© 2013 Plant Management Network.
Weed Species Not Impaired by Verticillium dahliae and Meloidogyne incognita Relationships that Damage Chile Pepper
S. Sanogo, Associate Professor, J. Schroeder, Professor, S. Thomas, Professor, Department of Entomology, Plant Pathology, and Weed Science, New Mexico State University, Las Cruces, NM 88003; L. Murray, Professor, Department of Statistics, Kansas State University, Manhattan, KS 66506; N. Schmidt, College Professor, Department of Economics, Applied Statistics and International Business, New Mexico State University, Las Cruces, NM 88003; and J. Beacham, Research Specialist, C. Fiore, Research Assistant, and L. Liess, Research Assistant, Department of Entomology, Plant Pathology, and Weed Science, New Mexico State University, Las Cruces, NM 88003
Sanogo, S., Schroeder, J., Thomas, S., Murray, L., Schmidt, N., Beacham, J., Fiore, C., and Liess, L. 2013. Weed species not impaired by Verticillium dahliae and Meloidogyne incognita relationships that damage chile pepper. Online. Plant Health Progress doi:10.1094/PHP-2013-0920-01-RS.
The chile pepper (Capsicum annuum) crop is affected by several pests, pathogens, and weeds including Verticillium dahliae, Meloidogyne incognita, spurred anoda (Anoda cristata), Wright groundcherry (Physalis acutifolia), and tall morningglory (Ipomoea purpurea). These weed species are unimpaired hosts to V. dahliae and M. incognita. Chile plants have been found co-infected with V. dahliae and M. incognita in commercial fields. Greenhouse studies were conducted to determine the relationships among V. dahliae, M. incognita, and each of the four aforementioned plant species. Plants were either non-inoculated or inoculated with V. dahliae, M. incognita, or V. dahliae plus M. incognita. Six weeks after inoculation, plant infection by V. dahliae, M. incognita reproduction, plant height and biomass were measured. Three relationships were identified: V. dahliae was recovered from 100% of all four inoculated plant species, irrespective of M. incognita treatment; V. dahliae and M. incognita enhanced or had no effect on weed biomass but were pathogenic to chile; and co-infection by V. dahliae had no effect on nematode reproduction in the first M. incognita generation on the crop or weeds. These biological relationships suggest that the competitive impact of the weeds may increase and pathogen diversity may be affected in infested fields, ultimately impacting the efficacy of our common IPM tools.
Chile pepper (Capsicum annuum L.) is of great ethnobotanical and economic importance in New Mexico and other states in the southwestern United States, with far-reaching importance to other regions of the country. Many pests and pathogens constitute a serious challenge to production of chile pepper. Of particular concern are the biological relationships among these pests and the effects of such relationships on crop performance, yield, and the efficacy of control measures. For example, the southern root-knot nematode, Meloidogyne incognita, has been shown to increase the competitive impact of weeds on chile pepper and to enhance tuber production in perennial weeds such as yellow (Cyperus esculentus L.) and purple (C. rotundus L.) nutsedge (13). The tubers from these nutsedges also harbor and protect M. incognita from the soil fumigant 1,3-dichloropropene (17).
In August 2007, during routine chile surveys in Luna Co., NM (10) three weed-infested fields were found with wilted chile pepper plants infected by both V. dahliae and M. incognita (Figs. 1A, B, and C). The weed species included asymptomatic Wright groundcherry [Physalis acutifolia (Miers) Sandw.] and spurred anoda [Anoda cristata (L.) Schlecht.], two weed species that have been shown to harbor V. dahliae (8), as well as tall morningglory [Ipomoea purpurea (L.) Roth]. Both V. dahliae and M. incognita were found infecting tall morningglory for the first time (Figs. 1C, D, E, and F). Chile wilt incidence ranged from 40 to 90% (Fig. 1D). One of the fields harvested for green chile yielded about 50% less than stipulated by processor contract (Fig. 1A). Furthermore, 20% of the chile plants in a field in Doña Ana Co., NM in 2012 were found to be co-infected with V. dahliae and M. incognita.
