Co-evolution model of Colletotrichum lindemuthianum (melanconiaceae, melanconiales) races that occur in some Brazilian regions

Short Communication

Co-evolution model of Colletotrichum lindemuthianum (melanconiaceae, melanconiales) races that occur in some Brazilian regions

Ana Lilia Alzate-Marin¹, Everaldo Gonçalves de Barros^1,2 and Maurílio Alves Moreira^1,3

¹Núcleo de Biotecnologia Aplicada à Agropecuária (BIOAGRO), Universidade Federal de Viçosa (UFV), 36571-000 Viçosa, MG, Brasil. Send correspondence to A.L.A.M.

²Departamento de Biologia Geral, UFV, Viçosa, MG, Brasil.

³Departamento de Bioquímica e Biologia Molecular, UFV, Viçosa, MG, Brasil.

ABSTRACT

Colletotrichum lindemuthianum, the causal agent of anthracnose in the common bean (Phaseolus vulgaris L.), displays a high level of virulence diversity, which explains the large number of existing pathotypes. Several lines of evidence indicate that such diversity is, at least in part, due to plant and pathogen co-evolution. A co-evolution model based on the binary classification of 25 races identified in Brazil by inoculation of differential cultivars and random amplified polymorphic DNA (RAPD) data is proposed. In this model, races 8 and 64 that infected bean cultivar Cornell 49-242 (Are gene) and Mexico 222 (Mexico I gene) are considered to be sources of two important evolutionary routes. Inferences about undescribed races from Brazil could be made.

INTRODUCTION

In Brazil, Rava et al. (1994) identified 25 races of Colletotrichum lindemuthianum (Sacc. & Magn.) Scrib (Melanconiaceae, Melanconiales), the causal agent of anthracnose in the common bean (Phaseolus vulgaris L.), collected in different regions of Brazil. These races were identified and classified by inoculation of 12 differential cultivars (Pastor-Corrales, 1992).

Alzate-Marin et al. (1997) used random amplified polymorphic DNA (RAPD) analysis to evaluate the genetic diversity of 22 races of anthracnose fungus (Colletotrichum lindemuthianum). Three groups were defined based on these data. No correlation was found between RAPD classification and geographical distribution of the fungus or grouping defined by inoculation of the pathogens in differential cultivars. These results are similar to previous data in which C. lindemuthianum diversity was analyzed with isoenzymes and DNA markers (Figueredo et al., 1993; Fabre et al, 1995; Vilarinhos et al., 1995; Otoya et al., 1995). High diversity of Colletotrichum lindemuthianum virulence has been observed and correlation between pathogen and host diversity has been demonstrated (Pastor-Corrales et al., 1994).

In this work a co-evolution model is proposed, based on the classification of C. lindemuthianum races identified in Brazil, based on virulence to 12 differential cultivars of Phaseolus vulgaris (Rava et al., 1994) and RAPD data (Alzate-Marin et al., 1997).

MATERIAL AND METHODS

The races of C. lindemuthianum used in this work were previously characterized by Rava et al. (1994). The original cultures were provided by Dr. Carlos Rava (Embrapa/Arroz e Feijão, Goiânia, GO).

Three separate RAPD groups of C. lindemuthianum races were previously identified (Table I and Figure 1): RAPD group I (585, 72, 23, 73 and 79), RAPD group II (339, 343, 67, 64, 87, 95, 81, 65, 89, 97, 453, 117, 119, 55, 7 and 83) and RAPD group III (race 102) (Alzate-Marin et al., 1997).

Table I
- Genetic distance (%) of the Colletotrichum lindemuthianum races (Alzate-Marin et al., 1997).

