Survival of Intervarietal Grafts of Sweet and Serrano Peppers (Capsicum annuum L.) on Pasilla 18M as a New Rootstock Against Phytophthora capsici Leo

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Araceli Guadalupe Mendieta-Vázquez Centro de Ciencias Básicas, Universidad Autónoma de Aguascalientes, Aguascalientes 20100, México

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Fidel Guevara-Lara Centro de Ciencias Básicas, Universidad Autónoma de Aguascalientes, Aguascalientes 20100, México

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Sylvia Patricia Fernández-Pavía Instituto de Investigaciones Agropecuarias y Forestales, Universidad Michoacana de San Nicolás de Hidalgo, Michoacán 58880, México

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Jorge Alejandro Torres-González Centro de Ciencias Agropecuarias, Universidad Autónoma de Aguascalientes, Aguascalientes 20100, México

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Jesús Martín Fuantos-Mendoza Centro de Ciencias Agropecuarias, Universidad Autónoma de Aguascalientes, Aguascalientes 20100, México

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Joaquín Sosa-Ramírez Centro de Ciencias Agropecuarias, Universidad Autónoma de Aguascalientes, Aguascalientes 20100, México

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José de Jesús Luna-Ruiz Centro de Ciencias Agropecuarias, Universidad Autónoma de Aguascalientes, Aguascalientes 20100, México

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Abstract

The genus Capsicum has been distinguished by its lack of compatible rootstocks with commercial cultivars to successfully protect against Phytophthora capsici. Criollo de Morelos 334 (CM334) has been used worldwide in crosses and as a rootstock to protect against P. capsici. However, novel sources of resistance to this pathogen, such as ‘Pasilla 18M’ have not yet been explored as rootstocks. A good rootstock should be highly compatible with the scion and also maintain the quality and/or provide a benefit to the grafted cultivar. Our objectives were 1) to evaluate grafting survival using ‘Pasilla 18M’ and CM334 as rootstocks of two susceptible commercial cultivars: Sweet Pepper California Wonder (CW) and Serrano Coloso; and 2) to evaluate the efficiency of ‘Pasilla 18M’ as rootstock against P. capsici using CM334 as a resistant control. Grafting survival was analyzed over 58 days after grafting in sets of 60 plants per varietal combination. Disease severity and incidence were recorded during 24 days after inoculation with P. capsici (DAI). Incidence was also evaluated at 54 and 84 DAI. A severity scale from 0 (healthy plant) to 4 (dead plant) was applied to evaluate root rot per plant. Incidence was recorded as the percent of diseased plants (severity >0). Grafting survival of intervarietal grafts was 87% to 94%, similar to ungrafted cultivars, and exceeding autograft survival. Ungrafted and autografted Sweet Pepper and Serrano showed root rot severities 2.3 to 3.3, with 89% to 100% incidence. In contrast, intervarietal grafts remained almost free of infection (severity 0.14; incidence 0% to 4%). CM334 and ‘Pasilla 18M’ rootstocks are highly compatible with ‘Serrano Coloso’ and ‘Sweet Pepper CW’. ‘Pasilla 18M’ confers the same level of protection against P. capsici as CM334.

Chili pepper (Capsicum annuum L.) is one of the most important vegetables in the world; it is the most widely cultivated and popular spice (Duan et al. 2017; Kraft et al. 2014). Chili pepper domestication and diversification is well documented in Mexico (Aguilar-Rincón et al. 2010). The basic food basket of Mexicans includes chili pepper, which is consumed as a vegetable, food colorant, and medicine due to its bioactive compounds (Barchenger et al. 2018; Palma-Martínez et al. 2017). Thus, chili pepper is a high-value crop, contributing to economic benefits for producers (Barchenger et al. 2018).

Sweet and hot peppers present variable degrees of susceptibility to soilborne pathogens such as Phytophthora capsici, Verticillium dahliae, and Meloidogyne spp. (Ergun and Aktas 2018). P. capsici causes root rot, as well as stem, leaf, and fruit blight. Phytophthora root rot is associated with root browning and small root lesions that can rapidly expand into surrounding tissues, killing the root (Barchenger et al. 2018) and limiting crop production. For this reason, P. capsici is considered the most devastating pathogen in the world for chili pepper production, causing losses from 10% to 100% (Sánchez-Chávez et al. 2015) and millions of dollars in annual losses (Bosland 2008; Richins et al. 2010).

Management practices to avoid or reduce the impact of P. capsici include control of irrigation, crop rotation, soil solarization, application of fungicides, and biological control with fungal and bacterial antagonists (Granke et al. 2012; Hausbeck and Lamour 2004; Ristaino 1991; Ristaino and Johnston 1999). In general, management strategies try to reduce losses associated with the pathogen. However, once P. capsici is established in the field, it is difficult to eradicate (Lamour et al. 2012). The strategies applied so far to control this pathogen have not been very effective (Barchenger et al. 2018).

The grafting technique is widely used in Cucurbitaceous and Solanaceous crops (King et al. 2010; Navarrete-Mapen et al. 2020; Osuna-Ávila et al. 2012). Grafting is used to increase vegetable production and resistance to soil abiotic stress such as heat and frost, salinity, drought, water lodging, heavy metals, and organic contaminants (Jang et al. 2012; King et al. 2010). Grafting has been efficient against soilborne pathogens and nematodes (Fallik and Ilic 2014; López-Marín et al. 2013). Commercial grafted cultivars take advantage of the resistance conferred by the rootstock (Navarrete-Mapen et al. 2020). Selected rootstocks provide excellent levels of tolerance in vegetables to devasting diseases caused by fungi, oomycetes, and bacteria such as Didymella bryoniae, Fusarium, Monosporascus cannonballus, Verticillium, Phytophthora, Pseudomonas, and nematodes (Lee et al. 2010).

