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Chilean journal of agricultural research

On-line version ISSN 0718-5839

Chilean J. Agric. Res. vol.73 no.4 Chillán Dec. 2013

http://dx.doi.org/10.4067/S0718-58392013000400001 

RESEARCH

Morphological characterization of Capsicum annuum L. accessions from southern Mexico and their response to the Bemisia tabaci-Begomovirus complex

 

Horacio Ballina-Gómez1, Luis Latournerie-Moreno1, Esaú Ruíz-Sánchez1*, Alfonso Pérez-Gutiérrez1, and Gabriel Rosado-Lugo1

1Instituto Tecnológico de Conkal, División de Estudios de Posgrado e Investigación, km 16.3, antigua carretera Merida-Motul, C.P 97345, Conkal, Yucatan, Mexico. *Corresponding author (esau_ruiz@hotmail.com).


The high diversity of chili pepper (Capsicum annuum L.) in Mexico offers an excellent alternative to search for wild and semi-domesticated genotypes as sources of resistance to the complex Bemisia tabaci (Genn.) (Hemiptera: Aleyrodidae)-Begomovirus, which has caused enormous losses in commercial production of various horticultural crops. The goal of the present work was to characterize ex situ 18 genotypes of C. annuum from southern Mexico through 47 morphological descriptors, and to evaluate its response to the B. tabaci-Begomovirus complex. Morphological characterization showed the variables calyx annular constriction (CAC), number of branch bifurcation (NBB), and calyx pigmentation (CP) had the highest variation. Principal components analysis (PCA) of 47 morphological characteristics showed that 12 components were selected as meaningful factors. These components explained 94% of the variation. Cluster analysis showed three major clusters and seven sub-clusters. On the other hand, evaluation of the response to B. tabaci-Begomovirus showed that the genotypes have differential susceptibility to this vector-pathogen complex. Genotypes 'Chawa', 'Blanco', 'Maax' and 'X'catic' were into the low susceptibility to B. tabaci and low severity of viral symptoms. Surprisingly, the genotype 'Simojovel' showed high susceptibility to whitefly, but was grouped into genotypes with low symptom severity. This study shows the potential of native germplasm of pepper to explore sources of resistance to the B. tabaci-Begomovirus complex.

Key words: Plant resistance, semi-cultivated peppers, whitefly.


INTRODUCTION

Chili pepper (Capsicum annuum L.) is a widely cultivated species that has been used since ancient times as food flavoring and for human health (Milla, 2006). Mexico, as center of domestication and genetic diversity of C. annuum, has the cultivated species C. annuum L. var. annuum and the wild C. annuum L. var. glabriusculum (Dunal) Heiser & Pickersgill (Loaiza-Figueroa et al., 1989). In southern Mexico chili pepper is cultivated in backyard gardens as well as in extensive areas as highly managed crop in Southern Mexico (Pérez-Casteñeda et al., 2008). The first attempts to characterize the pepper germplasm in Southern Mexico showed a great genetic diversity of three species: Capsicum frutescens L., C. annuum, and C. chinense Jacq. (Castañón-Nájera et al., 2008; Pérez-Casteñeda et al., 2008; Prado, 2008).

Commercial production of C. annuum faces various constraints, particularly those related to phytophagous insects. In this context, the whitefly Bemisia tabaci (Genn.) (Hemiptera: Aleyrodidae) is the most dangerous pest in tropical and neotropical regions (Brown and Bird, 1992). Bemisia tabaci induces losses in pepper crops by direct feeding and transmission of a wide variety of Begomoviruses (Oliveira et al., 2001). Management of the complex B. tabaci-Begomovirus has been typically carried out by chemical insecticides to control vector populations. This action has selected B. tabaci populations with high level of resistance (Elbert and Nauen, 2000). To cope with the potential risk associated to the use of chemical insecticides, host plant resistance to insects is an effective, economical, and environmentally friendly method for pest control. This alternative uses wild and semi-domesticated relatives of cultivated species as sources of pest resistance genes and in turn as an effective tool to minimize losses due to phytophagous insects or vector-borne virus diseases (Sharma and Ortiz, 2002).

