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Plant Health 2023

 

Genetic Analysis of Phytophthora Root Rot Race-specific Resistance in Chile Pepper

Authors:
Ariadna Monroy-BarbosaDepartment of Plant and Environmental Science, New Mexico State University, Las Cruces, NM 88003-8003

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Paul W. BoslandDepartment of Plant and Environmental Science, New Mexico State University, Las Cruces, NM 88003-8003

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Abstract

Phytophthora capsici Leon., causal agent of phytophthora root rot, is one of the most devastating pathogens attacking chile pepper (Capsicum annuum L.) plants. Many studies have tried to better understand phytophthora resistance, but the genetic behavior is not completely understood. To determine if phytophthora root rot resistance in chile pepper is controlled by multiple alleles at a few loci, or multiple genes at different loci, five recombinant inbred lines (RILs) were evaluated. The resistant accession, Criollo de Morelos-334, and the susceptible cultivar, Early Jalapeno, were hybridized to develop multiple RILs. After seven generations of selfing using the single seed descent method, four RILs were selected based on their phenotypic response to inoculation by five P. capsici isolates. The RILs were hybridized to each other to obtain F1 and F2 populations. The F2 populations were inoculated with single and a pair of races of P. capsici. When the F2 populations were inoculated with a single race, ratios of three resistant:one susceptible were obtained in the majority of the populations, indicating the action of an independent single gene. When the F2 populations were inoculated with a combination of two races, segregation ratios of 15 resistant:one susceptible were observed in two populations out of the four populations. The presence of susceptible individuals in all of the F2 population indicates that the resistant genes for the different P. capsici races are located at different loci. However, the rejection of the segregation ratio in one of the F2 population under a single race inoculation and in two of the F2 populations challenged with a combination of two races suggest a linkage phenomenon between some of the R genes. None of the RILs evaluated in this study displayed allelism for phytophthora root rot resistance.

Chile pepper is a very important crop worldwide, being used in the food industry as well as a coloring agent for food and cosmetics, an ingredient in pain relief medicine, antimugger sprays, and so on (Bosland, 1996; Lucier and Jerardo, 2006; Morrison and Skaggs, 2004). Chile pepper production can be dramatically reduced by a soilborne disease called phytophthora blight caused by the oomycete Phytophthora capsici. In 1922, P. capsici was first described as the pathogen of chile pepper in New Mexico (Leonian, 1922). This pathogen can completely devastate a field of chile peppers (Sanogo and Carpenter, 2006). The pathogen causes multiple disease syndromes such as phytophthora root rot, fruit rot, stem blight, and foliar blight (Sy et al., 2005). Based on host differential studies, nine P. capsici races for root rot syndrome were reported by Oelke et al. (2003) and, after that, 11 more races were identified by Sy et al. (2008). Thus, the presence of different P. capsici races complicates the control of this pathogen even more.

To develop strategies to control P. capsici, it is necessary to understand the genetic interaction between the plant and the pathogen. A gene-for-gene theory explains the specificity of this interaction as the recognition of an elicitor encoded by an Avr gene in the pathogen by a receptor encoded by its complementary R gene in the host and that this matching gene pair has an epistatic effect over any other incompatible gene pair (Crute and Pink, 1996; Flor, 1955). The specific recognition of R genes and Avr genes results in the induction of a signal transduction in the host that will initiate host defense responses against all the pathogen races and the inhibition of the pathogen growth (Staskawicz, 2001; Tyler, 2002). According to the gene-for-gene model when a resistant trait is manifested by the effect of dominant alleles, it is not possible to observe segregation. The complete lack of segregation for susceptibility provides strong evidence that the resistant phenotype is located at one locus (Chen et al., 2001). On the other hand, when two independent loci control the resistance phenotype, a segregating F2 population should contain at least 1/16 susceptible segregants, which represent the presence of double homozygous recessives (Chen et al., 2001).