Grafting of Capsicum spp. has been investigated for various purposes, such as grafting survival, grafting effects on phenology (Soltan et al. 2015), yield and quality of the fruits (Camposeco-Montejo et al. 2018; Jang et al. 2013; Rouphael et al. 2010). In addition, grafting in peppers has been evaluated to avoid abiotic stress (Abidalrazzaq et al. 2021; Schwarz et al. 2010) and to prevent soil diseases caused by different pathogens (Duan et al. 2017; Jang et al. 2012; Navarrete-Mapen et al. 2020; Sánchez-Chávez et al. 2015).

Traditionally, the main rootstock used in Capsicum has been the P. capsici–resistant Criollo de Morelos CM334 (Osuna-Ávila et al. 2012; Sánchez-Chávez et al. 2015). The genetic resistance of CM334 against P. capsici has been used in pepper grafting experiments with satisfactory results (García-Rodríguez et al. 2010; Leal-Fernández et al. 2013; Pintado-López et al. 2017). However, more research is necessary to identify new Capsicum rootstocks, with resistance to P. capsici that are compatible with susceptible cultivars of high economic and market value.

Few sources of resistance to biotic and abiotic stress have been reported in vegetable crops to serve as efficient rootstocks due to compatibility problems that result in weak or null compatibility (de Miguel et al. 2007; King et al. 2010). For example, de Miguel et al. (2007) and Kawaguchi et al. (2008) noted that C. annuum is only compatible with species of the same genus. However, compatibility of intergeneric grafting has been reported for Capsicum and Solanum (Ives et al. 2012). We recently obtained different degrees of grafting compatibility among different species and cultivars of Capsicum using cultivated and wild Solanum as a rootstock (34% with Solanum tuberosum and 24% with S. cardiophyllum as rootstocks) (unpublished data).

The research and development of grafts in the genus Capsicum is an excellent alternative to protect and improve the performance of cultivars of commercial importance against soilborne infections. Currently, most commercial cultivars are susceptible to P. capsici (Barchenger et al. 2018; Hausbeck and Lamour 2004). Therefore, new resistant rootstocks are required to reduce root rot diseases (Abebe et al. 2016). Landraces are good potential sources of resistance against P. capsici (Palma-Martínez et al. 2017), but grafting compatibility and level of protection of new rootstocks must be tested with different commercial cultivars.

Pepper landraces from Mexico could be used to develop cultivars and rootstocks against P. capsici (Retes-Manjarrez et al. 2020). Recently, new sources of resistance against P. capsici have been found in 14 landraces of Piquin, Manzano, Cola de Rata, Jalapeño, and Pasilla peppers (Retes-Manjarrez et al. 2020; Reyes-Tena et al. 2021). Specifically, different landraces of Pasilla are cultivated and consumed in Mexico. In north-central Mexico, they are commercialized and consumed dried to prepare typical dishes; they are also harvested and commercialized unripe, commonly known as Chilaca (Reyes-Tena et al. 2021). Commercial fields of Pasilla landraces showing severe infestations of root rot in Central Mexico are common every year during the rainy season. Single plant selection based on root rot field resistance have been practiced since 1995 by our research group to develop resistant Pasilla cultivars such as Pasilla 18M (Rodríguez-Moreno et al. 2004). Our breeding strategy confirms the genetic resistance of selected plants via controlled inoculations with different P. capsici isolates from Mexico (Reyes-Tena et al. 2021).

The objectives of the present study were 1) to evaluate grafting survival using ‘Pasilla 18M’ and CM334 as rootstocks of two susceptible commercial cultivars: Sweet Pepper CW and Serrano Coloso; and 2) to evaluate the efficiency of ‘Pasilla 18M’ as rootstock against P. capsici.

Materials and Methods

Scions and rootstocks

Four chili pepper cultivars (C. annuum) were used: Serrano Coloso and Sweet Pepper CW as scions of high commercial value, but susceptible to P. capsici; and two P. capsici-resistant rootstocks: Pasilla 18M, and CM334 as a resistant control.

Seedling production

Five hundred seeds per cultivar were treated with fungicide (Quintozeno + Thiram; 1.2 g/100 mL of distilled water). The planting was carried out on 26 Jan 2021 at the facilities of the Comité Estatal Sistema Producto Chile de Aguascalientes (CEPROCH) in Rincón de Romos, Aguascalientes, México. Seeds of scions and rootstocks were sown in previously disinfected 338-cell polystyrene trays with peatmoss (Kekkilä®, Vantaa, Finland). After sowing, the trays were covered with vermiculite, watered, wrapped, and incubated for 10 d in a germination chamber at 20 to 22 °C and 70% relative humidity. When the first emergences were observed, the trays were spread out on tables in the greenhouse, and 42 d after sowing (DAS), 240 seedlings per cultivar were transplanted into 60-cell forest trays with peatmoss. The seedlings received the nutrition program for chili pepper seedlings, preestablished by CEPROCH (0.5 g/L of NPK 12–43–12, 3rd week 1 g/L of NPK 12–43–12 + 0.5 g/L of NPK 19–19–19, from the 4th to 7th week 2 g of NPK 19–19–19). At 45 DAS, seedlings were transferred to a greenhouse of the Centro de Ciencias Agropecuarias of the Universidad Autónoma de Aguascalientes in Jesús María, Mexico.