The combined effects of V. dahliae and M. incognita were first reported in 1955 in Peru, demonstrated by increased symptom development of Verticillium wilt on cotton in the presence of M. incognita (4). However, the biological relationships between these two pathogens with chile pepper and weeds have not been described. Verticillium dahliae, M. incognita, and weeds are capable of separately causing significant yield losses in chile (9,14,18). Therefore, the simultaneous presence of these pathogens in the same fields and same plants constitutes a concern, particularly given that associations between M. incognita and nutsedges can reduce the effectiveness of nematicides and herbicides (11,17).
The objective of this study was to examine relationships among V. dahliae,M. incognita and individual plants of chile pepper, spurred anoda, Wright groundcherry, and tall morningglory. Specifically, the study assessed the effects of: (i) M. incognita and the four plant species on plant infection by V. dahliae; (ii) V. dahliae and M. incognita, either separately or in combination, on height and biomass of the four plant species; and (iii) V. dahliae and plant species on M. incognita reproduction.
The Pathogens: Verticillium dahliae and Meloidogyne incognita
Inoculum was prepared from a V. dahliae culture originally isolated from a field-infected chile pepper as previously described (7). Briefly, a 1-cm mycelial plug of V. dahliae grown on water agar was added to 500 ml of sterilized Czapek-Dox broth in a 1-liter Erlenmeyer flask, and incubated on a rotary shaker at room temperature (23 to 25°C) for 7 to 10 days. Contents of the flask were passed through three layers of cheesecloth to separate conidia from mycelial plugs and mats. The concentration of conidia in the suspension was estimated with a hemacytometer.
Meloidogyne incognita isolated from cotton was maintained on tomato cultivar Rutgers prior to the 2008 and 2009 studies and chile pepper cultivar NM 6-4 for the 2010 study. Nematode egg inoculum was recovered by agitating infected roots for 2 min in a 0.51% sodium hypochlorite solution, after which eggs were captured on a 400-mesh sieve, rinsed to remove residual sodium hypochlorite, and transferred to an 1-liter Erlenmeyer flask containing tap water (2). Egg concentration in the suspension was quantified using a chambered counting slide and adjusted to a final concentration of 1000 eggs/ml.
Plant Production and Inoculation
Greenhouse experiments were conducted in the summers of 2008, 2009, and 2010. Treatments included individual plants of chile pepper, spurred anoda, tall morningglory, or Wright groundcherry, each inoculated with V. dahliae, M. incognita, or V. dahliae plus M. incognita. Non-inoculated plants of each species served as controls. Environmental conditions were monitored using a permanent weather station (CR10 Measurement and Control Module, Campbell Scientific Inc., Logan, UT). Soil temperature was used to calculate daily heat unit accumulation for monitoring M. incognita development (19).
Seeds of chile pepper cultivar AZ-20 and the three weed species obtained from local populations were sown into a pasteurized (75°C for 18 h) 2:1 mixture by volume of sand and Maricopa fine sandy loam (coarse-loamy over sandy or sandy-skeletal, mixed, superactive, calcareous, thermic Typic Torrifluvents) in plastic pots (25 cm in diameter × 19 cm in depth) and thinned to a single plant per pot after emergence. Based on prior work, chile and weed planting dates were staggered so each species reached the 4- to 6-leaf stage at the same time. Chile seeds were planted on 8 July 2008, and on 1 June 2009 and 2010. Wright groundcherry was planted on 18 July 2008, and on 9 June 2009 and 2010. Tall morningglory and spurred anoda seeds were planted on 25 July 2008, and 9 June 2009 and 2010. At the 4- to 6-leaf developmental stage, plants were inoculated with M. incognita, V. dahliae, or both M. incognita and V. dahliae. Inoculation with M. incognita consisted of delivering 5000 eggs per pot in 1.250 ml aliquots into four holes around the base of the plant at a depth of 5 cm in 2008, and 2.5 cm in 2009 and 2010. Similarly, plants were inoculated with 6 ×107 conidia of V. dahliae per pot delivered in four equal amounts of inoculum of 1.5 × 107 conidia in each hole. For plants co-inoculated with M. incognita and V. dahliae, each of the four holes received both eggs and conidia simultaneously.
