Breeding common bean for resistance to insect pests and nematodes: A review

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Breeding common bean for resistance to insect pests and nematodes: A review Shree P. Singh1 and Howard F. Schwartz2 1

Soil and Entomological Sciences Department, University of Idaho, 3793 North 3600 East, Kimberly, Idaho 83341-5076, USA (e-mail: [email protected]); and 2Department of Bioagricultural Sciences & Pest Management, Colorado State University, Fort Collins, CO 80523-1177, USA. Received 7 January 2010, accepted 4 November 2010. Singh, S. P. and Schwartz, H. F. 2011. Breeding common bean for resistance to insect pests and nematodes: A review. Can. J. Plant Sci. 91: xxxxxx. Various insect pests and nematodes cause severe losses (3590%) globally to the yield and quality of dry and green common bean (Phaseolus vulgaris L.). The objectives of this review are to briefly describe major insect pests and nematodes in the Americas, breeding strategies and methods used, and research progress achieved. We also describe integrated genetic improvement for resistance to multiple insect pests and nematodes and cultivar development. Breeding for resistance to one insect pest or nematode at a time has been practiced in most instances. Backcross, pedigree, and bulkpedigree breeding methods have been used. Considerable progress has been made in genetics and germplasm enhancement for resistance to bean pod weevil (Apion godmani Wagner), tropical bruchid (Zabrotes subfasciatus Boheman), leafhoppers (Empoasca kraemeri Ross and Moore), and root- knot nematode (Meloidogyne species). However, improvement in resistance to Acanthoscelides obtectus (Say), lesion (Pratylenchus species) and soybean cyst (Heterodera glycines) nematodes, and other regional insect pests has been minimal or non-existent. Furthermore, dry or green common bean cultivars with high levels of resistance to one or more insect pests and nematodes are rare. Breeding strategies for integrated and simultaneous genetic improvement of multiple qualitatively and quantitatively inherited resistances for cultivar development are briefly described. Key words: Integrated genetic improvement, introgressing resistance, multiple-parent crosses, Phaseolus vulgaris, pyramiding resistance Singh, S. P. et Schwartz, H. F. 2011. Ame´lioration du haricot pour le rendre re´sistant aux insectes et aux ne´matodes: tour d’horizon. Can. J. Plant Sci. 91: xxxxxx. Divers insectes et ne´matodes causent de lourdes pertes (de 35 a` 90%) a` la culture mondiale du haricot vert et du haricot sec (Phaseolus vulgaris L.) par une diminution de leur rendement et de leur qualite´. Ce tour d’horizon a pour but de de´crire brie`vement les principaux ravageurs qui se´vissent dans les Ame´riques, les strate´gies et les me´thodes d’hybridation, ainsi que les progre`s re´alise´s par la recherche. Les auteurs abordent aussi la question de l’ame´lioration ge´ne´tique inte´gre´e visant a` confe´rer simultane´ment une re´sistance contre plusieurs insectes et ne´matodes et celle du de´veloppement de cultivars. Dans la plupart des cas, les varie´te´s sont ame´liore´es pour re´sister a` un ravageur a` la fois. On recourt au re´trocroisement, aux ligne´es ge´ne´alogiques et a` l’hybridation massive de ligne´es ge´ne´alogiques. Graˆce a` la ge´ne´tique et a` l’ame´lioration du mate´riel ge´ne´tique, on a re´alise´ des progre`s conside´rables dans la re´sistance au charanc¸on du haricot (Apion godmani Wagner), a` la bruche bre´silienne (Zabrotes subfasciatus Boheman), aux cicadelles (Empoasca kraemeri Ross and Moore) et au ne´matode ce´cidoge`ne (Meloidogyne species). Cependant, on a tre`s peu ou pas du tout ame´liore´ la re´sistance contre le ne´matode Acanthoscelides obtectus (Say), ceux du genre Pratylenchus et le ne´matode du kyste du soja (Heterodera glycines), ainsi que d’autres ravageurs re´gionaux. Par ailleurs, les haricots secs ou verts tre`s re´sistants a` un ou a` plusieurs insectes et ne´matodes sont rares. Suit une bre`ve description des strate´gies d’hybridation axe´e sur l’ame´lioration inte´gre´e et simultane´e de nombreux caracte`res de re´sistance acquis qualitativement ou quantitativement en vue du de´veloppement de cultivars. Mots cle´s: Ame´lioration ge´ne´tique inte´gre´e, re´sistance introgressive, croisements a` parents multiples, Phaseolus vulgaris, re´sistance pyramidale

Dry and green, garden, snap, or stringless common bean (Phaseolus vulgaris L.) are important food legume crops worldwide, with dry bean occupying the largest hectarage [13 million ha, (Singh 1992, 1999)]. Several insect pests and nematodes attack aerial and underground parts of the common bean (Cardona 1989; Kornegay and Cardona 1991; Singh 1992, 2001; Cardona and Kornegay 1999). Unlike diseases such as bean common mosaic (caused by an aphid-vectored potyvirus) and common bacterial blight [caused by Xanthomonas campestris Can. J. Plant Sci. (2011) 91: xxxxxx doi:10.4141/CJPS10002

pv. phaseoli (Smith) Dye (synonymous with X. axonopodis pv. phaseoli (Smith) Vauterin et al.] that are widely distributed, most insect pests and some nematodes are often of regional importance. Even if an insect pest is widely distributed, different species may occur in different ecological regions causing similar damage. For example, leafhoppers Empoasca kraemeri Ross and Moore