Grafting process

The grafting process was done 46 DAS and the splicing method was used. During the process, water was sprayed on the plants to keep them turgid. The stem of the rootstock was bevel-cut at ∼45° above the cotyledons; a silicone clamp was placed at the end of the cut stem. The aerial part of the commercial cultivar was cut in a bevel at the same angle and diameter as the rootstock stem; the scion was inserted into the clamp already placed on the rootstock, so that the two cut areas were placed in contact. The cotyledons were removed when abundant callus formation was observed in the graft union area.

Intervarietal grafts and controls

Four intervarietal graft combinations were used: ‘Sweet Pepper’–‘Pasilla 18M’, ‘Sweet Pepper’–CM334, ‘Serrano’–‘Pasilla 18M’, and ‘Serrano’–CM334. Autografts of each cultivar (Sweet Pepper–Sweet Pepper, Serrano–Serrano, Pasilla 18M–Pasilla 18M, and CM334–CM334) were included as controls, as well as ungrafted plants of each cultivar. A total of 12 bifactorial treatments were generated: four intervarietal graft combinations + four autografts + four ungrafted cultivars. Each of the 12 treatments was represented by 60 plants, organized in four experimental units (four replications) of 15 plants each (Table 1).

Table 1.

Organization of treatments.

Table 1.

All grafted plants and their controls were transferred and kept in a healing tunnel with temperatures between 22 and 28 °C, relative humidity between 70% and 90%, without direct sunlight. The maximum light intensity recorded in the tunnels (136 µmol·m−2·s−1) was between 1200 and 1300 HR. All plants remained in the tunnels for 14 d with a humidification program of 2 to 4 h continuous every 1 to 2 h, giving a total of 12 to 15 h of humidification per day, until the start of acclimatization at 14 d after grafting (DAG).

Acclimatization and maintenance of intervarietal grafts and controls

Acclimatization began 14 DAG and consisted of gradually uncovering the healing tunnels to ventilate the grafted and control plants and simultaneously lowering the hours of humidification daily until the plants were completely uncovered and independent of the healing tunnel. This process lasted 5 d (14 to 19 DAG). Starting at 20 DAG, all plants were maintained completely uncovered in the greenhouse with temperatures between 13 and 32 °C, and natural radiation of 230 µmol·m−2·s−1. Once a week, a nutrient solution based on 1 g/L of NPK (18–18–18), and 0.5 g/L of microelements (Fe 6.25%, Zn 2.00%, Mn 2.00%, B 0.40%, Cu 0.15%, and Mo 0.05%) was applied.

Evaluation of grafting survival

Survival of grafts was recorded at 14, 21, 28, 35, 42, and 58 DAG by counting surviving plants (grafted, autografted, and ungrafted plants). The records were organized in a database and the evolution of survival rates were calculated and analyzed by graft treatment.

Inoculation of intervarietal grafts and controls with P. capsici

Inoculum source.

The P. capsici CPV-293 isolate with mating type A1 was used as a source of inoculum. This isolate was obtained from the Phytophthora collection of the Plant Pathology laboratory of Universidad Michoacana de San Nicolás de Hidalgo, México. CPV-293 was isolated from a Poblano pepper commercial field in Yurécuaro, Michoacán. The virulence of isolate CPV-293 was also confirmed in Pasilla cultivars (unpublished).

Inoculum production and plant inoculation.

P. capsici was grown in sterile petri plates with a V8-agar culture medium (250 mL of V8 juice, 2 g of calcium carbonate, 18 g of agar in 1 L of distilled water (Atlas 2010; Fernández-Pavía et al. 2020). Petri plates with P. capsici were incubated at 25 °C; when the mycelium covered the entire plate, eight 8 × 8-mm agar plugs were aseptically removed and transferred to new sterile petri plates with 15 mL of sterile-distilled water and subsequently incubated at room temperature under natural light with water changes every 24 h. All petri plates were checked daily under an optical microscope to verify the formation of sporangia.

When abundant sporangia were observed, release of zoospores was induced by thermal shock exposing the petri plates with sporangia to 4 °C for 30 min. The release of zoospores was verified under an optical microscope; when abundant zoospores were observed in the suspension, they were collected in a sterile Erlenmeyer flask. The concentration of zoospores per milliliter in the stock suspension was estimated with a Neubauer chamber, and the final inoculum was adjusted to 2000 zoospores/mL.

Inoculation of plants was performed in the greenhouse at 58 DAG. Before inoculation, all plants of the 12 varietal combinations (grafted, autografted, and ungrafted controls) were preflooded with water until saturation. Each plant received 5 mL of inoculum (10,000 zoospores) at the base of the stem. Excess water was removed 24 h after inoculation.

Response to P. capsici.

The disease severity and incidence caused by P. capsici were recorded daily from 1 to 24 DAI. The incidence was also evaluated at 54 and 84 DAI. Disease severity per plant was scored based on a severity scale from 0 to 4 where 0 = healthy plant; 1 = slight loss of leaf turgor; 2 = advanced loss of leaf turgor and/or fall of mature leaves; 3 = severe loss of turgor in young and mature leaves, defoliation, visible necrosis at stem base; 4 = wilting and general defoliation, advanced necrosis at the base of the stem. The incidence of the disease per varietal combination was based on the number of diseased plants (severity > 0) and expressed as percent of diseased plants. Disease progression was analyzed for each of the 12 varietal combinations using the area under the disease progress curve (AUDPC):
AUDPC=iYi+Yi+12*(t i+1ti),
where Yi = intensity of the disease on day i (registration of severity or incidence on day i), ti = evaluation period in days after inoculation.

Statistical analysis.