Plants were harvested on 22 September 2008, 11 August 2009, and 23 August 2010. The number of days from inoculation to harvest was 46, 49, and 47 in 2008, 2009, and 2010, respectively. At harvest, plant height was measured from the base of the stem at the soil line to the highest shoot bud on the stem. A longitudinal incision was made in the stem 6 cm above the soil line to evaluate the presence of vascular discoloration. A 5-cm portion of each stem was collected just above the soil line for confirmation of infection by V. dahliae. Thereafter, the plants were separated into shoots, fruits, and roots. Lateral roots were separated from the tap root and cut into smaller pieces for M. incognita egg extraction. Weights of shoots, fruits, and roots (minus the tap root) were obtained after drying at 70°C.
Each 5-cm stem segment was surface sterilized for 3 min in 0.5% sodium hypochlorite prepared in 95% ethyl alcohol, rinsed in sterile distilled water, and cut into 0.5-cm pieces, which were plated onto either water agar or acidified potato dextrose agar in 9-cm diameter plastic petri plates. These were maintained at room temperature (23 to 25°C) and monitored for mycelium growth and examined for morphological characteristics of V. dahliae. A plant was confirmed as infected if the fungus grew from a stem piece.
Meloidogyne incognita eggs were extracted from the roots of each plant as previously described for inoculum preparation except agitation time was increased to 10 min. Egg production provides a direct measurement of root-knot nematode fecundity (virulence) on plants, and is not subject to host-related factors that reduce the reliability of gall ratings as assessment tools (3). Eggs were counted and expressed per gram root dry weight and as a ratio of inoculum level [reproductive factor RF = (egg recovery per plant)/(inoculum level)] (6).
Experimental Design and Statistical Analyses
In 2008, 160 pots (experimental units) were arranged in a generalized randomized complete block design where the 3 greenhouse benches were the blocks, and species by pathogen combinations were replicated within each bench. In 2009 and 2010, 96 pots were arranged in a balanced randomized complete block design with 6 blocks. Overall treatment structure was a 4 (plant species) × 2 (M. incognita) × 2 (V. dahliae) factorial. Plant responses were analyzed statistically in two ways. First, because growth habits are very different for the four plant species, shoot and root weight were compared among species by calculating the response of the inoculated plant as a percent of the non-inoculated control. The treatment structure for this analysis was a 4 (plant species) × 3 (pathogen) factorial where the three pathogen levels were M. incognita, V. dahliae, and M. incognita + V. dahliae. When there was a significant interaction, simple-effect tests were used to compare pathogen treatments within plant species. Second, actual plant responses, including height, were analyzed separately for each species, with treatment structure being a 2 (M. incognita) × 2 (V. dahliae) factorial. When there was a significant interaction, pairwise comparisons were used to compare the four pathogen treatments. Responses for M. incognita egg recovery (number of eggs per dry root weight and RF) were analyzed using a 4 (plant species) × 2 (V. dahliae) factorial treatment structure. When the interaction was significant, simple-effect tests were conducted within each plant species to compare responses with and without V. dahliae inoculation. Finally, data collected on recovery of V. dahliae and stem discoloration were not analyzed statistically because there was 100% recovery of V. dahliae from inoculated plants, while discoloration in stem did not correlate well with infection of weeds by V. dahliae. All responses were analyzed initially using the MIXED procedure of SAS (v9.3) but residuals for many responses were found to be non-normal and skewed upward. Therefore, data were analyzed using the GLIMMIX procedure with the gamma distribution and the log link function, to account for the long upper tail. Statistical results included F-tests, means, and 95% confidence intervals for treatment fixed effects. Tests of significance were assessed at a significance level of 0.10 because the study involves the first investigation of the relationships among three biological trophic groups (four plant species, a nematode, and a fungus) with a large inherent variation within each trophic group.
