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. Author manuscript; available in PMC: 2016 May 12.
Published in final edited form as: Crop Sci. 2013 May 14;53(4):1412–1418. doi: 10.2135/cropsci2012.12.0681

An Aegilops ventricosa Translocation Confers Resistance Against Root-knot Nematodes to Common Wheat

Valerie M Williamson 1,*, Varghese Thomas 2, Howard Ferris 3, Jorge Dubcovsky 4
PMCID: PMC4864860  NIHMSID: NIHMS784597  PMID: 27182071

Abstract

Root knot nematodes (RKN; Meloidogyne spp.) cause severe losses worldwide to a wide range of crops. Crop rotations with resistant hosts can be used to control losses, but the wide host range of RKN limits this option. In this study, we found that the wheat cultivar Lassik is resistant to several isolates of the RKN species M. incognita and M. javanica, including those that can reproduce on tomato with the resistance gene Mi-1. Comparison of near-isogenic lines of wheat showed that the wheat resistance gene(s) is localized within a segment of the short arm of chromosome 2N from Aegilops ventricosa (Zhuk.) Chennav translocated into common wheat (Triticum aestivum L.) chromosome arm 2AS and is associated with a highly significant decrease in RKN eggs in the roots. This RKN resistance gene has been assigned the name Rkn3. While wheat itself is tolerant of RKN infection, a microplot experiment coupled with tomato bioassays showed less RKN root galling in the tomato samples grown in soil from the previous microplots including RKN resistant wheat varieties than in those including a susceptible wheat isogenic line. This result suggests that rotation with Rkn3 resistant wheat cultivars has the potential to be a valuable component of nematode management for crops that are highly susceptible to nematode damage and for which alternative strategies are limited.

Root knot nematodes (RKN; Meloidogyne spp.) cause severe losses worldwide to a wide range of crops (Sasser, 1977; Trudgill and Blok, 2001). The species Meloidogyne incognita (Kofoid and White) Chitwood (southern RKN) and M. javanica (Treub) Chitwood (Javanese RKN) have a particularly broad host range and can reproduce on most food and fiber crops (Trudgill and Blok, 2001). Infective juveniles in the soil penetrate behind the tips of growing roots of their hosts. They migrate intercellularly within the root towards differentiating vascular tissues where they stimulate development of feeding sites. The feeding sites include modified host cells (giant cells) that serve as the source of nutrients for the developing parasite. Swelling and proliferation of cortical cells surrounding the giant cells form the gall or “root-knot” that is associated with these parasites. Females become sedentary, develop within roots and lay their eggs in egg masses on the root surface. Although RKNs are biotrophic parasites and must keep their feeding site alive to complete their life cycle, nematode infection can cause a range of symptoms, depending on the host, from total crop loss to tolerance in which the host has no observable damage (Roberts, 1992). In addition, nematode infection can increase susceptibility of the host to other plant pathogens, most notably Fusarium wilt fungi (Mai and Abawi, 1987).

Use of chemical nematicides is the most common control measure in higher value crops, but many of these compounds are hazardous to the environment and human health, and their use has become highly regulated in recent years (Zasada et al, 2010). Crop rotation with non-hosts can be useful, but this option is limited by the wide host range of RKNs. Host resistance is of value when available and incorporation of genes that confer resistance to RKNs is a goal of many breeding programs (Roberts, 1995; Starr and Mercer, 2009; Williamson and Roberts, 2009). The tomato gene Mi-1, which confers effective field resistance to both M. incognita and M. javanica, is one of the best-characterized nematode resistance genes (Williamson and Kumar, 2006) and is widely deployed for root-knot nematode management in tomato (Williamson 1998). In California, resistant processing tomatoes carrying Mi-1 have been grown intensively for more than 20 years. However, coincident with the intense selection pressure associated with frequent use of such cultivars, populations of M. incognita and M. javanica virulent on Mi-1-tomato have been found in California as well as many other tomato growing regions of the world (Kaloshian et al., 1996; Castagnone-Sereno et al., 1994). While novel sources of resistance have been identified in wild tomato relatives, none that provide resistance against these nematode populations have been successfully incorporated into processing tomato cultivars (Williamson and Kumar, 2006).