The complete experiment included three factors with different levels per factor: cultivars (Serrano Coloso, Sweet Pepper CW, Pasilla 18M, CM334); graft treatments (intervarietal grafts, autografts, ungrafted plants); and exposure to P. capsici (inoculated, uninoculated). The three factors and their levels (four cultivars × three graft treatments × two inoculation levels) generated a total of 24 combined treatments (12 inoculated and 12 uninoculated varietal combinations). Graft survival, severity, and incidence data were registered upon inoculation with P. capsici. All data were analyzed with Statistica StatSoft 8.0. The survival rate of intervarietal grafts, autografts and ungrafted plants and severity of the disease caused by P. capsici were analyzed by analysis of variance (ANOVA) and Tukey’s test at 0.05 significance. The AUDPC was used to compare the evolution of the disease among intervarietal grafts, autografts, and ungrafted plants.

Results

Grafting survival.

The results of the factorial ANOVA for grafting survival of the 12 varietal combinations at 14, 21, 28, 35, 42, and 58 DAG showed highly significant differences (P < 0.01) for the simple effects of varietal combinations and DAG, but the interaction between varietal combination and DAG was not significant (P = 0.9806). The absence of interaction indicates that the evolution of survival at different DAG was similar among the 12 varietal combinations. In general, the survival of intervarietal grafts remained above 90% up to 58 DAG, surpassing the survival of autografted plants.

Survival of the 12 varietal combinations at 58 DAG is summarized in Table 2. Even when the ANOVA showed significant differences (P = 0.0117) among the 12 varietal combinations, Tukey’s test at 58 DAG indicates that, except for the ‘Serrano’–‘Serrano’ autograft (75% survival), there were no significant differences among 11 of the 12 varietal combinations. Survival among these 11 combinations fluctuated from 80% in the Sweet Pepper–Sweet pepper autograft through 100% in the ungrafted Sweet Pepper and Pasilla 18M cultivars.

Table 2.

Grafting survival of the 12 varietal combinations at 58 d after grafting.

Table 2.

The intervarietal grafts reached survival rates at 58 DAG close to 90% (from 87% in ‘Sweet pepper’–CM334 to 94% in ‘Sweet Pepper’–‘Pasilla 18M’) (Table 2). The partial ANOVA of intervarietal grafts did not detect significant differences (P = 0.6883) for this subgroup, which indicates similar graft-taking efficiency of Pasilla 18M and CM334 rootstocks with susceptible commercial cultivars Serrano Coloso and Sweet Pepper CW.

According to the survival results, the CM334 and Pasilla 18M rootstocks are highly compatible with the commercial cultivars Serrano Coloso and Sweet Pepper CW (Fig. 1).

Fig. 1.
Fig. 1.

Grafting survival of the varietal combinations at 21 and 58 d after grafting (DAG). (A) Intervarietal grafts, (B) autografts, and (C) ungrafted plants at 21 DAG. (D) Scion–rootstock compatibility at 21 DAG. (E) Intervarietal grafts, autografts, and ungrafted plants at 58 DAG. (F) Scion–rootstock compatibility at 58 DAG.

Citation: HortScience 58, 6; 10.21273/HORTSCI17084-23

Graft response to inoculation with P. capsici.

The response of the 12 varietal combinations to P. capsici was evaluated based on disease severity and incidence (Table 3).

Table 3.

Mean severity at 24 d after inoculation with Phytophthora capsici (DAI) and % incidence at 24, 54, and 84 DAI of 12 varietal combinations.

Table 3.

Disease severity.

The factorial ANOVA for severity detected highly significant differences (P < 0.01) among the 12 varietal combinations and among DAI. Likewise, the interaction between varietal combination and DAI was also highly significant (P < 0.01), indicating that the severity caused by P. capsici over 24 DAI evolved differently among the varietal combinations.

The two commercial ungrafted cultivars (Sweet Pepper CW and Serrano Coloso) and their autografts (Sweet Pepper–Sweet Pepper and Serrano–Serrano) showed symptoms at 6 DAI (Fig. 2A, 2B). The mean severity reached at 24 DAI was 3.3 in ungrafted and autografted ‘Sweet Pepper’, and 3.15 in ungrafted ‘Serrano’, whereas the ‘Serrano’ autograft reached a mean severity of 2.33 at 24 DAI, as shown in Table 3. The affected plants showed the typical symptoms caused by P. capsici (wilting and/or loss of turgor in the leaves, necrosis at the base of the stem, and defoliation) (Fig. 2C, 2D). All ungrafted and autografted plants of ‘Sweet Pepper’ and ‘Serrano’ that presented symptoms eventually died within 1 week after the first symptoms appeared (Fig. 3A).

Fig. 2.
Fig. 2.

Severity and incidence of Phytophthora root rot at 6 and 24 d after inoculation with Phytophthora capsici (DAI). (A and B) Evident symptoms of severity and incidence in autografted ‘Sweet Pepper’ and ungrafted ‘Serrano’ at 6 DAI. (C and D) Advanced levels of severity and incidence at 24 DAI in autografted ‘Sweet Pepper’ and autografted ‘Serrano’ at 24 DAI. (E and F) Intervarietal grafts with ‘Pasilla 18M’ and Criollo de Morelos 334 (CM334) rootstocks are free of Phytophthora rot root at 24 DAI.

Citation: HortScience 58, 6; 10.21273/HORTSCI17084-23

Fig. 3.
Fig. 3.

Progress of % incidence of plants affected by P. capsici from 1 to 84 d after inoculation with Phytophthora capsici in the 12 varietal combinations.