Environmental Conditions and Plant Growth
Relative greenhouse temperatures were similar during the course of this experiment. Cumulative heat unit measurements differed by <10% (400 ± 14 degree day) midway through all three studies and <19% (828 ± 97 degree day) among studies at termination (data not presented). The average maximum and minimum air temperatures ranged from 30.8 to 33.8°C and 20.2 to 22.5°C, respectively, and the average maximum and minimum soil temperatures were 33.7 to 35.7°C and 21.1 to 22.6°C, respectively. During the same period, the average maximum and minimum photosynthetically active radiation (PAR) levels ranged from 14,550 to 22,350 mmol/m² and 3,790 to 9,070 mmol/m², respectively. In general plant growth was more vigorous in 2008 and 2010 than in 2009.
Plant Response to Pathogens
Plant infection and disease data. Across all three years, chile infected by V. dahliae or V. dahliae plus M. incognita was stunted, especially in 2008 and 2009, and vascular tissues of the stem were discolored. Stunting was also observed with infection by M. incognita in 2010. No plant wilting was observed in any of the three years. Unlike in chile, very little expression of disease symptoms was manifested in any weed species. Verticillium dahliae was re-isolated from 100% of the treated plants whether inoculated with V. dahliae alone or V. dahliae plus M. incognita. In addition, stem discoloration was not observed in all of the infected weeds and, as a result, is not a good predictor of infection.
Plant responses compared among species as percent of control. Dry shoot and root weights expressed as a percent of the untreated control responded similarly to treatments within a year. In addition, analysis of actual plant responses provided similar information. Therefore, only results for percent shoot weight are shown in Fig. 2. Although a significant interaction was found between plant species and pathogens (Table 1) only in 2008 (P = 0.0255; P = 0.1315 in 2009 and P = 0.3316 in 2010), the graphical representation in Fig. 2 of the data across the factors is displayed in a similar fashion in each of the three years for purpose of comparability of discussion of results, despite the lack of significant interaction in 2009 and 2010.
Table 1. Significance (P values) of the fixed effects of plant species main effect, pathogens (Meloidogyne incognita = r and Verticillium dahliae = v) main effect, and their interaction on plant shoot dry weight expressed as a percent of control.
In 2008, the interaction is explained by the fact that the pattern of chile response to the three pathogen treatments was different than the pattern of weed response to inoculation. Chile shoot weight averaged 102% (SE = 21), 65% (SE = 65), and 36% (SE = 36) of the control when inoculated with M. incognita, V. dahliae, and the combination of pathogens, respectively. In comparison, response of each weed species was similar across all three pathogen treatments. Evaluation of the significant main effects for plant species (P = 0.0001) showed that percent shoot weight of Wright groundcherry and spurred anoda was not affected by pathogen treatment [average of 96% (SE = 15) and 88% (SE = 15) of the control, respectively] while tall morningglory biomass was significantly increased to an average of 155% (SE = 27) of the control. Chile percent shoot weight was significantly decreased, particularly compared to tall morningglory, and averaged 62% (SE = 10) of the control.
In 2009, the plant species main effect (P = 0.0012) and the pathogen main effect (P = 0.0120) were significant. Percent shoot weight for chile was significantly reduced compared to the three weed species averaging 61% (SE = 11) of the control compared to greater than 100% for each of the three weed species. Spurred anoda, tall morningglory, and Wright groundcherry percent shoot weight averaged 114% (SE = 21), 136% (SE = 26), and 152% (SE = 28) of the control, respectively. Percent shoot weight averaging over plant species was approximately 124% (SE = 21) of the control when plants were inoculated with M. incognita alone or M. incognita plus V. dahliae, while percent shoot weight was 86% (SE = 14) in the presence of V. dahliae alone.
In 2010, only the plant species main effect was significant (P = 0.0002; pathogen main effect P = 0.1583). Percent shoot weight for chile averaged 80% (SE = 8) of the control and the upper confidence limit was less than 100% indicating that this species was negatively impacted by the pathogen treatment. Confidence limits for the weed species all included 100% and average shoot weight was 88% (SE = 9), 93% (SE = 10), and 138% (SE = 15) for spurred anoda, Wright groundcherry, and tall morningglory, respectively.
