susceptibility assessment of bell pepper genotypes to crown and root rot disease

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Susceptibility assessment of bellpepper genotypes to crown and rootrot diseaseMehdi Nasr Esfahania, Abbas Nasehia, Pegah Rahmanshirazia, HajarGhadiriana & Farnaz Abed Ashtianiaa Isfahan Agricultural and Natural Resources Research Center,Plant Pests and Diseases Research Institute, Isfahan, Iran.Published online: 16 Aug 2013.

To cite this article: Mehdi Nasr Esfahani, Abbas Nasehi, Pegah Rahmanshirazi, Hajar Ghadirian& Farnaz Abed Ashtiani (2014) Susceptibility assessment of bell pepper genotypes to crownand root rot disease, Archives Of Phytopathology And Plant Protection, 47:8, 944-953, DOI:10.1080/03235408.2013.826541

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Susceptibility assessment of bell pepper genotypes to crown and rootrot disease

Mehdi Nasr Esfahani*, Abbas Nasehi, Pegah Rahmanshirazi, Hajar Ghadirian andFarnaz Abed Ashtiani

Isfahan Agricultural and Natural Resources Research Center, Plant Pests and Diseases ResearchInstitute, Isfahan, Iran

(Received 26 June 2013; final version received 16 July 2013)

Bell Pepper (Capsicum annuum) is one of the important vegetable crops with valuablefood sources, which is used almost around the world. Crown and root rot diseasecaused by Phytophthora capsici is one of the most important diseases of bell pepperin Iran. The present study was conducted to evaluate the susceptibility of differentvarieties of bell pepper to crown and root rot disease under glasshouse condition.Fourteen commonly planted genotypes of bell pepper in Iran were evaluated for theirsusceptibility to infection with the pathogen. For this purpose, disease severity of thechosen genotypes in different growth stages was evaluated. The results indicated thatthe bell pepper genotypes respond differently to pathogenicity tests. Based on clusteranalyses confirmed by the results of SAS analyses, bell pepper cultivars werecategorised in five distinct groups.

Keywords: bell pepper; genotypes; Phytophthora capsici; resistance

Introduction

Bell pepper (Capsicum annum L.), from the family of Solanaceae (genus Capsicum), isan important vegetable crop planted in most parts of the world including Iran. Crownrot disease caused by Phytophthora capsici for the first time was studied on pepper,pumpkin, squash and vegetable marrow in British Colombia in 2004. The pathogencauses destructive blight diseases on Cucurbitaceae and Solanaceae crops as well as onbeans, beets, turnips, cocoa, papaya, etc. (Lamour & Hausbeck 2000; Zamani et al.2007). P. capsici can affect all parts of the plant and causes root, crown and fruit rot inbell pepper plants. Disease symptoms appear 3–4 days after initial infection whentemperature is high. Pre- and post-emergence seedlings damping-off may occur ininfected plants. Infection by the pathogen causes typical symptoms of crown rot, wiltingand eventually complete death of the plant. White fungal growth appears in contami-nated areas when relative humidity is high. Disease is favoured by humid soil with thetemperature of 20–30 °C (Islam et al. 2005; Pavon et al. 2007). P. capsici is introducedby Polach and Webster (1972) as a high potential fungus even with low amount ofinoculums. Mature sporangium of this species is capable to produce 20–40 zoospores(Hickman 1970) with the ability to move in water (Schlumb 1983). The zoosporesmove towards host plants (Erwin & Ribeiro 1996) and produce germ tube in contact

*Corresponding author. Email: [email protected]

Archives of Phytopathology and Plant Protection, 2014Vol. 47, No. 8, 944–953, http://dx.doi.org/10.1080/03235408.2013.826541