Citation: HortScience 58, 6; 10.21273/HORTSCI17084-23

The two rootstocks (CM334 and ‘Pasilla 18M’) and their autografts (CM334–CM334 and ‘Pasilla 18M’–‘Pasilla 18M’) did not present symptoms (except for one ungrafted plant of ‘Pasilla 18M’). Therefore, the mean severity was maintained close to zero at 24 DAI, reaffirming their resistance to P. capsici isolate CPV-293.

‘Sweet Pepper’–CM334 and ‘Serrano’–CM334 interactions presented a mean severity of 0.14 at 24 DAI, whereas the ‘Sweet Pepper’–‘Pasilla 18M’ and ‘Serrano’–‘Pasilla 18M’ grafts remained at zero severity during the 24 DAI (Table 3), confirming that resistance of intervarietal grafts is conferred by the rootstocks (Fig. 2E, 2F). Table 3 shows the mean severity achieved at 24 DAI by the 12 varietal combinations grouped according to graft treatment. Tukey’s test groups with letter “a” eight varietal combinations with mean severity ≤0.15. This group of resistance to P. capsici isolate CPV-293 consists of the four intervarietal grafts together with the two ungrafted and autografted rootstocks. The three varietal combinations most severely affected by P. capsici (severity >3) form group “c” (ungrafted and autografted ‘Sweet Pepper’ and ungrafted ‘Serrano’). The ‘Serrano’–‘Serrano’ autografted (letter b) reached a mean severity of 2.33.

The severity results at 24 DAI clearly show that the two rootstocks ‘Pasilla 18M’ and CM334 conferred the same protection to the susceptible cultivars (Sweet Pepper and Serrano) against P. capsici. The intervarietal grafts remained healthy during the whole phenological cycle until fruit maturity.

Disease incidence.

Ungrafted and autografted commercial cultivars showed incidences from 19% to 33% at 6 DAI, reaching the maximum of 89% to 100% at 54 and 84 DAI (Table 3, Fig. 3A). Conversely, the two rootstocks and their autografts showed disease incidences close to 0% from 1 to 84 DAI (Fig. 3B), reaffirming their resistance to P. capsici and showing a high degree of genetic purity for resistance to isolate CPV-293 in both rootstocks.

The intervarietal grafts with CM334 showed incidences lower than 4% from 1 to 84 DAI. Similarly, intervarietal grafts with ‘Pasilla 18M’ presented 0% incidence from 1 to 84 DAI (Fig. 3C). The incipient or near-zero disease incidence observed in the four intervarietal graft combinations was similar to the disease incidence observed in the two rootstocks.

The disease incidence observed at 84 DAI clearly demonstrates the excellent protection against P. capsici conferred to the susceptible cultivars (Sweet Pepper and Serrano) by the two resistant rootstocks (Pasilla 18M and CM334) (Table 3). The high level of protection conferred by these rootstocks during 84 DAI allowed virtually all grafted and inoculated plants of the susceptible Sweet Pepper and Serrano cultivars to set fruits and complete their commercial harvest cycle free of Phytophthora root rot.

The results clearly show the protection against P. capsici conferred to the susceptible cultivars by the two resistant rootstocks.

Area under the disease progress curve.

The amount of disease accumulated during the 24 DAI of severity assessment and the 84 DAI of incidence in the 12 varietal combinations is shown in Fig. 4. The highest AUDPC severity and incidence values were obtained in ungrafted and autografted commercial cultivars (32.3 to 44.6 for severity, and 6138 to 6872 for incidence) as illustrated in Fig. 4A, 4B, 4D, and 4E. In contrast, the CM334 and Pasilla 18M rootstocks showed low AUDPC values (0 to 2.6 for severity and 0 to 265 for incidence) as shown in Fig. 4A, 4B, 4D, and 4E.

Fig. 4.
Fig. 4.

Area under the disease progress curve (AUDPC) of the 12 combinations (intervarietal grafts and their controls). AUDPC based on disease severity from 1 to 24 d after inoculation with Phytophthora capsici (DAI) (A–C); AUDPC based on disease incidence from 1 to 84 DAI (D–F).

Citation: HortScience 58, 6; 10.21273/HORTSCI17084-23

The AUDPC in intervarietal grafts with Pasilla 18M was null and almost null in grafts with CM334 as shown in Fig. 4C and 4F. The AUDPC values close to zero for severity and incidence observed in the intervarietal grafts reveal the excellent level of protection of these two rootstocks against the isolate CPV-293. Both rootstocks were shown to be resistant to P. capsici and highly compatible with the two commercial and susceptible cultivars Sweet Pepper CW and Serrano Coloso. Therefore, the efficiency of Pasilla 18M and CM334 against P. capsici is equivalent.

The results of the present study demonstrate that grafting is an excellent alternative to reduce problems caused by P. capsici in susceptible cultivars. This is the first report of Pasilla 18M used as a rootstock to protect susceptible cultivars against P. capsici.

Discussion

Survival to the grafting process.

According to the results for grafting survival, CM334 and Pasilla 18M are excellent rootstocks for the susceptible cultivars Sweet Pepper CW, and Serrano Coloso, recognized for their commercial importance (Aguirre-Hernández and Muñoz-Ocotero 2015) and for their high susceptibility to P. capsici (Pintado-López et al. 2017; Sánchez-Chávez et al. 2015).

All intervarietal grafts, as well as their autografted and ungrafted controls, had high and very similar survival rates. The Tukey’s test showed no significant differences among the four intervarietal grafts, therefore it is concluded that both rootstocks are highly compatible with Serrano and Sweet pepper.

