▪ Abstract We hypothesize that the evolutionary potential of a pathogen population is reflected in its population genetic structure. Pathogen populations with a high evolutionary potential are more likely to overcome genetic resistance than pathogen populations with a low evolutionary potential. We propose a flexible framework to predict the evolutionary potential of pathogen populations based on analysis of their genetic structure. According to this framework, pathogens that pose the greatest risk of breaking down resistance genes have a mixed reproduction system, a high potential for genotype flow, large effective population sizes, and high mutation rates. The lowest risk pathogens are those with strict asexual reproduction, low potential for gene flow, small effective population sizes, and low mutation rates. We present examples of high-risk and low-risk pathogens. We propose general guidelines for a rational approach to breed durable resistance according to the evolutionary potential of the pathogen.

Pathogen population genetics, evolutionary potential, and durable resistance

Resistance to anthracnose in common bean is conditioned primarily by nine major independent genes, Co-1 to Co-10 as the Co-3/Co-9 genes are allelic. With the exception of the recessive co-8 gene, all other nine are dominant genes and multiple alleles exist at the Co-1, Co-3 and Co-4 loci. A reverse of dominance at the Co-1 locus suggests that an order of dominance exists among individual alleles at this locus. The nine resistance genes Co-2 to Co-10 are Middle American in origin and Co-1 is the only locus from the Andean gene pool. Seven resistance loci have been mapped to the integrated bean linkage map and Co-1 resides on linkage group B1; Co-2 on B11, Co-3 on B4; Co-4 on B8; Co-6 on B7; and Co-9 and Co- 10 are located on B4 but do not appear to be linked. Three Co-genes map to linkage groups B1, B4 and B11 where clusters with genes for rust resistance are located. In addition, there is co-localization with major resistance genes and QTL that condition partial resistance to anthracnose. Other QTL for resistance may provide putative map locations for the major resistance loci still to be mapped. Molecular markers linked to the majority of major Co- genes have been reported and these provide the opportunity to enhance disease resistance through marker-assisted selection and gene pyramiding. The 10 Co-genes are represented in the anthracnose differential cultivars, but are present as part of a multi-allelic series or in combination with other Co-genes, making the characterization of more complex races diffi cult. Although the Co-genes behave as major Mendelian factors, they most likely exist as resistance gene clusters as has been demonstrated on the molecular level at the Co-2 locus. Since the genes differ in their effectiveness in controlling the highly variable races of the anthracnose pathogen, the authors discuss the value of individual genes and alleles in resistance breeding and suggest the most effective gene pyramids to ensure long-term durable resistance to anthracnose in common bean.

/pdf/a-comprehensive-review-of-the-major-genes-conditioning-3u180twgd2.pdf

A Comprehensive Review of the Major Genes Conditioning Resistance to Anthracnose in Common Bean

Two independently assorting dominant genes conditioning resistance to bean anthracnose were identified in an F2 population derived from the highly resistant bean differential cultivar, ‘G 2333’. One gene was allelic to the Co-4 gene in the differential cultivar ‘TO’ and was named Co-4

 2
 , whereas the second gene was assigned the temporary name Co-7 until a complete characterization with other known resistance genes can be conducted. Two RAPD markers linked to the Co-4

 2
 allele were identified. One RAPD, OAS13950, co-segregated with no recombinants in two segregating populations of 143 F2 individuals, whereas the second RAPD, OAL9740, mapped at 3.9 cM from the Co-4

 2
 allele. Two 24-mer SCAR primers (SAS13), developed from the OAS13950 RAPD marker, were dominant and polymorphic, similar to the original RAPD, and supported the tight linkage between the marker(s) and the Co-4

 2
 allele. The markers were present in germplasm with known resistance alleles at the Co-4 locus. The presence of the markers in two other differential cultivars not previously characterized and in four navy bean cultivars suggests the existence of a gene family for anthracnose resistance at or near the Co-4 locus. Since the Co-7 gene was present only in germplasm which also possessed the Co-4

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 and Co-5 genes, the SAS13 markers were used in combination with standard inoculation techniques to identify F3 lines in which the Co-7 gene was homozygous and the Co-4

 2
 allele was absent. A similar strategy of marker-assisted dissection is proposed to identify resistant lines in which the Co-5 gene is absent and the Co-7 gene is present by selecting against the OAB3450 marker, which has been shown previously to be linked to the Co-5 gene. These genes cannot be distinguished using traditional screening methods since all current races of the pathogen virulent to the Co-5 gene are avirulent to the Co-4

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 and Co-7 genes. We describe the use of molecular markers tightly linked to resistance genes to facilitate the identification of an uncharacterized resistance gene for which no discriminating race of the pathogen is known.