� 2013 Taylor & Francis

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with the plant surface (Hickman 1970). Breeding and planting resistant varieties areamong the most proper methods for controlling plant diseases by altering the structureas well as physiology of host plants temporarily or permanently in order to induce theirresistance and tolerance against pathogens (Babadoost 2005). Studies on bell pepperresistance to crown rot disease have previously been conducted on Reinger and Emeraldgenotypes. Aristotle and Paladin varieties are highly resistant to crown and root rot(caused by Phytophthora), but the resistance in aerial parts of the plant is not consider-able. Inia, Diego, Conquest, Corona, Commandant, Colossal and Choco are consideredas resistant varieties of bell pepper to infection by P. capsici (Babadoost et al. 2002).Moreover, based on isozyme analyses, P. capsici is a pathogen with high geneticdiversity among its population (Alizadeh 1983; Mchau & Coffey 1995). Pepper,eggplant, cucumber, squash, cherry, peach and clove have been reported as host plantsfor P. capsici in Iran (Ershad & Hille 1975; Mansoori & Banihashemi 1982; Alavi &Saber 1985; Fassihiani & Ershad 1988; Banihashemi & Fatehi 1989; Alizadeh &Agharafee 1998; Mirabolfathy & Ershad 1998; Ommati & Karimi 1998). Consideringthe importance of bell pepper cultivation in the country, especially under glasshousecondition, the need to do research on the response of pepper cultivars to crown rotdisease is inevitable. Therefore, 14 genotypes of most planted bell pepper plants werechosen and disease resistance was evaluated in two experiments under glasshousecondition.

Materials and methods

Collection of the isolate

The fungal isolate was collected from the infected farms in Shahreza, located in IsfahanProvince, Iran. To isolate the pathogen, diseased crowns and roots were washed undertab water for 30min and then surface sterilised with spirit and flame to remove allsurface contaminations. Small sections (2–3mm) from the area between infected andnon-infected parts were taken by scalpel and sterilised with 1% sodium hypochlorite(NaOCl) for 1min and then rinsed in sterile distilled water for three times and dried onfilter paper. Eventually, segments were cultured on potato dextrose agar culture medium(PDA) and incubated at 28 ± 3 °C under 12 h light/dark photoperiod (Ershad 1992).After initial growth of the fungus on the incubated petri dishes, the pathogen wasisolated from single hypha and recultured onto PDA to purify the fungus (Tsao 1983;Ershad 1992). The pathogen was kept in 4 °C for further study.

Greenhouse assessment

Seeds of 14 bell pepper varieties, provided by Sepahan Royesh Company of Isfahan,were used as source of plant materials in this experiment. Prior to sowing, seeds weresurface sterilised with 1% sodium hypochlorite (NaOCl) and then washed with steriledistilled water and kept in wet paper towels at 25 ± 2 °C for 24 h under laboratorycondition to enhance germination. Forty-five germinated seeds were used for eachexperiment with three replications (15 seeds for each replication). Germinated seedswere sown into planting pots containing perlite and peat moss and placed in thechambers at 28 ± 1 °C with relative humidity of 80%.

Small sections (5mm in diameter) of grown P. capsici on PDA medium were placedaround the crown of bell pepper seedlings, when they were at 2–3 leaf growth stageand then seedlings were irrigated regularly. For confirming whether infection exists,

Archives of Phytopathology and Plant Protection 945

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inoculation was done at three stages including seedling, mature plants and floweringstage. Seven days after inoculation, disease severity was evaluated by calculating ofdamping-off percentage in weekly intervals for each replication of different genotypes(Khosrowfar & Banihashemi 2004; Babadoost 2005). The experiments were repeatedtwice to confirm the results.

Statistical analysis

Damping-off of bell pepper plants in different growth stages of all experiments wasanalysed by performing Analysis of Variance (ANOVA) using SAS statistics softwarepackage. Statistical differences among treatments were determined using the Duncan’sMultiple Range Test (DMRT) and T test at 1% probability level. Dendrogram analysiswas performed to categorise different genotypes of bell pepper in relation to thepathogenicity tests using SPSS and SAS software (Alizadeh & Rezaee, 1999).

Results

Assessment of varieties in two different times

The results of this study indicated that inoculation with P. capsici significantly increaseddisease severity in all assessed varieties with a significant difference in various growthstages of bell pepper plants. The results were obtained from two experiments in weeklyintervals, starting seven days after inoculation and were recorded until eighth week asfollows:

First week after inoculation, the highest rate of damping-off was observed in varietyLirica with 12.66 and 12.00 dead plants for the first and second experiments, respec-tively, while the lowest rate of damping-off was observed in variety Hora with 2.33 and2.00 dead plants in the first and second experiments, respectively. After second week,variety Lirica showed the highest number of damping-off in the first (12.66 dead plants)and second (13.66 dead plants) experiments while variety Hora with 3.00 and 2.33 deadplants in the first and second experiments showed the lowest rate of damping-off. In thethird week after inoculation, the highest rate of damping-off was observed in varietyLirica with 13.33 and 14.33 dead plants for the first and second experiments, respec-tively, while the lowest rate of damping-off was observed in variety Hora with 3.33 and3.00 dead plants in the first and the second experiments, respectively. After fourthweek, the highest rate of damping-off was observed in varieties Lirica and Horn (14.00dead plants) in the first and in variety Lirica (15.00 dead plants) in the second experi-ments, while variety Hora had the lowest damping-off in the first (3.33 dead plants)and second (4.66 dead plants) experiments. Variety Horn with 15.00 dead plants in thefirst experiment and variety Lirica with 15.00 dead plants in the first and second experi-ments showed the highest rate of damping-off and variety Hora showed the lowest rateof damping-off in the first (4.00 dead plants) and second (4.66 dead plants) experimentsin the fifth week after inoculation. Six weeks after inoculation, varieties Horn and Liricawith 15.00 dead plants had the highest rate of damping-off in the first and secondexperiments, respectively while the lowest rate of damping-off was observed in varietyHora with 5.00 and 4.66 dead plants in the first and second experiments, respectively.Varieties Horn and Helsinky with 15.00 dead plants in the first experiment and varietiesHorn, Helsinky and Lirica with 15.00 dead plants in the second experiment had thehighest rate of damping-off seven weeks after inoculation, while variety Hora with 6.00

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dead plants in the first experiment and 5.00 dead plants in the second experiment hadthe lowest rate of damping-off. The results after eight weeks indicated that varietiesHorn and Helsinki with 15.00 dead plants in the first experiment and varieties Lirica,Helsinki and Horn with 15.00 dead plants in the second experiment showed the highestrate of damping-off. The lowest rate of damping-off was observed in variety Hora with7.33 dead plants for the first experiment and 7.00 dead plants for the second

Table 1. Average crown and root rot disease in pepper varieties by fungus Phytophthora capsiciin various growth stages (the first test).

Variety

Crown and root rot disease

Stage 1 Stage 2 Stage 3 Stage 4 Stage 5 Stage 6 Stage 7 Stage 8

Ganga 3.67de 4.67d 5.67cd 7.33c 9.33cd 12.00abc 14.00a 14.00aLirica 12.67a 12.67a 13.33a 14.00a 14.00a 14.00a 14.00a 14.00aAranica 4.00cde 4.67d 5.67cd 6.67cd 8.67bcd 11.33c 14.00a 14.00aHelsinki 10.33ab 11.33ab 12.67a 13.33a 14.33a 14.67a 15.00a 15.00aHora 2.33f 3.00e 3.33e 3.33e 4.00e 5.00def 6.00c 7.33cZamboni 6.67bc 7.50c 8.33c 10.33abc 13.33ab 14.33a 14.67a 14.67aBachata 8.67b 11.00ab 11.67ab 12.00ab 12.33ab 13.33ab 14.33a 14.33aPaleo 3.67de 4.00de 4.67d 6.00cd 6.67d 7.33de 8.67bc 10.00bFogo 4.67d 5.00d 5.67cd 6.33cd 6.67d 8.00d 10.33b 13.67aSirena 6.33c 7.00cd 8.00c 8.67bc 9.67bc 11.00c 13.00ab 14.00aHorn 10.67ab 11.67ab 13.00a 14.00a 15.00a 15.00a 15.00a 15.00aPs 9.00b 10.67abc 11.33ab 12.33ab 12.33ab 12.33abc 13.67a 13.67aHot chilli 6.00bcd 7.00cd 8.33c 9.33bc 11.00b 13.00ab 13.00ab 13.00abSirvisi 6.00bcd 7.33c 8.67c 10.33abc 11.67b 13.33ab 14.00a 14.33a

Note: Means with different letters are significantly different using DMRT test at 1% level.

Table 2. Average crown and root rot disease in pepper varieties by fungus Phytophthora capsiciin various growth stages (the second test).