Reproduction of Meloidogyne incognita
Eggs per gram root response. A significant interaction was recorded between plant species and inoculation with V. dahliae for nematode eggs per gram root dry weight in 2008 only (P = 0.0667; P > 0.382 in both 2009 and 2010) (Table 2), when numbers were significantly higher in chile (313% greater; simple effect P = 0.0335) and spurred anoda (500% greater; simple effect P = 0.0130) inoculated with V. dahliae (Fig. 3). The plant species main effect was significant in 2009 and 2010 (P < 0.001 in both years), when nematode reproduction on spurred anoda was always less than on other hosts [2009 = 1,472 eggs/g dry root (SE = 385); 2010 = 1,033 eggs/g dry root (SE = 220)]. Nematode reproduction was between four and eight times greater on chile [174,219 (SE = 50,418) and 257,059 (SE = 54,857) eggs/g dry root], Wright groundcherry [194,859 (SE = 57,746) and 162,966 (SE = 34,778) eggs/g dry root], and tall morningglory [145,855 (SE = 51,681) and 114,441 (SE = 24,422) eggs/g dry root] in 2008 and 2010 than the nematode reproduction on these same hosts in 2009 [chile = 30,715 (SE = 8,127); Wright groundcherry = 18,474 (SE = 5,078); tall morningglory = 30,936 (SE = 8,186) eggs/g dry root, respectively].
Table 2. Significance (P values) of the fixed effect of plant species main effect, Verticillium dahliae main effect, and their interaction on the number of eggs per gram of root dry weight (Eggs) and reproduction factor (RF) of Meloidogyne incognita in 2008, 2009, and 2010.
x RF = egg recovery at harvest ÷ egg inoculum level.
RF response. The reproductive factor (RF = egg recovery ÷ egg inoculum level) for M. incognita assesses nematode reproduction as a function of inoculum level rather than root mass. There was again a significant interaction of plant species and inoculation with V. dahliae (Table 2) for RF only in 2008 (P = 0.0073; P > 0.285 in both 2009 and 2010). Co-infection of spurred anoda with V. dahliae and M. incognita in 2008 resulted in a RF approximately 6-fold greater (P = 0.0004) relative to plants not inoculated with V. dahliae (Fig. 4). In all other plant species, RF for M. incognita was not significantly affected by V. dahliae. The plant species main effect was again significant in 2009 and 2010 (P < 0.001 in both years), with the demonstration of spurred anoda as a host less suitable for nematode reproduction than chile.
Scope and Implication for Disease and Weed Management
This study documents the first report of a neutral or positive relationship among the three weed species (spurred anoda, tall morningglory, and Wright groundcherry) and V. dahliae and M. incognita. The response of chile was negative to the combination of V. dahliae and M. incognita based on reduction of percent shoot dry weight. Generally, symptoms of plant infection by these two pathogens − stunting, vascular discoloration, and root galling − were well manifested in chile and not consistently expressed in the weed species. These results are reflective of the scenario found under field conditions, where none of the weeds typically display consistent above-ground symptoms of infection by V. dahliae (8) or M. incognita. Similarly, high M. incognita galling levels have frequently been found on morningglory and sporadically observed on spurred anoda and Wright groundcherry with healthy-appearing shoot growth under field conditions. Gall formation, which is a secondary host response to M. incognita infection, was not observed under greenhouse conditions. This response could be ascribed to differences in population density of M. incognita and environmental conditions (3) or variability among weed populations.
Wilting and reduced plant growth are symptoms that may accompany chile infection by V. dahliae and M. incognita and affect the yield of infected plants. Severely stunted chile plants do not typically produce fruit of marketable value. Onset of wilting in chile before anthesis leads to direct yield loss. Even when wilting is initiated after anthesis or fruit set, yield loss may occur because chile fruit on wilted plants lack turgor − a desired attribute − and therefore are rejected by the harvesting crew. Therefore, although fruit yield was not measured in this study, the reduction in percent shoot weight provides information on possible yield loss that may be incurred. Stunting and yield reduction due to M. incognita result when the parasite population exceeds numbers the host can support. Such conditions usually occur after M. incognita completes multiple generations, unless initial populations are extreme. Previous research has reported mild increases in plant growth and yield of crops and weeds attributed to enhanced early season root proliferation associated with low to moderate M. incognita and M. hapla infection (5,13,15).