Studies of plant resistance to the vector B. tabaci have found that this phytophagous is affected mainly by the external/physical characteristics of the leaf surface, such as hairiness, glandular trichomes, leaf shape and cuticle thickness (Berlinger, 1986; Boiça et al., 2007; Oriani and Vendramim, 2010; Oriani et al., 2011). Resistance to B. tabaci and its relation to plant morphological traits has been well documented in other crops, such as tomato, cotton, and cassava (Bellotti and Arias, 2001; Boiça et al., 2007; Oriani and Vendramim, 2010). Physical barriers, such as the cuticle thickness of leaf may prevent the insect stylet from reaching the phloem (Janssen et al., 1989), while the presence of high density of glandular trichomes may cause high mortality of whitefly as compounds act as a glued trap for adult whiteflies, in addition, the acylsugars produced by such trichomes deters settling and probing of B. tabaci (Heinz and Zalom, 1995; Liedl et al., 1995; Roónguez-López et al., 2012). The internal characteristics of the leaves, such as chemical composition of leaf sap, nutritional value of leaves, and activity of plant defense-related enzymes has been also implicated but less studied in host resistance to B. tabaci. Particularly, the increased activity of plant defense-related enzymes can induce synthesis of toxic metabolites in leaves, which in turn can affect negatively the survivorship, growth and reproduction of herbivore insects (Bowles, 1990; McKenzie et al., 2002).

In field, severe population outbreaks of B. tabaci are usually accompanied by a high incidence of Begomovirus. This group of viruses is exclusively transmitted by B. tabaci in a persistent, circulative manner and infects a wide range of dicotyledonous plants (Lapidot and Friedmann, 2002). Studies on host plant resistance to Begomovirus have been carried out in various crops, such as tomato, bean, and cassava. The outcomes of such studies have been difficult to widely adopt due to the variation in occurrence of virus strains in certain geographic areas (Borah and Dasgupta, 2012).

The exploration of wild and semi-cultivated land-race genotypes of chili peppers offers an excellent opportunity to identify possible sources of resistance to the B. tabaci-Begomovirus complex. Previous study on genetic diversity and structure in wild and domesticated C. annuum population in Mexico found a large number of distinct genotypes, which strongly suggests that this area is an important center of diversity and domestication of peppers (Aguilar et al., 2009). As part of a long-term project to potentiate the local germplasm of C. annuum, the present study was carried out to characterize the morphological diversity of C. annuum from southern Mexico (Chiapas, Tabasco, and the Yucatan Peninsula) and to evaluate the response of such genotypes to the B. tabaci-Begomovirus complex.

MATERIAL AND METHODS

Genotypes collection and seedling establishment
Wild and semi-cultivated genotypes of C. annuum were collected in home gardens and rural markets in the states of Tabasco, Chiapas, and Yucatan (Table 1). Two commercial genotypes ('Jalapeno' and 'Pimiento') were also included in the collection as standard controls for susceptibility to the B. tabaci-Begomovirus complex. To homogenize germination, seeds obtained from dried fruits were immersed in 250 mL water containing 250 mg L-1 gibberellic acid (Plant Health Care, Mexico DF., Mexico) for 48 h. Seeds were kept in constant oxygenation using an aquarium air pump (Hagen Elite 803, Montreal, Quebec, Canada). Seeds were sown in polystyrene trays using Cosmopeat® (Cosmocel, Canada) as substrate. Seedling was maintained with 60% of moisture in the substrate and fertilized twice a week with 2 g L-1 of Triple 17® (FLUGSA, Mexico DF., Mexico) dissolved in the irrigation water.


Table 1. Origin of Capsicum annuum genotypes evaluated in this study.

Establishment of pepper genotypes in field
The experiment was carried out at the Instituto Tecnológico de Conkal, located in Conkal (21°06' N, 89°31' W, 10 m a.s.l.), Yucatan, Mexico. Koppen climate classification is AWo"(X'),(i') g, tropical wet and dry, the average annual high temperatures range from 28 to 36 °C, and the low temperatures range between 18 to 23 °C. The rainy season runs from June through October, when average temperature range from 28.5 to 26.8 °C. The year rainfall is in average 1036.9 mm. The soil type is litosol/ rendzina, usually stony, highly alkaline, and with low content of organic matter (Cabadas et al., 2010).

The pepper plantation was established in a randomized block design with three replicates. Forty-day-old seedlings of all genotypes were individually transplanted in small plots (4 m x 2 m) that contained 16 plants. Plants were fertilized with the formula 250-200-150, supplied in the dripping irrigation system. No application of insecticide was carried out to allow successful infestation of B. tabaci.