Abbreviation: QTL, quantitative trait loci 1

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aphid-vectored potyviruses. Bean golden mosaic occurring in Argentina, Bolivia, and Brazil and bean golden yellow mosaic found in tropical and subtropical Central America, coastal Mexico, the Caribbean, and southeastern USA are caused by whitefly-transmitted geminiviruses. Beet curly top occurring in common bean production regions in western USA is caused by a leafhopper-vectored curtovirus, and bean yellow mosaic in the USA, Chile, and other parts of the world is caused by an aphid-transmitted potyvirus. Other viral diseases of local or regional importance that are transmitted by insects include alfalfa mosaic (an aphid-transmitted potyvirus), bean dwarf mosaic (a whitefly-vectored geminivirus), and cucumber mosaic (an aphid-transmitted potyvirus). Singh and Schwartz (2010) recently reviewed advances in genetics and breeding for resistance to many of these viral and other diseases. Average yield losses caused by major insect pests and nematodes in the American continents may range from 35 to 100% (Table 1) depending on the occurrence and severity of the individual and collective insect pests and nematodes occurring in the same field, production systems and management practices used, environmental conditions, common bean cultivars grown, and crop stages when affected. Two or more insect pests and nematodes may occur at the same time in the same field, thus accentuating the problem. The quality of harvested seed, its germinability, and market value may also be reduced. Some insect pests and nematodes may have alternate hosts, and/or survive on the plant debris left in the field. Development and use of cultivars resistant to insect pests and nematodes therefore (1) minimize yield losses and improve pod and seed quality, (2) broaden adaptation and improve stability of performance of cultivars, (3) reduce pesticide use and enhance pesticide use efficiency, (4) minimize health hazards and adverse environmental impacts, (5) reduce production costs, (6) increase profitability and competitiveness of producers in domestic and international market places, and (7) support reduced-input and sustainable organic and conventional production systems. The use of resistant common bean cultivars is pivotal to any sound, economical, and integrated pest management strategy. However, breeding for resistance to insect

occur in warm and dry tropical and sub-tropical production regions of Latin America and the Caribbean, whereas E. fabae Harris (i.e., potato leafhopper) causes similar damage to common bean in cool temperate environments in the midwestern USA and Canada. Leafhoppers E. kraemeri and E. fabae are the most widely distributed insect pests in common bean fields on the American continents, especially in relatively drier areas. Bean pod weevil (Apion godmani and A. aurichalceum Wagner) causes severe damage to developing pods and seeds in the highlands of Mexico, in Guatemala, El Salvador, Honduras, and Nicaragua. In the highlands of Mexico and in the western USA, Mexican bean beetles (Epilachna varivestis Mulsant) also cause severe leaf damage, especially in late-maturing cultivars. Bean weevil, Zabrotes subfasciatus Boheman, in warm tropical and subtropical environments, and Acanthoscelides obtectus (Say), in cool and temperate environments, cause severe post-harvest problems when common bean is not properly stored (Cardona 1989). Key insect pests in other parts of the world, including Africa, are the leafhopper, thrips, weevils, whitefly, bean fly (Ophiomyia phaseoli Tryon), aphids (e.g., Aphis fabae Scopoli), chrysomelids (Ootheca species), pod borer [Maruca testulalis (Geyer)], and mites [Tetranychus cinnabarinus Boisd., Polyphagotarsonemus latus (Banks)] (Karel and Autrique 1989; Schwartz and Peairs 1999). Occurrence, distribution, and losses caused by nematodes are poorly documented. However, root-knot (Meloidogyne species), lesion (Pratylenchus species), and soybean cyst (Heterodera glycines) nematodes can pose major threats to common bean production. The population densities of these nematodes are exacerbated by the continual plantings of susceptible cultivars. Rotation with other susceptible crops such as tomato, pepper, and potato aggravates problems for the succeeding common bean crop (Schwartz and Pastor-Corrales 1989; Abawi and Widmer 2000; Schwartz et al. 2005). In addition to causing direct damage to foliar and underground plant parts including pod and seed yield and quality, insects are important as vectors of numerous common bean viruses and viral diseases (Schwartz et al. 2005). For example, bean common mosaic and bean common mosaic necrosis are caused worldwide by

Table 1. Summary of major insect pests and nematodes attacking common bean in the Americas, yield loss potential, and survival Common name

Organism

Yield loss potential (%)

Survivalz

Bean pod weevil Bruchid

Apion godmani Acanthoscelides obtectus, Zabrotes subfasciatus Empoasca and Circulifer species Heterodera glycines Meloidogyne spp. Pratylenchus spp. Thrips palmi

95 35

Egg, larval, prepupal, and pupal stages require 6 to 8 wk Egg, larval and pupal stages require 30 d

Leafhopper Nematodes Thrips z

80 55 90 80 100

Egg and nymphal stages require 20 d Infested soil, plant debris, irrigation water Immature stages require B15 d and adults live B20 d

Plant debris includes volunteer bean plants that emerge from previous seed and debris during succeeding growing seasons.

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pests and nematodes requires a thorough knowledge of the origin, domestication, and evolution of the crop and its relatives, other major production problems, germplasm screening methods, sources of resistant germplasm in the primary, secondary, and tertiary gene pools, genetics of resistance, breeding strategies and methods, and a collaborative team of dedicated researchers with necessary resources over a long period of time. Cardona and Kornegay (1999) and Kornegay and Cardona (1991) reviewed breeding common bean for insect pest resistance. Singh (1992, 2001) Kelly (2001), Kelly et al. (2003), Kelly and Vallejo (2004), and Miklas et al. (2006) reviewed broadening of the genetic base and breeding for resistance to abiotic and biotic stresses and other agronomic traits. More recently, Singh and Schwartz (2010) reviewed progress made in genetic improvement of resistance to major bacterial, fungal, and viral diseases with emphasis on the American continents. Therefore, only a brief account of the common bean and its relatives, followed by their major insect pests and nematodes, will be given. We will then review the sources of resistance germplasm and recent progress made in genetics and breeding of dry bean for resistance to major insect pests and nematodes with emphasis in the American continents. We also will briefly describe an integrated strategy for simultaneous genetic improvement of multiple insect pest resistance for cultivar development. The immediate ancestors of dry and green common bean (2n2x 22) are its wild populations distributed from northern Mexico to northern Argentina (Gepts et al. 1986; Gepts 1998). Dry bean can be small (B25 g 100 seed weight), medium (25 to 40 g 100 seed weight), or large-seeded (40 g 100 seed weight) depending upon its evolutionary origin and domestication regions in Andean South America, Middle America, and Mexico (Singh 1989; Singh et al. 1991a). For example, largeseeded dry bean is of Andean South American origin, whereas small-seeded dry bean originated in tropical Middle America, and medium-seeded in the highlands of Mexico. Large differences exist in consumer preferences for common bean, whether for green pods or for dry or semi dry seed, size, shape, color, taste, and other quality attributes are all important and must be met before even the most productive genotypes will be considered for commercial production and marketing (Singh 1992; Voysest et al. 1994). Common bean is a short-day crop (White and Laing 1989) adapted to mildly cool environments (15 to 258C mean growing temperatures). Most cultivars and landraces grown in the highlands of Mexico, Central America, and the Andes (above 1500 m elevation) are often indeterminate prostrate semiclimbing growth habit Type III (Singh 1982) or climbing growth habit Type IV (Singh 1989; Singh et al. 1991a), and highly sensitive to long photoperiods. Consequently, such cultivars and landraces may not complete their growing cycle under long summer months in the USA and Canada. However,