Several inheritance studies on P. capsici resistance in chile pepper have produced different results such as single-gene, two-gene, or multiple-gene systems (Barksdale et al., 1984; Guerrero-Moreno and Laborde, 1980; Ortega et al., 1995; Saini and Sharma, 1978; Smith et al., 1967; Sy et al., 2005; Walker and Bosland, 1999). The disparity in the reports published could be because of the use of different isolates, the cultivars, or environmental conditions. Resistance to P. capsici in C. annuum is genetically and physiologically complex (Quirin et al., 2005). Thus, despite the existence of resistant accessions such as Criollo de Morelos-334 (CM-334) and extensive breeding efforts, no chile pepper cultivars with universal resistance to phytophthora root rot have been commercially released (Oelke et al., 2003). Thus, the main objective of this study was to determine whether different phytophthora root rot race-specific resistance phenotypes for P. capsici races 1, 4, 5, 6, and 12 are controlled by multiple alleles at few loci or multiple genes at different loci using a set of New Mexico recombinant inbred lines (NMRILs). This information will aid in characterizing the genotype of resistant materials and also facilitate the mapping of phytophthora root rot resistance in chile pepper. In addition, these results will increase the efficiency of breeding programs in developing phytophthora root rot-resistant cultivars.

Materials and Methods

Plant materials

A population of 67 NMRILs was developed by Sy et al. (2008) from the hybridization of the resistant line CM-334 with the susceptible commercial cultivar Early Jalapeno. The NMRILs were obtained through the single seed descent procedure (Lister and Dean, 1993). This procedure was repeated until the seventh generation. From the previous population, four NMRILs—NMRILA, NMRILB, NMRILK, and NMRILX—were hybridized to generate F1 and F2 populations. The four NMRILs were chosen based on their phenotypic reaction when inoculated with a given isolate (Table 1). The hybridizations evaluated were: NMRILA × NMRILX, NMRILB × NMRILX, and NMRILB × NMRILK.

Table 1.

Phenotypic response of four Capsicum annuum New Mexico recombinant inbred lines inoculated with five different Phytophthora capsici isolates.

Table 1.

In a greenhouse, two seeds of each NMRIL were sown per cell in plastic trays of 72 cells (TOD 1804; T.O. Plastics, Clearwater, MN). Trays were filled with a commercial peatmoss–vermiculite soil mixture (Sun Gro Redi-earth Plug and Seedling Mix; Sun Gro Horticulture, Bellevue, WA), and they were placed on propagation pads to maintain soil temperature at 28 °C to promote seed germination. The trays were watered twice per day and fertilized with a 14N–6.2P–11.6K slow-release fertilizer (Osmocote 14-14-14; Scotts, Marysville, OH) as needed until the four- to six-true-leaf stage.

Inoculum

For this study, five P. capsici races were used: race 1 (ATCC no. MYA-2289), race 4 (6021EPPWS), race 5 (6021EPPWS), race 6 (6022EPPWS), and race 12 (6534EPPWS). The first isolate is located at American Type Culture Collection (ATTC), the rest of the isolates were provided by S. Sanogo of New Mexico State University. The races were maintained separately on water agar plates at 24 °C (Oelke et al., 2003). For inoculation, a 0.5-cm diameter plug was cut from the water agar medium, transferred to V8 agar, and maintained in an incubator at 28 °C for a period of 4 to 8 d until sporangia formation. After this, the V8 agar was cut into 15 to 18 pieces and transferred to 15-mm petri plates partially filled with sterilized distilled water. The plates were maintained in an incubator for 2 d at 28 °C. To promote zoospore release, the water plates were incubated at 10 °C for 1 h and placed back into the 28 °C incubator for another hour. The zoospores were collected and counted using a hemacytometer. The inoculum concentration was adjusted to 2000 zoospores/mL. The seedling screening method used is described by Bosland and Lindsey (1991). Seedlings were inoculated at the four- to six-true-leaf stages.

Inoculation with a single race.

Each cell was inoculated with 5 mL of the 2000 zoospores/mL inoculum, giving a final concentration of 10,000 zoospores per cell. The root area of the cell was kept in a flooded condition for 48 h. Propagation pads ensured a soil temperature of 28 °C.

Inoculation with a combination of two races.

The combinations of races used in this study were races 1 + 4, races 1 + 5, races 1 + 12, and races 4 + 6. These combinations were chosen because they varied in their specific phenotypic reaction to the NMRILs (Table 1). Plants were inoculated with 2.5 mL of each race, giving a final inoculum concentration of 10,000 zoospores per cell, the same concentration as with the single race.

Scoring

In this study, two phenotypic reactions were evaluated: resistant and susceptible. A disease assessment described by Bosland and Lindsey (1991) was used for the scoring. Plants with no symptoms (0 to 1) were considered resistant, although plants with brown roots, slight stunting (2), and very small lesion from stems (3); brown roots, small lesions on stems, lower leaves wilted, and stunted plants (5); brown roots, large lesion on stems, girdling, whole plant wilted, and stunted (7) to death (9) were considered susceptible. Even numbers for levels were used for intermediate responses. CM-334 was used as the resistant control, and ‘Early Jalapeno’ was used as the susceptible control. The plants were scored ≈10 d after inoculation when the susceptible control, ‘Early Jalapeno’, was dead (9). According to Bosland and Lindsey (1991), any plant that displays symptoms will be considered susceptible because it will not be able to reach the reproduction stage. Resistant:susceptible ratios were given as result of the scoring.