Variety



Ganga 4.00 f 5.33c 6.00cde 6.67e 9.00cd 11.00bc 12.67bc 12.67cLirica 12.00a 13.67a 14.33a 15.00a 15.00a 15.00a 15.00a 15.00aAranica 4.67ef 5.67de 6.33cd 6.67e 7.67d 10.67bcd 14.67a 14.67aHelsinki 11.00ab 12.00ab 13.33ab 14.00ab 14.00ab 14.67a 15.00a 15.00aHora 2.00g 2.33f 3.00f 4.67f 4.67f 4.67f 5.00f 7.00fZamboni 7.00cde 8.00c 8.67c 11.33bc 12.33b 13.67ab 13.67b 13.67abcBachata 9.67bc 10.67b 10.67b 11.33bc 11.67bc 12.67abc 13.67b 13.67abcPaleo 4.67ef 5.00ef 5.33d 6.33e 7.00de 7.67de 9.00d 11.00dFogo 5.33def 5.67dce 6.33cd 6.67e 7.67d 9.00d 11.00c 13.00bcSirena 5.67e 6.67dc 6.67cd 7.67de 8.67cd 10.33c 12.67bc 14.67aHorn 10.33b 12.67ab 13.00ab 13.33abc 13.33abc 14.67a 15.00a 15.00aPs 8.33c 11.33ab 12.33ab 13.33abc 13.33abc 13.33ab 14.67a 14.67aHot

chilli5.33def 6.33c 7.67bcd 9.33cd 10.67c 12.00b 12.67abc 13.00bc

Sirvisi 5.67e 6.67cd 8.33c 9.67cd 11.33 bc 12.33abc 13.33b 14.00ab



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Table 4. ANOVA for crown and root rot disease in pepper varieties by fungus Phytophthoracapsici in various growth stages (the first test).

Stages DF Squares Mean square F value Pr>F

Stage 1 13 763.80 54.56 28.08⁄⁄ <0.0001Stage 2 13 961.38 68.67 18.00⁄⁄ <0.0001Stage 3 13 1178.99 84.21 34.46⁄⁄ <0.0001Stage 4 13 1427.07 101.93 23.04⁄⁄ <0.0001Stage 5 13 1726.1 123.29 22.13⁄⁄ <0.0001Stage 6 13 2054.41 146.74 18.66⁄⁄ <0.0001Stage 7 13 2237.23 159.80 32.15⁄⁄ <0.0001Stage 8 13 2556.34 182.60 27.48⁄⁄ <0.0001

⁄⁄Significant at 1% level of probability.

Table 5. ANOVA for crown and root rot disease in pepper varieties by fungus Phytophthoracapsici in various growth stages (the second test).




Table 3. Average crown and root rot disease in pepper varieties by fungus Phytophthora capsiciin various growth stages (the compound test).

Variety



Ganga 3.83gh 5.00de 5.83f 7.00ef 9.17cd 11.50b 13.33ab 13.33abLirica 12.33a 13.17a 13.83a 14.50a 14.50a 14.50a 14.50a 14.50aAranica 4.33efg 5.17de 6.00efg 6.67e 8.17d 11.00abc 14.33a 14.33aHelsinki 10.67b 11.67ab 13.00ab 13.67ab 14.17a 14.67a 15.00a 15.00aHora 2.17h 2.67f 3.17h 4.00g 4.33f 4.83f 5.50d 7.17dZamboni 6.83d 7.67c 8.50d 10.83c 12.83b 14.00a 14.17a 14.17aBachata 9.17bc 10.33b 11.17c 11.67bc 12.00abc 13.00ab 14.00a 14.00aPaleo 4.17efg 4.50ef 5.00fg 6.17f 6.83e 7.50e 8.83c 10.50cFogo 5.00ef 5.33de 6.00efg 6.50f 7.17e 8.50de 10.67bc 13.33abSirena 6.00de 6.83cd 7.33e 8.17d 9.17cd 10.67c 12.83abc 14.33aHorn 10.50b 12.16ab 13.00ab 13.67ab 14.17a 14.83a 15.00a 15.00aPs 8.67c 11.00b 11.83bc 12.83b 12.83b 12.83ab 14.17a 14.17aHot chilli 5.67de 6.67cd 8.00de 9.33de 10.83c 12.50ab 12.83abc 13.00abSirvisi 5.83de 7.00cd 8.50d 10.00bcd 11.50bc 12.83ab 13.67ab 14.17a



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experiment. The other varieties in all stages were also significantly different and weregrouped in distinct groups (Tables 1, 2, 4 and 5).