photoperiod-insensitive cultivars of determinate growth habit Type I and indeterminate growth habit Type II (upright) and Type III are grown (in addition to Latin America and the Caribbean) at higher latitudes in the USA, Canada, Europe, Japan, and other parts of the world. While green bean is often grown in monoculture, dry bean, in addition to monoculture, is grown in diverse intercropping and strip-cropping production systems with different annual and perennial crops, fruit trees, and shrubs in Latin America, the Caribbean, and other parts of the world (Woolley et al. 1991; Singh 1992). Thus, the insect pest and nematode problems and the extent of crop losses may be affected by the production system, agronomic management, growing environment, and dry and green bean cultivars used. Hybrids between cultivated and wild common bean are fully fertile. However, F1 hybrid dwarfism or lethality may occasionally be encountered between the Middle American and Andean wild (Koinange and Gepts 1992) and cultivated (Singh and Gutie´rrez 1984) genotypes carrying the Dl-1 and Dl-2 alleles, respectively. Similarly, some recombinants in inter-gene pool and inter-racial crosses may exhibit crippled leaves or virus-like symptoms and deformed plants in the F2 and subsequent generations of bi-parental or single-crosses, and in the F1 onwards of multiple-parent crosses in the presence of Dl-1 or Dl-2 alleles (Singh and Molina 1996). Excluding these occasional problems, there was no overall incompatibility between the Andean and Middle American wild and cultivated gene pools of common bean (Mumba and Galwey 1999). Nonetheless, it is often difficult to recover the parental phenotype with the introgressed traits from bi-parental crosses even between the cultivated Andean and Middle American gene pools of common bean (Paredes and Gepts 1995; Welsh et al. 1995). Furthermore, because differences in reciprocal crosses were widespread, the direction (i.e., using as a female or male) in which crosses are made may affect the type of genotypes that could be obtained from inter-gene pool crosses (Mumba and Galwey 1999). While the common bean and species within its tertiary and quarternary gene pool are self-pollinated, the secondary gene pool species exhibit considerable amount of outcrossing (from 20 to 40%). Crosses of common bean with the two Phaseolus species in the tertiary gene pool, namely P. acutifolius (Thomas and Waines 1984; Parker and Michaels 1986; Mejı´ a-Jı´ menez et al. 1994) and P. parvifolius (Singh et al. 1998) require embryo rescue. The probability of successful crossing and embryo rescue is enhanced if common bean is used as the female, and is dependent on the genotypes of both species used (Parker and Michaels 1986; Mejı´ a-Jı´ menez et al. 1994). The three species in the secondary gene pool (P. coccineus, P. costaricensis, P. polyanthusP. dumosus) are crossed with common bean without embryo rescue, particularly when the common bean is used as the female (Shii et al. 1982; Singh et al. 1997, 2009).

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However, hybrid progenies between crosses of common bean and any of the three secondary gene pool species may be occasionally dwarf lethal (Singh and Narvae´z 1999) or often partially sterile, and it may be difficult to recover the desired stable common bean phenotypes with introgressed genes and quantitative trait loci (QTL) from the secondary gene pool (Guo et al. 1991; Singh et al. 2009). INSECT PEST AND NEMATODE RESISTANCES LACKING IN COMMON BEAN The major insect pests and nematodes attacking common bean in the Americas for which resistance in cultivated common bean is inadequate include bruchids A. obtectus, leafhoppers, and root-knot, lesion, and soybean cyst nematodes. Thus, to protect the crop from significant loss in yield and quality, other elements, including crop rotation and cultural practices, are essential to supplement the gains realized through breeding for genetic resistance of new cultivars. Hall and Nasser (1996) and Schwartz and Peairs (1999) reviewed integrated pest management components and strategies for common bean. Therefore, integrated pest management strategies for any insect pests and nematodes will not be discussed here. SOURCES OF RESISTANCE TO INSECT PESTS AND NEMATODES Adequate levels of resistance to bean pod weevil are found in the common bean landraces from the Mexican highlands belonging to race Jalisco (discussed later). But resistance to bruchids Z. subfaciatus was found only in wild P. vulgaris (Schoonhoven et al. 1983; AcostaGallegos et al. 1998; Sparvoli and Bollini 1998), P. acutifolius, and other Phaseolus species (Dobie et al. 1990; Cardona and Kornegay 1999). Phaseolus acutifolius also has the highest levels of resistance to A. obtectus (Shade et al. 1987; Dobie et al. 1990) and leafhoppers, E. kraemeri (Cardona and Kornegay 1999). Thus, favorable genes and QTL are scattered across cultivated and wild populations in the primary, secondary, tertiary, and other gene pools of common bean. Furthermore, some common bean landraces from race Mesoamerica possess resistance to two or more pests. For example, Carioca (a small-seeded cream-striped dry bean) from Brazil tolerates leafhoppers and root-knot nematodes. The identification and use of such landraces would accelerate breeding for resistance to multiple insect pests and nematodes. BREEDING FOR RESISTANCE TO INSECT PESTS Principal factors determining strategies and methods used for breeding for resistance to insect pests and nematodes and other desirable traits include (1) the genetic distance between the cultivar to be improved and resistant donor germplasm, (2) the direct and indirect screening methods available, (3) the genetics of resistance, and

