Genetic control of the fungus Colletotrichum lindemuthianum (Sacc. & Magn.) Scrib. reaction and corona color in the common bean (Phaseolus vulgaris L.)

Genetic control of the fungus Colletotrichum lindemuthianum (Sacc. & Magn.) Scrib. reaction and corona color in the common bean (Phaseolus vulgaris L.)

H.A. de Mendonça, J.B. dos Santos, M.A.P. Ramalho and D.F. Ferreira

Departamento de Biologia, Universidade Federal de Lavras, Caixa Postal 37, 37200-000 Lavras, MG, Brasil. Send correspondence to J.B.S.

ABSTRACT

An important trait for common bean (Phaseolus vulgaris L.) cultivars with Carioca type grain is resistance to Colletotrichum lindemuthianum, which causes anthracnose and a pale corona. The present study was conducted to understand the genetic control of common bean reaction to the fungus and of the corona color, to provide guides to future breeding studies. Genotypes P-45, with brown corona, and EMGOPA 201-Ouro, with yellow corona, are resistant to C. lindemuthianum. Cultivar Carioca is susceptible to anthracnose, but it has desirable grain and corona color. Anthracnose resistance and corona color were studied in the F₁ and F₂ generations of three populations resulting from crosses of P-45, EMGOPA 201-Ouro, and Carioca. The Carioca x P-45 cross indicated that the Mex.2 allele, which conditions resistance to the pathogen, is linked with a recombination frequency of 0.0604 ± 0.0232 to one of the alleles which determines the dark brown corona color. The EMGOPA 201-Ouro x Carioca cross revealed that the resistance allele of EMGOPA 201-Ouro was independent from the alleles which determine the yellow corona. These resistance alleles were also determined to be independent according to EMGOPA 201-Ouro x P-45 cross results.

INTRODUCTION

Reaction to pathogens, yield and other consumption-oriented traits should be considered when developing new common bean cultivars. In the case of pathogen resistance, one of the most important is Colletotrichum lindemuthianum (Sacc. & Magn.) Scrib, which causes anthracnose. Since producers generally do not use only healthy seeds, the adoption of resistant cultivars is the most efficient method to control anthracnose. Sources of resistance to anthracnose, however, are not adapted to our conditions and are carriers of undesirable phenotypes. For example, some lines derived from the TO cultivar had the Mex. 2 resistance allele, but also had a dark brown corona, which is an undesirable color (Resende, 1989). Thus, the hypothesis that the alleles which control corona color may be linked to those responsible for C. lindemuthianum resistance was proposed.

This study was conducted to analyze the linkage relationship between the Mex. 2 allele, which provides resistance to C. lindemuthianum, and the allele that conditions the dark brown corona. A second objective was to identify the genetic control of the resistance of cultivar EMGOPA 201-Ouro to anthracnose and to determine if this resistance allele is linked to the alleles which control yellow corona color.

MATERIAL AND METHODS

The crosses were conducted in greenhouses in the Biology Department at the Federal University of Lavras (UFLA) to obtain segregant populations and their assessment.

Carioca 300V, EMGOPA 201-Ouro cultivars, and the P-45 line were used to generate the segregant populations. The Carioca cultivar has cream colored seeds with dark brown stripes, a colorless corona, and is susceptible to C. lindemuthianum. The EMGOPA 201-Ouro cultivar originated from the PI 207262 line (Beebe and Pastor-Corrales, 1991), has small yellow seeds, yellow corona, and is resistant to the kapa, delta, iota, and alfa-brazil races (Hubbeling, 1977), as well as the alfa, delta, epsilon, eta, theta, kapa, lambda and mu races (Menezes, 1985) of C. lindemuthianum. The P-45 line was obtained from the TO x ESAL 501 cross, has cream colored seeds with dark brown stripes, a dark brown corona, and is resistant to C. lindemuthianum. P-45 carries the Mex.2 allele, which gives resistance to alfa, beta, delta, gama, capa, mu, eta, Mexican I, Brazilian I, lambda and alfa-brazil races of C. lindemuthianum (Fouilloux, 1976; Vieira, 1983, Rava and Sartorato, 1994).

