
The 12 cotton genotypes used in the field experiments also were evaluated in two greenhouse trials for their ability to host M. incognita race 3 reproduction. Each trial had six replications in a randomized complete block design. Soil temperatures in the pots varied between 24 and 32°C during the study. Cotton seeds were planted into 15-cm-diameter pots on 20 Feb. 2003 for Trial 1 and on 13 July 2003 for Trial 2. Seedlings were thinned to one plant per pot before inoculation.

Nematode eggs were collected from tomato roots (Lycopersicon esculentum Mill. ‘Rutgers’) by agitating roots in 0.5% sodium hypochlorite solution for two minutes (Hussey and Barker, 1973) approximately 1 h before inoculation. Nematode inoculum of 8000 M. incognita eggs per pot (approximately 800 eggs 150 cm–3 soil) was added on 3 Mar. 2003 for Trial 1 and 29 July 2003 for Trial 2. Inoculum was distributed into two holes (approximately 2.5 cm deep) and covered with soil. Pots were watered immediately following inoculation.

Nematode eggs were extracted from all roots in a pot on 1 May 2003 for Trial 1 and 29 Sept. 2003 for Trial 2 (both 56 d after inoculation). Roots were washed free of soil, cut into 5-cm pieces, and agitated in a 1% sodium hypochlorite solution in a 1-L flask for four minutes. Eggs were collected and rinsed with tap water on nested 150- over 25-µm-pore sieves. Egg counts were subjected to a square-root transformation to normalize the error variances before statistical analysis. Data from the two trials were analyzed separately by analysis of variance and means separation by Fisher's protected least significant difference (LSD0.05). Root galling was evaluated before egg extraction on 29 September using the 0 to 10 scale described previously.

Multiple regression analysis was used to determine the combined effects of the amount of M. incognita reproduction and yield potential (achievable yield) on percentage yield suppression caused by M. incognita. For this analysis, yield potential and yield suppression means for each genotype in each year were estimated from the field trials as previously described, and nematode reproduction was estimated on the basis of reproduction data from the two greenhouse evaluations (12 observations per genotype). Reproduction data were standardized as a percentage of the known susceptible cultivar DP5415.


   RESULTS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
There were greater (P ≤ 0.01) nematode population densities in nonfumigated plots than in fumigated plots at midseason in both 2002 and 2003. Mean midseason nematode densities in 2002 were 119 M. incognita juveniles per 150 cm3 of soil in the nonfumigated plots and 7 in the fumigated plots. By harvest, population densities had increased to 269 per 150 cm3 in fumigated plots and 609 per 150 cm3 in nonfumigated plots. In 2003, mean midseason nematode levels were 65 in the nonfumigated plots and 12 in the fumigated plots. By harvest, population densities had increased to 493 per 150 cm3 in fumigated plots and 646 per 150 cm3 in nonfumigated plots. Root galling averaged 2.1 in fumigated plots and 5.8 in nonfumigated plots in 2002, and 2.2 in fumigated plots and 3.9 in nonfumigated plots in 2003.

The percentage yield suppression caused by M. incognita differed among cotton genotypes in both 2002 and 2003, though yield suppression was greater in 2002 (Table 1). Yield potential of the genotypes ranged from 1504 to 2095 kg lint ha–1 in 2002 and from 926 to 1486 kg lint ha–1 in 2003. Yield suppression ranged from 18.0 to 47.3% in 2002 and from 8.5 to 35.7% in 2003. In both years, the moderately resistant germplasm GA96-211 suffered the lowest percentage yield suppression. There was a significant year x genotype interaction, so the data could not be pooled for a combined analysis. No cultivar consistently had a lower percentage yield loss than the other cultivars.


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  		Table 1. Yield suppression caused by the southern root-knot nematode, Meloidogyne incognita, in cotton cultivars in 2002 and 2003.

 
Nematode reproduction varied among genotypes in the two greenhouse trials (Table 2). There was a significant trial x genotype interaction, so the data could not be pooled for a combined analysis. The moderately resistant germplasm GA96-211 supported the least reproduction in both trials, and the cultivar DP458BR consistently supported lower reproduction than the most susceptible cultivars. The 11 cultivars tested did not all support similar levels of reproduction in either trial, but as indicated by the trial x genotype interaction, the relative level of reproduction supported by a genotype was not consistent between trials.


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  		Table 2. Reproduction of the southern root-knot nematode, Meloidogyne incognita, on cotton cultivars in greenhouse studies.

 
Evaluation for root galling was done only in the second greenhouse trial. Galling generally was severe and statistically similar among the cultivars (Table 2). The cultivar DeltaPearl had the highest mean gall rating in the study, though all other genotypes except the cultivars DP451BR and DP458BR and the germplasm GA96-211 had levels of galling that were similar to DeltaPearl. The moderately resistant germplasm GA96-211 suffered the least galling.