A test for goodness-of-fit was developed for the F1 progeny and F2 populations against Mendelian ratios for inheritance of one gene (three resistant:one susceptible) and two independent dominant genes (15 resistant:one susceptible). The segregation ratios were evaluated using an α = 0.05. The hypothesis was considered rejected for that specific segregation ratio for any population with P ≤ 0.0001.

Results

The resistant control, CM-334, had a resistant phenotype against all the races, and combination of races; CM-334 never displayed any disease symptoms. The susceptible control, ‘Early Jalapeno’, displayed disease symptoms against all the races and combination of races. Usually, 10 d after inoculation ‘Early Jalapeno’ scored between levels 8 and 9. When NMRILA, NMRILB, NMRILK, and NMRILX were challenged with a single race, the NMRILs displayed different phenotypic reactions. Thus, a host differential reaction was observed when the NMRILs were inoculated with the same race, and one displayed a resistant phenotype and the other displayed a susceptible phenotype (see phenotypic reaction of NMRILs in Table 2). The NMRILs' phenotypic reactions obtained in this study agreed with the results obtained by Sy et al. (2008). The F1 populations from all the hybridizations displayed complete resistance when a single race was used for inoculation (Table 2).

Table 2.

Phenotypic response of Capsicum annuum New Mexico recombinant inbred lines hybridizations for Phytophthora capsici root rot resistance in parent, F1 progeny, and F2 populations.

Table 2.

When the F2 populations were inoculated with a single race, segregation ratios of three resistant:one susceptible were found in all the hybridization with the exception of NMRILB × NMRILX inoculated with race 4 (Table 2). In this case, the hypothesis was rejected (Table 2).

When the F2 populations from the hybridizations NMRILA × NMRILX and NMRILB × NMRILK were inoculated with the combination of two races, segregation ratios of 15 resistant:one susceptible were observed [i.e., races 1 + 5 and 4 + 6 (Table 2)]. On the contrary, when the F2 populations from the hybridization NMRILB × NMRILX were inoculated with the combination of two races [i.e., isolates 1 + 4 and 1 + 12], segregation ratios of 15 resistant:one susceptible were rejected (P < 0.0001) (Table 2). Nevertheless, susceptible individuals were found in all the F2 populations.

Discussion

The resistance guided by a gene-for-gene relationship is also called race-specific resistance, in which the activation of the resistance depends on specific recognition on the invading pathogen by the plant (Keen, 1990). When the F2 populations were inoculated with a single race, segregation ratios of three resistant:one susceptible were observed in the majority of the hybridizations, confirming that the resistant phenotypes are determined by a single dominant gene for each P. capsici race as reported by Sy et al. (2005) and Walker and Bosland (1999). Thus, the gene-for-gene relationship between C. annuum and P. capsici for root rot resistance was confirmed in this study, and one specific R gene was required for each P. capsici race to trigger a resistant reaction in the NMRILs. The recognition of race-specific resistance in the P. capsici–C. annuum interaction will aid plant breeders in selecting appropriate resistant cultivars for future hybridizations (Sy et al., 2008; van de Weg, 1997). Because different geographical regions may have different races of P. capsici, plant breeders may need to breed for a specific production region, pyramiding a number of specific genes to confer resistance into a cultivar (Acquaah, 2007). On the other hand, the rejection of the 3:1 segregation ratio in the F2 population of the hybridization NMRILB × NMRILX under single inoculation of race 4 suggested a linkage phenomenon, in which linkage affects the frequencies of various gene combinations (Chahal and Gosal, 2002).