(4) the number of resistances and other traits to be improved. Given the diversity and genetic distance between the cultivars of specific market classes to be improved and the resistance donor germplasm, a two- or three-tiered integrated breeding approach is often used to broaden the genetic base and introgress and pyramid resistance genes and QTL from across market classes, races, gene pools, and related species into successful new common bean cultivars (White and Singh 1991; Kelly et al. 1998; Singh 2001). Often, the pedigree, masspedigree, and single seed descent breeding methods suffice for transferring major resistance alleles and QTL between cultivars and elite breeding lines within market classes. Some form of backcrossing, such as recurrent backcrossing, inbred-backcrossing, or congruitybackcrossing (i.e., backcrossing alternately with either parent), becomes essential as the genetic distance between the cultivar under improvement and the resistance donor germplasm increases. Thus, for most of the between-market class, inter-racial, and inter-gene pool crosses, and for introgressing resistance alleles and QTL from wild populations of common bean and Phaseolus species in the secondary and tertiary gene pools, recurrent or congruity backcrossing or modifications become the methods of choice in early stages of the program. Gamete selection using multiple-parent crosses (Singh 1994; Singh et al. 1998; Asensio et al. 2005, 2006; Tera´n and Singh 2009) and recurrent selection (Kelly and Adams 1987; Singh et al. 1999; Tera´n and Singh 2010a, b), respectively, may be more effective. But, the use of these latter methods is not common in common bean because of the large number of pollinations required and other demands on resources. Bean Pod Weevil Bean pod weevil (A. godmani Wagner) is an endemic problem at medium to high elevations in Mexico and Central America. In the highlands of Mexico and Guatemala, the races Jalisco and Guatemala cultivars, respectively, are grown, whereas race Mesoamerica cultivars are popular at lower elevations in Mexico and Central America. The adult female of A. godmani chews a small hole in the mesocarp of young developing pods, usually above the developing seed over the length of the pod, and lays a white semi-translucent egg that hatches in 8 to 10 d (Garza et al. 2001). In contrast, the female of a related species, A. aurichalceum Wagner, lays approximately 35 eggs only in the distal portion of the pod, thus remaining seeds escape attack. Apion aurichalceum is therefore of minor economic importance. The three larval instars feed on the developing seeds, the last instar forms a pupational chamber inside the pod, and after about 10 d the adult emerges. Thus, one generation each of A. godmani and A. aurichalceum is completed per growing season. Yield losses up to 94% due to A. godmani have been reported in dry beans (see Cardona 1989).

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Most of race Mesoamerica cultivars are highly susceptible to A. godmani. High levels of resistance (antibiosis) are found in some landraces of the common bean race Jalisco (Garza and Muruaga 1993; Garza et al. 1996, 2001) and wild common bean populations from central highlands of Mexico (Acosta et al. 1992). The Agr allele alone confers an intermediate level of resistance, but when Agr is present with the Agm allele, resistance to the pod weevil is higher (Garza et al. 1996). However, the Agm allele alone has no effects on resistance. Blair et al. (2006) identified molecular markers linked with these resistance genes. The effectiveness of molecular markers for indirect selection for resistance to bean pod weevil has yet to be determined. Beebe et al. (1993) transferred high levels of A. godmani resistance from the race Jalisco landraces into small black and red-seeded breeding lines and cultivars for Central America using the mass-pedigree selection method. They also combined resistance to BCMV and other diseases with A. godmani resistance. Apion godmani resistance from wild bean, if found to be different from that of race Jalisco landraces, needs to be combined with resistance found in race Jalisco landraces and transferred into agronomically acceptable cultivars. Furthermore, germplasm from Phaseolus species of the secondary and tertiary gene pools and interspecific breeding lines derived from them need to be screened. Subsequently, complementary and additive resistance from across Phaseolus species need to be pyramided and introgressed into cultivars. Bruchid The post-harvest storage insects, Z. subfasciatus in the tropics, and A. obtectus in cool highlands of the tropics and sub-tropics and at higher latitudes in temperate regions, cause an estimated damage of 15% if dry bean seed is not properly stored (Kornegay and Cardona 1991). Zabrotes subfasciatus infestation and damage only occurs in the storage starting from pre-existing insect populations. However, A. obtectus infestation may begin from the standing crop in the field by the female ovipositing eggs on growing pods. In storage, Z. subfasciatus glues eggs to the seed and A. obtectus scatters eggs among seeds. After hatching, the young larvae bore through their eggshell and the seed coat in one process, and the life cycles of both species are similar (see Cardona 1989). The larvae molt four times before pupating, and during the last larval instar, the rounded outline of the feeding and pupational cell becomes externally visible on the seed surface. After pupation the adult pushes or bites its way out of the cell, leaving a circular hole in the seed. Thus, the damaged seed has an ugly appearance, market and nutritional values may be drastically reduced, and there could be germination loss and poor seedling vigor. Resistance to Z. subfasciatus was not found in thousands of common bean cultivars and landraces (Schoonhoven and Cardona 1982), and only a few wild