Wheat is commonly used as a rotation crop for tomato in California and is a host for both M. incognita and M. javanica (Roberts and Van Gundy, 1981). Although wheat is tolerant of nematode infection and shows no reduction in yield or quality, nematode populations can be supported to a level that would damage the following rotation crop. Here we report the discovery of a new source of root-knot nematode resistance in wheat cultivars carrying a large segment of chromosome arm 2NS from Aegilops ventricosa (Zhuk.) Chennav translocated into the distal part of chromosome arm 2AS of common wheat (T. aestivum L.), henceforth referred as the 2NS translocation. We then compared the effect of resistant and susceptible wheat cultivars on nematode levels in a microplot experiment.

MATERIALS AND METHODS

Plant Materials

The hard red spring cultivar Lassik (PVP No. 200800176) is genetically similar to ‘Anza’ CItr 15284 (Qualset et al., 1984) but carries the 2NS translocation and the high grain protein locus Gpc-B1 (Uauy et al. 2006) from T. turgidum ssp. dicoccoides (Körn. ex Asch. and Graebn.) Thell. The common winter wheat cultivar ‘VPM1’ was the source of the 2NS translocation (Maia, 1967). Anza was backcrossed six times (BC6) to produce an isogenic line carrying the 2NS translocation (henceforth Anza-2NS), which has been previously released and deposited in the National Small Grain Collection as PI 638742 (Chicaiza et al. 2006). A second Anza isogenic line, which carries Gpc-B1 (henceforth Anza-Gpc-B1), has been previously described (Brevis et al. 2010). Anza-2NS and Anza-Gpc-B1 were intercrossed with a third Anza isogenic line carrying the high molecular weight glutenin subunits Glu-D1 5+10 replacing the subunits 2+12 to develop Lassik. Nematode reproduction was compared in near isogenic wheat lines Lassik, Anza, Anza-2NS and Anza-Gpc-B1 to determine which introgression was responsible for the lower nematode egg counts observed in Lassik compared to Anza. Two additional near-isogenic pairs of lines of near-isogenic lines were produced with the 2NS translocation from VPM1 in Yecora Rojo CItr 17414 (Qualset et al., 1985) and Express (developed by WestBred Inc.), both hard red spring wheat cultivars. Nematode reproduction was also compared on these pairs of lines. In each generation the 2NS segment was selected using a cleaved amplification polymorphic sequence (CAPS) marker (Helguera et al. 2003). After BC6, plants were self-pollinated and lines homozygous for the 2NS translocation were selected. The 25–38 cM 2NS segment translocated to the 2AS chromosome does not recombine with the wheat chromosomes in the presence of the Ph1b gene (Helguera et al. 2003) and, therefore, it is not expected to be altered in the derived near-isogenic lines.

Nematodes

Root-knot nematode strains (Table 1) were maintained as cultures on tomato plants in the greenhouse. Meloidogyne javanica strain VW4, M. incognita strain VW6, and M. hapla Chitwood (northern RKN) strain VW9 have previously been characterized (Gleason et al., 2008; Opperman et al., 2008; Wang et al., 2009). Strains Y2 and Y3 were obtained from California tomato fields in which galling on tomato with the Mi-1 gene had been noted and were identified to species using species-specific primers (Zijlstra et al., 2000) and a CAPs marker from the mitochondrial genome (Powers and Harris, 1993). Virulence on tomato with Mi-1 was confirmed in greenhouse assays. Strains VW4 and VW6 were maintained on tomato cultivar UC82, and the remaining strains were maintained on cv VFNT cherry. VFNT cherry is homozygous for the nematode resistance gene Mi-1 and UC82 does not carry this gene.

Table 1.

Root-knot nematode strains used in this work

Strain
name		 Species Virulence on
tomato with Mi-1 		Source/reference
VW4 Meloidogyne javanica Avirulent Gleason et al., 2008
VW6 M. incognita Avirulent Wang et al., 2009
Y2 M. javanica Virulent Tomato, Yolo County, CA
Y3 M. incognita Virulent Tomato, Yolo County, CA
VW9 M. hapla Virulent Opperman et al., 2008
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Nematode reproduction assays