Spurred anoda was a relatively poor host of M. incognita, compared to the other plant species. Similar results were reported with M. incognita reproduction under field microplot conditions (13). For the most part, M. incognita reproduction on weeds was not adversely affected by co-infection with V. dahliae. The apparently significant reduction in M. incognita egg counts per gram dry root on spurred anoda co-infected with V. dahliae in 2009 is most likely an anomaly resulting from the 40% increase in root mass that occurred in co-infected spurred anoda that year. The lack of any significant reduction in M. incognita reproductive factor (RF) for co-infected spurred anoda in 2009 supports this conclusion. Similarly, the three-fold increase in the number of M. incognita eggs per gram co-infected chile root in 2008 is accompanied by a three-to-four-fold reduction in chile root mass. Again, M. incognita RFs were similar between noninoculated and co-infected chile, supporting the conclusion that this apparent difference in nematode reproduction per unit root mass is actually the result of changes in host root mass. Given the similarity in heat unit accumulation among all three studies, the 75 to 90% reduction in M. incognita counts in 2009 does not appear temperature-related. Possible explanations include reduced initial nematode inoculum viability and/or poor quality of the hosts necessary for parasite proliferation. Changes in the population levels of V. dahliae in soil and in plants were not considered in this study because the emphasis was on plant infection and expression of symptoms such as stunting and vascular discoloration in stem, and re-isolation of the fungus from infected plants.
The methodological approaches used in this study are comparable to studies where chile was inoculated with V. dahliae (8,9) and where chile and weed responses to M. incognita were compared (11,12,16). This work assumed simultaneous plant infection by the fungus and the nematode. However, scenarios such as sequential plant infection are also plausible (7). Little information on the manner in which plant infection takes place in the presence of V. dahliae and M. incognita in the field is available. Simultaneous plant infection represents the greatest risk to the host by minimizing interference in colonization and was therefore considered in this study.
The scope of this study was limited to the response of four plant species to the pathogens when plants were grown separately, and provides a benchmark assessment of each plant species without interference. However, under field conditions, intra- and inter-specific interference among plants are typically the norm. Competition among plants may impact the relationships between V. dahliae and M. incognita and requires further research.
This research did not measure the effect of the pathogens on weed fecundity, an important factor in understanding the long-term ecology of these pests. To address part of this question, a field microplot study was conducted in 2009-2010 to assess the impact of M. incognita on growth rate and fecundity of the three weed species (1). Meloidogyne incognita did not affect growth rate of any of these weed species. In addition, M. incognita had no effect on seed production as measured by total seed weight of tall morningglory or spurred anoda while Wright groundcherry produced more seed when infected by M. incognita. These findings suggest that the lack of pathogenic effects of M. incognita on weeds in the greenhouse study was not related to study duration, but rather M. incognita does not have a major effect on growth and competition of these weeds as we observed in the initial field settings.
Three major findings of this research include: (i) V. dahliae was recovered from 100% of all four inoculated plant species, irrespective of the presence or absence of M. incognita; (ii) V. dahliae and M. incognita enhanced or had no effect on weed above-ground biomass but were pathogenic to chile as anticipated; and (iii) co-infection by V. dahliae had no effect on reproduction of the first M. incognita generation produced on the crop or weeds. The ability of weeds to harbor V. dahliae and M. incognita and remain unimpaired has serious implications for disease and weed management. Weeds may perpetuate pathogens even in the absence of the crop, and thereby maintain inoculum of V. dahliae and M. incognita in the field. Previous research documented that V. dahliae isolated from spurred anoda, morningglory, and Wright groundcherry can infect and adversely affect chile (8,10). An additional concern is that V. dahliae and M. incognita populations harbored by these weeds may help maintain and enhance genetic diversity among these pests. Additional research is needed to determine whether weed populations may contribute to long-term survival and ability of these pests to infect resistant crop cultivars. Additionally, the fact that weed growth was not affected and sometimes enhanced by infection in these experiments, while chile growth was stunted, suggests that the impact of weed interference may be exacerbated in an infested field. Therefore, for many reasons, weed control should be a central component of integrated crop management. Additional research is needed to understand these biological relationships and identify effective management strategies.
This research was funded by New Mexico Agricultural Experiment Station and the New Mexico Chile Association.
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