F₁ generations from the following crosses were obtained: Carioca 300V x EMGOPA 201-Ouro, Carioca 300V x P-45, and EMGOPA 201-Ouro x P-45. The crosses were produced using a methodology similar to that presented by Ramalho et al. (1993). F₁ seeds from each cross were sown to generate F₂ seeds. F₂ generation corona color was only expressed in the seeds produced by F₂ plants, because of maternal effect of the trait and the reaction to C. lindemuthianum expressed in young F₂ plants. It was, therefore, necessary to assess the reaction of the F2 plant to the pathogen by their respective F₃ families, since after inoculation the susceptible F₂ plants would be eliminated before seed production. Thus, each F₂ plant was harvested individually, resulting in 89 families from the Carioca 300V x EMGOPA 201-Ouro cross, 184 families from the Carioca 300V x P-45 cross, and 62 families from the EMGOPA 201-Ouro x P-45 cross.

Seed corona color from each family was recorded and the 335 families were assessed for C. lindemuthianum resistance. For this assessment, 12 seeds from each family were sown in plastic trays containing sterilized soil. Seven days after emergence, the plants were inoculated with the physiologic race 89, by spraying with a suspension containing 1.2 x 10⁶ conidia/ml. After inoculation, the trays were covered with plastic bags to form a damp environment and placed in a refrigerated chamber at a temperature of approximately 20^oC, alternating 12 h of light and 12 h of darkness for 72 h.

Seven days after inoculation, the reaction of each family to C. lindemuthianum was recorded. There were three types of reactions: a) family with 100% resistant plants, considered to come from an F₂ plant homozygous for resistance; b) segregant family, considered to come from a heterozygous F₂ plant; c) family with 100% susceptible plants, considered to come from an F₂ plant homozygous for susceptibility. The scale of marks described by Rava et al. (1993) was used to assess the symptoms, where seedlings with degrees from 1 to 3 were considered resistant and those with degrees from 4 to 9 were considered susceptible. Identification of the 89 race (the alfa group) of the pathogen was previously made, using the binary system proposed by Habgood (1970) and the differential plants recommended by the International Center for Tropical Agriculture - CIAT (1990).

Phenotypic proportions observed in the F₂ generations were compared with those expected by the chi-square test (c²), as described by Steel and Torrie (1980), to assess reaction to C. lindemuthianum, corona color and the two traits simultaneously.

The recombination frequency (r) among the linked genes (F₁ plant gametes used to form the F₂ generation) was estimated using a non-linear least squares iterative process, following the genetic model:

where x_i, with i = 1, 2,..., 6, represents a dummy variable, assuming the values of 0 or 1. If a certain individual belongs to the i phenotypic class, the value of x_i corresponds to 1, if not the value of x_i is 0, and f_i, with i = 1, 2, ..., 6, represents the expected frequency of the F₂ generation.

The solution of the non-linear genetic model was obtained by the modified Gauss-Newton method (Gallant, 1987) and used the first partial "derivative" for the r parameter. An estimate of the recombination frequency among the alleles was obtained using PROC NLIN (SAS, 1990). Adjustment of the model was assessed by the determination coefficient (R²), which is provided by the following expression:

where error SS and corrected total SS were obtained from the ANAVA regression for non-linear models (SAS, 1990).

RESULTS AND DISCUSSION

Normally assessment of segregant populations from crosses of resistant versus susceptible parents for pathogen reaction is conducted in the F₂ generation. However, in this study assessments were made in F₃ families derived from F₂ plants. Consequently, it was possible to assess not only the reaction to C. lindemuthianum, but also corona color of the bean seed. This is because the corona has a maternal effect, that is, for this trait the maternal phenotype is expressed in the seeds of the F₁ generation, the F₂ phenotype in the seeds of the F₁ generations, and so on successively. If assessments for C. lindemuthianum reaction were determined in F₂ generation plants, it would not be possible to assess corona color simultaneously, because seedlings susceptible to C. lindemuthianum would die before producing seeds. Thus, in the seeds of each F₃ family corona color (due to the genotype of the parental F₂ plant) and reaction to the pathogen were assessed. This procedure provided information on the two traits, and allowed rigorous evaluation of plant reactions to C. lindemuthianum, considering that the phenotype of the F₂ plant was established from the reaction of its derived F₃ family containing 12 plants.