common bean accessions from the central highlands of Mexico were resistant (Schoonhoven et al. 1983; AcostaGallegos et al. 1998; Sparvoli and Bollini 1998). The storage arcelin protein present in the cotyledons of wild common bean was responsible for the resistance (Osborn et al. 1988; Cardona et al. 1989). There are seven dosage-dependent or partially dominant alleles at the arcelin locus, each with a different effect on Z. subfasciatus resistance (Acosta-Gallegos et al. 1998; Cardona et al. 1990; Sparvoli and Bollini 1998). The presence of arcelin can be detected by SDS-PAGE electrophoresis. However, the enzyme-linked immunosorbant assay (ELISA, antiserum to the protein) is easier, faster, and cheaper for large-scale germplasm screening. This discovery facilitated breeding for bruchid resistance and minimized dependence on screening using insect infestation that was time-consuming, required large quantities of seed for replicated trials and insect rearing, and was affected by the environment. A recurrent backcross program was used to introgress high levels of resistance to bruchids from wild bean into a range of dry bean market classes (Cardona et al. 1990). Arcelin, like lectin and other related proteins, is heat labile and its anti-nutritional and harmful effects are lost during prolonged (30 min) cooking. Because resistance to A. obtectus in cultivated and wild common bean is inadequate, and all resistance alleles for Z. subfasciatus in wild common bean occur at the arcelin locus, there is good reason to introgress additive and complementary bruchid resistance genes and QTL from P. acutifolius and other Phaseolus species (Shade et al. 1987; Dobie et al. 1990). Leafhopper The nymph of leafhoppers (E. kraemeri) in relatively warm, semi-arid production regions in Latin America (e.g., northeastern Brazil) and the Caribbean (Schoonhoven et al. 1978) and potato leafhopper (E. fabae) in Canada and the USA (Whitefield and Ellis 1976; Gonzalez and Wyman 1991; Lindgren and Coyne 1995; Schaafsma et al. 1998) feed on young tender leaves. Infested seedlings are stunted, and leaf margins develop yellowish borders, necrosis, or leaf burn with downward cupping, curling, or puckering (Kornegay and Cardona 1991; Murray et al. 2004b). Empoasca kraemeri has a more damaging feeding style than E. fabae (Calderon and Backus 1992). Leafhopper injury symptoms were positively associated with reduction in seed yield, seed weight, and number of seeds per plant (Kornegay and Cardona 1990). The nymph and adult counts were positively associated with leaf curl score and plant height in Canada, but not in Colombia (Murray et al. 2004b). There was also a lack of correlation between nymph counts and visual injury scores due to E. kraemeri (Kornegay and Cardona 1990). The seedling, flowering, and pod-filling stages were more sensitive to leafhopper attack; thus, cumulative insect populations could be high at the latter growth stage

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(Schoonhoven et al. 1978). The early severe infestation results in leaf burn, leaf curl, and overall plant stunting. Severe leafhopper attack during the reproductive stages results in excessive flower and pod abortion and development of twisted curved pods, each with few shriveled seeds. Yield under leafhopper pressure was the most reliable measure of tolerance to E. kraemeri followed by leafhopper injury scores, and nymph and adult insect populations were poor indicators of tolerance (Kornegay and Cardona 1990). Potential yield losses in excess of 80% in dry (Whitefield and Ellis 1976; Eckenrode 1981; Lindgren and Coyne 1995; Schaafsma et al. 1998) and green (Gonzalez and Wyman 1991) common bean could be expected under severe leafhopper pressure. Leafhopper injury symptoms and yield losses are higher in determinate large-seeded Andean cultivars and landraces than in small and mediumseeded indeterminate Middle American common beans (Murray et al. 2001). Resistant dry bean genotypes had fewer nymph populations in Canada, and resistant small-seeded indeterminate cultivars (e.g., ICA Pijao, ICA Tui, Carioca), in general, had higher levels of tolerance and were able to sustain higher leafhopper populations throughout the growing season in Colombia (Kornegay et al. 1989; Murray et al. 2004b). The majority of dry bean genotypes tolerant to E. kraemeri in Colombia were also tolerant to E. fabae in Canada (Schaafsma et al. 1998). Heritable differences for ovipositional nonpreference or antixenosis and tolerance to feeding by leafhoppers were reported in the small-seeded race Mesoamerica cultivars and landraces (Schoonhoven et al. 1978; Kornegay et al. 1986, 1989; Calderon and Backus 1992). Tolerance to E. kraemeri was more common than antixenosis in dry bean (Schoonhoven et al. 1978). However, the mechanism of tolerance had no effect on adult leafhopper populations, especially under no-choice situations. Leafhopper tolerance and antixenosis are inherited quantitatively with low heritability (Galwey and Evans 1982; Kornegay and Temple 1986). In crosses of potato leafhopper tolerant small black bean Tacaragua and medium-seeded pinto Sierra with susceptible great northern Starlight, Gonzalez et al. (2001) also reported low narrow-sense heritability estimates that were obtained by regressing the F3 on F2. Kornegay et al. (1989) reported transgressive segregation between crosses of dry bean genotypes that possessed tolerance and antixenosis. Habibi et al. (1993) found that plant lectins recovered from red kidney beans reduced survival of potato leafhoppers indicating antibiosis. Gonzales et al. (2001) and Murray et al. (2004a) reported eight molecular markers that were associated with tolerance to E. fabae and four with tolerance to E. kraemeri, of which three markers located in linkage groups B1, B3, and B7 were linked with tolerance to both species. Through recurring cycles of the bulk-pedigree method of selection, significantly higher tolerance to leafhoppers

was obtained in dry bean breeding lines of different market classes (Kornegay and Cardona 1990). When tested in temperate environments in Canada, most of these breeding lines also have shown tolerance to E. fabae (Schaafsma et al. 1998). However, much higher resistance to leafhoppers was found in some tepary bean (Cardona and Kornegay 1999) such as accession G 40036. Genetic control of leafhopper resistance in tepary bean is not known nor has any attempt been made to transfer that resistance into common bean. Because tepary bean can be crossed with common bean (Thomas and Waines 1984; Parker and Michaels 1986; Mejı´ aJime´nez et al. 1994), leafhopper resistance from tepary bean and other Phaseolus species needs to be combined with the tolerance available in common bean. Thrips The melon thrips (Thrips palmi Karny), native of Asia, became a serious insect pest of common bean and other crops in the Americas during the last quarter of the twentieth century (Cardona et al. 2002). Females insert single eggs in leaf tissues, where the mean total duration of immature stages is B15 d, and golden colored adults have an average life span of B20 d (Dura´n et al. 1999; Bueno and Cardona 2001). Thus, thrips have a short life cycle and high reproductive rate. Thrips attack all aerial plant parts and larvae and adults suck the sap with their piercing-sucking mouthparts leaving silvery feeding scars that are more conspicuous on the upper leaf surface, often along the midrib and veins. Heavily infested plants exhibit a silvered or bronzed appearance, deformed and stunted leaves, scarred and deformed green pods, and dead terminal shoots (Cardona et al. 2002). An average yield loss of 30% in green bean with some green and dry bean genotypes exhibiting 100% yield loss were reported in Colombia (Rendo´n et al. 2001; Cardona et al. 2002). Of 1138 dry bean genotypes screened, only 60 (5.3%) were resistant to thrips in Colombia (Cardona et al. 2002). Among the resistant genotypes after repeated testings included five germplasm accessions (G 2402, G 2852, G 3177, G 3569, G 4055), Brunca (synonymus with BAT 304), and six breeding lines, namely A 216, DOR 714, EMP 486, FEB 115, FEB 161, and FEB 162. But none of these genotypes had a high level of resistance (i.e., score of 53 on a 1 to 9 scale). Leaf pubescence, growth habit, maturity, seed color, and seed size were not associated with insect resistance. However, positive correlations between visual damage scores and seed yield were recorded (Cardona et al. 2002). Subsequently, Frei et al. (2004) reported tolerance as a mechanism of resistance to thrips. Frei et al. (2003) also reported some evidence of antibiosis in dry bean genotypes BH-130 and Brunca, antixenosis in FEB 115, and tolerance in EMP 486. Among recombinant inbred lines derived from single-cross populations a continuous distribution of damage scores indicated a quantitative inheritance of resistance to thrips in dry bean. Frei et al.