Morphological characterization of pepper genotypes
Morphological characteristics were taken from Capsicum descriptors documented by IPGRI, AVRDC and CATIE (1995). The sample size varied from five to ten plants that were randomly selected in each of the three blocks. For leaf, flower and fruit traits, three to ten samples were taken per selected plant. Forty seven morphological characteristics were measured; 17 for plant: Plant height (PH, cm), number of branch bifurcation (NBB), stem shape (SS), stem pubescence (SP), plant growth habit (PGH), plant canopy width (PCW, cm), stem length (SL, cm), stem diameter (SD, cm), branching habit (BH), tillering (T), leaf density (LD), leaf color (LC), leaf shape (LS), lamina margin (LM), leaf pubescence (LP), mature leaf length (MLL, cm), and mature leaf width (MLW, cm); 14 for flower: Days to flowering (DF), number of flowers per axil (NFA), flower position (FP), corolla color (CC), corolla shape (CS), anther color (AC), filament color (FC), calyx pigmentation (CP), calyx margin (CM), calyx annular constriction (CAC), corolla length (CL, cm), anther length (AL, mm), filament length (FiL, mm), and pistil length (PiL, mm); and 16 for fruits: Fruit length (FL, cm), pedicel length (PeL, cm), fruit color at intermediate stage (FCIS), fruit shape (FS), fruit shape at pedicel attachment (FSPA), fruit shape at blossom end (FSBE), neck at base of fruit (NBF), fruit blossom end appendage (FBEA), type of fruit surface (TFS), number of locules (NL), fruit diameter (FD, cm), fruit wall (FW), placenta length (PL, cm), pedicel with fruit (PF), pedicel with stem (PS), and fruit cross-sectional corrugation (FCSC).

Evaluation of whitefly population in pepper leaves
Population densities of whitefly adults, eggs and nymphs (first to fourth instar) in pepper leaves were evaluated in five sampling times. Sampling time 1 was carried out 30 d after transplant and the four subsequent samples were taken at 15 d intervals. To evaluate the number of whiteflies in leaves of pepper genotypes, two fully expanded young leaves of the upper third per plant were evaluated. Number of adults in the leaves was directly counted in the field by carefully observing abaxial side of selected leaves. Leaves then were detached and taken to the laboratory, where they were individually observed, and eggs and nymphs were counted in a stereomicroscope (BME L13395H11, Leica, Wetzlar, Germany). Leaf area was measured in a leaf area meter (LI-3100C, Li-Cor, Lincoln, Nebraska, USA). Results were expressed as number of nymphs per squared centimeter.

Evaluation of viral incidence and severity
Incidence and severity of viral symptoms were evaluated weekly. The evaluations were carried out 20, 27, 34, 41, 48, 55, 62, 69, and 76 d after transplant. For viral incidence, percent of plants with symptoms was determined based on the total number of plants in each plot replicate. For viral severity, a scale of five levels was modified from Anaya-López et al. (2003): Level 1, asymptomatic; level 2, slight crumpling and presence of yellow spots on apical leaves; level 3, groups of yellow spots coalesced forming a network on the base of apical leaves and protuberances observable in the middle zone of apical leaves; level 4, network clearly visible and slight leaf curling; level 5, severe yellowing/distortion of leaves.

Data analyses
The morphological characterization was analyzed with descriptive statistics. Principal Component Analysis (PCA) was carried out with the statistics mean and modes of each variable, which allow for the identification of the most important variables in the description of the observed variance of germplasm. Hierarchical Cluster Analysis (CA) was carried out with the most valued variables from the PCA. Cluster Analysis was determined by Unweighted Pair Group Method with Arithmetic Mean (UPGMA), where the differences among elements were calculated using the Euclidian Distance as a Similarity Metric. ANOVA and mean comparison for whitefly population and intensity of viral symptoms were performed by Scott-Knott test (Scott and Knott, 1974). Incidence and severity of viral symptoms were transformed to area under the disease progress curve as described by Campbell and Madden (1990). Comparisons of means were considered significantly different if P < 0.05. Prior to run, data in percent were transformed to y = arcsin(V(x/100)). The rate of apparent incidence and severity over time were estimated following the logistic model as the regression coefficient of the logit x on time in days (van der Plank, 1963). All data were analyzed in the statistical software InfoStat (Di Rienzo et al., 2008). The relationships among the 17 morphological characteristics of 18 pepper genotypes, and the complex B. tabaci (nymphs and adults abundance only)-Begomovirus (severity and incidence) was assessed using Redundancy Analysis (RDA; Legendre and Legendre, 1998), which was selected over Canonical Correspondence Analysis because of reduced length of gradient of our variables (Ter Braak and Smilauer, 2002). The length of gradients was calculated by detrended correspondence analysis (Hill, 1979). The significance of each indicator of severity and incidence, as well as the first axis, was tested within the forward selection procedure using a Monte Carlo random permutation test (499 permutation, P < 0.05). The analysis was performed using Canoco 4.5 (Ter Braak and Smilauer, 2002).