Regression analysis based on the 2 yr of field data revealed a linear relationship in which increasing yield potential was associated with increasing percentage yield suppression (Fig. 1) . Comparison of the slope and intercept values of the regression lines calculated for the 2002 and 2003 data verified that both the slope and intercept values were similar (LSD0.10) for the two years, so the data were combined and a single regression was calculated on the basis of all the data. The predicted percentage yield loss when yield potential was zero (the regression intercept) was 0.41%, which is not statistically different from zero (P = 0.95). The combined regression predicted that percentage yield suppression was equal to 0.414 + (yield potential)(0.0165) (P = 0.0005, R2 = 0.43).



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  		Fig. 1. The relationship between yield potential of cotton and percentage yield suppression caused by Meloidogyne incognita in Tifton, GA, in 2002 and 2003.

 
Regression analysis showed that post-harvest root gall ratings were not related to percentage yield suppression (P > 0.10) in either year or when the two years were combined. Midseason nematode population densities were related to percentage yield suppression. The calculated slope and intercept values did not differ (P > 0.10) between 2002 and 2003, so the data was combined and a single regression was calculated. The combined regression predicted that percentage yield suppression was equal to 18.9 + (midseason nematode levels)(0.100) (P = 0.0015, R2 = 0.37).

Multiple regression analysis revealed that yield potential (P = 0.0016) and the relative amount of M. incognita reproduction (P = 0.0700) both affected the percentage yield suppression caused by M. incognita in a linear manner. Yield suppression increased as either yield potential or nematode reproduction increased. The predicted percentage yield loss when both yield potential and nematode reproduction were zero (the regression intercept) was –7.808%, which is not different from zero (P = 0.336). The combined regression predicted that percentage yield suppression was equal to –7.808 + (yield potential)(0.0159) + (reproduction)(0.1136) (P = 0.0005, R2 = 0.51).

Multiple regression analysis revealed that yield potential (P = 0.0287) and midseason M. incognita population levels (P = 0.0862) both affected the percentage yield suppression caused by M. incognita in a linear manner. Yield suppression increased as either nematode levels or yield potential increased. The predicted percentage yield loss when both yield potential and nematode population levels were zero (the regression intercept) was –4.043%, which is not different from zero (P = 0.5644). The combined regression predicted that percentage yield suppression was equal to –4.043 + (yield potential) (0.0125) + (number of M. incognita)(0.0563) (P = 0.0006, R2 = 0.50).


   DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The objective of this study was to determine if any cotton cultivars are more tolerant than others of parasitism by M. incognita. Though significant levels of tolerance were measured in our study, tolerance was not consistently related to specific cultivars in the absence of nematode resistance. Resistant germplasm consistently suffered the least yield suppression in the study, but the level of yield suppression for each of the susceptible cultivars was inconsistent. This is in contrast to nematode tolerance in potato, where tolerance in susceptible genotypes is linked to specific cultivars (Evans and Haydock, 1990). In cotton, it appears unlikely that cultivar selection for tolerance to M. incognita can be utilized to minimize yield suppression, although nematode-susceptible cultivars not included in this study could consistently express tolerance.

Stress has been defined in terms of a plant's negative response to a causal factor, and reaction to stress can be altered by either affecting the causal factor directly or by modifying the plant such that the causal factor has less effect (Tollenaar and Wu, 1999). Enhanced tolerance to biotic or abiotic stress can lead to increased crop yields (Fasoula and Fasoula, 2002). For example, increased yield in corn (Zea mays L.) in recent decades is due mostly to increased tolerance to stresses (Tollenaar and Lee, 2002; Tollenaar and Wu, 1999). Unfortunately, selection for tolerance to one type of stress does not necessarily confer tolerance to other stresses (Van Oosterom et al., 1995). Our data suggests that cotton breeding has not improved tolerance to the root-knot nematode. In fact, cotton becomes more sensitive to nematode damage as yield potential increases.

The relationship in this study between percentage yield suppression and midseason nematode levels is consistent with the assumption that yields generally should decrease as nematode population levels increase. It is noteworthy that the relationship between yield potential and percentage yield suppression is significant even when the effect of nematode population density is considered. The relatively low R2 value of the regression shows that there was a lot of unexplained variation in the data, which might be reduced if data were collected from a greater number of more diverse genotypes. Environmental effects which differ between years, and possible genotype x environment interactions, may also contribute to unexplained variation in the data. Regression slopes and intercepts were similar between years despite differences in environment, yield potential, and percentage yield suppression.