Genetic control of corona color

The large number of genes involved and color tone variation make seed coat color assessment difficult in beans. Comparison among results reported in the literature is hindered, since the same color tone may be described as different colors when reported by different authors.

The same difficulties are present for corona color evaluation, although the number of genes involved in the control of this trait is smaller. The phenotypic segregation of corona color observed in the F₂ generation of the crosses P-45 x EMGOPA 201-Ouro, P-45 x Carioca 300V, and Carioca 300V x EMGOPA 201-Ouro are listed in Table I. Analyses of the F₂ generation of these three crosses indicated the presence of at least two genes that segregate for corona color. In the cross P-45 x EMGOPA 201-Ouro, the segregation observed in the F₂ generation adjusted to the expected segregation of 13 yellows:3 dark browns, indicating the existence of two independently distributed genes segregating for the corona color, and the presence of interaction among the dominant and recessive genes (Ramalho et al., 1990). The P-45 x Carioca 300V cross showed the following corona color segregation in the F₂ generation, 12 dark browns:3 yellows:1 colorless, also indicating the segregation of two independent genes for corona color, and the presence of gene interaction of the dominant epistatic type (Ramalho et al., 1990). Segregation of the F₂ generation from the Carioca 300V x EMGOPA 201-Ouro cross was 15 yellows:1 colorless, also indicating two genes with independent distribution and duplicate effects (Ramalho et al., 1990).

According to Vieira (1967) and Yarnell (1965), the genes responsible for different seed coat color are the same genes for partial coloring. The Cor genes determine dark corona color in a CorCor genotype, pale colors in the Corcor genotype, and absence of color in the corcor genotype. Our results, however, indicate that the Cor gene must be present for corona color expression, but it is not responsible for color formation, which is determined by complementary or seed coat coloring genes, such as C, J, D, B, G, and V (Basset, 1996).

Thus, it may be inferred that besides the Cor gene, which is necessary for color to be shown, there are three additional genes responsible for the presence of color in the corona, named here B, D and G genes. Individuals of --D-Cor-gg genotypes have a dark brown corona. Individuals with B-ddCor-gg and ---Cor-G- have a yellow corona. Individuals with bbddCor-gg do not have a colored corona.

Basset (1995), however, disagrees that the Cor allele conditions corona color or that it is responsible for color in the corona. In a study conducted by that author, crosses among offspring with dark corona and pink flowers versus offspring with white flowers and colorless corona were made, and only two phenotypes were observed in the descendants: pink flowers and dark corona, and white flowers and colorless corona. Thus, Basset (1995) suggested that the dark corona phenotype was due to pleiotropic effects of the v^lae alleles, which conditions pink flowers. Consequently, plants with pink flowers always have a dark corona and plants with white flowers always have colorless corona. Another explanation is a close linkage among the genes which determine dark corona and pink flowers and the absence of recombinants. Observations made by the author suggest that the pleiotropic hypothesis is more likely. However, when conducting the present study it was observed that both TO line and the descendent P-45 line have dark brown corona and white flowers, contradicting Basset's (1995) hypothesis that the dark corona is a pleiotropic effect of the v^lae allele.

Based on the corona color phenotypes obtained from the F₁ and F₂ generations of the crosses P-45 x EMGOPA 201-Ouro, P-45 x Carioca 300V and Carioca 300V x EMGOPA 201-Ouro, the proposed parental genotypes are BBDDCorCorgg for P-45 (dark brown corona), BBddCorCorGG for EMGOPA 201-Ouro (yellow corona), and bbddCorCorgg for Carioca 300V (colorless corona).

Genetic control of reaction to C. lindemuthianum

All plants from the F₁ generation of the three crosses were resistant (Table II), but the level of resistance of F₂ generation plants varied according to the cross. In the cross of P-45 x EMGOPA 201-Ouro, the observed proportion adjusted to the expected 15 resistant:1 susceptible (Table II). This segregation occurs when two genes with independent distribution are involved. The dominant allele of either of the genes, alone or together, contributes to resistance. This segregation is characteristic of genes with duplicate effects (Ramalho et al., 1990).