Our survival rates agreed with those obtained by Kawaguchi et al. (2008). They obtained 88% survival rates on homogeneous Capsicum–Capsicum grafts with the cultivar Long Red Cayenne. Jang et al. (2012) reported 80% survival in all plants grafted using five commercial rootstocks of C. annuum and nine breeding lines. Johkan et al. (2008) obtained 89% survival in ‘Sweet Pepper’ homografts using young tissue, but only 44% grafting survival with tissue in old stages due to poor cell differentiation and vascular connection caused by low callus formation. However, according to these authors, application of ascorbic acid (AA) improved graft survival to 100%, and 89% in young and old tissue, respectively because AA promotes callus formation.

In the present study, we obtained high grafting survival with no applications of AA or any other phytochemical. The successful assembly of grafting tissues could be explained by plant age and young tissue (46 DAS) of rootstocks and scion cultivars, in agreement with the findings of Johkan et al. (2008). Also, grafting success, according to Acosta-Muñoz (2005) and Lee (1994), is influenced by the high affinity and compatibility of the grafted species. Other factors that enhance grafting success are an environment with abundant oxygen, a temperature of 25 to 27 °C, relative humidity of 80% to 100% (Acosta-Muñoz 2005), and no direct sunlight (de Miguel et al. 2007). Variations in grafting survival among different investigations, however, could be due to the genotype of rootstock and scion, the grafting technique, type of grafting, as well as the skill of the grafter (Osuna-Ávila et al. 2012).

The compatibility of CM334 as rootstock has already been tested and demonstrated with Jalapeño, Chilaca, and Cayenne, with 90% grafting survival each (Osuna-Ávila et al. 2012). Grafting compatibility of CM334–‘Sweet Pepper Triple Star’ has also been tested (Leal-Fernández et al. 2013), but no grafting survival rates have been reported for CM334 with sweet pepper.

Grafting studies on Capsicum have been focused on different aspects—for example, to determine the effect of grafting on bioactive compounds (Chávez-Mendoza et al. 2015); to evaluate agronomic performance of grafts (Ergun and Aktas 2018); to analyze the influence of grafting on fruit characteristics and quality (Jang et al. 2013); to evaluate heat stress and vegetative growth in grafts (López-Marín et al. 2013); to evaluate Capsicum grafts against Begomovirus (Navarrete-Mapen et al. 2020); to evaluate grafting effects on the genotype of subsequent generations (Tsaballa et al. 2013); and to evaluate rootstock genotypes under salt stress (Abidalrazzaq et al. 2021). The rate of survival to the grafting process has not been extensively reported; therefore, it is mandatory to determine the level of compatibility among different races and/or cultivars of Capsicum.

Here the choice of rootstocks was based on the utility or attribute they could confer to the scion and also because landrace populations of pepper have not been sufficiently explored as new sources of genetic resistance to P. capsici (Retes-Manjarrez et al. 2020) or as rootstocks. CM334 has the highest known level of resistance to P. capsici (Lamour et al. 2012; Reyes-Tena et al. 2021; Sánchez-Chávez et al. 2015), therefore it has been used as a resistant rootstock to protect the scion against P. capsici (García-Rodríguez et al. 2010; Leal-Fernández et al. 2013; Osuna-Ávila et al. 2012; Pintado-López et al. 2017; Richins et al. 2010). On the contrary, ‘Pasilla 18M’ had not been previously tested as a rootstock. ‘Pasilla’ peppers have the potential to be used as novel sources of genetic resistance against local pathotypes of P. capsici (Reyes-Tena et al. 2021). In addition, we recently observed genetic incompatibility in crosses of ‘Pasilla 18M’ with ‘Serrano Coloso’ and ‘Sweet Pepper CW’. Therefore, the value of ‘Pasilla 18M’ against P. capsici relies mostly as a rootstock.

‘Pasilla 18M’ is a breading line originally selected in a commercial field of Pasilla landrace showing a severe infestation of Phytophthora root rot in Central Mexico (Rodríguez-Moreno et al. 2004). Single plant selection was based on root rot field resistance, followed by single plant selection of resistant plants after controlled inoculation with different P. capsici isolates from north-central Mexico (Rodríguez-Moreno et al. 2004). In this sense, the use of cultivars as rootstocks with genetic resistance to P. capsici is an effective alternative to avoid problems to cross transferring genetic resistance to susceptible cultivars (García-Rodríguez et al. 2010). The tolerance of Pasilla landraces from north-central Mexico to different isolates of P. capsici has been recently published (Reyes-Tena et al. 2021), confirming that Pasilla landraces could be used in pepper breeding programs as new sources of genetic tolerance and resistance against P. capsici. This is the first research that investigates the use of ‘Pasilla 18M’ as rootstock to test grafting compatibility and protection against P. capsici with commercially important cultivars of Sweet Pepper and Serrano.

Also, the efficacy against P. capsici of both rootstocks has been revealed, as well as their excellent grafting compatibility with ‘Serrano Coloso’ and ‘Sweet Pepper CW’.

Grafting response to P. capsici.