RESULTS AND DISCUSSION

Variation in morphologic characteristics of the pepper genotypes
All the C. annuum genotypes displayed variation for all the morphological characteristics evaluated in the present work (Table 2). Days to flowering (DF) and fruit color at intermediate stage (FCIS) were the variable with minor variation (coefficient of variation CV 8.07 and 13.17, respectively). In other studies, low variation in DF has been also observed. For example, Sharma et al. (2010) found 8.18% CV in DF in a collection of accessions of sweet pepper C. annuum. Although we observed low CV for FCIS, other studies have reported the opposite, like that of Sudre et al. (2010), who showed high CV in fruit color when assessing the morphological and agronomic characteristics of Capsicum species.

Table 2. Central tendency and dispersion values obtained with 47 morphological
characteristics in 18 Capsicum annuum genotypes from Southern Mexico.


On the other hand, the highest CV of our pepper collection were observed in calyx annular constriction (CAC), number of branch bifurcation (NBB) and calyx pigmentation (CP), which showed CV values of 576.9, 287.06, and 190.03, respectively (Table 2). Due to its wide variation, CAC has been established as a descriptor of great importance in pepper, even to distinguish among pepper species (Sudre et al., 2010). The high variation in CAC in our study supports the idea of a high intra-genotypes variation in C. annuum (Castañón-Nájera et al., 2008). Other authors have also documented various characteristics with high variation in C. annuum genotypes, for example, fruit yield per plant (Ukkund et al., 2007), number of fruits per plant (Sreelathakumary and Rajamony, 2002), and plant height (Ibrahim et al., 2001).

Principal components analysis of morphologic characteristics of pepper genotypes
Principal components analysis (PCA) was performed using 47 morphological characteristics. Twelve components were selected as meaningful factors with eigenvalues > 1. These components explained 94% of the variation. The first principal component (PC 1) explained 22% of total variation in original data, second component (PC 2) explained 15%, and third principal component (PC 3) explained 11% of variation. The other principal components (PC 4-PC 12) explained an additional 46% of the variation (a total 94% of explained variation, Table 3). The percentages of variance explained by the 12 components and the correlation between the PC and the original morphological characteristics of the pepper genotypes are shown in Table 3. The 94% total variability obtained in PCA indicated an adequate percentage of variation, as indicated by Pla (1986), who suggests at least an 80% total variability. Likewise, the number of PC formed indicates high variation in C. annuum genotypes as reported by Matthew et al. (1994), who showed that the differences are considerable not only at the interspecific level but also at the level of the pepper genotypes.

Table 3. Variance explained by twelve principal components derived from 47 morphological characteristics of Capsicum annuum genotypes, and the weights of the original variables in each component.

PH: plant height; NBB: number of branch bifurcation; SS: stem shape; SP: stem pubescence; PGH: plant growth habit; PCW: plant canopy width; SL: stem length; SD: stem diameter; BH: branching habit; T: tillering; LD: leaf density; LC: leaf color; LS: leaf shape; LM: lamina margin; LP: leaf pubescence; MLL: mature leaf length; MLW: mature leaf width; DF: days to flowering; NFA: number of flowers per axil; FP: flower position; CC: corolla color; CS: corolla shape; AC: anther color; FC: filament color; CP: calyx pigmentation; CM: calyx margin; CAC: calyx annular constriction; CL: corolla length; AL: anther length; FiL: filament length; PiL: pistil length. FL: fruit length; PeL: pedicel length; FCIS: fruit color at intermediate stage; FS: fruit shape; FSPA: fruit shape at pedicel attachment; FSBE: fruit shape at blossom end; NBF: neck at base of fruit; FBEA: fruit blossom end appendage; TFS: type of fruit surface; NL: number of locules; FD: fruit diameter; FW: fruit wall; PL: placenta length; PF: pedicel with fruit; PS: pedicel with stem; FCSC: fruit cross-sectional corrugation.