When the crosses P-45 x Carioca and Carioca x EMGOPA 201-Ouro were examined, the segregation observed in the F₂ generation adjusted to the proportion of 3 resistant:1 susceptible (Table II). It is inferred, in these crosses, that the trait is controlled by only one dominant gene for resistance. P-45, therefore, is likely to have a resistance allele for C. lindemuthianum different from that present in EMGOPA 201-Ouro. This explains the 15 resistant:1 susceptible segregation in this cross and of 3 resistant:1 susceptible in the others.

There are several literature reports on genetic control of C. lindemuthianum resistance in common bean. Some of these studies mention the occurrence of a single dominant gene expressing resistance (Burkholder, 1918; Mastenbroek, 1960; Bannerot (1969) quoted by Fouilloux, 1979; Fouilloux, 1976; Fukuda, 1982). In other cases, the use of different parents, such as the case of the P-45 x EMGOPA 201-Ouro cross, led to the conclusion that more genes were involved (Schreiber, 1932; Cárdenas et al., 1964; Muhalet et al., 1981; Vidigal, 1994; Pastor-Corrales et al., 1994).

Menezes (1985) concluded that the PI 207262 and TO lines are similar because they had the same resistance and susceptibility reactions when they were inoculated with nine physiologic races of C. lindemuthianum. Studying the inheritance of resistance to the alfa race, Vidigal (1994) proposed that the Q and Mex.2 genes were responsible for resistance in PI 207262. Because EMGOPA 201-Ouro cultivar originated from PI 207262, it is expected that this cultivar also has the Mex.2 resistance allele. However, the results obtained in the present study do not agree with the presence of the Mex.2 gene in the two parents, P-45 and EMGOPA 201-Ouro, because the observed segregation led us to infer that they have different genes. Menezes (1985) observed that the PI 207262 and TO lines have similar genotypes for C. lindemuthianum resistance because the lines, in spite of having different genes, are resistant to the same fungus races. This would contradict the results obtained in this study. A fact which reinforces this observation is that PI 207262 and TO are recommended by CIAT (1990) as differential cultivars to determine the C. lindemuthianum races. According to Rava et al. (1994), the allele present in PI 207262 confers resistance to several races, including races 339 and 343, which overcomes the resistance given by the Mex.2 allele present in the TO line. Consequently, the EMGOPA 201-Ouro cultivar has only the Q resistance allele.

Genetic control of reaction to C. lindemuthianum and corona color

The observed F₂ segregation of the P-45 x EMGOPA 201-Ouro, P-45 x Carioca, and Carioca x EMGOPA 201-Ouro crosses for resistance to C. lindemuthianum and corona color, taken simultaneously, are shown in Table III. For the Carioca x EMGOPA 201-Ouro cross, the observed segregation in the F₂ generation fits the proportion, 45 resistant yellow:15 susceptible yellow:3 colorless resistant:1 colorless susceptible. Therefore, it is inferred that the genes which determine corona color and reaction to the pathogen are independently distributed. EMGOPA 201-Ouro resistance to C. lindemuthianum allele is independent of the alleles which determine the yellow corona color. Therefore, the expected phenotypic proportion in F₂ (Table III) could be obtained from the product of the expected proportions for corona color (Table I) and reaction to C. lindemuthianum (Table II), that is, (15 yellow:1 colorless) (3 resistant:1 susceptible) = 45 resistant yellow:15 susceptible yellow:3 colorless resistant:1 colorless susceptible.

In the P-45 x EMGOPA 201-Ouro cross, the observed proportion fit the expected proportion, 195 resistant yellow:13 susceptible yellow:45 resistant dark brown [(13 yellow:3 dark brown) (15 resistant:1 susceptible)]. In this cross it may also be inferred that the genes which determine corona color and reaction to the pathogen are independently distributed.