More than 89% incidence was observed at 84 DAI in ungrafted and autografted plants of ‘Sweet Pepper’ and ‘Serrano’. On the contrary, ungrafted, and autografted ‘Pasilla 18M’ and CM334 showed practically no disease at 84 DAI. Similar results were obtained in intervarietal grafts, with 0% incidences in ‘Serrano’–‘Pasilla 18M’ and ‘Sweet Pepper’–‘Pasilla 18M’, and 4% incidence in ‘Serrano’–CM334 and ‘Sweet Pepper’–CM334 at 84 DAI; therefore, it is evident that ‘Sweet Pepper’ and ‘Serrano’ were protected against P. capsici by the two resistant rootstocks. These results are similar to those from previous reports with CM334 as a rootstock. Pintado-López et al. (2017) obtained 0% incidence in ‘Serrano’–CM334 grafts after inoculation with P. capsici, and 100% incidence in ungrafted Serrano plants, which died from the disease caused by P. capsici. García-Rodríguez et al. (2010) observed 0% incidence and null severity in ‘Ancho Rebelde’–CM334 grafts, inoculated with P. capsici, compared with ungrafted ‘Ancho’ plants, which died 15 DAI.

The typical symptoms of severity by Phytophthora root rot were observed by Jang et al. (2012) in grafts with C. annuum, such as stem necrosis, loss of turgor in leaves, defoliation, general wilting, and plant death. In the present study, the highest severities were reached in the autografted and ungrafted plants of ‘Sweet Pepper CW’ and ‘Serrano Coloso’. On the contrary, autografts and ungrafted plants of CM334 had null severity, thus grafts with CM334 as a rootstock had almost null severity. Similar results were obtained in ‘Pasilla 18M’, and the corresponding grafts with ‘Pasilla 18M’ as rootstock. It is evident that both rootstocks prevented the spread of infection.

Two factors in the present study clearly explain disease severity and incidence: DAI and variety combination. Pintado-López et al. (2017) reported that the disease caused by P. capsici began at 17 DAI in ungrafted Serrano plants inoculated with 300,000 zoospores/plant. In the present investigation using 10,000 zoospores/plant, the first symptoms were detected at 3 DAI in ‘Serrano’ and ‘Sweet Pepper’, whereas at 6 to 7 DAI, the disease was already evident in most plants of both cultivars, which presented a gradual and rapid increase of incidence and severity. All infected plants of these two commercial cultivars eventually died in less than 10 d after the first symptoms. On the contrary, the intervarietal grafts of ‘Serrano’–‘CM334’ reported by Pintado-López et al. (2017) showed null severity and 0% incidence after inoculation with P. capsici. We obtained similar results with intervarietal grafts of ‘Serrano’ and ‘Sweet Pepper’ on CM334 and ‘Pasilla 18M’ rootstocks.

The AUDPC also exhibited the highest incidence and severity of P. capsici in the commercial and susceptible cultivars Serrano and Sweet Pepper, compared with the lowest values of AUDPC in the Pasilla 18M and CM334 resistant rootstocks. The AUDPC values were null or almost null in intervarietal grafts. The resistance to P. capsici observed in the grafts is attributed to the rootstocks, which completely suppressed the infection by P. capsici. The AUDPC was reduced in grafted plants of watermelon exposed to Verticillium (Wimer et al. 2015) and in grafts of habanero pepper (C. chinense) with rootstocks of C. annuum var. glabriusculum exposed to Begomovirus (Navarrete-Mapen et al. 2020). It is important to mention that the AUDPC is an epidemiology instrument to compare rates of disease progress over time, based on incidence and severity (Soto-Rojas et al. 2009).

No commercial chili pepper cultivars with genetic resistance to P. capsici are currently available (Glosier et al. 2008). Therefore, the search of resistant rootstocks is a priority to expand the protection of susceptible commercial cultivars to the oomycete (Jang et al. 2012).

García-Rodríguez et al. (2010) determined that the hybrids of ‘Sweet Pepper Tresor’, ‘Atlante’, AR-96030, and AR-96058 are not a source of resistance to P. capsici. These hybrids had 100% disease incidence when exposed to the pathogen, compared with CM334 plants that showed 1% disease incidence. Likewise, Sánchez-Chávez et al. (2015) tested the commercial ‘Sweet Pepper Terrano’ as a rootstock of two sweet pepper cultivars (Fascinato and Janette). ‘Fascinato’–‘Terrano’ and ‘Janette’–‘Terrano’ grafts presented mortalities of 32% and 36% respectively, whereas the ungrafted cultivars of Fascinato and Janette reached 57% and 53% mortality. Therefore, ‘Terrano’ as a rootstock decreased the disease incidence of P. capsici. In our results, ‘Pasilla 18M’, which is also of commercial importance in central Mexico, proved to be highly efficient as a rootstock in protecting ‘Sweet Pepper CW’ and ‘Serrano Coloso’; both intervarietal grafts with Pasilla 18M showed 0% disease incidence and 0 severity.

Although grafting in chili peppers (Capsicum spp.) has not been as widely explored as in other vegetables (López-Marín et al. 2013), this technology should be considered as an alternative to chemical control (Granke et al. 2012; Lamour et al. 2012). Therefore, it is imperative to continue with the search of new rootstocks with resistance not only to P. capsici but also to other biotic and abiotic factors causing important and recurrent crop losses. A good rootstock must have resistance attributes and good compatibility with susceptible cultivars (García-Rodríguez et al. 2010; Gisbert et al. 2011; Lee and Oda 2010).

Although many of the Mexican chili pepper types or races that are resistant or tolerant to P. capsici can be considered as a source of germplasm (Palma-Martínez et al. 2017; Retes-Manjarrez et al. 2020; Reyes-Tena et al. 2021), not all of them can be used as rootstocks of susceptible cultivars to P. capsici. As demonstrated in the investigations by García-Rodríguez et al. (2010) and Sánchez-Chávez et al. (2015), rootstocks can confer certain resistance to the pathogen and reduce incidence and severity rates, but there may be better rootstocks that reduce the percentage of damage, such as CM334. In the present investigation, a new rootstock is proposed, ‘Pasilla 18M’, based on 0% disease incidence and 0 severity in intervarietal grafts with susceptible Sweet Pepper CW and Serrano Coloso cultivars.