The PC 1 was contributed by positive loading of CL, FiL, PiL, FL, FD, FW, and PF, followed by negative and minor loading of T, LD, and FC. The PC 2 was strongly contributed by positive loading of MLL and MLW, followed by negative and minor loading of NBB, NFA, CS, FS, and FSBE. The PC 3 was contributed by positive loading for FCSC, followed by negative and minor loading of BH, AL and NBF (Table 3; Figure 1). As for the PC1, only FD, FCSC, and FL have been previously reported as important contributors to the main principal component in morphological characterization of C. annuum (Latournerie et al., 2002; Castañón-Nájera et al., 2008). Notably, fruit morphological characteristics were the principal contributors in this case, which is in agreement with the studies mentioned above. This is the result of the major variation in fruit shape of C. annuum complexes (Pardey et al., 2006; Moscone et al., 2007; Castañón-Nájera et al., 2010).

Figure 1. Biplot graph of 18 genotypes of Capsicum annuum based on 47 morphological traits. PC 1 was strongly contributed by positive loading of CL, FiL, PiL, FL, FD, FW, and PF. PC 2 was strongly contributed by positive loading of MLL and MLW. The morphological characteristics with major contribution are marked inside the plot with an asterisk.

PH: plant height; NBB: number of branch bifurcation; SS: stem shape; SP: stem pubescence; PGH: plant growth habit; PCW: plant canopy width; SL: stem length; SD: stem diameter; BH: branching habit; T: tillering; LD: leaf density; LC: leaf color; LS: leaf shape; LM: lamina margin; LP: leaf pubescence; MLL: mature leaf length; MLW: mature leaf width; DF: days to flowering; NFA: number of flowers per axil; FP: flower position; CC: corolla color; CS: corolla shape; AC: anther color; FC: filament color; CP: calyx pigmentation; CM: calyx margin; CAC: calyx annular constriction; CL: corolla length; AL: anther length; FiL: filament length; PiL: pistil length. FL: fruit length; PeL: pedicel length; FCIS: fruit color at intermediate stage; FS: fruit shape; FSPA: fruit shape at pedicel attachment; FSBE: fruit shape at blossom end; NBF: neck at base of fruit; FBEA: fruit blossom end appendage; TFS: type of fruit surface; NL: number of locules; FD: fruit diameter; FW: fruit wall; PL: placenta length; PF: pedicel with fruit; PS: pedicel with stem; FCSC: fruit cross-sectional corrugation.

Hierarchical clustering of pepper genotypes
In the hierarchical clustering analysis, three major clusters of pepper genotypes and seven sub-clusters were observed (Figure 2). The subgroup 1 included genotypes: 'Pijadegato', 'Chawa', 'Miraparriba', and 'Blanco' (Euclidean distance between 10 and 12.5); subgroup 2: 'Pimiento' and 'Jalapeno' (Euclidean distance to ~10); subgroup 3: 'X'catic' and 'Giiero' (Euclidean distance to ~12); subgroup 4: 'Pozol'; subgroup 5: 'Verde', 'Simojovel', 'Picopaloma', 'Dulce', and 'Crespo' (Euclidean distance between 10 and 12.5); group 6: 'Sucurre'; and group 7: 'Maax', 'Bolita', and 'Amaxito' (Euclidean distance between 10 and 12). The first major cluster included only subgroup 1. The second major cluster included groups 2 and 3, and the third major cluster included groups 4, 5, 6, and 7. The clustering showed a clear distinction between some pepper genotypes.

Figure 2. Cluster analysis of 18 genotypes of Capsicum annuum based on Euclidean distance using 47 plant, flower and fruit traits. Numbers 1 to 7 are subgroups formed inside each major cluster.