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(2005) also found transgressive segregation for thrip resistance in recombinant inbred lines derived from BAT 881G 21212 cross. Quantitative trait loci were detected on linkage groups b02, b03, b06 and b08; and should be useful for marker-assisted selection and development of resistant cultivars. Other Insect Pests There are several common bean insect pests such as aphids, chrysomelids, cutworms, leaf feeding caterpillars, leafminers, Mexican bean beetle, slugs, spider mites, and whiteflies, among many others for which there are no recent germplasm screening, genetics, and breeding reports. Furthermore, for additional information on breeding and genetics of common bean for resistance to insect pests and nematodes readers should refer to Cardona (1989), Kornegay and Cardona (1990), Singh (1992, 2001), Cardona and Kornegay (1999), Beaver et al. (2003), and Miklas et al. (2006). BREEDING FOR RESISTANCE TO NEMATODES Root-knot Nematode Root-knot nematodes (Meloidogyne spp.) are endemic in many common bean production regions in the Americas. Several species of Meloidogyne such as M. incognita (Kofoid & White) Chitwood, M. javanica (Treub) Chitwood, M. hapla Chitwood, and M. arenaria (Neal) Chitwood infest common bean and numerous other crops worldwide (Mullin et al. 1991a, b; Roberts 1992, 1995). While these species from common bean fields in Colombia were detected at frequencies of 62, 21, 14, and 14%, respectively, in Peru only M. incognita and M. javanica were found at frequencies of 66 and 7%, respectively (Mullin et al. 1991a). The juveniles of biotrophic endoparasitic nematodes invade plant roots and settle to feed on modified (galls) living cells (Trudgill 1997). Seed yield loss from combined infestation of M. incognita and M. javanica ranged from 45 to 63% on susceptible large-seeded, determinate Type I Andean dry bean cultivar DIACOL Calima, and from 26 to 32% on less susceptible breeding line PVA 916 with similar seed and growth habit characteristics (Mullin et al. 1991a). The use of highly resistant common bean cultivars, where available, is the most effective and economical method for managing root-knot nematodes. Periodically, common bean germplasm accessions, breeding lines, and cultivars have been screened, and resistance to root-knot nematodes identified (Omwega et al. 1989; Mullin et al. 1991b; Sydenham et al. 1996; Widmer and Abawi 2000). However, resistance to one species or one race of root-knot nematodes may be independent of resistance to other species, races, or biotypes (Mullin et al. 1991b; Chen and Roberts 2003). For example, PI 165426 was resistant to M. incognita but susceptible to simultaneous infestation with M. incognita and M. javanica. Similarly, green bean NemaSnap and dry

bean Yolano were resistant to one biotype of M. hapla, but susceptible to another, indicating transagonal interactions and a gene-for-gene relationship (Chen and Roberts 2003). Some common bean genotypes that were resistant or moderately resistant to biotypes of M. incognita and M. javanica from two or more locations in Colombia include NemaSnap, germplasm accessions G 2587 and G 12727, and breeding lines A 211, A 252, and A 445, among many others (Mullin et al. 1991b). The Brazilian dry bean cultivar, Carioca, belonging to race Mesoamerica (Singh et al. 1991a), was used to develop breeding lines A 211, A 252, and A 445 at CIAT (Centro Internacional de Agricultura Tropical), Cali, Colombia. In addition, A 252 and A 445 had G 2618 (synonymous with Guanajuato 31) belonging to race Durango from the central highlands of Mexico, known to be resistant to Meloidogyne spp., in their pedigree. Nonetheless, none of these breeding lines was ever deliberately and knowingly selected under root-knot nematode pressure. Resistance to Meloidogyne spp. was identified among Mexican landraces of common bean, and a single dominant gene, Me-1 controlled the resistance (Omwega et al. 1990a, b). Resistance to M. incognita in PI 165426 was controlled by one dominant gene Me-2 and one recessive gene me-3, and the resistance due to Me-2 was non-dominant at 288C transistional temperature (Omwega and Roberts 1992). The Me-1 gene resisted M. incognita race 1 populations, M. arenaria, and M. javanica. In contrast, the Me-2 and me-3 combination resisted most M. incognita populations, but not M. arenaria and M. javanica (Omwega and Roberts 1992; Omwega et al. 1989, 1990a). A single dominant gene controlled resistance to M. hapla in NemaSnap (Chen and Roberts 2003). Furthermore, the resistance to M. hapla in NemaSnap was not derived from PI 165426, which was variable for M. hapla resistance. PI 165426 contributed resistance to M. incognita to NemaSnap via breeding line B4175 (Wyatt et al. 1980, 1983). Lesion Nematode Limited information is available on the reaction of common bean cultivars and germplasm to lesion nematodes. The navy bean cultivars Saginaw, Seafarer, and Tuscola were reported to be tolerant of Pratylenchus penetrans (Cobb) Filip. & Schuur.-Stek. Great northern cultivars US 1140 and UI 11 were resistant to both P. neglectus (Rensch) Filip. & Schuur.-Stek. and P. hexincisus Taylor and Jenkins (Abawi and Widmer 2000; Elliott and Bird 1985). However, there are no reports of genetics and breeding for resistance to lesion nematodes per se. Soybean Cyst Nematode Like lesion nematodes, very limited information is available on the extent of damage caused by, reaction of common bean cultivars and other cultivated and wild