In the P-45 x Carioca cross, the observed proportion did not fit the expected proportion of 9 resistant yellow:3 susceptible yellow:36 resistant dark brown:12 susceptible dark brown:3 resistant colorless:1 susceptible colorless [(3 yellow:12 dark brown:1 colorless) (3 resistant:1 susceptible)]. This indicates that at least one of the genes responsible for color determination is linked to the gene for reaction to C. lindemuthianum in the P-45 parent. It seems that the allele responsible for resistance to C. lindemuthianum present in the P-45 is the Mex.2, and the allele which determines the dark brown color of P-45 is the D allele. Resistant lines, selected from the TO x ESAL 501 cross, are carriers of dark brown corona (Resende, 1989), and it is probable that the Mex.2 allele for resistance to C. lindemuthianum and the D allele for dark brown corona are linked.

Using an iterative process of the non-linear least squares procedure, the recombination frequency (r) among the Mex.2 and D alleles of the P-45 x Carioca 300V cross was estimated following the genetic model:

The solution of the non-linear genetic model was obtained by the modified Gauss-Newton method (Gallant, 1987) using the first partial "derivative" for the r parameter, resulting in the following equation:

Using the PROC NLIN (SAS, 1990) procedure, the recombination frequency among the Mex.2 and D alleles was estimated as 6.04 cM with 2.32 standard error. The determination coefficient was 99.5%, indicating a near perfect fit of the model to the phenotypic proportions observed in the F₂ generation. This confirmed the close linkage between the Mex.2 and D genes. The close linkage of the Mex.2 and D genes explains why all the resistant lines, selected from the TO x ESAL 501 cross, also have dark brown corona (Resende, 1989).

The confirmed linkage among the Mex.2 and D alleles makes breeding more difficult for those interested in using the Mex.2 allele to control C. lindemuthianum resistance, as the cultivars with dark brown corona are unacceptable on the Brazilian market. However, as seen in Table III, it is possibile to associate the resistance allele with the colorless corona, as recombinants with this phenotype occur in the F₂ generation.

Although the nonsignificant c² test for the P-45 x EMGOPA 201-Ouro cross indicates no linkage between the C. lindemuthianum resistance allele and the alleles which determine corona color, there is linkage between these alleles. The genotype of the parent P-45 is

and EMGOPA 201-Ouro is

There are recombinants in the descendants.

However, this linkage was not detected in this cross, probably due to the non-expression of the recombinant phenotypes because the effect of the Mex.2 allele is masked by the Q allele.

Basset (1996) suggests that the genes responsible for reaction to C. lindemuthianum receive a new classification, Co-1 to Co-7, according to the physiological races of C. lindemuthianum, which supersedes the one used in this study. Co-4 corresponds to Mex.2 discovered by Bannerot (1969), quoted by Fouilloux (1979).

RESUMO

As cultivares de feijão com grão tipo Carioca devem possuir, entre outros caracteres, resistência ao Colletotrichum lindemuthianum, agente causal da antracnose, e possuir halo de cor clara. Assim, o objetivo do presente estudo foi conhecer o controle genético desses dois caracteres, visando orientar os futuros trabalhos de melhoramento. Os genitores utilizados foram P-45, EMGOPA 201-Ouro e Carioca-300V, sendo que o P-45 possui halo marrom escuro e o EMGOPA 201-Ouro, halo amarelo, ambos resistentes ao Colletotrichum lindemuthianum. O genitor Carioca-300V é suscetível, porém possui cor de grão e de halo desejáveis. Do intercruzamento desses genitores obtiveram-se três populações que foram avaliadas nas gerações F₁ e F₂ para os dois caracteres. O cruzamento Carioca-300V x P-45 indicou que o alelo Mex.2, que condiciona resistência ao patógeno, está ligado a um dos alelos que determinam a cor marrom escura do halo com uma freqüência de recombinação de 0,0604 ± 0,0232. Do cruzamento EMGOPA 201-Ouro x Carioca-300V, verificou-se que o alelo de resistência do EMGOPA 201-Ouro é independente dos alelos que determinam halo amarelo e também independente do alelo de resistência Mex.2, de acordo com o cruzamento EMGOPA 201-Ouro x P-45.

(Received July 23, 1997)

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Publication Dates

• Publication in this collection
  23 Feb 1999
• Date of issue
  Sept 1998

History

• Received
  23 July 1997