For example, commercial genotypes were noticeable in subgroup 2. These results match those found by Chavez and Castillo (1999) working with accessions of C. pubescens, and Castañón-Nájera et al. (2008) working with C. annuum genotypes. These authors found that commercial peppers have an oblique fruit position, in contrast to erect fruit position of wild peppers. Similarly, Hernández et al. (2006) showed the same pattern when separating wild from commercials genotypes. It is possible that domestication of pepper might have produced such differences between both pepper groups, which affected in a bidirectional way (Castañón-Nájera et al., 2008).

Response of peppers to the Bemisia tabaci-Begomovirus complex
Pepper genotypes showed distinct levels of susceptibility to B. tabaci. Adult population in leaves varied significantly among pepper genotypes at 45 and 60 d after transplant (dat); in both recording times the genotype "Simojovel" showed the highest number of adult in leaves (mean ± standard error SE: ranking 0.05 ± 0.2 to 0.06 ± 0.02). In the evaluation at 45 dat genotypes 'Bolita', 'Amaxito', 'Crespo', 'Maax' and 'Verde' showed also higher number of adults (ranking 0.04 ± 0.0 to 0.04 ± 0.01) in leaves than that by the rest of the genotypes (Table 4). Egg population of whitefly in leaves showed no difference among pepper genotypes (Table 5). Nymphal population in leaves varied significantly among pepper genotypes at 45, 60, and 75 dat, while no difference was observed at 30 and 90 dat (Table 6). In general, 'Chawa', 'Pimiento', 'Dulce', 'Blanco', 'Sucurre', 'Pijadegato', 'Maax', 'X'catic' and 'Verde' showed lower number of nymphs (ranking 0.00 ± 0.0 to 0.03 ± 0.02) on leaves when compared to the rest of the genotypes. In contrast, higher numbers of nymphs on leaves were observed in the genotypes 'Simojovel' and 'Crespo' (ranking 0.08 ± 0.02 to 0.12 ± 0.03).

Table 4. Mean (± SE) number of adults per cm2 of Bemisia tabaci in leaves of
Capsicum annuum at different days after transplant (dat).



Values are means ± standard error of adults/cm2 in leaves of Capsicum annuum genotypes.
Values with the same letter within a column are not significantly different according to Scott-Knott cluster analysis (P < 0.05).


Table 5. Mean (± SE) number eggs Bemisia tabaci cm-2 in leaves of
Capsicum annuum
at different days after transplant (dat).


Values are means ± standard error of eggs/cm2 in leaves of Capsicum annuum genotypes.
Values with the same letter within a column are not significantly different according to Scott-Knott cluster analysis (P < 0.05).


Table 6. Mean (± SE) number Bemisia tabaci nymphs cm-2 in
leaves of Capsicum annuum at different days after transplant (dat).



Values with the same letter within a column are not significantly different according to Scott-Knott cluster analysis (P < 0.05).

The intensity of the viral symptoms was evaluated by recording the incidence and severity of plant symptoms. Interestingly, no difference (Scott-Knott P > 0.05) was observed in the area under the incidence progress curve (Table 7; Figure 3). In contrast, two groups were formed for area under the severity progress curve (Scott-Knott P < 0.05), where the low severity group was formed by 'Dulce', 'Verde', 'X'catic', 'Chawa', 'Blanco', 'Amaxito', 'Miraparriba', 'Maax', and 'Simojovel' (ranking 7.75 ± 4.51 to 84.62 ± 16.64). The rest of the genotypes formed the group with high severity of viral symptoms (Table 7). The latter genotypes showed values (mean ± SE) that ranged from 97.87 ± 10.24 to 131.87 ± 10.16 for area under the severity progress curve.

Table 7. Incidence and severity of viral symptoms in the genotypes of Capsicum annuum.

Values are means ± standard error of incidence and severity of virus symptoms in Capsicum annuum genotypes. Area under the curve was calculated as indicated in material and methods.
Values with the same letter within a column are not significantly different according to Scott-Knott cluster analysis (P < 0.05).


Figure 3. Progress of the viral incidence (%) in 18 pepper genotypes from Southern Mexico.