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Phaseolus species germplasm to, and genetics and breeding for, soybean cyst nematode (Heterodera spp.). Nonetheless, Abawi and Jacobsen (1984), Smith and Young (2003), and Poromarto and Nelson (2009), among others, reported on the response of diverse common bean genotypes to H. glycines. For example, small black bean cultivar Jaguar exhibited high levels of tolerance (Poromarto and Nelson 2009). Noel et al. (1982) found most green bean cultivars susceptible to soybean cyst nematode. Similarly, large-seeded Andean dry beans, such as G 122, Taylor Horticultural, and Montcalm were susceptible to one or more races of H. glycines. In contrast, some Middle American dry beans such as Burke, Chase, Dorado, and Porrillo Sintetico exhibited high levels of resistance to H. glycines (Smith and Young 2003). BREEDING FOR RESISTANCE TO MULTIPLE INSECT PESTS AND NEMATODES FOR FUTURE CULTIVARS Bueno et al. (1999) combined resistance to bean pod weevil, bruchids, and leafhoppers using two different breeding methods. But there are no reports of commercial dry or green bean cultivars with resistance to two or more insect pests and nematodes, despite several decades of dry and green bean breeding and genetics studies in the Americas and elsewhere. For a successful broadly adapted commercial cultivar, resistance to multiple insect pests and nematodes and other biotic and abiotic stresses must be combined with consistent high yield, seed quality, nutritional value, and desirable maturity and plant type. This process would be facilitated if for each market class all parental germplasm including available cultivars, elite breeding lines, and donor germplasm of resistance genes (including those obtained from introgression and pyramiding of resistance alleles from alien germplasm) would be adapted and be similar in growth habit, maturity, seed color and size. Thus, each cross would only be made among elite recipients and donor parents. A few multipleparent (i.e., two genotypes) crosses with considerably large number of F1 seed (100) should be preferred over a large number of single-crosses and backcrosses. Although comparatively more time may be spent during hybridization to generate multiple-parent crosses, the process should allow production of recombinants with resistance alleles/QTL for multiple pests in the shortest time possible. This production of recombinants would not be possible through single-crosses and backcrosses without repeated cycles of selection for specific pests, one pest at a time. Thus, in the first step, all resistance alleles and QTL would be combined through multipleparent crosses, and the time required for cultivar development would be reduced. Gamete selection (Singh 1994) for dominant and codominant resistance alleles in the multiple-parent F1, combined with selection in the F1-derived families using replicated trials in the early generations (F2 to F5) for

seed yield, tolerance or resistance to insect pests (e.g., bean pod weevil and leafhoppers for Central America) and nematodes and other biotic and abiotic stresses, and agronomic traits across contrasting and complementary environments in the target production regions, should help identify promising populations and families within populations. The latter could then be used to develop superior breeding lines for further testing and subsequent cultivar identification. Asensio et al. (2005, 2006) used the above methodology to introgress resistance to bean common mosaic, common bacterial blight, and halo blight from inter-gene pool multiple-parent crosses. Similarly, Singh et al. (1998) developed an upright carioca bean with resistance to leafhoppers and five diseases using gamete selection in multiple-parent interracial populations. Furthermore, the use of robust markers (e.g., arcelin seed protein for bruchid resistance and tightly linked PCR-based molecular markers for A. godmani and leafhoppers) linked with resistance alleles and other desirable traits could easily be combined with direct screening for resistance controlled by dominant alleles (e.g., Arc resistance gene for tropical bruchids, Agr and Agm resistance alleles for bean pod weevil, and Me-1 for root knot nematode resistance) for multiple pests in the F1. Also, use of molecular markers for selection of early generation segregating families and populations that would be harvested in bulk may now be feasible only if cost-effective technologies such as GoldenGate assay (Hyten et al. 2009) are applicable to common bean. For resistance inherited by recessive alleles, intensive selection in early generations using direct screening should be avoided. The frequency of resistant recombinants would be very low and there may be a danger of losing potentially useful recombinants that might arise in later generations. For such traits, it would be preferable to initiate evaluation and selection in the F4 or F5 onwards. For insect pests, nematodes, and other biotic and abiotic stresses that could not be screened simultaneously, different locations or environments and nurseries may be required to select promising populations and families within populations (Singh et al. 1991b, 1998; Bueno et al. 1999). CONCLUSIONS AND PROSPECTS Significant advances have been made in the development of common bean breeding lines and enhanced germplasm resistant to specific insect pests and nematodes. However, resistance to insect pests and nematodes in otherwise high-yielding, high-quality cultivars of broad adaptation is lacking. Furthermore, large numbers of pest-resistant germplasm accessions from the primary, secondary, and tertiary gene pools remain to be utilized. Integrated linkage maps of common bean are available (Freyre et al. 1998; Gepts 1999; Tar’an et al. 2002; Kelly et al. 2003; Miklas et al. 2006; Miklas and Singh 2007) and the map positions of some pest resistance alleles and QTL are known (Gonzales et al. 2001; Murray et al. 2004a; Frei et al. 2005; Blair et al. 2006). Marker-assisted