Racesa		1	2	3	4	5	6	7	8	9	10	11	12	13	14	15	16	17	18	19	20	21
(89)	1	-
(67)	2	13	-
(7)	3	13	14	-
(97)	4	6	9	15	-
(73)	5	28	17	25	24	-
(23)	6	27	24	24	25	11	-
(453)	7	8	13	13	8	26	23	-
(585)	8	30	21	31	26	8	7	27	-
(339)	9	16	19	15	18	28	23	16	25	-
(55)	10	14	17	15	14	30	29	12	29	14	-
(81)	11	10	15	15	10	28	23	8	25	14	10	-
(87)	12	11	12	14	11	25	22	9	25	15	11	5	-
(65)	13	10	13	15	10	24	23	10	27	18	14	6	7	-
(119)	14	13	18	16	13	27	24	7	28	17	13	11	12	11	-
(79)	15	27	24	26	25	15	14	25	13	25	28	27	26	25	20	-
(343)	16	17	14	14	15	23	24	17	26	5	17	17	16	15	18	24	-
(64)	17	10	5	15	8	22	23	10	22	16	16	12	11	14	15	23	17	-
(95)	18	9	10	14	9	23	24	11	25	17	15	7	4	7	14	26	16	11	-
(117)	19	11	18	20	9	31	30	13	31	19	13	11	12	11	16	30	18	17	12	-
(83)	20	19	16	20	15	27	30	21	25	21	17	13	16	17	22	26	22	15	16	18	-
(102)	21	31	26	32	29	25	26	27	25	21	27	29	28	31	28	22	26	23	28	34	28	-
(72)	22	28	25	29	26	12	9	28	4	22	28	26	25	28	27	11	25	22	25	29	27	25

^aRaces were identified and classified based on virulence to 12 common bean differential cultivars (Rava et al., 1994).

Figure 1
- Grouping analysis (dendrogram) of Colletotrichum lindemuthianum races based on genetic distances (%) (Alzate-Marin et al., 1997).

In the evolution model proposed in this work, each race of C. lindemuthianum is characterized by a set of virulence genes (a to j) compatible with each of the resistance genes present in the first 10 common bean differential cultivars for anthracnose (Table II). For instance, virulence genes a and b are compatible with resistance genes of Michelite and MDRK, respectively. Virulence gene j is compatible with the resistance gene Mexico III present in cultivar TU (Tamayo et al., 1995). AB 136 and G 2333, the last two differential cultivars, are resistant to all C. lindemuthianum races found in Brazil.

Table II
- General information for the common bean differential cultivars and Colletotrichum lindemuthianum characterization.

Order	Differential cultivarsa	Resistance genes identifiedb, c	Binary value for susceptible reactiona	Virulence genes compatible with each differential cultivard
1	Michelite	-	1	a
2	MDRK	Ab Co-1c	2	b
3	Perry marrow	-	4	c
4	Cornell 49 242	Areb Co-2c	8	d
5	Widusa	-	16	e
6	Kaboon	-	32	f
7	Mexico 222	Mex Ib Co-3c	64	g
8	PI 207262	-	128	h
9	TO	Mex IIb Co-4c	256	i
10	TU	Mex IIIb Co-5c	512	j
11	AB 136	Co-6c	1024	k
12	G 2333	Co-5c Co-7c	2048	l

Sources: ^aPastor-Corrales (1992); ^bPastor-Corrales and Tu (1989); ^cLIST of genes (1996); ^dTamayo et al. (1995).

A co-evolution model was constructed analyzing the compatibility of C. lindemuthianum races with resistance genes of differential cultivars of common bean for anthracnose. Correlation among evolutionary routes within each RAPD group was analyzed.

RESULTS AND DISCUSSION

RAPD group I (Figure 2) includes virulence genes dg of C. lindemuthianum race 72, that is, genes that are compatible with Are and Mexico I resistance genes present in differential cultivars Cornell 49-242 and Mexico 222, respectively. As both races 72 and 64 contain the g virulence gene, race 72 could have evolved from race 64. However, considering that the genetic distance between them is one of the largest (Table I), they could also have evolved separately. Although the RAPD group for race 8 was not defined, this group could have originated from gene d. According to Flor's (1971) gene-to-gene theory, this idea is valid since Are and Mexico I genes were important resistance sources in Europe and America in the past (Vieira, 1988), and the virulence genes from the pathogen would have evolved separately. Race 23 did not show any correlation with other races in this group. Race 23 could be part of the race 7 route from group II, but the relatively long genetic distances of races 7, 55 and 119, when compared to race 23 (Table I), suggest that it should be placed in group I.