Assays were carried out on single plants grown in 1L Styrofoam cups with drainage holes in the bottom and filled with sterilized, coarse sand. Plants were watered with nutrient solution. Experiment 1 was carried out in a growth chamber (photoperiod of 16 h of light at 22 °C and 8 h of darkness at 18 °C); 2-week-old plants were inoculated with 2000 freshly hatched RKN juveniles. At 8 weeks after inoculation, four replicates of each treatment were assessed for egg production. Roots were washed and eggs extracted as described in Hussey and Barker (1973). The number of eggs was counted in three or more aliquots of the total egg suspension. Experiments 2 and 3 were carried out in a greenhouse at the University of California, Davis. For Experiment 2, reproduction of M. javanica Y2, M. incognita Y3, and M. hapla VW9 were compared on Anza, Lassik, Anza-2NS and Anza-Gpc-B1. In this experiment, 2-week-old plants were inoculated with 10,000 eggs and egg production on wheat roots was assessed after 6 weeks. Three replicates were assessed for each combination. For Experiment 3, reproduction of M. incognita VW6, M. incognita Y3, M. javanica VW4, and M. javanica Y2 were compared on the wheat genotypes used in Experiment 2 as well as on two near isogenic pairs, Express and Express-2NS and Yecora Rojo and Yecora Rojo-2NS. In this experiment, 2-week-old wheat plants were inoculated with 5,000 eggs and egg production was assessed after 8 weeks. Four replicates were used.

Microplot experiment

A set of 48 microplots, consisting of plastic barrels 61 cm in diameter and 1.1 m deep, embedded in the soil and located on the University of California, Davis campus, were utilized in this experiment (Figure 1). On 18 April 2011, chopped tomato roots with galls and egg masses of Meloidogyne hapla VW9, M. incognita VW6, or M. javanica VW4, or no nematodes were incorporated into the surface soil of each microplot. Each plot was planted with 20 seedlings of Anza or Lassik, or left fallow. Four replicates were made of each combination in a randomized block design. Plants were watered by automatic sprinklers. All plots were hand-weeded throughout the experiment, and the fallow treatment was maintained free of plants. On 25 July 2011, 99 days after experiment initiation, above-ground, dry-weight biomass of wheat was determined by cutting plants at soil level and oven-drying at 65°C for 1 week. Duplicate bioassays for nematode reproduction or survival were set up with soil cores from each of the 48 microplots. For each bioassay, five cores of soil from a microplot were added to sand in a pot and a tomato seedling (UC82) was planted. These 96 pots with tomato plants were maintained in the greenhouse and the roots were assessed after 6 weeks according to the Root-knot Infection Index of Daulton and Nusbaum (1961). The Root-knot Index spans a 0 to 100 scale where 100 represents mass invasion of roots of bioassays plants by nematodes and severe galling.

Figure 1.

Figure 1

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Microplots with wheat. Representative microplots planted with wheat cultivars Lassik or Anza or left fallow. Microplots were covered with wire mesh baskets to keep out pests. This picture was taken in early July 2011.

Statistical analysis

Data were analyzed using ANOVA (analysis of variance) as implemented in SAS statistical package version 9.2 (SAS Institute Inc., Cary, NC). Contrasts were performed between lines carrying the 2NS translocation and the corresponding near-isogenic controls lacking the translocation. Homogeneity of variances was tested using Levene’s test and normality of residuals using the Shapiro-Wilk test as implemented in SAS 9.2. When significant departures from homogeneity of variances or normality of residuals were found, data were transformed using either the log(Y+1) or the square root (Y+0.05) transformations, which in all cases restored normality of residuals and homogeneity of variances. The original untransformed means are provided in the Tables. Experiments 1 and 2 were organized as a Complete Randomized Design and the microplot experiment was organized as a Randomized Complete Block Design.

RESULTS

Wheat cultivars Lassik and Anza differ in resistance to Meloidogyne javanica

In preliminary experiments we found that the wheat cultivar Lassik supported little or no egg production for several RKN isolates. This result was unexpected as the genetically similar wheat cultivar Anza was previously reported to be a host for both M. incognita and M. javanica (Roberts and Van Gundy, 1981; Roberts et al., 1982). To investigate this further, we compared reproduction of M. javanica VW4 on Anza and Lassik in a growth chamber assay (Experiment 1). At 8 weeks after inoculation, significantly more (P <0. 001) eggs were produced on Anza than on Lassik (42,000 vs. 5,000 eggs per plant).

Resistance is localized to the 2NS introgression

A second experiment (Experiment 2) was performed to determine which of the two alien introgressions in Lassik (2NS from T. ventricosum or Gpc-B1 from T. turgidum ssp. dicoccoides) was the source of the RKN resistance and to investigate the spectrum of the observed nematode resistance. Egg production of M. javanica Y2, M. incognita Y3, and M. hapla VW9 was assessed on Anza, Lassik and two independent BC6 isogenic lines of Anza carrying either the 2NS or the Gpc-B1 introgression (Table 2).