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selection has successfully been used for bruchids, Z. subfasciatus, and molecular markers are increasingly being used for indirect selection for resistance to bacterial, fungal, and viral diseases in common bean [see review by Singh and Schwartz (2010)]. Because direct germplasm screening and selection under natural conditions can often only be effected in certain regions (e.g., for bean pod weevil in the Mexican highlands and Central America and leafhoppers in dry warm growing environments in Latin America), which may take a fullgrowing season, the use of molecular marker-assisted selection should be emphasized for breeding for resistance to insect pests and nematodes to expedite the breeding process. Genome-wide search for and use of molecular markers linked with maximum number of useful traits, if feasible before planting seed of F1 of multiple-parent crosses and early generation populations and families as is done in cereal and soybean (Somers et al. 2005), would modernize and expedite common bean improvement. Transformation of common bean, although very difficult to popularize at the moment, is no doubt possible (Araga˜o et al. 1998, 2002; Faria et al. 2006). Its use to introgress pest and pesticide resistance alleles from distantly related Phaseolus (e.g., quarternary gene pool and beyond) and non-Phaseolus species may still be an impractical goal due to political barriers to acceptance and costs involved. Researchers should nonetheless strive to combine the best of conventional and modern molecular approaches to improve common bean germplasm and cultivars for resistance to multiple insect pests and nematodes. Abawi, G. S. and Jacobsen, B. J. 1984. Effects of initial inoculum densities of Heterodera glycines on growth of soybean and kidney bean and their efficiency as hosts under greenhouse conditions. Phytopathology 74: 14701474. Abawi, G. S. and Widmer, T. L. 2000. Impact of soil health management practices on soilborne pathogens, nematodes and root diseases of vegetable crops. Appl. Soil Ecol. 15: 3747. Acosta-Gallegos, J., Quintero, C., Vargas, J., Toro, O., Tohme, J. and Cardona, C. 1998. A new variant of arcelin in wild common bean, Phaseolus vulgaris L., from southern Mexico. Genet. Resour. Crop Evol. 45: 235242. Acosta, J., Rosales, R. and Garza, R. 1992. Resistance to the pod weevil in wild Phaseolus vulgaris. Annu. Rep. Bean Improv. Coop. 35: 103104. Araga˜o, F. J. L., Ribeiro, S. G., Barros, L. M. G., Brasileiro, A. C. M., Maxwell, D. P., Rech, E. L. and Faria, J. C. 1998. Transgenic beans (Phaseolus vulgaris L.) engineered to express viral antisense RNAs show delayed and attenuated symptoms to bean golden mosaic virus. Mol. Breed. 4: 491499. Araga˜o, F. J. L., Vianna, G. R., Albino, M. M. C. and Rech, E. L. 2002. Transgenic dry bean tolerant to the herbicide glufosinate ammonium. Crop Sci. 42: 12981302. Asensio, S., Manzanera, M. C., Asensio, C. and Singh, S. P. 2005. Introgressing resistance to bacterial and viral diseases from the Middle American to Andean common bean. Euphytica 143: 223228. Asensio, S., Manzanera, M. C., Asensio, C. and Singh, S. P. 2006. Gamete selection for resistance to common and halo

bacterial blights in dry bean intergene pool populations. Crop Sci. 46: 131135. Beaver, J. S, Rosas, J. C., Myers, J., Acosta, J., Kelly, J. D., Nchimbi-Msolla, S., Misangu, R., Bokosi, J., Temple, S., Arnaud-Santana, E. and Coyne, D. P. 2003. Contributions of the bean/cowpea CRSP to cultivar and germplasm development in common bean. Field Crops Res. 82: 87102. Beebe, S., Cardona, C., Diaz, O., Rodrı´ guez, F., Mancı´ a, E. and Ajquejay, S. 1993. Development of common bean (Phaseolus vulgaris L.) lines resistant to the pod weevil, Apion godmani Wagner, in Central America. Euphytica 69: 8388. Blair, M. W., Mun˜oz, C., Garza, R. and Cardona, C. 2006. Molecular mapping of genes for resistance to the bean pod weevil (Apion godmani Wagner) in common bean. Theor. Appl. Genet. 112: 913923. Bueno, J. M. and Cardona, C. 2001. Biologı´ a y ha´bitos de Thrips palmi (Thysanoptera: Thripidae) como plaga de frı´ jol y habichuela. Rev. Colomb. Entomol. 27: 4954. Bueno, J. M., Cardona, C. and Quintero, C. M. 1999. Comparacio´n entre dos me´todos de mejoramiento para desarrollar resistencia multiple a insectos en frijol (Phaseolus vulgaris L.). Rev. Colomb. Entomol. 25: 7378. Calderon, J. D. and Backus, E. A. 1992. Comparison of the probing behaviors of Empoasca fabae and E. kraemeri (Homoptera: Cicadellidae) on resistant and susceptible cultivars of common beans. J. Econ. Entomol. 85: 8889. Cardona, C. 1989. Insects and other invertebrate bean pests in Latin America. Pages 505570 in H. F. Schwartz and M. A. Pastor-Corrales, eds. Bean production problems in the tropics. 2nd ed. CIAT, Cali, Colombia. Cardona, C. and Kornegay, J. 1999. Bean germplasm resources for insect resistance. Pages 8599 in S. L. Clement and S. S. Quisenberry, eds. Global plant genetic resources for insect resistance. CRC Press, Boca Raton, FL. Cardona, C., Frei, A., Bueno, J. M., Dı´ az, J., Gu, H. and Dorn, S. 2002. Resistance to Thrips palmi (Thysanoptera: Thripidae) in beans. J. Econ. Entomol. 95: 10661073. Cardona, C., Kornegay, J., Posso, C. E., Morales, F. and Ramı´ rez, H. 1990. Comparative value of four arcelin variants in the development of dry bean lines resistant to the Mexican bean weevil. Entomol. Exp. Appl. 56: 197206. Cardona, C., Posso, C. E., Kornegay, J. L., Valor, J. and Serrano, M. 1989. Antibiosis effects of wild dry bean accession on the Mexican bean weevil and the bean weevil (Coleoptera: Bruchidae). J. Econ. Entomol. 82: 310315. Chen, P. and Roberts, P. A. 2003. Virulence in Meloidogyne hapla differentiated resistance in common bean (Phaseolus vulgaris). Nematology 5: 3947. Dobie, P., Dendy, J., Sherman, C., Padgham, J., Wood, J. A. and Gatehouse, A. M. R. 1990. New sources of resistance to Acanthoscelides obtectus (Say) and Zabrotes subfasciatus Boheman (Coleoptera: Bruchidae) in mature seeds of five species of Phaseolus. J. Stored Prod. Res. 26: 177186. Dura´n, I., Mesa, N. and Estrada, E. 1999. Ciclo de vida de Thrips palmi (Thysanoptera: Thripidae) y registro de hospedantes en el Valle del Cauca. Rev. Col. Entomol. 25 (34): 109120. Eckenrode, C. J. 1981. Influence of potato leafhopper control on kidney beans in New York. J. Econ. Entomol. 85: 8899. Elliott, A. P. and Bird, G. W. 1985. Pathogenicity of Pratylenchus penetrans to navy bean (Phaseolus vulgaris L.). J. Nematol. 17: 8185.

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