When the F2 populations were inoculated with a combination of two races, segregation for susceptible individuals was observed. In many cases, a single R gene can provide complete resistance to one or more strains of particular pathogen (McDowell and Woffenden, 2003). Thus, the absolute absence of segregation for susceptibility indicates that the genes share a common locus with other alleles (Chen et al., 2001). On the other hand, the presence of susceptible individuals in the F2 populations is strong evidence that the genes involved in controlling the resistance in this study are not allelic (Boiteux, 1995). The segregation ratio of 15 resistant:one susceptible in the hybridization NMRILB × NMRILK against combination of races 1 + 5 and NMRILA × NMRILX against races 4 + 6 revealed the presence of two dominant independent R genes located at different loci (Ma et al., 2002; Zhen et al., 2006), each one providing resistance to a different P. capsici race. The segregation ratio of 15 resistant:one susceptible individuals in the F2 population indicates that the resistant genes act independently in the recognition of each specific P. capsici race. Digenic segregation was expected in the hybridizations evaluated as a result of differential responses of the NMRILs toward the different P. capsici isolates used. For the hybridization NMRILB × NMRILX against races 1 + 4 and races 1 + 12, the appearance of susceptible individuals in the F2 population is proof of two loci. However, the rejection of a 15:1 ratio suggests that the two loci are linked for the R genes of those specific races. Linkage is defined as the tendency of various genes to be inherited as a block because of being situated on the same chromosomal region (Chahal and Gosal, 2002). Several genetic and molecular studies have shown that plant pathogen-specific R genes are frequently linked within genome regions of various sizes (Grube et al., 2000; Huang et al., 2004; Moreau et al., 1998).

The results reported here for the R genes for races 1, 4, 5, 6, and 12 indicate they are located at different loci. However, resistant genes for races 1 and 4 are linked. Possible linkage was observed also between R genes for races 1 and 12. Other studies in chile pepper have shown the presence of linkage between different R genes. For instance, Yeam et al. (2005) reported for potyvirus resistance the presence of two dominant alleles that were tightly linked but clearly distinct.

The five R genes evaluated in this study segregated independently, indicating different loci for each resistant gene. Screening more P. capsici isolates, different from the five isolates used in this study, could display evidence of allelism for different resistant genes as was reported by Thabuis et al. (2004).

In the results reported here, all populations displayed segregation; thus, no evidence of allelism was observed. The presence of susceptible individuals in all of the F2 populations indicates that at least five loci for R genes to phytophthora root rot are present in the C. annuum genome. Having several loci for phytophthora root rot resistance will enable plant breeders to pyramid resistant alleles in Capsicum L. Pyramiding of genes involves the accumulation of several R genes into the same line to create a multiple gene-resistant cultivar (Chahal and Gosal, 2002). Because Capsicum is a diploid plant, it is only possible to introduce two resistant alleles per locus. Thus, the information obtained in this study will assist in introducing several phytophthora root rot R genes into chile pepper cultivars.

Literature Cited

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    • Crossref
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    • Search Google Scholar
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    • Crossref
    • Search Google Scholar
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  • Acquaah, G. 2007 Principles of plant genetics and breeding 1st Ed Blackwell Publishing Malsen, MA

  • Barksdale, T.H. , Papavizas, G.C. & Johnston, S.A. 1984 Resistance to foliar blight and crown rot of pepper caused by Phytophthora capsici Plant Dis. 68 506 509

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Boiteux, L.S. 1995 Allelic relationship between genes for resistance to tomato spotted wilt tospovirus in Capsicum chinense Theor. Appl. Genet. 90 146 149

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Bosland, P.W. 1996 Capsicums: Innovative uses of an ancient crop 479 487 Janick J. Progress in new crops ASHS Press Arlington, VA

  • Bosland, P.W. & Lindsey, D.L. 1991 A seedling screen for phytophthora root rot of pepper, Capsicum annuum Plant Dis. 75 1048 1050

  • Chahal, G.S. & Gosal, S.S. 2002 Principles and procedures of plant breeding: Biotechnological and conventional approaches Alpha Science Intl Harrow, UK

    • Search Google Scholar
    • Export Citation
  • Chen, P. , Ma, G. , Buss, G.R. , Gunduz, I. , Roane, C.W. & Tolin, S.A. 2001 Inheritance and allelism test of Raiden soybean for resistance to soybean mosaic virus J. Hered. 92 51 55

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Crute, I.R. & Pink, A.C. 1996 Genetics and utilization of pathogen resistance in plants Plant Cell 8 1747 1755

  • Flor, H.H. 1955 Host-parasite interaction in flax rust—Its genetic and other implications Phytopathology 45 680 685

  • Grube, R.C. , Radwansky, E.R. & Jahn, M. 2000 Comparative genetics of disease resistance within the Solanaceae Genetics 155 873 887

  • Guerrero-Moreno, A. & Laborde, J.A. 1980 Current status of pepper breeding for resistance to Phytophthora capsici in Mexico. Synopsis IVth Mtg Capsicum Working Group of EUCARPIA 52 56