Table 2.

Egg production of Mi-1-virulent nematodes on wheat cultivars with different introgressions 6 weeks after inoculation. Experiment 2.

Mean number of eggs per root system
Wheat cultivar Meloidogyne
javanica Y2† 		Meloidogyne
incognita Y3† 		Meloidogyne
hapla VW9
Anza 1467 300 0
Lassik 133 6 0
Anza-2NS 33 33 0
Anza-Gpc-B1 833 267 0
P contrasts‡ 0.045 0.008 NA
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†

Data was transformed using log10 (Y+1) to meet the assumptions of homogeneity of variance (Levene’s test P > 0.05) and normality of residuals (Shapiro-Wilk P > 0.05). Untransformed means are reported in the Table.

‡

P values correspond to statistical contrasts between 2NS (Lassik and Anza-2NS) and non-2NS lines (Anza and Anza-Gpc-B1)..

None of the wheat cultivars tested supported reproduction of M. hapla VW9. A statistical contrast showed significantly fewer eggs for the lines with the 2NS translocation (Lassik and Anza-2NS) than for the near-isogenic lines without the 2NS translocation (Anza and Anza-Gpc-B1) for both M. javanica Y2 (P=0.008) and M. incognita Y3 (P=0.04). No significant differences were detected for the contrast between the lines including Gpc-B1 (Lassik and Anza-Gpc-B1) and those lacking this gene (Anza and Anza-2NS, P=0.99). These results clearly indicate that resistance to RKN is associated with the 2NS introgression and not with the Gpc-B1 introgression. However, the egg numbers recovered from Anza roots in this experiment were low compared to our previous experiment and results of others (Roberts and Van Gundy, 1981). A likely explanation for the low egg numbers is that eggs were collected from roots and counted at 6 weeks rather than eight weeks after inoculation.

Indeed, when the experiment was repeated with four different nematode strains and eggs were counted after 8 weeks (Experiment 3), significantly higher numbers of eggs were obtained for both resistant and susceptible wheat cultivars (Table 3). In addition to the Anza isogenic lines, this experiment included two other pairs of near-isogenic lines with and without the 2NS translocation in the spring wheat cultivars Yecora Rojo and Express (Table 3). The overall factorial ANOVA showed highly significant differences between both nematode strains (P<0.001) and wheat genotypes (P<0.001). A Tukey test showed that all nematode strains were significantly different from each other in the number of eggs that they produced; therefore the effect of wheat genotypes is presented separately by nematode strain in Table 3. When analyzed across the three wheat genotypes, the lines with the 2NS translocation had significantly fewer RKN eggs than the near-isogenic lines without the 2NS translocation for all four nematode strains (P<0.001, Table 3). The individual contrasts between 2NS and non-2NS isogenic lines by individual wheat genotypes were also significant for all four nematode strains.

Table 3.

Mean number of eggs per root system produced by four Meloidogyne strains on wheat cultivars with or without the 2NS introgression. Experiment 3.

Mean number of eggs per root system
Host Genotype M. incognita
VW6† 		M. incognita
Y3† 		M. javanica
VW4† 		M. javanica
Y2†
Anza 7638 17930 13244 32875
Lassik (2NS) 838 1665 2688 22844
Anza-2NS 988 1685 3148 15804
Anza-Gpc-B1 3438 12113 6695 47250
Express 7683 32067 24820 67917
Express-2NS 175 7225 656 24188
Yecora Rojo 1920 24545 4318 44500
Yecora Rojo-2NS 126 2225 604 14888
P Anza ‡ <0.001 <0.001 0.004 0.002
P Yecora Rojo ‡ 0.019 <0.001 0.026 0.002
P Express ‡ <0.001 <0.001 <0.001 <0.001
P overall ‡ <0.001 <0.001 <0.001 <0.001
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†

Data was transformed using SQUARE ROOT (Y+0.5) to meet the assumptions of homogeneity of variance (Levene’s test P >0.05) and normality of residuals (Shapiro-Wilk P >0.05). Untransformed means are reported in the Table.

‡

P values correspond to contrasts between 2NS and non-2NS lines by genotype and for the three genotypes combined (last row).