Figure 2
- Proposed model for evolution of the 25 races of Colletotrichum lindemuthianum identified in Brazil based on pathogenic phenotypes and RAPD analysis.

*DNA from C. lindemuthianum races 8, 75 and 101 was not amplified.

**Races proposed. Numbers refer to the binary classification of the pathogen and the letters to their respective virulence phenotype.

In RAPD group II, seven evolutionary routes for the acquisition of virulence genes were observed, of which six began with the g virulence gene (compatible with resistance gene Mexico I), showing the importance of this gene as the beginning of the great variability present in this group. In this group, race 95 which contains six virulence genes could have evolved along three different routes. Two routes evolved into race 119, one into 343 and the other into 453. Race 7, with virulence genes a, b and c, does not have the same ancestor of the other six races present in group II. It is probable that this race evolved from the b gene, since this gene is compatible with resistance gene A from differential cultivar MDRK, widely used as a source of anthracnose resistance (Vieira, 1988; Young and Kelly, 1997).

Group RAPD III consists solely of race 102. Analysis of the virulence genes suggests that this race evolved into race 119. However, the large genetic distance between races 102 and 119 (Table I) gives evidence that this is not the evolutionary route of this race. It is possible that race 102 evolved from b, c and f virulence genes that are compatible with differential cultivars MDRK, Perry Marrow and Kaboon. It did not, however, evolve from race 7 (RAPD group II), based on the large genetic distance between these two races (Table I).

Inferences were made in the model, such as the existence of races 39, 69, 91, 93, 193 and 197, which may be present in Brazil, but were not identified by Rava et al. (1994). However, race 69 was recently identified by Mesquita et al. (1997).

C. lindemuthianum has a broad virulence spectrum in Brazil, as it attacks Andean (MDRK, Perry Marrow and Kaboon) as well as Middle American common bean cultivars (Michelite, Cornell 49-242, Widusa, Mexico 222, PI 207262, TO, and TU). Pastor-Corrales (1996) observed that races obtained from Middle American hosts attacked a broader range of cultivars than the races obtained from Andean hosts. All races used in the present study were obtained from small- and medium-seeded Brazilian beans of Middle American origin, suggesting that these races co-evolved with the Middle American common bean cultivars.

C. lindemuthianum races with six (races 95, 119 and 343), five (races 79 and 453) and four (races 102 and 585) virulence genes represent a great risk to the common bean culture in Brazil. These races can attack a large number of cultivars that have any of the following resistance genes: A (Co-1), Are (Co-2), Mexico I (Co-3), Mexico II (Co-4) or Mexico III (Co-5). All these races have compatible reactions with Mexico I and A resistance genes, except 453 and 585. Races 79, 95 and 585 have compatible reactions with Are resistance gene. Races 453 and 343 have compatible reactions with Mexico II resistance gene and 585 with Mexico III resistance gene (Table II). Therefore, the incorporation and pyramidation of new resistance genes, for example Co-6 or Co-7 from AB 136 and G 2333 cultivars, will be an important strategy for stabilizing resistance against anthracnose in common bean cultivars grown in Brazil.

ACKNOWLEDGMENTS

This work is part of a project supported by PADCT/FINEP (No. 64.93.0430.00) and FAPEMIG (No. 1157/97). Ana Lilia Alzate-Marin was the recipient of a post-doctoral fellowship from FAPEMIG.

RESUMO

Colletotrichum lindemuthianum (Sacc. & Magn.) Scrib., agente causal da antracnose do feijoeiro comum (Phaseolus vulgaris L.), possui alto nível de diversidade de virulência, o que explica o elevado número de patótipos existentes. A partir de trabalhos anteriores sobre a classificação binária de 25 raças identificadas no Brasil e sua relação com agrupamentos RAPD, foi possível construir um modelo de evolução de tais raças. As raças 8 e 64, que foram compatíveis com os cultivares Cornell 49-242 (gene Are) e México 222 (gene México I), se apresentam como possíveis origens de duas importantes rotas de evolução. Inferências de raças ainda não detectadas no Brasil puderam ser feitas.

(Received February 2, 1998)

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Publication Dates

• Publication in this collection
  02 June 1999
• Date of issue
  Mar 1999

History

• Received
  02 Feb 1998