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Genetics and mapping of a new anthracnose resistance locus in Andean common bean Paloma

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A broad genetic base is essential for the protection of crops, especially for their protection against pathogens with high virulence diversity. The utilization of Andean common bean for the genetic improvement of the common bean crop has lagged far behind the use of Mesoamerican common bean [6]. Paradoxically, the underutilized genetic diversity of Andean common bean contains genes conferring effective resistance to highly virulent Mesoamerican races of the pathogens that cause anthracnose, angular leaf spot, and rust diseases of common bean [10, 37, 46]. Incorporating Andean anthracnose resistance genes, such as the new gene (Co-Pa) in Paloma in common bean-breeding programs, would make possible the development of common bean cultivars with broad resistance to C. lindemuthianum.

The results of this study showed that the Andean cultivar Paloma is a very important source of anthracnose resistance, particularly for the protection against Mesoamerican races of this pathogen. We observed that Paloma was resistant to C. lindemuthianum Andean races 23 and 55 and to Mesoamerican races 65, 73, 1545, 2047 and 3481. Interestingly, Paloma as shown to be effective against Mesoamerican races of the anthracnose pathogen that are frequent in countries such as: United States, Brazil and Central America. The resistance of Paloma to races 23, 55, 65 and 73 has a great importance for common bean breeding programs in Brazil, especially on places where these races are widespread [47]. Race 73 is present in 13 of the 14 states of Brazil, while race 65 is present in 12 states of this country [9]. Race 65 has also been reported in Honduras, Mexico, USA, Costa Rica, Guatemala, Puerto Rico, India and Canada [9]. Among the resistance genes in Andean cultivars, Co-1 4, Co-12 and Co-14 are resistant to Andean race 55. This race overcomes the resistance of the Andean Co-1, Co-1 2 , Co-1 3 , Co-1 5 , Co-13 and Co-15 resistant genes. Race 55 also overcomes the resistance of Andean common bean Jalo EEP558, which contains the Co-w, Co-x, Co-y and Co-z anthracnose resistant genes.

Paloma is also resistant to the highly virulent Mesoamerican races 2047 and 3481. Race 2047 is virulent on 11 of the 12 differential cultivars. Thus, this race overcomes the resistance of the Co-1 and four of its alleles, Co-2, Co-3, some of the alleles of Co-4, Co-5, Co-6, Co-11, Co-12, Co-13, and the four anthracnose genes present in Jalo EEP 558. G 2333 was the only differential cultivar that was resistant to race 2047. Among the Andean anthracnose resistance genes, only Co-14, Co-15 and Co-1 4 were resistant to race 2047. Similarly, race 3481 overcomes the resistance of seven of the 12 differential cultivars, including G 2333 that contains the Co-3 5, Co-4 2 and Co-5 2 alleles. Andean alleles Co-1, Co-1 2 , Co-1 3 , Co-1 4 , and gene Co-13 were resistant to race 3481. Therefore, only AND 277 (Co-1 4 ) and Paloma (Co-Pa) were resistant to the highly virulent 2047 and 3481 races of C. lindemuthianum.

The inheritance of resistance evaluation from the cross Paloma (R) × Cornell 49–242 (S) – inoculated with race 2047, and the cross Paloma (R) × PI 207262 (S) – inoculated with race 3481, revealed the presence of a single dominant gene in Paloma. Furthermore, bulk segregant analysis, using the BARCBean6K_3 BeadChip in common bean, positioned the resistance gene in Paloma (Co-Pa) in the lower arm of chromosome Pv01 where other anthracnose resistant genes have been mapped. These genes include Co-1 and its alleles, Co-14, Co-x and Co-w. The allelism tests showed that Co-Pa is independent from the allelic series Co-1 and the Co-14 genes. No allelism test was conducted with Jalo EEP558, which contains two anthracnose resistant genes (Co-x and Co-w) in Pv01. However, the anthracnose resistant phenotype of Paloma and Jalo EEP558 were different for races 55, 449, 453, and 2047, suggesting that Co-Pa may be different from Co-x and Co-w (Table 1).

The Co-Pa anthracnose resistant gene in Paloma is mapped to a cluster containing anthracnose (Co-1 and its alleles, Co-14, Co-x, Co-w), rust (Ur-9) and angular leaf spot (Phg-1) disease resistant genes [21, 4850]. Dense clusters of tightly linked resistance-associated genes in the common bean genome encode mostly NB-LRR (nucleotide-binding, leucine-rich repeat) genes [5]. The identification of this protein class across diverse plant species demonstrated that NB-LRR genes are a pillar of plant defense [51]. NB-LRR gene clusters enriched with an N-terminal coiled-coil domain (CNL) or an N-terminal Toll-interleukin-1 receptor (TIR)-like domain (TNL) were identified at the ends of common bean chromosomes, such as the distal part of Pv01 [5, 23]. It is worth noting that all resistance genes currently mapped on chromosome Pv01 are from common bean of Andean origin. This is a unique situation among the chromosomes of common bean containing disease resistance genes.

The combined results of SS82 and SS83 SNP markers, with the monogenic inheritance and allelism tests, confirmed the hypothesis that a single dominant gene confers resistance to C. lindemuthianum races 65, 73, 2047 and 3481 in the Andean common bean cultivar Paloma. Likewise, this gene is independent from those common bean anthracnose resistance genes previously characterized. The authors propose that this single dominant anthracnose resistance gene in Paloma to be temporarily named as Co-Pa, until a new designation is defined by the Genetics Committee of the Bean Improvement Cooperative.

Future efforts will focus on fine mapping of the 390,998 bp region in Pv01 containing the Co-Pa, the resistance gene in Paloma. Co-x and Co-1 4 anthracnose resistance genes have been closely mapped to Co-Pa. Thus, genetic analysis of segregating populations from the cross between Paloma and cultivars containing Co-1 4 and Co-x will be the subject of future studies.

The Co-Pa anthracnose resistant gene in Paloma provides resistance to the Mesoamerican races 2047 and 3481 of C. lindemuthianum that overcome the most of known resistance genes in common bean. Furthermore, the Co-Pa gene in Paloma confers resistance to these and many other Mesoamerican races. On the other hand, the Mesoamerican genes Co-4 and its alleles, Co-5, Co-6 and other anthracnose Mesoamerican resistant genes confer effective resistance to Andean races that overcome the resistance of Co-Pa and other Andean resistance genes.

These results suggest that combining Co-Pa with Mesoamerican resistant genes in a single cultivar will confer effective and possibly durable resistance to all known races of the highly variable anthracnose pathogen of common bean. In addition, the flanking SNP markers SS82 and SS83 linked to resistance gene Co-Pa of Paloma, will be very useful for gene pyramiding of Co-Pa with other Mesoamerican and Andean genes.

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