Assessment of varieties with combined data

The results of combined experiments indicated that in the first week, varieties Liricawith 12.33 and Hora with 2.16 dead plants had the highest and lowest rate of damping-off, respectively. Variety Ganga with 3.83 dead plants showed the lowest rate of diseaseafter variety Hora. In the second week, the highest rate of damping-off was againobserved in variety Lirica (13.16 dead plants) and the lowest rate of disease wasobserved in varieties Hora and Paleo with 2.66 and 4.55 dead plants, respectively.Based on third-week observations, varieties Lirica (13.83 dead plants), Horn andHelsinki had the most dead plants (13 dead plants) while varieties Hora, Paleo, Aranicaand Fogo (3.16, 5.00, 6.00 and 6.00 dead plants, respectively) had the least dead plants.Four weeks after inoculation, varieties Lirica, Horn and Helsinki (14.5, 13.66 and 13.66dead plants, respectively) showed the highest damping-off while varieties Hora, Paleo,Fogo and Aranica (4.00, 6.16, 6.5 and 6.66 dead plants, respectively) showed thelowest rate of the disease. Based on fifth week observations, variety Lirica with 14.5dead plants and variety Horn as well as variety Helsinki with 14.16 dead plants werethe most infected varieties while varieties Hora with 4.33 dead plants and Paleo with6.83 dead plants were recorded as the least infected varieties. Six weeks afterinoculation, varieties Horn, Lirica and Helsinki (15.00, 14.5 and 14.16 dead plants,respectively) showed the highest damping-off while variety Hora (4.83 dead plans)showed the lowest rate of the disease. In the week seven, varieties Helsinki and Hornwith 15.00 dead plants were recorded as the varieties with the highest infectionfollowed by varieties Lirica, Aranica and PS (14.50, 14.33 and 14.16 dead plants,respectively). Variety Hora with 5.5 dead plants was the least infected variety. In theeighth week after inoculation, varieties Horn, Lirica, Aranica, Sirena, Zamboni, and PS(15.00, 14.5, 14.33, 14.33, 14.16 and 14.16 dead plants, respectively) were the mostsusceptible varieties, while varieties Hora and Paleo (7.16 and 10.5 dead plants,respectively) were recorded as resistant varieties. The other varieties were alsosignificantly distinctive and categorised in related statistical groups based on the rate ofdamping-off (Tables 3 and 6).

Based on the obtained results in this study, the relationship between the diseaseseverity with the different growth stages of plant was linear and positive (although the

Table 6. ANOVA for crown and root rot disease in pepper varieties by fungus Phytophthoracapsici in various growth stages (the compound test).





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severity of disease was different in various varieties of bell pepper) (Table 7). Dendro-gram analysis of the first and second experiments categorised the genotypes into fivedistinct groups. These results are consistent with the obtained results using the DMRT(Figure 1).

Discussion

In the present study, various varieties of bell pepper responded differently to P. capsiciat different growth stages. Fourteen varieties of bell pepper were evaluated in eightdifferent growth stages and the results indicated that in the first growth stage, varietyLirica was significantly different with variety Hora by 82 and 48% damping-off,respectively. Likewise in the second stage, varieties Lirica and Ganga were different (79and 78% damping-off, respectively). Differences of damping-off were observed between

Figure 1. Dendrogram of cluster analysis for resistance to crown and root rot disease in 14varieties based on Ward’s minimum variance method.

Table 7. Comparison of growth stages in terms of crown and root rot disease.

– Stage 1 Stage 2 Stage 3 Stage 4 Stage 5 Stage 6 Stage 7 Stage 8

Stage 1 – �0.84ns �1.53ns �2.37⁄ �3.22⁄⁄ �4.31⁄⁄ �5.53⁄⁄ �6.68⁄⁄

Stage 2 – �0.68ns �1.48ns �2.26⁄ �3.27⁄⁄ �4.38⁄⁄ �5.33⁄⁄

Stage 3 – �0.78ns �1.53ns �2.50⁄ �3.56⁄⁄ �4.42⁄⁄

Stage 4 – �0.74ns �1.69ns �2.74⁄⁄ �3.53⁄⁄

Stage 5 – �0.96ns �2.01⁄ �2.78⁄⁄

Stage 6 – �1.05ns �1.76ns

Stage 7 – �0.64ns

Stage 8 –

ns, ⁄ and ⁄⁄Non-significant and significant at 5 and 1% level of probability, respectively.