Together the results of Experiments 1 through 3 strongly support the hypothesis that the introgressed 2NS region is the source of RKN resistance and that this resistance is functional in different wheat genetic backgrounds.

Microplot experiment

We hypothesized that using a RKN-resistant wheat cultivar rather than a susceptible wheat cultivar as a rotation crop would result in lower levels of infective juveniles in the soil and less damage to the following susceptible crop. Ninety-nine days after establishing a microplot experiment with four different RKN treatments (M. hapla VW9, M. incognita VW6, or M. javanica VW4, or no nematodes) and three plant treatments (Anza, Lassik, no wheat), there were no obvious differences in appearance (Figure 1) and no differences in the biomass of harvested Anza and Lassik among the different nematode treatment plots.

In the subsequent bioassay of nematode population levels using tomato plants grown in soils from the different microplots, the Root-knot Index was lowest on the control tomato plants inoculated with soil cores that received no nematodes (Table 4). Tomato plants grown in soils that were previously inoculated with M. hapla also showed very low Root-knot Indexes that did not differ significantly from the fallow treatment. This was expected since Experiment 2 showed that wheat is not a good host for M. hapla. The Root-knot Indexes of tomato plants grown in soils inoculated with M. incognita and M. javanica did not differ from each other, and therefore were analyzed together. Data was transformed using a square root transformation to satisfy the ANOVA requirements of homogeneity of variances and normality of residuals. Two orthogonal contrasts were used to compare the means of the three treatments. The Root-knot Indexes of tomato plants grown in soils with no wheat (fallow) were significantly lower (P=0.002) than those with wheat, and Indexes for tomato plants in soil from microplots previously planted with the nematode-resistant cultivar Lassik were significantly lower (P=0.02) than those planted with soil planted with the susceptible cultivar Anza.

Table 4.

Root-knot Index of tomato grown with soil cores from microplots after growth of indicated wheat cultivars or fallow. Data shown are the means of 4 blocks*.

Nematode fallow Lassik Anza
No nematodes 0.0 0.0 0.0
M. hapla 0.0 0.1 0.8
M. incognita 3.6 11.3 28.1
M. javanica 2.4 18.1 50.8
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*

No nematodes vs. M. hapla: no significant differences; M. incognita vs. M. javanica: no significant differences; Lassik & Anza vs. fallow for combined M. incognita vs. M. javanica: P= 0.002; Lassik vs. Anza: P= 0.02.

DISCUSSION

Root-knot nematode resistance in cultivated wheat is in the 2NS segment

Comparisons of nematode egg production on near-isogenic pairs of wheat cultivars that differ in the presence of a 2NS segmental translocation derived from the wild wheat relative Aegilops ventricosa (2n = 4x = 28, genomes DDNN) indicate that the nematode resistance gene is present in this 2NS segment. Ae. ventricosa was used to introgress resistance to eyespot caused by the necrotrophic fungus Pseudocercosporella herpotrichoides (Fron) Deighton into the common wheat line 'VPM1' (Maia, 1967). This resistance gene, designated Pch1, was mapped on chromosome 7DL (Jahier et al. 1989). The VPM1 line was later found to carry a translocation between the distal 25–40 cM of Ae. ventricosa chromosome 2NS and wheat chromosome 2AS that includes resistance genes Yr17, Lr37 and Sr38, which confer wheat resistance against stripe rust (Puccinia striiformis West. f. sp. tritici), leaf rust (Puccinia triticina Eriks) and stem rust (Puccinia graminis Pers. f.sp. tritici Eriks. & E. Henn.) (Dyck and Lukow, 1988; Robert et al, 1999). The same Ae. ventricosa 2NS/2AS translocation also confers an intermediate level of resistance to the French pathotype Ha12 of the cereal cyst nematode (Heterodera avenae Wollenweber). This resistance gene was designated Cre5 (Jahier et al 2001). However, the 2NS chromosomal translocation has not been previously reported to carry resistance to root-knot nematodes.

Rkn3 differs from known root-knot nematode resistance in wheat

Previous reports have suggested that there is resistance against various species of root-knot nematodes in wheat and its relatives. Wheat cultivars Laurier (Belair, 1992) and Stephens (Kronstad et al. 1978) have been reported to be resistant to the northern root-knot nematode M. hapla (Mojtahedi et al., 1993). Our results indicate that both Anza and Lassik are also resistant to M. hapla (Table 2), and it may be that wheat is not a host for this nematode species. In contrast, wheat does appear to be a host for M. incognita and M. javanica (Roberts and Van Gundy, 1981; Johnson and Motsinger, 1989) although some wheat cultivars from Egypt and southern USA have been reported to be resistant (Ibrahim et al., 1991; Birchfield, 1983).