Marker-assisted dissection of the oligogenic anthracnose resistance in the common bean cultivar, 'G 2333'

The recent cloning of plant resistance (R) genes and the sequencing of resistance gene clusters have shed light on the molecular evolution of R genes. However, up to now, no attempt has been made to correlate this molecular evolution with the host-pathogen coevolution process at the population level. Cross-inoculations were carried out between 26 strains of the fungal pathogen Colletotrichum lindemuthianum and 48 Phaseolus vulgaris plants collected in the three centers of diversity of the host species. A high level of diversity for resistance against the pathogen was revealed. Most of the resistance specificities were overcome in sympatric situations, indicating an adaptation of the pathogen to the local host. In contrast, plants were generally resistant to allopatric strains, suggesting that R genes that were efficient against exotic strains but had been overcome locally were maintained in the plant genome. These results indicated that coevolution processes between the two protagonists led to a differentiation for resistance in the three centers of diversity of the host. To improve our understanding of the molecular evolution of these different specificities, a recombinant inbred (RI) population derived from two representative genotypes of the Andean (JaloEEP558) and Mesoamerican (BAT93) gene pools was used to map anthracnose specificities. A gene cluster comprising both Andean (Co-y; Co-z) and Mesoamerican (Co-9) host resistance specificities was identified, suggesting that this locus existed prior to the separation of the two major gene pools of P. vulgaris. Molecular analysis revealed a high level of complexity at this locus. It harbors 11 restriction fragment length polymorphisms when R gene analog (RGA) clones are used. The relationship between the coevolution process and diversification of resistance specificities at resistance gene clusters is discussed.

https://apsjournals.apsnet.org/doi/pdf/10.1094/MPMI.1999.12.9.774

Identification of an ancestral resistance gene cluster involved in the coevolution process between Phaseolus vulgaris and its fungal pathogen Colletotrichum lindemuthianum.

Incorporation of the dominant gene Are, of Middle American origin, into commercial cultivars of Phaseolus vulgaris L., has been the main disease control strategy of plant breeders to limit the potential damage of Colletotrichum lindemuthianum (Sacc. & Magnus.) Lams.-Scrib. A random amplified polymorphic DNA (RAPD) marker designated OQ41440, generated by a 5'-AGTGCGCTGA-3' decamer primer, was found tightly linked in coupling with the Are gene. OQ41440 mapped at 2.0 ± 1.4 centimorgans (cM) from the Are allele in the Andean genetic background and at 5.5 ± 2.3 CM in the Middle American background. A second coupling phase RAPD marker B3551000, generated by the 5'-GTATGGGGCT 3' primer mapped at 5.4 ± 2.3 cM from the Are allele in the Andean genetic background and at 7.7 ± 2.7 CM in the Middle American background. Based on a recombination distance of 7.0 ± 1.9 cM between the two markers, OQ4 1440 and B3551000 RAPDs appear to flank the Are gene. The bracketing molecular markers allowed tagging of the Are allele with a selection fidelity of 99%. Use of the OQ41440 and B3551000RAPD markers for marker-based selection will afford the opportunity to retain the Are anthracnose resistance gene in bean germplasm, as other epistatic resistance genes are characterized, and incorporated into contemporary bean cultivars. Anthracnose, caused by Colletotrichum lindemuthianum, is a serious seedborne fungus capable of inducing complete yield loss in susceptible bean genotypes. Surveys in a wide range of produc- tion areas have identified several distinct races, suggesting exten- sive pathogenic variation on all continents (Pastor-Corrales and Tu, 1989). In North America, reported races include alpha, alpha Brazil, beta, gamma, delta, epsilon, and lambda in Canada (Tu, 1992, 1994). Recently, Kelly et al. ( 1994) identified two new races of C. lindemuthianu m in the United States, which are pathogenic on resistance genes currently deployed. The dominant allele at the Are locus, which confers resistance to alpha, beta, gamma, delta, epsilon, and lambda races of the fungus, was first found in a black bean from Venezuela, Cornell 49-242 (Mastenbroek, 1960) and has been used widely in North America and Europe as the main source of resistance against anthracnose (Fouilloux, 1979; Tu,

/pdf/rapd-markers-flanking-the-are-gene-for-anthracnose-3keerx3376.pdf

M.J. Jeger

Papers

Colletotrichum lindemuthianum on bean: population dynamics of the pathogen and breeding for resistance.