The term yield potential has been defined as "the yield of a cultivar when grown in environments to which it is adapted; with nutrients and water non-limiting; and with pests, diseases, weeds, lodging and other stresses effectively controlled" (Evans and Fischer, 1999). When cotton is parasitized by M. incognita, yields will be below the yield potential. A generic damage function that relates the degree of yield suppression to nematode population density is

where y = the relative yield (between 0.0 and 1.0) at nematode density P; yieldP = yield at nematode density P; yieldmin = a minimum yield that will be achieved even at the highest nematode densities; and yieldmax = a maximum yield achieved in the absence of nematodes (Seinhorst, 1965). Yieldmax in Seinhorst's equation would be the crop's yield potential when other limiting factors are effectively minimized. The model, which is not specific to any crop or any nematode, helps explain the relationship between nematode population density and yield loss. For a specific nematode population density, the relative yield will decrease if the yield potential increases. This predicts that nematode parasitism will decrease yield by a greater percentage as yield potential increases, which was documented in our study.

The relationship between the percentage yield suppression caused by nematodes and yield potential has not been examined previously in any crop. Some studies have examined the effect of nematode resistance on yield suppression, but not on percentage suppression, and information may be gleaned from genotypes with similar levels of resistance. A study of tolerance in potato to Globodera rostochiensis (Woll.) Behrens included two susceptible standards, ‘Pentland Dell’ and ‘Désirée’. Désirée had a higher yield potential and suffered a greater percentage yield loss than Pentland Dell (Evans and Russell, 1990). It is more difficult to interpret the results of some studies. For example, a study of Globodera spp. on potato found that percentage yield loss did not change as yield potential changed (Mulder et al., 1997), but the yield potential and crop loss data were generated at different times in fields with different soil types. Soil type likely affects both yield potential and percentage yield suppression, so data combined from a range of soil types may not indicate a clear or consistent relationship between yield potential and percentage loss.

Host-plant resistance to a nematode increases the tolerance of the plant to the nematode, and higher levels of resistance should impart higher levels of tolerance (Davis and May, 2003; Evans and Haydock, 1990). Incorporating high levels of resistance should reduce yield losses greatly, whereas slight or moderate levels of resistance will likely impart slight or moderate tolerance. As breeders increase nematode resistance they also may increase yield potential. If yield potential is increased, but only slight to moderate levels of resistance are achieved, then yield suppression by nematodes will be affected by conflicting forces: increased resistance will decrease the percentage yield loss caused by nematodes whereas increased yield potential will increase the percentage loss. Depending on the magnitude of the effects, the net result could be that increased tolerance achieved through nematode resistance may be offset by an increase in percentage yield suppression. A high level of resistance should have a much greater effect on yield suppression than would an increase in yield potential, but a slight to moderate level of resistance may not. This situation may have occurred in cotton in the USA. Upland cotton yields in the USA averaged 479 kg ha–1 from 1955 to 1959 and 737 kg ha–1 from 1999 to 2003, a 54% increase (USDA, National Agricultural Statistics Service, www.usda.gov/nass/ [verified 21 June 2005]). During roughly the same time period, 1950 to 1996, resistance in cotton cultivars to M. incognita increased such that new cultivars supported only 70% of the nematode reproduction supported on old cultivars (Robinson et al., 1999). Yet, the National Cotton Council of America disease loss estimates (available at www.cotton.org/tech/pest/index.cfm [verified 14 June 2005]) show average annual losses to nematodes of 1.1% from 1955 to 1959 increasing to 4.3% from 1999 to 2003. This does not prove that the aforementioned situation occurred because there are many factors contributing to these increased yields and increased percentage yield losses, but the observations are consistent with the concept.

Yield potential can be increased through breeding and selection for genotypes that allow the plants to be more responsive to inputs and exploit favorable growing conditions (Fasoula and Fasoula, 2002; Pala et al., 2004; Tokatlidis and Koutroubas, 2004). Although genotypes usually are evaluated under a range of conditions, cultivars often are selected on the basis of outstanding performance in favorable environments (Calhoun et al., 1994). Meloidogyne incognita infection impairs root function and limits growth of the root system, which reduces a plant's ability to exploit favorable environments fully. If nematode parasitism inhibits exploitation of favorable growing conditions, then the percentage yield suppression would be greater for input-responsive genotypes (which have higher yield potentials) than for genotypes that were less capable of exploiting favorable conditions.

High yield under ideal conditions, which is one definition of yield potential (Evans and Fischer, 1999), is often one of the primary goals of plant breeding. Unfortunately, increasing yield potential increases the percentage yield suppression in cotton caused by M. incognita. An increase in relative damage as yield potential increases probably also occurs in other crops with other nematodes. Therefore, because the absolute and percentage losses to nematodes increase as yield potential increases, nematode management becomes increasingly important and beneficial.


   NOTES
TOP
 NOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

Received for publication January 12, 2005.


   REFERENCES
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 


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Crop Science 2005 45: vii. [Full Text]  




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