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varieties Lirica and Paleo as well (65 and 80%). At the third growth stage, varietiesLirica and Hora were significantly different in the rate of damping-off (77 and 11%,respectively). The difference between varieties Lirica and Paleo as well as betweenvarieties Lirica, Aranica and Fogo were 63, 86, 56 and 63%, respectively. At the fourthgrowth stage, varieties Lirica and Hora were different in the rate of damping-off(72 and 4%). The difference between varieties Lirica and Paleo was 57 and 48%.Varieties Lirica and Fogo as well as varieties Lirica and Aranica were also different(55.17 and 54.02%, respectively). At the fifth growth stage, the rate of disease invariety Lirica was significantly different when compared to variety Hora (70.14%).Difference also was observed between varieties Lirica and Paleo (52.88%). At the sixthgrowth stage, the rate of damping-off in Helsinky variety was significantly differentfrom variety Hora (67.04%). The difference of disease severity between varietiesHelsinky and Paleo was recorded as 48.68%. At seventh growth stage, both varietiesHelsinky and Horn were significantly different in the rate of damping-off when com-pared with variety Hora (63.33%). Variety Helsinky also was different with varietiesPaleo and Fogo (41.11 and 28.89%, respectively). At the eighth growth stage, damping-off bell pepper plants in varieties Helsinky and Horn were significantly different fromvariety Hora (52.27%).

Results of this study were consistent with previous ones (Kim & Kim 2009) indicat-ing that in susceptible varieties, epidermal cells as well as vascular cells get severelyinfected by the pathogen while in resistant varieties such as CM344, infection isobserved in epidermal cells rather than in skin cells. They believe that this mechanismof resistance could be related to proteins and polysaccharides discharge from plant rootand thicker layer between epidermis and skin as well as injured periderm. Howard et al.(1976), Alizadeh and Rezaee (1999), Mirabolfathy (2002) studied the susceptibility ofplants to Phytophthora, but there are little studies which evaluated effect ofPhytophthora on bell pepper plants. Babadoost et al. (2002) investigated the effect ofpathogen on different varieties of bell pepper and observed that plants responddifferently to infection by pathogen. The documentation of effectiveness of plantingresistant varieties for controlling the disease caused by Phytophthora drechsleri has alsobeen substantiated by Kim et al. (2001). Their study was enriched using biometricmethods. In their study, 18 varieties of squash were introduced as resistant varieties andwere used as resistant rootstock. The study confirmed effectiveness of planting resistantvarieties to control damping-off disease caused by P. drechsleri.

Pande et al. (2005) conducted an experiment to assess the resistance of chickpeaplants to Phytophthora damping-off caused by P. drechsleri and the results indicatedthat among studied lines, <10% were resistant, 10–20% were tolerant resistant, 20–40%were tolerant susceptible and 40–100% were susceptible to the disease. Although thehost plant of their study was different from present study, the same genus of funguswas used as pathogen in both studies which confirms the effectiveness of plantingresistant varieties.

Phytophthora damping-off caused by P. drechsleri in lettuce has been reported byHyeong-Jin et al. (2001). Different host plants including lettuce, cabbage, tomato andbell pepper were inoculated with different isolates of fungus and the results indicatedthat the rate of resistance was different among the host plants as well as amongdifferent varieties of a selected plant such as bell pepper. Molot et al. (1984) showedthat the pepper stems which were treated with elicitor G5 were resistant to infection byP. capsici. This effect was more pronounced in resistant varieties rather than susceptiblevarieties. Based on their observations, stem treatment with elicitor G5 did not induce


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capsidiol production. Therefore, other defence mechanisms seem to be associated withthis issue. Quantitative resistance loci (QRLs) in host plant genome play an importantrole in bell pepper resistance to damping-off caused by the fungus P. capsici. Six QRLsregions which were associated with resistance to P. capsici were identified on 4, 5, 6,11 and 12 chromosomes (Thabuis et al. 2003).

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susceptibility assessment of bell pepper genotypes to crown and root rot disease

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