Conclusions

Intervarietal grafts with ‘Pasilla 18M’ and CM334 rootstocks had more than 90% grafting survival. ‘Pasilla 18M’ and CM334 are good rootstocks for control of P. capsici. Therefore, ‘Pasilla 18M’ can be used as a new source of resistance against the Mexican isolate CPV-293 of P. capsici.

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  • Fig. 1.

    Grafting survival of the varietal combinations at 21 and 58 d after grafting (DAG). (A) Intervarietal grafts, (B) autografts, and (C) ungrafted plants at 21 DAG. (D) Scion–rootstock compatibility at 21 DAG. (E) Intervarietal grafts, autografts, and ungrafted plants at 58 DAG. (F) Scion–rootstock compatibility at 58 DAG.

  • Fig. 2.

    Severity and incidence of Phytophthora root rot at 6 and 24 d after inoculation with Phytophthora capsici (DAI). (A and B) Evident symptoms of severity and incidence in autografted ‘Sweet Pepper’ and ungrafted ‘Serrano’ at 6 DAI. (C and D) Advanced levels of severity and incidence at 24 DAI in autografted ‘Sweet Pepper’ and autografted ‘Serrano’ at 24 DAI. (E and F) Intervarietal grafts with ‘Pasilla 18M’ and Criollo de Morelos 334 (CM334) rootstocks are free of Phytophthora rot root at 24 DAI.

  • Fig. 3.

    Progress of % incidence of plants affected by P. capsici from 1 to 84 d after inoculation with Phytophthora capsici in the 12 varietal combinations.

  • Fig. 4.

    Area under the disease progress curve (AUDPC) of the 12 combinations (intervarietal grafts and their controls). AUDPC based on disease severity from 1 to 24 d after inoculation with Phytophthora capsici (DAI) (A–C); AUDPC based on disease incidence from 1 to 84 DAI (D–F).

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    • Search Google Scholar
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  • Abidalrazzaq O, Yetisir H, Ulas F & Ulas A. 2021 Enhancing salt stress tolerance of different pepper (Capsicum annuum L.) inbred line genotypes by rootstock with vigorous root system Gesunde Pflanzen. 73 3 375389 https://doi.org/10.1007/s10343-021-00564-4

    • Search Google Scholar
    • Export Citation
  • Acosta-Muñoz AA. 2005 La técnica del injerto en plantas hortícolas Horticultura Internacional. 1 6265

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    • Search Google Scholar
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Araceli Guadalupe Mendieta-Vázquez Centro de Ciencias Básicas, Universidad Autónoma de Aguascalientes, Aguascalientes 20100, México

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Fidel Guevara-Lara Centro de Ciencias Básicas, Universidad Autónoma de Aguascalientes, Aguascalientes 20100, México

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Sylvia Patricia Fernández-Pavía Instituto de Investigaciones Agropecuarias y Forestales, Universidad Michoacana de San Nicolás de Hidalgo, Michoacán 58880, México

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Jorge Alejandro Torres-González Centro de Ciencias Agropecuarias, Universidad Autónoma de Aguascalientes, Aguascalientes 20100, México

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Jesús Martín Fuantos-Mendoza Centro de Ciencias Agropecuarias, Universidad Autónoma de Aguascalientes, Aguascalientes 20100, México

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Joaquín Sosa-Ramírez Centro de Ciencias Agropecuarias, Universidad Autónoma de Aguascalientes, Aguascalientes 20100, México

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José de Jesús Luna-Ruiz Centro de Ciencias Agropecuarias, Universidad Autónoma de Aguascalientes, Aguascalientes 20100, México

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Contributor Notes

The first author was supported by a CONACyT doctoral scholarship number 616194.

To Comité Estatal Sistema Producto Chile de Aguascalientes (CEPROCH) and Juan Martín Díaz Hernández for their support in the production of the experimental seedlings.

J.d.J.L.R. is the corresponding author. E-mail: jesus.luna@edu.uaa.mx.

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  • Fig. 1.

    Grafting survival of the varietal combinations at 21 and 58 d after grafting (DAG). (A) Intervarietal grafts, (B) autografts, and (C) ungrafted plants at 21 DAG. (D) Scion–rootstock compatibility at 21 DAG. (E) Intervarietal grafts, autografts, and ungrafted plants at 58 DAG. (F) Scion–rootstock compatibility at 58 DAG.

  • Fig. 2.

    Severity and incidence of Phytophthora root rot at 6 and 24 d after inoculation with Phytophthora capsici (DAI). (A and B) Evident symptoms of severity and incidence in autografted ‘Sweet Pepper’ and ungrafted ‘Serrano’ at 6 DAI. (C and D) Advanced levels of severity and incidence at 24 DAI in autografted ‘Sweet Pepper’ and autografted ‘Serrano’ at 24 DAI. (E and F) Intervarietal grafts with ‘Pasilla 18M’ and Criollo de Morelos 334 (CM334) rootstocks are free of Phytophthora rot root at 24 DAI.

  • Fig. 3.

    Progress of % incidence of plants affected by P. capsici from 1 to 84 d after inoculation with Phytophthora capsici in the 12 varietal combinations.

  • Fig. 4.

    Area under the disease progress curve (AUDPC) of the 12 combinations (intervarietal grafts and their controls). AUDPC based on disease severity from 1 to 24 d after inoculation with Phytophthora capsici (DAI) (A–C); AUDPC based on disease incidence from 1 to 84 DAI (D–F).

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