A single, dominant gene, Rkn1, mediating resistance to M. javanica in the wild species Ae. tauschii, has been localized genetically to chromosome 6 in the D genome (Kaloshian et al., 1991). However, this trait has not been transferred to cultivated wheat. A second gene, Rkn2, conferring resistance against Meloidogne naasi, commonly known as the cereal root-knot nematode, was derived from Ae. variabilis and has been mapped to chromosome 3S (Yu et al., 1990). Rkn2 is tightly linked to, or may be the same gene as, CreY, which confers resistance against the cereal cyst nematode Heterodera avenae (Barloy et al., 2007). The introgressed 2NS translocation that carries the RKN resistance identified in this paper is on a different homoeologous linkage group than Rkn1 and Rkn2, and therefore, the new designation Rkn3 was assigned to this gene (McIntosh et al. 2011).

The 2NS translocated segment does not recombine with the wheat chromosomes in the presence of the Ph1b gene (Helguera et al., 2003), and therefore any of the markers developed for this translocation (Helguera et al., 2003) can be used to select for the Rkn3 resistance in wheat breeding programs using marker assisted selection. While the lack of recombination of the 2NS segment limits attempts to further reduce the size of the introgressed region, the rust and cyst nematode resistance genes present in the 2NS translocation provide additional value to this alien introgression. Fortunately, the 2NS translocation does not seem to be associated with grain yield penalties. Lassik, which is a backcross derivative of Anza, showed no significant differences in yield from Anza. In addition, high yielding commercial cultivars have been released including this translocation (e.g. Madsen in the US Pacific Northwest, Allan 1989). Preliminary experiments performed at the UC Experimental Field Station in Davis, CA (38° 32’N, 121° 46’ W) in 2005 and 2006 using 7 m2 plots organized in a Split Plot Design with four replications showed no significant decrease in grain yield in the Anza, Express and Yecora Rojo lines with the 2NS translocation relative to the corresponding varieties without the translocation (Dubcovsky unpublished data).

Potential value of Rkn3 wheat in crop rotations

Although susceptible wheat supports nematode reproduction, our findings here and the work of others (Roberts and van Gundy, 1981) indicate that wheat is tolerant of infection by M. incognita and M. javanica and shows little or no yield loss. However, these same nematodes can cause significant yield loss to high value crops grown in rotation sequence with wheat (e.g., tomato or carrots). The use of resistant cultivars as a rotation crop may result in lower soil nematode levels and reduced damage to a less tolerant susceptible crop that follows. The microplot experiment presented here supports this scenario and suggests that use of wheat with Rkn3 is a better rotation choice than susceptible wheat. In the future, it would be interesting to test if combinations of Rkn3 with Rkn1 can be used to further increase the levels of wheat resistance to RKN. As with any management strategy utilizing host resistance, additional tests and monitoring will be required to optimize efficacy.

Acknowledgments

This project was supported by funds from the California Tomato Research Institute, the California Fresh Carrot Advisory Board, the National Research Initiative Competitive Grants 2011-68002-30029 (Triticeae-CAP) from the USDA National Institute of Food and Agriculture and the Howard Hughes Medical Institute and Gordon & Betty Moore Foundation. We acknowledge the technical assistance of XuYun Wang and Liang Zheng.

Abbreviations

2NS

short arm of chromosome 2N from Aegilops ventricosa

ANOVA

analysis of variance

CAPS

cleaved amplified polymorphic sequences

cM

centiMorgan

Gpc

grain protein content

RKN

root knot nematode

Contributor Information

Valerie M. Williamson, Department of Plant Pathology; University of California, Davis, CA 95616.

Varghese Thomas, Dept. of Entomology and Nematology; University of California, Davis, CA 95616.

Howard Ferris, Dept. of Entomology and Nematology; University of California, Davis, CA 95616.

Jorge Dubcovsky, Howard Hughes Medical Institute and Gordon & Betty Moore Foundation Investigator, Dept. of Plant Sciences, University of California, Davis, CA 95616.

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