    • Search Google Scholar
    • Export Citation
  • Huang, S. , Vleeshouwers, V.G.A. , Werij, J.S. , Hutten, R.C.B. , van Eck, H.J. , Visser, R.G.F. & Jacobsen, E. 2004 The R3 resistance to Phytophthora infestans in potato (Solanum tuberosum L.) is conferred by two closely linked R-genes with distinct specificities Mol. Plant Microbe Interact. 4 428 435

    • Search Google Scholar
    • Export Citation
  • Keen, N.T. 1990 Gene-for-gene complementarity in plant–pathogen interactions Annu. Rev. Genet. 24 447 463

  • Leonian, L.H. 1922 Stem and fruit blight of peppers caused by Phytophthora capsici Phytopathology 12 401 408

  • Lister, C. & Dean, C. 1993 Recombinant inbred lines for mapping RFLP and phenotypic markers in Arabidopsis thaliana Plant J. 4 745 750

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lucier, G. & Jerardo, A. 2006 Vegetables and melons outlook, commodity highlight: Chile peppers 23 Feb. 2006 <http://www.ers.usda.gov/publications/vgs/2006/02Feb/vgs313.pdf>.

    • Search Google Scholar
    • Export Citation
  • Ma, G. , Chen, P. , Buss, G.R. & Tolin, S.A. 2002 Complementary action of two independent dominant genes in columbia soybean for resistance to soybean mosaic virus J. Hered. 93 179 184

    • Crossref
    • Search Google Scholar
    • Export Citation
  • McDowell, J.M. & Woffenden, B.J. 2003 Plant disease resistance genes: Recent insights and potential applications Biotechnology 21 178 183

    • Search Google Scholar
    • Export Citation
  • Moreau, P. , Thoquet, P. , Olivier, J. , Laterrot, H. & Grimsley, N. 1998 Genetic mapping of Ph-2, a single locus controlling partial resistant to Phytophthora infestans in tomato Mol. Plant Microbe Interact. 11 259 269

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Morrison, L. & Skaggs, R. 2004 U.S. Imports and exports of chile pepper and pepper products: Frequently asked questions New Mexico Chile Task Force Rpt. No. 15. New Mexico State Univ., College Agr. Home Economics. Coop. Ext. Serv., Agr. Expt. Sta Las Cruces

    • Search Google Scholar
    • Export Citation
  • Oelke, L.M. , Steiner, R. & Bosland, P.W. 2003 Differentiation of race specific resistance to phytophthora root rot and foliar blight in Capsicum annuum J. Amer. Soc. Hort. Sci. 128 213 218

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ortega, R.G. , Palazon Español, C. & Cuartero Zueco, J. 1995 Interaction in the pepper–Phytophthora capsici system Plant Breed. 111 74 77

    • Search Google Scholar
    • Export Citation
  • Quirin, E.A. , Ogundiwin, E.A. , Prince, P.J. , Mazourek, M. , Brigs, M.O. , Chlanda, T.S. , Kim, K.-T. , Falise, M. , Kang, B.-C. & Jahn, M.M. 2005 Development of sequence characterized amplified region (SCAR) primers for the detection of Phyto.5.2, a major QTL for resistance to Phytophthora capsici Leon. in pepper Theor. Appl. Genet. 110 605 612

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Saini, S.S. & Sharma, P.P. 1978 Inheritance of resistance to fruit rot (Phytophthora capsici Leon.) and induction of resistance in bell pepper (Capsicum annuum) Euphytica 27 721 723

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sanogo, S. & Carpenter, J. 2006 Incidence of phytophthora blight and verticillium wilt within chile pepper in New Mexico Plant Dis. 90 291 296

  • Smith, P.G. , Kimble, K.A. , Grogan, R.G. & Millet, A.H. 1967 Inheritance of resistance in pepper to phytophthora root-rot Phytopathology 57 377 379

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Ariadna Monroy-BarbosaDepartment of Plant and Environmental Science, New Mexico State University, Las Cruces, NM 88003-8003

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Paul W. BoslandDepartment of Plant and Environmental Science, New Mexico State University, Las Cruces, NM 88003-8003

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Contributor Notes

A contribution of the New Mexico Agr. Expt. Sta., New Mexico State Univ., Las Cruces.

Graduate Research Assistant.

Regents Professor.

Corresponding author. E-mail: arimon@nmsu.edu.

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