Possible relationships among morphological characteristics of the genotypes and susceptibility to B. tabaci-Begomovirus complex were analyzed. The RDA triplot showed a reduced separation of the pepper genotypes on the axes, and Monte Carlo permutation test was not significant for the first axis (Table 8). However, axis 1 was closely related to severity (r = 0.86). Severity was, indeed, the only variable with marginal effects in the model (F ratio = 3.27, P = 0.06), where a strong negative relationships among disease severity and various morphological characteristics were observed; among these were stem diameter (SD), leaf density (LD), leaf shape (LS), number of branch bifurcation (NBB), tillering (T) and plant canopy width (PCW). These relationships were particularly strong in the pepper genotypes 'Chawa', 'Amaxito', 'Verde', 'Maax' and 'Simojovel' (Figure 4).


Table 8. Eigenvalues and Monte Carlo results for Redundancy Analysis (RDA) of pepper genotypes in the complex Bemisia tabaci-Begomovirus.


Test of significance of first canonical axis: F ratio = 3.95 P value = 0.31

Figure 4. Redundancy Analysis (RDA) scatterplot illustrating the relationship between 17 morphological characteristics of 18 pepper genotypes with four variables of complex Bemisia tabaci (nymphs and adults abundance)-Begomov£rus (severity and incidence). Dots represent pepper genotypes. Bold arrows Nymphs, Adults, Severity and Incidence refer to complex B. tabaci-Begomovirus. Thin arrows refer to 17 morphological characteristics of pepper genotypes.

Resistance to either B. tabaci or Begomovirus has been previously studied in various groups of horticultural crops, such as tomato, pepper, bean, cotton, soybean, and cassava. In horticultural crops, enormous losses caused by this biotic constraint have been widely recognized (Berlinger, 1986; Lapidot and Friedmann, 2002; Morales, 2011; Borah and Dasgupta, 2012). Literature available have documented that in pepper, host resistance to B. tabaci is mainly mediated by morphological traits of plants, such as leaf trichomes and leaf thickness (Firdaus et al., 2011). On the other hand, Begomovirus resistance has been suggested to be due to constraints in viral movement, which in turn leads to no symptoms, delayed symptoms, and symptom remission (Anaya-López et al., 2003). For the best of our knowledge, no studies have been carried out on pepper resistance to both B. tabaci and Begomovirus. This type of studies might have bigger significance as in field B. tabaci-Begomovirus complex occurs concomitantly. In the present work, we observed that B. tabaci was able to colonize all genotypes. Moreover, viral symptoms appeared in all genotypes as well. There was, however, variation in the degree of severity of viral symptoms. In general, genotypes 'Chawa', 'Blanco', and 'X'catic' were grouped into the genotypes that showed low adult and nymphal population in leaves and low severity of viral symptoms. Surprisingly, the genotype 'Simojovel' showed high susceptibility to whitefly, but was grouped into genotypes with low symptom severity. A plausible explanation in this case would be that while the morphological or biochemical traits of the plant would favor the colonization of B. tabaci, viral infection would not succeed in such genotype due to resistance to Begomovirus infection. In practical terms, farmers would tend to prefer genotypes that are not susceptible to Geminivirus infection compared to those that show only resistant to B. tabaci.

CONCLUSIONS

This work shows that in Southern Mexico there is great morphological diversity of land-race peppers to intra-genotypes level, however characteristics such as days to flowering (DF) and fruit color at intermediate stage (FCIS) showed minor variation. Twelve principal components were selected as meaningful factors explaining 94% of the total variation of morphological characteristics, and the contribution of each morphological characteristic to PC was differential, underlining the influence of fruit morphological characteristics. Among morphological characteristics of the genotypes, only "Tillering" and "Plant Canopy Width" showed strong negative relationship with disease severity, while no relationship was observed for disease incidence and density of B. tabaci population. Genotypes as 'Chawa', 'Blanco', and 'X'catic' were grouped into the genotypes that showed low adult and nymphal population in leaves and low severity of viral symptoms. Notably, genotype 'Simojovel' showed high susceptibility to whitefly, but was grouped into genotypes with low symptom severity. This data highlight the potential of native pepper germplasm to explore sources of resistance to this pest complex. In a long-term scenario, resistance to the B. tabaci-Begomovirus complex might be used in breeding programs related to pest management.

ACKNOWLEDGEMENTS

This work was supported by ProIFOPEP 2012, a program administrated by the general direction of technical higher education (DGEST, Mexico). Authors thank Julio Monforte, Eder Poot, Nancy Pech, and Luis Hernández for their assistance in the development of this experiment.

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Received: 6 February 2013.
Accepted: 2 September 2013.

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